case study of uti in pregnancy

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http://orcid.org/0000-0003-3121-0441 Dominique Esmée Werter 1 ,
Brenda M Kazemier 1 ,
Elisabeth van Leeuwen 2 ,
Maurits C F J de Rotte 3 ,
Sacha D Kuil 4 ,
Eva Pajkrt 5 ,
Caroline Schneeberger 6 , 7
1 Department of Obstetrics and Gynaecology , University of Amsterdam , Amsterdam , The Netherlands
2 Department of Obstetrics and Gynaecology , Amsterdam University Medical Centres , Duivendrecht , The Netherlands
3 Department of Clinical Chemistry , University of Amsterdam , Amsterdam , The Netherlands
4 Department of Microbiology , University of Amsterdam , Amsterdam , The Netherlands
5 Obstetrics and Gynaecology , Amsterdam UMC Location AMC , Amsterdam , The Netherlands
6 Department of Microbiology , Amsterdam UMC-Locatie AMC , Amsterdam , The Netherlands
7 Center for Infectious Disease Control , National Institute for Public Health and the Environment (RIVM) , Bilthoven , Netherlands
Correspondence to Ms Dominique Esmée Werter; d.e.werter{at}amsterdamumc.nl

Introduction Symptoms of urinary tract infections in pregnant women are often less specific, in contrast to non-pregnant women where typical clinical symptoms of a urinary tract infection are sufficient to diagnose urinary tract infections. Moreover, symptoms of a urinary tract infection can mimic pregnancy-related symptoms, or symptoms of a threatened preterm birth, such as contractions. In order to diagnose or rule out a urinary tract infection, additional diagnostic testing is required.

The diagnostic accuracy of urine dipstick analysis and urine sediment in the diagnosis of urinary tract infections in pregnant women has not been ascertained nor validated.

Methods and analysis In this single-centre prospective cohort study, pregnant women (≥16 years old) with a suspected urinary tract infection will be included. The women will be asked to complete a short questionnaire regarding complaints, risk factors for urinary tract infections and baseline characteristics. Their urine will be tested with a urine dipstick, urine sediment and urine culture. The different sensitivities and specificities per test will be assessed. Our aim is to evaluate and compare the diagnostic accuracy of urine dipstick analysis and urine sediment in comparison with urine culture (reference test) in pregnant women. In addition, we will compare these tests to a predefined ‘true urinary tract infection’, to distinguish between a urinary tract infection and asymptomatic bacteriuria.

Ethics and dissemination Approval was requested from the Medical Ethics Review Committee of the Academic Medical Centre; an official approval of this study by the committee was not required. The outcomes of this study will be published in a peer-reviewed journal.

Urinary tract infections
BACTERIOLOGY
Protocols & guidelines
Microbiology
Maternal medicine

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/ .

https://doi.org/10.1136/bmjopen-2022-063813

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STRENGTHS AND LIMITATIONS OF THIS STUDY

The urine of every participating woman will be tested with a set of tests including a urine dipstick, urine sediment and a urine culture.

We will investigate the course of complaints in pregnant women with a possible urinary tract infection to gain more insight in the diagnostic value.

The research will be done prospectively; therefore, we expect less bias than in a retrospective cohort.

It will be a single-centre cohort study, so it could possibly make the participants more homogeneous.

Introduction

The prevalence of urinary tract infections (UTIs) during pregnancy reported in literature varies between 2.3% and 15%. 1–5 It is hypothesised that anatomical changes during pregnancy such as dilatation of the ureters, decreased ureteral tone and increased bladder volume contribute to urinary stasis and ureterovesical reflux increasing the risk of a UTI. 6–8 Besides the anatomical changes, pregnancy-related glomerular filtration rate increases the alkalinity of the urine and the urinary glucose concentration, which facilitates bacterial growth. 9 The association between UTIs during pregnancy and maternal complications such as hypertensive disorders and caesarean delivery has been reported, although there is contradictory evidence. 4 6 10 Moreover, UTIs during pregnancy have also been associated with neonatal complications such as preterm birth, low birth weight and perinatal death. 2 4 10 In addition, an untreated UTI may lead to pyelonephritis, which further increases the risk of preterm birth. 11 Preterm birth has major consequences at the individual level as well as for society (costs).

In contrast, overtreating pregnant women with antibiotics may also cause harm. Overuse and incorrect use of antibiotics are the main causes of antimicrobial resistance. Moreover, the unnecessary exposure of the unborn child to antibiotics may also not be without risks. Associations between antibiotics during pregnancy and adverse neonatal outcomes including increased risk of cerebral palsy, early-onset sepsis with antibiotic-resistant microorganisms, malformations and epilepsy have been published. 10 12 13 Also, maternal exposure to certain antibiotics is associated with childhood asthma and childhood obesity. 14 15 It is recently found that prenatal exposure to antibiotics can probably lead to alterations in the differential methylation at regulatory regions of imprinted genes. 16 If we can improve diagnostics and related antibiotic prescribing, we possibly can also influence fetal development and possibly long-term health with the results of this study. All of them impact future healthcare costs. Next to that, if we could decrease the number of tests for an accurate diagnosis, costs could be saved.

In the non-pregnant population, a diagnostic test to confirm the diagnosis of UTI is not always considered necessary, since typical clinical symptoms such as dysuria and urgency are regarded distinctive enough. 7 17–20 In pregnancy, the diagnosis of a UTI is less well studied and more challenging. First of all, many women during pregnancy experience symptoms that mimic a UTI such as frequency as a result of pressure of the baby’s head on the bladder. 8 21 On the other hand, symptoms of a UTI can be aspecific in pregnancy; UTIs in pregnant women may solely present with abdominal pain or Braxton Hicks contractions. 9 21 All this makes it more difficult to distinguish between asymptomatic bacteriuria (ASB) and UTI. Furthermore, in pregnancy, ASB can also be present: bacteriuria without any UTI signs or symptoms. ASB is not an active infection and the risk of adverse outcomes like preterm birth is low or absent compared with UTIs. 11 22

Most hospital protocols recommend testing pregnant women for a UTI when they present with symptoms suggestive of UTI or in case of symptoms suspicious of threatened preterm birth. In the diagnostic work-up, various methods are used: urine dipstick test, urine sediments and bacterial cultures, which are used in various ways and come with several limitations.

First, a urine dipstick is a strip with different reagents present. The reagents react on the presence of certain substances, for example, protein, glucose, nitrite and leucocyte esterase. The most important parameters to diagnose UTI on a dipstick are nitrite and leucocyte esterase. Many gram-negative bacteria produce the enzyme nitrate reductase, which converts urinary nitrate into nitrite indicating the presence of bacteria. 23 In the adult population, the sensitivity of nitrite dipstick reported in a systematic review is 0.54 (CI 0.44 to 0.64), the specificity is 0.98 (CI 0.96 to 0.99), positive likelihood ratio of 29.3 (CI 14.4 to 59.7) and a negative likelihood ratio of 0.48 (CI 0.37 to 0.62). Eight out of 14 of the studies included in this review reported on pregnant women, but none of them reported on symptomatic women. 24 Another study shows that the sensitivity and specificity of nitrite to test for ASB in pregnant women are, respectively, 0.55 (95% CI 0.42 to 0.67) and 0.99 (95% CI 0.98 to 0.99). 25

Leucocyte esterase is an enzyme released by neutrophils and macrophages. The leucocyte dipstick has a sensitivity of 0.72 (0.61 to 0.84) and a specificity of 0.82 (0.74 to 0.90), and a positive likelihood ratio of 4.87 (3.26 to 7.29) and a negative likelihood ratio of 0.31 (0.18 to 0.51) in the adult population. 24

Physiological pyuria can appear in pregnant women. 26

Second, for urine sediments, urine samples are centrifuged to obtain a sediment including red and white blood cells, squamous cells and bacteria, which are counted automatically by microscopy. 16 For a UTI, both the presence or absence of leucocytes and bacteria are of interest. A systematic review in the general population reported a sensitivity range of 57.1%–97%, a specificity of 27.0%–97.0%, a positive likelihood ratio of 1.59–24.57 and a negative likelihood ratio of 0.07–0.655 in studies where they used the sediment. 27 Yet again, physiological pyuria can appear in pregnant women. 26 The advantage of the urine sediment over the urine dipstick is that the urine sediment counts all bacteria. The urine dipstick only indicates if there are nitrite-forming bacteria present. However, not all bacteria are uropathogenic.

Finally, the reference test to detect a UTI is a urine culture, which determines bacterial growth. However, the urine dipstick takes a few minutes, the urine sediment about an hour and the urine culture at least 24 hours up to 5 days.

The exact number of bacteria present in urine to define a ‘positive’ urine culture and a UTI is not clear cut. The most common definition is ≥10 5 colony-forming units (CFU)/mL of uropathogens. 28 However, the cut-offs used in practice range from ≥10 3 CFU/mL to ≥10 5 CFU/mL. 18 29 30

The Dutch guideline of obstetrics and gynaecology recommends performing both a nitrite dipstick and a urine culture when pregnant women present with UTI symptoms. In case of a positive nitrite dipstick, treatment should start immediately. In case of a negative nitrite dipstick, treatment should only be started if the culture is positive. The role of the other diagnostic methods is unclear. 9 The Dutch general practitioners’ guideline recommends performing a nitrite dipstick. In case of a positive nitrite dipstick, people will be treated for UTI. Leucocyte esterase test will be performed when the nitrite result is negative. Urine sediments are recommended if leucocyte esterase is present since a positive result of leucocyte esterase is considered as insufficient proof of a UTI. When either the nitrite or the sediment is positive, treatment should be started. When the leucocyte esterase dipstick is negative but there is still a suspicion for a UTI, a sediment is performed additionally. When both urine dipstick and sediment are negative, a UTI is ruled out. If either urine dipstick or sediment results are positive, a urine culture is performed while antibiotics are directly initiated, awaiting the urine culture results. 31

Both in the UK and the USA, guidelines do not state the diagnostic work-up for UTIs in pregnancy (Royal College Obstetricians and Gynaecologist (RCOG) guideline, National Institue for Health and Care Excellence (NICE)guideline and American College of Obstetricians and Gynecologist (ACOG) guideline).

Despite the differences in guidelines, in daily practice, the urine is often only tested with a dipstick. In case of a negative test result, often no additional tests are done. The approach when to perform a sediment or a urine culture is equally ambiguous. There is no clear evidence that the diagnostic accuracy of a standalone dipstick urine (including both the presence of nitrite and leucocyte esterase) is equal to a combined approach of urine dipstick and sediment to diagnose a UTI in pregnancy. Furthermore, pyuria can be present in pregnant women without a UTI. 26 Moreover, the additional value of a urine culture in all women, as recommended by the Dutch guideline of obstetrics and gynaecology, is also unknown. For something as common as a UTI during pregnancy, it is undesirable that the available evidence is too limited to properly inform (diagnostic) guidelines, which results in great diagnostic variation, and potential harmful overtreatment and undertreatment.

Methods and analysis

This study aims to evaluate the diagnostic accuracy of urine dipstick analysis and urine sediment to bacterial cultures in the diagnosis of UTI in pregnant women.

Study design

This study is a single-centre prospective cohort study.

Participants

All consecutive pregnant women attending the outpatient clinic, the pregnancy ward or emergency department for women’s health in the Amsterdam UMC with symptoms warranting a diagnostic work-up to rule out a UTI can be included, after oral and written consent. These symptoms include dysuria, urgency, frequency, fluid loss, difficulties with voiding, painful voiding, haematuria, or aspecific abdominal pain, (Braxton Hicks) contractions and vaginal blood loss. 7 9

Exclusion criteria are a previous UTI episode in the past 2 weeks, antibiotic use in the past 2 weeks or a structural abnormality of the urogenital tract.

Inclusion of women in the study takes place since 1 November 2021. We plan to include all women in the study in 3 years.

Test methods

The urine samples will be clean-catch midstream urine samples. The index test will be a urine dipstick and a urine sediment. The dipstick that we will use is Clinitek novus 10 (Siemens). The urine sediment will be checked with Atellica 1500 Siemens. For both the urine dipstick and the urine sediment, different cut-offs will be used to investigate which cut-off has the best diagnostic value ( table 1 ).

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Expected outcomes

The reference test will be a urine culture.

No blinding will take place for the different tests. The outcome of the test has no influence on the treatment and is necessary for daily practice.

Because of the difficulties to distinguish between ASB and UTI, we will use a different definition for UTI than commonly used. We would like to make sure that we are dealing with a UTI and not ASB.

In this study, a ‘true UTI’ is present when the following three criteria are met:

Presence of at least two specific or non-specific symptoms of a UTI. 26

A positive urine culture.

Symptom improvement during adequate antibiotic treatment, where adequate treatment is defined by proven susceptibility of isolated uropathogens to the administered antibiotic.

The definition of a positive culture is:

Urine with ≥10 3 CFU/mL of a uropathogen.

Maximum of two uropathogens ≥10 3 CFU/mL present. When there are more than two uropathogens present of ≥10 3 CFU/mL, the culture will be considered as contaminated.

Next to that, the woman will be asked to fill out a questionnaire. The questionnaire contains questions about risk factors for UTI and possible clinical symptoms of a UTI. After 5–8 days, when the result of the culture will be available, the woman will be called to evaluate the presenting symptoms. This check-up is part of standard care. Both the woman and the clinician have access to the test result; it is not blinded. Women will be asked permission to collect data from the midwife, gynaecologist or general practitioner about their pregnancy and delivery.

The statistical analysis will be performed using IBM SPSS Statistics V.26.

Primary outcome

We will determine which combination of leucocyte esterase, nitrite presence in the dipstick and bacteria presence and leucocyte count in the sediment yield the best performance of both methods separately and combined to predict a ‘true UTI’ according to our definition. Different cut-offs and combinations of cut-offs of the urine analysis components will be explored to calculate sensitivity, specificity, positive and negative predictive value, and positive and negative likelihood ratios ( table 1 ). In addition, we aim to develop a diagnostic model based on all available evidence on leucocyte esterase, nitrite presence, bacteria presence, leucocyte count and symptoms.

After the best performing cut-offs for both urine dipstick and urine sediment have been determined, we will compare the performance of these two tests together in terms of sensitivity, specificity, positive and negative predictive value, and positive and negative likelihood ratios. Urine culture will be used as the reference test. The performance will be compared with the predefined ‘true’ UTI. To do this, we first select all true positives and true negatives using the reference test. In addition, we compare the classifications of urine dipstick with urine sediment in a 2×2 table for true positives (sensitivity) and a 2×2 table for true negatives (specificity) and calculate a p value for the difference in classification using a paired McNemar test.

