heat stress essay

HEAT STRESS

Workers who are exposed to extreme heat or work in hot environments may be at risk of heat stress. Exposure to extreme heat can result in occupational illnesses and injuries. Heat stress can result in heat stroke, heat exhaustion, heat cramps, or heat rashes. Heat can also increase the risk of injuries in workers as it may result in sweaty palms, fogged-up safety glasses, and dizziness. Burns may also occur as a result of accidental contact with hot surfaces or steam.

Workers at risk of heat stress include outdoor workers and workers in hot environments such as firefighters, bakery workers, farmers, construction workers, miners, boiler room workers, factory workers, and others.

Workers at greater risk of heat stress include those who are 65 years of age or older, are overweight, have heart disease or high blood pressure, or take medications that may be affected by extreme heat.

Prevention of heat stress in workers is important. Employers should provide training to workers so they understand what heat stress is, how it affects their health and safety, and how it can be prevented.

OSHA-NIOSH Heat Safety Tool App A useful resource for planning outdoor work activities based on how hot it feels throughout the day. The app is available in English and Spanish.

NIOSH Criteria for a Recommended Standard: Occupational Exposure to Heat and Hot Environments Provides safety professionals and employers an evaluation of the scientific data on heat stress and hot environments, and NIOSH recommendations.

NIOSH Prevent Heat Related Illness Poster Basic reminders for workers exposed to heat and hot environments.

NIOSH Fast Facts: Protecting Yourself from Heat Stress   [ español , Kreyol Haitien (Haitian Creole) , Việt (Vietnamese) ] Print or order this free card for easy access to important safety information.

NIOSH Infographic: Protect your workers from Heat Stress   [ español ] Learn some tips to protect workers including: acclimatization, rest breaks, and fluid recommendations.

NIOSH-CPWR Infographic: Extreme Heat and Construction Falls  [español] Heat exposure increases risk of traumatic injuries such as falls.

NIOSH Heat Stress: Risk Factors Workers should be aware of the many factors that can impact the risk of heat illness.

NIOSH Heat Stress Podcast Heat stress can be a major concern for indoor and outdoor workers, especially during the hot summer months. Learn how to identify the symptoms and protect yourself from heat stress.

NIOSH Workplace Solution: Preventing Heat-related Illness or Death of Outdoor Workers   [ español ] Provides employers and safety professionals with information and case studies.

OSHA-NIOSH Infosheet: Protecting Workers from Heat Illness   [ español ] Provides information to employers on measures they should take to prevent heat-related illnesses and death. Now available in ePub format.

NIOSH Mining Product: Keeping Cool: Training to Reduce Heat Stress Incidents A training module that will help mining workers recognize the signs of heat-related illness and provide appropriate first aid.

NIOSH Science Blog: Keeping Workers Hydrated and Cool Despite the Heat Keeping workers cool and well-hydrated are the best ways to protect them when working in hot environments.

NIOSH Science Blog: Adjusting to Work in the Heat: Why Acclimatization Matters The natural adaptation to the heat takes time, and from a management perspective, it may require careful planning.

NIOSH Science Blog: Extreme Heat – Are you prepared for summer work? The approach of summer is a reminder to us all of the need to recognize, and act to prevent, the harmful effects of excessive heat.

MMWR: Heat Illness and Death Among Workers – United States, 2012-2013 This report describes findings from a review of Occupational Safety and Health Administration (OSHA) federal enforcement cases (i.e., inspections) resulting in citations.

MMWR: Heat-Related Deaths among Crop Workers, 1992-2006 This report describes a heat-related death and summarizes heat-related fatalities among crop production workers in the United States.

CDC: Extreme Heat   [ español ] Additional information on heat-related illnesses and prevention.

National Integrated Heat Health Information System (NIHHIS) An integrated system that builds understanding of extreme heat, and improves capacity, communication, and societal understanding of the problem.

Hazards to Outdoor Workers

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Heat is a ‘silent killer’

January 24, 2019 — Climate change will mean more extreme weather, including heat waves. And it’s not a distant threat—we’re already seeing the effects now in the United States. In this week’s episode, we explore the health threat posed by severe heat and how our society needs to adapt in the decades ahead. You’ll hear from Augusta Williams , a doctoral student at Harvard T.H. Chan School of Public Health, who studies how extreme heat can affect our bodies and minds. She’ll explain why heat is considered a “silent killer” and how we can combat the effects of our warming world.

This episode was produced with assistance from Veritalk , a podcast from Harvard University’s Graduate School of Arts and Sciences.

You can subscribe to Harvard Chan: This Week in Health by visiting  iTunes  or  Google Play  and you can listen to it by following us on  Soundcloud , and stream it on the  Stitcher  app or on  Spotify .

Extreme heat linked with reduced cognitive performance among young adults in non-air-conditioned buildings ( Harvard Chan School news )

How ‘heat islands’ can harm health ( Harvard Chan School news )

Full Transcript

AUGUSTA WILLIAMS: So my research all focuses on the impacts of extreme heat on human health. A lot of my research is focused here in Boston and Cambridge, which is fun. And then we further examine the influence of the built environment and its role in either mitigating or exacerbating extreme heat exposures and the resulting health impacts on the populations of Boston and Cambridge.

ANNA FISHER-PINKERT: Can you tell me a little bit about, like, why is heat bad for our health?

AUGUSTA WILLIAMS: So heat is one of the most well-understood public health impacts of climate change. There’s been a wide variety of research that has shown that heat is one of the largest killers of all meteorological phenomena, more so than floods or tornadoes and hurricanes, which a lot of people are surprised by since a lot of those other weather events look much scarier than extreme heat does. But it’s really a silent killer is what a lot of public health researchers call it because you can’t see it.

But it’s extremely dangerous. There’s been a lot of research that has shown that heat has a role in exacerbating cardiovascular disease, respiratory health outcomes, even renal in diabetes complications, outcomes related to pregnancy and the health of newborn babies, and even things like our cognitive function, our sleep, and our productivity. So there’s a wide range of health outcomes that heat influences and really across all sectors of society.

ANNA FISHER-PINKERT: Tell me some of the medical conditions that could be exacerbated by heat.

AUGUSTA WILLIAMS: So things like cardiovascular outcomes related to either heart attacks, or heart failure can be complicated during extreme heat exposures. People with diabetes are more prone to heat stress or have complications related to their diabetes condition. Respiratory outcomes, especially asthma– that’s an important one, because also during heat waves, there’s usually high air pollution rates that also then trigger asthma, especially in vulnerable populations, like children and the elderly.

ANNA FISHER-PINKERT: So you mentioned earlier that there are these cognitive effects of heat. What do we know about that?

AUGUSTA WILLIAMS: So there’s been some great research happening here at Harvard on this, as well as elsewhere. My team recently published a study that was led by Dr. Memo Cedeno, where we actually worked in the dorms here on campus at Harvard and tracked students for 12 days. Half of the students we worked with had access to air-conditioning in their dorm rooms, and the other half did not.

And we found that during this time, we were able to see before, during, and after a heat wave. And those without air-conditioning experienced significant reductions in their cognitive performance. And we measured that with two tests. One was a color word test that the students completed, and the other was an addition and subtraction test. And on both of these, saw impairments in their performance when they didn’t have access to air-conditioning during the heat wave.

ANNA FISHER-PINKERT: What’s a color word test?

AUGUSTA WILLIAMS: So that test is one that you see a lot in a variety of forms on the internet. It’ll pop up where the word is written in a certain color, but the word is also a color word. And you have to determine what color the word is written in.

So the word might be “black,” but it’s written in blue ink. And you have to pick that it’s the color the ink is, is blue. So kind of getting at some complex cognitive processes.

ANNA FISHER-PINKERT: Although when you say complex cognitive processes, it’s not like we’re asking them to do, like, calculus.

AUGUSTA WILLIAMS: No, not at all. I don’t even think I would be able to perform well on that test without the heat exposure. But looking at some of the ways our brain, our active memory, the way we’re able to process words and numbers can have relationship to the decisions we make when we maybe leave for work. We get in our car, and we commute to our job or to school, or if you have a test to take– some of those similar things.

And this was supported by other work. There was a study that Jisung Park did during his time here at Harvard, showing that students in New York State who took a Regents exam on a 90-degree day versus a 72-degree Fahrenheit day performed worse. And looking at how heat really can play a role in short and long-term learning and thinking.

ANNA FISHER-PINKERT: So I can see why that’s a problem if you’re a student and you need to pass your Regents. But, I mean, if we just have a slightly less cognitively smart population in a city, what are the consequences for that?

AUGUSTA WILLIAMS: I think it can have consequences that may be more immediate in terms of maybe people are making poor decisions in the morning, because our work was really looking at these tests happened right after waking up. So kind of looking at overnight temperatures, what is the role of these extreme heat exposures indoors during your sleep periods on your ability to wake up in the morning and, you know, how active your cognitive thinking is? But there’s a lot more research that’s needed to determine what are the long-term effects of this.

How long into the day do these processes happen? Is this an acute or a more long-term effect that heat has on our thinking and performance? But looking at how the economy and how many of our workplaces are still currently functioning, if we look at extreme heat and the role that would play on those, there may be wider effects on larger sectors of the population than previously thought.

ANNA FISHER-PINKERT: In terms of, like, cognitive impairment, why is that a public health concern?

AUGUSTA WILLIAMS: So when we think about the role heat plays on our cognitive function, there’s a lot happening in our brain that can have outward-facing effects on society, whether that’s how we are performing at work or school. There’s a lot of research showing that on hot days, there’s increased aggressive and violent crime in many urban centers. There’s even a newer area of research looking at car accidents happening on hotter days, that our brain’s ability to make decisions, reducing our risk-taking behaviors are all inhibited as temperatures increase. So there’s a lot of outward-facing effects on society that this heat and cognitive function relationship can have on the public.

ANNA FISHER-PINKERT: So tell me a little bit about how climate change plays into this story.

AUGUSTA WILLIAMS: So with climate change, heat is one of the largest climate change outcomes that we’re seeing, especially here in the Northeast United States. There were a lot of really important landmark climate-change assessments that came out at the end of November, beginning of December that are showing that the heat story is only worsening in many parts of the world, unfortunately. Here in Boston, we typically have about 11 days per year that are above 90 degrees Fahrenheit, looking at the last 30 to 40 years of climate averages.

But by 2030, that number is expected to grow to potentially 40 days above 90 degrees Fahrenheit. And by 2070, that number is expected to be almost our entire summer could be above 90 degrees Fahrenheit, with a significant portion of that even above 100 degrees Fahrenheit. So some comparisons that were outlined in these reports is that by the middle of the century, Boston could have summers that currently look more like Washington, DC, but towards the end of the century, more like Birmingham, Alabama.

ANNA FISHER-PINKERT: So I came here from Washington, DC. And I can tell you, I do not want to live through those summers.

[CHUCKLING]

AUGUSTA WILLIAMS: You came to escape–

ANNA FISHER-PINKERT: I did.

AUGUSTA WILLIAMS: –the heat.

ANNA FISHER-PINKERT: Yes. So that sounds pretty dire. Are there specific concerns? First of all, I guess my question is, is this worse in cities?

AUGUSTA WILLIAMS: Yes, heat can definitely have a larger burden on urban centers because of the urban heat island effect. And this is because of the way urban centers are structured, we have a lot of high-rise buildings close together that are made out of materials that really absorb a lot of heat. And because of this and other sources of heat– like we have more cars that are exhausting their air into the cities– you can have upwards of a 10, sometimes even a 20-degree Fahrenheit temperature difference between an urban center and surrounding areas. And that depends on the day and the structure of the individual city but can range anywhere up to 22 degrees Fahrenheit, some researchers have found.

ANNA FISHER-PINKERT: Are there specific impacts for a city like Boston versus a city elsewhere in the country?

AUGUSTA WILLIAMS: So the impacts in the Northeast are showing that heat waves are increasing in frequency, intensity, and duration. So in places like Boston and New York and Philadelphia, heat’s going to become more of an issue. And as a result, on our current greenhouse gas emissions trajectories, they’re looking that heat-related mortality could upwards of triple by the end of the century, which is really scary.

But I think heat is increasing in all places across the world, that this is not a story unique to the Northeast. Something that is more unique to the Northeast is the fact that a lot of our buildings and our building stocks were created for the cold winters that we also have and will continue to have, that we have very low rates of central air-conditioning penetration. And studies have found that of all types of air-conditioning, central air-conditioning is really the one that helps most combat and reduce the high thermal loadings of indoor environments during heat waves. So that’s something that more on the adaptation side, the Northeast is more unique than other areas like the South, that has a much higher rate of air-conditioning at home.

ANNA FISHER-PINKERT: What’s a high thermal loading?

AUGUSTA WILLIAMS: So high thermal loading is when a building just has the ability to maintain a high thermal mass– lots of temperature– whether that be from it’s made out of materials that absorb a lot of heat, it’s oriented in a way– like the building I live in is a south-facing building made of brick. So it’s just hit by the sun all day and made of materials that really maintain that heat, which is great in the winter this time of year but not so helpful in the summertime.

ANNA FISHER-PINKERT: I mean, aren’t our winters also supposed to get worse over time, too?

AUGUSTA WILLIAMS: Yeah, so I think our winters, for the most part, as average global temperatures increase, there will be a slight warming throughout the entire year. But extreme cold will still be a thing that is happening here in the Northeast and elsewhere across the globe. So extreme cold spells and cold waves, which also have their own set of public health impacts, will also continue to be important. So there’s some really unique adaptation problems that we’re facing of how can we adapt these urban centers to still continue to experience both extreme heat and extreme cold, more so than historically we faced here in Boston?

ANNA FISHER-PINKERT: So it seems like the thing that’s getting cut out of the calendar are those, like, nice sunny days in June and September when you can just kind of walk outside in a T-shirt and jeans.

AUGUSTA WILLIAMS: Yes, those are my favorite.

ANNA FISHER-PINKERT: Well, and they’re going away.

AUGUSTA WILLIAMS: Yes.

ANNA FISHER-PINKERT: Uh, OK. So I want to talk about air-conditioning because what you’re saying is that air-conditioning really helps with these public health outcomes. But isn’t that also a contributor to climate change?

AUGUSTA WILLIAMS: Air-conditioning is a really challenging problem right now. Air-conditioning is a vital public health tool. It saves lives. It keeps indoor spaces cool, which is very important for vulnerable populations.

But at the same time, air-conditioning has a few problems. The first is that in many areas in the United States, the energy generated to run these air-conditioners is generated by fossil fuels. And during those times, there are significant increases in the air pollutants that the fossil fuels generate that, both whether it’s carbon dioxide, which contributes more to climate change, or things like sulfur dioxide and nitrogen oxides that have really significant public health impacts, that both of these things threaten the health of communities, either by the direct air-pollutant exposures or through exacerbating climate change, and therefore worsening our heat problem so that we need even more air-conditioning to begin with.

But then at the same time, air-conditioners are also one of the largest sources of certain refrigerants. The cooling mechanisms that are inside of air-conditioning actually have huge greenhouse gas potential. They have the ability to warm even more than carbon dioxide.

And whether those are leaking, they’re not being efficiently used, or when people get rid of them, they do so in a way that these gases then leak out of them, and go back into the atmosphere, and then further contribute to climate change, leading to more heat. So air-conditioning is a really complicated problem that I think, for the most part, we have great technologies that could help us solve these issues so that we could use more air-conditioning in a sustainable way.

ANNA FISHER-PINKERT: Can you tell me about some of those technologies? Because I’m thinking, like, all right, I’m listening to this. And I’m trying to, like, build a new building. What am I supposed to do?

AUGUSTA WILLIAMS: Right. So some of the problems from air-conditioning we have the technology to solve. Right now, the Kigali Amendment to the Montreal Protocol would help us reduce the amount of refrigerants in the air-conditioning and other cooling systems across the world. It would help us mitigate upwards of 0.5 degrees Celsius of warming by the end of the century, which would be huge.

We would be able to use these air-conditioners without the negative climate potential of the gases inside of them. However, the US has not yet ratified that amendment. So that’s a step we could take and is one that both all the political parties, as well as industry folks, are supportive of because it would allow more air-conditioning use in a more sustainable way.

And then the second is to increase our use of renewable energy. If we are running air-conditioning on energy that is not producing harmful greenhouse gases and air pollutants, we can then mitigate the role air-conditioning has in worsening climate change. So I think those are two real key solutions that we have the ability to do better and to do more if we want to move in that direction.

ANNA FISHER-PINKERT: Is there a health consequence to people staying indoors in climate-controlled environments for more hours during their day?

AUGUSTA WILLIAMS: Yeah, I think that’s a great question. There’s been a lot of research– upwards of 40 years of research– looking at the role of indoor environments and indoor environmental quality on human health, whether that’s in our homes, or at work, or at school. I’m a member of the Healthy Buildings Team at the T.H. Chan School of Public Health. And that’s really our purview of looking at anywhere we live, work, or play.

What is the role of the indoor spaces that we’re existing in on our health? And temperature and thinking of thermal health is a really– there’s a sweet spot for getting thermal health conditions somewhere where you’re not using a ton of energy, where you’re able to cool spaces and create enough ventilation that indoor sources of pollutants are able to disperse, but also so that you’re not overheating or over-cooling the people that are existing in these spaces, and doing so in a way that health is maintained and productivity and performance are as well. And with certain populations like the elderly, they have different heating and cooling needs and comfort levels than, say, you know, young 30-something adults working in an office building.

ANNA FISHER-PINKERT: So as someone who is, like, relatively healthy and in– maybe I don’t need air-conditioning, like, am I doing good for the world by shutting it off when I can?

AUGUSTA WILLIAMS: I think finding that balance for you personally of conserving energy, not using air-conditioning when we don’t really need it, using more natural sources of ventilation, whether it’s using windows or fans, can be better. But as temperatures rise and get to more dangerous levels, I think that’s when it becomes harder to rely on those sources of ventilation. Even if we’re feeling OK, I think some of the work on the cognitive function has showed that without those cooling sources, even if we’re feeling OK and feeling fine, there might be internal processes that are being negatively impacted by heat. So we really need to do more work in figuring out where are these thresholds for different sectors of the population when it comes to thermally healthy and comfortable indoor spaces.

ANNA FISHER-PINKERT: I also wanted to ask you how inequality in a city plays into this.

AUGUSTA WILLIAMS: Yeah, that’s one of my biggest interests and passions in looking at climate change adaptation, of thinking of environmental justice communities and communities that may have the social demographic disadvantages that relate to them– these populations– being more vulnerable to heat, whether it’s more elderly people or people of low to no income who can’t afford an air-conditioner or afford the energy to run their air-conditioner, who maybe do not speak the native language of that area. For Boston, it would be English– that a lot of the heat warnings are disseminated in that language. And they might not be able to access that information.

When we think of access to cooling, cooling centers are a great resource but are not located in every community. Or say someone cannot physically get to the cooling center. Boston has, luckily, done some great work at increasing free transportation to these centers and things like that.

But we definitely have a long way to go, especially my work focusing on the built environment, that perhaps in those communities we’re doing some really great messaging around getting the word out about heat dangers. But we could do more in offering energy assistance for cooling, like we do for heating purposes in the winter, to do more about focusing on these communities where we’re planting our trees, where we’re painting our roofs lighter colors to help reduce the thermal loads of these communities.

ANNA FISHER-PINKERT: Yeah, I imagine, like, as you were describing, these older buildings that are close together have those high thermal loads. So I would imagine a neighborhood without green spaces, where buildings haven’t been renovated in several decades– those are places where people with less privilege often live.

AUGUSTA WILLIAMS: Yes. That is definitely very common in a lot of urban areas, that access to green space and parks or little splash pads, as well as neighborhoods that are made of materials that just keep those communities cooler to begin with, as well as not having the income to sustain air-conditioning use throughout the summer are usually very well co-located. Part of my research moving forward is to do an in-depth assessment related to all those variables I just mentioned, as well as building characteristics, to look at the role of these built environment factors on the vulnerability of communities in Boston to see if there’s areas where we could better strategize the types of adaptation measures or public health campaigns that we’re doing. So I’m excited to dive into that and see what we find, and see where we can better prioritize certain communities that need some of this adaptation work the most and the soonest.

ANNA FISHER-PINKERT: I thought it was interesting, also, you talked about incentivizing people to make changes to the built environment by repainting roofs, adding greenery. We kind of do that for solar panels. But is there a model for doing that for things that reduce heat?

AUGUSTA WILLIAMS: I haven’t yet seen a model about the incentivizing cooler communities yet. But it’s something that I’ve been to a couple of talks throughout the city of Boston this year in the last few months and have heard early discussions of that, both related to heat and to sea-level rise and storm flooding, of how can we think of as Boston continues to grow and expand, prioritizing climate resilience as developers move in, or as existing structures need to be updated and need to re be renovated? How can we think about providing incentives and allowing developers who want to be resilient in the face of climate change to get some type of reward so that it’s more market based, that we’re helping these developers continue to grow, continue to positively impact the Boston area, but in a way that doesn’t set us up for more problems in the future?

ANNA FISHER-PINKERT: I think it’s, like, it’s somewhat of a tight spot, right? Because you have developers who maybe aren’t going to be tied to that community once the buildings are built and the people have moved in. And then you also have citizens who aren’t necessarily, as you said, aware of the dangers of heat because it is silent. It’s not the same as having a nor’easter come through town or having a hurricane come through town. How do we get past that hurdle?

AUGUSTA WILLIAMS: I think that’s a great question, and one a lot of scientists working in this space are grappling with right now. I know on our team, we work with a very interdisciplinary team of folks. We have urban planners and architects and engineers on our team and have built close partnerships with both the developers, real estate companies, the people running and managing the buildings, and are trying to translate our science in a way that allows all of these stakeholders to understand the health impacts of the buildings that they are creating and running, and how they play a huge role on our health, perhaps equal to our more than our actual physicians and doctors do. Because we spend upwards of 90% of our time indoors, these people need to be part of the equation. And they’re extremely receptive to this information of how can we better work together to prioritize health in the face of climate change, in all of these structures that really play such a huge role in our lives.

ANNA FISHER-PINKERT: One thing that’s a theme in all of the stories I’m talking to people about– one thing that’s come up a lot is who controls the destiny of your city? And it seems like when it comes to climate change, it’s out of our control. Is there a way that we can take back control over what’s happening?

AUGUSTA WILLIAMS: I think if we continue to think about the ways we can adapt to climate change, the ways we can mitigate climate change from occurring, a lot of that action is happening at local levels, at the city levels. I think Cambridge and Boston are really leaders in a lot of areas when we look at other cities across the world, that we have people who are really dedicated to these causes, as well as leaders who are dedicated to these causes. And perhaps the steps that are taking, people can disagree on. But I think we’re all motivated by moving forward, whether that’s switching to renewable energy to mitigate greenhouse gas emissions, or thinking of ways we can better retrofit the downtown area to protect against sea-level rise, to planting trees.

Cambridge just got a huge grant. It was a participatory budget grant that the residents of Cambridge voted for. And the top result of that was to plant trees across Cambridge. So I think this is a really hopeful place to be, that we cannot necessarily control the warming that’s been set into place today, that we are experiencing more hot days. But we do have a role as citizens living in these areas, and also in partnership with the leadership of the area you’re living in, to take steps to mitigate and adapt in ways that are most beneficial to your community.

ANNA FISHER-PINKERT: I think it’s interesting. It’s like a lot of these adaptations are just things that people would like to have anyway.

AUGUSTA WILLIAMS: Exactly.

ANNA FISHER-PINKERT: So I’m sure some people voting for planting more trees in Cambridge just like trees. Like they’re not thinking about heat.

AUGUSTA WILLIAMS: Exactly. And there’s so many ways. I think there’s a comic about that of, well, what if we create more parks, and reduce air pollution, and make the air cleaner? And it’s all just to make a better world, that it will improve the climate-change problem and the health benefits we see in the future. But it also will make our world a better place. And I think that’s a great kind of part to the equation.

ANNA FISHER-PINKERT: Right. Right. You don’t have to be, like, a climate-change activist to think that it’s a good idea to live in a city with green spaces.

AUGUSTA WILLIAMS: Right.

ANNA FISHER-PINKERT: So what motivates you personally to do the work that you do? Why do you– I ask a lot of people this. Like, why do you get up in the morning and go do this work?

AUGUSTA WILLIAMS: That’s a great question. I’ve always been really motivated and passionate about health. And kind of it came more from an infectious disease standpoint, even though that’s not at all the work I’ve ever been directly involved in or do today. But looking at how health burdens can spread throughout society, whether that is through an infectious means or other things, like the health impacts of climate change that are impacting societies at a huge scale.

And I have always been really drawn and motivated by the fact that the science we can do, the actions we can take can have a ripple effect on entire populations and shift the burden of health in a positive direction, bring everyone together with you, as opposed to working on the health of one individual at a time, which is extremely important. But I’m more drawn by shifting the curve for all kind of simultaneously.

ANNA FISHER-PINKERT: It sounds like what you’re saying is, like, we tend to think about, like, an individual’s, like, healthy choices. And that’s how their health is going to improve, as opposed to saying, like, let’s look at the whole city. And does it function in a way that creates health for everybody?

AUGUSTA WILLIAMS: Exactly. In environmental health, many of the huge public health successes that have come throughout our time in a civilized society have been related to environmental health, which is really exciting to me, or other areas of public health. When we think of sanitation and kind of the strides we’ve made in that. Seat belt laws is another one that is a huge public health achievement that has saved countless number of lives, that when we think of the wins we’ve had over time and kind of where we’re headed in the future, I think climate change is really the next big one that we need to tackle. But through public health and interacting with all other sectors of society and important stakeholders, I think we can shift that curve in the correct direction.

ANNA FISHER-PINKERT: I think it’s interesting because probably if you asked someone– if we were doing this interview before the advent of urban sanitation, it would have also seemed like an intractable problem. Like, well, how are we going to get rid of all this waste? That’s not possible.

AUGUSTA WILLIAMS: Exactly, and was another one that required a lot of different stakeholders to come together, because the problem was the health burdens that were being faced by these society members. But you needed the engineers and the urban planners and the city managers to all come together and work through this health lens to solve this public health problem. And I think that’s an interesting comparison to many of the issues that we’re facing today, and even more stakeholders that might need to come to the table to solve some of these.

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• Heat Stress

What is Heat Stress?

Heat stress occurs when the body cannot get rid of excess heat. When this happens, the body's core temperature rises and the heart rate increases. As the body continues to store heat, the person begins to lose concentration and has difficulty focusing on a task, may become irritable or sick, and often loses the desire to drink. The next stage is most often fainting and even death if the person is not cooled down.

Factors that contribute to heat stress are high air temperatures, radiant heat sources, high humidity, direct physical contact with hot objects, and strenuous physical activities.

The Occupational Safety and Health Administration (OSHA) has developed a Heat Stress National Emphasis Program (NEP). The purpose of the program is to protect workers from the increasing threat of heat-related illness in both indoor and outdoor work locations. In conjunction with this, EHS has developed resources to help UI departments put in place an effective Heat Stress Prevention Program. The NEP requires departments establish a program if they have employees that work in outdoor locations, or have indoor employees that are exposed to work temperatures that exceed 80°F. Occupational Safety staff will be contacting several departments to evaluate the risk for heat stress and helping to establish a program, where required.

Contact information and areas of expertise can be found on the  Contact Us  page.

Heat Stress Prevention Program  

• This course covers the signs, symptoms and treatment of heat-related illnesses and how to prevent them from happening.
• Audience: All employees that work outdoors, their supervisors, and their departmental safety person should take this course on a yearly basis. All employees that work inside and are exposed to a Wet Bulb Globe Temperature Effective (WBGTE) above 75°F, their supervisors, and their departmental safety person should also take this course on a yearly basis. 

For further training and registration information, go to  EHS Safety Training.  

Also known as prickly heat, is skin irritation caused by sweat that does not evaporate from the skin. Heat rash is the most common problem in hot work environments.

• Clusters of red bumps on skin
• Often appears on neck, upper chest, folds of skin
• Try to work in a cooler, less humid environment when possible
• Keep the affected area dry

Heat Cramps

Are caused by the loss of body salts and fluid during sweating. Low salt levels in muscles cause painful cramps. Tired muscles—those used for performing the work—are usually the ones most affected by cramps. Cramps may occur during or after working hours.

• Muscle spasms
• Have worker rest in shady, cool area
• Worker should drink water or other cool beverages
• Wait a few hours before allowing worker to return to strenuous work
• Have worker seek medical attention if cramps don't go away

Heat Exhaustion

Is the body's response to loss of water and salt from heavy sweating? 

• Cool, moist skin
• Heavy sweating
• Nausea or vomiting
• Light headedness
• Irritability
• Fast heartbeat
• Have worker sit or lie down in a cool, shady area
• Give worker plenty of water or other cool beverages to drink
• Cool worker with cold compresses/ice packs
• Call 911 if signs or symptoms worsen or do not improve within 60 minutes.
• Do not return to work that day

Heat Stroke

The most serious form of heat-related illness happens when the body becomes unable to regulate its core temperature. Sweating stops and the body can no longer rid itself of excess heat.

