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  • Research article
  • Open Access
  • Open Peer Review

Assisted reproductive technology and the risk of preeclampsia: an updated systematic review and meta-analysis

BMC Pregnancy and Childbirth201919:149

https://doi.org/10.1186/s12884-019-2291-x

  • Received: 11 January 2018
  • Accepted: 12 April 2019
  • Published:
Open Peer Review reports

Abstract

Background

The objective of this systematic review and meta-analyses was to assess the risk of preeclampsia among women who conceived with assisted reproductive technology (ART).

Methods

We searched the ISI Web of Knowledge, Medline/PubMed, Scopus, and Embase (from inception to May 2017) for English language articles using a list of key words. In addition, reference lists from identified studies and relevant review articles were also searched. Data extraction was performed by two authors, and the study quality was assessed using the Newcastle–Ottawa Scale. Random-effects model meta-analysis was applied to pool the relative risks (RR) across studies.

Results

A total of 48 studies (5 case-control studies and 43 cohort studies) were included in this meta-analysis. The Cochran Q test and I2 statistics revealed substantial heterogeneity (Q = 26,313.92, d.f. = 47, p < 0.001 and I2 = 99.8%). Meta-analysis showed a significant increase in preeclampsia in women who conceived by ART compared with those who conceived spontaneously (RR = 1.71, 95% CI = 1.11–2.62, p = 0.015).

Conclusions

The findings of this systematic review indicate that the use of ART treatment is associated with a 1.71-fold increase in preeclampsia.

Keywords

  • Assisted reproductive technology
  • Preeclampsia
  • Infertility
  • Meta-analysis
  • Systematic review

Background

Assisted reproductive technologies (ART) are used to treat infertility problems and contain methods in which oocyte and sperm are manipulated in vitro [1]. The use of ART has increased exponentially worldwide and is responsible for over than one million births annually [2, 3]. Having been treated by ART, the women who conceived had numerous adverse outcomes, both for themselves and the infants [3]. Previous studies have demonstrated that ART is associated with small for gestational age infants, preterm delivery, perinatal mortality, preeclampsia (PE), gestational diabetes, placenta previa, placental abruption, and cesarean delivery [4]. Of several adverse pregnancy consequences, hypertensive disorders affect 6–8% of all pregnancies through gestational hypertension and PE [5, 6]. In contrast to spontaneous pregnancy, pregnancies with ART are at an increased risk of PE [7]. It remained unclear whether either ART itself [in vitro fertilization (IVF), intracytoplasmic sperm injection (ICSI), intrauterine insemination (IUI), oocyte donation (OD), or embryo donation (ED)] or maternal risk factors associated with ART (that is, advanced maternal age, obesity, change of partner, longer interval between births, reduced smoking, and chronic hypertension) were related to increased risk of PE [7, 8]. Some studies have shown the probability of the taking of some medications during pregnancy, such as low-dose aspirin, [9] prevents for PE in high-risk women [1012]. Thus, identifying high-risk women during the early period of gestation will be worthwhile for the prevention and management of the pregnancy complications [13]. Finally, the lack of diagnostic criteria for pregnancy complications associated with hypertension, especially for PE, make the research in this field more complicated [14].

In the present paper, the authors conducted a comprehensive systematic review of ART procedures and PE. The aim of this review was to investigate whether ART mediated pregnancies (i.e., IUI, IVF, ICSI, OD, and ED) increased the incidence of PE in pregnancy compared with spontaneous pregnancies.

Methods

Search strategy

This meta-analysis was performed according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) checklist [15]. We conducted a systematic literature search in Medline/PubMed, Embase, Scopus, and the ISI Web of Knowledge from inception through June 2017 for studies examining the association between ART and PE. In addition, reference lists from all retrieved papers were checked. Table 1 provides more details about the search strategy.
Table 1

Search strategy for MEDLINE (MeSH, Medical Subject Headings)

1

Preeclampsia [Text Word])

2

Pre-Eclampsia [Text Word])

3

“Pre-Eclampsia” [Text Word])

4

“Pre-Eclampsia” [MeSH Terms]

5

1 OR 2 OR 3 OR 4

6

Reproductive Techniques, Assisted [Text Word]

7

Reproductive Techniques, Assisted [MeSH Terms]

8

6 OR 7

9

Cohort Studies [Text Word]

10

Cohort Studies [MeSH Terms]

11

Retrospective Studies [Text Word]

12

Retrospective Studies [MeSH Terms]

13

Prospective Studies [Text Word]

14

Prospective Studies [MeSH Terms]

15

Case-Control Studies [Text Word]