Planned sensitivity analyses will also be performed for different cut-off values for pathogens in urine cultures ≥10 3 CFU/mL, ≥ 10 4 CFU/mL and ≥10 5 CFU/mL.

Contaminated urine cultures will be considered as negative cultures.

Secondary outcome

We will evaluate which clinical symptoms are best at predicting a UTI in pregnancy and which symptoms are not. The symptoms of a UTI will be studied with incidences and p values to identify which symptoms are associated with UTI.

To identify risk factors for UTI, univariate logistic regression will be used. In case it is possible, multivariate logistic regression will be used to identify the risk factors. We will use a forward stepwise selection for our regression model.

Pregnancy duration will be measured in weeks and days of gestational age and will be compared between women with and without UTI with a Student’s t-test.

The timing of the performed urine test (urine dipstick, urine sediment and urine culture) and the gestational age of delivery will be noted. Time between diagnosis of UTI and delivery will be compared using Kaplan-Meier survival curve.

Power analysis

To provide an estimated sample size, we calculated the sample sizes necessary for 80% power in a McNemar paired test comparing urine dipstick with urine sediment in women with true-positive UTI (sensitivity) and true-negative UTI (specificity). The expected discrepant cells for sensitivity are 14% and 5%, with a calculated 181 true-positive cases necessary for 80% power. The expected discrepant cells for specificity are 10% and 4% with a calculated 302 true-negative cases necessary for 80% power. We expect that around 30% of the included women will have a UTI such that the necessary sample size to include is 603 for sensitivity and 432 for specificity.

With a 10% expected drop-out, the sample size would be 660 pregnant women.

Data will be collected using Castor, which is an application system that enables collection and clean-up of trial data using the internet. Data handling will be done coded. The data will be saved for 15 years.

Patient and public involvement

There was no patient or public involvement in this research.

Ethics and dissemination

Approval was requested from the Medical Ethics Review Committee of the Academic Medical Centre; an official approval of this study by the committee was not required (METC review number W21_291 #21.318). All participants will give written and oral informed consent prior to entry to the study and will be made aware that participation is strictly voluntary.

The outcomes of this study will be published in a peer-reviewed journal.

The diagnostic accuracy of a urine dipstick and, less often, a urine sediment for the diagnosis of bacteriuria in pregnancy has been evaluated. 23 32 However, no studies are available in pregnant women on the diagnostic accuracy of symptomatic UTIs. As a result, different guidelines in the Netherlands advise different ways of testing for UTIs in pregnant women. International guidelines lack any recommendations on specific urine tests. However, in pregnant women with a UTI, both undertreatment and overtreatment are potentially harmful; therefore, correct diagnosis is very important.

The focus of this study is the diagnostic work-up. We will not intervene in the treatment given or follow-up provided to the participating women. It is likely that certain types of bias will be introduced as a result of implementation of this study. Bias could be introduced because more diagnostics will be performed and all three urine test results will be reported to the treating clinician (not blinded). Since more result will be available, this could affect the prescription of antibiotics.

We do not expect a lot of women with partial verification bias since the three different urine tests will be most of the time executed at the same time from the same urine sample. Because of this, we avoid that only the urine dipstick and/or sediment is performed and the urine culture is not executed.

The urine culture has been used, both in daily practice and in research, for a long time. There are no logical alternative reference standards. The urine culture has been proven to be effective. We do not expect an inappropriate reference standard.

Since the result of the urine culture is only available a few days after the results of the urine dipstick and sediment, we do not expect a review bias.

Clinical impact

Due to the different cut-offs to report uropathogens and their susceptibilities (10 3 instead of 10 4 ), the rate of prescribing antibiotics may increase too. However, the result of the culture will only come in after a few days, so the decision to start antibiotics has most likely already been made. With this study, we hope to provide either better evidence for the current advice in guidelines and/or guide necessary adjustments.

To avoid unnecessary treatments, diagnostic tests and costs, and to minimise possible harmful neonatal outcomes, the diagnostic process of UTIs should be optimised. This new workflow should be implemented in the daily care to create a more evidence-based treatment strategy. Since the diagnostic work-up for UTIs takes place on a daily basis, the results of this research will have a major impact on daily routine care. To find an optimal strategy for diagnosing a UTI is only the start of tackling the challenges around the diagnosis of UTIs in pregnancy.

Ethics statements

Patient consent for publication.

Not required.

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Contributors DEW wrote the proposal and the manuscript. BMK initiated the research, and critically revised the proposal and manuscript. EvL critically revised the proposal and manuscript. MCFJdR critically revised the manuscript. SDK critically revised the proposal and manuscript. EP critically revised the proposal and manuscript. CS critically revised the proposal and manuscript. All authors read and approved the final manuscript.

Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

Competing interests None declared.

Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

Provenance and peer review Not commissioned; externally peer reviewed.

Read the full text or download the PDF:

Pathogen-specific alterations in intestinal microbiota precede urinary tract infections in preterm infants: a longitudinal case-control study

Affiliations.

1 Department of Neonatology, Children's Hospital of Fudan University, Shanghai, China.
2 NHC Key Laboratory of Neonatal Diseases, Children's Hospital of Fudan University, Shanghai, China.
3 National Children's Medical Center, Department of Clinical Epidemiology of Children's Hospital of Fudan University, Shanghai, China.
4 State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, China.
PMID: 38561312
PMCID: PMC10986765
DOI: 10.1080/19490976.2024.2333413

Urinary tract infections (UTIs) are among the most common late-onset infections in preterm infants, characterized by nonspecific symptoms and a pathogenic spectrum that diverges from that of term infants and older children, which present unique diagnostic and therapeutic challenges. Existing data on the role of gut microbiota in UTI pathogenesis in this demographic are limited. This study aims to investigate alterations in gut microbiota and fecal calprotectin levels and their association with the development of UTIs in hospitalized preterm infants. A longitudinal case-control study was conducted involving preterm infants admitted between January 2018 and October 2020. Fecal samples were collected weekly and analyzed for microbial profiles and calprotectin levels. Propensity score matching, accounting for key perinatal factors including age and antibiotic use, was utilized to match samples from UTI-diagnosed infants to those from non-UTI counterparts. Among the 151 preterm infants studied, 53 were diagnosed with a UTI, predominantly caused by Enterobacteriaceae (79.3%) and Enterococcaceae (19.0%). Infants with UTIs showed a significantly higher abundance of these families compared to non-UTI infants, for both Gram-negative and positive pathogens, respectively. Notably, there was a significant pre-UTI increase in the abundance of pathogen-specific taxa in infants later diagnosed with UTIs, offering high predictive value for early detection. Shotgun metagenomic sequencing further confirmed the dominance of specific pathogenic species pre-UTI and revealed altered virulence factor profiles associated with Klebsiella aerogenes and Escherichia coli infections. Additionally, a decline in fecal calprotectin levels was observed preceding UTI onset, particularly in cases involving Enterobacteriaceae. The observed pathogen-specific alterations in the gut microbiota preceding UTI onset offer novel insight into the UTI pathogenesis and promising early biomarkers for UTIs in preterm infants, potentially enhancing the timely management of this common infection. However, further validation in larger cohorts is essential to confirm these findings.

Keywords: Preterm infants; calprotectin; microbiome; urinary tract infection; virulence factor.

Anti-Bacterial Agents / therapeutic use
Case-Control Studies
Enterobacteriaceae
Escherichia coli
Gastrointestinal Microbiome*
Infant, Newborn
Infant, Premature
Leukocyte L1 Antigen Complex
Urinary Tract Infections*
Anti-Bacterial Agents

Grants and funding

Can Pregnancy Accelerate Aging for Women? Study Says Yes

By Dennis Thompson HealthDay Reporter

TUESDAY, April 9, 2024 (HealthDay News) -- Pregnancy transforms women's bodies in many obvious ways, but new research suggests it may also accelerate aging.

Women who had been pregnant appeared to be biologically older than women who had never carried a child, the genetic analysis revealed.

Further, more pregnancies meant more aging.

“Our findings suggest that pregnancy speeds up biological aging, and that these effects are apparent in young, high-fertility women,” said lead researcher Calen Ryan , an associate research scientist with the Columbia University Aging Center in New York City.

U.S. Cities With the Most Homelessness

“Our results are also the first to follow the same women through time, linking changes in each woman’s pregnancy number to changes in her biological age,” Ryan added in a university news release.

For the study, researchers tracked the health of more than 1,700 young people in the Philippines.

Prior studies have found that very fertile women suffer in health and longevity as they age. However, it’s not known whether pregnancy affects health earlier in life, before age-related declines become apparent, researchers said.

To examine this, the investigators used advanced genetic techniques to determine the cellular aging of the participants in the study.

These “epigenetic clocks” let researchers study aging earlier in life and to track people’s biological age as compared to their chronological age.

The relationship between a woman’s number of pregnancies and her biological age persisted even after taking into account other contributors to accelerated aging, researchers said. These other factors included social and economic status, smoking and genetics.

Meanwhile, men showed no accelerated aging related to the number of pregnancies their partners had.

This indicates that something specific about pregnancy or breastfeeding accelerates biological aging, the researchers concluded.

The findings were published April 8 in the Proceedings of the National Academy of Sciences.

Why might pregnancy speed aging in a woman?

Pregnancy as a young adult can be particularly hard on the body of a woman who’s still developing, Ryan noted.

“Many of the reported pregnancies in our baseline measure occurred during late adolescence, when women are still growing,” Ryan explained. “We expect this kind of pregnancy to be particularly challenging for a growing mother, especially if her access to healthcare, resources or other forms of support is limited.”

Future research should investigate more closely why pregnancy might accelerate aging, and whether that will impact the health of women in old age, Ryan added.

Researchers “do not know the extent to which accelerated epigenetic aging in these particular individuals will manifest as poor health or mortality decades later in life,” Ryan noted.

More information

Northwestern Medicine has more on biological versus chronological age .

SOURCE: Columbia University, news release, April 8, 2024

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Open access
Published: 08 April 2024

Clinical analysis of complete uterine rupture during pregnancy

Jing Xie 1 , 2 ,
Xuefang Lu 3 &
Miao Liu 1 , 2

BMC Pregnancy and Childbirth volume 24 , Article number: 255 ( 2024 ) Cite this article

76 Accesses

Metrics details

Uterine rupture in pregnant women can lead to serious adverse outcomes. This study aimed to explore the clinical characteristics, treatment, and prognosis of patients with complete uterine rupture.

Data from 33 cases of surgically confirmed complete uterine rupture at Chenzhou No.1 People’s Hospital between January 2015 and December 2022 were analyzed retrospectively.

In total, 31,555 pregnant women delivered in our hospital during the study period. Of these, approximately 1‰ ( n = 33) had complete uterine rupture. The average gestational age at complete uterine rupture was 31 +4 weeks (13 +1 –40 +3 weeks), and the average bleeding volume was 1896.97 ml (200–6000 ml). Twenty-six patients (78.79%) had undergone more than two deliveries. Twenty-five women (75.76%) experienced uterine rupture after a cesarean section, two (6.06%) after fallopian tube surgery, one (3.03%) after laparoscopic cervical cerclage, and one (3.03%) after wedge resection of the uterine horn, and Fifteen women (45.45%) presented with uterine rupture at the original cesarean section incision scar. Thirteen patients (39.39%) were transferred to our hospital after their initial diagnosis. Seven patients (21.21%) had no obvious symptoms, and only four patients (12.12%) had typical persistent lower abdominal pain. There were 13 cases (39.39%, including eight cases ≥ 28 weeks old) of fetal death in utero and two cases (6.06%, both full term) of severe neonatal asphyxia. The rates of postpartum hemorrhage, blood transfusion, hysterectomy were 66.67%, 63.64%, and 21.21%. Maternal death occurred in one case (3.03%).

Conclusions

The site of the uterine rupture was random, and was often located at the weakest point of the uterus. There is no effective means for detecting or predicting the weakest point of the uterus. Rapid recognition is key to the treatment of uterine rupture.

Peer Review reports

Uterine rupture(UR) is a serious complication that directly jeopardizes the life of the mother and the fetus [ 1 ]. It refers to the rupture of the uterine body or the lower uterine segment in late pregnancy or during labor [ 2 ], requiring a cesarean section to terminate the pregnancy as soon as the diagnosis is confirmed. The most common risk factors of UR are a history of previous cesarean section (CS), myomectomy, multiparity, malpresentation, breech extraction, and instrumental deliveries [ 3 ].

The incidence of uterine rupture in China has recently been reported to range from 0.1% to 0.55% [ 4 ]; although this incidence rate is low, UR is highly likely to lead to serious adverse outcomes.

Currently, there are no effective means for detecting or predicting the weakest points of the uterus. Therefore, in this study, we aimed to provide reference information and practical experience for the early recognition, management and emergency treatment of uterine rupture.

The Department of Obstetrics and Gynaecology of the First people’s Hospital of Chenzhou is a critical care center wherein treatment, consultation, referral, and technical guidance are proviede to pregnant women in Southern Hunan and the city with acute and critical illnesses. This was a retrospective study aimed at exploring the clinical characteristics, treatment, and prognosis of patients with complete uterine rupture between January 2015 and December 2022. The data (complete clinical data, medical history, and surgical records) of all patients with complete uterine rupture admitted to our hospital were retrospectively analyzed.

Diagnostic criteria

Complete uterine rupture was defined as rupture of the entire wall of the uterine myometrium, with the uterine cavity communicating with the abdominal cavity during late pregnancy or labor [ 1 ].

Postpartum hemorrhage (PPH) was defined as bleeding of ≥ 500 ml for vaginal delivery and ≥ 1000 ml for cesarean delivery within 24 h after delivery of the fetus [ 1 ].

Research methods

Basic maternal information (age, pregnancies, number of deliveries), previous pregnancy and surgery-related indicators (risk factor, causes and clinical manifestations, comorbidities, distance between periconceptional caesarean section scar and vesicovaginal fold), situation at the time of uterine rupture (gestational age, interval between the current pregnancy and previous cesarean section delivery, rupture site and length, bleeding volume and number of required blood transfusions, minimum hemoglobin level), mode of the current delivery (induced delivery, transvaginal delivery, or cesarean section), and outcomes of the mother and child (postpartum hemorrhage, hysterectomy, maternal death, perinatal deaths, severe neonatal asphyxia (Apgar scores are recorded at 1, 5, and 10 min after birth, with a score below or equal to 3 indicating severe asphxia) were cllected from the patients’ medical records. This study meticulously adheres to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement guidelines.