• Excessive sweating or red, hot, dry skin
• Very high body temperature
• Place worker in shady, cool area 
• Loosen clothing, remove outer clothing
• Fan air on worker; cold packs in armpits
• Wet worker with cool water; apply ice packs, cool compresses, or ice if available
• Provide fluids (preferably water) as soon as possible 
• Stay with worker until help arrives 

General Controls

• Monitor the heat index or wet bulb globe temperature throughout the day.
• Allow time for employees to adjust to hot jobs when possible. It often takes two to three weeks for an employee to become acclimated to a hot environment.
• Adjust the work schedule, if possible. Assign heavier work on cooler days or during the cooler part of the day.
• Establish a schedule for work and rest periods during hot days.
• Train workers to recognize signs and symptoms of heat stress disorders and be prepared to give first aid if necessary.
• Drink at least one cup of fluids for every 20 minutes of work in the heat.

Job Specific Controls

• Use adequate fans for ventilation and cooling, especially when wearing personal protective equipment (PPE).
• Wear light-colored, loose clothing or clothing designed to cool the person down.
• Keep shaded from direct heat where possible (e.g., wear a hat in direct sunshine).
• Reduce the workload. Increase the use of equipment on hot days to reduce physical labor.
• Monitor the employees heart rate while working, core body temperature, recovery heart rate, and weight loss during the shift. Consult with EHS and Employee Health before implementing.  

To determine if it is too hot a heat hazard assessment (HHA) needs to be conducted. This can be done using either the wet bulb globe temperature (WBGT) or the heat index. EHS recommends using the WBGT as it is more accurate, and the method OSHA uses in issuing citations.  

If you are working outside you can use the WBGT from the Kinnick Weather station and use WBGT HHA Worksheet to complete the HHA. An Excel version of the WBGT HHA is also available that will automatically update with the current WBGT, if the spreadsheet is downloaded to your computer, and color code based on the risk. If you are working inside you will need to use a WBGT meter along with 1 of the worksheets. 

The heat index HHA can only be used for outside locations. The easiest way to complete the heat index HHA is to use the OSHA NIOSH Heat safety tool app for Android or IOS . If you do not have the app you can use the HI HHA Worksheet to complete the assessment.

• Wet Bulb Globe Temperature Heat Hazard Assessment Instructions
• Excel Wet Bulb Globe Temperature Heat Hazard Assessment
• Heat Index Heat Hazard Assessment Worksheet

External Links

• Kinnick Weather station
• OSHA Safety and Health Topic: Occupational Heat Exposure
• OSHA NIOSH Heat Safety Tool for Android
• OSHA NIOSH Heat Safety Tool for iPhone
• OSHA Quick Card: Protecting Workers from Heat Stress
• OSHA Fact Sheet: Protecting Workers from the Effects of Heat

Occupational

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• Ladder Safety
• Local Exhaust Ventilation (LEV)
• Lockout/Tagout Program
• Machine Guarding
• Office Safety
• Personal Protective Equipment (PPE)
• Respirator (Required and Voluntary)
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• Welding and Cutting

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Climate Change Impact of Heat Stress on Labor Productivity and Decent Work

Basic page sidebar menu perry world house, may 28, 2023 by sévane ananian | perry world house.

Sévane Ananian is a research specialist at the International Labour Organization (ILO). This thought piece was written for the 2023 Perry World House Global Shifts Colloquium, “ Living with Extreme Heat: Our Shared Future ,” and draws on on a 2019 ILO report by Tahmina Karimova, Tord Kjelltrom, Nicolas Maitre, Matthias Otto, and Catherine Saget,“ Working on a warmer planet: The effect of heat stress on productivity and decent work . ”  The colloquium was made possible in part by a grant from Carnegie Corporation of New York.

Heat stress is projected to reduce total working hours worldwide by 2.2 percent

Excessive heat is an occupational and safety hazard. Above a certain threshold of heat, the body’s internal regulation mechanisms are not able to maintain body temperature at a level required for normal functioning. This entails increased risks of discomfort, physical functions limitations, and eventually injuries and heat-related illness. Body temperatures higher than 38°C impair physical and cognitive functions, while the risk of organ damage, loss of consciousness, and ultimately death increase sharply when body temperatures rise above 40.6°C . For workers, exposure to extreme heat can cause occupational illnesses, increase risk of injury, and lower productivity through natural defense mechanisms such as slowing down, taking more frequent and longer breaks, or limiting working hours. For economies, it threatens their productivity.

Assuming a pathway toward a 1.5°C rise in global temperatures by the end of the 21st century, the ILO projected that 2.2 percent of total working hours will be lost to high temperatures globally in 2030 - a productivity loss equivalent to 80 million full-time jobs. However, since it posits that work is carried out in the shade, this estimate is conservative. If instead, work is carried out in the sun, the projected loss of working hours worldwide goes up to 3.8 percent, or 136 million full-time jobs. With the increase of temperatures beyond 2030, it is expected that climate warming will reduce labor productivity even further.

Agricultural and construction workers are expected to be the worst affected

Increased heat is felt differently across occupations and industries. Physically demanding jobs and those that involve prolonged work outside are particularly impacted by high levels of heat. In this framework, agricultural and construction workers are expected to be the worst affected. According to ILO estimates, these two sectors of activities will account for 60 percent and 19 percent of the working hours lost to heat stress in 2030, respectively.

Further increases in temperature will make agriculture unproductive in some areas, displacing many workers. Other employment sectors are projected to account for an increasing number of working hours lost to heat stress, in part because the share of these industries in total employment is expected to rise in some countries. This is especially the case for construction, which represented only 6 percent of the total hours lost in 1995.

In Southern Asia and Western Africa, the number of working hours lost to heat stress will be particularly high

Projections show that Southern Asia and Western Africa could be the regions worst affected by heat stress. Heat stress is expected to lead to the loss of approximately 5 percent of working hours in these two subregions in 2030, corresponding to approximately 43 million and 9 million full time jobs, respectively. Other regions such as Southeast Asia and Central Africa are also expected to experience a reduction in working hours above the global average. Indeed, in areas located in tropical and subtropical latitudes, the combination of extreme temperature and large shares of total employment in agriculture make heat stress a substantial risk. The European subregions should experience a smaller impact, with an estimated loss in working hours below 0.1 percent. Specifically, most of the working hours lost in Western, Northern, and Southern Europe are expected to be in the construction sector, a pattern also anticipated for North America and the Arab states.

In this context, the negative consequences of extreme heat on working hours and labor productivity are concentrated in subregions with already precarious labor market conditions and degraded employment quality. Productivity losses due to heat stress tend to be larger in regions with low social protection coverage rates, high shares of informal workers in total employment, and high working poverty rates.

International labor standards provide guidelines to adapt to heat-related hazards

The ILO’s 2015 Guidelines for a just transition towards environmentally sustainable economies and societies for all provide practical orientation for government and social partners on how to design, implement, and monitor policies and measures that can tackle the labor implications of climate change in accordance with national circumstances and priorities.

In particular, the guidelines recommend governments, employers, and workers to conduct assessments of increased or new occupational safety and health (OSH) risks that result from climate change and identify adequate prevention and protection measures to ensure occupational safety and health. By making the adoption of a national OSH policy an obligation to “prevent accidents and injury to health arising out of, linked with or occurring in the course of work”, the ILO Occupational Safety and Health Convention No. 155   promotes a framework for managing extreme heat at workplaces. The accompanying Recommendation No. 164 highlights that a national OSH policy should include measures dealing with “temperature, humidity and movement of air in the workplaces”. Other international labor standards also offer useful tools for the management of heat stress, such as the Hygiene (Commerces and offices) Convention No. 120   and the Protection of Workers’ Health Recommendation No 97 .

Social dialogue is instrumental

As underscored by the ILO Guidelines for a just transition, the design and implementation of policies aiming to mitigate and adapt to climate change must involve workers and employers’ organizations alongside the government . Workers and employers are best placed to design and implement heat stress policies that meet their specific needs.

Therefore, social dialogue is instrumental to the development of national OSH policies . In addition, collective bargaining offers a framework to employers and workers to develop tailored measures dealing with high temperature, including at the sectoral and company level. For instance, a collective bargaining agreement in Canada foresees that when the designated temperature index exceeds 39°C, workers may choose either to be paid an additional 25 percent of their regular hourly rate for the shift or to be excused from the shift.

Governments, employers, and workers can reduce vulnerability to heat stress through regulation, adequate infrastructures, and technology, as well as capacity building

Guided by international standards, policy is key to facilitating behavioral changes among employers and individual workers and to promote the development of measures tackling occupational heat stress. Examples of regulations include the prescription of a maximum temperature to which workers may be exposed and the adoption of measures to prevent excessive body heat. Beyond the regulations set by governments, employers play a critical role in the implementation of effective adaptation measures to limit the impact of heat stress. As stated in ILO Convention 155, employers are to “ensure that so far as is reasonably practicable, workplaces, machinery, equipment and processes under their control are safe and without risk to health”. Heat-related hazards should hence be considered in the OSH management system implemented by the employer with the participation of the workers.

Complementary to OSH standards, measures for the improvement of early warning systems for heat events and the monitoring of on-site weather conditions are particularly relevant to enable workers and employers to adapt to heat stress conditions. Raising awareness about the effects of extreme heat, including heat-related illnesses and training on recognizing and managing heat stress are also part of the preventive measures. In addition, the enforcement of policies aiming to improve the characteristics of buildings and developing adequate infrastructures. For instance, access to a safe water supply should also be considered in the strategies to protect workers against heat stress.

In agriculture, long-term options for reducing the consequences of extreme heat include the promotion of mechanization and skill development, both to limit physical demands and to ensure higher productivity and improved food security. Policy design may also take into consideration the payment system, as evidence shows that piecework, for instance, is associated with a greater risk of health-related illness, probably because economic incentives prompt workers to work longer hours and take fewer breaks . For outdoor workers, ensuring their regular access to drinking water and shade and providing them with personal protective equipment and appropriate clothing is essential, and must be included in companies’ adaptation plans.

Social protection helps workers and their families adapt to the consequences of heat stress

Social protection policies are key to defending workers against the detrimental effects of heat that jeopardize their ability to earn income. Without social protection, not only may lost output due to heat stress translate into reduced wages and incomes, but workers are also less likely to have healthcare coverage that could help them cope with the health effects of working in high temperatures. Social protection policies, such as unemployment insurance, also have the capacity to facilitate workers transitioning to sectors that are growing. In agricultural areas, where heat stress is expected to displace workers, ensuring full social protection coverage is particularly relevant.

Mitigation efforts also reduce heat-related hazards.

Climate change mitigation is any “human intervention to reduce the sources or enhance the sinks of greenhouse gases” , including decarbonization of the energy sector, electrification of transport, promotion of sustainable agriculture, reforestation and afforestation, and investment in carbon capture and storage technologies. Mitigation involves structural changes in various sectors, including energy, transport, and agriculture and construction, which are projected to create a net employment gain at the global level .

As the COVID-19 crisis ceases to be the only OSH priority, many countries are realizing the impact of heat on workers' health and their export industry. For instance, coffee plantations in Vietnam and the tomato industry in Mexico are currently collaborating with the ILO and universities to monitor on-site temperature conditions and workers' health.

The statements made and views expressed in this article are solely the responsibility of the authors.

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Effect of heat stress on DNA damage: a systematic literature review

• Review Paper
• Published: 30 September 2022
• Volume 66 , pages 2147–2158, ( 2022 )

Cite this article

• Peymaneh Habibi 1 ,
• Seyed Naser Ostad 2 ,
• Ahad Heydari 3 ,
• Shima Aliebrahimi 4 ,
• Vahideh Montazeri 4 ,
• Abbas Rahimi Foroushani 5 ,
• Mohammad Reza Monazzam 1 ,
• Mahmoud Ghazi-Khansari 6 &
• Farideh Golbabaei 1  

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Thermal stress has a direct effect on various types of DNA damage, which depends on the stage of the cell cycle when the cell is exposed to different climate conditions. A literature review was conducted to systematically investigate and assess the overall effect of heat stress and DNA damage following heat exposure. In this study, electronic databases including PubMed, Scopus, and Web of Science were searched to find relevant literature on DNA damage in different ambient temperatures. Outcomes included (1) measurement of DNA damage in heat exposure, (2) three different quantification methods (comet assay, 8-hydroxy-2-deoxyguanosine (8-OHdG), and γ-H2AX), and (3) protocols used for moderate (31) and high temperatures (42). The evidence shows that long exposure and very high temperature can induce an increase in DNA damage through aggregate in natural proteins, ROS generation, cell death, and reproductive damage in hot-humid and hot-dry climate conditions. A substantial increase in DNA damage occurs following acute heat stress exposure, especially in tropical and subtropical climate conditions. The results of this systematic literature review showed a positive association between thermal stress exposure and inhibition of repair of DNA damage.

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Introduction

The effect of global warming on climate change has been noticeable throughout the increase in heat strain among humans. Health risks due to heat stress have become a major concern for experts (Golbabaei et al. 2020 ). The direct effects of thermal stress on human health include fatigue (Kjellstrom et al. 2014 ), reduced psychomotor performance (Xiang et al. 2014 ), reduced alertness, increased core body temperature (Habibi et al. 2015 ), increased sweat rate (Vanos et al. 2019 ), and dehydration. It is well known that thermal stress at the workplace can cause occupational health hazards, and climate change can aggravate the effects of these hazards and create new risks (Habibi et al. 2021a ). Thus, maintaining safety and health promotion in warm workplaces will keep being an important challenge (Habibi et al. 2021b ). Heat stress (heat shock, hyperthermia) is considered an important factor for biological effects, damage to cellular structures, interference with important functions, and disturbance of vital enzymes activity (Lepock and Borrelli 2005 ). Cell injury such as genotoxicity, oxidative stress, and DNA damage is induced by hot-dry and hot-wet environments in several workplaces including steel industry and agriculture. Cellular responses to thermal stress such as various cellular compartments and enzymes such as activating signaling pathways induce the transient heat shock proteins (Hsps) expression (Nasr et al. 2019 ; Richter et al. 2010 ). Heat radiosensitization is a physical hazard in which cells are exposed to thermal stress and ionizing radiation (IR) that can increase double-stranded DNA breaks (DSBs) and other agents. In addition, heat stress can inhibit some DNA repair pathways including base excision repair (BER) and nucleotide excision repair (NER) (Kantidze et al. 2016 ). The damaged DNA, the opposite of lipids and proteins, cannot be removed through cell mechanisms and must be repaired, otherwise, it can lead to lethal mutations and cancer cells (Evans et al. 2004 ). Physical (heat stress and radiation (ultraviolet (UV) and IR radiation)) and chemical agents can inhibit DNA repair mechanisms and act as exogenous DNA damage factors (Mohammadi et al. 2021 ). In summary, high and moderate temperature directly results in DNA damage and effect on cellular macromolecules functions, respectively (Milani and Horsman 2008 ). Interestingly, the type of the heat stress-induced DNA damage depends on the stage of the cell cycle, such as S phase (which leads to top 1 dependent single-stranded DNA breaks (SSBs)) or G1–G2 stage (which induces DSB formation), when the cell is exposed to different climate conditions (Kantidze et al. 2016 ). Although some studies have investigated the effect of heat stress on DNA damage, no comprehensive study has been done to evaluate the effect of different temperatures and humidity on DNA damage. DNA damage in response to exposure to thermal stress and whole-body hyperthermia (WBH) in mammals has not been investigated thoroughly in a systematic literature review. The aim of this study was to systematically investigate data reporting DNA damage following heat stress exposure, and explore their relationships. There are inconsistencies about thermal stress-induced oxidative DNA damage in exposure to very hot and warm climate conditions, and this review will aim to clear this subject. Furthermore, the possible physiological and pathological responses to heat stress-induced DNA damage need to be investigated in different climate conditions.

Materials and methods

Bibliography search strategy.

A systematic review was performed according to the Preferred Reporting Items for Systematic Reviews (PRISMA) statement (Shamseer et al. 2015 ). Databases such as PubMed, Scopus, and Web of Science were searched for articles published from 2000 to 18.04.2020. All the search terms related to “heat stress” were found by the PubMed Mesh system, and also a specialist’s opinion about synonyms of terms in a combination with “DNA damage.” The search syntax was produced using keywords and synonyms searched in the title, abstract, or keyword fields in the databases. In addition, to find relevant studies, the reference lists of the included studies were manually searched. Databases were investigated using the following search syntaxes to find the relevant studies.

TITLE-ABS-KEY(“Heat shock” OR “heat stress” OR “IR radiation” OR Hyperthermia OR “DNA injury” OR (DNA AND injury*)) AND TITLE-ABS-KEY(“DNA damage” OR (DNA AND damage*) OR “DNA repair” OR (DNA AND repair*) OR “DNA replication” OR (DNA AND replicate*)).

At first, all titles and abstracts were checked for inclusion by two reviewers (PH and AH). Then, the full texts of the articles were reviewed ( n  = 15). Two articles were included from the reference lists and one article was included from an additional search in the Google Scholar.

Eligibility criteria

The “PICO” strategy for systematic exploratory review was: P (humans and animals), I (heat stress), C (DNA), and O (DNA damage). The inclusion/exclusion criteria are shown in Table 1 . In addition, the full-text articles and conference papers that were not available were excluded from the study.

Inclusion/exclusion criteria

All published studies were checked for the following criteria: (1) the study assessed humans and animals; and (2) combining keywords used heat stress, heat shock, heat strain, IR radiation, DNA damage, DNA repair, and DNA replication. Note that for this review, we used the term DNA damage to encompass SSBs, DSBs, and nucleotide base oxidation. One investigator initially reviewed records extracted from all databases and applied the inclusion/exclusion criteria to identify eligible studies for inclusion in agreement with at least three authors. The inclusion/exclusion criteria are shown in Table 1 . The ambient temperature was defined as hot temperature (over 41) and moderate temperature (around 31–33) (Golbabaei et al. 2020 ; Prandini et al. 2005 ). To minimize the limitation of various biological samples, studies using urine samples, RBC count, and muscle cells were also excluded. In addition, mathematical models and dynamics of the heat stress response of the cells were excluded. We concentrated on studies with clear and direct effects of thermal stress exposure on DNA damage and did not include the studies in which physical and chemical hazards were a byproduct of exposure to other agents (e.g., air pollution, cancer therapy, and acute injury) (Table 1 ).

Data extraction and quality assessment

After conducting screening and selection, two checklists were applied for data extraction. The first checklist included the characteristics of the studies such as the first author’s name, publication year, location, participants, biomarkers, protocols, techniques, findings, and quality scores. Two independent reviewers (PH and AH) assessed the methodological quality of included studies using the 16-item quality assessment tool for studies with diverse designs (QATSDD) (Sirriyeh et al. 2012 ). The characteristics of the participants (humans and animals such as the sample size, age, and sex) for in vivo studies, type of cells for in vitro studies, climate conditions (ambient temperature, relative humidity, etc.), assayed biomarkers, and methods of DNA quantification were extracted by two investigators.

The outcome measure of DNA damage was expressed using multiple descriptors, and about the comet assay technique including DNA in the tail (%), tail moment, and the length of DNA migration (tail length) (Evans et al. 2004 ). In this study, 8-OHdG, γ-H2AX, and HSPs were as considered biomarkers and tRNAs sensors. In addition, the analytical approach including high-performance liquid chromatography (HPLC), enzyme-linked immunosorbent assay (ELISA), fluorescent in situ hybridization (FISH), 8-OHdG (pg/ml), and 8-OHdG/105 dG was also reported [8-OHdG (ng/ml) or (pg/ml) and 8-OHdG/105 dG correspond to HPLC and ELISA methods, respectively].

Search results

Figure  1 presents a detailed list of search results. The initial electronic search yielded 36,902 papers. Then, after removing duplicate records, 31,683 papers were screened through reviewing their titles and abstracts. In total, 47 articles were excluded. After title and abstract screening, 15 articles were considered eligible for full-text evaluation. Subsequently, 17 articles were included in the qualitative analysis. Table 2 summarizes the characteristics of the included studies.

Flow diagram of screening process of included studies the heat stress on DNA damage

Descriptive analysis

Our review identified 17 relevant studies out of 36,902 were eligible for data extraction, of which 12 presented in vitro studies in different climate conditions and cells including human HeLa cells, human fibroblasts, and human ESC. Five were in vivo studies in animal and human cells including lymphocytes, germ cells, cerebellum and hippocampus, and spermatozoa. The results of these studies showed that the effect of thermal stress on DNA damage had the greatest impact. Most of the studies have also emphasized the impacts of thermal stress including the spread of negative impacts on oxidative DNA damage in the future, how high temperatures and humidity creates hyperthermic cell killing risks and inhibit the repair of DNA damage challenges; how thermal stress will affect the integrity of the genome, and how these are often intertwined with heat shock responses. Four publications came from Russia, three from the USA, two from Japan, two from Canada, one from Australia, one from India, one from Taiwan, one from Italy, one from Ukraine, and one from Scotland. To measure DNA damage, five studies used comet assay, two used FISH, three used ELISA kit, two used surviving fraction, one used MN assay, one used gene chip system and bioinformatics tools, one used gel electrophoresis (EMSA), one used PFGE, and one used immunofluorescence. Concerning the biomarker and the techniques used to quantify DNA damage, 2 studies used 8-OHdG (Houston et al. 2018 ; Liu et al. 2015 ) with either comet assay or ELISA kit. A total of 4 studies used tail moment, tail length, and tail DNA (%), with the comet assay technique (Roti Roti et al. 2010 ; Ryabchenko et al. 2013 ; Velichko et al. 2012 , 2015 ), one used HSF with FISH or surviving fraction (Bettaieb and Averill-Bates 2015 ), and 3 studies used γ-H2AX with immunofluorescence (molecular probes), PFGE, and comet assay (Hunt et al. 2007 ; Laszlo and Fleischer 2009 ; Velichko et al. 2012 ). Of the studies using different climate conditions, all of the studies were conducted in a range of (33–50) mild to hot temperatures.

In our review, we explored the effects of heat stress on DNA damage in various cells. Heat stress triggers active and passive cellular reactions that depend on environmental conditions as an important factor and the dominant response. High temperatures can induce the denaturation of thermal proteins and impose adverse effects on local proteins, disrupting protein synthesis and inducing DNA damage via affecting intracellular metabolic pathways and components (Lepock and Borrelli 2005 ). On the other hand, DNA repair suppression and complications such as cellular apoptosis are triggered by exposure to physical stressors such as radiation, thermal stress, and cytotoxic agents. Heat stress can lead to a variety of DNA damages, depending on the cell cycle phase and the ambient temperature. Regarding the global warming trend, it is necessary to understand the genetic damages caused by thermal stress, the pathogenic mechanisms of heat-related illnesses (HRIs), and related physiological and perceptual responses at molecular levels to develop preventive and therapeutic strategies in the future.

Sensitive molecular markers of DNA damage

HSPs belong to a family of the proteins produced by cells in response to stress. These proteins were first recognized in relation to heat shock, but now, they are known to be expressed in response to other stresses such as exposure to cold and UV radiation, during wound healing and tissue regeneration, and in diseases that are directly related to inflammation. The upregulation of these proteins under these conditions is regulated at the transcriptional level. The tight regulation of the expression of heat shock proteins is an important part of the heat shock reaction and is primarily induced by the heat shock factor. These proteins are responsible for preserving cellular integrity and regulating the signaling pathways that are essential for cell survival. HSPs include a combination of groups known as HSP27 (also named HSPB), HSP60 (HSPD), HSP70 (HSPA), HSP90 (HSPC), and HSP110 (also called HSPH), which have been recognized as highly preserved guardians of molecules and have remained highly protected throughout evolution (Dubrez et al. 2020 ). In a study conducted by Yang et al., it was suggested to use HSP70 as a biomarker for heat-induced DNA damage (Yang et al. 2008 ). Wu et al. also reported that HSPs could provide useful biomarkers for assessing cellular damages among those working in hot environments (Wu et al. 2001 ). The quantification of γ-H2AX was recommended as a primary marker to assess cellular responses and a sensitive tool for detection of DNA DSBs, resolution, and recognizing DNA damage initiation (Mah et al. 2010 ). Lazlo et al., however, revealed no role for heat stress-induced γ-H2AX in assessing DSBs and cell death (Laszlo and Fleischer 2009 ). In this regard, the mechanisms by which γ-H2AX is induced following thermal stress should be further investigated.

Heat stress and gene response

There are a few studies on the effects of delayed heat stress on gene expression regulation and cellular function. Heat stress has been noted to trigger p21-dependent cell aging only in the early S phase, which is similar to cell cycle arrest that induces DNA SSBs (Velichko et al. 2015 ). Harrouk et al. showed that the exposure of sperms to heat during fertilization could alter the expression of DNA repair genes in the early stages of embryonic development (Harrouk et al. 2000 ). In an animal model, exposure to thermal stress could reduce the expression of polyADP ribose polymerase (PARP) through two pathways, including BER and NER, which contribute to the detection of SSBs (Tramontano et al. 2000 ; Van’t Veer et al. 2002 ). Also, exposure to heat stress (the range of 39–42 °C) increased DNA damage in Sertoli cells and significantly boosted oxidative stress-induced damages in the exposed cells compared to the control group (Nezhad et al. 2013 ). Cryptorchidism can lead to thermal stress, in which the expression of the repair genes acting in the final stages of DNA repair is reduced, such as DNA polymerase beta, which promotes the recruit of DNA ligase III (Tramontano et al. 2000 ). An in vitro study showed that cigarette smoking could enhance the formation of micronuclei in the human lymphocytes exposed to heat stress (Feng et al. 1998 ). The formation of heat-induced γ-H2AX foci is dependent on ataxia-telangiectasia mutated (ATM) protein, which is known as a DNA damage sensor. Moreover, thermal stress, by activating a subset of ATM proteins, can interfere with IR-induced signaling pathways involved in the repair of chromosomal DNA DSBs. Hunt et al. showed that high temperatures could enhance cells’ sensitivity to radiation (Hunt et al. 2007 ). Heat stress was also shown to induce partial DNA replication, boost cellular DNA content, and cause excessive centrosome growth in the early S phase, triggering an aging-like phenotype in human HeLa cells (Petrova et al. 2016 ). Further investigations are warranted to divulge the molecular mechanisms underlying the exit of tumor cells from the aging stage under various thermal stressors. Heat stress can stimulate different DNA damage responses (DDRs) in the S phase, leading to the suppression of DNA replication (the S phase) and the formation of DNA DSBs (in the interphase at the stages of G1 and G2), which depend on H2AX phosphorylation and γ-H2AX foci formation, respectively (Velichko et al. 2015 ). Heat stress-induced DSBs and DNA damage depend on the cell type, cell cycle phase, and ambient temperature (Kantidze et al. 2016 ). Nevertheless, more studies are needed to confirm the role of hyperthermia in inducing DSBs. The combination of heat stress and infrared radiation was shown to exaggerate genotoxic effects and DNA damage in cells (Ryabchenko et al. 2013 ). A study revealed a link between heat stress-induced tRNA depletion and motility in HeLa cells. Research has suggested that heat stress-induced tRNA granules in the nucleus may be applicable as important sensors for detecting DNA damage (Miyagawa et al. 2012 ). Tabuchi et al. mentioned that mild heat stress (41 °C for 30 min) could induce the differential expression of common genes in normal human fibroblasts (Tabuchi et al. 2013 ). Some studies have negated a direct role for heat stress in creating DSBs (Hunt et al. 2007 ; Laszlo and Fleischer 2009 ); however, others have reported that heat stress can provoke DSBs via inducing γ-H2AX (Nam et al. 2013 ; Velichko et al. 2012 ).

Heat stress and HSPs

In the cells exposed to various climatic conditions, especially hot-dry and hot-humid, HSPs (HSP27, HSP70, and HSP90) can promote cell death and inflammatory responses (Maghsudlu and Yazd 2017 ; Nam et al. 2013 ). Yan et al. asserted the main role of HSPs in cellular responses to heat stress and protecting cells against heat stress by regulating the body’s temperature and facilitating the intracellular trafficking of repair proteins, as well as inducing either the refolding of denatured proteins or their degradation following stress or injury. Therefore, HSPs can prevent the adverse metabolic effects of incorrect protein folding and subsequently proteotoxic-induced cell death (Yan et al. 2006 ). Stocker et al. noted that heat shock could affect cellular proliferation by blocking the entry of precursors into the cell cycle; however, further studies are needed to clarify this issue (Stocker et al. 2006 ). After exposure to heat stress, HSP70 levels alter in lymphocytes and plasma, suggesting these proteins as biomarkers to investigate protective responses. Nevertheless, other factors regulating the production of intracellular and extracellular stress proteins remain completely unknown (Yang et al. 2008 ). A close relationship has been noted between HSP70 expression and DNA damage in peripheral blood lymphocytes (Venugopal et al. 2018 ). Heat stress can also increase HSP72 plasma level, a biomarker of cardiovascular disease (Tang-Chun et al. 1995 ). In the lymphocytes exposed to acute heat stress, there was a good association between positive autoantibodies (respective to negative antibodies) and increased DNA damage (Yili et al. 1997 ). The expression of HSP70 was reported as a sensitive biomarker for a wide range of detrimental physical and chemical stressors in cultured cells (Bierkens 2000 ). Thermal stress induces a wide range of complex cellular responses, the most important of which is the induction of HSPs, ROS production, disruption of proteins, DNA and RNA damage, abnormal protein homeostasis, imbalanced cell cycle progression, and, finally, cell death (Tabuchi et al. 2013 ). Nasr et al. indicated that mitochondrial proteins, especially HSP70 proteins, could protect DNA-binding proteins and oxidative stress-scavenging systems following exposure to thermal stress up to 52 °C (Nasr et al. 2019 ).

