Skip to main content
NCBI home page
PLOS One logoLink to PLOS One
. 2019 Mar 14;14(3):e0213784. doi: 10.1371/journal.pone.0213784

Mode of delivery and preterm birth in subsequent births: A systematic review and meta-analysis

Yinghui Zhang 1, Jie Zhou 2, Yubo Ma 3, Li Liu 4, Qing Xia 5, Dazhi Fan 6,*,#, Wen Ai 1,*,#
Editor: Abraham Salinas-Miranda7
PMCID: PMC6417656  PMID: 30870524

Abstract

Preterm birth continues to be an important problem in modern obstetrics and a large public health concern and is related to increased risk for neonatal morbidity and mortality. The aim of this study was to evaluate the data in the literature to determine the relationships between mode of delivery (cesarean section and vaginal birth) in the first pregnancy and the risk of subsequent preterm birth from a multi-year population based cohorts (PROSPERO registration number: 42018090788). Five electronic databases were searched. Observational studies that provided mode of delivery and subsequent preterm birth were eligible. Ten cohort studies, involving 10333501 women, were included in this study. Compared with vaginal delivery, women delivering by previous cesarean section had a significantly higher risk of preterm birth in subsequent births (RR 1.10, 95%CI 1.01–1.20). After adjusting confounding factors, there was still statistical significance (aRR 1.12, 95%CI 1.01–1.24). However, both before and after adjustment, there was no difference among very preterm birth (RR 1.14, 95%CI 0.90–1.43; aRR 1.16, 95%CI 0.80–1.68; respectively). To the best of our knowledge, this is the first systematic review and meta-analysis that suggests previous cesarean section could increase the risk of preterm birth in subsequent pregnancies. The result could provide policy makers, clinicians, and expectant parents to reduce the occurrence of unnecessary cesarean section.

Introduction

Preterm birth, defined as iatrogenic or spontaneous delivery before 37 completed gestational weeks, continues to be an important problem in modern obstetrics and remains a large public health concern. It affects 7.2% and 9.6% of pregnancies in China and United States, respectively [1, 2], and about 15 million pregnancies worldwide each year [3]. It is related to increased risk for neonatal morbidity and mortality [4, 5]. Most convincing are the findings that preterm birth is significantly associated with various adverse health outcomes, including low birth weight, visual and hearing impairment, neurodevelopmental impairment, lung disease, neonatal and infant death, and maternal adverse cardiovascular outcomes [6–9]. It is still a global priority to prevent preterm birth, although the exact pathogenesis is poorly understood [10]. Cesarean delivery rates varied markedly across worldwide and data showed that it increased in most countries during the past decade [11]. In China, it reported that 32.7% of births were delivered by cesarean between 2008 and 2014 [12]. Several investigations have demonstrated that previous cesarean delivery can elevate the risk of maternal complications including bleeding and intrauterine infection. More importantly, it can also increase the risk of adverse reproductive outcomes including ectopic pregnancy, uterine rupture, morbidly adherent placenta, hysterectomy, and preterm birth in subsequent pregnancies [13–15].

Over the past two decades, several cohort studies have investigated the association between previous mode of delivery and preterm birth in subsequent births. The positive association between cesarean section in the first pregnancy and subsequent preterm birth has been well documented [16–19]. However, other cohort studies [20, 21] showed that there didn’t seem to be enough evidence to come to a conclusion on the association between cesarean delivery in the first pregnancy and preterm birth in subsequent pregnancies. After adjusting for confounder factors, researchers [22, 23] even found that previous cesarean delivery could reduce the incidence of subsequent preterm birth. It is unclear whether previous cesarean section could increase the risk of subsequent preterm birth and to what extent compared with previous vaginal birth. Small cohort studies may be underpowered to distinguish the risk of previous cesarean section in subsequent pregnancies. Therefore, it is required a comprehensive study to clarify the risk of previous cesarean delivery in the subsequent pregnancies.