General information

This was a retrospective study aimed at exploring the clinical characteristics, treatment, and prognosis of all patients with complete uterine rupture between January 2015 and December 2022. The data (complete clinical data, medical history, and surgical records) of all patients with uterine rupture admitted to our hospital were retrospectively analyzed. Thirty-three patients with surgically confirmed complete uterine rupture were included into the study.

Incidence of uterine rupture in our hospital

The total number of pregnant women who delivered in our hospital during the study was 31,555, with 33 cases of complete uterine rupture, accounting for approximately 0.1%(Table 1 ). The average gestational age at complete uterine rupture was 31 +4 weeks (13 +1 –40 +3 weeks), and the average bleeding volume was 1896.97 ml (200–6000 ml) (Table 2 ).

Causes of uterine rupture

The causes of uterine rupture are shown in Table 3 . Ten patients (30.3%) had a history of cesarean section and rupture at an incision site other than the original cesarean section. Patient 2 was involved in a car accident. Patient 11 underwent an elective cesarean section, and uterine rupture was found intraoperatively: the blood flow around the rupture was not rich, the bleeding was not much, and there were no obvious symptoms. Patient 14 had a history of laparoscopic right tubal surgery with poor symptomatology due to adhesion coverage. Patient 16 had a history of cesarean section and wedge resection of the right uterine horn (> 5 years prior), two artificial abortions (AA2), and one induction of labor in middle pregnancy (20 + weeks gestation, fetal anomaly, postpartum evacuation), with poor symptomatology due to adhesion coverage. Patient 27 has a cesarean section after transabdominal cerclage (intraoperative discovery of placental implantation), with uterine rupture in the cerclage line. Patient 33 had a history of two cesarean sections; this time, she was treated with ritodrine for fetal preservation and low molecular heparin in an outside hospital due to the presence of contractions, small vaginal bleeding, fast heart rhythm, and incomplete suppression of contractions, which were not taken seriously. She was transferred to our hospital for shock and stillbirth where she underwent an emergency cesarean section.

Six patients (18.18%) had a history of uterine operation. Patient 17 had a history of one AA and two vaginal births (VB). She was involved in coitus multiple times in the week prior to the delivery, and the night before delivery, resulting in premature rupture of the membranes; she did not notify the medical staff, and the labor did not come to term. The cervical canal did not open, HS-1 (the lowest point of the fetal skull is 1 cm below the sciatic ischiadica), and 10 min after using oxytocin, cervical dilatation was at 3 cm. Oxytocin was discontinued once abnormal fetal presentation was observed. A cesarean section was performed immediately fetal heart monitoring revealed a deceleration. Patient 20 underwent a breech vaginal trial of labor, with difficulty delivering the fetal head, vaginal rupture, and uterine rupture.

Clinical signs and symptoms of uterine rupture

The clinical signs and symptoms associated with complete uterine rupture are shown in Table 4 .

There were a few special cases. Patient 1 had an intellectual disability and was unable to express her discomfort accurately. Patient 25 had a metal ring at the breach site. Patient 10 had a cesarean scar pregnancy (CSP) with abdominal blood accumulation (mass) of approximately 3200 ml. Four (12.21%) placental implantation at the incision sites. Three patients presented with severe postpartum hemorrhage, and two of them underwent hysterectomies. The third patient had a repeat vaginal delivery after three VB, two cesarean sections (CS), and one vaginal birth after cesarean (VBAC), and was transferred to our hospital with hemorrhage after delivery; intraoperative rupture of the original cesarean section incision and placenta implantation at the rupture site were observed. Patient 21 had a post-VBAC.

Treatment of uterine rupture and maternal and fetal outcomes

The fetal outcomes and treatment of uterine rupture are shown in Table 5 . Postpartum hemorrhage did not occur in 11 patients (33.33%); six (18.18%) were found to have uterine rupture during full-term, elective surgery, with little blood flow around the rupture, and little bleeding with no obvious symptoms. Two patients (6.06%) had severe adhesions. One (Patient 21) was promptly delivered by cesarean section due to abnormal fetal heart rate monitoring; and two (Patients 28 and 29) had uterine tenderness after ethacridine administration and promptly underwent cesarean section.

Incidence of complete uterine rupture

Since the opening of the separate two-child policy in 2013, full liberalization of the two-child policy in 2016, and opening of the three-child policy in 2021, the cesarean section rate in China has increased from 34.9% (2014) to 41.1% (2016) [ 15 ]. Following this, the rate of scarred uterus has increased from 9.8% (2012) to 17.7% (2016) [ 16 ], which is far beyond the World Heallth Organizations ideal range.

The incidence of uterine rupture has been reported in several countries and regions; it is not consistent across countries and regions. This rate is related not only to the high-risk factors of the pregnant women themselves, but also to the economic level of each country, number of years of occurrence (which is related to the country's policy at that time), level of medical care, and transportation status (referral time). The reported incidence of uterine rupture: is 0.06% in Northern Europe [ 17 ], 0.67% in the University of Pakistan Teaching Hospital [ 18 ], 0.01% in the First Maternity and Infant Hospital of Shanghai [ 19 ], 0.2% in the Jiangxi Maternity and Child Healthcare Hospital [ 20 ], and 0.05% in the Women's Hospital of the Medical College of Zhejiang University [ 21 ]. Following the latest data [ 22 ], the total incidence of uterine rupture in China is 0.13%, consistent with 0.1% found in this study.

Analysis of the etiology and risk factors for complete uterine rupture

Due to the low cesarean section rate and the large number of patients with two or multiple deliveries between 1960 and 1990, uterine rupture was the predominantly primary. After 1990, with the implementation of family planning policies, the cesarean section rate increased, and subsequently, cesarean section scar rupture became the primary cause of uterine rupture [ 23 ]. Therefore, with the improvement in medical standards, doctors' awareness of uterine rupture, and repeated emergency drills, the main etiology has changed.

The known etiologies and risk factors for uterine rupture are as follows [ 1 , 23 ].

Previous uterine injury or history of abnormalities.

A history of myometrial surgery and short or long intervals between surgeries, which include cesarean section (incidence of uterine rupture was 0.071% [ 21 ], 0.095% for a history of one cesarean Sect [ 24 ]., and 1.92% for a history of two or more cesarean Sects [ 24 ].), history of repair of uterine rupture (33% [ 25 ]), myomectomy, wedge resection of the uterine horn (incidence of uterine rupture is up to 30% [ 26 ]), tubal surgery, hysteroscopic septum resection (incidence of uterine rupture is 1.0%–2.7% [ 27 , 28 ]), and separation of adhesions in the uterine cavity. Human Immunodeficiency Virus (HIV) infection may increase the incidence of cesarean delivery complications [ 29 ]. Current research suggests that the uterine wound healing takes 12 weeks [ 30 ], while myometrial incision healing and scar formation takes 6–12 months [ 31 ]; however, wound healing does not mean that it is able to withstand the pressure of pregnancy immediately. It also undergoes a process of tissue reconstruction, which further strengthens the elasticity of the uterine myometrial wall in the area of the scar. Therefore, less than 12–18 months is a high-risk factor for uterine rupture [ 32 ], and 2–3 years after cesarean section is the optimal period for uterine incision healing [ 33 ]. After > 5 years [ 6 ], the uterine scar’s degree of muscularization will gradually deteriorate and it will lose elasticity, making uterine rupture more likely during another pregnancy. The risk of uterine rupture for second pregnancies has been reported in the literature, even when tubal surgery does not involve the mesosalpinx or uterine horn, with a higher risk in the presence of electrocoagulation injuries, injury to or absence of part of the myometrial layer of the uterine horn, localized unsutures, and short intervals between pregnancies. The incidence of uterine rupture in our study was 0.79 per 1000 in those with a history of cesarean section, 0.057% in those with a history of one cesarean section, and 0.022% in those with a history of two or more cesarean sections. In our study, 11 patients (33.33%) had an interval of pregnancy out of 1.5 and 5 years, two (6.06%) had a history of tubal surgery, one (3.03%) had a history of wedge resection of the uterine horn, and one (3.03%) was a person living with HIV. It is important to note that in patients with a history of uterine rupture, the rupture was not at the same location. Uterine injuries include abortion, curettage, as well as sharp or blunt contusions such as car accidents, knives, and hidden uterine ruptures. In the present study, six (18.18%) patients had a history of intrauterine manipulation as a risk factor. Congenital abnormalities include uterine dysplasia, and connective tissue defects. In the present study, two patients (6.06%) had a double uterus. Furthermore, one patient (case 7) had a history of transabdominal cervical cerclage. During pregnancy, the cerclage line increases with the uterus, creating a chronic transverse cutting effect on the cervix, Uterine rupture occurs at the site of the cervical cut once there is significant uterine contraction.

Combined uterine injuries or abnormalities in this pregnancy

Postnatal etiologies include advanced age, muliple pregnancies and deliveries, spontaneous tonic uterine contractions, excessive contractions due to the use of oxytocin or prostaglandins and maternal sensitivity to drugs, prostaglandin or saline intra-amniotic infusion, sharp forceps contusion, external inversion, amniotic fluid overload, or multiple pregnancies. In this study, one patient (3.03%) was treated with uterotonics and three (9.09%) underwent induction of labor.

Intrapartum etiologies include any mechanism leading to obstruction of fetal descent, such as pelvic stenosis, cephalopelvic disproportion, obstruction of the soft birth canal, abnormal fetal position, and macrosomia; internal inversion; forceps delivery; emergency labor; breech traction; fetus destruction; excessive dilatation of the uterus in the lower part of the uterus caused by fetal anomalies; excessive pressure in the uterine cavity during delivery; implantation of the placenta or severe adhesion; and difficulty in manually stripping the placenta. One patient (case 20) in this study had uterine rupture due to breech traction during vaginal delivery and eight (24.24%) had placenta implantation.

Acquired etiologies include gestational trophoblastic disease, adenomyosis, posterior flexion uterine implantation, and uterine artery embolization surgery. One patient in this study had adenomyosis.

CSP involves a poorly healed uterine incision, wide scarring, and inflammation, leading to the development of microscopic fissures through which the fertilized ovum is deposited into the myometrium. Most cases have a poor prognosis [1]. Only one case of CSP was reported in this study.

Placental implantation: when it occurs at the site of the original cesarean section scar is caused by a structural defect in the endometrium [ 23 ] that allows the placenta to attach abnormally to the uterine myometrium. In our study, four patients (12.12%) had placental implantation, with three who had severe postpartum hemorrhage and two who underwent hysterectomies.

Trial of labor after cesarean (TOLAC), during a second pregnancy or request for a vaginal trial of labor; A meta-analysis showed that TOLAC results in a 0.27% higher risk of uterine rupture [ 9 ]. The management of TOLAC is a multifactorial. Factors [ 34 , 35 ] such as a previous vaginal delivery, use of epidural anesthesia, indication for previous cesarean section, pregnancy complications (such as preeclampsia, and placental anomalies), fetal weight above 4000 g, dose of oxytocin used, induction of labor with prostaglandins, women who delivered at > 41 +0 weeks of gestation, ethnicity, cervical length, head-perineum distance, maternal age (maybe), inter-delivery interval, body mass index (maybe), and prolonged second stage of labor (maybe) contribute to uterine rupture during TOLAC. However, there are no data or literature supporting whether to perform a TOLAC and assess the risk of uterine rupture in a second pregnancy after a history of two cesarean deliveries and after one VBAC.

Endometriosis causes tissue adhesions. Surgical separation of these adhesions results in localized myometrial destruction and thinning, affecting the healing, brittleness, and elasticity of the scar. Patient 6 had this clinical presentation. It has also been shown that the distance from the cesarean scar to the vesicovaginal fold (suggestive of the horizontal position of the uterine incision from the previous cesarean section) is significantly increased in patients with a gestational age > 22 weeks and antepartum uterine rupture, and may be predictive of uterine rupture [ 9 ].

Regardless of how the uterus is damaged, scarring occurs during the repair process, which constitutes non-normal muscle tissue (connective and scar tissue) [ 1 ]. This forms a weak site of the uterus during pregnancy. We obseerved that uterine rupture occurred at a random site, mainly at the weakest point of the uterus. There is no effective means for detecting or predicting the weakest point of the uterus. In addition, the uterus may have ruptured in more than one location (Patient 2 had three ruptures).