16

Case-Control Studies [MeSH Terms]

17

9 OR 10 OR 11 OR 12 OR 13 OR 14 OR 15 OR 16

18

5 AND 8 AND 17

Inclusion and exclusion criteria

We included published case-control studies and cohort studies evaluating the association between ART and PE risk. No geographic restrictions were used. The following types of studies were excluded: (a) non-English full-text studies, (b) animal studies, (c) repeated or overlapping studies, (d) reviews, meta-analysis and cross-sectional articles, case reports, editorials, and letters to the editor, (e) abstract-only publications or unpublished studies. There were five case-control studies added to the study. However, it was not substantially possible to estimate the relative risk (RR) with case-control design due to the fact that the marginal probabilities were not available; under the rare disease assumption, the odds ratio will be approximate the RR.

Outcome and exposure

In the present study, all types of ART treatments were considered as the interested exposure variable. Our outcome was PE defined as “elevated blood pressure (BP) (more than 140/100 mmHg) and proteinuria (0.3 g over 24 hours or more).”

Data extraction

Two authors (MM and SM) independently extracted the following data from all studies meeting the inclusion criteria: first author’s name, year of publication, location, study period, design, sample size, and study results. In addition, outcome data were extracted from each study in a 2 × 2 table, and the results were expressed as RR with their respective 95% confidence intervals (CIs) [9].

Quality assessment

Two authors (MM and SM) independently assessed the quality of studies using the Newcastle–Ottawa Scale (NOS) [16]. This scale assesses methodology in three domains: (a) selection of study groups, (b) comparability of groups, and (c) ascertainment of exposure and outcomes. Total score ranged from 0 to 9 with a score of ≥8 indicating high quality.

Statistical analysis

Statistical analysis was conducted using Stata version 13.0 (Stata Corp, College Station, TX, USA). The RR was used as the effect size of association across studies. The Cochran Q test and the I2 statistic were used to evaluate heterogeneity among studies [17]. Concerning the Cochrane Q test, P < 0.10 was deemed statistically significant for heterogeneity. The I2 statistic indicates the percentage of total variation across studies that is due to heterogeneity rather than chance and is classified as mild (25%), moderate (50%), or high (75%) [17]. The Galbraith plot was used to detect the potential sources of heterogeneity [18]. The pooled RR estimate and corresponding 95% CI were calculated by using the random-effect model incorporating between-study variability. The Begg’s rank correlation test, Egger’s weighted regression test, and visual inspection of a funnel plot were used to assess publication bias [19, 20]. All tests were two-tailed and a P value of < 0.05 was deemed statistically significant.

Results

Study selection

The process of study selection is illustrated in Fig. 1. A total of 1244 relevant papers were identified using diverse search strategies in four databases (113 from PubMed, 140 from Embase, 897 from Scopus, and 94 from Web of Knowledge) and three records of gray literature. After removing duplicates, 1057 papers remained, and 749 papers were deemed ineligible after title and abstract screening, and 308 relevant papers were considered for further screening through full-text reading. After the exclusion of all non-eligible studies (n = 260), a total of 48 studies (5 case-control studies and 43 cohort studies) were included in this meta-analysis.
Fig. 1
Fig. 1

Flow diagram of study process

Study characteristics

For each study, sample size, total number of ART and non-ART group, number of PE cases in each group, publication date, first author, target country, type of study, and participant mean age of each group were extracted. Cross-sectional studies and non-English studies were excluded from the meta-analysis. All of the primary studies were published between 1999 and 2017 and out of 48 studies, 11 were carried out in the United States, 11 in Asia, and 26 in Europe. The characteristics of studies considered in the meta-analysis are presented in Table 2.
Table 2

Characteristics of the primary studies included in the meta-analysis

Author

DOP

Country

Period

Design

PE in ART

ART group

PE in NART

NART group

Julie Hoy [42]

1999

Australia

1982–1995

Cohort

131

1552

399

7717

O.Salha [43]

1999

UK

1992–1997

Cohort

13

112

1

112

A.Geipel [44]

2001

Germany

1995–1999

Cohort

6

114

11

114

Anne Lynch [45]

2002

USA

1994–2000

Cohort

27

198

40

330

Syeda Zaib-un-Nisa [46]

2003

Emirates

1997–2001

Cohort

4

36

4

96

Pinborg [47]

2004

Denmark

1997

Cohort

71

870

49

566

Barbara Luke [48]

2004

USA

1990–2002

Cohort

25

228

24

725

Bengt Kallen [49]

2005

Sweden

1982–2001

Cohort

978

13,261

55,728

2,013,633

Fiona Thomson [50]