Heat stress exposure and effect on male fertility and pregnancy outcome

Normal testicular function depends on the temperature of the body and the ambient environment. A rise in testes temperature may occur in the men residing in tropical and subtropical countries, especially during summer and in those working in hot outdoor environments. Exposure to occupational heat stress happens in various professions requiring working in hot environments, such as bakery, construction, municipal services, farming, mining, and welding. Also, heavy workload, prolonged exposure to heat, reduced air movement around the skin, and wearing personal protective equipment (PPE) can lead to an increase in the core body temperature and alteration in other physiological parameters in hot and humid environments (Habibi et al. 2021b ; Paul et al. 2008 ). Thermal stress significantly affects spermatogenesis in mammals, inflicting damage to DNA damage in germ cells and increasing apoptosis in these cells, culminating in infertility due to processes such as hypoxia, oxidative stress, and apoptosis (Paul et al. 2009 ). Heat stress can increase the temperature in testes, increasing the production of abnormal and immature sperms and leading to infertility and ejaculation. In the mice kept in hot environments, there were reports of alterations in DNA integrity, reduced sperm quality, and loss of germ cells with normal chromatin packaging. Exposure to thermal stress (up to 40 °C) led to the premature loss of the fetus, spermatocytes, and spermatids. In the thermal range of 40 to 42 °C, there was a report of testicular dysfunction, as well as changes in testicular weight, increased apoptotic biomarkers, and increased rate of death in germ cells (MacLachlan et al. 1995 ; Paul et al. 2008 ). Rockett et al. described an increased rate of apoptosis and the upregulation of heat-induced proteins, Hsp70-1 and Hsp70-3, in spermatocytes after exposure to 43 °C for 20 min. Also, heat can increase DNA SB in Pachytene stage spermatocytes via inducing primary cellular responses leading to the overexpression of γ-H2AX, a highly specific and sensitive molecular marker (Rockett et al. 2001 ). The ability to reproduce is affected by exposure to extreme heat, as evidenced by the abnormal growth of germ cells and reduced sperm quality. Exposure to heat stress increases mitochondrial ROS levels in sperms and induces oxidative DNA damage and DNA SSBs in germ cells in men (Houston et al. 2018 ). Heat stress also upregulates the mRNA expression of the hypoxia-inducible factor 1 alpha (Hif1a) gene and promotes mild testicular hyperthermia and the translocation of the HIF1A protein to the nucleus in germ cells (Paul et al. 2009 ). As well, Pena et al., in a study on boars, showed that heat stress increased DNA damage in sperms and decreased sperm quantity in a hot summer. It has been suggested that DNA integrity assessment in the sperm nucleus can be a good indicator of sperm quality in exposure to hot weather (Peña et al. 2019 ), especially in tropical and subtropical areas where changes in temperature are beyond the thermal comfort zone of animals and humans (Penã et al. 2017 ). In a female animal model exposed to heat stress (36 °C for 24 h), a decrease in the number of embryos and an increase in heat stress responses were observed (Zhu and Setchell 2004 ). In male mice, the whole-body temperature was shown to affect sperm count, with a decrease in fertility rate within 10 to 14 days after exposure to thermal stress (36 °C for 24 h) (Yaeram et al. 2006 ). In an investigation on the effects of thermal stress on mice sperm count, the results showed a reduction in fertility rate, altered fetal weight, and changes in the expression of the repairing genes involved in embryonic growth before implantation and in the single-cell stage (Harrouk et al. 2000 ). Alekseenko et al. showed that heat stress could induce apoptosis via different mechanisms in human embryonic stem cells (ESC) and their differentiating daughter cells (Alekseenko et al. 2012 ).

Limitations and current research gaps and future directions

Due to gaps in our knowledge about the effects of exposure to heat stress on DNA damage, there is a need for further investigations. As mentioned before, two studies have addressed these effects in animal models, and one study has been conducted on human workers. Other studies have examined these effects in vitro (Table 1 ). In addition, there are no epidemiological studies on the epidemiological aspects of diseases and the effects of heat stress on DNA alterations in men and women exposed to heat in different work environments, which should be addressed in upcoming studies. In addition, the effects of heat stress on fertility (spermatozoa) observed in male animal models should also be evaluated in humans (Houston et al. 2018 ). We also need to scrutinize the effects of heat stress at the cellular level on the reproductive organs of both females and males. Animal and human studies are needed to discover all the mechanisms behind heat stress-induced formation of DNA DSBs.

This is important considering that the outcomes of studies can be variable depending on parameters such as study design, the animal used, ambient temperature, relative humidity, the number of animals, and the duration of exposure to heat. So, these determinants should be taken into mind when generalizing results to humans (Kampinga et al. 2005 ). Such new approaches can help characterize the concepts related to thermal stress biology and its molecular indicators and investigate their relationships with epidemiological parameters, such as the incidence and prevalence of diseases. In addition, some studies have identified the adverse effects of heat stress (e.g., inducing cell damage, altering cellular function, and triggering apoptosis) on immune cells such as monocyte-derived dendritic cells (DCs) in vitro; however, these effects have not been validated in vivo that should be considered in future studies (Beachy and Repasky 2011 ). Climate change and global warming have potentially exposed millions of humans and animals to hot-humid and hot-dry environments. Therefore, it is essential to characterize the cellular damages caused by this phenomenon and its relationship with HSPs’ levels in tissues and organs so that we can implement preventive interventions, management strategies, and protective instructions in different societies and countries according to climate conditions (Habibi et al. 2021b ; Venugopal et al. 2018 ). Finally, if a link between heat stress and DNA damage is established, it will be necessary to review and adjust the regulations of working in hot-humid and hot-dry environments so that the health of employees is warranted.

Heat stress induces DNA DSBs in human and animal models, which is one of the deadliest types of DNA damage. Nonetheless, the effects of heat stress on the molecular mechanisms involved in DNA damage are not well-understood. Although cellular and molecular responses to heat stress have been extensively studied in recent decades, in this systematic review of the literature, we found that a few studies have been conducted to scrutinize the effects of heat stress on DNA damage, DNA replication, and nucleic acid repair mechanisms. Studying the physiological responses to heat stress and their molecular mechanisms can help understand the biological effects of heat stress, especially in tropical and subtropical countries. As well, identifying the main biomarkers of molecular responses to heat stress, including HSPs and other related biomarkers, can help early detect heat-induced cellular damages and destructive effects, especially in people working in hot environments. Finally, it is required to implement appropriate interventions, such as technical-engineering, managerial, and therapeutic measures, and to design and develop standard preventive guidelines to avoid the rise of heat-induced diseases.

Alekseenko LL, Zemelko VI, Zenin VV, Pugovkina NA, Kozhukharova IV, Kovaleva ZV, ..., Nikolsky NN (2012a) Heat shock induces apoptosis in human embryonic stem cells but a premature senescence phenotype in their differentiated progeny. Cell Cycle 11(17):3260-3269. https://doi.org/10.4161/cc.21595

Beachy SH, Repasky EA (2011) Toward establishment of temperature thresholds for immunological impact of heat exposure in humans. Int J Hyperth 27(4):344–352

Article   Google Scholar  

Bettaieb A, Averill-Bates DA (2015) Thermotolerance induced at a mild temperature of 40°C alleviates heat shock-induced ER stress and apoptosis in HeLa cells. Biochimica Et Biophysica Acta - Molecular Cell Research 1853(1):52–62. https://doi.org/10.1016/j.bbamcr.2014.09.016

Article   CAS   Google Scholar  

Bierkens JG (2000) Applications and pitfalls of stress-proteins in biomonitoring. Toxicology 153(1–3):61–72

Dubrez L, Causse S, Borges Bonan N, Dumetier B, Garrido C (2020) Heat-shock proteins: chaperoning DNA repair. Oncogene 39(3):516–529. https://doi.org/10.1038/s41388-019-1016-y

Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: induction, repair and significance. Mutation Research/reviews in Mutation Research 567(1):1–61

Feng H, Sun L, Li Y, Yang B (1998) Study on induced mutagenesis interaction of the high temperature and/or cigarette smoke. Wei sheng yan jiu= Journal of hygiene research, 27(6):379–381

Golbabaei F, Heydari A, Moradi G, Dehghan H, Moradi A, Habibi P (2020) The effect of cooling vests on physiological and perceptual responses: a systematic review. International J Occup Saf Ergon(just-accepted) 1–36.

Habibi P, Momeni R, Dehghan H (2015) Relationship of environmental, physiological, and perceptual heat stress indices in Iranian Men. International Journal of Preventive Medicine 6

Habibi, P., Moradi, G., Moradi, A., & Golbabaei, F. (2021a). A review on advanced functional photonic fabric for enhanced thermoregulating performance. Environmental Nanotechnology, Monitoring & Management, 100504.

Habibi P, Moradi G, Moradi A, Heydari A (2021b) The impacts of climate change on occupational heat strain in outdoor workers: a systematic review. Urban Climate 36:100770

Harrouk W, Codrington A, Vinson R, Robaire B, Hales BF (2000) Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutation Research/DNA Repair 461(3):229–241

Houston BJ, Nixon B, Martin JH, De Iuliis GN, Trigg NA, Bromfield EG, ..., Aitken RJ (2018) Heat exposure induces oxidative stress and DNA damage in the male germ line. Biol Reprod 98(4):593-606

Hunt CR, Pandita RK, Laszlo A, Higashikubo R, Agarwal M, Kitamura T, ..., Pandita TK (2007) Hyperthermia activates a subset of ataxia-telangiectasia mutated effectors independent of DNA strand breaks and heat shock protein 70 status. Cancer Res 67(7):3010-3017. https://doi.org/10.1158/0008-5472.can-06-4328

Kampinga HH, Laszlo A, Takahashi A, Mori E, Ohnishi T (2005) DNA double strand breaks do not play a role in heat-induced cell killing [1] (multiple letters). Can Res 65(22):10632–10633. https://doi.org/10.1158/0008-5472.CAN-05-0006

Kantidze OL, Velichko AK, Luzhin AV, Razin SV (2016) Heat Stress-Induced DNA Damage Acta Naturae 8(2):75–78. https://doi.org/10.32607/20758251-2016-8-2-75-78

Kjellstrom T, Lemke B, Hyatt O, Otto M (2014) Climate change and occupational health: a South African perspective. Samj South Afr Med J 104(8), 586-+. https://doi.org/10.7196/samj.8646

Laszlo A, Fleischer I (2009) The heat-induced-H2AX response does not play a role in hyperthermic cell killing. Int J Hyperth 25(3):199–209. https://doi.org/10.1080/02656730802631775

Lepock JR, Borrelli MJ (2005) How do cells respond to their thermal environment? Int J Hyperth 21(8):681–687. https://doi.org/10.1080/02656730500307298

Liu FW, Liu FC, Wang YR, Tsai HI, Yu HP (2015) Aloin protects skin fibroblasts from heat stress-induced oxidative stress damage by regulating the oxidative defense system. PloS one 10(12). https://doi.org/10.1371/journal.pone.0143528

MacLachlan TK, Sang N, Giordano A (1995) Cyclins, cyclin-dependent kinases and cdk inhibitors: implications in cell cycle control and cancer. Critical Reviews™ in Eukaryotic Gene Expression 5(2)

Maghsudlu M, Yazd EF (2017) Heat-induced inflammation and its role in esophageal cancer. J Dig Dis 18(8):431–444. https://doi.org/10.1111/1751-2980.12511

Mah L, El-Osta A, Karagiannis T (2010) γH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 24(4):679–686

Maroni P, Bendinelli P, Tiberio L, Rovetta F, Piccoletti R, Schiaffonati L (2003) In vivo heat-shock response in the brain: signalling pathway and transcription factor activation. Brain Res Mol Brain Res 119(1):90–99. https://doi.org/10.1016/j.molbrainres.2003.08.018

Milani V, Horsman M (2008) Cellular and vascular effects of hyperthermia. Int J Hyperth 24(1):1–2. https://doi.org/10.1080/02656730701858313

Miyagawa R, Mizuno R, Watanabe K, Ijiri K (2012) Formation of tRNA granules in the nucleus of heat-induced human cells. Biochem Biophys Res Commun 418(1):149–155. https://doi.org/10.1016/j.bbrc.2011.12.150

Mohammadi B, Safaiyan A, Habibi P, Moradi G (2021) Evaluation of the acoustic performance of polyurethane foams embedded with rock wool fibers at low-frequency range; design and construction. Appl Acoust 182:108223

Nam JW, Kim SY, Yoon T, Lee YJ, Kil YS, Lee YS, Seo EK (2013) Heat shock factor 1 inducers from the bark of Eucommia ulmoides as cytoprotective agents. Chem Biodivers 10(7):1322–1327. https://doi.org/10.1002/cbdv.201200401

Nasr MA, Dovbeshko GI, Bearne SL, El-Badri N, Matta CF (2019) Heat shock proteins in the “hot” mitochondrion: identity and putative roles. Bioessays 41(9). https://doi.org/10.1002/bies.201900055

Nezhad FS, Lavvaf A, Karimi S (2013) Influence of heat stress on DNA damage on sheep’s Sertoli cells. International Research Journal of Applied and Basic Sciences 6(10):1396–1400

Google Scholar  

Paul C, Murray AA, Spears N, Saunders PT (2008) A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136(1):73–84. https://doi.org/10.1530/rep-08-0036

Paul C, Teng S, Saunders PT (2009) A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 80(5):913–919. https://doi.org/10.1095/biolreprod.108.071779

Penã ST, Gummow B, Parker AJ, Paris DBBP (2017) Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development? Animal Production Science 57(10):1975–1983. https://doi.org/10.1071/AN16079

Peña ST, Stone F, Gummow B, Parker AJ, Paris DBBP (2019) Tropical summer induces DNA fragmentation in boar spermatozoa: implications for evaluating seasonal infertility. Reprod Fertil Dev 31(3):590–601. https://doi.org/10.1071/RD18159

Petrova NV, Velichko AK, Razin SV, Kantidze OL (2016) Early S-phase cell hypersensitivity to heat stress. Cell Cycle 15(3):337–344. https://doi.org/10.1080/15384101.2015.1127477

Prandini MN, Neves A, Lapa AJ, Stavale JN (2005) Mild hypothermia reduces polymorphonuclear leukocytes infiltration in induced brain inflammation. Arq Neuropsiquiatr 63(3B):779–784. https://doi.org/10.1590/s0004-282x2005000500012

Raaphorst GP, LeBlanc JM, Li LF, Yang DP (2005) Hyperthermia responses in cell lines with normal and deficient DNA repairs systems. J Therm Biol 30(6):478–484. https://doi.org/10.1016/j.jtherbio.2005.05.010

Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40(2):253–266

Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ (2001) Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod 65(1):229–239

Roti Roti JL, Pandita RK, Mueller JD, Novak P, Moros EG, Laszlo A (2010) Severe, short-duration (0–3 min) heat shocks (50–52°C) inhibit the repair of DNA damage. Int J Hyperth 26(1):67–78. https://doi.org/10.3109/02656730903417947

Ryabchenko NM, Rodionova NK, Sychevska IS, Muzalev II, Mykhailenko VM, Druzhina MO (2013) Genotoxic effects of radiation and hyperthermia in linear mice with different radiation sensitivity. Cytol Genet 47(1):39–43. https://doi.org/10.3103/s0095452713010088

Shamseer LMD, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. Bmj 2:7647

Sirriyeh R, Lawton R, Gardner P, Armitage G (2012) Reviewing studies with diverse designs: the development and evaluation of a new tool. J Eval Clin Pract 18(4):746–752

Stocker AJ, Madalena CR, Gorab E (2006) The effects of temperature shock on transcription and replication in Rhynchosciara americana (Diptera: Sciaridae). Genetica 126(3):277–290. https://doi.org/10.1007/s10709-005-7407-8

Tabuchi Y, Furusawa Y, Kariya A, Wada S, Ohtsuka K, Kondo T (2013) Common gene expression patterns responsive to mild temperature hyperthermia in normal human fibroblastic cells. Int J Hyperth 29(1):38–50. https://doi.org/10.3109/02656736.2012.753163

Tang-Chun W, Han-Zhen H, Tanguay RM, Yang W, Dai-Gen X, Currie RW, ..., Guo-gao Z (1995) The combined effects of high temperature and carbon monoxide on heat stress response. J Tongji Med Univ 15(3):178-183

Tramontano F, Malanga M, Farina B, Jones R, Quesada P (2000) Heat stress reduces poly (ADPR) polymerase expression in rat testis. Mol Hum Reprod 6(7):575–581

Van’t Veer LJ, Dai H, Van De Vijver MJ, He YD, Hart AA, Mao M, . . ., Witteveen AT (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871): 530–536.

Vanos J, Vecellio DJ, Kjellstrom T (2019) Workplace heat exposure, health protection, and economic impacts: a case study in Canada. Am J Ind Med 62(12):1024–1037. https://doi.org/10.1002/ajim.22966

Velichko AK, Petrova NV, Kantidze OL, Razin SV (2012) Dual effect of heat shock on DNA replication and genome integrity. Mol Biol Cell 23(17):3450–3460. https://doi.org/10.1091/mbc.E11-12-1009

Velichko AK, Petrova NV, Razin SV, Kantidze OL (2015) Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress. Nucleic Acids Res 43(13):6309–6320. https://doi.org/10.1093/nar/gkv573

Venugopal V, Krishnamoorthy M, Venkatesan V, Jaganathan V, Paul S (2018) Occupational heat stress, DNA damage and heat shock protein—a review. Medical Research Archives 6(1)

Venugopal V, Krishnamoorthy M, Venkatesan V, Jaganathan V, Shanmugam R, Kanagaraj K, Paul SF (2019) Association between occupational heat stress and DNA damage in lymphocytes of workers exposed to hot working environments in a steel industry in Southern India. Temperature 6(4):346–359

Wu T, Chen S, Xiao C, Wang C, Pan Q, Wang Z, ..., Tanguay RM (2001) Presence of antibody against the inducible Hsp71 in patients with acute heat-induced illness. Cell Stress Chaperones 6(2):113

Xiang JJ, Bi P, Pisaniello D, Hansen A (2014) Health impacts of workplace heat exposure: an epidemiological review. Ind Health 52(2):91–101. https://doi.org/10.2486/indhealth.2012-0145

Yaeram J, Setchell B, Maddocks S (2006) Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev 18(6):647–653

Yan Y-E, Zhao Y-Q, Wang H, Fan M (2006) Pathophysiological factors underlying heatstroke. Med Hypotheses 67(3):609–617

Yang X, Yuan J, Sun J, Wang H, Liang H, Bai Y, ..., Wang J (2008) Association between heat-shock protein 70 gene polymorphisms and DNA damage in peripheral blood lymphocytes among coke-oven workers. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 649(1-2):221-229

Yili X, Tangchun W, Yongxing Z, Tanguay R, Nicole L, Ye Y, Guogao Z (1997) Preliminary studies on the relationship between autoantibodies to heat stress proteins and heat injury of pilots during acute heat stress. J Tongji Med Univ 17(2):83–85

Zhu B-K, Setchell BP (2004) Effects of paternal heat stress on the in vivo development of preimplantation embryos in the mouse. Reprod Nutr Dev 44(6):617–629

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The researchers express their gratitude to the School of Public Health Research Council of Tehran University of Medical Sciences, Tehran, Iran, for their advices and support.

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Habibi, P., Ostad, S.N., Heydari, A. et al. Effect of heat stress on DNA damage: a systematic literature review. Int J Biometeorol 66 , 2147–2158 (2022). https://doi.org/10.1007/s00484-022-02351-w

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Review article, poultry response to heat stress: its physiological, metabolic, and genetic implications on meat production and quality including strategies to improve broiler production in a warming world.

• 1 College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang, China
• 2 Aquatic Animals Precision Nutrition and High-Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, China

The continuous increase in poultry production over the last decades to meet the high growing demand and provide food security has attracted much concern due to the recent negative impacts of the most challenging environmental stressor, heat stress (HS), on birds. The poultry industry has responded by adopting different environmental strategies such as the use of environmentally controlled sheds and modern ventilation systems. However, such strategies are not long-term solutions and it cost so much for farmers to practice. The detrimental effects of HS include the reduction in growth, deterioration of meat quality as it reduces water-holding capacity, pH and increases drip loss in meat consequently changing the normal color, taste and texture of chicken meat. HS causes poor meat quality by impairing protein synthesis and augmenting undesirable fat in meat. Studies previously conducted show that HS negatively affects the skeletal muscle growth and development by changing its effects on myogenic regulatory factors, insulin growth factor-1, and heat-shock proteins. The focus of this article is in 3-fold: (1) to identify the mechanism of heat stress that causes meat production and quality loss in chicken; (2) to discuss the physiological, metabolic and genetic changes triggered by HS causing setback to the world poultry industry; (3) to identify the research gaps to be addressed in future studies.

Introduction

The increasing world population demands a more efficient food production system since the global food shortage issue keeps on rising. The poultry sector is noted to make a considerable contribution to global nutrition and food security, which helps in the provision of cheap protein, essential micronutrients, and energy to humans ( 1 ). Poultry, owing to their short production cycles and having the potential of converting wide ranges of agricultural food waste and by-products into eggs and meat edible for humans. Poultry meat production have been reported to increase from 120.5 MMT (million metric tons) in 2017 to 122.5 MMT in 2018 ( 2 ). FAO ( 3 ) also estimated its production to reach 137 MMT in 2020, with growth being anticipated in China, Britain, the EU, Mexico, and Brazil, suggesting the poultry industry's hidden potentials.

Recently, there has been a remarkable escalation in global environmental temperature, which poses serious implications to the farming sector in both tropical and subtropical regions of the world. A gradual increase in ambient temperature affects all living organisms ( 4 , 5 ). In living organisms, if the temperature exceeds the normal range (thermo-neutral zone), it disturbs the normal physiological functioning and induces cell injury. Usually, high ambient temperature leads to stress associated problems such as production losses, metabolic changes, growth depression, and poor efficiency ( 6 , 7 ). In temperate regions of world the high ambient temperature during the summer season often proves disastrous for poultry farming as thermal stress induced by extremely high temperatures is responsible for massive economic losses to poultry industry. According to a report, the U.S. livestock production industry suffers a severe loss of $1.69 to $2.36 billion because of high environmental temperature; out of which poultry industry accounts the loss of $128 to $165 million ( 8 ). Heat stress (HS) is widely classified into acute heat stress (AHS), which is the intense environmental temperature for a brief period and chronic heat stress (CHS) characterized by high temperature for a longer duration. Unluckily, both AHS and CHS challenge the genetic, nutritional, pharmaceutical, and management developments made by the animal farming industries that cause a considerable drop in production, proving to be one of the major hurdles to achieve efficient livestock farming in many regions of the world ( 9 , 10 ). Chronic heat stress has permanent damaging effect on the broiler chicken, if heat stress persists for longer period of time it increases fat content and damages the muscle portion of chicken unlike acute heat stress. Apart from duration of heat stress, the extent of production damage is also dependent on the intensity of heat stress ( 11 ). Harmful consequences of heat exhaustion (temperature exceeds beyond thermo-neutral zone and animal no more able to regulate body temperature) in animal farming would become more challenging as temperature keeps rising due to global warming. Climate change due to global warming is becoming more relevant these days, especially for the chicken meat industry ( 12 , 13 ). The broiler industry faces the challenge of HS, which increases production cost and severely damages the meat quality due to poultry's susceptibility to heat because of their rapid metabolic rate and high growth. Metabolic changes occur in chickens, specifically, broilers, reared in a HS environment, causing a considerable decrease in breast muscle size of the broiler chicken. HS is also responsible for the reduction in the protein content of muscles ( 14 ). Both AHS and CHS could cause a sharp decline in the metabolism of birds, which in turn will induce serious complications regarding the growth and performance of the broilers, such as a change in color, the decline in muscle pH, water-holding capacity (WHC), and juiciness of chicken meat ( 15 , 16 ). Many studies have revealed that high ambient temperature causes oxidative stress by producing reactive oxygen species (ROS). ROS has severe implications on skeletal muscle development, as they are responsible for lipid peroxidation in muscles ( 17 , 18 ). Thus, understanding the mechanisms underlying, the causes, and effects of HS and the strategies that can be put in place to curb or control such global menace, can be beneficial in solving the global food insecurity issues. This review dealt deep in analyzing the available information surrounding HS impact and the strategies to limit the unwanted implications of this threat. Figure 1 illustrates the physiological, metabolic and genetic changes amid HS and its relation to meat production and quality in chicken.

Figure 1 . Relationship of HS with physiological and biochemical changes in chicken and how it affects broiler chickens' meat quality.

Heat Stress in Broilers; How Does it Proceed?

Any foreign stimuli, which alters the normal biological and physiological mechanisms within living cells and threatens the living organism's survival, is referred as stress ( 18 , 19 ). In broiler production, environmental stress is often caused by numerous factors, including ambient temperature, which severely compromises birds' normal physiology, leading to poor production efficiency and food safety ( 20 ). In animals, stress often manifests in three stages. Firstly, the recognition of external stress by the body is known as a state of alarm. Secondly, stress induces the immune mechanism in living cells; thus, if stress persists, the body tries to adapt to that new environment. Despite all resistance, if the body still fails to cope with that stress, it leads to the exhaustion stage ( 21 ). Every living organism responds to HS accordingly, depending on the intensity and duration of stress. Numerous studies reported a substantial reduction in feeding and walking duration (discrete values) of birds kept under HS conditions as heat-stressed birds spend most of the time in acclimatizing activities such as panting, drinking more water, and resting to cope with the HS ( 22 ).

The neuroendocrine system plays a very significant role in HS response by inducing the autonomic nervous system (ANS) that often regulates fight and flight situations in living organisms ( 23 ). In response to HS, the ANS takes charge and triggers tachycardia (increased heartbeat), increases respiration rate and enhances the blood flow toward the body peripheries (skin) for maximum heat loss to maintain body temperature ( 23 , 24 ). It also promotes the breakdown of glycogen into glucose in muscles and reduces their capacity to store energy ( 6 , 13 ). Activation of the neuroendocrine system positively regulates the release of catecholamine. Catecholamine acts on beta androgenic receptors of skeletal muscles and initiates a series of reactions, disturbing the normal enzymatic activity in skeletal muscles as it inhibits the enzyme glycogen phosphorylase and activates the muscle glycogenolysis ( 25 ). HS also activates the hypothalamic-pituitary-adrenal axis (HPA) along with the sympathetic-adrenal-medullar axis (SAM), which promotes the release of glucocorticoids, vasodilation, lipolysis, and proteolysis in muscles ( 26 , 27 ). Glucocorticoids enhance glucose synthesis to confirm the survival of animals under such critical conditions as HS. The substantial release of glucocorticoids characterizes AHS as compared to CHS. Glucocorticoids encourage proteolysis by damaging myofibrils in skeletal muscles facilitated through major proteolytic mechanisms (ca +2 dependent, ubiquitin-proteasome system) ( 28 , 29 ).

Furthermore, glucocorticoids initiate the hydrolysis of circulating triglycerides, intensifying the activity of lipoprotein lipase that leads to an increase in lipolysis. Moreover, anabolic factors like insulin growth factor (IGF-1) are negatively regulated by glucocorticoids to worsen the skeletal muscle damage. HPA is considered a better indicator of HS than corticosterone as it could be secreted in many other conditions like fear of invading animals etc. ( 30 , 31 ). Corticosterone is secreted from both the HPA axis and the pituitary gland, corticosterone's secretion rate is relatively as slow compared to adrenaline but displays more compound and prominent effect during HS ( 32 , 33 ). Long-term secretion of corticosterone during chronic HS is linked to many deleterious consequences in broiler chicken, including compromised immunity, muscle breakdown, cardiac issues, and depression ( Figure 2 ). HS also induces infertility by disturbing reproductive hormones, severely affecting poultry gut health (leaky gut), as well as the altering of the immune functioning by triggering inflammatory cytokines ( 34 ).

Figure 2 . Mechanism of heat stress in broiler. HPA, Hypothalamic pituitary adrenal axis; ANS, Autonomic nervous system.

Thermoregulatory Apparatus in Chicken

All homoeothermic organisms have an optimal temperature range considered as the thermo-neutral zone unlike poikilotherms whose body temperature varies greatly depending on environmental temperature. In case the environmental temperature increases, the birds require more energy to maintain their body temperature ( 35 ). During HS conditions, metabolic heat increases, and animal succumbs to hyperthermia. Birds do not have sweat glands unlike mammals, but they have developed some behavioral adaptations to cope with heat, including elevated respiration rate, panting and raised wings ( 35 , 36 ). In commercial poultry, high production always remained a priority that made the broiler more vulnerable to environmental stressors. The insulation provided by feathers in commercial poultry is one of the major hindrances in birds' thermoregulation ( 35 , 37 ). To sum up, high ambient temperature beyond the thermo-neutral zone during the production phases badly affect meat production, meat quality and cause severe immune problems in the broiler flocks.

Impact of HS on Poultry Meat Production

Reduction in feed intake and poor weight gain.