Clinical manifestations and early diagnosis of uterine rupture

In general, most uterine ruptures progress from uterine rupture precursors, with the main clinical manifestations being abdominal pain (especially during the intervals between contractions), uterine tenderness (reported in the literature to be approximately 36.0% [ 21 ]), fetal abnormalities, abnormal vaginal bleeding, pathological contractions, hematuria, disappearance of contractions, hemodynamic instability (tachycardia, hypotension, or shock), change of fetal position, signs of uterine rupture detected by ultrasound, and changes in abdominal contour [ 1 ]. Some symptoms are asymptomatic; however, typical symptoms are rare (less than 10% [ 36 ]). Currently, pregnancy relies on the co-monitoring of history, clinical presentation, signs, and ultrasonography or magnetic resonance imaging (MRI). It is very difficult to rely on pregnancy management to prevent uterine rupture, which may be due to the following: the timing of uterine rupture is random, the rupture may be unrelated to the original surgical site, most patients have multiple risk factors, and the weakest part of the uterus may change with gestational age and cannot be predicted in advance. The time window for uterine rupture is difficult to control. The time may be longer in patients with thick abdominal fat and varying pain tolerance. If referral is required (long travel time), the optimal time for resuscitation is easily delayed. Abdominal pain, fetal distress, and vaginal bleeding do not allow us to initially consider uncommon uterine ruptures. Clinicians have limitations in considering abdominal pain, which is prone to misdiagnosis as other acute abdominal conditions or labor precursors. Furthermore, multiple pregnancies, literacy levels, and family economic status may lead to irregularities during obstetrical tests. Uterine rupture most often occurs suddenly most ofter, with immediate surgery performed upon diagnosis, failure to achieve continuous fetal heart monitoring, or fetal death at the time of presentation. Other conditions that do not directly lead to uterine rupture but can interfere with early recognition, such as mental retardation, history of frequent coitus, history of abdominal trauma, unawareness of the condition by family members (inability to provide an accurate history when the patient is in shock), use of ritodrine (rapid heart rate) and vomiting during pregnancy, can mask the early signs of shock. Color ultrasonography and MRI can be affected by the level of the examiner, thickness of abdominal fat in the pregnant woman, measurement site, number of measurements, bladder filling, rupture site (posterior wall rupture is difficult to diagnose), fetal movement, dynamic monitoring or not, and clarity of the ultrasound machine. In addition, the presence of unknown previous surgery (inverted T-shaped incision, uterine monolayer suture, weak local myometrium, infection, poor healing of incision, cause of postpartum hemorrhage, and method used to stop bleeding), diverticulum of the uterine incision (occurs in approximately 60% of patients after a primary cesarean section and 100% after three cesarean Sects [ 37 ].), any perforation during uterine manipulation, artificial placental removal during previous delivery, and subsequent follow-ups can affect the diagnosis of uterine rupture. In particular, the healing of the original cesarean section scar is unknown; a study showed that the use of synthetic absorbable monofilament sutures for uterine closure was associated with increased residual myometrial thickness, with respect to synthetic absorbable multifilament sutures. A uterine segment thickness after cesarean section below 2.0 mm between 35 and 38 gestational weeks has been repetitively associated with a greater risk of uterine rupture or scar dehiscence [ 37 ]. Furthermore, when the breach is small and there are no blood vessels at the breach, there may be no obvious symptoms or imaging changes. Atypical symptoms, difficult diagnosis of intra-abdominal hemorrhage, and unsupportive ancillary tests plague surgical decision-making. There is limited data on some factors that may affect the healing of the uterine incision [ 23 ] (previous history of postpartum hemorrhage, gestational diabetes mellitus or diabeties as a comorbidity, embryo transplantation, hypertensive disorders of pregnancy, and hypoproteinemia), and factors that may provide local protection, such as the severity of the pelvic-abdominal adhesions (three patients in this study had little hematochezia or peritoneal hemorrhage). Therefore, the education of pregnant women and their families, as well as the rapid recognition of uterine rupture after it occurs, are key to early diagnosis.

Complications of complete uterine rupture

Uterine rupture can cause severe postpartum hemorrhage, shock, disseminated intravascular coagulation, impaired organ function (ischemia–reperfusion), bladder injury, massive blood transfusion, hysterectomy, maternal death, neonatal asphyxia, ischemic-hypoxic encephalopathy, perinatal death (fetal or neonatal death), and other serious adverse outcomes.

Good prenatal and pregnancy care (contraceptive promotion, previous surgical records, control of diet weight gain, etc.), graded management (all women need to be risk-graded, strict control of high-risk factors, and timely referral), and early hospitalization of patients with high-risk factors for uterine rupture are key to the early diagnosis and treatment of uterine rupture. For patients with reproductive requirements, strict control of surgical indications, strengthening of suturing skills, guidance on postoperative precautions, strict control of indications for uterotonics and close monitoring are important. Correct management of the labor process, mastery of the indications for obstetric surgically assisted delivery and operation norms, and strict inspection during surgery (e.g., abdominal cervical cerclage patients to check the integrity of the lower segment of the uterus in the posterior wall) are also required. Regardless of high-risk factors, vigilance for uterine rupture, early recognition, proactive management, and training of rapid response teams should be strengthened to achieve favorable maternal and fetal outcomes.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Abbreviations

Artificial Abortion

Caesarean Section

Caesarean Scar Pregnancy

Complete Placenta Previa

Caesarean Scar to Vesicovaginal Fold Distance

Chronic Hypertension

Chronic Hypertension with Superimposed Preeclampsia

Ectopic Pregnancy

Endometriosis

Gestational Diabetes Mellitus

Pregestational Diabetes Mellitus

Hypertensive Disorders of Pregnancy

Induce Childbirth

In Vitro Fertilization and Embryo Transfer

Low Molecular Weight Heparin

Marginal Placenta Previa

Placenta Accreta

Placenta Increta

Pernicious Placenta Previa

Postpartum Hemorrhage

Trial Of Labor After Cesarean

Uterine Myomectomy

Vaginal Birth

Vaginal Birth after Cesarean

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Jing Xie & Miao Liu

The First Affiliated Hospital of Xiangnan University, Chenzhou, 423000, China

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JX performed the data analysis; ML performed the formal analysis; XFL performed the validation; JX wrote the manuscript. All authors read and approved the final manuscript.

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JX, female, 1989.06, resident physician, Master's Degree, Department of Obstetrics, the First People’s Hospital of Chenzhou/ the First Affiliated Hospital of Xiangnan University, Chenzhou 423000, China. Main research interest: Obstetric hemorrhage related diseases. XFL, female, 1988.10, attending physician, Master's Degree, Department of Radiology, Renmin Hospital of Wuhan University, Wuhan 430060, China. Main research interest: Radiodiagnosis. ML, female, 1975.11, head physician, Master's Degree, Department of Obstetrics, the First People’s Hospital of Chenzhou/ the First Affiliated Hospital of Xiangnan University, Chenzhou 423000, China. Main research interest: Obstetric hemorrhage related diseases.

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Xie, J., Lu, X. & Liu, M. Clinical analysis of complete uterine rupture during pregnancy. BMC Pregnancy Childbirth 24 , 255 (2024). https://doi.org/10.1186/s12884-024-06394-2

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Network analysis of posttraumatic stress and posttraumatic growth symptoms among women in subsequent pregnancies following pregnancy loss

Qiaoqiao Shen 1 , 2 ,
Qi Fu 1 &
Chen Mao 1

BMC Psychiatry volume 24 , Article number: 266 ( 2024 ) Cite this article

Metrics details

Pregnant women who have undergone pregnancy loss often display both posttraumatic stress (PTS) and posttraumatic growth (PTG). However, the precise relationship and structure of symptomatic levels of PTS and PTG have not been well understood. This study aimed to assess the associations between PTS and PTG symptoms in women during subsequent pregnancies following a previous pregnancy loss.

A total of 406 pregnant women with a history of pregnancy loss were included in this study. The Impact of Events Scale-6 (IES-6) and the Posttraumatic Growth Inventory Short Form (PTGI-SF) were used to assess symptoms of PTS and PTG, respectively. The Graphical Gaussian Model was employed to estimate the network model. Central symptoms and bridge symptoms were identified based on “expected influence” and “bridge expected influence” indices, respectively. The stability and accuracy of the network were examined using the case-dropping procedure and nonparametric bootstrapped procedure.

The network analysis identified PTG3 (“Ability to do better things”) as the most central symptom, followed by PTS3 (“Avoidance of thoughts”) and PTG6 (“New path for life”) in the sample. Additionally, PTS3 (“Avoidance of thoughts”) and PTG9 (“Perception of greater personal strength”) were bridge symptoms linking PTS and PTG clusters. The network structure was robust in stability and accuracy tests.

Conclusions

Interventions targeting the central symptoms identified, along with key bridge symptoms, have the potential to alleviate the severity of PTS experienced by women with a history of pregnancy loss and promote their personal growth.

Peer Review reports

Pregnancy loss, also known as the unintentional demise of the fetus before reaching viability or the termination of pregnancy due to medical reasons [ 1 ], is a traumatic event that profoundly impacts a significant number of women worldwide [ 2 ]. For many women, especially those aspiring to conceive, it is likely that they will become pregnant again within 1–2 years following a pregnancy loss [ 3 ]. Throughout subsequent pregnancies, women may grapple with conflicting emotions and psychological phenomena [ 4 , 5 , 6 ]. On one hand, the previous pregnancy loss casts a shadow over them, resurfacing with the new pregnancy [ 4 , 5 ]. They may find themselves revisiting past pregnancy experiences repeatedly, questioning their efforts, and experiencing feelings of guilt or remorse for the lost child [ 4 , 5 ]. On the other hand, through the process of self-adjustment, women may gradually come to accept and confront the reality of pregnancy loss [ 6 ]. The new pregnancy can provide an opportunity for them to regain confidence in fertility and contribute to reshaping a positive mindset and emotional connection [ 7 ].

Previous research has indicated that women who experience pregnancy loss may manifest both posttraumatic stress (PTS) and posttraumatic growth (PTG) symptoms [ 8 , 9 ]. However, there is a lack of quantitative studies focusing on the concurrent presence of PTS and PTG in this specific demographic, particularly during subsequent pregnancies. Research conducted among other populations indicates that the correlation direction between PTS total scores and PTG total scores does not always remain consistent, showing positive correlations, negative correlations, and curvilinear relationships [ 10 ]. In recent times, scholars have proposed that examining the relationship between PTS and PTG solely from a holistic perspective may overlook their interaction at symptom levels [ 11 , 12 ]. As a result, some studies have attempted to utilize network analysis techniques to explore central symptoms and bridge symptoms in PTS and PTG networks, enhancing the understanding of the underlying psychopathological mechanisms associated with PTS and PTG [ 13 , 14 , 15 , 16 , 17 ].

Given the considerable heterogeneity in responses to various types of trauma among different populations [ 18 ], it is challenging to apply existing co-occurrence networks of PTS and PTG to pregnant women who have experienced pregnancy loss. Therefore, this study aimed to utilize network analysis to explore the interaction between PTS and PTG symptoms during early pregnancy in women who have undergone pregnancy loss, with the objective of establishing a theoretical foundation for future interventions by identifying crucial nodes with cascading effects within the network.

Participants

This was a multicenter, cross-sectional study conducted in Guangdong Province, China, from October 8, 2022, to July 20, 2023. Clinical staff recruited participants on-site, and upon obtaining informed consent from eligible individuals, they promptly distributed electronic versions of the survey questionnaire. The inclusion criteria for participants were as follows: (1) aged 18 years or older, (2) in the first trimester of pregnancy, (3) having a single intrauterine pregnancy, (4) having experienced miscarriage, stillbirth, or termination for medical reasons, and (5) expressing willingness to participate in this study. Individuals diagnosed with severe pregnancy complications, a history of psychological disorders, or those currently receiving psychological therapy were excluded. Ultimately, 379 pregnant women from three tertiary hospitals and 94 from a community hospital were invited to participate. A total of 406 individuals successfully completed the survey questionnaire, resulting in an effective response rate of 85.8%.

Measurement

Sociodemographic characteristics.

Participants self-reported their information, providing details on age, educational background, monthly household income, marital status, number of children, current conception method (natural conception or assisted reproductive technology), pregnancy complications, as well as the number and types of prior pregnancy losses.

PTS symptoms

The Impact of Events Scale-6 (IES-6) [ 19 ] was utilized to assess PTS symptoms related to a previous pregnancy loss. The IES-6 comprises three subscales: intrusion, avoidance, and hyperarousal, each consisting of two items. Each item is rated on a scale from 0 (not at all) to 4 (extremely), resulting in a total score ranging from 0 to 24. A total score of 10 or higher indicates the presence of posttraumatic stress disorder (PTSD) [ 19 ]. The IES-6 has been widely used among Chinese populations [ 20 ], and it demonstrated good reliability and validity in this study.

PTG symptoms

The Posttraumatic Growth Inventory Short Form (PTGI-SF) [ 21 ] was utilized to assess the manifestations of personal growth in women who had experienced pregnancy loss. The PTGI-SF comprises five dimensions: interpersonal relationships, personal strength, new possibilities, spiritual change, and appreciation of life, totaling 10 items. Each item is rated on a scale from 0 (no change) to 5 (complete change). The overall score ranges from 0 to 50, with higher scores indicating a greater level of PTG. The PTGI-SF is the most commonly used tool for measuring PTG [ 15 ], and it demonstrated acceptable reliability and validity in this study.

Statistical analysis

All analyses were conducted using R software (Version 4.2.3). Continuous variables were described as mean (standard deviation, SD), and categorical variables were presented as frequencies and percentages.

We computed polychoric correlations between all nodes to examine the edges of the network and estimated the Graphical Gaussian Model (GGM) using the graphical least absolute shrinkage and selection operator (LASSO) in combination with the Extended Bayesian Information Criterion (EBIC) model [ 22 ]. In the network model, each symptom is represented as a “node,” and the association between symptoms is defined as an “edge.” As the association between PTS and PTG symptoms can be either positive or negative, we utilized the expected influence (EI) to quantify the impact of each node in the network. Nodes with high EI values can activate other nodes within the network, making them essential components of their own network [ 11 ]. To identify bridge nodes that connect PTS and PTG, we calculated the bridge expected influence (BEI). A higher positive value of the BEI for a node indicates a greater activation capacity towards nodes in another cluster, whereas a higher negative value signifies a stronger deactivation capacity towards nodes in another cluster [ 11 , 23 ].

Additionally, we conducted verification of network accuracy and stability [ 22 ]. First, centrality stability was evaluated through a case-drop bootstrap procedure, whereby centrality indices were repeatedly computed from subsets of data with an increasing proportion of cases removed. A correlation stability (CS) coefficient value above 0.5 indicates a high level of stability for centrality indices of nodes within the network. Second, edge weight accuracy was estimated with bootstrapped 95% confidence intervals (CIs) by resampling the data 1,000 times. Finally, bootstrapped difference tests (α = 0.05) were conducted to determine if there were significant differences among edge weights and node EIs.

Characteristics of the participants

The study involved participants with an average age of 30.93 years (SD = 4.76). Out of the 406 participants, 296 (72.9%) reported experiencing a single pregnancy loss, while 110 (27.1%) reported having undergone recurrent pregnancy losses (two or more losses). Concerning the current pregnancy, the majority (89.4%) occurred through natural conception, while 43 participants utilized assisted reproductive technology. Further demographic details of the participants can be found in Table 1 . The average score for IES-6 was 6.64 (SD = 3.65), and 14.3% of participants scored above the cutoff point of 10, suggesting the presence of post-traumatic stress disorder (PTSD). The mean score for PTGI-SF was 32.29 (SD = 8.90). The mean and standard deviation for both IES-6 and PTGI-SF items can be found in Supplementary Table S1 .

Network structure

Figure 1 illustrates the network structure of the co-occurrence of PTS and PTG. The network exhibited a high density (0.72) with an average weight of 0.06. The PTS and PTG symptoms formed distinct clusters, with a few modest connections between them. Among the 86 non-zero edges connecting 16 nodes, 58 were positive edges, and 28 were negative edges. The strongest positive edge was found between PTS3 (“Avoidance of thoughts”) and PTS4 (“Avoidance of feelings”) (Edge weight value: 0.56), while the strongest negative edge was observed between PTG9 (“Perception of greater personal strength”) and PTS2 (“Intrusive rumination”) (Edge weight value: -0.25). The correlation matrix for PTS and PTG items is presented in Supplementary Table S2 .