2005

Scotland

1989–1999

Cohort

70

1437

556

21,688

Sonia Hernandez-Diaz [51]

2006

USA & Canada

1998–2006

Cohort

18

349

115

4762

Erez [52]

2006

Israel

1988–2002

Cohort

51

292

193

2336

Prefumo [53]

2007

UK

NA

Case Control

1

31

1

62

Apantaku [24]

2008

UK

1999–2004

Cohort

6

88

7

88

Chen [54]

2009

Canada

2005

Cohort

34

1357

77

5190

Sun [55]

2009

Canada

2004–2007

Cohort

31

2118

112

8420

Morcel [56]

2010

France

2001–2005

Cohort

12

104

13

173

Miyake [57]

2010

Japan

2005–2007

Cohort

15

20

111

230

Suzuki [58]

2010

Japan

2000–2007

Cohort

4

64

9

87

Lehnen [28]

2011

Germany

2000–2009

Cohort

10

74

8

305

Yang [59]

2011

Korea

1995–2008

Cohort

9

67

22

143

Kuivasaari-Pirinen [60]

2012

Finland

1996–2007

Cohort

16

255

967

26,870

Bamberg [61]

2012

Germany

1998–2008

Cohort

14

426

24

813

Lubovnik [62]

2012

Slovenia

1997–2009

Case Control

55

246

126

477

Sazonova [63]

2012

Sweden

2002–2006

Cohort

520

11,292

15,984

571,914

Mohammed [64]

2012

Qatar

2002–2011

Cohort

27

145

30

175

Le Ray [65]

2012

France

2008–2010

Cohort

24

144

9

236

Emily Werder [66]

2013

USA

2002–2008

Cohort

45

215

62

232

Sara S. Malchau [67]

2013

Denmark

1995–2010

Cohort

1185

24,305

2519

56,022

Rocio Revello [68]

2013

Italy

2000–1010

Cohort

28

88

14

59

Sari Raisanen [69]

2013

Finland

2006–2010

Cohort

90

5647

3138

285,357

Alex Fong [70]

2014

USA

2009

Case Control

29

551

7487

406,334

Nathan S. Fox [71]

2014

USA

2005–2012

Case Control

61

376

15

137

Tandberg [39]

2014

Norway

1967–2009

Cohort

5516

8549

24,971

493,217

Tali Silberstein [72]

2014

Israel

NA

Cohort

113

1294

7889

171,513

Cagrı Arıoglu Aydın [23]

2015

Istanbul

2007–2010

Cohort

13

137

46

133

Anne-Maude Morency [73]

2015

Canada

2000–2013

Cohort

39

181

4

49

Robert Johnston [27]

2015

USA

2009

Cohort

29

551

7847

406,334

Malinda S. Lee [74]

2015

USA

2006–2008

Cohort

17

108

176

2284

Bay [75]

2016

Denmark

1999–2013

Cohort

2675

30,418

37,531

896,448

DoPierala [76]

2016

UK

1992–2009

Cohort

203

3188

2341

52,443

Nejdet [77]

2016

Sweden

2003–2012

Cohort

1156

27,084

27,912

999,804

Zhu [78]

2016

China

2006–2014

Cohort

98

2641

110

5282

Vikstrom [79]

2016

Sweden

1988–2012

Case Control

607

10,412

822

18,624

Ben-Yaakov [80]

2016

Israel

1988–2012

Cohort

378

4153

4471

95,138

Sun [81]

2016

China

2010–2014

Cohort

42

411

54

742

Valenzuela-Alcaraz [26]

2016

Spain

2004–2010

Cohort

6

488

0

200

Rizzo [82]

2016

Italy

2007–2014

Cohort

17

249

6

260

Guilbaud [25]

2017

France

2010–2014

Cohort

41

303

32

369

DOP Date of publication, PE Preeclampsia, ART Assisted Reproductive Technology, NART Non-Assisted Reproductive Technology

Quantitative data synthesis

A total of 156,246 ART cases (with 14,560 cases of PE) and 6,558,249 non-ART cases (with 202,064 cases of PE) were included in the analysis. Risk ratios and their 95% CIs were reported using the Mantel–Haenszel method. The relationship of ART and the risk of PE were estimated using the 48 primary included studies. The pooled estimate of RR in this meta-analysis revealed that ART was significantly associated with a higher risk of PE (pooled RR = 1.708, 95% CI = 1.111–2.624, z = 2.44, p = 0.015), that is, the PE risk in ART group was 1.687 times greater compared to the non-ART group (Fig. 2, Table 3).
Fig. 2
Fig. 2

