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. 2021 Mar 31;9(6):e759–e772. doi: 10.1016/S2214-109X(21)00079-6

Effects of the COVID-19 pandemic on maternal and perinatal outcomes: a systematic review and meta-analysis

Barbara Chmielewska a, Imogen Barratt a, Rosemary Townsend a, Erkan Kalafat b,c, Jan van der Meulen d, Ipek Gurol-Urganci d, Pat O'Brien e,f, Edward Morris e,g, Tim Draycott e,h, Shakila Thangaratinam i, Kirsty Le Doare j, Shamez Ladhani j,l,m, Peter von Dadelszen n, Laura Magee n, Asma Khalil a,k,*
PMCID: PMC8012052  PMID: 33811827

Abstract

Background

The COVID-19 pandemic has had a profound impact on health-care systems and potentially on pregnancy outcomes, but no systematic synthesis of evidence of this effect has been undertaken. We aimed to assess the collective evidence on the effects on maternal, fetal, and neonatal outcomes of the pandemic.

Methods

We did a systematic review and meta-analysis of studies on the effects of the pandemic on maternal, fetal, and neonatal outcomes. We searched MEDLINE and Embase in accordance with PRISMA guidelines, from Jan 1, 2020, to Jan 8, 2021, for case-control studies, cohort studies, and brief reports comparing maternal and perinatal mortality, maternal morbidity, pregnancy complications, and intrapartum and neonatal outcomes before and during the pandemic. We also planned to record any additional maternal and offspring outcomes identified. Studies of solely SARS-CoV-2-infected pregnant individuals, as well as case reports, studies without comparison groups, narrative or systematic literature reviews, preprints, and studies reporting on overlapping populations were excluded. Quantitative meta-analysis was done for an outcome when more than one study presented relevant data. Random-effects estimate of the pooled odds ratio (OR) of each outcome were generated with use of the Mantel-Haenszel method. This review was registered with PROSPERO (CRD42020211753).

Findings

The search identified 3592 citations, of which 40 studies were included. We identified significant increases in stillbirth (pooled OR 1·28 [95% CI 1·07–1·54]; I2=63%; 12 studies, 168 295 pregnancies during and 198 993 before the pandemic) and maternal death (1·37 [1·22–1·53; I2=0%, two studies [both from low-income and middle-income countries], 1 237 018 and 2 224 859 pregnancies) during versus before the pandemic. Preterm births before 37 weeks' gestation were not significantly changed overall (0·94 [0·87–1·02]; I2=75%; 15 studies, 170 640 and 656 423 pregnancies) but were decreased in high-income countries (0·91 [0·84–0·99]; I2=63%; 12 studies, 159 987 and 635 118 pregnancies), where spontaneous preterm birth was also decreased (0·81 [0·67–0·97]; two studies, 4204 and 6818 pregnancies). Mean Edinburgh Postnatal Depression Scale scores were higher, indicating poorer mental health, during versus before the pandemic (pooled mean difference 0·42 [95% CI 0·02–0·81; three studies, 2330 and 6517 pregnancies). Surgically managed ectopic pregnancies were increased during the pandemic (OR 5·81 [2·16–15·6]; I2=26%; three studies, 37 and 272 pregnancies). No overall significant effects were identified for other outcomes included in the quantitative analysis: maternal gestational diabetes; hypertensive disorders of pregnancy; preterm birth before 34 weeks', 32 weeks', or 28 weeks' gestation; iatrogenic preterm birth; labour induction; modes of delivery (spontaneous vaginal delivery, caesarean section, or instrumental delivery); post-partum haemorrhage; neonatal death; low birthweight (<2500 g); neonatal intensive care unit admission; or Apgar score less than 7 at 5 min.

Interpretation

Global maternal and fetal outcomes have worsened during the COVID-19 pandemic, with an increase in maternal deaths, stillbirth, ruptured ectopic pregnancies, and maternal depression. Some outcomes show considerable disparity between high-resource and low-resource settings. There is an urgent need to prioritise safe, accessible, and equitable maternity care within the strategic response to this pandemic and in future health crises.

Funding

None.