The network structure of PTS and PTG symptoms

Nodes: Blue edges represent positive associations, and red edges indicate negative associations. Thicker edges reflect stronger associations

In terms of EI centrality, the node PTG3 (“Ability to do better things”) had the highest EI value (2.06), followed by PTS3 (“Avoidance of thoughts”) (EI value: 1.17), and PTG6 (“New path for life”) (EI value: 0.92) in the network. These findings align with the results observed in the individual network models for PTS and PTG, as depicted in Supplementary Figure S1 . Regarding BEI centrality, PTS3 (“Avoidance of thoughts”) within the PTS cluster exhibited the highest positive BEI (BEI value: 1.68), while PTG9 (“Perception of greater personal strength”) in the PTG cluster showed the highest negative BEI (BEI value: -2.21). The EI and BEI values for each node are illustrated in Fig. 2 .

Expected influence and bridge expected influence of PTS and PTG symptoms

Network stability and accuracy

Figure 3 shows the results of the case-dropping bootstrap test. In terms of network stability, the CS coefficient of centrality EI was 0.67 (95% CI: 0.59–0.75), suggesting that 67% of the nodes in the sample could be randomly dropped without significantly changing the network structure. The bootstrapped 95% CIs for most edge weights were relatively narrow, indicating an accurate network structure (see Supplementary Figure S2 ). Additionally, nonparametric bootstrapped difference tests revealed significant differences among most edge weights and node EIs (see Supplementary Figure S3 and S4 ).

Stability of expected influence indices using case-dropping bootstrap

To the best of our knowledge, this study represents the first attempt to apply network analysis to examine the co-occurring patterns of PTS and PTG in pregnant women who have experienced pregnancy loss. In the network model, the PTS symptoms and PTG symptoms displayed visually distinct clusters, along with shared positive and negative connections, consistent with findings from previous network analysis studies [ 16 , 17 ].

Our findings revealed the central role of avoidance symptoms within the network, as evidenced by their strong edge weights and high centrality. Consistent with our research, women with a history of traumatic childbirth often employ avoidance as a psychological defense mechanism, attempting to sidestep directly confronting distressing memories and emotions associated with the experience [ 24 ]. Moreover, prior experiences of pregnancy loss may cause women to feel extremely anxious about their current pregnancy or childbirth, and avoiding thoughts related to pregnancy loss could serve as a means of protecting oneself from triggering these anxious emotions and seeking psychological shelter [ 25 ]. Regarding PTG symptoms, the most influential aspect is the transformation of new possibilities, aligning with the majority of findings in current research on PTG network analysis [ 13 , 14 , 26 ]. In studies related to pregnancy loss, participants also reported experiencing personal growth by adapting to their needs, cultivating new interests, and engaging in charitable volunteer work [ 27 ]. In the realm of network theory, alterations in central symptoms can significantly impact other symptoms within the model [ 11 ]. Therefore, guiding pregnant individuals who have experienced pregnancy loss to shift their focus towards new possibilities can assist them in better adapting to their circumstances and achieving personal growth.

The observed bridge symptoms play a crucial role in comprehending the shared psychopathological structure of PTS and PTG [ 23 ]. In this study, for the sample of pregnant women, avoidance of traumatic thoughts related to prior pregnancy loss was found to activate the PTG symptom cluster. Although prior research has predominantly suggested that avoidance coping hinders adaptation to loss and inhibits PTG, some findings have indicated that short-term avoidance does not necessarily imply a negative avoidance strategy but rather signifies a flexible “adaptive avoidance” [ 28 ]. Actively redirecting attention from past painful loss experiences to the current hopeful pregnancy, refraining from dwelling on the past, and adopting a future-oriented coping approach seem to promote positive cognition and psychological transformations in pregnant women [ 6 , 27 ]. Moreover, it is intriguing to note that within the PTG cluster, perceiving greater personal strength can suppress the PTS symptom network, particularly when it exhibits a strong negative correlation with intrusive rumination. Qualitative research has demonstrated that some women, following a pregnancy loss event, discover their resilience and realize that their inner strength aids them in actively countering negative emotions and reducing intrusive thoughts [ 27 ]. Consequently, it is essential to explore methods for enhancing self-efficacy (i.e., confidence in coping with difficulties) in pregnant women with a history of pregnancy loss to alleviate their PTS symptoms.

There are some limitations that should be acknowledged. First, due to the cross-sectional study design, we could not assess the causal relationship and dynamic changes related to the association between PTS symptoms and PTG symptoms. Second, although both the IES-6 and PTGI-SF scales have good psychometric properties in Chinese populations [ 19 , 21 ], the use of simplified scales for measuring PTS and PTG symptoms may limit the comprehensiveness of symptom assessment. Third, our investigation was conducted during the COVID-19 pandemic, a period in which the post-traumatic psychological well-being of pregnant women may be influenced by the stress of contracting the virus. Fourth, this study focused on pregnant women in the early stages of pregnancy, thereby restricting the generalizability of our findings to pregnant women in different phases of gestation. Finally, while the sample size in this study is sufficient for network analysis [ 22 ], it is not adequate to support network comparison tests among different subgroups. Future research should expand the sample size to more comprehensively explore the differences in the co-occurrence networks of PTS and PTG among various samples.

In summary, this study identifies the central symptoms in the co-occurrence network of PTS and PTG as “Avoidance of thoughts,” “Ability to do better things,” and “New path for life.” The bridge nodes connecting PTS and PTG are “Avoidance of thoughts” and “Perception of greater personal strength.” This provides a theoretical foundation for targeted interventions aimed at alleviating the severity of PTS among pregnant women with a history of pregnancy loss in the future and promoting their personal growth.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Abbreviations

Posttraumatic stress
Posttraumatic growth

Impact of Events Scale-6

Posttraumatic Growth Inventory-Short Form

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The authors are grateful to all participants and medical staff involved in this study.

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Q-QS and Q-F contributed to questionnaire design and data collection. Q-QS conducted the statistical analysis and drafted the manuscript. C-M reviewed the statistical results and revised the manuscript. All authors have read and approved the final manuscript.

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Shen, Q., Fu, Q. & Mao, C. Network analysis of posttraumatic stress and posttraumatic growth symptoms among women in subsequent pregnancies following pregnancy loss. BMC Psychiatry 24 , 266 (2024). https://doi.org/10.1186/s12888-024-05702-6

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ORIGINAL RESEARCH article

Outdoor artificial light at night exposure and gestational diabetes mellitus: a case–control study.

1 National Center for Respiratory Medicine, State Key Laboratory of Respiratory Health and Multimorbidity, Department of Pediatrics, China-Japan Friendship Hospital, National Clinical Research Center for Respiratory Diseases, Institute of Respiratory Medicine, Chinese Academy of Medical Sciences, Beijing, China
2 Precision and Smart Imaging Laboratory, Beijing Friendship Hospital, Capital Medical University, Beijing, China
3 Graduate School of Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China

Objective: This study aims to explore the association between outdoor artificial light at night (ALAN) exposure and gestational diabetes mellitus (GDM).

Methods: This study is a retrospective case–control study. According with quantiles, ALAN has been classified into three categories (Q1-Q3). GDM was diagnosed through oral glucose tolerance tests. Conditional logistic regression models were used to evaluate the association between ALAN exposure and GDM risk. The odds ratio (OR) with 95% confidence interval (CI) was used to assess the association. Restricted cubic spline analysis (RCS) was utilized to investigate the no liner association between ALAN and GDM.

Results: A total of 5,720 participants were included, comprising 1,430 individuals with GDM and 4,290 matched controls. Pregnant women exposed to higher levels of ALAN during the first trimester exhibited an elevated risk of GDM compared to those with lower exposure levels (Q2 OR = 1.39, 95% CI 1.20–1.63, p < 0.001); (Q3 OR = 1.70, 95% CI 1.44–2.00, p < 0.001). Similarly, elevated ALAN exposure during the second trimester also conferred an increased risk of GDM (second trimester: Q2 OR = 1.70, 95% CI 1.45–1.98, p < 0.001; Q3 OR = 2.08, 95% CI 1.77–2.44, p < 0.001). RCS showed a nonlinear association between ALAN exposure and GDM risk in second trimester pregnancy, with a threshold value of 4.235.

Conclusion: Outdoor ALAN exposure during pregnancy is associated with an increased risk of GDM.

1 Introduction

Exposure to artificial light at night (ALAN) has emerged as a progressively ubiquitous environmental hazard within contemporary society ( 1 ). Over the past several decades, urbanization and shifts in modern lifestyle have led to a continuous escalation of ALAN in our daily lives ( 2 ). While ALAN offers convenience and safety, it also brings forth an array of potential health concerns ( 3 ).

It is worth noting that recent research has employed satellite remote sensing data to validate the correlations between ALAN and a range of human health issues, including obesity ( 4 ), metabolic syndrome ( 5 ), sleep disorder ( 6 , 7 ), and cancer ( 8 ). Furthermore, emerging evidence suggests an association between ALAN and the risk of type 2 diabetes (Minjee ( 9 – 11 )). However, the relationship between outdoor ALAN exposure and gestational diabetes mellitus (GDM) remains poorly understood.

The mechanisms through which ALAN impacts human health remain unclear; however, research indicates that ALAN can disrupt circadian rhythms in humans and other organisms, thereby influencing various physiological processes and behavioral patterns ( 12 , 13 ). Exposure to ALAN may even lead to suppressed secretion of melatonin, a hormone that plays a crucial role in regulating sleep and other physiological functions ( 14 ). Furthermore, ALAN may impact the functioning of other endocrine systems, such as the secretion of adrenal corticosteroids and insulin regulation ( 15 ).

GDM is a condition characterized by abnormal blood glucose levels during pregnancy ( 16 ). Reports indicate that the prevalence of GDM varies across different countries and regions, with a notably higher incidence of 14.8% reported in China, making it a noteworthy public health concern in the country ( 17 ). This increased prevalence can primarily be attributed to behavioral and environmental risk factors ( 18 ). For mothers, having GDM can lead to heightened risks of pregnancy complications such as hypertension ( 19 ) and preterm birth ( 20 ), along with an elevated risk of developing type 2 diabetes later in life ( 21 ). Additionally, GDM can have enduring consequences for the newborn, including neonatal cardiovascular health ( 22 ) and respiratory distress syndrome ( 23 ). Consequently, the identification of potential risk factors for gestational diabetes is of paramount importance in mitigating the risks posed to both mothers and their offspring.

Pregnant women constitute a unique population group, as they are more susceptible to the influence of environmental factors during pregnancy due to hormonal effects ( 24 ). Current research suggests that exposure to ALAN may have adverse effects on fetal size and the metabolism of offspring ( 25 , 26 ). Hence, this study postulates that ALAN among pregnant women may is the risk of GDM through alterations in circadian rhythms and metabolism. The primary objective of this study is to investigate the association between outdoor ALAN exposure and gestational diabetes, aiming to address existing knowledge gaps and offer pertinent public health recommendations.

2 Materials and methods

2.1 study population.

This retrospective case–control study was conducted at the China-Japan Friendship Hospital. The geographic distribution of the study participants is illustrated in Figure 1 . Participants were selected based on specific inclusion criteria, which included: (1) residence in Beijing; (2) delivery at the China-Japan Friendship Hospital; (3) maternal age ≥ 18 years; (4) singleton pregnancies; (5) live-born infants. Exclusion criteria encompassed: (1) missing residential address ( n = 1,122); (2) presence of complications during pregnancy, such as gestational hypertension, placental abruption, etc. ( n = 320); (3) missing information on age, delivery date, last menstrual period (LMP) date, and other related data ( n = 670). A 1:3 propensity score matching was performed based on nation and offspring sex to select the control group. The final study comprised 5,720 participants, and the workflow is depicted in Figure 2 .

Figure 1 . Geographical distribution of participants in Beijing. ALAN: artificial light at night; Red dots represent GDMs, and green dots represent controls. GDM, gestational diabetes mellitus.

Figure 2 . Flowchart of the study. LMP, Last Menstrual Period; GDM, Gestational diabetes mellitus; NDVI, normalized difference vegetation index; PM 2.5 , ambient fine particulate matter; PM 10 , ambient inhalable particulate matter.

The retrospective case–control study design precluded the acquisition of informed consent from the participants. Nevertheless, this approach aligns with the ethical review approved by the Ethics Committee of the China-Japan Friendship Hospital (Ethics Review Number: 2023-KY-137), which acknowledges the impracticality of obtaining informed consent in retrospective research studies.

2.2 Assessment of outdoor ALAN

In this study, ALAN measurements were obtained using the Suomi National Polar-Orbiting Partnership Visible Infrared Imaging Radiometer Suite (NPP-VIIRS), which offers superior spatial resolution, enhanced temporal resolution, an extended spectral range, and advanced calibration and correction when compared to the Operational Linescan System of Defense Meteorological Satellite Program (OLS-DMSP) ( 27 ). Commencing in April 2012, NPP-VIIRS captures data within the wavelength range of 500 nm to 900 nm, with a spatial resolution of 500 m × 500 m at the Equator ( 28 ). Monthly NPP-VIIRS nighttime light data for the period from 2013 to 2020 were obtained from the Earth Observation Group. 1 The unit of measurement is nanowatts per square centimeter per steradian (nW/cm 2 /sr), which quantifies the radiative intensity per unit area, accounting for solid angles in all directions.

2.3 Outcomes and covariates

In this study, we directly acquired the diagnosis of GDM in participants from electronic health records. This diagnosis was based on the results of the 75 g oral glucose tolerance test (75 g OGTT) conducted on participants between gestational weeks 24–28. Participants were diagnosed with GDM if they met any of the following diagnostic criteria: fasting blood glucose level ≥ 5.1 mmol/L (92 mg/dL); 1-h blood glucose level ≥ 10.0 mmol/L (180 mg/dL); 2-h blood glucose level ≥ 8.5 mmol/L (153 mg/dL) ( 29 ). This study concurrently collected data on fetal sex and birth weight. Additionally, information on the following covariates was gathered: maternal race (Han, non-Han), age (years), parity (primiparous, multiparous), gravidity (1, 2, >2 times), pre-pregnancy body mass index (BMI, kg/m 2 ), and conception season (Spring, Summer, Autumn, and Winter).