Through a systematic review and meta-analysis, our aim of this study was to evaluate the data in the literature to determine the relationships between mode of delivery (cesarean section and vaginal birth) in the first pregnancy and the risk of subsequent preterm birth from a multi-year population based retrospective cohort. Understanding the intertwined relationship between mode of delivery (cesarean section and vaginal birth) in the first pregnancy and the risk of subsequent preterm birth may remind policy makers, gynecologists and obstetricians, and expectant parents to reduce the occurrence of unnecessary cesarean section.

Materials and methods

We reported this systematic review and meta-analysis following the Preferred Reporting Item for Systematic Reviews and Meta-analyses statement [24]. Before data collecting, it was prospectively registered with the University of York Centre for Reviews and Dissemination International Prospective Register of Systematic Reviews (PROSPERO Identifier: CRD42018090788). It was designed a priori to define methods for searching terms, assessing the quality of included studies, collecting, extracting, and analyzing data in the review protocol.

Search strategy

In this systematic review and meta-analysis, published articles were searched with no language restrictions by two independent reviewers (LL and YM) in PubMed, Web of Science, Embase, Elsevier ScienceDirect and the Cochrane Library (updated on November 27, 2018). The search terms were “mode of delivery”, “cesarean delivery”, “cesarean section” “vaginal delivery”, “preterm birth”, and “preterm delivery”. A detailed search processes used for the PubMed was shown in S1 Text. Bibliographies of identified articles were also reviewed and searched manually for additional references.

Study selection

Observational studies (including cohort and case-control) assessing previous mode of delivery (cesarean delivery vs. vaginal delivery) and preterm birth in subsequent births were included. Only single pregnancy in our analyses was included, and twin pregnancy was excluded. First, based on the predetermined eligibility criteria, titles and abstracts of the potentially eligible articles were independently screened by YM and LL. Any duplicates were excluded. Then, potentially eligible studies were assessed and appraised full texts. Two authors (YM and LL) independently read the full text of the included studies and extracted the relevant data via a recognized data extraction form in Microsoft Excel software. Study characteristics, such as published journal and year, and first author’s name, study setting, such as period of enrollment and country, study design, study population characteristics, such as number of participants, gestational week, and outcomes such as risk estimates with corresponding confidence intervals, and confounding factors were extracted in each included study. Diagnosis and confirmation of preterm birth (before gestational week 37) and very preterm birth (before gestational week 32) were done according to the criteria of each study. If there were disagreement or uncertainty, consensus with the team members was used to resolve it.

Study quality assessment

To assess the risk of bias of observational studies, two authors (LL and QX) used the Newcastle Ottawa Scale (NOS) [25, 26] to assess it. Individual quality items were assessed using stars including selection, comparability, and outcome. The selection included four items. Each item was one star. The comparability included one item, and the item can gain two stars. The outcome included three items, and each item was also one star. Each study was got the number of stars and the maximum number of star was nine in one study. It was considered high quality if the studies gained six or more stars [27]. Consensus with the team members was used to resolve it if there were disagreement or uncertainty.

Statistical analysis

Relative risk (RR) with 95% confidence intervals (CI) was collected from the included articles. To examine the statistical heterogeneity, Higgins I2 statistics was used. According to I2-value, the statistical heterogeneity was divided into three categories: mild (< 25%), moderate (25–50%), and large (> 50%) [28, 29]. Meanwhile, Cochran’s Q statistic was also applied. Based on the heterogeneity, random- or fixed-effects meta-analysis was used to calculate the pooled effect value [30, 31]. To examine potential publication bias, Begg’s and Egger’s test were used. To assess whether study influenced the overall results, sensitivity analysis was performed. Two-sided P-value of 0.05 was considered statistically significant. Data analysis was completed using Stata 12.0 (Stata Corporation, College Station, TX, USA).

Results

Characteristics of included studies

The flow diagram, detailed process of inclusion and exclusion criteria (PRISMA template), was shown in Fig 1. Eight hundred and sixty-two unique citations were identified with the initial search. Six hundred and fifty-nine relevant citations were excluded after careful review the titles and abstracts. One hundred and three were selected for full-text review, and ninety-three of these were excluded, leaving 10 retrospective cohort studies [16, 17, 19–23, 32–34]. Table 1 presented the detailed characteristics and outcomes of these studies. The sample size ranged from 31573 to 8772705, and year of publication dated from 2001 to 2018. Total 10333501 women were included in these studies, and the women in previous cesarean section and vaginal delivery group were 2019506 and 8313995, respectively. Reported preterm births was 8506349 (rang from 27556 to 7297132). Four included studies [16, 19, 23, 32] reported the very preterm births. Eight of ten studies also reported the adjusted results [16, 17, 21–23, 32–34]. According to the Newcastle-Ottawa Scale, a total of 8.8 points were awarded for the ten included studies. Table 2 showed the detailed score of each article.