Introduction

The SARS-CoV-2 pandemic has had profound effects on health-care systems, societal structures, and the world economy.1 The adverse effects of the COVID-19 pandemic on maternal and perinatal health are not limited to the morbidity and mortality caused directly by the disease itself. Nationwide lockdowns, disruption of health-care services, and fear of attending health-care facilities might also have affected the wellbeing of pregnant people and their babies.2, 3

Emerging evidence suggests that rates of stillbirth and preterm birth might have changed substantially during the pandemic.4, 5 A reduction in health-care-seeking behaviour, as well as reduced provision of maternity services, has been suggested as a possible cause.6 Robust estimates of the indirect maternal health effects of the pandemic can be derived from historical cohorts by examining the change in outcomes and calculating the excess event rate.7 This before–after approach applied to key pregnancy outcomes can be used to estimate the indirect effects of the COVID-19 pandemic.

Research in context.

Evidence before this study

Before conducting this study, we electronically searched MEDLINE and Embase from Jan 1, 2020, to Jan 8, 2021, with no language restriction, to identify any previous systematic reviews and meta-analyses. Search terms included stillbirth, perinatal mortality, maternal mortality and morbidity, preterm birth, obstetric complications, mode of delivery, and COVID-19. Large systematic reviews have consistently reported that pregnant individuals infected with SARS-CoV-2 are more likely to require intensive care treatment and experience preterm birth. Although individual studies have reported pandemic-associated changes in pregnancy outcomes in the general maternity population, particularly for preterm birth and stillbirth, no global synthesis of this kind has previously been reported.

Added value of this study

This review provides a comprehensive assessment of the global effects of the COVID-19 pandemic on maternal, fetal, birth, and neonatal outcomes. We identified significant increases in maternal and fetal mortality (particularly in low-income and middle-income countries [LMICs]), ruptured ectopic pregnancies, and maternal symptoms of depression. Moreover, we found a reduction in preterm birth in high-income countries during the pandemic epoch.

Implications of all the available evidence

The disruption caused by the COVID-19 pandemic has led to avoidable deaths of both mothers and babies. Policy makers and health-care leaders must urgently investigate robust strategies for preserving safe and respectful maternity care, even during the ongoing global emergency. Our findings highlight a disproportionate impact on LMICs. Immediate action is required to avoid rolling back decades of investment in reducing mother and infant mortality in low-resource settings. There is also an unprecedented opportunity to investigate the mechanisms underlying the observed reduction in preterm birth and generate novel preventive interventions.

We aimed to assess the collateral effects on maternal, fetal, and neonatal outcomes of the global COVID-19 pandemic.

Methods

Overview

We did a systematic review and meta-analysis of studies on the effects of the pandemic on maternal, fetal, and neonatal outcomes. The review was registered with PROSPERO (CRD42020211753) and reported according to PRISMA guidelines.8 The study protocol is available online.

Search strategy, selection criteria, and data extraction

We electronically searched the MEDLINE and Embase databases from Jan 1, 2020, to Jan 8, 2021. The search included relevant medical subject heading terms, keywords, and word variants for stillbirth, perinatal mortality, maternal mortality and morbidity, preterm birth, obstetric complications, mode of delivery, and COVID-19 (appendix p 4). No language restrictions were applied. One article, which was subsequently excluded, was translated from Mandarin.

Abstracts and potentially relevant full texts were reviewed independently by three authors (BC, IB, and RT) with any conflicts resolved by consensus. Case-control studies, cohort studies, and brief reports were eligible for inclusion. Case reports, studies without comparison groups, narrative or systematic literature reviews, preprint papers, and studies reporting on overlapping populations were excluded. Studies of only SARS-CoV-2-infected women were excluded.

Data were extracted with use of Covidence systematic review software (version 2, Veritas Health Innovation, Melbourne, VIC, Australia). The following data were extracted: author's name, publication date, study design, sampling period, study period, study population, and location. The total number of pregnant women and the sum of adverse events in each group were extracted for categorical outcomes (eg, stıllbirth, caesarean section). Mean, standard deviation, and the total number of pregnant women in each outcome group were extracted for outcomes reported on a continuous scale (Edinburgh Postnatal Depression Scale [EPDS] scores).