2.4 Other environmental variables

Given the role of environmental factors in GDM, we incorporated environmental covariates including inhalable particulate matter (PM 10 ) and fine particulate matter (PM 2.5 ), as well as green space, into the study. The data for PM 2.5 and PM 10 were sourced from the China High-resolution Air Pollutants (CHAP) database. PM 2.5 and PM 10 data were obtained using a spatiotemporal extreme random tree model that leveraged model data to fill spatial gaps in Moderate Resolution Imaging Spectroradiometer Multi-Angle Implementation of Atmospheric Correction Aerosol Optical Depth satellite products. This approach integrated ground observations, atmospheric reanalysis, emissions inventories, and other large-scale data sources, generating seamless nationwide surface PM 2.5 and PM 10 data from 2000 to 2021. The ten-fold cross-validation coefficient of determination (R 2 ) for PM 2.5 data was 0.92, with a root mean square error (RMSE) of 10.76 μg/m 3 ( 30 ). For the PM 10 data, the ten-fold cross-validation yielded an R 2 of 0.9 and an RMSE of 21.12 μg/m 3 ( 31 ). The Normalized Difference Vegetation Index (NDVI) was employed as a surrogate indicator for residential greenness. NDVI is a widely utilized metric in environmental research for quantifying the density and health status of vegetation in various regions ( 32 ). This index ranges from 0 to 1, where higher NDVI values indicate denser and healthier vegetation, while lower values suggest sparse or stressed vegetation ( 33 ). In our study, NDVI was estimated based on 16-day composite images from the NASA Terra Moderate Resolution Imaging Spectroradiometer satellite. 2 After obtaining annual data for PM 2.5 , PM 10, and NDVI, we performed weighting matching for the residential locations of pregnant women and computed annual prenatal environmental pollution exposures.

2.5 Exposure time window

Participants’ residential addresses were geocoded using Baidu Maps. 3 Subsequently, we proceeded to estimate the average exposure levels during the first and second trimesters of pregnancy to investigate potential heterogeneity in the association between ALAN and GDM across different exposure windows. These exposure windows corresponded to the first and second trimesters of pregnancy, corresponding to 3 and 6 months after the last menstrual period, respectively.

2.6 Statistical analysis

Continuous variables, normally distributed, are presented as mean ± standard deviation, while categorical variables are presented as counts (percentages). Differences between groups for continuous variables were compared using t-tests or Wilcoxon tests. Differences between groups for categorical variables were compared using chi-square tests or Fisher’s exact tests.

We employed conditional logistic regression to assess the link between ALAN exposure and GDM, calculating odds ratios (ORs) with 95% confidence intervals (CIs). Initially, we established an unadjusted model, without considering any potential confounding factors. Subsequently, we adjusted for potential confounders including age, ethnicity, gravidity, parity, pre-pregnancy body mass index, and conception season. Covariate selection guided by Directed Acyclic Graph Analysis ( Supplementary Figure S1 ). Finally, while controlling for potential confounding, we further controlled for PM 2.5 , PM 10 , and NDVI. Employing Pearson correlation analysis, we identified a strong correlation between PM 2.5 and PM 10 (correlation coefficient = 0.97, p < 0.001). To mitigate issues of multicollinearity, principal component analysis was utilized to reduce the dimensionality of PM 2.5 and PM 10 , incorporating the first principal component (PC1), which accounted for 71.65% of the variance, into the final model as a substitute for both PM 10 and PM 2.5 .

To investigate the association between exposure to ALAN and GDM, restricted cubic spline (RCS) analysis was utilized in this study. The analysis was focused on ALAN exposure in first and second trimester pregnancy, assessing its nonlinear relationship with the risk of GDM. Additionally, we conducted a stratified analysis by infant sex to examine potential effect modification and assessed the interaction between ALAN and infant sex. The inclusion of interaction terms in the model was employed to assess whether fetal sex modifies the effect of exposure on the risk of GDM.

All statistical analyses were performed using R (version 4.1.0, available at https://www.r-project.org/ ).

2.7 Sensitivity analyses

This study conducted multiple sensitivity analyses: (1) ALAN per SD increase was employed to assess the relationship with GDM ( Supplementary Tables S1, S2 ). (2) Evaluation of Han ethnicity participants was performed to assess potential influences related to ethnicity ( Supplementary Table S3 ). (3) Similar analyses were conducted within the primiparous population to assess potential differences that might arise from multiple pregnancies ( Supplementary Table S4 ). (4) Excluding participants with pre-existing diabetes prior to pregnancy ( Supplementary Table S5 ). (5) Using linear regression to investigate the effect of ALAN exposure on participants’ fasting blood glucose levels ( Supplementary Table S6 ).

3.1 Characteristics of the study population

Table 1 provides an overview of the characteristics of pregnant women and newborns in the control group ( n = 4,290) and GDM group ( n = 1,430). While there were no significant differences in Han Chinese ethnicity between the group, the GDM group had a slightly higher mean age (GDM: 31.85 ± 3.96 years; Controls: 30.69 ± 3.41 years, p < 0.001). Furthermore, the GDM group showed a higher proportion of multiparous women (23.92% compared to 19.91% in the control group, p = 0.001). Gravidity distribution also significantly differed between the groups ( p < 0.001). The distribution of neonatal sex was similar, with 51.40% males in the control group and 51.89% males in the GDM group. Additionally, there were slight differences in neonatal length (Control: 50.67 ± 2.39 cm; GDM: 50.47 ± 2.51 cm, p = 0.007), birth weight (Control: 3302.70 ± 479.89 g; GDM: 3270.36 ± 510.18 g, p = 0.030), and gestation duration (Control: 276.77 ± 12.90 days; GDM: 274.92 ± 33.59 days, p = 0.003) between the groups.

Table 1 . Characteristics of pregnant women and newborns.

3.2 Distribution of environmental factors in different trimesters

Table 2 presents the differences in outdoor ALAN levels between the GDM and Control groups. There were no statistically significant differences in PM 10 levels (Control: 102.85 ± 21.33 μg/m 3 ; Case: 103.41 ± 20.70 μg/m 3 , p = 0.391) or PM 2.5 levels (Control: 64.87 ± 17.72 μg/m 3 ; Case: 65.90 ± 17.47 μg/m 3 , p = 0.054) between the two groups. Similarly, the NDVI showed no significant difference (Control: 0.32 ± 0.07; Case: 0.31 ± 0.07, p = 0.216). However, there were substantial differences in ALAN levels between the groups. In the first trimester (T1), ALAN levels were significantly higher in the GDM group (27.46 ± 16.86 nW/cm 2 /sr) compared to the Control group (24.42 ± 16.64 nW/cm 2 /sr, p < 0.001). This trend was consistent in the second trimester (T2) (Control: 24.69 ± 16.81 nW/cm 2 /sr; Case: 27.34 ± 16.61 nW/cm 2 /sr, p < 0.001).

Table 2 . Differences in outdoor ALAN levels between the GDM and control groups.

3.3 Association of outdoor ALAN exposure in different trimesters with GDM

In Table 3 , we present the results of conditional logistic regression models examining the association between outdoor ALAN exposure and the risk of GDM across various trimesters (T1 and T2). In the initial unadjusted model (Model 1), participants in the second (Q2) and third (Q3) quartiles of ALAN exposure exhibited significantly elevated odds of developing GDM compared to those in the first quartile (Q1) during all trimesters (all p -values <0.001). These results remained consistent after accounting for potential confounders. Specifically, for the first trimester, the ORs were as follows: Q2 OR = 1.39 (95%CI 1.20–1.63, p < 0.001), Q3 OR = 1.70 (95%CI 1.44, 2.00, p < 0.001). In the second trimester, the ORs were: Q2 OR = 1.70 (95%CI 1.45–1.98, p < 0.001), Q3 OR = 2.08 (95%CI 1.77–2.44, p < 0.001). No significant interaction between ALAN exposure and sex was observed across all models. Table 4 presents the sex-specific associations of ALAN exposure with the risk of GDM across different trimesters, along with tests for interaction. ALAN exposure exhibited consistent associations with GDM risk across trimesters, particularly among females. In our study, RCS analysis showed no significant nonlinear relationship between ALAN exposure and GDM risk in first trimester pregnancy. However, a significant nonlinear association was found in second trimester pregnancy, with a threshold value of 4.235 ( Figure 3 ).

Table 3 . Association of outdoor ALAN exposure with GDM.

Table 4 . Sex-specific associations of ALAN exposure with GDM.

Figure 3 . Restricted cubic spline analysis. (A) The association between first-trimester ALAN and GDM; (B) The relationship between second trimester ALAN and GDM; ALAN, Artificial Light at Night; GDM, Gestational Diabetes Mellitus.

4 Discussion

To investigate the association between outdoor ALAN exposure and GDM, we conducted a retrospective case–control study. Our study found a significant association between exposure to outdoor ALAN during pregnancy and an increased risk of GDM after adjusting for confounding factors. Furthermore, the association between outdoor ALAN and the risk of GDM did not differ between male and female infants. Our findings provide evidence supporting the role of outdoor ALAN in the risk of GDM among pregnant women.

In recent decades, the impact of ALAN on human health has gained global attention. Numerous studies have investigated the associations between ALAN exposure and chronic conditions such as cardiovascular diseases ( 34 ), obesity ( 35 ), and mental disorders ( 36 ). Recent research has suggested that exposure to outdoor ALAN may increase the risk of type 2 diabetes mellitus (T2DM) (Minjee ( 9 , 10 )). Furthermore, a cross-sectional study has shown a significant association between long-term exposure to higher-intensity outdoor ALAN and an increased risk of impaired glucose metabolism ( 11 ). Recent studies have elucidated the relationship between ALAN and GDM. In the United States, the risk associated with GDM has been correlated with pre-sleep exposure to light, as measured by wrist-worn activity monitors ( 37 ). Consistent with our findings, a prospective cohort study in Sichuan Province, China, utilizing satellite data to estimate outdoor ALAN exposure, offered a broader perspective on environmental exposure ( 38 ). Furthermore, a study conducted in Hefei City revealed that outdoor ALAN was associated with elevated early-pregnancy glucose homeostasis markers, yet it did not correlate with GDM risk ( 39 ). The variability in these findings may be attributed to differences in study populations and geographical locations. Our research, conducted in Beijing, a major metropolitan area, underscores the significant public health implications of addressing light pollution in densely populated urban environments. Moreover, our study surpassed traditional methods by thoroughly adjusting for critical environmental variables, including PM 2.5 , PM 10 , and NDVI, thereby reinforcing the robustness and credibility of our findings.

Exploring the critical windows of association between maternal ALAN exposure and the risk of GDM is of paramount importance for devising targeted intervention measures. The early and mid-stages of pregnancy are crucial periods for embryonic and fetal development, being particularly susceptible to external environmental influences ( 40 ). In our study, we observed that pregnant women exposed to higher levels of ALAN during the first and second trimesters exhibited an increased risk of GDM. However, considering the timing of GDM diagnosis ( 41 ), the relationship between ALAN exposure during the second trimester of pregnancy and GDM may be subject to constraints, necessitating further investigation.

The mechanisms underlying the relationship between ALAN exposure during pregnancy and the risk of GDM remain poorly understood. Several potential mechanisms may be involved. Firstly, ALAN exposure could potentially impact the risk of GDM by disrupting the circadian rhythms of pregnant women. Circadian rhythm regulation during pregnancy is critical for normal fetal and maternal physiological processes ( 42 ). ALAN may induce circadian rhythm disruption ( 43 ), leading to sleep disturbances and reduced sleep quality among pregnant women, consequently increasing the risk of GDM. Secondly, hormonal changes may play a significant role. ALAN exposure may influence hormone levels in pregnant women ( 44 ), particularly melatonin, a hormone crucial for regulating circadian rhythms during pregnancy ( 45 ). ALAN exposure might suppress melatonin secretion, potentially affecting maternal physiology and fetal development negatively. Lastly, ALAN exposure may contribute to an elevated risk of GDM by provoking alterations in inflammation and immune responses. Animal experiments have demonstrated that prolonged illumination can lead to changes in both the immune system and inflammatory processes ( 46 ). Although these mechanisms remain multifaceted and not fully elucidated, further research is needed to unravel these intricate pathways. In-depth investigations in both laboratory and epidemiological settings will contribute to a better understanding of the relationship between ALAN exposure and GDM, offering more precise directions for future intervention strategies.

This study has several limitations that warrant discussion. Firstly, in our research, we estimated outdoor ALAN exposure during pregnancy using high-resolution satellite images. However, we lacked data on indoor light exposure and whether participants used blackout curtains during the night, which could potentially lead to exposure misclassification. Future studies should consider collecting information on both indoor and outdoor light exposure. Secondly, while we adjusted for environmental confounders related to GDM, such as environmental particulate matter ( 47 ) and greenness ( 48 ) at the residential area, we did not account for other potential confounding factors, such as temperature ( 49 ), household income and education level. The absence of this information needs to be addressed and improved in future research. Thirdly, our study adopted a retrospective case–control study design, limiting the ability to establish causality between ALAN exposure and GDM. Therefore, the relationship between ALAN and GDM needs further confirmation through prospective study designs. Fourthly, the annual inclusion of study participants was not uniform ( Supplementary Table S7 ), which was due to the COVID-19 pandemic. Although the ratio of cases to controls remained consistent, this could potentially introduce a certain degree of bias. Finally, our single-center study involved participants from the Beijing area with relatively higher socioeconomic status. Caution is advised when extending the study results to regions with lower economic development. Future research should validate these findings in diverse socioeconomic contexts.

Despite these limitations, our study possesses several strengths. Firstly, we elucidated the association between ALAN exposure during pregnancy and GDM, identifying the critical exposure window for this relationship. This finding provides valuable reference for targeted intervention measures during the identified exposure window. Additionally, we conducted a series of sensitivity analyses and performed stratified analyses by newborn sex to assess the consistency and robustness of this relationship.

5 Conclusion

In summary, our study reveals that higher outdoor ALAN exposure during pregnancy is associated with an elevated risk of GDM. These findings emphasize the need for targeted interventions and further research to better understand the mechanisms underlying this relationship and mitigate the health risks associated with light pollution during pregnancy.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Ethics statement

The studies involving humans were approved by Ethics Committee of the China-Japan Friendship Hospital. The studies were conducted in accordance with the local legislation and institutional requirements. The ethics committee/institutional review board waived the requirement of written informed consent for participation from the participants or the participants' legal guardians/next of kin because this was a retrospective study and the ethics committee waived informed consent.

