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. 2025 Feb 27;14(1):tfaf028. doi: 10.1093/toxres/tfaf028

Meta-analysis of studies testing the association between air pollution and live birth rates in women undergoing assisted reproductive technology

Juan Hu 1,#, Huiqiu Zheng 2,#, Yan Wu 3,#, Qing Yan 4, Minghao Zhang 5, Shikun Sun 6, Meidi Gong 7, Rao Zheng 8, Shujing Jia 9, Rui Zhou 10, Jing Wu 11,12,✉
PMCID: PMC11878799  PMID: 40046769

Abstract

Amidst a proliferation of research on air pollutants and negative pregnancy outcomes, uncertainty lingers regarding their impact on live birth rates in women receiving assisted reproductive technology (ART). This meta-analysis aims to clarify this vital issue. We searched EMBASE, PubMed, and Web of Science databases, targeting articles published prior to 2023 August 2. We pooled relative risks (RRs) and their corresponding 95% confidence intervals (95%CIs) across all included studies to assess the relationship between exposure to air pollutants and live birth rates. From an initial 5,785 citations, we identified five eligible papers with a total sample size of approximately 282,000 participants. In the year prior to oocyte retrieval, for every 10 μg/m3 increase in fine particulate matter (PM2.5) (RR: 0.94, 95%CI: 0.92–0.97) and coarse particulate matter (PM10) (RR: 0.95, 95%CI: 0.92–0.97), the probability of live birth decreased by 6% and 5%, respectively. For every additional ppb increase in nitrogen dioxide (NO2) (RR: 0.92, 95%CI: 0.87–0.98), the likelihood of live birth decreased by 8%. This meta-analysis demonstrates adverse associations between air pollution and live birth rates in women undergoing ART. These findings highlight further elucidate the observed associations, as well as to explore potential mechanisms and implications for reproductive health.

Keywords: air pollution, assisted reproduction technology, live birth, meta-analysis

Introduction

Air pollution stands as a major environmental risk factor with far-reaching implications for human health, giving rise to a multitude of adverse health effects.1 There is growing evidence that air pollution adversely affects the reproductive system and is linked to adverse pregnancy outcomes such as preterm birth, low birth weight, and intrauterine growth restriction.2–4 Simultaneously, evidence has substantiated that exposure to air pollutants can reduce human fertility.5,6

Infertility has become a significant global reproductive health challenge, affecting an estimated 8%–12% of reproductive-aged couples worldwide.7 This upward trend has been attributed to factors such as delayed childbearing, environmental pollution, lifestyle changes, and increasing rates of obesity and other health conditions associated with reproductive dysfunction.8,9 In China, estimates place infertility rates at approximately 15%–20% for women and 10%–12% for men.10 With the increasing advancement and accessibility of assisted reproductive technology (ART), its utilization among infertile patients has grown significantly as a means to aid conception. ART including a series of involving the human oocytes and sperm or embryos in vitro operating procedures. These procedures include but are not restricted to in vitro fertilization (IVF), embryo transfer (ET), intrafollicular transfer of gametes, and intrafollicular transfer of fertilized oocytes, among others.11 Many factors can potentially effect embryo development within the realm of ART, among which air pollution has been identified as a significant risk factor due to its well-documented adverse effects on human reproductive health. Research has shown a concerning correlation between pregnancy loss among women undergoing ART and exposure to ambient air pollutants in a short period, such as coarse particulate matter (PM10) and nitrogen dioxide (NO2).12,13 However, the most crucial metric in assessing the efficacy of ART therapy is the live birth rate.14 Over the past few years, a series of epidemiological investigations have provided evidence linking environmental air pollutant exposure with diminished pregnancy and live birth rates among individuals undergoing ART.15–17

A large multicenter retrospective study spanning four cities in northern China identified associations indicating that exposure to ozone (O3), NO2 and carbon monoxide (CO) across various exposure windows during the fresh embryo transfer cycle was associated with lower live birth rates.18 However, a separate cohort study conducted in the United States found no significant correlation in relation to reproductive outcomes and daily average concentrations of exposure to fine particulate matter (PM2.5) and O3 among women undergoing IVF treatment.19 Nevertheless, current research on the effects of ambient air pollutants on the pregnancy outcomes of women undergoing ART remains limited. The outcomes of these studies frequently present inconsistencies or even conflicting results. Therefore, our study aims to comprehensively gather and synthesize all relevant literature published to date, subsequently employing a meta-analysis to evaluate the existing evidence.