Reduction in feed intake in HS animals is an adaptive mechanism to minimize metabolic heat production. A significant decrease in feed intake, body weight gain, and feed efficiency has been reported in many studies conducted on birds and other animals. During stress conditions, the priority of every living organism is to survive rather than growth. A recent study on broilers revealed that both cyclical and continuous heat stress significantly compromises growth performance by reducing protein digestibility up to 9.7%. Broilers under heat stress (32°C) have shown increased metabolizable energy intake (20.3%) and heat production (35.5%), and decreased energy retention (20.9%) and energy efficiency (32.4%) as compared to control group ( 38 ). Another study in laying hens reported a significant decrease in weight gain as average body weight (BW) of heat stressed hens was recorded 1.233 kg as compared to 1.528 kg BW of control group after 5 weeks of chronic heat stress (35°C). The significant decrease in weight is possibly due to reduced feed intake as birds under heat conditions ate less feed in relation to the control ones ( 39 ). This reduction in feed intake and nutrient digestibility severely compromises production efficiency and product quality. Chicken meat quality deteriorates since poor nutrients availability causes a sharp decline in muscle glycogen reserves, leading to dark, firm, and dry (DFD) meat ( 16 ).

Increase in Fat and Reduction in Protein Contents of Poultry Meat

High ambient temperature disrupts normal lipid metabolism (lipolysis) by downregulating the enzymes involved in lipid breakdown resulting in more fat deposition and reduced protein content in muscles ( 40 , 41 ). Many publications reported increased fat content in chicken under HS that seems to be an adaptive mechanism in birds as they store more energy in the form of fat to avoid further heat production during metabolism. A study conducted by Zhang et al. ( 14 ) reported that broiler birds raised under CHS (34–36°C) showed reduction in breast muscle mass (31.53%) and thigh muscle (11.17%) as compared to the normal control group. Considerable reduction in breast muscle mass was characterized by a significant change in chemical composition with higher fat quantity and lower protein concentration in muscles. Another study also concluded that cyclical HS (33°C for 9 h, 25°C for 15 h 1–42 days) in broiler reduced breast muscle weight by 16% ( 42 ). Lu et al. ( 43 ) reported higher intramuscular fat, increased activity of pyruvate kinase and lactate dehydrogenase in pectoral muscles of broilers under HS (32°C for 14 days). Moreover, CHS reduces the rate of aerobic metabolism by disturbing the mitochondrial functioning, decreasing aerobic metabolic activity and promoting glycolysis consequently leading to more fat deposition in muscles, which ultimately deteriorates meat quality ( 44 ). A study reported more fatness and low protein content in HS-broiler-chicken as compared to those maintained at the thermo-neutral condition ( 45 ). Production and quality losses in broiler chicken are not merely due to the reduced intake. Many other factors, including physiological, biochemical, and hormonal changes, are equally involved in all these losses to the poultry industry.

Excessive Heat Burden Triggers Metabolic Stress That Deteriorates Meat Quality

Excessive production of ros impairs meat quality.

Genetic modifications for rapid growth in broiler chicken has made the chicken more vulnerable to environmental stressors ( 17 , 46 ). Oxidative stress is among the major stressors, which can potentially halt chicken growth, having severe consequences on the broiler's meat quality. Increased ROS liberation is potentially damaging as it aggravates the aging of muscles, protein degradation and inactivates the nuclear proteins, including DNA and RNA. HS induces ROS production by impairing mitochondrial function leading to reduced aerobic metabolism of fat and glucose and enhanced glycolysis, which ultimately results in poor meat quality characterized by low pH and high drip loss ( 47 ). Living tissues have many antioxidants to cope with oxidants, if the balance among antioxidants and oxidants disturbs and oxidants exceed a certain limit within the body, this condition indicates oxidative stress. Mostly oxidants are produced during cellular metabolism in the mitochondria of living cells. Cellular metabolism is not the only source of oxidants, some external sources, including feed comprised of oxidized lipids and fats, are responsible for producing reactive oxygen species ( 48 ). According to Mujahid et al. ( 49 ), leakage of electrons from the mitochondrial respiratory chain during oxidative phosphorylation is the main source of ROS. HS increases ROS production by compromising the electron transport chain's functioning, which is necessary for energy production in the muscles ( 50 ).

ROS changes calcium sensitivity by oxidizing the thiol groups in the ryanodine receptor and damages an enzyme sarcoendoplasmic reticulum Ca +2 -ATPase (SERCA). This enzyme maintains calcium balance within the sarcoplasmic reticulum by removing extra calcium. Due to ROS, this system for calcium control collapses leading to overwhelming muscle contractions, culminating in muscle dystrophy ( 51 – 53 ). Numerous studies reported that oxidative stress leads to cell death and causes oxidation of protein and lipids, which ultimately deteriorates production efficiency and quality. Production of ROS in mitochondria leads to cellular oxidative stress, and it has severe consequences on physiological and behavioral characteristics in birds, which ultimately reduces the performance efficiency of the commercial meat birds. In short, oxidative stress lowers ATP production, creates calcium imbalance, and oxidizes several proteins within mitochondria along with mitochondrial membrane disruption ( 48 , 53 , 54 ).

Acidosis Lowers Water Holding Capacity (WHC) and Damages Meat Texture

Rapid pH reduction in chicken muscle is also associated with HS, and it has severe implications on meat quality or texture. Multiple studies indicated HS to potentially reduce muscle pH leading to harmful changes in muscles ( 55 ). HS triggers anaerobic glycolysis within the muscles during and after slaughtering of the animal, thus, more H + and lactic acid accumulate in the muscles due to hydrolysis of ATP during the anaerobic glycolysis. This result in a rapid drop in the pH of muscles leading to low water holding capacity which then develop into an abnormal condition called pale, soft, and exudative meat ( 56 , 57 ).

Thyroid Hormone Imbalance Under HS Impairs Skeletal Muscle Development

Thyroid hormone plays crucial role in the thermogenesis of avian via the thermoregulation by controlling metabolic heat production that is crucial to maintain normal body temperature. Tri-iodothyronine (T3) and tetra-iodothyronine (T4) enhance basal metabolism by modifying the mitochondrial function and assists skeletal muscles to acclimatize with a changing environment. Recent study regarding thyroid hormones in heat-stressed chicken found that high ambient temperature reduces both activity and size of thyroid. Lower level of thyroid hormone has observed in different studies conducted on heat stressed (38 °C for 24 h) quail ( 58 ) and domestic fowl ( 59 ). Thyroid hormones from external sources have also been observed to have lower survival time during HS ( 60 ). In broiler chicken, the thyroid gland's size, along with activity, decreases by high ambient temperatures and vice-versa ( 15 ). High ambient temperature normally responsible for drop in T3 and T4 plasma concentration. This mechanism is an adaptive tool to escape extra heat load, by decreasing metabolic heat production, plummeting maintenance energy requirements and increasing fat deposition by discouraging lipolysis ( 45 , 61 ).

How Does Meat Quality Deteriorate?

After slaughtering, when muscle converts to meat, it loses some of its contents, including water, myofibers, iron, and proteins. Loss of muscle contents during which meat tends to lose its original texture and taste are often referred as drip loss ( 62 ). When frozen meat is being thawed, it loses its texture and taste due to loss of water contents and leakage of other nutritional contents through the water. Drip loss is related to overall meat quality as it reduces meat palatability, juiciness, and acceptability of meat. It is one of the major meat quality defects, of which experts are trying to resolve, most particularly in pork and chicken ( 63 ). HS before slaughtering of bird increases metabolic rate and rigor mortis that results in protein denaturation. As protein is involved in the water-binding capacity of meat, so protein damage due to high carcass temperature hinders protein ability to bind water that culminates into pronounced reduction in poor water-holding ability characterized by higher drip loss and cooking loss ( 64 ). According to a recent study, constant high temperature harms water-holding capacity because it increases drip loss in poultry meat. The researchers found that broiler birds' meat under high temperatures had increased value of cook loss, shear force, and decreased pH. Birds under cyclic heat had higher cook loss value in breast muscles as compared to those raised under the thermo-neutral environment ( 14 ). Practical observations and studies have demonstrated both AHS and CHS during the housing period of broiler to be responsible for poor water-holding capacity.

Development of Pale, Soft, and Exudative Meat

In chicken, the development of PSE is mainly due to the rapid decrease in pH after birds' slaughtering. Birds with high metabolic activities and efficient growth rates often have poor thermoregulatory ability; consequently, these birds are more prone to HS during the growing period ( 65 ). HS, during the broiler's growth period especially, causes multiple problems, including muscle atrophy, acid-base imbalance, and poor meat quality. In chicken, mostly muscles are comprised of fast twitching fibers. Fast twitching fibers are mainly dependent on anaerobic glycolysis ( 66 ). HS before slaughtering accelerates the anaerobic glycolysis in muscles and lowers pH during the conversion of muscles into the meat while the body temperature is high ( 67 ). High carcass temperature with low pH causes protein degradation and develops PSE condition ( 68 ). The processing capability of PSE meat is poor making processed meat more dry and brittle due to lack of proper WHC and protein extractability ( 69 , 70 ). During hot weather, the broiler industry reports extensive losses in meat production due to reduced water holding capacity, poor meat texture, and pale color ( 57 ).

Production of Protein Carbonyls

AHS downregulates the protein synthesis at the transcriptional level, and it alters both ribosomal gene transcription and protein synthesis, consequently reducing protein deposition. The different durations of HS have different implications on the protein metabolism of hyperthermic animals ( 15 ). Short duration HS increases protein catabolism (marked by an increased plasma uric acid level), reduces protein synthesis and N retention, which decreases plasma concentrations of aspartic acid (Asp), serine (Ser), tyrosine (Tyr), and cysteine (Cys) ( 71 ). However, CHS knockdown protein synthesis in various muscles, decreases protein breakdown, with lower levels of plasma amino acids (especially sulfur and branched-chain amino acids) and higher serum levels of Asp, glutamic acid (Glu), and phenylalanine (Phe) ( 45 , 72 ).

The Genetic Basis of Muscle Development and Heat Stress

Skeletal muscles contribute up to 40–60% of total animal body weight and play a crucial role in the movement, respiration, and homeostasis of the animal body ( 73 ). Moreover, they play significant role in the food industry and have significant economic importance. Especially in meat-producing animals, scientists and researchers are busy finding multiple ways to enhance skeletal muscle mass ( 74 ). Each muscle cell in skeletal muscle is termed as myofibril having multiple nuclei. This myofibril arises from the fusion of mesoderm progenitor cells called myoblast. In almost every major species, the number of myofibrils set at the time of birth and cannot be increased after birth, but muscle size can be increased ( 75 ). In chickens, muscle growth after birth is only due to hypertrophy, characterized by proliferation and fusion of activated satellite cells with muscle fibers and increased protein synthesis ability. Myogenesis is an intricate process having multiple steps determined by numerous myogenic factors including transcription factors, adhesion, molecules, growth hormones, and myogenic regulatory factors ( 76 ). Figure 3 illustrates the stepwise process of muscle cell formation and highlights genetic factors, which regulate the myofiber formation at every step.

Figure 3 . Step wise progress of myofiber formation during skeletal muscle development.in chicken.

Myogenic Regulatory Factors (MRFs), namely; Myf5, MyoD, myogenin, and MRF4, are members of the basic helix-loop-helix family of transcription factors that control the determination and differentiation of skeletal muscle cells during embryogenesis and postnatal myogenesis ( 77 ). MRFs form a family of transcription factors whose function and activity represent a paradigm where a series of molecular switches determine an entire cell lineage's fate. The MRFs are a group of muscle-specific proteins that act at multiple points in the muscle lineage to cooperatively establish the skeletal muscle phenotype by regulating the muscle cell proliferation, irreversible cell cycle arrest of precursor cells, followed by a regulated activation of sarcomeric and muscle-specific genes to facilitate differentiation and sarcomere assembly ( 78 ). A study on the mouse model has shown that MyoD, Myf5, and MRF4 are responsible for a myogenic determination as in the absence of these factors, there will be no skeletal muscle formation. At the same time, myogenin works as a differentiation factor. As myogenesis initiates, Myf5 is the first regulatory gene to be activated near the neural tube while Mrf4 is also activated during the early stages, but later on, it expresses only during the differentiation of the skeletal muscles ( 79 , 80 ).

Constituents of the endocrine system, such as growth hormone (GH), IGF-1, and androgens, are the principal regulators of muscle metabolism. These endocrine components significantly impact muscle growth and act as anabolic factors, the major regulators of muscle's bulk ( 81 ). IGF-1 is considered to play key roles in fetal development and growth up to adolescence and in maintaining homeostasis in adult tissues by regulating cell proliferation, differentiation, and survival ( 82 ). IGF-1 exhibits a direct and crucial influence on muscle growth and differentiation during skeletal muscle development. Numerous studies have reported that IGF-1 is a positive regulator of myogenesis, which tightly controls the whole process of myogenic development. It is involved in various phases of myogenesis and muscle regeneration: triggering satellite cell proliferation, increasing protein synthesis, and promoting differentiation ( 82 , 83 ).

MRFs are key regulators in skeletal muscle development, and numerous studies reported that HS has negative implications on myogenic regulatory factors. Low expression levels of MyoD, myogenin had been observed in chicken embryos at high temperatures ( 84 ). HS, during the embryonic development phase, postpones the formation of myofibers, consequently affecting the muscle proliferation and differentiation at later stages. The number of muscle fibers is fixed at the time of birth and can never increase; the only size of those fibers increases, and major muscle growth in chicken is carried out by hypertrophy lead by protein deposition ( 85 , 86 ). A study on muscle development reported that HS impairs muscle hypertrophy by reducing the IGF-1 gene expression level and circulating IGF-1 concentration. HS also decreases the expression of MyoD, MyoG, and consequently hinders muscle hypertrophy by inhibiting S6K1. S6K1 plays a major role in cell growth regulation and muscle hypertrophy ( 84 , 87 ). A study demonstrated that knockdown of S6K1 in rats caused a significant reduction in muscle size. This molecule is responsible for cell growth by increasing muscle cell size without affecting the cell number ( 84 , 88 ).

To conclude, HS reduces growth performance, breast muscle mass, and yield in broilers. HS also reduced the mRNA expressions of IGF-1 and its downstream genes in breast muscle, thereby induced inactivity of mTOR and its downstream target S6K1 that regulates MRFs to decrease muscle hypertrophy. Meanwhile, the reduction of muscle protein synthesis is caused by reductions in both muscle amino acid uptake and the expressions of specific transporter isoforms due to the inactivity of mTOR and S6K1 ( 84 ).

Heat Shock Proteins During Heat Stress

Heat shock proteins are widely considered as stress proteins found within the cells of all living organisms. During the high ambient temperature, living cells trigger a response named “heat shock response,” which activates the specific set of proteins to protect cells from stressors like heat ( 89 ). The primary function of heat shock proteins is housekeeping, they maintain order in the cell by synthesizing other proteins while during stressful environment or any pathological condition, their expression level increases and they incline to attract immune cells at the respective site or organ ( 90 , 91 ). HSPs comprised six members classified and named on the basis of molecular weight, including HSP40, HSP70, HSP90, HSP100, small HSPs, and chaperonins. HSPs originate from an extracellular environment and function in specific parts of the body as stress signals and trigger immune cells during any stress and unfavorable conditions. HSPs also play an important role in protein formation and degradation by regulating folding/unfolding and translocation of proteins. All living organisms produce heat shock proteins under HS environment as these proteins are only produced under the stimuli of any stressor such as high temperature ( 91 – 94 ).

Role of HSPs as Stress Indicator and Cell Protector

HSP70 is very crucial for cell recovery after the damage done by HS ( 95 ). Increased expression levels of HSPs during HS is an adaptive phenomenon that improves tolerance level against HS in living cells as the studies on the transcriptional behavior of heat shock proteins have revealed that HSPs are the heat polypeptides produced due to high temperature. HSP70 and 90 are more extensively studied families among heat shock proteins, and these two families exhibit a plethora of functions from involving in cell tolerance to control cell cycle ( 96 – 99 ). Exposure to high ambient temperature enhances the production of heat shock proteins, which are synthesized in respective cells experiencing stress, and helps synthesize other proteins. It also regulates many processes, including protein refolding, translocation, and prevents the oxidative breakdown and apoptosis of damaged proteins during stress conditions. All these functions carried out by Heat shock proteins are very handy for cell recovery after stress ( 96 , 100 – 102 ). Studies revealed that HSPs play regulatory roles in various types of immunity. Production of HSPs during HS is mainly to attract immune cells. Numerous studies on differentially expressed genes during HS have shown that HSPs are related to birds' immune functioning during HS ( 103 ).

HSPs Protect the Muscle Cells From Damage

In an HS environment, HSPs repair the damaged proteins. In normal climatic conditions, HSP 70 is present in low concentrations as molecular chaperones, while the level of HSPs increases rapidly in muscles during cellular stress (hyperthermia, oxidative stress, changes in pH). An increase of HSPs leads to significant changes in gene expression leading to remodeling of skeletal muscles ( 104 ). Numerous studies in broiler chickens reported that the HSP family is playing a key role to repair the damaged cells, and it has observed during acute stress, HSP70 expressed in the muscles, liver, heart, kidney, and blood vessels ( 101 , 105 ). During AHS, an upregulated gene expression of HSP70 and 90 have been observed in muscle cells of broiler chicken. Moreover, AHS triggers both protein and mRNA expression of HSP70 and 90 in the kidney of chicken. A study conducted on Taiwanese roosters under acute HS has revealed the upregulation of HSP70 and 90 in Taiwanese roosters' testes. In contrast, another study reported depression in the expression level of HSP 90 and HSP25, which are believed to be involved in protein folding ( 101 , 106 , 107 ).

HSPs Regulates Meat Quality by Inhibiting Muscle Apoptosis

After the slaughtering of animals, muscles undergo cell apoptosis due to the unavailability of oxygen and nutrients within muscle cells. All those factors involved in the apoptotic activity of muscle cells are considered to control the animal's ultimate meat quality. Multiple studies reported the role of small heat shock proteins as an anti-apoptotic factor in muscle cells during post-mortem changes in muscles of slaughtered animals and influences the meat quality attributes including color, tenderness, juiciness, and the meat flavor ( 108 , 109 ). After the muscle undergoes cell death due to apoptosis, the number of small heat shock protein increases at that side and lowers the rate of apoptosis and unfolding of proteins in muscles ( 110 ). They delay protein degradation in muscle cells and try to maintain homeostasis at the cellular level. In this way, small heat shock proteins impede the aging process and play a crucial part in developing meat quality ( 110 , 111 ).

Dealing With HS to Improve Meat Production and Meat Quality

Dietary supplementation.

Multiple nutritional strategies have been suggested to alleviate HS destructive effects in the poultry industry. Previous studies revealed that protein metabolism is severely affected by chronic HS and leads to reduced protein deposition in muscles. This dwindling protein level cannot be compensated through dietary protein because it further aggravates HS by producing more metabolic heat ( 112 , 113 ). On the other hand, reducing protein concentration in diet culminates in to poor weight gain and lower feed efficiency. Chickens on a low protein diet often consume more feed to fulfill their protein requirements and the consumption of more feed results in poor feed efficiency. It has suggested that feed with more fat supplementation and low protein contents could minimize HS mischievous impact ( 114 , 115 ). A similar study ( 116 ) proposed that feed supplemented with 5% fat and 4% palm oil can improve broiler production performance under the HS environment by lowering feed retention and optimizing the nutrient utilization. Secondly, Feed restrictions during the early period of life in chicken have been proved handy in reducing HS's damaging effects. A study demonstrated that feed restriction during early days of broiler chicken (4–6 days after birth) promotes heat tolerance later in life (35–40 days of age) ( 7 , 116 ). Early feed reduction (EFR) and fat supplemented feed have a beneficial impact on heat-stressed broiler birds.

Thirdly, ample supplementation of vitamins is obligatory for better broiler production, especially amid harsh environment ( 10 , 116 , 117 ). Vitamin supplementation through drinking water is common practice in some poultry farms that have proved helpful to boost immunity and enhance heat-stressed broilers' performance. Diets containing vitamin A help broilers to fight against oxidative injuries induced by high environmental temperature ( 118 ). Kucuk et al. ( 118 ) also reported that vitamin A fortification has positive effects on production status as it enhances body weight gain, feed efficiency and reduces oxidative damage. Poultry birds can synthesize Vitamin C by itself and does not seek an external supply of vitamin C during normal conditions. However, under stress conditions, the additional supplementation of vitamin C might be fruitful for broilers' better performance as it promotes fatty acid oxidation instead of protein breakdown and reduces respiratory quotient ( 119 ). Studies reported increased hunger of birds for vitamin C during HS as vitamin C promotes fatty acid oxidation instead of protein breakdown and reduces respiratory quotient ( 119 , 120 ). Moreover, it enhances meat quality by producing meat with high protein and low-fat contents and maintains redox status during high temperature because of its ability to be one of the best antioxidants. A study based on vitamin E diet supplementation reported that vitamin E supplementation promotes the phagocytic activity of macrophages and increases serum antibodies (IgM and IgG) levels in broiler under HS ( 121 ).

Use of Herbs

There has been much attention placed on how herbal feed additives can be used in alleviating the adverse effects of HS, which in a way will help to enhance the production and performance of other animals, including poultry, pigs, and rabbits ( 122 ). The advantages of herbal additives include pharmacological and nutritional values and amelioration of many animal diseases. For example, there was noticeable recovery reported in animals which suffered harmful HS sequence after dietary supplementation of some herbs such as Ginger, Fennel, Black seed, hot red pepper, Artemisia annua , Rosemary, Moringa, Radix bupleurum , Chicory, and Dill ( 123 ).

Ginger ( Zingiber officinale ) as widely known to be used in the treatment of lots of disorders ( 119 ), contains compounds such as gingerdione, gingerdiol, and shagaols, which possess quite a lot of antioxidant and antimicrobial activities ( 119 , 124 ). The addition of ginger (2%) to heat-stressed broilers significantly improved the biochemical blood parameters and the growth performance in comparison to the control whereby the changes which emanated were attributed to antibacterial potential of the supplement, which in effect improved the digestibility, palatability, metabolism, and health status of the chicken ( 119 , 124 ). HS is noted to affect the poultry by reducing the villus height in quail ( 125 ) and broiler chicks ( 126 ). However, broilers supplemented with 2 and 4 g/kg garlic diets revealed the highest intestinal villi and most significant crypt depth in comparison to the control as reported by Shewita and Taha ( 127 ) although negative impacts on body weight, FCR, and FI at higher levels (6 g/kg) were reported. A report by Khonyoung et al. ( 128 ) showed that dietary supplemented with fermented-dried ginger products at 1% can help reduce abdominal fat, which in effect can help improve the health of heat-stressed broilers. For Fennel ( Foeniculum vulgare ), lots of research showcases the role that its essential oil plays as an antioxidant, antimicrobial, and a potent hepatoprotective agent ( 129 , 130 ). A study conducted by Ragab et al. ( 131 ) revealed an improvement of feed intake, meat breast (%), and leukocytes of heat-stressed Ross broilers after 1 or 2% of this herb. Correspondingly, fennel fruits supplementation at 10 or 20 g/kg diet in heat-stressed laying hens significantly improved the quality of eggs, reduced the malondialdehyde (MDA) contents, carboxyl levels in eggs, and again reduced the triglyceride and cholesterol contents ( 132 ). Again, Mohammed and Abbas ( 133 ) also observed that feeding of chicks with 1, 2, and 3 g fennel/kg diet significantly increased the RBCs, Hb, and PCV in comparison to the control.

Again, Nigella sativa , commonly known as the black seed, has been used in many HS research of poultry, and effect has shown encouraging results due to the higher nutritional values it carries. Active materials such as thymoquinone, nigellone, and thymohydroquinone, which aids in exerting antitoxic and antimicrobial properties through increased defense mechanisms against infectious diseases, are reported to be contained in black seed ( 134 ). Heat stressed pigeon which was fed with 2% black seed aided in weight gain and body weight improvement, hepatic lesion protection, which led to mild vascular congestion and vacuolization of the hepatocyte without creating damages to sinusoids in comparison to the control [EL ( 135 )]. Heat stressed broilers subjected to a 1% black seed diet increased the feed intake, dressing percentage, body gain while reducing the panting behavior, water to feed ratio, corticosterone, and T3 levels ( 136 ). Judging from these, ginger, fennel and black seed herb among others can be used to reduce the bad effects HS is noted to have on the poultry production.

Probiotic Effects on HS in Poultry

The supplementation of feed additives such as probiotics, prebiotics, and symbiotics has been used lately to curb the negative impacts HS poses in birds ( 9 ). Probiotics are “live microorganisms which, when administered in adequate amounts, confer a health benefit on the host ( 137 ).” Lots of research have been conducted proving that probiotics administration in diets is a sure way of improving the growth, immune response, digestive enzyme activity, disease resistance, gut microbiota in aquatic animals ( 138 – 141 ) chicken ( 142 ), pigs ( 143 ), etc. Given this, probiotics have gained lots of attentions from scientists in the poultry industry as the addition of this additive is a sure way of enhancing the intestinal morphology, physiological conditions, immunity; thus, the overall well-being and performance of heat-stressed poultry as previously reported ( 144 , 145 ). A study conducted by Zulkifli et al. ( 146 ) reported that a probiotic-enhanced water acidifier ( S . faecium and L . acidophilus + citric acid + sorbic acid + sodium citrate + sodium chloride + zinc sulfate + ferrous sulfate + potassium chloride + cellulase +magnesium sulfate) aided in the restoration of Na and K levels in broilers after 1 day HS. Broilers subjected to HS saw an increase in T 3 ( 147 ) and T 4 ( 148 ) in the serum after administering probiotics.

There has been a report that “Protexin ® Boost,” a probiotic treatment, improved serum uric acid levels of heat-stressed birds. Uric acid plays a critical role as an antioxidative agent ( 149 ); thus, an increase in its level after the probiotic treatment depicts that the probiotic exerts some mechanism in alleviating the oxidative damage after the HS in birds. Hasan et al. ( 150 ) observed an increase in hemoglobins in heat-stressed birds after dietary supplementation of probiotics (Protexin ® Boost). Furthermore, probiotics have also been revealed to improve the immune system of HS birds ( 151 ). It has been established that, the administration of probiotics enhances not only the responses of antibody ( 146 , 151 , 152 ) but also leukocytes count ( 153 ) in heat-stressed birds. Intraepithelial lymphocyte (IEL), an important host immune system component, is noted to respond rapidly when host organisms are infected ( 154 ). An experiment executed by Deng et al. ( 151 ) revealed a lower IEL number in the cecum and ileum of laying hens at week 61. Hasan et al. ( 155 ) revealed that the lymphoid organ's involution due to HS in poultry could be prevented by B . subtilis supplementation. Correspondingly, Lei et al. ( 156 ) observed a reduction in the corticosterone levels, which causes lymphoid organ involution after HS. Studies show that probiotics' dietary supplementation enhances the intestinal composition after HS conditions ( 144 ). Many studies on the health and well-being of heat-stressed poultry after supplementation have been established, as some have been discussed. Table 1 also enlists other research performed previously, which reveals the positive effects of probiotics in improving microbiota, morphology, and immune response of heat-stressed poultry.

Table 1 . Role of different probiotics to counter the damaging impact of heat stress in poultry.

Introducing Heat Tolerant Traits From Indigenous Breeds Into Commercial Breeds

Introduction of new technologies such as genomics provides valuable data and new approaches to address these challenges. The commercial broiler industry's focus largely remained only on fast weight gain and feed efficiency from previous two decades. Commercial breeds capable of gaining more weight in thermo-neutral conditions when raised under a high-temperature environment fail to maintain their growth performance ( 15 ). Genetic selection for heat tolerance in broilers needs to be taken into account, especially in tropical and subtropical regions of the world. A specific phenotype “frizzled feather,” characterized by curly feathers waving outside, was reported by Darwin ( 163 ). It was proposed that this type of chicken gives the best protection against the severe environment and the specific gene revealing such characteristics expresses in many chicken breeds ( 164 ). A study reported that 69-bp deletion in KRT6A was responsible for frizzle character in chicken. On the other hand, our research group conducted study on local Chinese frizzle breed found a 15-bp deletion in the KRT75L4 gene ( 165 ). This natural mutation in the chicken genome is reflected as an adaptive mechanism as these birds can tolerate heat better and are mostly found in warm regions. Data on the country-wise distribution of different animal breeds on the FAO website revealed both naked neck and frizzled feather chicken found worldwide. The naked neck gene has also been observed to withstand extreme climatic changes like high temperature ( 116 ).

Naked neck (Na), Frizzle (F, candidate gene: KRT6A and KRT75L4), and Dwarf (Dw, candidate gene: GHR) genes in poultry are considered candidate genes to tolerate thermal stress. Naked neck gene reduces the feather mass up to 40% and lowers the chances of heat insulation due to more feathers on the skin ( 166 , 167 ). Studies reported that Na chicken perform better under heat stress compared to birds with normal feathers. Better immunity and production performance have also been observed in the Na chicken line ( 168 ). Lack of feathers on the neck provides more space for heat dissipation and discourages heat insulation, helping birds tolerate the harsh temperature. Na gene has a considerable positive role in production performance and immunity development in birds. It also minimizes the fat deposition in the breast region, promoting heat dissipation, leading to heat tolerance ( 166 , 169 , 170 ). The dwarf (GHR) gene is also considered a heat-tolerant gene as it reduces body size from 30 to 40%. Na, F, and Dw genes could prove beneficial for the commercial poultry industry in tropical and subtropical parts of the world ( 171 ). Figure 4 shows different heat-tolerant breeds, including naked neck, frizzled feather, and dwarf chicken.