Fig 1. Flow chart for search and selection of studies for inclusion in this meta-analysis.

Fig 1

Open in a new tab

Table 1. Characteristics of the studies included in the meta-analysis.

Author, Year City/Country During Study Design Follow-up
(year)		 Sample Size
(CS group/VD group)		 Adjusted Confounding Factors NOS Score
Yasseen Iii AS, 2018 Ontario/Canada 2005–2012 Retrospective cohort 9.5 481531 (119983/361548) Adjusted for maternal age at birth, year and quarter of infant birth date, socioeconomic position measured using the material and social deprivation index, number of previous pregnancies, smoking during pregnancy, a history of preterm birth, and pre-existing diabetes and/or hypertension 9
Jackson S, 2012 /Denmark 1994–2010 Retrospective cohort 10 31573
(4030/27543)		 Controlled for age, body mass index, tobacco, alcohol, socioeconomic status 9
Salihu HM, 2011 Missouri/USA 1978–2005 Retrospective cohort 19.5 450141
(146443/303698)		 Adjustment for infant sex, maternal age, race, BMI, educational level, marital status, smoking and alcohol use during pregnancy, inter-pregnancy interval, adequacy of prenatal care and history of SGA or LGA, respectively 9
Huang X, 2011 /USA 1995–2002 Retrospective cohort 12.5 8772705
(1638456/7134249)		 Adjusting variables: mother age, race, education years, prenatal care in first trimester, marital status, child sex. 9
Wood SL, 2008 Alberta/Canada 1991–2004 Retrospective cohort 10.5 157929
(30110/127819)		 Unadjusted 8
Kennare R, 2007 South Australian/Australia 1998–2003 Retrospective cohort 6.5 36038
(8725/27313)		 Adjusted for age, indigenous status, patient type, smoking, pregnancy interval, hypertension, diabetes, antepartum hemorrhage, history of termination of pregnancy 9
Taylor LK, 2005 New South Wales/Australia 1998–2003 Retrospective cohort 4.5 136101
(25596/110505)		 Adjusted for maternal age; prior uterine curettage; smoking in pregnancy; health insurance status (public/private); ethnicity (Australian born non-Indigenous, Australian Indigenous, non-Australian born); socio-economic group; pre-existing diabetes; gestational diabetes; pre-existing hypertension; pregnancy-induced hypertension and infant sex. 9
Hemminki E, 2005 /Finland 1987–1998 Retrospective cohort 12.5 51220
(8534/42686)		 Adjusted for age, smoking, and infant sex at second birth 9
Smith GC, 2003 Scotland/UK 1980–1998 Retrospective cohort 14 120633
(17754/102879)		 Adjusted for maternal age, height, social deprivation quintile, and smoking status 9
Lydon-Rochelle M, 2001 Washington/USA 1987–1996 Retrospective cohort 9.5 95630
(19875/75755)		 Unadjusted 8
Open in a new tab

CS: Cesarean Section; NOS: Newcastle-Ottawa Scale; VD: Vaginal Delivery

Table 2. Quality assessment of included cohort studies using the Newcastle-Ottawa Scale.