Materials and methods

Inclusion criteria

(a) Cohort study; (b) The outcomes of live birth in women exposed to air pollutants and receiving assisted reproductive technology were clearly defined in these studies; (c) The quantitative estimation of air pollutant concentration was calculated, and the effects of exposure to one or more pollutants on live birth outcomes were analyzed and reported; (d) The original study provided its sample size and adjusted odds ratio (OR), relative risks (RRs) or hazard ratio (HR) as well as its 95% confidence interval (95%CI), or other useful information that could help to obtain these results.

Exclusion criteria

We excluded animal experiments, case reports, review articles, personal experience summaries, meta-analyses, meeting summaries, letters to editors, and studies inconsistent with the inclusion criteria or with poor data quality.

Search strategy

We conducted this study according to the Preferred Reporting Items (PRISMA) for Systematic Reviews and Meta-Analyses.20 A comprehensive search of EMBASE, PubMed and Web of Science databases was conducted to find all articles published in English before 2023 August 2, reporting the impact of outdoor air pollution on live birth outcomes in patients receiving ART. Relevant studies were identified and retrieved using the following MeSH terms: (air pollution OR atmospheric pollutants OR air contamination OR environmental pollution OR atmospheric pollution OR air quality OR PM2.5 OR fine particulate matter OR PM10 OR particulate matter OR SO2 OR NO2 OR CO OR O3) AND (in vitro fertilization OR IVF OR ICSI OR intracytoplasmic sperm injection OR assisted reproduction OR ART OR embryo transfer OR ET OR embryo implantation) AND (live birth OR pregnancy OR IVF outcomes OR live-birth rate OR clinical outcomes). All studies were stored and managed using EndNote Library (X8), and duplicates were identified and removed. In addition, we conducted a manual examination of the citations for each of the original research and critical review articles to find other eligible literatures.

Study selection and data extraction

Two authors conducted independent reviews of all the citations based on the title, abstract and full text to determine whether the article met the criteria for inclusion. Conflicts were resolved through consultation with a third review author.

Two authors independently extracted the data from each available study based on the predefined data collection table and were reviewed by the third author. The data collection table covers the following information for each study: title, author, year of publication, country in where the study was conducted, study design, population involved in the study, definition of outcomes, sample size, type and concentration of air pollutant, exposure time window, exposure variable, and effect estimates with 95%CIs. We have also referred to the supplementary materials of the original articles to ensure that we have all the necessary information.

Definition of outcomes

We defined live birth as the delivery of a viable infant after 28 wk of gestation.

Quality assessment

All included literatures were independently evaluated by two authors using the Newcastle–Ottawa Scale (NOS).21 The NOS evaluates the quality of cohort studies in three dimensions from eight items: population selection (4 items), comparability (1 item) and outcome or exposure (3 items). NOS scores ranged from 0 to 9, the higher the score shows the higher the research quality. Studies with a score greater than 7 were regarded as “high quality”; below 7 was categorized as “moderate quality” or “low quality.”

Data analysis

Some studies have suggested that RR could be used as a common measure of association. After referring to similar articles published previously, all estimates were reported as RRs with 95%CIs.22 To facilitate the comparison of effect sizes between different papers, we standardized the units of effect estimates for all studies into a 10 μg/m3 change in particulate matter (PM) concentrations or a 10 ppb change in NO2 and O3 concentrations before conducting the meta-analysis. We assumed a linear relationship between exposure and outcome, given that most air pollution epidemiology studies used generalized linear models to assess the association between air pollution exposure and health outcomes.23–26 To ensure comparability across studies, we standardized the correlation effect values using the following formula, which indicates the change in relative risk and its 95%CI per standardized increment in pollutant concentration.25

graphic file with name DmEquation1.gif

For the convenience of analysis, we divided all the air pollutant exposure periods in previous studies into three stages based on the important time nodes of the IVF cycle: period 1: before oocyte retrieval, period 2: spanning from oocyte retrieval to embryo transfer, and period 3: encompassing the time from embryo transfer to 14 days after embryo transfer.

The Q statistic and I2 statistic were employed to test for the heterogeneity of all included articles. We calculated the pooled effect sizes and their 95%CIs using the random-effect model if there was significant heterogeneity (I2 > 50%); otherwise, we adopted the fixed-effect model.

A funnel plot was used to assess publication bias, and we used Egger regression to assess the asymmetry of funnel plots to further explore potential publication bias. P < 0.05 indicates there may exist publication bias. Furthermore, a series of sensitivity analyses were carried out by omitting each study one by one to examine the reliability and stability of the analysis results.

All statistical analyses were performed by two authors using Stata SE 15.0 software (Stata Corp, College Station, TX, USA), and the consistency of all analyses was checked. Differences were considered statistically significant at P < 0.05.