Figure 4. (A) Frizzled feather chicken (B) Naked neck chicken (C) Comparison among normal and frizzle feathers, frizzle feathers on the left side, normal feathers on right side (D) Dwarf size plymouth rock chicken with normal Plymouth rock chicken (E) Shank length of dwarf chicken as compared to normal chicken (These pictures have been taken in Guangdong Ocean University, Zhanjiang, China by our research group).

With time, HS issue is becoming more challenging for poultry industry. Genotype selection in broiler birds for higher growth rates to meet ever-increasing food requirement has made broiler chicken vulnerable to HS. Unluckily, the detrimental consequences of heat stress for poultry health and production are likely to continue and to be acquired by next generation during gestation if selection for only production traits is prioritized against heat tolerance and climate adaption according to current trends of global warming. High producers, commercial broiler breeds cannot withstand HS resulting in substantial economic losses to the industry, which triggers food security issues. Genetic selection for heat tolerance in poultry is the only durable solution to curb HS's negative implications. Realizing this threat to food security, scientists and industry's concerted efforts will be required to overcome this problem. These efforts should include (a) Genotype profiling of heat-tolerant breeds along with comprehensive studies on the interaction between genotype and phenotype in both heat tolerant and susceptible broiler breeds. (b) To explore the complete molecular mechanism of muscle development and muscle growth during HS environment. (c) Crossing frizzled feathers chicken breed to dwarf breed may give more apparent illustration about molecular and genetic mechanisms underlying heat resistance. Apart from breeding strategies, adopting modern managerial and environmental strategies could minimize the deleterious effects of heat on meat production and quality.

Author Contributions

AHN did the majority of the writing by communicating with KA and coordinated the document editing. LZ provided advice on the research input to the review article and performed significant edits to the document as well the funding acquisition. QYL, JHZ, and WLZ helped to gather and analyze information regarding the topic of review.

This work was supported by the Natural Science Foundation of China (31672412 and 31972550) and Guangdong Province (2020A1515011576).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

1. Mottet A, Tempio G. Global poultry production: current state and future outlook and challenges. Worlds Poult Sci J. (2017) 73:245–56. doi: 10.1017/S0043933917000071

CrossRef Full Text | Google Scholar

2. Bahri SIS, Ariffin AS, Mohtar S. Critical review on food security in Malaysia for broiler industry. Int J Acad Res Bus Soc Sci. (2019) 9:869–76. doi: 10.6007/IJARBSS/v9-i7/6186

3. FAO. Meat Market Review . Rome (2018).

4. Nardone A, Ronchi B, Lacetera N, Ranieri MS, Bernabucci U. Effects of climate changes on animal production and sustainability of livestock systems. Livest Sci. (2010) 130:57–69. doi: 10.1016/j.livsci.2010.02.011

5. Sejian V, Bhatta R, Gaughan JB, Dunshea FR, Lacetera N. Review: adaptation of animals to heat stress. Animal. (2018) 12:431–44. doi: 10.1017/S1751731118001945

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Afsal A, Sejian V, Bagath M, Devaraj C, Bhatta R. Heat stress and livestock adaptation: neuro-endocrine regulation. Int J Vet Anim Med. (2018) 2:1–7. doi: 10.31021/ijvam.20181108

7. Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ. Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal. (2012) 6:707–28. doi: 10.1017/S1751731111002448

8. St-Pierre NR, Cobanov B, Schnitkey G. Economic losses from heat stress by US livestock industries. J Dairy Sci. (2003) 86:52–77. doi: 10.3168/jds.S0022-0302(03)74040-5

9. Lara L, Rostagno M. Impact of heat stress on poultry production. Animals. (2013) 3:356–69. doi: 10.3390/ani3020356

10. Pawar SS, Basavaraj S, Dhansing LV, Pandurang KN, Sahebrao KA, Vitthal NA, et al. Assessing and mitigating the impact of heat stress in poultry. Adv Anim Vet Sci. (2016) 4:332–41. doi: 10.14737/journal.aavs/2016/4.6.332.341

11. Adu-Asiamah P, Zhang Y, Amoah K, Leng QY, Zheng JH, Yang H, et al. Evaluation of physiological and molecular responses to acute heat stress in two chicken breeds. Animal. (2021) 15:100106. doi: 10.1016/j.animal.2020.100106

12. Abd El-Hack ME, Abdelnour SA, Taha AE, Khafaga AF, Arif M, Ayasan T, et al. Herbs as thermoregulatory agents in poultry: an overview. Sci Total Environ. (2020) 703:134399. doi: 10.1016/j.scitotenv.2019.134399

13. Gregory NG. How climatic changes could affect meat quality. Food Res Int. (2010) 43:1866–73. doi: 10.1016/j.foodres.2009.05.018

14. Zhang ZY, Jia GQ, Zuo JJ, Zhang Y, Lei J, Ren L, et al. Effects of constant and cyclic heat stress on muscle metabolism and meat quality of broiler breast fillet and thigh meat. Poult Sci. (2012) 91:2931–7. doi: 10.3382/ps.2012-02255

15. Gonzalez-Rivas PA, Chauhan SS, Ha M, Fegan N, Dunshea FR, Warner RD. Effects of heat stress on animal physiology, metabolism, and meat quality: a review. Meat Sci. (2020) 162:108025. doi: 10.1016/j.meatsci.2019.108025

16. Song DJ, King AJ. Effects of heat stress on broiler meat quality. Worlds Poult Sci J. (2015) 71:701–9. doi: 10.1017/S0043933915002421

17. Altan Ö, Pabuçcuoglu A, Altan A, Konyalioglu S, Bayraktar H. Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. Br Poult Sci. (2003) 44:545–50. doi: 10.1080/00071660310001618334

18. Kumar B. Stress and its impact on farm animals. Front Biosci. (2012) 4:e496. doi: 10.2741/e496

19. Cirule D, Krama T, Vrublevska J, Rantala MJ, Krams I. A rapid effect of handling on counts of white blood cells in a wintering passerine bird: a more practical measure of stress? J. Ornithol. (2012) 153:161–6. doi: 10.1007/s10336-011-0719-9

20. Nawab A, Ibtisham F, Li G, Kieser B, Wu J, Liu W, et al. Heat stress in poultry production: mitigation strategies to overcome the future challenges facing the global poultry industry. J Therm Biol. (2018) 78:131–9. doi: 10.1016/j.jtherbio.2018.08.010

21. Virden WS, Kidd MT. Physiological stress in broilers: ramifications on nutrient digestibility and responses. J Appl Poult Res. (2009) 18:338–47. doi: 10.3382/japr.2007-00093

22. Mack LA, Felver-Gant JN, Dennis RL, Cheng HW. Genetic variations alter production and behavioral responses following heat stress in 2 strains of laying hens. Poult Sci. (2013) 92:285–94. doi: 10.3382/ps.2012-02589

23. Chen Y, Arsenault R, Napper S, Griebel P. Models and methods to investigate acute stress responses in cattle. Animals. (2015) 5:1268–95. doi: 10.3390/ani5040411

24. Minton JE. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim Sci. (1994) 72:1891–8. doi: 10.2527/1994.7271891x

25. Roach PJ. Control of glycogen synthase by hierarchal protein phosphorylation. FASEB J. (1990) 4:2961–8. doi: 10.1096/fasebj.4.12.2168324

26. Kuo T, Harris CA, Wang J-C. Metabolic functions of glucocorticoid receptor in skeletal muscle. Mol Cell Endocrinol. (2013) 380:79–88. doi: 10.1016/j.mce.2013.03.003

27. Shini S, Kaiser P, Shini A, Bryden WL. Biological response of chickens ( Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comp Biochem Physiol Part B Biochem Mol Biol. (2008) 149:324–33. doi: 10.1016/j.cbpb.2007.10.003

28. Bell RAV, Al-Khalaf M, Megeney LA. The beneficial role of proteolysis in skeletal muscle growth and stress adaptation. Skelet Muscle. (2016) 6:16. doi: 10.1186/s13395-016-0086-6

29. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. (2013) 280:4294–314. doi: 10.1111/febs.12253

30. Cockrem JF. Stress, corticosterone responses and avian personalities. J Ornithol. (2007) 148:169–78. doi: 10.1007/s10336-007-0175-8

31. Ognik K, Sembratowicz I. Stress as a factor modifying the metabolism in poultry. A review. Ann UMCS Zootech. (2012) 30:34–43. doi: 10.2478/v10083-012-0010-4

32. Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, et al. Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol Behav. (2007) 92:317–39. doi: 10.1016/j.physbeh.2006.12.003

33. Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dial Clin Neurosci. (2006) 8:383–95. doi: 10.31887/DCNS.2006.8.4/ssmith

34. Romero LM, Platts SH, Schoech SJ, Wada H, Crespi E, Martin LB, et al. (2012). Understanding stress in the healthy animal – potential paths for progress. Stress. (2015) 18:491–7. doi: 10.3109/10253890.2015.1073255

35. Spiers DE. Physiological basics of temperature regulation in domestic animals. In: R. J. Collier, J. L. Collier, editors. Environmental Physiology of Livestock. Oxford: Wiley-Blackwell (2012). p. 17–34. doi: 10.1002/9781119949091.ch2

36. Lin H, Zhang HF, Du R, Gu XH, Zhang ZY, Buyse J, et al. Thermoregulation responses of broiler chickens to humidity at different ambient temperatures. II Four weeks of age. Poult Sci . (2005) 84:1173–8. doi: 10.1093/ps/84.8.1173

37. Eppley ZA. Development of thermoregulation in birds: physiology, interspecific variation and adaptation to climate. In: Johnston IA, Bennett AF, editors. Animals and Temperature . Cambridge University Press (1996). p. 313–46. doi: 10.1017/CBO9780511721854.014

38. de Souza LFA, Espinha LP, de Almeida EA, Lunedo R, Furlan RL, Macari M. How heat stress (continuous or cyclical) interferes with nutrient digestibility, energy and nitrogen balances and performance in broilers. Livest Sci. (2016) 192:39–43. doi: 10.1016/j.livsci.2016.08.014

39. Mashaly MM, Hendricks GL, Kalama MA, Gehad AE, Abbas AO, Patterson PH. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci. (2004) 83:889–94. doi: 10.1093/ps/83.6.889

40. Cahaner A, Pinchasov Y, Nir I, Nitsan Z. Effects of dietary protein under high ambient temperature on body weight, breast meat yield, and abdominal fat deposition of broiler stocks differing in growth rate and fatness. Poult Sci. (1995) 74:968–75. doi: 10.3382/ps.0740968

41. Lu Z, He XF, Ma BB, Zhang L, Li JL, Jiang Y, et al. Increased fat synthesis and limited apolipoprotein B cause lipid accumulation in the liver of broiler chickens exposed to chronic heat stress. Poult Sci. (2019) 98:3695–704. doi: 10.3382/ps/pez056

42. Shakeri M, Cottrell J, Wilkinson S, Ringuet M, Furness J, Dunshea F. Betaine and antioxidants improve growth performance, breast muscle development and ameliorate thermoregulatory responses to cyclic heat exposure in broiler chickens. Animals. (2018) 8:162. doi: 10.3390/ani8100162

43. Lu Q, Wen J, Zhang H. Effect of chronic heat exposure on fat deposition and meat quality in two genetic types of chicken. Poult Sci . (2007) 86:1059–64. doi: 10.1093/ps/86.6.1059

44. Zaboli G, Huang X, Feng X, Ahn DU. How can heat stress affect chicken meat quality? – A review. Poult Sci. (2019) 98:1551–6. doi: 10.3382/ps/pey399

45. Geraert PA, Padilha JCF, Guillaumin S. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: biological and endocrinological variables. Br J Nutr. (1996) 75:205–16. doi: 10.1079/BJN19960125

46. Sihvo H-K, Immonen K, Puolanne E. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol. (2014) 51:619–23. doi: 10.1177/0300985813497488

47. Estévez M. Oxidative damage to poultry: from farm to fork. Poult Sci. (2015) 94:1368–78. doi: 10.3382/ps/pev094

48. Cadenas E, Davies KJA. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med. (2000) 29:222–30. doi: 10.1016/S0891-5849(00)00317-8

49. Mujahid A, Akiba Y, Warden CH, Toyomizu M. Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat-stressed chickens. FEBS Lett. (2007) 581:3461–7. doi: 10.1016/j.febslet,.2007.06.051

50. Huff Lonergan E, Zhang W, Lonergan SM. Biochemistry of postmortem muscle — lessons on mechanisms of meat tenderization. Meat Sci. (2010) 86:184–95. doi: 10.1016/j.meatsci.2010.05.004

51. Favero TG, Zable AC, Abramson JJ. Hydrogen peroxide stimulates the Ca2+ Release channel from skeletal muscle sarcoplasmic reticulum. J Biol Chem. (1995) 270:25557–63. doi: 10.1074/jbc.270.43.25557

52. Küchenmeister U, Kuhn G, Ender K. Preslaughter handling of pigs and the effect on heart rate, meat quality, including tenderness, and sarcoplasmic reticulum Ca2+ transport. Meat Sci. (2005) 71:690–5. doi: 10.1016/j.meatsci.2005.05.020

53. Zissimopoułos S, Lai FA. Redox regulation of the ryanodine receptor/calcium release channel. Biochem Soc Trans. (2006) 34:919–21. doi: 10.1042/BST0340919

54. Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperth. (2014) 30:513–23. doi: 10.3109/02656736.2014.971446

55. Wang Y, Du W, Lei K, Wang B, Wang Y, Zhou Y, et al. Effects of dietary bacillus licheniformis on gut physical barrier, immunity, and reproductive hormones of laying hens. Probiotics Antimicrob Proteins . (2017) 9:292–9. doi: 10.1007/s12602-017-9252-3

56. Strasburg GM, Chiang W. Pale, soft, exudative turkey—the role of ryanodine receptor variation in meat quality. Poult Sci. (2009) 88:1497–505. doi: 10.3382/ps.2009-00181

57. Van Laack RLJ, Liu C-H, Smith MO, Loveday HD. Characteristics of pale, soft, exudative broiler breast meat. Poult Sci. (2000) 79:1057–61. doi: 10.1093/ps/79.7.1057

58. Del Vesco AP, Gasparino E, Zancanela V, Grieser DO, Stanquevis CE, Pozza PC, et al. Effects of selenium supplementation on the oxidative state of acute heat stress-exposed quails. J Anim Physiol Anim Nutr. (2017) 101:170–9. doi: 10.1111/jpn.12437

59. Huston TM, Edwards HM, Williams JJ. The effects of high environmental temperature on thyroid secretion rate of domestic fowl. Poult Sci. (1962) 41:640–5. doi: 10.3382/ps.0410640

60. Bowen SJ, Washburn KW. Thyroid and adrenal response to heat stress in chickens and quail differing in heat tolerance. Poult Sci . (1985) 64:149–54. doi: 10.3382/ps.0640149

61. Collin A, Cassy S, Buyse J, Decuypere E, Damon M. Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones. Domest Anim Endocrinol. (2005) 29:78–87. doi: 10.1016/j.domaniend.2005.02.007

62. Ponsuksili S, Jonas E, Murani E, Phatsara C, Srikanchai T, Walz C, et al. Trait correlated expression combined with expression QTL analysis reveals biological pathways and candidate genes affecting water holding capacity of muscle. BMC Genomics. (2008) 9:367. doi: 10.1186/1471-2164-9-367

63. Forrest JC, Morgan MT, Borggaard C, Rasmussen AJ, Jespersen BL, Andersen JR. Development of technology for the early post mortem prediction of water holding capacity and drip loss in fresh pork. Meat Sci. (2000) 55:115–22. doi: 10.1016/S0309-1740(99)00133-3

64. Woelfel RL, Owens CM, Hirschler EM, Martinez-Dawson R, Sams AR. The characterization and incidence of pale, soft, and exudative broiler meat in a commercial processing plant. Poult Sci. (2002) 81:579–84. doi: 10.1093/ps/81.4.579

65. Petracci M, Mudalal S, Soglia F, Cavani C. Meat quality in fast-growing broiler chickens. Worlds Poult Sci J. (2015) 71:363–74. doi: 10.1017/S0043933915000367

66. Zhang X, Owens CM, Schilling MW. Meat: the edible flesh from mammals only or does it include poultry, fish, and seafood? Anim. Front. (2017) 7:12–8. doi: 10.2527/af.2017.0437

67. Yost J, Kenney P, Slider S, Russell R, Killefer J. Influence of selection for breast muscle mass on myosin isoform composition and metabolism of deep pectoralis muscles of male and female turkeys. Poult Sci. (2002) 81:911–7. doi: 10.1093/ps/81.6.911

68. Wilhelm AE, Maganhini MB, Hernández-Blazquez FJ, Ida EI, Shimokomaki M. Protease activity and the ultrastructure of broiler chicken PSE (pale, soft, exudative) meat. Food Chem. (2010) 119:1201–4. doi: 10.1016/j.foodchem.2009.08.034

69. Barbut S, Sosnicki AA, Lonergan SM, Knapp T, Ciobanu DC, Gatcliffe LJ, et al. Progress in reducing the pale, soft and exudative (PSE) problem in pork and poultry meat. Meat Sci. (2008) 79:46–63. doi: 10.1016/j.meatsci.2007.07.031

70. Owens CM, Alvarado CZ, Sams AR. Research developments in pale, soft, and exudative turkey meat in North America. Poult Sci. (2009) 88:1513–7. doi: 10.3382/ps.2009-00008

71. Emadi M, Kaveh K, Jahanshiri F, Hair-Bejo M, Ideris A, Alimon AR. Dietary tryptophan effects on growth performance and blood parameters in broiler chicks. J Anim Vet Adv. (2010) 9:700–4. doi: 10.3923/javaa.2010.700.704

72. Temim S, Chagneau A-M, Peresson R, Tesseraud S. Chronic heat exposure alters protein turnover of three different skeletal muscles in finishing broiler chickens fed 20 or 25% protein diets. J Nutr. (2000) 130:813–9. doi: 10.1093/jn/130.4.813

73. Yin H, Zhang S, Gilbert ER, Siegel PB, Zhu Q, Wong EA. Expression profiles of muscle genes in postnatal skeletal muscle in lines of chickens divergently selected for high and low body weight. Poult Sci. (2014) 93:147–54. doi: 10.3382/ps.2013-03612

74. Ge X, Zhang Y, Park S, Cong X, Gerrard DE, Jiang H. Stac3 inhibits myoblast differentiation into myotubes. PLoS ONE. (2014) 9:e95926. doi: 10.1371/journal.pone.0095926

75. Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche. Physiol Rev. (2013) 93:23–67. doi: 10.1152/physrev.00043.2011

76. Bryson-Richardson RJ, Currie PD. The genetics of vertebrate myogenesis. Nat Rev Genet. (2008) 9:632–46. doi: 10.1038/nrg2369

77. Hernández-Hernández JM, García-González EG, Brun CE, Rudnicki MA. The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol. (2017) 72:10–8. doi: 10.1016/j.semcdb.2017.11.010

78. Buckingham M, Rigby PWJ. Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell. (2014) 28:225–38. doi: 10.1016/j.devcel.2013.12.020

79. Fong AP, Tapscott SJ. Skeletal muscle programming and re-programming. Curr Opin Genet Dev. (2013) 23:568–73. doi: 10.1016/j.gde.2013.05.002

80. Moncaut N, Rigby PWJ, Carvajal JJ. Dial M(RF) for myogenesis. FEBS J. (2013) 280:3980–90. doi: 10.1111/febs.12379

81. Fink J, Schoenfeld BJ, Nakazato K. The role of hormones in muscle hypertrophy. Phys Sportsmed. (2018) 46:129–34. doi: 10.1080/00913847.2018.1406778

CrossRef Full Text

82. Winston BW, Ni A, Arora RC. Insulin-like growth factors. In: Laurent GJ, Shapiro SD, editors. Encyclopedia of Respiratory Medicine . Elsevier (2006). p. 339–46. doi: 10.1016/B0-12-370879-6/00453-1

83. Clemmons DR. Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab. (2009) 20:349–56. doi: 10.1016/j.tem.2009.04.002

84. Ma B, He X, Lu Z, Zhang L, Li J, Jiang Y, et al. Chronic heat stress affects muscle hypertrophy, muscle protein synthesis and uptake of amino acid in broilers via insulin like growth factor-mammalian target of rapamycin signal pathway. Poult Sci. (2018) 97:4150–8. doi: 10.3382/ps/pey291

85. Knapp JR. Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size. Development. (2006) 133:601–10. doi: 10.1242/dev.02249

86. Rehfeldt C, Te Pas MFW, Wimmers K, Brameld JM, Nissen PM, Berri C, et al. Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. I Regulation of myogenesis and environmental impact. Animal. (2011) 5:703–17. doi: 10.1017/S1751731110002089

87. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, et al. Atrophy of S6K1-/- skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol. (2005) 7:286–94. doi: 10.1038/ncb1231

88. Yin H, Li D, Wang Y, Zhao X, Liu Y, Yang Z, et al. Myogenic regulatory factor (MRF) expression is affected by exercise in postnatal chicken skeletal muscles. Gene. (2015) 561:292–9. doi: 10.1016/j.gene.2015.02.044

89. Frier BC, Locke M. Heat stress inhibits skeletal muscle hypertrophy. Cell Stress Chaperones. (2007) 12:132. doi: 10.1379/CSC-233R.1

90. Lindquist S. The heat-shock response. Annu Rev Biochem. (1986) 55:1151–91. doi: 10.1146/annurev.bi.55.070186.005443

91. Shankar K, Mehendale HM. Heat-shock proteins. In: Wexler P, editor. Encyclopedia of Toxicology . Bethesda, MD: Elsevier (2014). p. 830–1. doi: 10.1016/B978-0-12-386454-3.00320-1

92. Bernabòl P, Rebecchi L, Jousson O, Martínez-Guitarte JL, Lencioni V. Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy). Cell Stress Chaperones. (2011) 16:403–10. doi: 10.1007/s12192-010-0251-5

93. De Maio A, Vazquez D. Extracellular heat shock proteins. Shock. (2013) 40:239–46. doi: 10.1097/SHK.0b013e3182a185ab

94. Hartl FU. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. (2002) 295:1852–8. doi: 10.1126/science.1068408

95. Ming J, Xie J, Xu P, Liu W, Ge X, Liu B, et al. Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala Yih). Fish Shellfish Immunol. (2010) 28:407–18. doi: 10.1016/j.fsi.2009.11.018

96. Bakthisaran R, Tangirala R, Rao CM. Small heat shock proteins: role in cellular functions and pathology. Biochim Biophys Acta Proteins Proteomics. (2015) 1854:291–319. doi: 10.1016/j.bbapap.2014.12.019

97. Pockley AG. Heat shock proteins as regulators of the immune response. Lancet. (2003) 362:469–76. doi: 10.1016/S0140-6736(03)14075-5

98. Vamvakopoulos NO. Tissue-specific expression of heat shock proteins 70 and 90: potential implication for differential sensitivity of tissues to glucocorticoids. Mol Cell Endocrinol. (1993) 98:49–54. doi: 10.1016/0303-7207(93)90235-C

99. Wegele H, Müller L, Buchner J. Hsp70 and Hsp90—a relay team for protein folding. In: Mager T, editor. Reviews of Physiology, Biochemistry and Pharmacology. Berlin; Heidelberg: Springer Berlin Heidelberg (2004). p. 1–44. doi: 10.1007/s10254-003-0021-1

100. Jiang S, Mohammed AA, Jacobs JA, Cramer TA, Cheng HW. Effect of synbiotics on thyroid hormones, intestinal histomorphology, and heat shock protein 70 expression in broiler chickens reared under cyclic heat stress. Poult Sci. (2020) 99:142–50. doi: 10.3382/ps/pez571

101. Pei-Ming S, Yu-Tian L, Qing-Hua W, Zhi-Liang W, En-Dong B. HSP70 and HSP70 mRNA localization in heat-stressed tissues of broilers. Chinese J Agric Biotechnol. (2007) 4:181–6. doi: 10.1017/S1479236207001726

102. Yu J, Bao E. Effect of acute heat stress on heat shock protein 70 and its corresponding mRNA expression in the heart, liver, and kidney of broilers. Asian Australas J Anim Sci. (2008) 21:1116–26. doi: 10.5713/ajas.2008.70703

103. Shevtsov M, Multhoff G. Heat shock protein–peptide and hsp-based immunotherapies for the treatment of cancer. Front Immunol. (2016) 7:171. doi: 10.3389/fimmu.2016.00171

104. Abdelnour SA, Abd El-Hack ME, Khafaga AF, Arif M, Taha AE, Noreldin AE. Stress biomarkers and proteomics alteration to thermal stress in ruminants: a review. J Therm Biol. (2019) 79:120–34. doi: 10.1016/j.jtherbio.2018.12.013

105. Zhang WW, Kong LN, Zhang XQ, Luo QB. Alteration of HSF3 and HSP70 mRNA expression in the tissues of two chicken breeds during acute heat stress. Genet Mol Res. (2014) 13:9787–94. doi: 10.4238/2014.November.27.6

106. Lei L, Yu J, Bao E. Expression of heat shock protein 90 (Hsp90) and transcription of its corresponding mRNA in broilers exposed to high temperature. Br Poult Sci. (2009) 50:504–11. doi: 10.1080/00071660903110851

107. Wang SH, Cheng CY, Tang PC, Chen CF, Chen HH, Lee YP, et al. Differential gene expressions in testes of L2 strain Taiwan country chicken in response to acute heat stress. Theriogenology. (2013) 79:374–82.e7. doi: 10.1016/j.theriogenology.2012.10.010

108. Balan P, Kim YHB, Blijenburg R. Small heat shock protein degradation could be an indicator of the extent of myofibrillar protein degradation. Meat Sci. (2014) 97:220–2. doi: 10.1016/j.meatsci.2014.01.019

109. Lomiwes D, Farouk MM, Wiklund E, Young OA. Small heat shock proteins and their role in meat tenderness: a review. Meat Sci. (2014) 96:26–40. doi: 10.1016/j.meatsci.2013.06.008

110. Herrera-Mendez CH, Becila S, Boudjellal A, Ouali A. Meat ageing: reconsideration of the current concept. Trends Food Sci Technol. (2006) 17:394–405. doi: 10.1016/j.tifs.2006.01.011

111. Ouali A, Herrera-Mendez CH, Coulis G, Becila S, Boudjellal A, Aubry L, et al. Revisiting the conversion of muscle into meat and the underlying mechanisms. Meat Sci. (2006) 74:44–58. doi: 10.1016/j.meatsci.2006.05.010

112. Attia YA, Al-Harthi MA, Sh., Elnaggar A. Productive, physiological and immunological responses of two broiler strains fed different dietary regimens and exposed to heat stress. Ital J Anim Sci. (2018) 17:686–97. doi: 10.1080/1828051X.2017.1416961

113. Daghir N. Nutritional strategies to reduce heat stress in broilers and broiler breeders. Lohmann Inf. (2009) 44:6–15. Available online at: https://thepoultrypunch.com/2019/05/nutritional-strategies-to-alleviate-the-effect-of-heat-stress-in-broilers/

Google Scholar

114. Ghazalah AA, Abd-Elsa MO, Ali AM. Influence of dietary energy and poultry fat on the response of broiler chicks to heat therm. Int J Poult Sci. (2008) 7:355–9. doi: 10.3923/ijps.2008.355.359

115. Naga Raja Kumari K, Narendra Nath D. Ameliorative measures to counter heat stress in poultry. Worlds Poult Sci J. (2018) 74:117–30. doi: 10.1017/S0043933917001003

116. Fisinin VI, Kavtarashvili AS. Heat stress in poultry. II methods and techniques for prevention and alleviation (review). Sel'skokhozyaistvennaya Biol. (2015) 50:431–43. doi: 10.15389/agrobiology.2015.4.431eng

117. Sahin K, Smith MO, Onderci M, Sahin N, Gursu MF, Kucuk O. Supplementation of zinc from organic or inorganic source improves performance and antioxidant status of heat-distressed quail. Poult Sci. (2005) 84:882–7. doi: 10.1093/ps/84.6.882

118. Kucuk O, Sahin N, Sahin K. Supplemental zinc and vitamin a can alleviate negative effects of heat stress in broiler chickens. Biol Trace Elem Res. (2003) 94:225–36. doi: 10.1385/BTER:94:3:225

119. Khan RU, Naz S, Nikousefat Z, Selvaggi M, Laudadio V, Tufarelli V. Effect of ascorbic acid in heat-stressed poultry. Worlds Poult Sci J. (2012) 68:477–90. doi: 10.1017/S004393391200058X

120. Mahmoud UT, Mootaz AM, Abdel-Rahman MHAD. Effects of propolis, ascorbic acid and vitamin E on thyroid and corticosterone. J Adv Vet Res. (2014) 4:18–27. Available online at: https://www.cabdirect.org/cabdirect/abstract/20143121467

121. Habibian M, Ghazi S, Moeini MM. Effects of dietary selenium and vitamin e on growth performance, meat yield, and selenium content and lipid oxidation of breast meat of broilers reared under heat stress. Biol Trace Elem Res. (2016) 169:142–52. doi: 10.1007/s12011-015-0404-6

122. Liu P, Wang X, Hu C, Hu T. Inhibition of proliferation and induction of apoptosis by trimethoxyl stilbene (TMS) in a lung cancer cell line. Asian Pac J Cancer Prev. (2011) 12:2263–9. Available online at: https://europepmc.org/article/MED/22296367

PubMed Abstract | Google Scholar

123. Abd El-Hack ME, Alagawany M, Noreldin AE. Managerial and nutritional trends to mitigate heat stress risks in poultry farms. Handb Environ Chem . (2019) 77:325–38. doi: 10.1007/698_2018_290

124. Rehman Z, Chand N, Khan RU, Naz S, Alhidary IA. Serum biochemical profile of two broiler strains supplemented with vitamin E, raw ginger ( Zingiber officinale ) and L-carnitine under high ambient temperatures. S Afr J Anim Sci. (2019) 48:935. doi: 10.4314/sajas.v48i5.13

125. Sandikci M, Eren U, Onol AG, Kum S. The effect of heat stress and the use of Saccharomyces cerevisiae or (and) bacitracin zinc against heat stress on the intestinal mucosa in quails. Rev Med Vet. (2004) 155:552–6. doi: 10.5281/zenodo.1072271

126. Mitchell MA, Carlisle AJ. The effects of chronic exposure to elevated environmental temperature on intestinal morphology and nutrient absorption in the domestic fowl ( Gallus domesticus ). Comp Biochem Physiol Part A Physiol. (1992) 101:137–42. doi: 10.1016/0300-9629(92)90641-3

127. Shewita RS, Taha AE. Effect of dietary supplementation of different levels of black seed ( Nigella sativa L) on growth performance, immunological, hematological and carcass parameters of broiler chicks. World Acad Sci Eng Technol. (2011) 5:31325. Available online at: https://www.revmedvet.com/artdes-us.php?id=1273

128. Khonyoung D, Yamauchi K, Buwjoom T, Maneewan B, Thongwittaya N. Effects of dietary dried fermented ginger on growth performance, carcass quality, and intestinal histology of heat-stressed broilers. Can J Anim Sci. (2012) 92:307–17. doi: 10.4141/cjas2011-129

129. Özbek H, Ugraş S, Dülger H, Bayram I, Tuncer I, Öztürk G, et al. Hepatoprotective effect of Foeniculum vulgare essential oil. Fitoterapia. (2003) 74:317–19. doi: 10.1016/S0367-326X(03)00028-5

130. Ruberto G, Baratta MT, Deans SG, Dorman HJD. Antioxidant and antimicrobial activity of foeniculum vulgare and Crithmum maritimum essential oils. Planta Med. (2000) 66:687–93. doi: 10.1055/s-2000-9773

131. Ragab MS, Namra MMM, Aly MMM, Fathi MA. Impact of inclusion fennel seeds and thyme dried leaves in broiler diets on some productive and physiological performance during summer season. Egypt Poult Sci. (2016) 33:197–219. Available online at: https://www.researchgate.net/publication/338623480_IMPACT_OF_INCLUSION_FENNEL_SEEDS_AND_THYME_DRIED_LEAVES_IN_BROILER_DIETS_ON_SOME_PRODUCTIVE_AND_PHYSIOLOGICAL_PERFORMANCE_DURING_SUMMER_SEASON

132. Gharaghani H, Shariatmadari F, Torshizi M. Effect of fennel ( Foeniculum vulgare Mill.) used as a feed additive on the egg quality of laying hens under heat stress. Rev Bras Ciência Av í cola . (2015) 17:199–207. doi: 10.1590/1516-635x1702199-208

133. Mohammed AA, Abbas RJ. The effect of using fennel seeds ( Foeniculum vulgare L.) on productive performance of broiler chickens. Int J Poult Sci. (2009) 8:642–4. doi: 10.3923/ijps.2009.642.644

134. Forouzanfar F, Fazly Bazzaz BS, Hosseinzadeh H. Black cumin (Nigella sativa) and its constituent (thymoquinone): a review on antimicrobial effects. Iran J Basic Med Sci. (2014) 17:929–38.