Author contributions

QS: Methodology, Writing – original draft, Writing – review & editing. FY: Investigation, Visualization, Writing – original draft, Writing – review & editing. JL: Investigation, Writing – original draft, Writing – review & editing. YY: Investigation, Writing – original draft, Writing – review & editing. QH: Software, Writing – original draft, Writing – review & editing YC: Data curation, Resources, Writing – original draft, Writing – review & editing. DLi: Software, Writing – original draft, Writing – review & editing. JG: Data Curation, Writing – original draft, Writing – review & editing. CW: Software, Writing – original draft, Writing – review & editing. DLv: Visualization, Writing – original draft, Writing – review & editing. LT: Investigation, Writing – original draft, Writing – review & editing. QZ: Conceptualization, Supervision, Writing – original draft, Writing – review & editing.

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was funded by MOE Key Laboratory of Population Health Across Life Cycle (No: JK20225), Chinese Academy of Medical Sciences Clinical and Translational Medicine Research Project (No: 2021-I2M-C&T-B-089), Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences (No: 2021-I2M-1-049), and a grant from State Key Laboratory of Resources and Environmental Information System.

Acknowledgments

We thank all the participants in this study.

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.

Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpubh.2024.1396198/full#supplementary-material

Abbreviations

ALAN, artificial light at night; GDM, gestational diabetes mellitus; CI, confidence interval; OR, odds ratio; OLS-DMSP, Operational Linescan System of Defense Meteorological Satellite Program; NPP-VIIRS, Suomi National Polar-Orbiting Partnership Visible Infrared Imaging Radiometer Suite; PM10, ambient inhalable particulate matter; PM2.5, ambient fine particulate matter; CHAP, China High Air Pollutants; NDVI, normalized difference vegetation index; RMSE, root mean square error; R2, coefficient of determination.

1. ^ https://eogdata.mines.edu/

2. ^ https://ladsweb.modaps.eosdis.nasa.gov

3. ^ https://map.baidu.com

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46. Zhang, L, Liu, Y, Li, M, Zhu, X, and Shi, Y. Effect of a high-calorie diet and constant light exposure on female reproduction, metabolism and immune inflammation: a comparative study of different mouse models. Am J Reprod Immunol . (2021) 86:e13479. doi: 10.1111/aji.13479

47. Ren, Z, Yuan, J, Luo, Y, Wang, J, and Li, Y. Association of air pollution and fine particulate matter (PM2.5) exposure with gestational diabetes: a systematic review and meta-analysis. Ann Transl Med . (2023) 11:23–3. doi: 10.21037/atm-22-6306

48. Qu, Y, Yang, B, Lin, S, Bloom, MS, Nie, Z, Ou, Y, et al. Associations of greenness with gestational diabetes mellitus: the Guangdong registry of congenital heart disease (GRCHD) study. Environ Pollut . (2020) 266:115127. doi: 10.1016/j.envpol.2020.115127

49. Pace, NP, Vassallo, J, and Calleja-Agius, J. Gestational diabetes, environmental temperature and climate factors – from epidemiological evidence to physiological mechanisms. Early Hum Dev . (2021) 155:105219. doi: 10.1016/j.earlhumdev.2020.105219

Keywords: gestational diabetes mellitus, outdoor artificial light, pregnancy, risk factors, air pollution

Citation: Sun Q, Ye F, Liu J, Yang Y, Hui Q, Chen Y, Liu D, Guo J, Wang C, Lv D, Tang L and Zhang Q (2024) Outdoor artificial light at night exposure and gestational diabetes mellitus: a case–control study. Front. Public Health . 12:1396198. doi: 10.3389/fpubh.2024.1396198

Received: 05 March 2024; Accepted: 02 April 2024; Published: 10 April 2024.

Reviewed by:

Copyright © 2024 Sun, Ye, Liu, Yang, Hui, Chen, Liu, Guo, Wang, Lv, Tang 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: Qi Zhang, [email protected]

Disclaimer: 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.

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Outcomes of UTI and bacteriuria caused by ESBL vs . non-ESBL Enterobacteriaceae isolates in pregnancy: a matched case–control study

Infectious Diseases Institute, Soroka University Medical Center and Joyce and Irving Goldman Medical School, Ben-Gurion University of the Negev, Beer-Sheva, Israel

K. Riesenberg

L. saidel-odes, r. smolyakov.

Infections caused by extended-spectrum β -lactamase-producing Enterobacteriaceae (ESBL-E) have become increasingly prevalent, posing a serious public threat worldwide. It is commonly believed that untreated urinary tract infections (UTI) and asymptomatic bacteriuria (ABU) during pregnancy are associated with poor obstetric outcomes. Currently, there is a paucity of data regarding the outcomes or risk factors of such ESBL-E infections in pregnant women. We conducted a retrospective 1:2 matched case–control study of hospitalised pregnant women with ESBL-E- vs. non-ESBL-producing Enterobacteriaceae -positive urine cultures obtained between 2004 and 2015, and compared risk factors for the development of resistant bacteria, clinical course and outcomes. In total, 87 pregnant women with ESBL-E-positive urine cultures were matched to 174 controls by decade of age, ethnicity and pregnancy trimester. Significant risk factors for acquisition of ESBL-E included prior UTI/ABU episodes (50.6% vs. 26.3%, P < 0.001), previous isolation of ESBL-E in urine cultures (12.6% vs. 0.6%, P < 0.001) and prior antibiotic exposure (71.3% vs. 54%, P = 0.002). Previous hospitalisation, however, was not found to be a risk factor. No significant difference was found in adverse obstetric outcomes. We conclude that prior urinary infections and antibiotic exposure were significant risk factors for the isolation of ESBL-E pathogens from the urine of pregnant women; however, this was not associated with worse obstetric outcomes compared with non-ESBL-E pathogens.

Introduction

Urinary tract infection (UTI) in pregnancy represents one of the most prevalent infections in this young, relatively healthy population [ 1 ]. It is well established that asymptomatic bacteriuria (ABU) occurs in 2–10% of pregnancies. Early studies have shown that when left untreated, approximately 30% of women developed pyelonephritis, and that both ABU and pyelonephritis were associated with poor obstetric outcomes, including preterm labour and low birth weight [ 2 ]. Therefore, current guidelines recommend routine urine cultures during pregnancy, and antimicrobial treatment for positive urine cultures [ 3 ], although this concept is currently being challenged [ 4 ].

Extended-spectrum β -lactamase-producing Enterobacteriaceae (ESBL-E) have been a major health concern among hospitals and long-term care facilities, mostly affecting elderly patients with significant co-morbidities. However, they are also increasingly implicated as causes of community-acquired infections. In recently published data, the global prevalence of ESBL-E rectal colonisation among healthy individuals was 14%, varying greatly geographically, with the highest rates in developing countries [ 5 ]. Previously recognised risk factors for ESBL-E included: prior antibiotic use [ 6 – 9 ], prior hospitalisation, residence in a long-term care facility, age above 65 years, male gender, [ 6 , 7 ] prostate disease [ 8 ], prior episodes of UTI, proton pump inhibitor use and travel [ 9 ]. Among pregnant women, rectal colonisation of ESBL-E near term was found to be 2.9–18.5%, with the highest rates reported among women in Africa [ 10 , 11 ]. Furthermore, a study done at an antenatal clinic in India found that 45% of Escherichia coli isolates from the urine of both symptomatic and asymptomatic pregnant women had an ESBL phenotype [ 12 ].

Currently, there is a paucity of data regarding ESBL-E UTI/ABU during pregnancy. The aim of this study was therefore to assess the risk factors, clinical course and obstetric outcomes of pregnant women with ESBL-E-positive urine cultures, as opposed to pregnant women with non-ESBL-producing Enterobacteriaceae UTI/ABU.

This retrospective matched case–control study was performed at Soroka Medical Center, a 1100 bed tertiary care hospital in southern Israel. This is the only medical centre providing obstetrics and gynaecology services to over 1 million residents in the Negev region. After obtaining permission and waiver of informed consent from the institutional ethical review board, data were obtained from the microbiology laboratory on all positive urine cultures, taken in the obstetrics and gynaecology wards at our institution, between 1 January 2004 and 30 June 2015 ( Fig. 1 ). Medical files were reviewed, and only women, who were pregnant at the time of specimen collection, were included in the study. Urine cultures were taken by the treating physicians, at their clinical judgement, upon admission to the hospital or during hospitalisation. Files were then reviewed by the authors, and judged to be ABU or symptomatic infection. Cystitis was defined by the presence of frequency, urgency, dysuria or abdominal pain other than contraction, and pyelonephritis was considered when either flank pain, fever or chills were documented. All other clinical scenarios were classified as ABU.

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Selection of study population. *Controls were selected using frequency matching according to the year of the positive urine cultures, the women's age decade, ethically (Bedouin Arab vs . non-Bedouin Arab) and pregnancy trimester.

Identification of an ESBL-E phenotype was performed by disc diffusion tests using ceftazidime/clavulanate 30/10 µ g and cefotaxime/clavulanate 30/10 µ g combination discs, compared with ceftazidime 30 µ g and cefotaxime 30 µ g discs alone (Oxoid Ltd, Basingstoke, UK). An increase in a zone diameter >5 mm for either antimicrobial agent in combination with clavulanate vs. the zone diameter of the agent when tested alone defined ESBL-E according to the Clinical and Laboratory Standards Institute (CLSI) antimicrobial susceptibility testing standards [ 13 ]. Prior to 2008, the ESBL-E phenotype was defined as resistance to third-generation cephalosporins.

After obtaining information on pregnant patients with an ESBL-E urine isolate (cases), two pregnant patients with a non-ESBL-E urine isolate were matched as (controls) according to the year of the positive cultures, age decade, ethnicity (Bedouin Arab vs. non Bedouin) and pregnancy trimester. All other information collected was unmatched. These parameters were chosen, as both age and infection in late pregnancy, may pose a risk for adverse pregnancy outcomes [ 14 , 15 ], and there are discrepancies in access to medical care within different ethnic groups in our community. Matching was done using frequency matching in the controls, in order to get the same distribution of variable as in the cases and to minimise time differences effects [ 16 ]. After defining our groups according to the urine culture taken within the hospital, data were extracted both from medical records at our institution, and a computer database system, which included comprehensive information on all cultures taken in both the ambulatory and inpatient settings, and information on all hospital admissions, nationwide. Previous isolation of ESBL-E was defined as any prior positive culture with this phenotype. Other details, such as underlying medical conditions, obstetric history and antibiotics prescribed by the treating physician in the prior 6 months, were also recorded. Hospital-acquired UTI/ABU was defined as urine cultures obtained 72 h or more following hospitalisation, or from patients who were hospitalised within the previous 2 weeks.

Statistical analysis was performed using IBM Statistics SPSS (version 22). Univariate analysis was used to describe the groups. Bivariate analysis was used to compare baseline characteristics, risk factors for the development of ESBL-E infections, clinical course and obstetric outcomes for categorical variables by Pearson's χ 2 test. Normally distributed quantitative variables were analysed with either Student's t test or one-way analysis of variance test as appropriate. Abnormally distributed quantitative variables were processed using Mann–Whitney test or Kruskal–Wallis test. We also analysed the association between prior UTI/ABU episodes, previous isolation of ESBL-E in urine cultures and prior antibiotic exposure and ESBL-E-positive urine culture, using logistic regression analysis. ESBL-E-positive urine culture was defined as the dependent variable. Prior UTI/ABU episodes, previous isolation of ESBL-E in urine cultures and prior antibiotic exposure were defined as the independent variables. We employed two-tailed tests with P = 0.05 for statistical significance.

We identified 2469 hospitalised women with positive urine cultures, and of these, 153 cultures were ESBL-E-positive. After reviewing the medical charts, excluding 48 non-pregnant women, and 18 women for whom data were unavailable, 87 cases were included and randomly matched to 174 pregnant controls ( Fig. 1 ).

Baseline characteristics of the study groups ( Table 1 ) were similar overall in both groups. There was also no significant difference in various risk factors for adverse pregnancy outcomes including the proportions of nulliparity (34.5% vs. 33.9%, P = 0.77), pregnancy after fertility treatments (6.9% vs. 6.3%, P = 0.85) and most notably high-risk pregnancy (36.8% vs. 44.3%, P = 0.28) defined by standard obstetric criteria [ 17 ]. The majority of the ESBL-E group were E. coli (64.4%), but a significantly higher proportion of Klebsiella spp. isolates was evident in the ESBL-E group than in the non-ESBL-E group (31.1% vs. 17.8%, P = 0.01). Comparison of risk factors for ESBL-E between cases and controls showed a significant difference in: prior UTI/ABU episodes (50.6% vs. 26.3%, P < 0.001), previous isolation of ESBL-E in urine cultures (12.6% vs. 0.6%, P < 0.001) and prior antibiotic exposure in the last 6 months (71.3% vs. 54%, P = 0.002) ( Table 2 ). No significant difference was found in other parameters including diabetes mellitus (13.8% vs. 11.5%, P = 0.56), urinary tract abnormalities (5.7% vs. 5.2%, P = 0.47) and previous hospitalisation (33.3% vs. 28.1%, P = 0.39). We observed hospital-acquired infections in 17.2% of cases, and 20.6% of controls ( P = 0.50). Multivariate analysis identified previous isolation of ESBL-E in urine cultures ( P < 0.001) and prior UTI/ABU episodes ( P = 0.03) as statistically significant predictors of ESBL-E-positive urine culture during pregnancy.

Comparison of demographic and obstetric characteristics in the study groups

Comparison of risk factors for the development of ESBL-E infections in the study groups

Clinical manifestations were similar in both study groups. The majority of cases and controls were classified as ABU (47.1% vs. 43.1%, P = 0.70). Presentation as cystitis was observed in 28.7% of cases and 30.5% of controls ( P = 0.70), and 23% of both groups presented with pyelonephritis ( P = 1). Complications in both groups were uncommon; bacteraemia occurred in four cases and three controls (4.6% vs. 1.7%, P = 0.30), and three women, one case and two controls, were admitted to intensive care unit. Creatinine levels were within normal range in all women.