Cohort studies
Author (year)		 Selection Comparability Outcome Total
quality
scores
Representativeness of
the exposed cohort		 Selection of the
non-exposed cohort		 Ascertainment
of exposure		 Incident
events		 Assessment
of outcome		 Length of
Follow-up		 Adequacy of
Follow-up of cohort
Yasseen Iii AS, 2018 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Jackson S, 2012 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Salihu HM, 2011 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Huang X, 2011 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Wood SL, 2008 ★ ★ ★ ★ ★ ★ ★ ★ 8
Kennare R, 2007 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Taylor LK, 2005 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Hemminki E, 2005 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Smith GC, 2003 ★ ★ ★ ★ ★ ★ ★ ★ ★ 9
Lydon-Rochelle M, 2001 ★ ★ ★ ★ ★ ★ ★ ★ 8
Open in a new tab

Meta-analysis

In the quantitative meta-analysis, ten retrospective cohort studies, involving 10333501 women, were included. Compared with vaginal group, women delivering by cesarean section in the last pregnancy had a significantly higher risk of preterm birth in subsequent births (RR 1.10, 95%CI 1.01–1.20, I2 = 98.8%; Fig 2). I2-value indicated that there was a high heterogeneity after pooling together. However, Begg’s and Egger’s tests showed there was no small-study effects (z = 0.09, p = 0.929; t = 1.50, p = 0.172) in the publication bias. Sensitivity analysis showed each single study did not influence the stability of the overall result.

Fig 2. Pooled risk estimates of mode of delivery for preterm birth in subsequent births (cesarean section vs. vaginal delivery).

Fig 2

Open in a new tab

Eight studies, including 10079942 women, reported the adjusted results. Increased risk of preterm birth was also found in subsequent births for women delivering by cesarean section in the last pregnancy (aRR 1.12, 95%CI 1.01–1.24, I2 = 99.1%; Fig 3). Begg’s and Egger’s tests also showed no significant publication bias in the adjusted results (z = -0.12, p = 0.999; t = 1.42, p = 0.205). Similar results indicated that the result was also stable.

Fig 3. Pooled adjusted risk estimates of mode of delivery for preterm birth in subsequent births (cesarean section vs. vaginal delivery).

Fig 3

Open in a new tab

Four studies, including 764741 women, involved very preterm birth. However, both before and after adjustment, there were no found to be statistically significant in the risk of subsequent very preterm birth for women who had delivered by cesarean section in the last pregnancy (RR 1.14, 95%CI 0.90–1.43, I2 = 93.8%; aRR 1.16, 95%CI 0.80–1.68, I2 = 95.0%; respectively). There were no existing publication bias before and after adjustment was performed (z = 1.02, p = 0.308; t = 3.56, p = 0.071 and z = 0.001, p = 0.999; t = 2.39, p = 0.252, respectively) using Begg’s and Egger’s tests.

Discussion

This is the first systematic review and meta-analysis, to our knowledge, that utilized a based population cohort study to focus to the relationships between mode of delivery (cesarean section vs. vaginal birth) in the first pregnancy and the risk of subsequent preterm birth. With published data from ten retrospective cohort studies, for more than ten million women, our pooled analysis revealed that, compared with primary vaginal birth, cesarean section in the first pregnancy increased the risk of preterm birth (aRR 1.12, 95%CI 1.01–1.24) in subsequent pregnancies.

The uterine structure and/or intrauterine microenvironment may be changed by previous cesarean section [17]. These changes can elevate the risk of subsequent preterm birth in the next pregnancies. However, the pathogenesis of preterm birth in subsequent births of women who suffered a cesarean delivery remains unclear, but multiple hypotheses exist.

One possible risk factor that cervical trauma in the second stage of labor or unintentional incision into the uterine cervix during the previous cesarean section could disrupt the cervical integrity. This damage can affect the function of the cervix, and further increase the risk of preterm birth in future pregnancies. This phenomenon has been described in pregnant women by a Japanese obstetrician Koyama S [35]. Meanwhile, it was also found that compared to women with vaginal births, women with a full-term second-stage cesarean delivery have an increased risk of preterm birth in the subsequent pregnancy, as seen in a large retrospective cohort study [36].

Another possible explanation for the subsequent increase in preterm birth may be the formation of uterine scar after previous cesarean section. It has been found that adhesions created by the previous cesarean section could reduce utero-placental function and disturb the position of blastocyst implantation. These could further create sub-optimal conditions for fetal development [37]. A retrospective cohort study and a meta-analysis simultaneously reported that uterine scar dehiscence in a previous pregnancy was a potential risk factor for preterm delivery [38, 39]. Additionally, a large multi-high-income country study has also documented that an association was observed between preterm birth and decreasing clinician-initiated obstetric interventions, such as labor induction or cesarean delivery [40].