Outcomes of interest included maternal and perinatal mortality, maternal morbidity, pregnancy complications, and intrapartum and neonatal outcomes. We planned to record any additional maternal and offspring outcomes identified. Where papers described service configuration or resource-use changes without clinical outcomes, we excluded them from the analysis.

Pandemic mitigation response measures were extracted from the Oxford COVID-19 Government Response Tracker.9 We recorded the maximum restrictions implemented during the study timeframe. Quantitative assessment of the severity of mitigation measures was recorded according to the Government Response Stringency Index (GRSI) developed by the Blavatnik School of Government at the University of Oxford (Oxford, UK).9

Quality assessment

Each study was scored according to the Newcastle-Ottawa Scale10 independently by two assessors (BC, IB) on three broad characteristics: selection of study groups, comparability of groups, and ascertainment of the outcome of interest.

Statistical analysis

Quantitative meta-analysis was done for an outcome when more than one study presented relevant data. We excluded individual outcomes from studies reporting no adverse outcomes in one or both groups, and studies not satisfying the normality assumption for continuous variables. We divided studies according to World Bank classifications into high-income or low-income and middle-income contexts.

A random-effects estimate of the pooled odds of each outcome was generated with use of the Mantel-Haenszel method. Between-study heterogeneity was explored using the I 2 statistic, with substantial heterogeneity defined as an I 2 value greater than 50%. Meta-regression analyses were done for outcomes with substantial heterogeneity to investigate the relative contribution of the WHO Healthcare Efficiency Index11 and the stringency of lockdown measures (quantified with the GRSI).9 GRSI scores were scaled and regression coefficients corresponded to one standard unit change in the respective covariate. Positive regression coefficients indicate an increase in the effect size whereas negative coefficients show a decrease. We reported p values and the amount of accounted heterogeneity for each covariate. Potential publication bias was assessed with Egger's test and funnel plots for visual inspection when sufficient studies (n>10) were available.

Analyses were done with R software (version 4.0.2).

Role of the funding source

There was no funding source for this study.

Results

Of 3592 abstracts screened, 192 were relevant for full-text review and 40 met the inclusion criteria for systematic review (figure 1 ).4, 5, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49 A list of excluded studies with reasons for exclusion is provided in the appendix (p 6). Reporting on resource use or service reconfiguration outcomes is summarised in the appendix (p 27). Of the 40 included studies, 31 for which comparable outcomes were also reported in at least one other study were included in the meta-analysis.4, 12, 14, 15, 16, 17, 18, 19, 20, 21, 24, 25, 26, 27, 28, 30, 31, 32, 33, 34, 37, 38, 40, 42, 45, 46, 47, 48, 49 Table 1 shows the characteristics of the 40 included studies, all of which used a historical cohort design. 17 countries were represented, with substantial variation in pandemic mitigation measures among countries. No study reported data from countries in the lowest WHO Healthcare Efficiency Index quartile, and the majority (28 studies)4, 5, 12, 14, 16, 17, 19, 20, 22, 23, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 39, 40, 42, 44, 45, 46, 48, 49 reported data from countries in the highest quartile (table 2 ). 21 of the 31 studies included in the quantitative analysis were from high-income countries (HICs) according to the World Bank classification.4, 12, 14, 16, 17, 19, 20, 23, 28, 30, 31, 32, 33, 34, 42, 45, 46, 49 The reported outcomes and outcome measures are listed with the relevant studies in the appendix (p 31).

Figure 1.

Figure 1

PRISMA flow chart

Table 1.