Obstetric outcomes are presented in Table 3 . No significant difference was found between case and control groups in any of the various adverse maternal and neonatal outcomes assessed, including preterm labour (25.3% vs. 29.9%, P = 0.51) and low birth weight (20.7% vs. 26.4%, P = 0.48).

Comparison of obstetric outcomes in the study groups

Significant associations were found between prior episodes of UTI/ABU and ESBL-E bacteriuria during pregnancy, as well as prior history of ESBL-E in urine cultures and prior antibiotic use. As opposed to previously published studies [ 6 , 7 ], underlying medical conditions and prior hospitalisation were not found to be associated with an increased risk for ESBL-E bacteriuria. The association between antibiotic exposure and the risk for harbouring an ESBL-producing isolate, especially in community-acquired infection/carriage, is well described in recent years, in keeping with the persistent rise in the prevalence of these infections [ 5 , 8 , 9 ]. Our data imply that even in hospitalised pregnant women, the role of factors associated with community-acquired infection, such as prior antibiotic use, is of greater importance than prior health care exposure, making ESBL-E infection/colonisation an important public health issue. This may help clinicians who face the need to choose an empiric therapy for pregnant women with a UTI, select an appropriate regimen, especially in areas with a high prevalence of ESBL-E pathogens.

The effect of ESBL-E on the clinical course in controversial. Most studies show a trend towards higher morbidity and mortality in patients with ESBL-E infections in the non-pregnant general population [ 18 – 20 ]. However, Denis et al. [ 21 ] showed no significant difference in the clinical outcomes of adults with ESBL E. coli bacteraemia. Most of the patients described in these studies were bacteraemic, with differences in empiric treatment. In our study, in which 75% of patients presented with a mild infection or ABU, we found a similar clinical course and a relatively low complication rate. This can probably be attributed to the low rate of severe infections, but it is important to point out that that in our specific setting, these pathogens on their own were not associated with a worse clinical outcome.

When examining wider maternal and neonatal outcomes, including those associated with UTI/ABU such as low birth weight and preterm labour [ 2 ], we found no significant differences between cases and controls. Of note, as our studied population was composed of hospitalised women, we had a high, and yet similar, rate of pregnancies defined as ‘high-risk’ (36.8% vs 44.3%) according to standard obstetric criteria [ 17 ]. As such, the two groups were relatively homogeneous in their risk factors for adverse pregnancy outcomes, other than their ESBL-E status. The high rates of preterm labour (25.3% vs. 29.9%), noticed in our study, corresponds with the prevalence of high-risk pregnancies, and did not differ between groups. Having a higher prevalence of a somewhat rare outcome in our study makes the statistical power of similarity stronger, but makes it less applicable to the general healthy population. As for the contribution of the infection itself to the high rate of preterm labours, our study was not designed to answer this question.

As discussed above, the proportion of severe infections (e.g. pyelonephritis, ICU patients) was relatively low in our study group, representing real-life experience of the clinical presentation of bacteriuria in pregnant women, with the majority presenting with mild to no clinical symptoms. Evidently, this is both an advantage of our work, being relevant to daily practice, but also less applicable for a scenario of the severely infected patient.

The main limitation of our study was its retrospective nature. As such, the isolates were not available for further molecular testing and typing or identifying mechanisms or resistance. Our study population were hospitalised pregnant women with higher rates of complicated pregnancies, which limits the generalisation of the results.

In conclusion, our study examined the risk factors and outcomes of a widening and yet not extensively described phenomenon of ESBL-E bacteriuria in pregnant women. In an era of shifting trends in risk factors for infection with resistant bacteria, we found that prior antibiotic exposure was associated with ESBL-E bacteriuria; however, we did not find ESBL-E bacteriuria to be associated with a more severe clinical course or adverse pregnancy outcomes, as compared with non-ESBL-E bacteriuria.

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

Conflict of interest

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Urinary Tract Infections in Pregnant Individuals
In a European case-control study dominated by alpha and beta thalassemia traits (72%), people with hemoglobinopathy trait were found to have higher rates of ASB or UTI in pregnancy (RR 12.18, 95% 4.76-33.51) than people in a matched control group 24.
Urinary Tract Infection in Pregnancy and Its Effects on Maternal and
A urinary tract infection (UTI) is a common medical condition complicating pregnancy with adverse maternal and perinatal outcomes. This study aimed to assess any adverse maternal and perinatal morbidity related to UTI in pregnancy, focusing on identifying common uropathogens and their antibiotic sensitivity and resistance patterns.
Urinary tract infections in pregnancy: old and new unresolved
Epidemiology and risk factors. Urinary tract infections remain among the most common medical complications during pregnancy. It is estimated that the prevalence of ASB varies between 2% and 10-13%, similar to nonpregnant women [9-13].There is a scarcity of data concerning acute cystitis in pregnancy; according to the available studies it is observed in 1-4% [11, 14, 15].
Urinary Tract Infection in Pregnancy
Urinary tract infections (UTIs) are frequently encountered in pregnant women. Pyelonephritis is the most common serious medical condition seen in pregnancy. Thus, it is crucial for providers of obstetric care to be knowledgeable about normal findings of the urinary tract, evaluation of abnormalities, and treatment of disease. Fortunately, UTIs in pregnancy are most often easily treated with ...
Abdominal Pain in a 26-Yr-Old Pregnant Woman
About the Case. Urinary tract infection (UTI) is common during pregnancy due to urinary stasis, which results from hormonal ureteral dilation, hormonal ureteral hypoperistalsis, and pressure of the expanding uterus against the ureters. Asymptomatic bacteriuria occurs in about 15% of pregnancies and sometimes progresses to symptomatic cystitis ...
Urinary tract infections in pregnancy
Urinary tract infections (UTIs) are the most common infection among pregnant women and have been associated with maternal and foetal complications. Antimicrobial exposure during pregnancy is not without risk. International guidelines recommend a single screen-and-treat approach to asymptomatic bacteriuria (ASB); however, this approach has been questioned by recent studies.
Urinary tract infections and asymptomatic bacteriuria in pregnancy
Without treatment, as many as 20 to 35 percent of pregnant women with asymptomatic bacteriuria will develop a symptomatic urinary tract infection (UTI), including pyelonephritis, during pregnancy [ 6,7 ]. This risk is reduced by 70 to 80 percent if bacteriuria is eradicated (see 'Rationale for treatment' below).
Urinary Tract Infections in Pregnant Individuals
In a European case-control study dominated by alpha and beta thalassemia traits (72%), people with hemoglobinopathy trait were found to have higher rates of ASB or UTI in pregnancy (RR 12.18, 95% 4.76-33.51) than people in a matched control group .
Urinary Tract Infections in Pregnancy Clinical Presentation
Urinary tract infection during pregnancy, angiogenic factor profiles, and risk of preeclampsia. Am J Obstet Gynecol. 2016 Mar. 214 (3):387.e1-7. [QxMD MEDLINE Link]. Schneeberger C, Geerlings SE, Middleton P, Crowther CA. Interventions for preventing recurrent urinary tract infection during pregnancy. Cochrane Database Syst Rev. 2015 Jul 26 ...
Diagnostic work-up of urinary tract infections in pregnancy: study
Introduction Symptoms of urinary tract infections in pregnant women are often less specific, in contrast to non-pregnant women where typical clinical symptoms of a urinary tract infection are sufficient to diagnose urinary tract infections. Moreover, symptoms of a urinary tract infection can mimic pregnancy-related symptoms, or symptoms of a threatened preterm birth, such as contractions. In ...
The association between urinary tract infection during pregnancy and
Out of the 19 studies, 14 studies (6 cohort, 1 cross-sectional study, and 7 case-control studies) indicated UTI during pregnancy as a risk factor for PE; the other 5 studies (both cohort) did not reveal any association between the 2 . As rated on the NOS and AHRQ scale, all 19 studies scored ≥5 points, which attested to their high quality.
Urinary tract infections and antibiotic use in pregnancy
Pregnancy can increase the susceptibility of urinary tract infections (UTIs) in women because of physiological changes [].The vast majority of primary care antibiotic prescriptions issued to pregnant women in the UK are for UTIs [] which suggests a high prevalence.Evidence from studies shows that asymptomatic infection alone can affect 2-12% of women [].
Urinary Tract Infection in Pregnancy and Its Effects on ...
Background A urinary tract infection (UTI) is a common medical condition complicating pregnancy with adverse maternal and perinatal outcomes. This study aimed to assess any adverse maternal and perinatal morbidity related to UTI in pregnancy, focusing on identifying common uropathogens and their antibiotic sensitivity and resistance patterns.
Urinary tract infections in pregnancy
Urinary tract infections (UTIs) are the most common bacterial infection in pregnancy and have been estimated to affect 2% to 15% of the pregnant population, although recent data suggest that this may be higher. Using data from the National Birth Defects Study population (41 869 women), Johnson et al. [ 1] found that 11% to 26% of women reported ...
Characteristics of women with urinary tract infection in pregnancy
Pooling the participants is unlikely to bias results if sociodemographic factors associated with UTI in pregnancy are similar in case and control mothers, the prevalence of these factors is similar between groups, and each group has similar accuracy in reporting UTI in pregnancy. Our study data suggest that the first two conditions might be true.
PDF Clinical Practice Guideline Management of Urinary Tract Infections in
Urinary tract infections (UTIs) are one of the most frequent complications during pregnancy (Overturf et al., 1992). Traditionally UTI is classified as either involving the lower urinary tract (acute cystitis) or the upper urinary tract (acute pyelonephritis). A predisposing factor or precursor to UTI is bacteriuria.
Urinary Tract Infection (Chapter 21)
> Infections in Pregnancy > Urinary Tract Infection; Infections in Pregnancy. An Evidence-Based Approach. Buy print or eBook [Opens in a new window] Book contents. ... Acute maternal infection and risk of pre-eclampsia: a population-based case-control study. PLoS ONE. 2013; 8: e73047.Google Scholar. 6 Glaser, AP, Schaeffer, AJ.
UTI in pregnancy: Causes, risks, and treatments
A UTI is an infection in any part of the urinary system, including the bladder and kidneys. Research suggests it is common for pregnant women to get UTIs.. According to one study from the Centers ...
Maternal Age and Stage of Pregnancy as Determinants of UTI in Pregnancy
Introduction . Urinary tract infection (UTI) is the world's second most common cause of death, trailing only respiratory tract infections. Because of anatomical and physiological changes along the urinary tract, pregnant women accounted for approximately 20% of all cases of urinary tract infection. Aim. This study sought to assess maternal age and stage of pregnancy as determinants of UTI ...
Pregnant women admitted with urinary tract infections to a public
Abstract. Background: Urinary tract infection (UTI) is associated with poor maternal and foetal outcomes. There is little information on UTI in pregnancy in South Africa. Objectives: To evaluate the frequency of UTI admissions of pregnant women admitted to a public health facility; and, to describe the outcomes of pregnancies complicated by UTI in our study population.
Pathogen-specific alterations in intestinal microbiota precede ...
Urinary tract infections (UTIs) are among the most common late-onset infections in preterm infants, characterized by nonspecific symptoms and a pathogenic spectrum that diverges from that of term infants and older children, which present unique diagnostic and therapeutic challenges. ... A longitudinal case-control study was conducted involving ...
Association Between Urinary Tract Infection in the First Trimester and
In this case-control study, 92 pregnant women with a diagnosis of preeclampsia were selected as cases, and for comparison 92 pregnant women were selected as control. ... Therefore, it is necessary to reduce the risk of preeclampsia in the coming months by controlling and treating urinary tract infections during pregnancy during timely and ...
Management of Urinary Tract Infection Symptoms in Older Wome
of the study was to assess knowledge, attitudes, and practices regarding management of older women (>65 years) with symptoms attributed to UTIs among family and internal medicine providers. Study Design This cross-sectional study surveyed 330 primary care providers in November 2021 regarding management of UTI symptoms. The primary outcome was the proportion of primary care providers who felt ...
Full article: Validating the ratio of insulin like growth factor
The Viet Nam Preterm Birth Biomarker study was a case-cohort study of PTB and term deliveries. ... Ho Chi Minh City, for their mid-pregnancy anomaly ultrasound scan from September 27, 2016-May 9, 2018 were invited to participate in the study. Tu Du Hospital is one of the largest maternity hospitals in Southeast Asia, conducting around 60000 ...
Can Pregnancy Accelerate Aging for Women? Study Says Yes
Study Says Yes. By Dennis Thompson HealthDay Reporter. TUESDAY, April 9, 2024 (HealthDay News) -- Pregnancy transforms women's bodies in many obvious ways, but new research suggests it may also ...
Clinical analysis of complete uterine rupture during pregnancy
Background Uterine rupture in pregnant women can lead to serious adverse outcomes. This study aimed to explore the clinical characteristics, treatment, and prognosis of patients with complete uterine rupture. Methods Data from 33 cases of surgically confirmed complete uterine rupture at Chenzhou No.1 People's Hospital between January 2015 and December 2022 were analyzed retrospectively ...
Diagnostic work-up of urinary tract infections in pregnancy: study
Introduction. The prevalence of urinary tract infections (UTIs) during pregnancy reported in literature varies between 2.3% and 15%. 1-5 It is hypothesised that anatomical changes during pregnancy such as dilatation of the ureters, decreased ureteral tone and increased bladder volume contribute to urinary stasis and ureterovesical reflux increasing the risk of a UTI. 6-8 Besides the ...
Network analysis of posttraumatic stress and posttraumatic growth
Pregnant women who have undergone pregnancy loss often display both posttraumatic stress (PTS) and posttraumatic growth (PTG). However, the precise relationship and structure of symptomatic levels of PTS and PTG have not been well understood. This study aimed to assess the associations between PTS and PTG symptoms in women during subsequent pregnancies following a previous pregnancy loss.
Frontiers
This retrospective case-control study was conducted at the China-Japan Friendship Hospital. ... Yan, F-F, Chen, Z, et al. Effects of Prepregnancy body mass index, weight gain, and gestational diabetes mellitus on pregnancy outcomes: a population-based study in Xiamen, China, 2011-2018. Ann Nutr Metab. (2019) 75:31-8. doi: 10.1159/000501710
Outcomes of UTI and bacteriuria caused by ESBL
Currently, there is a paucity of data regarding ESBL-E UTI/ABU during pregnancy. The aim of this study was therefore to assess the risk factors, clinical course and obstetric outcomes of pregnant women with ESBL-E-positive urine cultures, as opposed to pregnant women with non-ESBL-producing Enterobacteriaceae UTI/ABU.

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