Forest plot showing effect of ART on preeclampsia

Table 3

Summary of meta-analysis results and subgroups analysis

Groups

Studies

Test of association

Heterogeneity

RR (95% CI)

P value

Model

Z

Chi square

P value

I square

Total studies

48

1.71 (1.11–2.62)

0.015

Random

2.44

26,313.92

< 0.001

99.8%

Subgroup analyses

Study design

 Cohort

43

1.73 (1.10–2.72)

0.018

Random

2.36

25,159.19

< 0.001

99.8%

 Case control

5

1.46 (0.97–2.20)

0.070

Random

1.81

28.38

< 0.001

85.9%

Time Period

 1999–2010

18

1.64 (1.31–2.05)

< 0.001

Random

4.29

117.09

< 0.001

85.5%

 2010–2017

30

1.74 (0.97–3.09)

0.062

Random

1.87

25,671.51

< 0.001

99.9%

Region

 Asia

11

1.71 (1.53–1.92)

< 0.001

Random

9.38

17.12

0.072

41.6%

 Europe

26

1.74 (0.95–3.21)

0.075

Random

1.78

25,090.51

< 0.001

99.9%

 America

11

1.78 (1.31–2.41)

< 0.001

Random

3.70

52.30

< 0.001

80.9%

RR Relative Risk, CI Confidence Interval

Heterogeneity analysis

Chi-square analysis showed that there was substantial heterogeneity between primary studies (heterogeneity χ2 = 26,313.92, p < 0.001, I2 = 99.8%, and τ2 = 2.17). Therefore, we concluded that the random-effect model was used to pool the studies. To discover the source of heterogeneity, subgroup analysis was carried out on the basis of study design (case control and cohort), study region (United States, Asia, and Europe), and study period (1999–2010 and 2010–2017) (Figs. 3, 4 and 5, and Table 3). After subgroup analysis, heterogeneity across studies did not decrease effectively; therefore, all estimations of RR were made by the random-effect model.
Fig. 3
Fig. 3

Forest plot showing effect of ART on preeclampsia based on study design

Fig. 4
Fig. 4

Forest plot showing effect of ART on preeclampsia based on study period

Fig. 5
Fig. 5

Forest plot showing effect of ART on preeclampsia based on regions

Risk of publication bias

Both graphical and statistical assessments were performed to check for the presence of publication bias. On the basis of the asymmetrical funnel plot (Fig. 6) and Begg’s test (p = 0.001), there was evidence of publication bias in this study. Accordingly, we excluded non-English papers from the meta-analysis and this can lead to bias.
Fig. 6
Fig. 6

Funnel plots of studies examining the association between ART and preeclampsia

Discussion

This study aimed to evaluate whether several studies agree with the effect of ART on the presence of PE. In this meta-analysis, 6,714,495 cases were recruited (156,246 ART cases and 6,558,249 non-ART cases). To detect the risk of PE regarding the use of ART, the heterogeneity among the studies was assessed, and the appropriate statistical tool was applied. To increase the validity of the results, the risk of publication bias was checked. Analysis of the important subgroups, such as publication date, type of study, and region, was performed.

Similar to the results achieved from our study, most of the studies have introduced the use of ART as a significant risk factor for placental abruption, low and very low birth weight in infants, placenta previa, gestational hypertension, risk of cesarean section, and PE [21, 22]. However, not all the investigators agree with the adverse effect of ART on pregnancy outcomes [23, 24]. Most of previous studies have proven the important impact of using ART on PE [2528]. The positive association between ART and PE is well demonstrated by the included studies. Regarding the magnitude of the effect size, the pooled results from case-control studies were in compliance with those of cohort studies. However, in contrast to the cohort studies, the pooled RR from the case-control studies was not statistically significant. Moreover, the impact of ART on PE did not differ in two distinct periods of time (2010 as the cut-off point). Although consistent results were observed among different regions, the pooled RR from the European studies was not significant. Moreover, the effect size of the Asian and United States studies was higher than that of Europe.