135. Shoukary RDEL, Sayed RK, Hassan RI. Behavioral, hepato-morphological, and biochemical studies on the possible protective effect of black seed and water bath against change-mediated heat stress on pigeon. J Basic Appl Zool. (2018) 79:23. doi: 10.1186/s41936-018-0035-5

136. El-Shoukary RDM, Darwish MHA, Abdel-Rahman MAM. Behavioral, Performance, carcass traits and hormonal changes of heat stressed broilers feeding black and coriander seeds. Adv Vet Res. (2014) 4:97–101. Available online at: https://advetresearch.com/index.php/AVR/article/view/79

137. FAO/WHO. WHO Working Group Guidelines for the Evaluation of Probiotics 734 in Food . London (2002).

138. Abarike ED, Jian J, Tang J, Cai J, Yu H, Lihua C, et al. Influence of traditional Chinese medicine and Bacillus species (TCMBS) on growth, immune response and disease resistance in Nile tilapia, Oreochromis niloticus . Aquac Res. (2018) 49:2366–75. doi: 10.1111/are.13691

139. Amoah K, Dong X, Tan B, Zhang S, Chi S, Yang Q, et al. Administration of probiotic Bacillus licheniformis induces growth, immune and antioxidant enzyme activities, gut microbiota assembly and resistance to Vibrio parahaemolyticus in Litopenaeus vannamei . Aquac Nutr . (2020) 26:1604–22. doi: 10.1111/anu.13106

140. Amoah K, Huang Q, Dong X, Tan B, Zhang S, Chi S, et al. Paenibacillus polymyxa improves the growth, immune and antioxidant activity, intestinal health, and disease resistance in Litopenaeus vannamei challenged with Vibrio parahaemolyticus. Aquaculture. (2020) 518:734563. doi: 10.1016/j.aquaculture.2019.734563

141. Amoah K, Dong X, Tan B, Zhang S, Kuebutornye FKA, Chi S, et al. In vitro assessment of the safety and potential probiotic characteristics of three Bacillus strains isolated from the intestine of hybrid grouper ( Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂). Front Vet Sci. (2021) 8:675962. doi: 10.3389/fvets.2021.675962

142. Xu S, Lin Y, Zeng D, Zhou M, Zeng Y, Wang H, et al. Bacillus licheniformis normalize the ileum microbiota of chickens infected with necrotic enteritis. Sci Rep. (2018) 8:1744. doi: 10.1038/s41598-018-20059-z

PubMed Abstract | CrossRef Full Text

143. Li X-Q, Zhu Y-H, Zhang H-F, Yue Y, Cai Z-X, Lu Q-P, et al. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS ONE. (2012) 7:e40666. doi: 10.1371/journal.pone.0040666

144. Al-Fataftah A-R, Abdelqader A. Effects of dietary Bacillus subtilis on heat-stressed broilers performance, intestinal morphology and microflora composition. Anim Feed Sci Technol. (2014) 198:279–85. doi: 10.1016/j.anifeedsci.2014.10.012

145. Faseleh Jahromi M, Wesam Altaher Y, Shokryazdan P, Ebrahimi R, Ebrahimi M, Idrus Z, et al. Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. Int J Biometeorol. (2016) 60:1099–110. doi: 10.1007/s00484-015-1103-x,

146. Zulkifli I, Juriah K, Htin NN, Norazlina I. Response of heat-distressed broiler chickens to virginiamycin and probiotic-enhanced water acidifier (Acid-Pak 4-Way TM ) supplementation, and early age feed restriction. Arch fur Geflugelkd. (2006) 70:119–26. Available online at: https://www.european-poultry-science.com/Response-of-heat-distressed-broiler-chickens-to-virginiamycin-and-probiotic-enhanced-water-acidifier-Acid-Pak-4-WaysupTMsup-supplementation-and-early-age-feed-restriction,QUlEPTQyMTY5MjcmTUlEPTE2MTAxNA.htm

147. Tollba AAH, Sabry MM, Medani GG. Effect of microbial probiotics on the performance of broiler chicks under normal or heat stress conditions. 2 - Bacteria concentration or yeast culture Egypt. Poult Sci J. (2004) 24:351–67. Available online at: https://www.mendeley.com/catalogue/d49176f5-db18-3496-b59d-6962b1d43672/?utm_source=desktop&utm_medium=1.19.8&utm_campaign=open_catalog&userDocumentId=%7B9a293449-c6bd-4921-9274-20c701a5a90b%7D

148. Sohail MU, Ijaz A, Yousaf MS, Ashraf K, Zaneb H, Aleem M, et al. Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poult Sci. (2010) 89:1934–8. doi: 10.3382/ps.2010-00751

149. de Oliveira EP, Burini RC. High plasma uric acid concentration: causes and consequences. Diabetol Metab Syndr. (2012) 4:12. doi: 10.1186/1758-5996-4-12

150. Hasan S, Hossain MM, Alam J, Bhuiyan MER. Benificial effects of probiotic on growth performance and hemato-biochemical parameters in broilers during heat stress. Int J Innov Appl Stud ISSN. (2015) 10:244–9. Available online at: https://www.semanticscholar.org/paper/Influences-of-prebiotic-on-growth-performance-and-Hasan-Hossain/3e1a9b73e675c80752f3ec81b50b7bada9214ac2?p2df

151. Deng W, Dong XF, Tong JM, Zhang Q. The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult Sci. (2012) 91:575–82. doi: 10.3382/ps.2010-01293

152. Haldar S, Ghosh TK, Toshiwati, Bedford MR. Effects of yeast ( Saccharomyces cerevisiae ) and yeast protein concentrate on production performance of broiler chickens exposed to heat stress and challenged with Salmonella enteritidis . Anim Feed Sci Technol . (2011) 168:61–71. doi: 10.1016/j.anifeedsci.2011.03.007

153. Rahimi S, Khaksefidi A. A comparison between the effects of a probiotic (Bioplus 2B) and an antibiotic (virginiamycin) on the performance of broiler chickens under heat stress condition. Iran J Vet Res. (2006) 7:23–8. Available online at: https://www.cabdirect.org/cabdirect/abstract/20063194510

154. Sheridan BS, Lefrançois L. Intraepithelial lymphocytes: to serve and protect. Curr Gastroenterol Rep. (2010) 12:513–21. doi: 10.1007/s11894-010-0148-6

155. Hasan S, Hossain M, Miah A, Bhuiyan M. Influences of prebiotic on growth performance and hemato-biochemical parameters in broiler during heat stress. Bangladesh J Vet Med. (2014) 12:121–5. doi: 10.3329/bjvm.v12i2.21273

156. Lei K, Li YL, Yu DY, Rajput IR, Li WF. Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poult Sci. (2013) 92:2389–95. doi: 10.3382/ps.2012-02686

157. Asli MM, Shariatmadari F, Hosseini SA, Lotfollahian H. Effect of Probiotics, Yeast, Vitamin E and Vitamin C supplements on performance and immune response of laying hen during high environmental temperature. Int J Poult Sci. (2007) 6:895–900. doi: 10.3923/ijps.2007.895.900

158. Huang Z, Mu C, Chen Y, Zhu Z, Chen C, Lan L, et al. Effects of dietary probiotic supplementation on LXRα and CYP7α1 gene expression, liver enzyme activities and fat metabolism in ducks. Br Poult Sci. (2015) 56:218–24. doi: 10.1080/00071668.2014.1000821

159. Landy N, Kavyani A. Effects of using a multi-strain probiotic on performance, immune responses and cecal microflora composition in broiler chickens reared under cyclic heat stress condition. IJAS . (2013) 3:703–8. Available online at: https://www.semanticscholar.org/paper/Effects-of-Using-a-Multi-Strain-Probiotic-on-Immune-Landy-Kavyani/e674fb972adac50cf74304868f13734841d1cbb2

160. Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, et al. Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. J Anim Physiol Anim Nutr. (2013) 97:68–73. doi: 10.1111/jpn.12041

161. Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, et al. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult Sci. (2014) 93:581–8. doi: 10.3382/ps.2013-03455

162. Sohail MU, Hume ME, Byrd JA, Nisbet DJ, Ijaz A, Sohail A, et al. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult Sci. (2012) 91:2235–40. doi: 10.3382/ps.2012-02182

163. Darwin CR. The Variation of Animals and Plants Under Domestication , Vol. 1, 1st ed. London, John Murray (1868). Available online at: http://darwin-online.org.uk/content/frameset?itemID=F877.1andviewtype=textandpageseq=1

PubMed Abstract

164. Duah KK, Essuman EK, Boadu VG, Olympio OS, Akwetey W. Comparative study of indigenous chickens on the basis of their health and performance. Poult Sci. (2020) 99:2286–92. doi: 10.1016/j.psj.2019.11.049

165. Dong J, He C, Wang Z, Li Y, Li S, Tao L, et al. A novel deletion in KRT75L4 mediates the frizzle trait in a Chinese indigenous chicken. Genet Sel Evol. (2018) 50:68. doi: 10.1186/s12711-018-0441-7

166. Patra BN, Bais RKS, Prasad RB, Singh BP. Performance of naked neck versus normally feathered coloured broilers for growth, carcass traits and blood biochemical parameters in tropical climate. Asian-Australasian J Anim Sci. (2002) 15:1776–83. doi: 10.5713/ajas.2002.1776

167. Yunis R, Cahaner A. The effects of the naked neck (Na) and frizzle (F) genes on growth and meat yield of broilers and their interactions with ambient temperatures and potential growth rate. Poult Sci. (1999) 78:1347–52. doi: 10.1093/ps/78.10.1347

168. Lin H, Jiao HC, Buyse J, Decuypere E. Strategies for preventing heat stress in poultry. Worlds Poult Sci J. (2006) 62:71–86. doi: 10.1079/WPS200585

169. Cahaner A, Deeb N, And Gutman M. Effects of the plumage-reducing naked neck (na) gene on the performance of fast-growing broilers at normal and high ambient temperatures. Poult Sci. (1993) 72:767–75. doi: 10.3382/ps.0720767

170. Raju MVLN, Shyam Sunder G, Chawak MM, Rama Rao SV, Sadagopan VR. Response of naked neck (Nana) and normal (nana) broiler chickens to dietary energy levels in a subtropical climate. Br Poult Sci. (2004) 45:186–93. doi: 10.1080/00071660410001715786

171. Ouyang J, Xie L, Nie Q, Zeng H, Peng Z, Zhang D, et al. The effects of different sex-linked dwarf variations on Chinese native chickens. J Integr Agric. (2012) 11:1500–8. doi: 10.1016/S2095-3119(12)60150-6

Keywords: heat stress, poultry, meat production, meat quality, muscle development

Citation: Nawaz AH, Amoah K, Leng QY, Zheng JH, Zhang WL and Zhang L (2021) Poultry Response to Heat Stress: Its Physiological, Metabolic, and Genetic Implications on Meat Production and Quality Including Strategies to Improve Broiler Production in a Warming World. Front. Vet. Sci. 8:699081. doi: 10.3389/fvets.2021.699081

Received: 22 April 2021; Accepted: 24 June 2021; Published: 23 July 2021.

Reviewed by:

Copyright © 2021 Nawaz, Amoah, Leng, Zheng, Zhang and Zhang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Li Zhang, zhangli761101@163.com

This article is part of the Research Topic

Strategies for Mitigating the Environmental Impacts of Pig and Poultry Production

Heat Stress in Flight Cockpits in the Desert Climate Research Paper

Introduction, materials and methods, conclusion and recommendations, reference list.

Heat stress is a common condition in hot climates. Aviators are the most affected based on the nature of the work they do. Desert climates such as the Arabian Peninsula pose a challenge to aviators. This research paper seeks to investigate the occurrence of heat stress in flight cockpits in desert climates. Besides, it makes a comparison between sources of heat on the performance of the pilot. The methodology used is an article review. The articles used were compiled from PubMed. The results show that heat stress has physiological and psychological effects on aviators and that the cockpit had different sources of heat depending on the ‘make’ of the aircraft and the climate. Clothing and height of flight are also important factors in the etiology of heat stress. The paper concludes that although the effects of heat stress on modern aircraft are subtle, they may greatly affect the performance of aviators in the cockpit. Therefore, recommendations are provided on how to prevent heat stress, including the development of better cooling systems and indices.

The Middle East and Arabian Peninsula Climate

The Arabian Peninsula has a relatively hotter climate compared to the rest of the world. It is one of the hottest places on earth (Perry, 1967). Working in this environment requires one to make adequate adaptations. Despite the hot climate, the area also has millions of inhabitants in different occupations, with the aviation industry being vibrant. Temperatures in the Middle East are often above 30 o Celsius. There is rarely any rain since the region has only one rainy season. The Arabian Peninsula is also categorized as a desert since there are inadequate natural water resources. The area is largely arid and semi-arid. There is often a lack of water and high temperatures (Perry, 1967).

The Middle East has mild winters once a year. However, the rest of the year is characterized by hot and dry weather (Perry, 1967). The region where the climate is different is in the mountains that form part of northern Iraq and Iran, and part of Eastern Turkey (Perry, 1967). The winters are long in this region, with temperatures dropping to below the freezing point in some areas. The monsoon that is frequently experienced in the area results from the hot and dry climate. The winds blow towards the land in one part of the year, with the reverse taking place when the temperatures on the land drop (Perry, 1967).

Temperatures above 100 F are common. However, the average recorded temperatures are 85 F for the whole region (Perry, 1967). Basra has some of the hottest temperatures in the Middle East. These temperatures are recorded to reach above 124 F (Perry, 1967). Another common phenomenon in the region resulting from the high temperatures is the sandstorms that the area experiences frequently. This phenomenon results from the collection of dust and sand from the desert surface by the strong winds blowing across it (Perry, 1967).

Arabia Area Climate

Different researchers have ventured into the study of the effects that the Arabian climate has on the different professionals working in the area. However, few researchers have documented the effects of the area’s climate on aviators, especially pilots (Perry, 1967). In one of these studies, the researchers sought to identify the effects of South Arabian Climate on army pilots (Perry, 1967). The results indicated that the area is particularly harsh to pilots in the army (Perry, 1967). The study was carried out through personal interviews, questionnaires, and reviews of medical records.

The Arabian climate is described as being rough for pilots, with documented cases of heat and cold stress in the course of operations of this personnel depending on the part they are working from. The aviation industry in the Middle East is rapidly evolving. It is currently a major part of the global aviation industry. The area is also home to many types of aircraft, with some being more susceptible to the elements in relation to others.

Heat Stress: Definition and Measurements

Heat stress is a condition in which the body is unable to maintain its temperature to the normal range after the environmental temperatures rise above certain levels (Razmjou, & Kjellberg, 1992). In normal individuals, a small rise in temperature causes sweating, which is a physiological reaction. However, in heat stress, the body is unable to cool itself through this process, resulting in several heat-induced illnesses (Razmjou, & Kjellberg, 1992). The heat-induced illnesses that occur in heat stress include heat cramps, exhaustion, and heat stress, which is the most severe of them (Razmjou, & Kjellberg, 1992).

Heat stress is a medical emergency that leads to the elevation of body temperature above levels that the body cannot control. Heat stress is often preceded by heat exhaustion, which is the elevation of temperatures in the body because of dehydration in the presence of high temperatures (Nunneley, & Myhere, 1976). Heat cramps are similar to any other type of cramps in the body. They are caused by working in extremely hot environments with resultant electrolyte imbalance (Nunneley, & Myhere, 1976). When sweat does not evaporate because of the high humidity in hot conditions, it may wet the clothing attire. The sweat may interact with the skin and result in heat rashes, which comprise another common component of heat stress.

There are many causes of heat stress in the body. They include dehydration in a hot environment, exposure to the sun, limited cooling in hot conditions, physical exertion, bulky dressing, the poor state of health, pregnancy, some medications, high temperatures, and humidity. The most important of them is exposure to hot conditions. The measurement for heat stress is possible through the estimation of body temperatures (Razmjou, & Kjellberg, 1992).

The Wet Bulb Globe Thermometer (WBGT) is the best measure for environmental heat stress. This measure incorporates humidity, the flow of air, and the ambient temperatures (Razmjou, & Kjellberg, 1992). Some of the other components in heat stress that may be measured independently include the wind speed, the humidity, and the estimation of the heat index. The measures provide an accurate way for heat stress estimation. The calculation allows for the estimation of the degree of heat stress.

Physiology of Heat Stress

Four basic mechanisms of heat transfer in the human body are known to include convention, radiation, evaporation (convention), and conduction (Nunneley, & Myhere, 1976). Evaporation and conduction are the main methods through which the body loses its heat. However, temperature gains can be by any process. The heat equation that is frequently used to explain the body temperature is a factor of all the processes. The core body temperature results from the interaction between the various processes of heat transfer. The difference between the heat gained by the body through conduction, radiation, convection, and convention and that lost through the same process contributes to the final standard body temperature.

In heat stress, the body temperature considerably rises and may exceed the ability of the various cooling mechanisms in place (Ailnut, & Allan, 1973). When these mechanisms are overwhelmed by the increase in temperature, the body cannot control its temperature. Hence, there is a rapid rise in the core temperatures. The rise in temperature interferes with the normal body processes that require a constant temperature to operate, with respiration being among the most affected processes (Ailnut, & Allan, 1973).

Aviators and Heat Stress

Heat stress is a problem for aviators, with pilots suffering from the condition in their pre-flight duties and/or while flying planes that are not air-conditioned such as helicopters (Perry, 1967). The aircraft characteristics combine with the humidity, ambient temperatures, and radiant heat, and wind speeds to cause high body temperatures and resultant heat stress (Sen-Jacobson, 1959). The aviation pilots, especially the army pilots, are forced to wear clothing and other gadgets to optimize their functioning. This situation also contributes to the rise in ambient temperatures (Perry, 1967).

Fatigue and elevated metabolic rates may cause the alteration of the body temperature regulatory ability for aviators, hence leading to heat stress. Many types of research done on the temperatures in some aircraft, especially helicopters, found that there were persistently raised body temperatures for these individuals. In some of the research findings, the elevated temperatures in cockpits are a result of the external high temperatures and the internal heat sources such as engine power, auxiliary power, and the electronic systems in the aircraft (Ailnut, & Allan, 1973).

Another major contributor to the high temperatures in the greenhouse effect (Perry, 1967), which will be discussed later. Studies that have evaluated the effects of heat stress on pilots have established a degree of reduction in cognitive performance for aviators (Ailnut, & Allan, 1973). The pilots also had disordered vigilance and time estimation, with an overall reduction in the reaction time (Perry, 1967). The effects of heat stress on the performance of aviators are important to evaluate, and hence the importance of this research.

Sources of Heat in a Cockpit

The cockpit takes different designs and shapes depending on the type of aircraft that is being discussed. There are differences in the materials that make the cockpit and the position of the different windows in the different aircraft. The sources of heat in any cockpit are dependent on the design of the cockpit and the involved four processes of heat transfer. The most significant of the sources of heat in the cockpit is the sun where solar radiation enters the cockpit from different sides (Nunneley, & Myhere, 1976). The windows and the front screen are the main areas where solar radiation enters the cockpit (Ailnut, & Allan, 1973).

The sun causes the air within the cockpit to be heated to temperatures above the normal, hence predisposing it to heat stress (Nunneley, & Myhere, 1976). Solar radiation that penetrates the aircraft’s body warms the sections of the aircraft that are not covered with opaque materials. The result of exposure to solar radiation is heating of the cockpit components, which in turn transmit the heat to the pilot and air in the same cockpit (Ailnut, & Allan, 1973). The pilots are also heated directly by solar radiation, with the result of this situation being the increased body temperature. When the plane is flying in the direction of the sun, or when the sun is directly overhead, the solar radiation is experienced most. The amount of cloud cover is important in the determination of heating from the sun (Ailnut, & Allan, 1973).

The cockpit is mostly equipped with instrumentation to aid the pilot and the flight engineers in their occupation. These components run on energy. Most of them produce considerable amounts of heat resulting from friction or resistance to the flow of electric current (Gibson, Cochrane, Harrison, & Rigden, 1979). Without proper insulation, the instruments in the cockpit produce enough heat to raise the temperatures in the cockpit. This may act in concert with the other sources of heat to cause heat stress. The engine in some aircrafts such as helicopters may also be a source of heat to the cockpit (Gibson, Cochrane, Harrison, & Rigden, 1979).

The other source of heat in the cockpit is that generated by the pilots because of the normal metabolic processes. When pilots are actively performing their duties in operating the aircraft, respiration rates increase, thus causing the production of heat. This heat may warm the cockpit via radiation and conduction and other methods of heat transfer. If the pilot is dressed in many types of attire or has different gadgets on the body, the body heat generated by radiation is not lost. Hence, the result is an increase in the core body temperatures (Gibson, Cochrane, Harrison, & Rigden, 1979). The clothing that the aviators wear also determines the conduction of heat away from the body, resulting in cooling. However, this cooling is interfered with if the pilots wear clothing that does o permit heat loss.

Greenhouse Effect

The greenhouse effect is a cause of raised temperatures in the cockpit of some types of aircraft. According to Perry (1967), this effect occurs in closed cabins. It is known to exacerbate the rise in temperature from other sources in the cockpit. The greenhouse effect is known to occur in cabins that have windows that are relatively opaque to long wavelengths (Perry, 1967) in the cockpit. The solar radiation causes heating of the internal surface in the cockpit, which transmits heat through the process of radiation (Perry, 1967). Since the windows are opaque to the long wavelengths emitted by the surfaces, they are reflected back to the cockpit, hence resulting in the amplification of heat in this space (Perry, 1967). In the cockpits that experience the greenhouse effect, the ambient temperatures have been measured to be higher than other cockpits.

The cabin air also affects the rise in temperature that is observed in the cockpits. According to Perry (1967), the rate of absorption of heat by cabin air is increased by the increase of humidity and carbon dioxide in the cockpit. The measurement of the WBGT heat stress index in cockpits reveals that the greenhouse effect causes significant heat stress (Perry, 1967). The high humidity in the cockpit that leads to the greenhouse effect comes from the respiration and sweating of the occupying pilots, with the respiration also leading to increased carbon dioxide that further worsens the greenhouse effect (Perry, 1967).

Avionic-produced Heat

Avionic-produced heat is also a major contributor to heat stress in aviation pilots during their work (Harrison, & Higenbottam, 1977, p. 522). Harrison and Higenbottam (1977, p. 522) state that although the measurement of avionic-produced heat is difficult, the combination of these forms of heat with solar radiation causes high temperatures. The heat produced from avionics varies from one type of plane to the other. The measures are difficult to estimate. The instrumentation in modern aircraft is a major source of avionic heat. There has been a challenge with the reduction of this heat, especially in the helicopters.

The clothing that pilots wear is an important determinant of heat stress and the frequency with which this stress occurs. Aviators usually wear different types of clothing depending on the prevailing weather conditions in the departure airport. The weather may be different at the airport where they land. In some of the researches done to establish the effects of clothing on heat stress, the researchers observed that there was a pragmatic increase in the body temperatures of individuals who wore certain types of clothing (Pellerin, Deschuyteneer, & Candas, 2004, p. 717).

Pellerin, Deschuyteneer, and Candas (2004, p. 717) state that the insulation that pilots get in the flights is due to the number and type of attire that they wear in their workplace. The clothing may inhibit the evaporation of sweat, thus leading to elevation of the pilots’ body temperature. Developments in the aviation industry have led to the introduction of new clothing that is supposed to protect the pilots while aiding in their work by increasing efficiency (Pellerin, Deschuyteneer, & Candas, 2004, p. 717). However, this clothing is a significant source of insulation for the pilots as they operate in hot conditions, thus contributing to the increase in body temperature and hence heat stress.

Different Environment, Locations, and Time of the Year

The temperature inside a cockpit varies with the environment, the location, and the time of the year. The weather is known to change in different parts of the year, with summers and winters occurring at different times. The seasonal variation of weather in line with the climate of an area is an important factor in the determination of how high temperatures in a cockpit will be (Perry, 1967). The location of an aircraft determines the temperatures that the cockpit is recording. Therefore, the Sahara desert will record higher temperatures than other parts of the world. The time of the year is also important. Pilots have to plan their journey while keeping this in mind. Among the most significant areas in terms of heat stress are deserted, which are important to discuss since the Arabian region is also mainly arid. In one of the researches evaluating the impact of the environment on their performance, Cardwell (1992) described heat stress as a major factor in the Persian Gulf war of 1991. The weather in this region was harsh to the servicemen operating here at that time. Pilots were treated for heat stress.

The arid region is one of the uncaring environments in the world. This climate has been known to trigger heat stress in many individuals. Many airports are located in the desert climate, with planes having to fly, land, and take off in these places (Perry, 1967). In the changes that have taken place in the aviation industry, planes are kept waiting for some time before takeoff. Most air conditioning systems are inefficient for stagnant planes (Cardwell, 1992). Therefore, planes in desert conditions are exposed to high temperatures even before takeoff. Cardwell (1992) describes the desert environment of Iraq as one of the places that the American military experienced heat stress.

This research was an article review. The benefits of using an article review over other forms of research include the shorter period required to carry out the research, the accuracy of information from other researchers, and the efficient utilization of resources. After the main objectives of the study were developed, the step that followed in the methodology was the search for articles to be used in the review. The keywords chosen for the search included heat, aviation, pilot, helicopter, and cockpit. After the determination of the keywords in the search, an appropriate database was selected for the search. The database that was selected for the search was PubMed. This site provided the best results of peer-reviewed articles.

The initial search produced over 100 articles using the keywords. These articles were later sorted to evaluate the most applicable ones. An inclusion criterion was used in the selection of articles. The basic rule is that they had to be written in English. To allow comparison of the various effects of heat stress, articles focusing on the heat stress in different aircraft types such as helicopters were chosen. The other articles that were selected in the search included those that discussed different situations, locations, environments, and climates. These articles were selected to help in the discussion of the subject from different angles.