Results

Description of studies

A comprehensive overview of the literature screening process is presented in Fig. 1. A total of 5,785 articles were retrieved in this study, of which 1,758 were duplicated. By screening titles and abstracts, 4,022 studies which did not meet inclusion criteria were ruled out. Through further full-text screening, five studies were ultimately confirmed to be included in our meta-analysis.

Fig. 1.

Fig. 1

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Flow diagram of literature selection in the meta-analysis.

The essential study characteristics for all included studies can be found in Table 1. All the research adopted a cohort design and examined the association between prolonged exposure to PM2.5 and live birth rate in female patients receiving ART treatment. Among them, three studies14,27,28 reported the effects of PM10 and NO2 exposure prior to oocyte retrieval on the live birth rates, and three studies14,19,27 assessed the impact of long-term O3 exposure on the live birth rate.

Table 1.

Characteristics of the studies included in the meta-analysis.

Author, year Country Study design Study period Sample size Inclusion criteria Exclusion criteria Air pollutants
Zhang et al, 2022 China Retrospective cohort 2015—2019 12,665 first embryo transfer cycles First cycles of IVF or ICSI Aged >45 years; used donor eggs; not undergo embryo transfer after oocyte retrieval; underwent frozen embryo transfer more than 180 days after oocyte retrieval; less than a year’s stay in the Delta region. PM2.5, PM10, NO2, O3
Boulet et al. 2019 USA Retrospective cohort 2010—2012 253,528 IVF cycles Noncancelled fresh, autologous IVF cycles Cycles used a gestational carrier; patients were non-US residents; with missing information on patient residential ZIP code and patients residing in locations where air quality data were not available. PM2.5, O3
Legro et al. 2010 USA Retrospective cohort 2000—2007 The first cycle of 7,403 patients undergoing IVF First cycles of IVF Multiple cycles PM2.5, PM10, NO2, O3
Quraishi et al. 2017 USA Retrospective cohort 2012—2013 7,681 IVF cycles First autologous cycle of IVF, cycles with the intent of a fresh embryo transfer, and cycles with a valid oocyte retrieval date. Multiple cycles PM2.5, PM10, NO2
Wang et al. 2023 China Prospective birth cohort 2015—2018 687 fresh embryo transfer cycles First IVF or ICSI cycle Multiple oocyte retrieval cycles; residential address was not provided for the assessment of PM2.5 PM2.5
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PM2.5, fine particulate matter; PM10, coarse particulate matter; NO2, nitrogen dioxide; O3, ozone; IVF, in vitro fertilization; ICSI, intracytoplasmic sperm injection.

Three studies19,27,28 were conducted in the United States and two14,29 in China. A total of 282,000 participants were included, with more than 90,000 live births. All eligible articles adjusted for potential confounders including patient age, body mass index, number of embryos transferred, season and year of IVF cycle start, parity, etc. All included studies were considered “high quality” according to the NOS score. Details of study quality assessments are provided in Table 2.

Table 2.

Quality assessment overview of the studies.

Cohort study Selection Comparability Outcome or exposure assessment NOS score
  Representativeness of the exposed cohort Selection of the nonexposed cohort Ascertainment of exposure Demonstration that outcomes of interest were not present at start of study Comparability of cohorts on the basis of the design or analysis Assessment of outcomes Was follow-up long enough for outcomes to occur Adequacy of follow up of cohorts  
Zhang et al. 2022 ★ ★ ★ ★ ★★ ★ ★ ★ 9
Boulet et al. 2019 ★ ★ ★ ★ ★★ ★ ★ ★ 9
Legro et al. 2010 ★ ★ ★ ★ ★ ★ ★ ★ 8
Quraishi et al. 2017 ★ ★ ★ ★ ★★ ★ ★ ★ 9
Wang et al. 2022 ★ ★ ★ ★ ★★ ★ ★ ★ 9
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NOS: Newcastle–Ottawa Scale.

The pooled effect estimates of air pollutant exposure on live birth

A total of five studies were included to quantitatively analyze the total effects of air pollutant exposure on the live birth rates of assisted reproductive technology patients. Based on the heterogeneity test results, I2 = 84.9%, P < 0.001, suggesting there was a high degree of heterogeneity in the included studies. As a result, we chose the random-effect model to assess the pooled effect sizes and their 95% CIs of PM2.5 exposure prior to oocyte retrieval on the live birth rate. According to the combined estimates yielding RRs, increased levels of PM2.5 exposure were associated with reduced probability of live birth (RR: 0.94, 95%CI: 0.92–0.97). We also investigated the consequences of exposure to various ambient air pollutants in the period before oocyte retrieval on live birth rates. The pooled estimates yielding RR showed that PM10 exposure was linked to decreased live birth probability (RR: 0.95, 95%CI: 0.92–0.97). In addition, there was no notable association between O3 exposure and live birth rate, while there was a negative association between NO2 exposure and live birth rate (RR: 0.92, 95%CI: 0.87–0.98) (Fig. 2). Only three studies19,27,29 have investigated the impact of air pollutant exposure on live birth rates during the period spanning from oocyte retrieval to embryo transfer and from embryo transfer to 14 days after embryo transfer. PM2.5 exposure in these two periods had no significant effect on the live birth rate, while O3 exposure from embryo transfer to 14 days after embryo transfer was considered to have a weak positive correlation with the live birth rate. The combined RR was 1.01 (95%CI: 1.01–1.02) (Figs 3 and 4).