Characteristics of included studies

Country Study population Reported outcome categories Sample size of exposed cohort Total sample size Data collection period
Newcastle-Ottawa Scale score
Pandemic group Control group
Ayaz et al, 202022 Turkey Single centre Maternal anxiety and depression 63 NR April 12 to May 27, 2020 June 1, 2018, to April 11, 2020 6
Been et al, 20205 Netherlands National Preterm birth 56 720 1 599 547 March 9 to July 16, 2020 Oct 9, 2010, to March 8, 2020 9
Berghella et al, 202033 USA Single centre Overall preterm birth, spontaneous preterm birth, iatrogenic preterm birth, caesarean section, vaginal delivery, perinatal death 1197 2108 March 1 to July 31, 2020 March 1 to July 31, 2019 8
Berthelot et al, 202044 Canada Regional (Quebec province) Maternal emotions and concerns 1258 1754 April 2 to April 23, 2020 April 1, 2018, to March 1, 2020 6
Bhatia et al, 202045 UK Regional (northwest England) Caesarean rate 8381 17 424 April 1 to July 1, 2020 Similar period in 2019 7
Bornstein et al, 202046 USA Multicentre Vaginal delivery, caesarean section 5877 11 770 March 15 to June 20, 2020 Dec 8, 2019, to March 14, 2020 7
Caniglia et al, 202047 Botswana National Stillbirth, preterm birth, neonatal death 10751 68 448 April 3 to July 20, 2020 Annual matched periods, 2017–19 9
Casadio et al, 202048 Italy Single centre Ectopic pregnancy 9 201 March 1 to April 30, 2020 Jan 1, 2014, to Feb 29, 2020 7
De Curtis et al, 202049 Italy Single centre Preterm birth, caesarean section, stillbirth 7755 16 808 March 1 to May 31, 2020 March 1 to May 31, 2019 6
Dell'Utri et al, 202012 Italy Single centre Ectopic pregnancy, vaginal delivery, induction of labour, stillbirth 3647 9291 Feb 23 to June 24, 2020 Feb 23 to June 24, 2019 7
Goyal et al, 202113 India Single centre Maternal death 633 1749 April 1 to Aug 31, 2020 Oct 1, 2019, to Feb 29, 2020 8
Greene et al, 202014 USA Single centre Vaginal delivery, caesarean section, instrumental delivery, NICU admission, 5-min Apgar score, cord blood gas, preterm birth 920 1936 March 1 to April 30, 2020 Jan 1 to Feb 29, 2020 9
Gu et al, 202015 China Single centre Gestational hypertension, gestational diabetes, preterm birth, caesarean section, vaginal delivery, stillbirth, 5-min Apgar score, NICU admission, maternal anxiety 271 582 Jan 1 to Feb 29, 2020 Jan 1 to Feb 28, 2019 5
Handley et al, 202116 USA Multicentre Stillbirth, overall preterm birth, spontaneous preterm birth, iatrogenic preterm birth 3007 8914 March 1 to June 30, 2020 Annual matched periods, 2018–19 9
Hedermann et al, 202117 Denmark National Preterm birth 5162 31 180 March 12 to April 14, 2020 Annual matched periods, 2015–19 7
Hui et al, 202018 Hong Kong Single centre Vaginal delivery, caesarean section, instrumental delivery, post-partum depression 954 4531 Jan 5 to April 30, 2020 Jan 1, 2019, to Jan 4, 2020 5
Justman et al, 202019 Israel Single centre Gestational hypertension, gestational diabetes, induction of labour, caesarean section, instrumental delivery, preterm birth, 5-min Apgar score, NICU admission, stillbirth, post-partum haemorrhage 610 1352 March 1 to April 30, 2020 March 1 to April 30, 2019 9
Kasuga et al, 202020 Japan Single centre Preterm birth, gestational hypertension 153 713 April 1 to June 30, 2020 Annual matched periods, 2017–19 7
Kc et al, 202021 Nepal Multicentre Induction of labour, caesarean section, preterm birth, stillbirth, neonatal death 7165 20 354 March 21 to May 30, 2020 Jan 1 to March 20, 2020 9