The other criterion used to sort the articles is the use of factors, sources, or situations producing heat stress on the crews. These were compared with regard to the effect they leave on the performance of cabin crews and their operation endurance ability. This resulting research paper tries to compare the effect of the heat stress sources and different situations on pilot performance and comfort in a cockpit and the physiological and psychological effects of heat stress. It focuses more on the helicopter cockpit by comparing it with the other types of aircraft.

Helicopter vs. Fighter Cockpit

The literature provided the differences between the different types of aircraft in relation to heat stress. In research by Breckenridge and Level (1970), the AH-IG helicopter was found to have increased temperatures in the cockpit. These temperatures predisposed pilots to experience heat stress. The helicopter is one of the types of planes that have a higher risk of heat stress compared to other types of airplanes. Some of the reasons that make this type of aircraft more predisposed to high temperatures include the heat dissipated from the engine and the absence of air conditioning among other factors (Breckenridge, & Level, 1970).

The helicopter cockpit is closer to the engine compared to other types of aircraft. This exposition may reveal higher ambient heat. Breckenridge and Level (1970) recommended that the helicopter models they studied be fitted with air conditioners to prevent any form of heat stress. In their research, they found that there was increased sweating in the cockpit of the helicopters, more than it was experienced in other forms of aircraft (Breckenridge, & Level, 1970). The other type of aircraft that the pilots and other aviators operating it were susceptible to heat stress is the fighter aircraft. According to Nunneley and Myhre (1976), unlike other aircraft that are completely covered with opaque materials except for the windows, the fighter aircraft have bubble canopies to improve vision, and hence the main cause of high temperatures inside the cockpits of fighter aircraft.

In fighter planes that are in flight or waiting on the runway, the exposure to sunlight causes increased radiant heat load. The sun directly heats the skin of the fighter pilots. The air inside the cockpit is also heated. The glass contributes to the greenhouse effect (Nunneley, & Myhre, 1976). Ventilation in the fighter planes is enhanced through the installation of air conditioning, although the pilots are still vulnerable to heat stress (Nunneley, & Myhre, 1976).

Type of Exercise heavy vs. Light

The type of exercise that the aviators are carrying out is an important determinant of heat stress as earlier stated. Heavy exercise causes the use of a high respiration rate in the pilots, resulting in an increase in temperature and sweating (Harrison, Higenbottam, & Rigby, 1978). When a pilot is carrying out a heavy or difficult maneuver, he or she may use a lot of energy in the process. This situation is known to be a significant source of body heat (Harrison, Higenbottam, & Rigby, 1978). If not adequately cooled, the body’s temperature may rise to a high level, thus resulting in heat stress and related conditions. The heat stress that is obtained in case of increased temperature results from the interaction between the radiant heat from the sun, the avionic heat, clothing, and instrumentation within the cockpit (Boutcher, Maw, & Tylor, 1995). However, there are cases where the body respiration rate may rise above normal without any predisposition such as disease.

Season and Climate

The climate that the aviators work in and fly in determines whether heat stress affects them or not. In cold climates, it is highly unlikely that pilots will get heat stress, with the most likely pathology being cold stress (Thornton, & Vyrnwy-Jones, 1984). Working in a hot environment such as flying across the Arabian region can precipitate heat stress. Pilots have to take adequate measures to prevent this occurrence (Perry, 1967). The Arabian climate is hot in most parts of the year. Pilots and other aviators in the region have a higher predisposition to heat stress as compared to other parts of the world (Thornton, & Vyrnwy-Jones, 1984). Seasonal variations are also known to cause a concurrent variation in the instances of heat stress. Some seasons such as the “summers” experienced in the Middle East have more cases of heat stress compared to other seasons.

The article review also identifies climate as a significant part of the factors determining the development of heat stress in aviators. As a rule, aviators working in a hot and dry climate are more predisposed than any other individual working in a cooler climate (Perry, 1967). However, heat stress can occur anywhere in the universe since the climate is not the only cause of heat stress (Thornton, & Vyrnwy-Jones, 1984). According to Perry (1967), the Saudi Arabian climate is one of the hottest climates in the world. The fortunes that have been realized in oil have meant that the aviation industry is well-performing. Some aviators working in this country have had to deal with the problem of heat stress, with a significant number of pilots who are new to the area having experienced heat stress at one time during their career (Perry, 1967).

Nunneley and Flick (1981) observed that the prevalence of heat stress in hot climates was high. In their research, they stated that pilots often have to deal with the high temperatures in hot climates (Nunneley, & Flick, 1981). According to Nunneley and Flick (1981), the planes get heat soaked even before they take off. Climatic heat input continues when they are flying at low altitudes. In cooler climates, the causes of heat stress may not necessarily be the climate, but other causes such as sickness and avionic heat (Caldwell, 1992).

Pilot Suits and Uniform

The clothing that aviators put on affects the retention of heat and the eventual development of heat stress. Aviators such as those in the army are required to put on special uniforms and suits that are designed to help them in their navigation to protect them from acceleration forces and accidents (Gaul, & Mekjavic, 1987; Vallerand, Michas, Frim, & Ackles, 1991). Reardon, Fraser, and Omer (1998) investigated the effects of thermal stress on the performance of helicopter pilots, with this stress being caused by aviator uniforms that they wore. The researchers concluded that there were minor effects of the uniforms on the cognitive performance of pilots who had occlusive dressings in their operations (Reardon, Fraser, & Omer, 1998; Zhang, Huizenga, Arens, Wang, 1987).

The core body temperature increases with an occlusive dressing and uniform for pilots. Therefore, Reardon, Fraser, and Omer (1998) recommended that helicopter pilots should avoid physiological stresses that may alter their performance. Gaul and Mekjavic (1987) are some of the other researchers who evaluated the effects of aviation suits worn by pilots on their performance. They reported that the commercial pilots were more affected by the heat stress due to their manner of clothing as compared to the military pilots (Gaul, & Mekjavic, 1987). The average flights for military pilots are 27% shorter in relation to those of commercial pilots. This finding may reveal the differences in the experienced temperature changes. Different types of suits exist for pilots. However, the suits have their own effects in relation to eat stress.

One of the suits whose effects on the performance of people in flight were investigated is the Nuclear Biological Chemical (NBC) Individual Protective Equipment (IPE) (Thornton, & Caldwell, 1993; McLellan, Frim, & Bell, 1999). This suit was created to allow life-saving for aviators in the event of an accident. However, experiments conducted showed that survivors would be affected by the resultant heat stress if they landed in a hot area (Thornton, & Caldwell, 1993, p. 72). In the experiment conducted by Thornton and Caldwell (1993), the core temperatures of the individuals wearing the suits were reported to increase at a fast rate. In the event of an actual accident, the temperature rises and cause the eventual death of the victims, or cause them to abandon the useful suit (Thornton, & Caldwell, 1993, p. 73).

Anti-G Protection Suit

The acceleration forces acting on a pilot in a jet plane can affect his or her concentration by affecting the eyes and the brain. Special suits have been developed against these acceleration forces. These suits were studied to establish the effect that they have on the body temperature in hot conditions. Sowood and O’Connor (1994, p. 998) studied the effects of the newly developed anti +G z suit that was meant to protect the pilots as they were in flight. The researchers compared the effectiveness of the new anti G system against previous versions of the same suit where they measured the core temperature of the wearers (Sowood, & O’Connor, 1994, p. 998).

The results of the experiments showed that there were significant increments in the core body temperatures for these individuals (Sowood, & O’Connor, 1994). The increased core body temperature was significant in affecting the cognitive performance of the individuals in the suits. Heat stress resulted in the case of extremes scenarios. However, there was a temperature rise in the participants, although the rise was inadequate to allow decreased cognitive functioning and eventual accident (Sowood, & O’Connor, 1994).

Low-Level Flights

The effects of low-level flights on the temperature inside the cockpit were the subject of some of the reviewed studies. The researchers evaluated the effects of flying at low altitudes on the core body heat and the cockpit temperatures (Bollinger, & Carwell, 1975). In the research by Bollinger and Carwell (1975), the flights were able to fly in hot conditions and in low altitudes. However, the temperatures recorded in the cockpit were higher than conventional flights in most cases. The research showed that low altitude planes have a significantly raised chance of experiencing heat stress as compared to the pilots that flew in high altitudes (Bollinger, & Carwell, 1975, p. 1225).

Ground Standby

According to Froom, Schochat, Strichman, Cohen, and Epsten (1991), the ground standby time for helicopters is often long. It may reach up to a period of one hour. The reason for the long standby time is to ensure that the helicopters can take off at the scheduled time. Froom et al. (1991) reveal that the high temperatures that are prevalent in most areas in summer may affect the cockpit while the planes are on standby. This situation may add to the stress in pilots. These researchers managed to show that there was an increase in the WBGT for pilots that remained on standby for about an hour in the airports (Froom et al., 1991).

Harrison and Higenbottam (1977, p. 519) were other researchers who obtained the same results as Froom et al. (1991) in their research. The researchers observed that the duration that the aircrafts remained on the standby state was proportional to the greenhouse effect to which the cockpit was subjected (Harrison, & Higenbottam, 1977, p. 523). Although the pilots would open the canopy partially during the standby times, the greenhouse effects were still evident, with temperatures in the cockpit increasing constantly. Therefore, the pilots were predisposed to an increase in temperature when they stayed longer on the runway waiting for their chance to take off.

Location in the Cockpit

The location of the aviators in the cockpit is significant in determining the extent of heat stress that they experience during flight. Nunneley, Stribley, and Allan (1981, p. 287) are some of the researchers who investigated the differences in temperature at the different parts of the cockpit (Nunneley, & Maldonado, 1983). In a fighter plane with two pilots, the rear seat was described as being hotter compared to the front seat, with the differences in temperature also being evident in the different heights in the aircraft (Nunneley, Stribley, & Allan, 1981). Therefore, aviators who sat in the back seat were more likely to be affected by heat stress as opposed to those in the front seat. The head level was also reported to be cooler than other lower levels in the aircraft. The differences in temperature were said to be a result of the cooling system that was being utilized (Bollinger, & Carwell, 1975, Nunneley, Stribley, & Allan, 1981, p. 290).

Comparison of Different Sources of Heat in the Cockpit

The sources of heat stress in the cockpit were listed in most of the literature materials that were reviewed. Few of the researchers focused on a single source of heat in the cockpit. On rare occasions, they compared the different sources. The researchers measured the performance of the pilots and other aviators in relation to heat stress irrespective of its cause in the cockpit. The main source of heat in the cockpit recognized in the various studies is the radiation through the windshield. This source was recognized as an important influence on the performance of pilots (Nunneley, & Maldonado, 1983). The rate at which the decrease in performance occurred was more than exposure to other sources of heat.

For the helicopters, the second-largest source of heat in the cockpit was the engine heat. Pilots were significantly affected when these two major sources of heat acted in concert. Some of the studies investigated the effect of heat stress from the engine and its effect on the performance of aviators (Razmjou, & Kjellberg, 1992). The findings indicate that the effects are similar to those that occur from heat stress caused by other sources of heat. Aviators’ performance in these conditions drops significantly. As a result, they are vulnerable to accidents.

The source of heat that ranks third in the causation of heat stress to the aviators under simulation conditions is the mechanical and electrical equipment in the aircraft (Nunneley, & Maldonado, 1983). Aviators were found to be affected by the heat that was dissipated from the electrical and mechanical systems. The different studies used different measures of performance for the aviators. However, most of them provided similar results in the decrease in performance. The researchers also stated some limitations that would not allow room for comparison between the many sources of heat in the cockpit and their effect on the performance of the cockpit.

The other source of heat that was largely natural in the cockpit is the body metabolic process for the aviators. Pilots, just like any other individuals, have active respiration, which leads to considerable heat within the cockpit. The body has physiological mechanisms that are aimed at regulating the heat generated from the normal respiratory processes and external sources. However, there are situations where the body gets overwhelmed by the heat that is produced through normal respiration. This situation results in heat stress for the individual. This form of heat stress ranked after the above causes of heat stress.

Instrumentation also emerged as a significant source of heat in the cockpit. Most of the instruments in the cockpit use electricity. The resistance to the flow of the current in the wires used to operate the instruments results in the generation of heat. Although this source may be insignificant when compared to other sources of heat in the cockpit, it causes heat stress in association with the other sources identified above. This source of heat causes a significant reduction in performance for aviators, especially if they are forced to work in this environment for long hours. The comparison of the above sources of heat in the cockpit and their effect of heat stress on aviators can be done using a graph-based on information from the researches as shown below.

Physiological and Psychological Effects

The research reviewed the relevant literature on heat stress in pilots. Nunnely, Dowd, Myhre, and Stribley state that the effects of heat stress on the body can be measured through the estimation of different parameters. The measurements that are important in the evaluation of the results of the heat stress can be grouped in terms of mental manipulation, perceptual speed, and learning (Nunnely, Dowd, Myhre, & Stribley, 1978). Heat stress was demonstrated to affect these processes in normal individuals, with perceptual disturbances.

Nunnely, Dowd, Myhre, and Stribley (1978) showed that the only part of mental functioning that was not affected was the addition of columns. Learning was the most affected, with grave impairments in performance (Nunnely, Dowd, Myhre, & Stribley, 1978; Razmjou, & Kjellberg, 1992). Aircrew members are described in the research paper to be subjected to heat stress when flying and working in hot climates and when wearing some special suits. Therefore, the findings indicate that these individuals will be affected in their performance in these conditions.

Effects on Performance

Physiological (g protection).

Nunnely and Myhre (1976) observe a number of physiological changes that occur before an individual succumbs to heat stress. There is an observed reduction in reaction time for individuals who are exposed to heat stress. This reduction may be fatal in the aviation industry that requires the aviators to have an intact, if not fast reaction time. Another physiological change is the rise in error rate in these conditions. While these changes are taking place, individuals usually do not realize and remain confident about their performance (Nunnely, & Myhre, 1976). The tolerance of aircrew to acceleration is also affected by the decreased perception occasioned by heat stress (Nunnely, & Myhre, 1976). Heat stress is also associated with marked sweating, which often results in dehydration, which worsens heat stress and G-tolerance for aviators.

Psychological Effects

The psychological effects of heat stress are described as subtle in most of the reviewed research (Nunneley, & Stribley, 1979). However, these psychological effects are dangerous to any pilot operating an aircraft. They can lead to accidents and other events. The psychological effects include decreased response time, decreased attention, cognitive defects, and reduced performance of motor activities. These skills are central to the aviation industry. Heat stress causes a reduction in their use. The result is the decreased performance of the aviators and eventual redundancy (Froom, Kristal-Boneh, Ribak, & Caine, 1992).

Cut-off Points and Limitations

The effects of heat stress on aviators, though described as subtle in most of the research, warranted a cut-off point that would assure the safety of the aircrew and their passengers. The Fighter Index of Thermal Stress (FITS) is a good example of a cut-off developed to control the exposure of aircrew to hazardous heat stress (Nunneley, & Stribley, 1979, p. 639). FITS is applicable as a scale for the control of the stress that is occasioned by hot climates. It minimizes the chances of developing the physiological and psychological effects that may compromise performance. The maximum safe thermal radiation load was also described. Aviators should be trained on how to observe and apply it to reduce the effects of heat stress (Davis, & Kaufman, 1963). The limitations of this study included the unavailability of current literature findings on the effects of heat stress on aviators, especially for different types of aircraft. The suggestion is that more research can be carried out in the future to compare the different models of aircraft and the different climates under standardized conditions.

Heat stress is established to be a significant cause of compromise for aviators. The factors that are important in the occurrence of this condition include differences in the type of aircraft and the different climates in which the aviators have to operate. The helicopters and fighter aircraft pilots are the most affected by heat stress. Sources of heat in the cockpit include solar radiation, avionic-produced heat, body metabolic heat, the instrumentation, and the engine heat.

The recommendations include that a maximum safe thermal radiation load and the Fighter Index of Thermal Stress should be more specific, with aviation industries being made to adhere strictly to it. The applied air conditioning systems must assure effective air distribution in the cockpit. Regulations should also be made for low-level flights in different aircraft in summer. These regulations should also focus on reducing the ground stand-by time for pilots. These measures need to be effective in reducing the chances of heat stress development.

Ailnut, F., & Allan, R. (1973). The effects of core temperature elevation and thermal sensation on performance. Ergonomics, 16 (1), 189-196.

Bollinger, R., & Carwell, G. (1975). Biomedical Cost of Low- Level Flight in Hot Environment. Aviat. Space Environ. Med, 46 (10), 1221-1226.

Boutcher, S., Maw, J., & Tylor, N. (1995). Forehead Skin Temperature and Thermal Sensation during Exercise in Cool and Thermo-neutral Environments. Aviat. Space Environ. Med, 66 (1), 1058-1062.

Breckenridge, J., & Levell, C. (1970). Heat Stress in the cockpit of the AH-1G Helicopter. Aerospace Med, 11 (6), 621-626.

Caldwell, J. (1992). A Brief Survey of Chemical Defense, Crew Rest, and Heat Stress/Physical Training Issues Related to Operation Desert Storm. Military Medicine , 157 (6), 275-280.

Davis, H., & Kaufman, C. (1963) Experimental Determination of the Maximum Safe Thermal Radiation Loads For a fighter –Bomber Cockpit. Aviat. Space Environ. Med, 8 (6), 519-523.

Froom, P., Kristal-Boneh, E., Ribak, J., & Caine, Y. (1992). Predicting Increases In Skin Temperature Using Heat Stress Indices And relative Humidity in Helicopter Pilots. Israel Journal of Medical Sciences, 28 (1), 608-610.

Froom, P., Schchat, I., Strichman, L., Cohen, A., & Epstein, Y. (1991). Heat Stress on Helicopter Pilots during Ground Standby. Aviat. Space Environ. Med, 62 (1), 978-981.

Gaul, C., & Mekjavic, I. (1987). Helicopter pilot suits for offshore application. A survey of thermal comfort and ergonomic design. Applied Ergonomics , 18 (2), 153-158.

Gibson, T., Cochrane, L., Harrison, M., & Rigden, P. (1979). Cockpit Thermal Stress and Aircrew Thermal Strain During Routine Jaquar Operations. Aviat. Space Environ. Med, 50 (8), 808-812.

Harrison, H., Higenbottam, C., & Rigby, R. (1978). Relationship between Ambient, Cockpit and Pilot Temperatures during Routine Air Operations, Aviat. Space Environ. Med, 49 (1), 5-13.

Harrison, M., & Higenbottam, C. (1977). Heat Stress in an Aircraft Cockpit at Ground Standby. Aviat. Space Environ. Med, 8 (6), 519-523.

McLellan, M., Frim, J., & Bell, G. (1999). Efficacy of air and liquid cooling during light and heavy exercise while wearing NBC clothing. Aviat. Space Environ Med., 70 (8), 802-11.

Nunneley, S., & Myhere, L. (1976). Physiological Effect of Solar Heat Load in a Fighter Cockpit. Aviat. Space Environ. Med , 47 (9), 969-973.

Nunneley, S., & Flick, S. (1981). Heat Stress in the A-10 Cockpit: Flights Over Desert. Aviat. Space Environ. Med, 52 (9), 513-516.

Nunneley, S., & Maldonado, R. (1983). Head and/or Torso Cooling during Simulated Cockpit Heat Stress. Aviat. Space Environ. Med, 54 (6), 496-499.

Nunneley, S., & Stribley, R. (1979). Fighter Index of Thermal Stress (FITS): Guidance for Hot-Weather Aircraft Operations. Aviat. Space Environ. Med, 50 (6), 639-642.

Nunneley, S., Stribley, R., & Allan, J. (1981). Heat Stress in Front and Rear Cockpits of F-4 Aircraft. Aviat. Space Environ. Med , 52 (5), 287-290.

Pellerin, N., Deschuyteneer, A., & Candas, V. (2004). Local thermal unpleasantness and discomfort prediction in the vicinity of thermoneutrality. Eur J Appl Physiol , 92 (1), 717–720.

Perry, I. (1967). A Medical Survey of Climatic Effects on Army Aviators Operating in South Arabia. J R Army Med Corps , 113 (1), 213-219.

Razmjou, S., &Kjellberg, A. (1992). Sustained Attention and Serial Responding in Heat: Mental Effort in the Control of Performance. Aviat. Space Environ. Med , 63 (1), 594-601.

Reardon, M., Fraser, E., & Omer, J. (1998). Flight Performance Effects of Thermal Stress and Two Aviator Uniforms in a UH-60 Helicopter Simulator. Aviat. Space Environ. Med, 67 (1), 569-576.

Sen-Jacobson, W. (1959). Electroencephalographic study of pilot stress in flight. Aerospace Med, 30 (1), 797-801.

Sowood, P., & O’Connor, E. (1994). Thermal Strain and G Protection Associated with Wearing an Enhanced Anti-G Protection System in a Warm Climate. Aviat. Space Environ. Med , 65 (6), 992-998.

Thornton, M., & Vyrnwy-Jones, M. (1984). Environmental Factors in Helicopter Operations. J R Army Med Corps, 130 (1), 157-161.

Thornton, R., & Caldwell, J. (1993). The Physiological Consequences of Simulated Helicopter Flight in NBC Protective Equipment. Aviat. Space Environ. Med , 64 (1), 69-73.

Vallerand, A., Michas, R., Frim, J., & Ackles, K. (1991). Heat Balance of Subjects Wearing Protective Clothing with a Liquid- or Air-Cooled Vest. Aviat. Space Environ. Med, 62 (6), 383-391.

Zhang, H., Huizenga, E., Arens, E., & Wang, D. (1987). Thermal sensation and comfort in transient non-uniform thermal Environments. Aviat. Space Environ. Med, 50 (8), 808-812.

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Impact of Heat Stress on Poultry Health and Performances, and Potential Mitigation Strategies

Simple summary.

High environmental temperature alters the poultry health and performances by causing heat stress. Heat stress elicits physiological, behavioral, and production changes in poultry. This review article summarizes these changes along with the strategies that have been used in the poultry industry to ameliorate the adverse effects of heat stress in poultry.

Heat stress is one of the major environmental stressors in the poultry industry resulting in substantial economic loss. Heat stress causes several physiological changes, such as oxidative stress, acid-base imbalance, and suppressed immunocompetence, which leads to increased mortality and reduced feed efficiency, body weight, feed intake, and egg production, and also affects meat and egg quality. Several strategies, with a variable degree of effectiveness, have been implemented to attenuate heat stress in poultry. Nutritional strategies, such as restricting the feed, wet or dual feeding, adding fat in diets, supplementing vitamins, minerals, osmolytes, and phytochemicals, have been widely studied and found to reduce the deleterious effects of heat stress. Furthermore, the use of naked neck (Na) and frizzle (F) genes in certain breed lines have also gained massive attention in recent times. However, only a few of these strategies have been widely used in the poultry industry. Therefore, developing heat-tolerant breed lines along with proper management and nutritional approach needs to be considered for solving this problem. Thus, this review highlights the scientific evidence regarding the effects of heat stress on poultry health and performances, and potential mitigation strategies against heat stress in broiler chickens and laying hens.

1. Introduction

The poultry industry is growing across the world to fulfill the increasing demands of poultry meat and eggs. Poultry meat contains a low amount of saturated fatty acids and is rich in protein, vitamins, and minerals [ 1 ]. Similarly, poultry eggs are the most affordable source of animal protein [ 2 ]. Besides vitamins, minerals, and proteins, eggs are also rich in antioxidants such as lutein and zeaxanthin, which possess major benefits for eye health [ 3 ]. Considering these facts, the global consumption of poultry meat and eggs have doubled in the past decade and is expected to be doubled by 2050 [ 4 ]. To fulfill the demands, there has been an immense improvement in chicken genetics in the past decade. Broiler chickens, which weighed around 900 g in 56 days in the 1950s, were around 4202 g in 2005 [ 5 ]. Similarly, laying hens in the early 1900s used to lay 150 eggs per year while current commercial laying hens lay around 300 eggs annually [ 6 ]. These improved broilers and laying hens have higher metabolic rates and production performances [ 7 ]. Due to a higher metabolic rate, they produce more body heat and are prone to heat stress. High stocking density of birds, along with the high ambient temperature, increases the propensity of heat stress [ 8 ].

Heat stress is a major problem in the poultry industry affecting the health and performances of poultry. As of 2003, heat stress resulted in annual economic losses of $128 to $165 million in the poultry industry [ 9 ], and with the rise of global temperature, this number is speculated to increase in the coming years. Heat stress is a condition where chickens are unable to maintain a balance between body heat production and heat loss. Heat stress results from the interaction of different factors such as high environmental temperature, humidity, radiant heat, and airspeed; among them, high ambient temperature plays a significant role [ 10 ]. The normal body temperature of the chicken is around 41–42 °C, and the thermoneutral temperature to maximize growth is between 18–21 °C [ 11 ]. Studies have shown that any environmental temperature higher than 25 °C elicits heat stress in poultry [ 12 ]. As there is extensive scientific evidence about the detrimental effects of heat stress on poultry health and performances, and potential mitigation strategies, it is crucial to summarize these findings for poultry researchers and industry. Therefore, the objectives of this review paper are to summarize the (1) physiological, neuroendocrine, and behavioral changes in poultry under heat stress, and (2) potential mitigation strategies against heat stress in broiler chickens and laying hens.

2. Biological Changes in Poultry Due to Heat Stress

Heat stress in poultry results in several behavioral, physiological, and neuroendocrine changes that influence health and performances ( Figure 1 ).

Effects of heat stress on behavioral, physiological, neuroendocrine, and production traits.

2.1. Physiological Changes

Major physiological changes that take place in the heat-stressed birds are:

2.1.1. Oxidative Stress

Reactive oxygen species (ROS) are free radicals and peroxides produced typically within the cells during regular metabolism. They are essential for many cellular processes such as cytokine transcription, immunomodulation, and ion transportation. The excess ROS produced within cells are eliminated by physiological detoxifying mechanisms present within the cells. During the thermoneutral condition, activation of transcriptional factor Nrf2 causes the additional synthesis of a group of antioxidant molecules, which deals with increased ROS produced inside the cell [ 13 ]. However, due to the imbalance between these systems, either by higher production of ROS or by a decrease in the effectiveness of the antioxidant defense system, the cells are exposed to stress conditions commonly known as oxidative stress [ 14 , 15 ]. Previous studies in poultry have shown that heat stress is associated with cellular oxidative stress [ 13 , 16 ]. Excess free radicals produced during oxidative stress damage all the components of the cells including proteins, lipids, and DNA ( Figure 2 ). Effects of oxidative stress depend upon its severity and range from small reversible changes to apoptosis and cell death in the case of severe oxidative stress [ 17 ]. The oxidative stress in poultry is associated with biological damage, severe health disorders, lower growth rates, and economic losses [ 16 ].

Schematic diagram showing the redox system. ( A ) Normal condition, and ( B ) under heat stress.

2.1.2. Acid-Base Imbalance

Birds lack sweat glands and have feathers throughout the body [ 18 ]. Those features impair thermoregulation, and as a consequence, they need to release heat via active mechanism (i.e., panting) during higher ambient temperature. Panting is a phenomenon exhibited by the birds by opening their beak to increase respiration rate and evaporative cooling from the respiratory tract. During panting, excretion of CO 2 occurs at a greater rate than the cellular production of CO 2 , which alters the standard bicarbonate buffer system in the blood. The reduction of CO 2 leads to a decrease in the concentration of carbonic acids (H 2 CO 3 ) and hydrogen ions (H + ). In contrast, the concentration of the bicarbonate ions (HCO 3 − ) is increased; thus, raising the blood pH, i.e., the blood becomes alkaline. To cope with this situation and maintain the normal blood pH, birds will start excreting more amount of HCO 3 − and retain H + from the kidney. The elevated H + alters the acid-base balance leading to respiratory alkalosis and metabolic acidosis ( Figure 3 ) and is associated with the decline in production performances of poultry [ 19 ].

Schematic diagram showing an acid-base imbalance in poultry under heat stress.

2.1.3. Suppressed Immunocompetence

Heat stress is known to suppress immunity in the chicken [ 10 ]. As a result, the prevalence of contagious and infectious poultry diseases, such as Newcastle disease (ND) and Gumboroo disease, is relatively higher during the summer season in tropical countries [ 20 ]. Besides this, the size of immune-related organs such as the spleen, thymus, and lymphoid organs are also regressed in the heat-stressed birds [ 21 , 22 ]. The level of antibodies was also lowered in the heat-stressed birds [ 23 ]. Likewise, total white blood cell counts (WBC) are significantly lowered, whereas the heterophils to lymphocytes (H/L) ratio is higher in heat-stressed birds [ 24 ].