Fig. 2.

Fig. 2

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Forest plot of air pollutant exposure during period 1 and live birth risk. (a) PM2.5, (b) PM10, (c) NO2, (d) O3. RR, relative risk; CI, confidence interval.

Fig. 3.

Fig. 3

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Forest plot of air pollutant exposure during period 2 and live birth risk. (a) PM2.5, (b) O3. RR, relative risk; CI, confidence interval.

Fig. 4.

Fig. 4

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Forest plot of air pollutant exposure during period 3 and live birth risk. (a) PM2.5, (b) O3. RR, relative risk; CI, confidence interval.

Sensitivity analysis

In this meta-analysis, we conducted sensitivity analysis by excluding each one of the studies. According to the results, for the pooled effect estimates of PM2.5, PM10, NO2 and O3 exposure on live birth rate in the period prior to oocyte retrieval, there was no significant change in the combined RRs values and their 95%CIs before and after excluding a study, indicating the reliability of our results that exposure to these pollutants was related with reduced live birth rates (Fig. 5a–d). In addition, since only two of the included studies19,27 explored the effects of O3 exposure in periods 2 and 3 on live birth rate, the pooled estimates and 95%CIs before and after omitting one of the two studies were significantly changed (Fig. 5e–h).

Fig. 5.

Fig. 5

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Sensitivity analyses on the association between air pollutant exposure and live birth risk. (a) PM2.5 exposure during period 1, (b) PM10 exposure during period 1, (c) NO2 exposure during period 1, (d) O3 exposure during period 1, (e) PM2.5 exposure during period 2, (f) O3 exposure during period 2, (g) PM2.5 exposure during period 3, (h) O3 exposure during period 3. CI, confidence interval.

Publication bias

The results from Egger’s linear regression test indicated that there was no obvious publication bias among the articles assessing the effects of PM2.5, PM10, O3 and NO2 (P = 0.924, P = 0.483, P = 0.134 and P = 0.357, respectively) exposure on live birth rate in the period prior to oocyte retrieval (Fig. 6a–d). However, there may be significant publication bias when assessing the effects of O3 exposure during oocyte retrieval to embryo transfer and from embryo transfer to 14 days after embryo transfer on the live birth rate (Fig. 6e–h). Then, we performed Duval and Tweedie trim and fill analysis, and the results showed that the adjusted effect was consistent with the original effect, indicating that our results were stable (Table S1, Fig. 7).

Fig. 6.

Fig. 6

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Egger’s regression of the effects of air pollutant exposure on live birth risks. (a) PM2.5 exposure during period 1, (b) PM10 exposure during period 1, (c) NO2 exposure during period 1, (d) O3 exposure during period 1, (e) PM2.5 exposure during period 2, (f) O3 exposure during period 2, (g) PM2.5 exposure during period 3, (h) O3 exposure during period 3. CI, confidence interval.

Fig. 7.

Fig. 7

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Tweedie’s and Duval’s trim and fill analysis of studies examining the association between O3 exposure and live birth rates. (a) O3 exposure during period 1, (b) O3 exposure during period 2.

Discussion

Ambient air pollution is increasingly recognized as a contributing factor to adverse pregnancy outcomes, including preterm birth, low birth weight, and stillbirth.30–33 Our study demonstrated a significant association between PM2.5, PM10, NO2 exposure and reduced live birth rates within the exposure window prior to oocyte retrieval (period 1). Our findings are supported by some studies. For example, a prospective cohort study conducted at the Boston Fertility Center revealed that PM2.5 exposure during the course of assisted reproductive therapy was correlated with a reduced live birth probability among individuals undergoing IVF treatment. Notably, this association was more significant before the stage of embryo transfer.34 Additionally, our results on PM10 are in line with the study which conducted in Shanghai indicated an association between outdoor PM10 exposure and reduced pregnancy and live birth rates in women undergoing ART.35 A similar retrospective cohort study involving 8,628 patients in Zhengzhou, China, also demonstrated a decrease in live birth rates with elevated PM10 exposure from early follicular stage to the pregnancy test period.36 For the air pollutant NO2, a previous study reported similar results that NO2 exposure before oocyte retrieval was associated with decreased clinical pregnancy probability.37 Furthermore, our results are consistent with the findings of Conforti A et al., who also documented a correlation between exposure to ambient NO2 during IVF cycles and a reduction in the live birth rate.26 The convergence of these multiple studies lends further support to the validity of our own outcomes.