Alternatively, underlying reasons, such as higher body mass index, advanced maternal age, or other maternal medical characteristics (e.g., diabetes mellitus, preeclampsia, etc.), which are indications for the cesarean section in the first pregnancy can also be an important cause of preterm birth in the next pregnancies [41–44]. From a center database, the researchers found that gestational weight gain is independently associated with preterm birth in Peruvian pregnant women [41]. A study from the Swedish Medical Birth Register also found that advanced maternal age is associated with an increased risk of preterm birth irrespective of parity, especially very preterm birth [42]. In addition, previous observational studies have respectively reported that women with a history of preeclampsia and diabetes mellitus in a prior pregnancy were significantly associated with higher odds of preterm birth in American [43, 44].

In this study, our results indicate that previous cesarean section could increase the risk of preterm birth (before gestational week 37) in subsequent birth, but we showed that previous cesarean section was not associated with very preterm birth (before gestational week 32) in subsequent birth. Although other confounders may be related to very preterm birth which are not known or addressed here, an important explanation could be that too few articles (only four articles) included very preterm birth. After all, small individual studies might be underpowered and easy to cause false negative to identify the risk of results in the analysis.

Interpregnancy interval can affect the outcome of the subsequent pregnancy. A previous study reported that a short interpregnancy interval may increase the risk for abnormally invasive placenta in subsequent pregnancy [37], which may influence outcomes of next pregnancy. In this study, we also want to explore the relationship between interpregnnacy interval and preterm birth in subsequent. However, none of the included studies provided the time interval between a previous cesarean section and the subsequent conception. Future systematic reviews could compare the effects of different interpregnancy interval on preterm birth in subsequent.

Strength of our systematic review is the access to a relatively large sample size, including more than ten million women, and the consistent results of both before and after adjustments factors are provided in the preterm birth in subsequent pregnancies. However, some limitations of the study merit attention. Firstly, only developed cohort studies, including data from multicenter and national registries, were included in this meta-analysis, and the differences in the reporting of preterm birth rate could have affected the quality of the reported data. We would hope that future studies would also consider the previous mode of delivery and preterm birth in subsequent pregnancies in developing countries. Secondly, there was a high heterogeneity among the studies evaluating the risk of preterm birth in the combined analysis. However, Begg’s test and Egger’s test for each site-specific analysis showed no publication bias or small-study effects. Third, although including more than ten million women included, there are only ten published articles that are suitable to include in this review. The number of articles included seems too small. Fourth, while the RR-value reached statistical significance, it is should also note that the small size suggest that the clinical significance is not very strong.

In conclusion, this is the first systematic review and meta-analysis to our knowledge that showed that previous cesarean section could increase the risk of preterm birth in subsequent pregnancies. The result could provide policy makers, clinicians, and expectant parents to reduce the occurrence of unnecessary cesarean section.

Supporting information

S1 Table. PRISMA checklist.

(DOC)

Click here for additional data file. (73KB, doc)
S1 Text. Search strategy.

(DOCX)

Click here for additional data file. (18KB, docx)

Acknowledgments

We appreciate the efforts of all the researchers whose articles were included in this study.

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

The authors received no specific funding for this work.