Khalil et al, 20204 UK Single centre Gestational hypertension, gestational diabetes, stillbirth, preterm birth, caesarean section, NICU admission 1718 3399 Feb 1 to June 14, 2020 Oct 1, 2019, to Jan 31, 2020 7
Kugelman et al, 202023 Israel Single centre NICU admission, umbilical cord blood pH, 5-min Apgar score 398 942 March 15 to April 12, 2020 March 15 to April 12, 2019 7
Kumar et al, 202124 India Single centre Stillbirth 3610 9771 March 1 to Sept 30, 2020 March 1 to Sept 30, 2019 9
Kumari et al, 202025 India Multicentre Caesarean section, maternal death, stillbirth 3527 9736 March 25 to June 2, 2020 Jan 15 to March 24, 2020 5
Li et al, 202026 China Single centre Preterm birth, caesarean section 3432 10 591 Jan 23 to March 24, 2020 Jan 1, 2019, to Jan 22, 2020 9
Lumbreras-Marquez et al, 202027 Mexico National Maternal death, post-partum haemorrhage 523* 7747* Jan 1 to Aug 9, 2020 2011–19 7
Main et al, 202028 USA Regional (California) Preterm birth 132 853 71 3567 April 1 to July 31, 2020 Annual matched periods, 2016–19 9
Matvienko-Sikar et al, 202029 Ireland Single centre Pregnancy-specific stress 235 445 June 16 to July 17, 2020 May 1, 2019, to Feb 29, 2020 5
McDonnell et al, 202030 Ireland Single centre Preterm birth, stillbirth, neonatal death, caesarean section, instrumental delivery, induction of labour, gestational hypertension, post-partum haemorrhage 2488 4309 April 1 to July 31, 2020 Annual matched periods, 2018–19 8
Meyer et al, 202031 Israel Single centre Induction of labour, preterm birth, vaginal delivery, instrumental delivery, caesarean section, stillbirth, 5-min Apgar score, NICU admission 2594 34 022 March 20 to June 27, 2020 Annual matched periods, 2011–19 7
Mor et al, 202032 Israel Single centre Gestational diabetes, gestational hypertension, stillbirth, preterm birth, vaginal delivery, caesarean section, instrumental delivery, induction of labour, birthweight, 5-min Apgar score, umbilical cord blood pH, NICU admission 1556 6120 Feb 21 to April 30, 2020 Annual matched periods, 2017–19 7
Pariente et al, 202034 Israel Single centre Gestational diabetes, gestational hypertension, post-partum depression, maternal depression and suicidal ideation 223 346 March 18 to April 29, 2020 Nov 1, 2016, to April 30, 2017 5
Philip et al, 202035 Ireland Regional Birthweight 1381 30 705 Jan 1 to April 30, 2020 Annual matched periods, 2001–19 7
Silverman et al, 202036 USA Single centre Postpartum depression 155 485 March 12 to June 12, 2020 Feb 2 to March 11, 2020 6
Stowe et al, 202137 UK National Stillbirth 131 218 270 963 April 1 to June 30, 2020 April 1, 2019, to June 30, 2020 7
Sun et al, 202038 Brazil Single centre Preterm birth, vaginal delivery, instrumental delivery, caesarean section, 5-min Apgar score 40 81 March 11 to June 11, 2020 March 11 to June 11, 2019 6
Suzuki et al, 202039 Japan Single centre Maternal depression and anxiety 117 251 March 11 to April 13, 2020 March 9 to April 11, 2019 8
Werner et al, 202040 USA Single centre Ectopic pregnancy 12 63 March 15 to May 17, 2020 2019–20 interval before pandemic 7
Wu et al, 202041 China Regional (ten provinces in China) Postpartum depression, maternal anxiety 1285 4124 Jan 21 to Feb 9, 2020 Jan 1 to Jan 20, 2020 9
Xie et al, 202143 China Regional (Zhejiang) Maternal depression, maternal anxiety 689 3348 Jan 1 to Aug 31, 2020 March 1 to Dec 31, 2019 5
Zanardo et al, 202042 Italy Single centre Postpartum depression 91 192 March 8 to May 3, 2020 March 8 to May 3, 2019 7