Our results indicated the absence of a significant association between ambient O3 exposure and the live birth rate before oocyte retrieval. However, a subtle positive correlation was observed between O3 exposure and the live birth rate during two specific periods: from oocyte retrieval to embryo transfer and from embryo transfer to 14 days post-embryo transfer. These findings align with those of Zeng et al., who reported appositive association between O3 levels and clinical pregnancies.38 Similarly, a retrospective cross-sectional study conducted in Shijiazhuang, China, also reported that reduced O3 exposure from the preantral follicle stage to the antral follicle stage was associated with a decreased likelihood of clinical pregnancy.39 However, a retrospective cohort study conducted in France yielded the opposite insight that heightened O3 exposure during the period from oocyte retrieval to embryo transfer was related to a decreased probability of pregnancy.40 There are several possible explanations for these discrepancies between studies. First, the studies included in our meta-analysis were performed in China and the USA, whereas this study was conducted in France. Pollution levels in China and the USA were higher than those in France, and differences in exposure levels and population characteristics could be potential reasons for the differences between the findings. In addition, our meta-analysis is a summary of the results of the single-pollutant model as some included studies failed to evaluate the potential interactions between different pollutants. However, it should be noted that ozone is a secondary air pollutant formed by the reaction of primary pollutants in the atmosphere, and nitrogen oxides are the main precursor pollutants to form ozone. Considering the complex temporal and spatial interactions between ozone and nitrogen oxides, more research is needed to assess the impact of O3 exposure on ART outcomes.

On the basis of previous animal and human observational studies, we integrated the most frequently discussed mechanisms to elucidate the harmful effects of air pollution on assisted reproductive outcomes. These include oxidative stress, DNA damage, epigenetic modifications, metabolic changes, and systemic inflammation.41–43 In addition, recent studies have suggested that mitochondrial DNA damage and placental reprogramming due to endocrine disruption are potential biological pathways through which air pollution affects pregnancy outcomes.44,45

Our findings indicated a detrimental impact of air pollution exposure on the live birth rates in women undergoing ART. However, the study possesses several limitations that warrant consideration. First, our stringent inclusion and exclusion criteria restricted the incorporation of solely cohort studies, consequently yielding a relatively limited pool of eligible studies for eventual inclusion. Second, due to the constrained number of available studies, we were unable to delve into the origins of heterogeneity through meta-regression and subgroup analysis. Subsequently, we meticulously re-evaluated all incorporated studies in an attempt to identify potential factors contributing to heterogeneity in the comprehensive evaluation. Through a thorough examination of all encompassed studies, some factors might be the sources of heterogeneity, such as study populations, adjustment variables, geographical locations, evaluation method of pollutant exposure concentrations, and the origins and constituents of air pollutants. Finally, our meta-analysis did not further consider potential interactions between different pollutants, because some of the included studies used a multi-pollutant model, while others did not.

In conclusion, our meta-analysis revealed a statistically significant association between exposure to ambient air pollutants (PM2.5, PM10 and NO2) and a decreased live birth rate among patients undergoing ART. However, it is worth noting that O3 exposure had no significant effect on live birth rate. To establish more robust evidence, larger scale prospective epidemiological studies are needed, with a broader range of covariates and more comprehensive pollutant exposure assessments. Additionally, future research should focus on identifying the precise biological mechanisms underlying the effects of air pollution on ART outcomes. Investigating effective intervention strategies to mitigate the adverse impact of air pollution on reproductive health will be critical in advancing our understanding and improving ART outcomes. Furthermore, some researchers emphasize the importance of improving the reporting of adverse events and promoting “free-to-publish, free-to-access” research, irrespective of author’s funding or institutional affiliations, to facilitate the broader dissemination of evidence-based findings.46,47 Finally, further investigation into the biological mechanisms underlying the effects of air pollution on ART outcomes, as well as the development of intervention strategies to mitigate these effects, is essential to improve reproductive health and ART outcomes.

Supplementary Material

Supplementary_Materials_tfaf028
supplementary_materials_tfaf028.docx (12.7KB, docx)

Contributor Information

Juan Hu, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Huiqiu Zheng, Department of Child and Adolescent Health and Health Education, School of Public Health, Inner Mongolia Medical University, Jinshan development Zone, Hohhot, Inner Mongolia 010110, China.