References

  • 1.Martin JA, Hamilton BE, Osterman MJ. Births in the United States, 2014. NCHS data brief. 2015;(216):1–8. . [PubMed] [Google Scholar]
  • 2.Guo T, Wang Y, Zhang H, Zhang Y, Zhao J, Wang Y, et al. The association between ambient temperature and the risk of preterm birth in China. The Science of the total environment. 2018;613–614:439–46. 10.1016/j.scitotenv.2017.09.104 . [DOI] [PubMed] [Google Scholar]
  • 3.Blencowe H, Cousens S, Chou D, Oestergaard M, Say L, Moller AB, et al. Born too soon: the global epidemiology of 15 million preterm births. Reproductive health. 2013;10 Suppl 1:S2 10.1186/1742-4755-10-S1-S2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Chang E. Preterm birth and the role of neuroprotection. Bmj. 2015;350:g6661 10.1136/bmj.g6661 . [DOI] [PubMed] [Google Scholar]
  • 5.Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science. 2014;345(6198):760–5. 10.1126/science.1251816 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Wu P, Gulati M, Kwok CS, Wong CW, Narain A, O'Brien S, et al. Preterm Delivery and Future Risk of Maternal Cardiovascular Disease: A Systematic Review and Meta-Analysis. Journal of the American Heart Association. 2018;7(2). 10.1161/JAHA.117.007809 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Minissian MB, Kilpatrick S, Eastwood JA, Robbins WA, Accortt EE, Wei J, et al. Association of Spontaneous Preterm Delivery and Future Maternal Cardiovascular Disease. Circulation. 2018;137(8):865–71. 10.1161/CIRCULATIONAHA.117.031403 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Kim SA, Lee SM, Kim BJ, Park CW, Park JS, Jun JK, et al. The risk of neonatal respiratory morbidity according to the etiology of late preterm delivery. Journal of perinatal medicine. 2017;45(1):129–34. 10.1515/jpm-2015-0191 . [DOI] [PubMed] [Google Scholar]
  • 9.Pimenta JM, Ebeling M, Montague TH, Beach KJ, Abell J, O'Shea MT, et al. A Retrospective Database Analysis of Neonatal Morbidities to Evaluate a Composite Endpoint for Use in Preterm Labor Clinical Trials. AJP reports. 2018;8(1):e25–e32. 10.1055/s-0038-1635097 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Margerison-Zilko CE, Talge NM, Holzman C. Preterm delivery trends by maternal race/ethnicity in the United States, 2006–2012. Annals of epidemiology. 2017;27(11):689–94 e4. 10.1016/j.annepidem.2017.10.005 . [DOI] [PubMed] [Google Scholar]
  • 11.Boatin AA, Schlotheuber A, Betran AP, Moller A-B, Barros AJD, Boerma T, et al. Within country inequalities in caesarean section rates: observational study of 72 low and middle income countries. Bmj. 2018:k55 10.1136/bmj.k55 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Li HT, Luo S, Trasande L, Hellerstein S, Kang C, Li JX, et al. Geographic Variations and Temporal Trends in Cesarean Delivery Rates in China, 2008–2014. Jama. 2017;317(1):69–76. 10.1001/jama.2016.18663 . [DOI] [PubMed] [Google Scholar]
  • 13.Lannon SM, Guthrie KA, Reed SD, Gammill HS. Mode of delivery at periviable gestational ages: impact on subsequent reproductive outcomes. Journal of perinatal medicine. 2013;41(6):691–7. 10.1515/jpm-2013-0023 . [DOI] [PubMed] [Google Scholar]
  • 14.Liang J, Mu Y, Li X, Tang W, Wang Y, Liu Z, et al. Relaxation of the one child policy and trends in caesarean section rates and birth outcomes in China between 2012 and 2016: observational study of nearly seven million health facility births. Bmj. 2018;360:k817 10.1136/bmj.k817 www.icmje.org/coi_disclosure.pdf (available on request from the corresponding author) and declare: no support from any organisation for the submitted work; no financial relationships with any organisations that might have an interest in the submitted work in the previous three years; no other relationships or activities that could appear to have influenced the submitted work. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.O'Neill SM, Agerbo E, Kenny LC, Henriksen TB, Kearney PM, Greene RA, et al. Cesarean section and rate of subsequent stillbirth, miscarriage, and ectopic pregnancy: a Danish register-based cohort study. PLoS medicine. 2014;11(7):e1001670 10.1371/journal.pmed.1001670 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Smith GC, Pell JP, Dobbie R. Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet. 2003;362(9398):1779–84. . [DOI] [PubMed] [Google Scholar]