2.2. Neuroendocrine Changes

The neuroendocrine system plays a crucial role in maintaining homeostasis and normal physiological functioning of birds during heat stress. In birds, the sympathoadrenal medullary (SAM) axis is activated and regulates homeostasis during the early stage of heat stress. The increase in ambient temperature is perceived by the sympathetic nerves, which transmit the impulse to the adrenal medulla. The adrenal medulla increases the secretion of catecholamines, which cause a surge of glucose release in the blood, deplete liver glycogen, reduce muscle glycogen, increase respiration rate, vasodilate the peripheral blood vessels, and increase neural sensitivity to cope with the stress [ 11 , 25 ]. As stress persists for a more extended period, the hypothalamic-pituitary-adrenal (HPA) axis is activated. In response to the stress, corticotrophin-releasing hormone (CRH) is secreted from the hypothalamus, which triggers the release of an adrenocorticotrophic hormone (ACTH) from the pituitary. ACTH increases the production and release of corticosteroid by the adrenal glands [ 26 ]. Corticosteroid stimulates gluconeogenesis to increase plasma glucose levels [ 11 , 25 ]. Thyroid hormones, triiodothyronine (T3) and thyroxine (T4), released by the thyroid gland, also play a critical role in maintaining metabolic rate. Previous studies have shown that T3 concentrations were lowered in the heat-stressed birds [ 27 , 28 , 29 ], whereas T4 concentrations were found inconsistent in different studies [ 27 ]. The reduction of T3 concentration during heat stress is due to a decrease in peripheral deiodination of T4 to T3 [ 30 ]. There is also a difference in T3 secretion between selected breeds and native breeds. The plasma T3 levels in dwarfs (dw) chicken are usually less than half of the levels in selected breeds of chicken. Dwarf gene (dw) is found to inhibit the conversion of T4 to T3 in peripheral tissue, resulting in a lower T3 level in dwarfs [ 31 ]. Melesse et al. [ 32 ] also reported a lower level of T3 in Naked neck laying hens as compared to Lohman white and New Hampshire laying hens. Besides this, the secretion of the gonadotrophin-releasing hormone is also found to be impaired in heat-stressed birds [ 33 ]. Moreover, sex hormones such as plasma progesterone, testosterone, and estradiol were also found to be lowered in heat-stressed White Leghorns [ 34 ]. These hormonal changes are responsible for reduced growth performance [ 22 ] and reproductive efficiency [ 35 ] of hyperthermic birds.

2.3. Behavioral Changes

When birds are exposed to a higher environmental temperature than their thermoneutral temperature, they try to dissipate excess heat produced inside the body, which is manifested by specific behavioral changes in birds. Chickens in the thermal stress condition spend less time walking and standing, consume less amount of feed and more water, spread wings, and cover their body surface in the litter. Furthermore, the characteristic signs of panting are also observed in heat-stressed birds [ 10 ].

These major physiological, neuroendocrine, and behavioral changes lead to increased mortality, decreased feed intake, reduced final body weight, decreased quality of meat and eggs, and increased feed conversion ratio (FCR) in poultry. Thus, heat stress has been of paramount importance in the poultry industry considering global warming and economic losses. To cope with this problem, different strategies have been employed by researchers and farmers [ 36 ].

3. Potential Strategies to Mitigate Heat Stress in Poultry

Major strategies that have been used to mitigate the detrimental effects of heat stress in poultry are discussed in this review paper.

3.1. Feeding Strategies

3.1.1. feed restriction.

Restricting the feed during the hotter period of the day has been a common practice in poultry production. In this practice, feed intake is reduced by withdrawing feed for a certain period (generally 8 a.m. to 5 p.m.) to reduce the metabolic rate of birds. Feed restriction is found to reduce rectal temperature, minimize mortality [ 37 , 38 ] and decrease abdominal fat [ 39 ] in heat-stressed broilers. Uzum et al. [ 38 ] found that restricting the availability of feed to 8 h a day during the hot periods in broilers improved feed efficiency and shortened tonic immobility; a measure to determine fearfulness in which birds are placed on its back for observing righting reflex. Similarly, in the case of broiler hens, limiting feed provision was found to reduce heat production by 23% [ 40 ]. Yet, this approach is not widely used in the poultry industry, as it results in reduced growth rate and delayed marketing age of the birds [ 37 , 38 , 41 , 42 ].

3.1.2. Dual Feeding Regime

Practical observations have shown that feed restriction results in overcrowding and rush at a re-feeding time resulting in some additional mortality. Thus, the dual feeding regime has been devised to ensure birds have access to feed throughout the day. The thermic effects of proteins are higher than carbohydrates and produce higher metabolic heat [ 43 ]. Taking this into account, the protein-rich diet is provided during cooler times and the energy-rich diet during the warmer period of the day. Studies have shown that providing a protein-rich diet from 4 p.m. to 9 a.m. and an energy-rich diet during the 9 a.m. to 4 p.m. heat stress period was found to reduce the body temperature [ 44 , 45 ] and mortality in the heat-stressed broilers [ 44 ]. However, this approach could not enhance growth and feed efficiency in heat-stressed birds [ 45 ].

3.1.3. Wet Feeding

During heat stress, birds lose a high amount of water through the respiratory tract, and there is a marked increase in water intake to restore thermoregulatory balance [ 18 ]. Adding water in the feed helps increase water intake and reduces viscosity in the gut resulting in the faster passage of the feed. Wet feeding stimulates pre-digestion, improves absorption of the nutrients from the gut, and accelerates the action of the digestive enzyme on the feed [ 46 ]. In broilers, wet feeding improved the feed intake, body weight, and weight of the GI tract [ 47 , 48 , 49 ]. In laying hens, feeding of wet feed during the high temperature increased dry matter intake, egg weight, and egg production [ 36 ]. Although this approach was found to have beneficial effects in heat-stressed birds, it is less common among poultry farmers, as there is a risk of fungal growth in the feed causing mycotoxicosis in the birds.

3.1.4. Adding Fat in the Diet

Higher energy diets were effective in partially mitigating the effects of heat stress in poultry. During metabolism, fat produces lower heat increment as compared to protein and carbohydrates [ 50 ]. Considering this fact, supplementation of fat in the diet has been a general practice in the hot climatic regions to increase the energy level and diminish the detrimental effects of heat stress. Supplementation of fat in the poultry diet not only helps to increase the nutrient utilization in the GI tract by lowering the rate of food passage [ 51 ] but also helps to increase the energy value of the other feed constituents [ 52 , 53 ]. Adding fat at the level of 5% to the diet in heat-stressed laying hens was found to increase feed intake by 17% [ 54 ]. Similarly, significant improvement in the broiler performance was observed when the 5% fat diet was provided [ 55 ]. Attia et al. [ 56 ] also reported that increasing the oil supplementation in the higher protein concentration diet relieved the negative effects of chronic heat stress on broiler performance, meat lipids, and physiological and immunological traits. In addition to these benefits, adding fat significantly increased abdominal fat in heat-stressed broilers [ 55 ].

3.1.5. Supplementation of Vitamins, Minerals, and Electrolytes

Vitamin E (alpha-tocopherol) is a fat-soluble vitamin that has antioxidant activity and helps to scavenge free radicals produced inside the cell. Vitamin E is found to modulate inflammatory signaling, regulate the production of prostaglandins, cytokines, and leukotrienes, and also improve the phagocytic activity of macrophages in broiler chickens [ 57 ]. Furthermore, Vitamin E also helps to improve immunity by inducing proliferation of lymphocytes [ 58 , 59 ]. Dietary supplementation of vitamin E in heat-stressed laying hens is found to improve egg production, egg weight, eggshell thickness, egg specific gravity, and Haugh unit [ 60 ]. Bollengier-Lee [ 61 ] concluded that dietary supplementation of 250 mg vitamin E/kg of feed is optimum for alleviating adverse effects of chronic heat stress in laying hens. The liver is an essential organ for egg formation as it helps in the synthesis and release of egg yolk protein-vitellogenin. Yardibi et al. [ 62 ] stated that vitamin E helps to improve the egg production by preventing liver damage in the heat-stressed birds and thus, facilitate the synthesis and release of vitellogenin [ 63 ]. Similarly, broilers supplemented with vitamin E (250 mg/kg of feed) have reduced liver and serum malondialdehyde (MDA) concentration, and increased serum and liver vitamin E and A concentration in heat stress conditions [ 64 ], as summarized in Table 1 . The combination of vitamin E (100 mg/kg of feed), vitamin C (200 mg/kg of feed) and probiotics ( Saccharomyces cerevisiae and Lactobacillus acidophilus at 2 g/kg of feed) was found to be more effective to attenuate negative effects of heat stress in broilers under chronic condition [ 65 ].

Summary of the beneficial effects of vitamins, minerals, phytochemicals, and osmolytes in heat-stressed poultry.

Vitamin A is associated with antibody production and T cell proliferation [ 66 ]. Vitamin A is the most effective antioxidant at low oxygen tensions, which is found to quench singlet oxygen, neutralize thiyl radicals, and combine with and stabilize peroxyl radicals [ 67 ]. In a study, supplementation of a higher level of vitamin A (6000 and 9000 IU/kg of feed) was found to increase the egg weight in the heat-stressed laying hens [ 68 ]. They also reported that hens exposed to heat stress immediately after NDV (Newcastle disease virus) vaccination require a higher amount of vitamin A for an adequate level of antibody production. In broilers, supplementation of vitamin A (IU/kg of feed) was found to increase the live weight gain, improve feed efficiency, and decrease the serum MDA concentration in the heat-stressed birds [ 69 ].

Vitamin C is a water-soluble antioxidant that protects against oxidative stress by scavenging ROS, neutralizing vitamin E-dependent hydroperoxyl radicals, and protecting proteins from alkylation and by electrophilic lipid peroxidation products [ 70 ]. Vitamin C is also known to improve immunity by enhancing the differentiation and proliferation of T and B cells [ 71 ]. Although poultry can synthesize vitamin C, the amount is limited during heat stress conditions [ 72 ]. Thus, dietary supplementation of vitamin C is an effective strategy to reduce the harmful effects of heat stress in poultry. Supplementation of vitamin C (250 mg/kg of feed) improved growth rate, nutrient utilization, egg production, and quality, immune response, and antioxidant status in heat-stressed birds [ 72 ]. Dietary supplementation of vitamin C lowered the serum concentration of MDA, homocysteine, and adrenal corticotropin hormone in heat-stressed Japanese quail [ 73 ]. In broilers, dietary supplementation of 200 mg ascorbic acid per kg of feed improved body weight gain and FCR [ 74 ].

Zinc is an essential nutrient required for the enzymatic activity for more than 300 different enzymes. Zinc is associated with the antioxidant defense system, immune function, and skeletal development [ 75 ]. Zinc also plays an essential role in the synthesis of metallothionein, which acts as a free radical scavenger [ 76 ]. Moreover, zinc is an integral component of carbonic anhydrase, the enzyme that catalyzes the formation of carbonates, an essential compound for eggshell mineralization. [ 77 ]. The supplementation of zinc helped to suppress the free radicals by being part of superoxide dismutase, glutathione, glutathione S-transferase, and hemeoxygenase-1 [ 78 ]. In broilers, supplementation of the organic form of zinc (40 mg/kg of feed) was effective in improving body mass growth, reducing the level of the lipid peroxide, and increasing the activity of superoxide dismutase enzyme during summer [ 79 ]. Supplementation of 30 mg of Zinc (Zn) and 600 mg of Magnesium (Mg) per kg of feed improved live weight gain, feed intake, and hot and chilled dressing percentage in the heat-stressed quails [ 80 ]. The supplementation of zinc (60 mg/kg of feed) in the diet of egg-laying Japanese quail was also associated with reduced MDA concentration, increased serum vitamin C and vitamin E level, and egg production [ 81 ]. In laying hens, dietary supplementation of zinc (80–100 mg/kg of feed) [ 82 , 83 ] as Zn-methionine was effective in improving the eggshell thickness and mitigating the eggshell defects seen in the laying hens under heat stress.

Chromium is an essential mineral, which is an integral component of chromodulin and is also necessary for insulin functioning [ 84 ]. Moreover, chromium is also involved in carbohydrate, protein, lipid, and nucleic acid metabolism [ 85 ]. Sahin et al. [ 86 ] researched the effects of chromium supplementation (chromium picolinate CrPic) at different doses (200, 400, 800 or 1200 µg/kg of feed) in heat-stressed broilers, where they found that increased supplementation of chromium was associated with an increase in body weight, feed intake, and carcass quality. They also observed a decreased level of serum corticosterone, serum glucose, cholesterol, and increased serum insulin level. Moreover, the organic form of chromium supplemented as chromium methionine was also found to improve the cellular and humoral immune responses in broilers during heat stress [ 87 ]. In laying hens, dietary supplementation of 0.4–2 mg chromium/kg of feed as CrPic improved immune response, egg quality, Haugh unit [ 88 , 89 ], and reduced serum glucose, cholesterol, and triglyceride concentration [ 90 ].

Selenium is a vital component of at least 25 different selenoproteins, most of which are the different parts of the enzymes, such as glutathione peroxidase and thioredoxin reductases [ 91 , 92 ]. Type I deiodinase enzyme is one such enzyme that helps in the conversion of thyroxin into active triiodothyronine [ 93 ]. Two different forms of selenium, i.e., inorganic forms (sodium selenite and selenite) and organic forms (selenomethionine and selenium-yeast) are used as supplements for poultry. The organic forms are more easily absorbed than inorganic forms [ 94 ]. Dietary supplementation of selenium (0.3 mg/kg of feed) is found to improve the live weight and FCR in broilers during heat stress [ 95 ]. Similarly, supplementation of sodium selenite at 0.1 or 0.2 mg/kg of feed improved the carcass quality and performance of quails reared under high temperature [ 64 ]. Selenium is found to improve the productive and reproductive performance of laying hens [ 96 ] Supplementation of the selenized yeast in the diet of laying hens also improved the egg weight, egg production, Haugh units, and eggshell strength during heat stress [ 97 ]. In laying quails, there was a linear increase in feed intake, body weight, and egg production; and improvement in feed efficiency upon selenium supplementation (0.15 and 0.30 mg/kg of feed sodium selenite or selenomethionine) under heat stress [ 98 ]. They reported that Haugh units and eggshell weights were also increased upon supplementation of both organic and inorganic selenium.

Electrolytes

Panting in heat-stressed bird alters the acid-base balance in blood plasma and ultimately leads to respiratory alkalosis. This acid-base imbalance can be recovered by supplementation of electrolytes such as NH 4 Cl, NaHCO 3 , and KCl. During respiratory alkalosis, birds excrete a higher amount of bicarbonate ions from the kidney to restore normal blood pH. These bicarbonates ions are further coupled with Na + and K + ions before being excreted through the kidney. Ultimately, the loss of ions results in an acid-base imbalance [ 99 ]. Thus, sodium and potassium supplementation is preferred in heat-stressed birds to increase the blood pH and blood HCO 3 − , while chloride is supplemented to reduce these parameters [ 100 ]. A higher range of dietary electrolyte balance (DEB), i.e., 200–300 mEq/kg, has been suggested to be effective in ameliorating the detrimental effects of heat stress in poultry [ 101 ]. Several studies have shown sodium bicarbonate (NaHCO 3 ) as the salt of choice during heat stress as it contains Na + and HCO 3 − [ 101 ]. Moreover, supplementation of NaHCO 3 in heat-stressed laying hens is also found to improve eggshell quality [ 77 ]. Incorporation of NaHCO 3 (up to 0.5%) into broiler diets also enhanced the performance of heat-stressed broiler birds [ 102 ]. Similarly, Smith et al. [ 103 ] found that dietary levels of 1.5–2.0% K from KCl were effective in improving FCR during chronic heat stress conditions. Besides including these salts in the diet, supplementation of 0.2% NH 4 Cl or 0.15% KCl, 0.6% KCl, 0.2% NaHCO3, and carbonated water in drinking water also improved the performance in the heat-stressed broiler chickens [ 36 ].

3.1.6. Supplementation of Phytochemicals

Different types of phytochemicals have been supplemented in the diet to mitigate heat stress in poultry. Some of them are discussed here.

Lycopene is a predominant carotenoid mainly found in tomatoes and tomato products, and is known to enhance the production of antioxidant enzymes through activation of antioxidant response element in the DNA [ 104 ]. Supplementation of lycopene (200 or 400 mg/kg of feed) in heat-stressed broilers improved the cumulative feed intake, body weight, and FCR [ 105 ]. Lycopene is found to improve the level of antioxidant enzymes such as superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) in broilers [ 104 ]. In laying hens, dietary supplementation of lycopene improved oxidative status, enhanced vitamin levels in the egg, and also improved oxidative stability and yolk color of the egg [ 104 ].

Resveratrol

Resveratrol is natural bioactive polyphenols mainly found in grapes, peanuts, berries, and turmeric. Previous studies have shown that supplementation of resveratrol (400 mg/kg of feed) enhanced the antioxidant capacity in the broilers during heat stress [ 106 ]. Supplementation of resveratrol at 300 or 500 mg/kg of feed improved the average daily gain, decreased the rectal temperature, lowered the level of corticosterone, adrenocorticotropin hormone, cholesterol, and MDA in yellow-feather broilers under heat stress [ 107 ]. Additionally, in the same study, resveratrol also increased the level of triiodothyronine, glutathione, total superoxide dismutase, catalase, and glutathione peroxidase during heat stress [ 107 ]. Resveratrol also improved different gut health parameters such as microbial profile, villus-crypt structure, and expression of the tight junction and adherence junction related genes in the heat-stressed broilers [ 108 ] Interestingly, resveratrol improved meat quality in the heat-stressed broilers by increasing the muscle total antioxidant capacity (T-AOC) and activity of antioxidant enzymes (catalase, GSH-Px) [ 109 ]. In laying hens, supplementation of 200 mg resveratrol/kg of feed improved the egg production, while 400 mg resveratrol/kg of feed reduced the total serum cholesterol and triglycerides, reduced egg cholesterol content, improved antioxidant activity, and improved egg sensory scores [ 110 ].

Epigallocatechin Gallate (EGCG)

Epigallocatechin gallate (EGCG) is the polyphenols present in green tea extract that possess high antioxidant and anti-inflammatory properties. Luo et al. [ 111 ] used different dosages of EGCG in the feed (0, 300 and 600 mg/kg) of heat-stressed broiler birds where they found a linear increase in body weight, feed intake, and level of serum total protein, glucose and alkaline phosphatase activity in the heat-stressed birds. In a similar experiment, Xue et al. [ 112 ] reported improvement in the body weight and antioxidant enzymes (GSH-Px, SOD, and catalase) in the liver and serum of heat-stressed broiler birds with the dietary inclusion of EGCG. Sahin et al. [ 113 ] supplemented 200 or 400 mg of EGCG/kg of feed in heat-stressed female quails where they observed that increased supplementation of the EGCG linearly increased feed intake, egg production, hepatic SOD, catalase, and GSH-Px activity and resulted in a linear decrease of hepatic MDA level.

Curcumin is the primary polyphenols extracted from turmeric and possesses antioxidant and anti-inflammatory properties [ 114 ]. As animals readily absorb curcumin, its use as a potential compound to mitigate heat stress in poultry has received attention in recent years [ 106 ]. Previous studies have shown that feed with curcumin improves the growth performance of heat-stressed broiler birds [ 115 , 116 , 117 ]. Zhang et al. [ 115 ] found that the inclusion of curcumin at 100 mg/kg of feed significantly improved the final body weigh in broilers under heat stress conditions. Curcumins fortification reduced the mitochondrial MDA level; reduced the ROS production by increasing the activity of Mn-SOD, GSH-Px, Glutathione S-transferase (GSST) [ 117 ] and increased gene expression of thioredoxin-2 and peroxiredoxin-3 [ 115 ] during heat stress in broilers. In laying hens, supplementation of 150 mg/kg of feed with curcumin improved the laying performance, egg quality, antioxidant enzyme activity, and immune function during heat stress [ 118 ].

3.1.7. Supplementation of Osmolytes

Betaine is a small zwitterionic quaternary ammonium compound found in microorganisms, animals, and plants [ 119 ]. Betaine is incorporated in the animal diets in different forms; as anhydrous betaine, betaine monohydrate, or betaine hydrochloride [ 120 ]. Betaine possesses two fundamental metabolic activities, i.e., methyl donor activity and osmotic activity. Under heat stress, betaine plays a vital role in regulating the cellular osmotic environment, preventing dehydration by increasing the water-holding capacity of the cell [ 120 ]. Furthermore, betaine is also found to have anti-inflammatory properties and improves the intestinal function [ 121 ]. During heat stress, supplementation of betaine ranging from 0.05–0.20% improved the feed intake, carcass trait, and egg production parameters in broilers, layers, and ducks [ 120 ]. Chand et al. [ 122 ] investigated the effect of betaine in chronic heat-stressed broilers by using three different (1, 1.5, and 2 g/kg of feed) dosages of betaine. They reported significant improvement in the feed intake, weight gain, and FCR for the higher level of betaine. Furthermore, they also found a lower H/L ratio and improvement in the dressing percentage in the treatment groups supplemented with betaine. In another study, besides growth performance parameters, dietary supplementation of betaine during the cyclic heat stress condition improved digestive function and carcass traits in indigenous yellow-feathered broilers [ 123 ]. Betaine supplementation (1 g/kg of feed) also increased feed intake, protein digestibility, dressing out percentage, and improved FCR in slow-growing chicks [ 124 ]. In laying hens, supplementing betaine (1000 mg/kg of feed) along with vitamin C (200 mg/kg of feed) improved laying performance during the chronic heat stress [ 125 ]. In roosters, supplementation of betaine (1000 mg/kg of feed) improved sperm concentration and livability, seminal plasma total antioxidant capacity, fertility, and welfare under chronic heat stress [ 126 ].

Taurine, 2-aminoethanesulfonic acid, is one of the most abundant amino acids distributed in different parts of animal tissues [ 127 ]. Taurine plays a role in antioxidant action, bile acid conjugation, maintenance of calcium homeostasis, osmoregulation, and membrane stabilization [ 127 ]. The use of taurine to mitigate heat stress in poultry has gained popularity in recent days under chronic heat stress. Supplementation of 0.1% taurine in the drinking water demonstrated significant improvement in the final body weight of chronic heat-stressed broilers. Moreover, expression of heat shock proteins was lowered in the taurine supplemented broilers indicating improved thermotolerance in these birds under heat stress [ 128 ]. Similarly, He et al. [ 129 ] reported that supplementation of taurine (5 g/kg of feed) in broilers under heat stress improved jejunal morphology, decreased the concentrations of serum ghrelin, increased the concentrations of somatostatin and peptide YY in the duodenum and increased the expression of appetite-related genes [ 129 ]. Taurine supplementation was found to reduce fat deposition in the liver of chronic heat-stressed broilers [ 130 ]. Supplementation of the taurine (0.1% of feed) in the laying hen exhibited enhanced oviductal health and reduced oviductal injury [ 131 ]. Taurine supplementation in the laying hens under heat stress, however, is not well studied, and thus, further research is warranted.

3.2. Genetic Approach

Improved broiler lines have a higher metabolic rate; as a result, they are more susceptible to heat stress. Thus, developing poultry lines incorporating some of the genes that help to reduce heat stress can be instrumental in further excelling the production traits of these breeds in the hot and arid areas.

3.2.1. Naked Neck (Na) Gene

Na gene is the single dominant autosomal gene that helps to reduce feathers in the neck region, thus helps to dissipate heat through the neck region in birds. The naked neck gene reduces the feather cover by 20% and 40% in Na/na (heterozygous necked neck) and Na/Na (homozygous necked neck), respectively, as compared to normal siblings (na/na) [ 132 ]. Na gene in broilers is associated with the increase in breast muscle and body weight [ 133 , 134 ], reduce abdominal fat [ 135 ], and body temperature [ 136 ]. The total plasma cholesterol level and H/L ratio were significantly lowered in the naked necked birds as compared to typical birds during the summer season [ 137 ]. Laying birds with a naked neck gene also displayed an improvement in egg mass, number, and quality under hot temperatures [ 138 ]. These studies indicate that there is a scope of incorporating such genes to develop a chicken breed that can cope with heat stress.

3.2.2. Frizzle Gene

The frizzle (F) gene causes the curving of the outline of the feather resulting in a reduced featherweight and insulating property of the feather cover and increases heat radiation from the body [ 36 ]. Homozygous frizzle gene in laying hens improved the egg production and quality traits by increasing the magnitude of heat dissipation as compared to heterozygous carriers and normal feathered hens [ 139 ]. Sharifi et al. [ 140 ] reported a significant interaction between feathering genotype (FF) and environmental temperature for all reproductive traits (egg production, hatchability, and chick production) except sexual maturity under heat stress. At higher temperatures, they reported a distinct reduction in all reproductive traits except sexual maturity for normally feathered hens compared with frizzle-feathered hens, whereas under lower temperatures (19 °C), egg production, and the number of chicks of the FF genotype were reduced and sexual maturity was delayed.

The beneficial effect of the F gene as compared to the Na gene is lower in broilers at high temperatures. However, there is an additive effect in the double heterozygous (Na/Na F/f) broiler [ 141 ]. So, the frizzle gene is another potential target for developing heat-tolerant chickens.

3.2.3. Dwarf (dw) Gene

The dwarf gene is a sex-linked recessive gene associated with reduced body weight by about 40% and 30% in homozygous males and females, respectively [ 54 ]. There has been a discrepancy regarding the advantage of the dw gene in the heat-stressed laying hens. Decuypere et al. [ 142 ] concluded that the inherent heat tolerance of dw genotype in laying hens was uncertain. It has been found that the dw gene in fast-growing broiler chickens under chronic heat stress conditions did not improve heat tolerance [ 143 ].

3.3. Housing

Naturally ventilated open-type housing is most common in the tropics, which should be oriented in the east-west direction [ 144 ]. The width of such housing should not exceed 12 m, while the length of the building can depend upon the convenience. In the case of long buildings, doors should be placed at an interval of 15–30 m. It is recommended to have a side-wall height of at least 2.1 m along with curtails that can be raised or lowered easily. Regarding the roof, a roof slope of 45 °C is recommended as it reduces the heat gain of the roof from direct solar radiation [ 54 ]. It has been observed that farmers used different local materials such as thatched and bamboo to insulate the roof. In the case of an uninsulated metal roof, a sprinkling roof with cool water has also been a common practice to reduce heat load in poultry houses [ 54 ]. Moreover, in this kind of housing, fans (either suspended from the interior building structures or vertical ceiling fans), interior fogging, and sprinkling systems have been used effectively [ 54 ].

With the advancement of technologies, there has been a surge in the use of a closed house system for more intensive farming systems recently [ 145 ]. Closed housed systems equipped with air conditioning, cooling pads, cool perches, and exhaust fans are found useful in attenuating the negative effects of heat stress in poultry. However, such houses are expensive to build and operate in developing nations [ 146 ], and therefore dietary manipulations are more appropriate.

3.4. Others

In addition to the aforementioned strategies, some other strategies have been used to combat heat stress in poultry, such as early heat conditioning (EHC) [ 36 ], early feed restriction (EFR) [ 36 ], reducing stocking density of birds [ 8 , 147 ], and thinning the litter during summer seasons. In EHC, birds are exposed to high temperatures (36 °C) for 24 h at 3 to 5 d of age [ 36 ], while in EFR about 60% of feed is restricted on days 4, 5, and 6 [ 36 ]. EHC and EFR developed the tolerance capacity of birds against high temperature during the later growth stage before marketing [ 36 ]. EHC may play a role in the acquisition of heat tolerance capacity by suppressing the expression of an uncoupled protein (avUCP) [ 148 ] and by improving the expression of HSP70 [ 149 ] while EFR might possess beneficial effects in heat stress by improving the expression of HSP70 [ 149 ]. Reducing the stocking density of birds increases the feed and water accessibility, and also increases heat dissipation from the body [ 8 ]. Thinning of the litter helps to make the litter dry, making it favorable for birds to cool their body by dust bathing.

In ovo supplementation of nutrients is known to induce post-hatch immunity, antioxidant indices, and growth performances. Sulfur amino acids are known to play a crucial role in protein structure, metabolism, immunity, and oxidation [ 150 ]. Recently, in ovo inoculation of sulfur-containing amino acids in heat-stressed embryo induced serum antioxidant indices and antioxidant related genes expression, reduced HSP70 gene expression, corticosterone concentrations, and lipid profile in hatched broiler chicks [ 151 ]. Dietary supplementation of N-acetylcysteine improved the growth performance and intestinal function of broilers exposed to heat stress [ 152 ]. N-acetylcysteine also mitigated heat stress in breeder Japanese quail under heat-stressed conditions [ 153 ]. Thus, further studies are required to delineate the dietary supplementation of Sulfur amino acids in heat-stressed broiler chickens and laying hens.

4. Conclusions

With the rising global temperature, heat stress has been a severe challenge to the growth of the poultry industry. Several strategies have been tried and tested to counteract heat stress in poultry. However, only a few of them are widely used in the poultry industry. Heat stress in poultry results from the interplay of several factors, such as high environmental temperature, humidity, radiant heat, and airspeed, and causes several physiological, neuroendocrine, and behavioral changes. So, no single approach alone is enough to negate the impacts of heat-stress on poultry. Therefore, there is a need for a holistic approach to attenuate the negative effect of heat stress in poultry. The potential use of Na and F genes, along with proper nutrition, housing, and management should be beneficial in mitigating heat stress. Further research testing a combination of some approaches for ameliorating heat-stress mentioned in this article, to observe their efficiency and cost-benefit in the poultry industry is warranted.

Author Contributions

S.W. reviewed the literature and drafted the manuscript. N.S. and B.M. reviewed the manuscript and provided critical review and suggestions and comments. All authors have read and agreed to the published version of the manuscript.

This work was supported by a Start-up grant from CTAHR University of Hawaii at Manoa, and USDA Hatch Multistate (2052R) to B.M.

Conflicts of Interest

The authors declare that there is no conflict of interest.