Yan Wu, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Qing Yan, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Minghao Zhang, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Shikun Sun, Department of Cardiology, First Affiliated Hospital of Soochow University, 188 Shizi Street, Gusu District, Suzhou 215006, China.

Meidi Gong, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Rao Zheng, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Shujing Jia, Department of Ultrasound, Hohhot Maternal and Child Health Care Hospital, 33 Baotou Street, Yuquan District, Hohhot, Inner Mongolia 010110, China.

Rui Zhou, Department of Neonatology, Hohhot Maternal and Child Health Care Hospital, 33 Baotou Street, Yuquan District, Hohhot, Inner Mongolia 010110, China.

Jing Wu, Department of Toxicology, School of Public Health, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China; Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow University, 199 Renai Road, Suzhou Industrial Park, Suzhou 215123, China.

Author contributions

Qing Yan and Jing Wu contributed to the study conception and design. Material preparation, data collection and analysis were performed by Juan Hu, Qing Yan, Yan Wu, Minghao Zhang, Shikun Sun, Meidi Gong, Rao Zheng, Shujing Jia, and Rui Zhou. The first draft of the manuscript was written by Juan Hu and Qing Yan. Huiqiu Zheng and Jing Wu performed the manuscript revision, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported and funded by the National Natural Science Foundation of China (NSFC) (81803271), Laboratory Open Fund Project of Beijing Key Laboratory of Environmental Toxicology (2021hjd102), General Project of Inner Mongolia Medical University (YKD2023MS030).

Conflicts of interest. There are no conflicts of interest to declare.