We found that the use of ART was a significant risk factor for PE. The application of ART has increased across many countries around the world as a way to cope with infertility problems. The prevalence of using ART differs among countries. Annually, more than 1.5% of all births in the United States are the result of ART. The prevalence of PE is almost 10% in Africa and 15% in China [2932]. In addition, the prevalence of PE has an increasing slope. Numerous factors, including the use of ART, hypertension, diabetes, obesity, and early diagnosis problems, are responsible for the ascending trend of PE prevalence [30, 33]. The adverse outcomes after ART cause damage to body organs, such as the kidney and liver, through PE as well as maternal mortality, perinatal deaths, preterm birth, intrauterine growth restriction, bleeding problems, and fetal growth retardation [34, 35]. In addition to ART, other factors such as anti-phospholipid syndrome, previous PE, family history of PE, insulin-dependent diabetes, obesity, multiple pregnancies, and nulliparity can affect PE [36]. The mechanism in which ART affects PE is not well known. However, it has been argued that abnormal placentation can influence PE. In some ART procedures, the blood flow is compromised and is diminished, which is then followed by obstetric complications. Moreover, placental insufficiency is caused by the transfer of the conceptus into the uterine cavity and the impact of the altered hormonal environment in the endometrium where the development of the maternal–fetal interface can be influenced [37, 38]. It has been argued that ART may have epigenetic effects. The pregnancies from ART are associated with PE through oxidative stress. In addition, ART has several types of reproductive dysfunction with the same strength as miscarriages. Recurrent spontaneous miscarriages, along with infertility treatments, increase the risk of PE in comparison to those without treatment [39]. Nonetheless, the excess RR in the association between ART and PE can be caused by multiple factors, such as previous fertility complications, lifestyle, smoking habits, long inter-birth intervals, multiple pregnancy, and advanced maternal age [39]. However, there are many other causal factors associated with infertility itself in which the relationship between PE and ART can be argued.

Thomopoulos et al. assessed the risk of hypertensive disorders in pregnancy following ART using an overview of the studies conducted from 1978 to 2016 [40]. Their study included papers from PubMed and the Cochrane Collaboration Library databases with a total of 32 papers with PE as an outcome. The present meta-analysis has added primary studies from other databases such as Embase, Scopus, and ISI Web of Knowledge with a total number of 48 papers up to June 2017.

The controversy of using statistical tools to determine the magnitude of heterogeneity in meta-analysis has several potential causes, including sample size and number of the included studies, the period of time, the geographical patterns, the level of development, and the types of studies, etc. In this regard, a non-significant result from a chi-square test must not be taken as evidence of a lack of heterogeneity. Furthermore, the chi-square test is very powerful when many studies are included in a meta-analysis. The other statistical tool to detect heterogeneity, the I2 value, depends on the magnitude of the rates [41]. In our meta-analysis, the result of the chi-square test was confirmed by the I2 test. Except for a region of Asia, significant heterogeneities were observed among the pooled and subgroup RRs. The source of heterogeneities may be due to the diversity in the ethnic and cultural conditions and uneven development regions.

However, this study has some limitations. Almost every meta-analysis study deals with uncontrolled confounders. Researchers are not able to control the analysis for the confounders unless the proper information is presented by the original articles. To overcome this problem, “individual patient or participant data (IPD)” is suggested in which requires the detailed information and data-sets from every single original article and it is not applicable in most of the cases regarding that the authors (original articles) might not be interested to present their data and other potential reasons.

This systematic review has several limitations. First, the most important limitation for this study as for other systematic review is the lack of data for subgroup analysis based on type of pregnancy (singleton versus twin pregnancy) or for data analysis controlling for known confounders. Second, our study included only English full-text papers. However, globally published papers might present higher quality research compared with those of local origin.

Conclusion

The present systematic review and meta-analysis revealed that the use of ART increases the risk of PE considerably. More attention must be paid to Asia and the United States, where the association is stronger and significant.

Abbreviations

ART: 

Assisted Reproductive Technology

CI: 

Confidence Interval

PE: 

Preeclampsia

RR: 

Relative Risk

Declarations

Acknowledgements

Not applicable.

Funding

This research did not receive any specific grant from any agency in the public, commercial, or not-for-profit sector. Esmaeil Khedmati Morasae is part-funded by the National Institute for Health Research Collaboration for Leadership in Applied Health Research and Care, North West Coast (NIHR CLAHRC NWC). The views expressed are those of the author and not necessary those of the NHS, NIHR or Department of Health.

Availability of data and materials

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

Authors’ contributions

SM, ROS, and AAH conceived the study. MM, PA, BN, and AA collected the data. All of the authors contributed equally to the writing of the manuscript. AAH and EKM analyzed the data, and all authors revised the manuscript and approved the final version.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Epidemiology, School of Health, Arak University of Medical Sciences, Arak, Iran
(2)
Department of Epidemiology and Reproductive Health, Reproductive Epidemiology Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
(3)
Department of Biostatistics and Epidemiology, School of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
(4)
Institute of Psychology, Health, and Society, Department of Health Services Research, University of Liverpool, Liverpool, UK
(5)
School of Nursing and Midwifery, Guilan University of Medical Sciences, Rasht, Iran

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