NR=not reported. NICU=neonatal intensive care unit.

*

Maternal deaths.

Table 2.

Summary of findings of included studies

Government Response Stringency Index12 WHO Healthcare Efficiency Index14 Outcomes
Statistically significant increase during pandemic Statistically significant decrease during pandemic Statistically non-significant change
Ayaz et al, 202022 77·78 0·734 Maternal anxiety (IDAS II score), moderate and severe maternal anxiety (BAI score) No maternal anxiety (BAI score), mild maternal anxiety (BAI score) None
Been et al, 20205 79·63 0·928 None Preterm birth before 37 weeks' gestation post mitigation measures introduced on March 9 Preterm birth before 37 weeks' gestation post mitigation measures introduced on March 15–23
Berghella et al, 202033 72·69 0·838 None Overall preterm birth before 37 weeks' gestation, preterm birth before 34 weeks' gestation, preterm birth before 28 weeks' gestation Caesarean section, vaginal delivery, stillbirth, iatrogenic preterm birth before 37 weeks' gestation, spontaneous preterm birth before 37 weeks' gestation
Berthelot et al, 202044 74·54 0·881 Depressive and anxiety symptoms, dissociative symptoms, symptoms of post-traumatic stress disorder, negative affectivity Positive affectivity None
Bhatia et al, 202045 79·63 0·925 Caesarean section None None
Bornstein et al, 202046 72·69 0·838 None None Caesarean section, vaginal delivery
Caniglia et al, 202047 86·11 0·388 None Preterm birth before 37 weeks' gestation, preterm birth before 32 weeks' gestation Neonatal death, stillbirth
Casadio et al, 202048 93·52 0·991 Ruptured ectopic pregnancy (needing surgical intervention) None None
De Curtis et al, 202049 93·52 0·991 Stillbirth Preterm birth before 37 weeks' gestation Caesarean section
Dell'Utri et al, 202012 75·46 0·991 Stillbirth, induction of labour None Vaginal delivery, surgical management of ectopic pregnancy
Goyal et al, 202113 100·0 0·617 None None Maternal death
Greene et al, 202014 72·69 0·838 None None Vaginal delivery, caesarean section, instrumental delivery, NICU admission, 5-min Apgar score <7, umbilical cord blood pH
Gu et al, 202015 81·02 0·485 Gestational hypertension, gestational diabetes None Caesarean section, stillbirth, gestational diabetes, vaginal delivery, NICU admission, mean Apgar score
Handley et al, 202116 72·69 0·838 None None Stillbirth, preterm birth before 37 weeks' gestation, spontaneous preterm birth, iatrogenic preterm birth
Hedermann et al, 202117 72·22 0·862 Preterm birth before 28 weeks' gestation None Preterm birth at 28–32 weeks' gestation, preterm birth at 32–36 weeks' gestation
Hui et al, 202018 66·67 0·485 Postnatal depression (EPDS score ≥10 1 day after delivery) None Vaginal delivery, caesarean section, instrumental delivery, postnatal depression (EPDS score)
Justman et al, 202019 94·44 0·884 Gestational diabetes, gestational hypertension None Caesarean section, induction of labour, instrumental delivery, stillbirth, preterm birth before 37 weeks' gestation and before 32 weeks' gestation, post-partum haemorrhage, 5-min Apgar score <7, umbilical cord blood pH, NICU admission
Kasuga et al, 202020 47·22 0·957 None Gestational hypertension, preterm birth before 27 weeks' gestation Preterm birth (gestation not specified)
Kc et al, 202021 96·3 0·457 Caesarean section, induction of labour, stillbirth, neonatal death, preterm birth before 37 weeks' gestation None Vaginal delivery, birthweight <2·5 kg
Khalil et al, 20204 79·63 0·925 Stillbirth Gestational hypertension Caesarean section, preterm birth before 37 weeks' gestation and before 34 weeks' gestation, gestational diabetes, NICU admission
Kugelman et al, 202023 94·44 0·884 None None NICU admission, umbilical cord blood pH <7·1, 5-min Apgar score <7
Kumar et al, 202124 100·0 0·617 Stillbirth None None
Kumari et al, 202025 100·0 0·617 Caesarean section, maternal death, stillbirth None None
Li et al, 202026 81·94 0·485 Caesarean section None None
Lumbreras-Marquez et al, 202027 82·41 0·755 No statistical analysis done No statistical analysis done No statistical analysis done
Main et al, 202028 72·69 0·838 Preterm birth at 28–32 weeks' gestation None Preterm birth before 28 weeks' gestation, at 32–37 weeks' gestation, before 37 weeks' gestation (combined)
Matvienko-Sikar et al, 202029 90·74 0·924 None None Pregnancy-specific stress (NuPDQ score)
McDonnell et al, 202030 90·74 0·924 None None Birthweight <2·5 kg, stillbirth, neonatal death (early and late), caesarean section, instrumental delivery (vacuum and forceps), vaginal delivery, induction of labour, gestational hypertension, pre-eclampsia, post-partum haemorrhage, preterm birth before 37 weeks' gestation, preterm birth before 26 weeks' gestation
Meyer et al, 202031 94·44 0·884 None Preterm birth before 34 weeks' gestation, NICU admission Induction of labour, preterm birth before 37 weeks' gestation and before 32 weeks' gestation, vaginal delivery, instrumental delivery, caesarean section, stillbirth, 5-min Apgar score <7
Mor et al, 202032 94·44 0·884 Stillbirth, induction of labour, 5-min Apgar score <7 None Gestational hypertension, gestational diabetes, vaginal delivery, instrumental delivery, caesarean section, umbilical artery pH <7·1, NICU admission
Pariente et al, 202034 94·44 0·884 None Postpartum depression (EPDS score) Gestational hypertension, pre-eclampsia, maternal suicidal ideations (EPDS question 10 positive)
Philip et al, 202035 90·74 0·924 None Very low birthweight (<1500 g) Extremely low birthweight (<1000 g)
Silverman et al, 202036 72·69 0·838 None Postnatal depression (EPDS score) None
Stowe et al, 202137 79·63 0·925 None None Stillbirths
Sun et al, 202038 81·02 0·573 No statistical analysis done No statistical analysis done No statistical analysis done
Suzuki et al, 202039 47·22 0·957 Maternal depression (Whooley questions) None None
Werner et al, 202040 72·69 0·838 No statistical analysis done No statistical analysis done No statistical analysis done
Wu et al, 202041 77·31 0·485 Postnatal depression (EPDS score), maternal anxiety (EPDS-3A score) None None
Xie et al, 202143 81·94 0·485 Maternal depression, maternal anxiety (SCL-90-R score) None None
Zanardo et al, 202042 93·52 0·991 Postnatal depression (EPDS score) None Caesarean section