References

  • 1. Manisalidis  I, Stavropoulou  E, Stavropoulos  A, Bezirtzoglou  E. Environmental and health impacts of air pollution: a review. Front Public Health. 2020:8:14. 10.3389/fpubh.2020.00014 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2. Nobles  CJ  et al.  Ambient air pollution and fetal growth restriction: physician diagnosis of fetal growth restriction versus population-based small-for-gestational age. Sci Total Environ. 2019:650:2641–2647. 10.1016/j.scitotenv.2018.09.362 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Grippo  A  et al.  Air pollution exposure during pregnancy and spontaneous abortion and stillbirth. Rev Environ Health. 2018:33:247–264. 10.1515/reveh-2017-0033 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4. Inoue  K  et al.  Air pollution and adverse pregnancy and birth outcomes: mediation analysis using Metabolomic profiles. Curr Environ Health Rep. 2020:7:231–242. 10.1007/s40572-020-00284-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Xue  T, Zhu  T. Association between fertility rate reduction and pre-gestational exposure to ambient fine particles in the United States, 2003-2011. Environ Int. 2018:121:955–962. 10.1016/j.envint.2018.10.013 [DOI] [PubMed] [Google Scholar]
  • 6. Xue  T, Zhu  T. Increment of ambient exposure to fine particles and the reduced human fertility rate in China, 2000-2010. Sci Total Environ. 2018:642:497–504. 10.1016/j.scitotenv.2018.06.075 [DOI] [PubMed] [Google Scholar]
  • 7. Inhorn  MC, Patrizio  P. Infertility around the globe: new thinking on gender, reproductive tec hnologies and global movements in the 21st century. Hum Reprod Update. 2015:21:411–426. 10.1093/humupd/dmv016 [DOI] [PubMed] [Google Scholar]
  • 8. Carson  SA, Kallen  AN. Diagnosis and Management of Infertility: a review. JAMA. 2021:326:65–76. 10.1001/jama.2021.4788 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Segal  TR, Giudice  LC. Systematic review of climate change effects on reproductive health. Fertil Steril. 2022:118:215–223. 10.1016/j.fertnstert.2022.06.005 [DOI] [PubMed] [Google Scholar]
  • 10. Tatum  M. China's fertility treatment boom. Lancet. 2020:396:1622–1623. 10.1016/S0140-6736(20)32475-2 [DOI] [PubMed] [Google Scholar]
  • 11. Zegers-Hochschild  F  et al.  International committee for monitoring assisted reproductive technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil Steril. 2009:92:1520–1524. 10.1016/j.fertnstert.2009.09.009 [DOI] [PubMed] [Google Scholar]
  • 12. Gaskins  AJ, Minguez-Alarcon  L, Williams  PL, et al.  Ambient air pollution and risk of pregnancy loss among women undergoing assisted reproduction. Environ Res. 2020:191:110201. 10.1016/j.envres.2020.110201 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13. Perin  PM, Maluf  M, Czeresnia  CE, Nicolosi Foltran Januário  DA, Nascimento Saldiva  PH. Effects of exposure to high levels of particulate air pollution during the follicular phase of the conception cycle on pregnancy outcome in couples undergoing in vitro fertilization and embryo transfer. Fertil Steril. 2010:93:301–303. 10.1016/j.fertnstert.2009.06.031 [DOI] [PubMed] [Google Scholar]
  • 14. Zhang  CY  et al.  Ambient air pollution on fecundity and live birth in women undergoing assisted reproductive technology in the Yangtze River Delta of China. Environ Int. 2022:162:107181. 10.1016/j.envint.2022.107181 [DOI] [PubMed] [Google Scholar]
  • 15. Choe  SA, Jun  YB, Lee  WS, Yoon  TK, Kim  SY. Association between ambient air pollution and pregnancy rate in women who underwent IVF. Hum Reprod. 2018:33:1071–1078. 10.1093/humrep/dey076 [DOI] [PubMed] [Google Scholar]
  • 16. Qiu  JH, Dong  M, Zho  FF, et al.  Associations between ambient air pollution and pregnancy rate in women who underwent in vitro fertilization in Shenyang. China Reprod Toxicol. 2019:89:130–135. 10.1016/j.reprotox.2019.07.005 [DOI] [PubMed] [Google Scholar]
  • 17. Dai  W  et al.  Ambient air pollutant exposure and in vitro fertilization treatment outcomes in Zhengzhou. China Ecotox Environ Safe. 2021:214:112060. 10.1016/j.ecoenv.2021.112060 [DOI] [PubMed] [Google Scholar]
  • 18. Wu  SS, Zhang  YS, Wu  XQ, et al.  Association between exposure to ambient air pollutants and the outcomes of in vitro fertilization treatment: a multicenter retrospective study. Environ Int. 2021:153:10. [DOI] [PubMed] [Google Scholar]
  • 19. Boulet  SL  et al.  Ambient air pollution and in vitro fertilization treatment outcomes. Hum Reprod. 2019:34:2036–2043. 10.1093/humrep/dez128 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Shamseer  L  et al.  Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. Br Med J. 2015:349:25. 10.1136/bmj.g7647 [DOI] [PubMed] [Google Scholar]
  • 21. Stang  A. Critical evaluation of the Newcastle-Ottawa scale for the assessment o f the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010:25:603–605. 10.1007/s10654-010-9491-z [DOI] [PubMed] [Google Scholar]
  • 22. Yu  SM  et al.  Different types of family history of stroke and stroke risk: results based on 655,552 individuals. J Stroke Cerebrovasc Dis. 2019:28:587–594. 10.1016/j.jstrokecerebrovasdis.2018.10.038 [DOI] [PubMed] [Google Scholar]
  • 23. Wang  X  et al.  Association between outdoor air pollution during in vitro culture and the outcomes of frozen-thawed embryo transfer. Hum Reprod. 2019:34:441–451. 10.1093/humrep/dey386 [DOI] [PubMed] [Google Scholar]
  • 24. Belotti  JT  et al.  Air pollution epidemiology: a simplified generalized linear model approach optimized by bio-inspired metaheuristics. Environ Res. 2020:191:110106. 10.1016/j.envres.2020.110106 [DOI] [PubMed] [Google Scholar]