  • 17.Yasseen Iii AS, Bassil K, Sprague A, Urquia M, Maguire JL. Late preterm birth and previous cesarean section: a population-based cohort study. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2018:1–8. 10.1080/14767058.2018.1438397 . [DOI] [PubMed] [Google Scholar]
  • 18.Wong LF, Wilkes J, Korgenski K, Varner MW, Manuck TA. Risk factors associated with preterm birth after a prior term delivery. BJOG: an international journal of obstetrics and gynaecology. 2016;123(11):1772–8. 10.1111/1471-0528.13683 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Wood SL, Chen S, Ross S, Sauve R. The risk of unexplained antepartum stillbirth in second pregnancies following caesarean section in the first pregnancy. BJOG: an international journal of obstetrics and gynaecology. 2008;115(6):726–31. 10.1111/j.1471-0528.2008.01705.x . [DOI] [PubMed] [Google Scholar]
  • 20.Lydon-Rochelle M, Holt VL, Easterling TR, Martin DP. First-birth cesarean and placental abruption or previa at second birth(1). Obstetrics and gynecology. 2001;97(5 Pt 1):765–9. . [PubMed] [Google Scholar]
  • 21.Huang X, Lei J, Tan H, Walker M, Zhou J, Wen SW. Cesarean delivery for first pregnancy and neonatal morbidity and mortality in second pregnancy. European journal of obstetrics, gynecology, and reproductive biology. 2011;158(2):204–8. 10.1016/j.ejogrb.2011.05.006 . [DOI] [PubMed] [Google Scholar]
  • 22.Jackson S, Fleege L, Fridman M, Gregory K, Zelop C, Olsen J. Morbidity following primary cesarean delivery in the Danish National Birth Cohort. American journal of obstetrics and gynecology. 2012;206(2):139 e1-5. 10.1016/j.ajog.2011.09.023 . [DOI] [PubMed] [Google Scholar]
  • 23.Salihu HM, Bowen CM, Wilson RE, Marty PJ. The impact of previous cesarean section on the success of future fetal programming pattern. Arch Gynecol Obstet. 2011;284(2):319–26. 10.1007/s00404-010-1665-0 . [DOI] [PubMed] [Google Scholar]
  • 24.Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. Bmj. 2009;339:b2700 10.1136/bmj.b2700 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Health Research Institute; 2011;http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. [Google Scholar]
  • 26.Fan D, Wu S, Liu L, Xia Q, Tian G, Wang W, et al. Prevalence of non-syndromic orofacial clefts: based on 15,094,978 Chinese perinatal infants. Oncotarget. 2018;9(17):13981–90. 10.18632/oncotarget.24238 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Yamada A, Komaki Y, Komaki F, Micic D, Zullow S, Sakuraba A. Risk of gastrointestinal cancers in patients with cystic fibrosis: a systematic review and meta-analysis. The Lancet Oncology. 2018;19(6):758–67. 10.1016/S1470-2045(18)30188-8 [DOI] [PubMed] [Google Scholar]
  • 28.Goldstein RF, Abell SK, Ranasinha S, Misso M, Boyle JA, Black MH, et al. Association of Gestational Weight Gain With Maternal and Infant Outcomes. Jama. 2017;317(21):2207 10.1001/jama.2017.3635 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Fan D, Li S, Wang W, Tian G, Liu L, Wu S, et al. Sexual dysfunction and mode of delivery in Chinese primiparous women: a systematic review and meta-analysis. BMC pregnancy and childbirth. 2017;17(1):408 10.1186/s12884-017-1583-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.DerSimonian R, Laird N. Meta-analysis in clinical trials revisited. Contemporary clinical trials. 2015;45(Pt A):139–45. 10.1016/j.cct.2015.09.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Fan D, Liu L, Xia Q, Wang W, Wu S, Tian G, et al. Female alcohol consumption and fecundability: a systematic review and dose-response meta-analysis. Scientific reports. 2017;7(1):13815 10.1038/s41598-017-14261-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Kennare R, Tucker G, Heard A, Chan A. Risks of adverse outcomes in the next birth after a first cesarean delivery. Obstetrics and gynecology. 2007;109(2 Pt 1):270–6. 10.1097/01.AOG.0000250469.23047.73 . [DOI] [PubMed] [Google Scholar]