  • 25. Shah  ASV  et al.  Global association of air pollution and heart failure: a systematic review and meta-analysis. Lancet. 2013:382:1039–1048. 10.1016/S0140-6736(13)60898-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Conforti  A  et al.  Air pollution and female fertility: a systematic review of literature. Reprod Biol Endocrinol. 2018:16:9. 10.1186/s12958-018-0433-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27. Legro  RS  et al.  Effect of air quality on assisted human reproduction. Hum Reprod. 2010:25:1317–1324. 10.1093/humrep/deq021 [DOI] [PubMed] [Google Scholar]
  • 28. Quraishi  SM  et al.  Exposure to ambient air pollution and live birth outcomes in women undergoing in virto fertilization. Fertil Steril. 2017:108:E89–E89. 10.1016/j.fertnstert.2017.07.277 [DOI] [Google Scholar]
  • 29. Wang  YF  et al.  Association between PM2.5 exposure and the outcomes of ART treatment: a prospective birth cohort study. Sci Total Environ. 2023:889:164099. 10.1016/j.scitotenv.2023.164099 [DOI] [PubMed] [Google Scholar]
  • 30. Proietti  E, Roosli  M, Frey  U, Latzin  P. Air pollution during pregnancy and neonatal outcome: a review. J Aerosol Med Pulm Drug Deliv. 2013:26:9–23. 10.1089/jamp.2011.0932 [DOI] [PubMed] [Google Scholar]
  • 31. Sram  RJ, Binkova  BB, Dejmek  J, Bobak  M. Ambient air pollution and pregnancy outcomes: a review of the literature. Environ Health Perspect. 2005:113:375–382. 10.1289/ehp.6362 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. Steinle  S  et al.  In utero exposure to particulate air pollution during pregnancy: impact on birth weight and health through the life course. Int J Environ Res Public Health. 2020:17:13. 10.3390/ijerph17238948 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Tan  YF  et al.  The associations between air pollution and adverse pregnancy outcomes in China. Adv Exp Med Biol. 2017:1017:181–214. 10.1007/978-981-10-5657-4_8 [DOI] [PubMed] [Google Scholar]
  • 34. Gaskins  AJ  et al.  Time-varying exposure to air pollution and outcomes of in vitro fertilization among couples from a fertility clinic. Environ Health Perspect. 2019:127:8. 10.1289/EHP4601 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Shi  WM  et al.  Association between ambient air pollution and pregnancy outcomes in patients undergoing in vitro fertilization in shanghai, China: a retrospective cohort study. Environ Int. 2021:148:106377. 10.1016/j.envint.2021.106377 [DOI] [PubMed] [Google Scholar]
  • 36. Liu  J  et al.  Associations between ambient air pollution and IVF outcomes in a heavily polluted city in China. Reprod Biomed Online. 2022:44:49–62. 10.1016/j.rbmo.2021.09.026 [DOI] [PubMed] [Google Scholar]
  • 37. Jin  HX  et al.  Effect of ambient air pollutants on in vitro fertilization-embryo transfer pregnancy outcome in Zhengzhou, China. Environ Toxicol Pharmacol. 2022:90:103807. 10.1016/j.etap.2021.103807 [DOI] [PubMed] [Google Scholar]
  • 38. Zeng  X, Jin  S, Chen  XL, Qiu  Y. Association between ambient air pollution and pregnancy outcomes in patients undergoing In vitro fertilization in Chengdu, China: a retrospective study. Environ Res. 2020:184:109304. 10.1016/j.envres.2020.109304 [DOI] [PubMed] [Google Scholar]
  • 39. Li  LP, Zhou  LX, Feng  TF, et al.  Ambient air pollution exposed during preantral-antral follicle transition stage was sensitive to associate with clinical pregnancy for women receiving IVF. Environ Pollut. 2020:265:9. [DOI] [PubMed] [Google Scholar]
  • 40. Tartaglia  M  et al.  Effects of air pollution on clinical pregnancy rates after in vitro fe rtilisation (IVF): a retrospective cohort study. BMJ Open. 2022:12:e062280. 10.1136/bmjopen-2022-062280 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. Moller  P  et al.  Oxidative stress and inflammation generated DNA damage by exposure to air pollution particles. Mutat Res-Rev Mutat Res. 2014:762:133–166. 10.1016/j.mrrev.2014.09.001 [DOI] [PubMed] [Google Scholar]
  • 42. Dai  YF, Huo  X, Cheng  ZH, Faas  MM, Xu  X. Early-life exposure to widespread environmental toxicants and maternal-fetal health risk: a focus on metabolomic biomarkers. Sci Total Environ. 2020:739:139626. 10.1016/j.scitotenv.2020.139626 [DOI] [PubMed] [Google Scholar]
  • 43. Saenen  ND  et al.  Air pollution-induced placental alterations: an interplay of oxidative stress, epigenetics, and the aging phenotype?  Clin Epigenetics. 2019:11:14. 10.1186/s13148-019-0688-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Li  Z  et al.  Impact of ambient PM2.5 on adverse birth outcome and potential molecular mechanism. Ecotoxicol Environ Saf. 2019:169:248–254. 10.1016/j.ecoenv.2018.10.109 [DOI] [PubMed] [Google Scholar]
  • 45. Street  ME, Bernasconi  S. Endocrine-disrupting Chemicals in Human Fetal Growth. Int J Mol Sci. 2020:21:1430. 10.3390/ijms21041430 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. Zhou  XL, Chen  C, Gao  Z, Qian  Z, Miao  J. Efficacy of traditional Chinese medicine containing hawthorn for hyperlipidemia: a systematic review and meta-analysis. Toxicol Res (Camb). 2024:13:tfae035. 10.1093/toxres/tfae035 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Vervoort  D, Ma  X, Bookholane  H. Equitable open access publishing: changing the financial power dynamics in academia. Glob Health Sci Pract. 2021:9:733–736. 10.9745/GHSP-D-21-00145 [DOI] [PMC free article] [PubMed] [Google Scholar]

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