  • 33.Hemminki E, Shelley J, Gissler M. Mode of delivery and problems in subsequent births: a register-based study from Finland. American journal of obstetrics and gynecology. 2005;193(1):169–77. 10.1016/j.ajog.2004.11.007 . [DOI] [PubMed] [Google Scholar]
  • 34.Taylor LK, Simpson JM, Roberts CL, Olive EC, Henderson-Smart DJ. Risk of complications in a second pregnancy following caesarean section in the first pregnancy: a population-based study. The Medical journal of Australia. 2005;183(10):515–9. . [DOI] [PubMed] [Google Scholar]
  • 35.Koyama S, Tomimatsu T, Kanagawa T, Sawada K, Tsutsui T, Kimura T. Cervical insufficiency following cesarean delivery after prolonged second stage of labor: experiences of two cases. The journal of obstetrics and gynaecology research. 2010;36(2):411–3. 10.1111/j.1447-0756.2009.01152.x . [DOI] [PubMed] [Google Scholar]
  • 36.Levine LD, Sammel MD, Hirshberg A, Elovitz MA, Srinivas SK. Does stage of labor at time of cesarean delivery affect risk of subsequent preterm birth? American journal of obstetrics and gynecology. 2015;212(3):360.e1-.e7. 10.1016/j.ajog.2014.09.035 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Timor-Tritsch IE, Monteagudo A, Cali G, Vintzileos A, Viscarello R, Al-Khan A, et al. Cesarean scar pregnancy is a precursor of morbidly adherent placenta. Ultrasound in obstetrics & gynecology: the official journal of the International Society of Ultrasound in Obstetrics and Gynecology. 2014;44(3):346–53. 10.1002/uog.13426 . [DOI] [PubMed] [Google Scholar]
  • 38.Klar M, Michels KB. Cesarean section and placental disorders in subsequent pregnancies—a meta-analysis. Journal of perinatal medicine. 2014;42(5):571–83. 10.1515/jpm-2013-0199 . [DOI] [PubMed] [Google Scholar]
  • 39.Baron J, Weintraub AY, Eshkoli T, Hershkovitz R, Sheiner E. The consequences of previous uterine scar dehiscence and cesarean delivery on subsequent births. International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics. 2014;126(2):120–2. 10.1016/j.ijgo.2014.02.022 . [DOI] [PubMed] [Google Scholar]
  • 40.Richards JL, Kramer MS, Deb-Rinker P, Rouleau J, Mortensen L, Gissler M, et al. Temporal Trends in Late Preterm and Early Term Birth Rates in 6 High-Income Countries in North America and Europe and Association With Clinician-Initiated Obstetric Interventions. Jama. 2016;316(4):410–9. 10.1001/jama.2016.9635 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Carnero AM, Mejia CR, Garcia PJ. Rate of gestational weight gain, pre-pregnancy body mass index and preterm birth subtypes: a retrospective cohort study from Peru. BJOG: an international journal of obstetrics and gynaecology. 2012;119(8):924–35. 10.1111/j.1471-0528.2012.03345.x [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Waldenstrom U, Cnattingius S, Vixner L, Norman M. Advanced maternal age increases the risk of very preterm birth, irrespective of parity: a population-based register study. BJOG: an international journal of obstetrics and gynaecology. 2017;124(8):1235–44. 10.1111/1471-0528.14368 . [DOI] [PubMed] [Google Scholar]
  • 43.Dorfman H, Srinath M, Rockhill K, Hogue C. The Association Between Diabetes Mellitus Among American Indian/Alaska Native Populations with Preterm Birth in Eight US States from 2004–2011. Maternal and child health journal. 2015;19(11):2419–28. 10.1007/s10995-015-1761-7 . [DOI] [PubMed] [Google Scholar]
  • 44.Connealy BD, Carreno CA, Kase BA, Hart LA, Blackwell SC, Sibai BM. A history of prior preeclampsia as a risk factor for preterm birth. American journal of perinatology. 2014;31(6):483–8. 10.1055/s-0033-1353439 . [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. PRISMA checklist.

(DOC)

Click here for additional data file. (73KB, doc)
S1 Text. Search strategy.

(DOCX)

Click here for additional data file. (18KB, docx)

Data Availability Statement

All relevant data are within the manuscript and its Supporting Information files.

Articles from PLoS ONE are provided here courtesy of PLOS

RESOURCES