IDAS-II=Inventory of Depression and Anxiety SymptomS, Expanded Form. BAI=Beck Anxiety Inventory. NICU=neonatal intensive care unit. EDPS=Edinburgh Postnatal Depression Scale. NuPDQ=Revised Prenatal Distress Questionnaire. SCL-90-R=Symptom Checklist 90 Revised.

The majority of the included studies were of moderate methodological rigour (ie, 6–8 stars on the Newcastle-Ottawa Scale; table 1; appendix p 35). The main weaknesses were inconsistent definition and reporting of outcomes, inconsistency in selection of control groups, and retrospective study design. For example, although 18 papers4, 5, 14, 15, 16, 17, 19, 20, 21, 26, 28, 30, 31, 32, 33, 38, 47, 49 reported on preterm birth, variation in the gestational age cutoffs and use of ranges limited their comparability.

There were five reports from national registries,5, 17, 27, 37, 47 six regional reports,28, 37, 41, 43, 44, 45 and four multicentre studies;16, 21, 25, 46 the remaining 25 were single-centre studies. 11 studies12, 15, 19, 23, 24, 33, 38, 39, 42, 45, 49 had a comparison group from the equivalent period in 2019, the year preceding the pandemic. Nine studies16, 17, 20, 28, 30, 31, 32, 35, 47 had a comparison group of annually matched periods from several preceding years (table 1). 18 studies4, 5, 13, 14, 18, 21, 22, 25, 26, 27, 29, 36, 37, 41, 43, 44, 46, 48 had a comparison group from immediately before the lockdown period in the respective country. Exposed sample sizes varied from nine to 56 720 pregnancies (table 2). Only 19 studies5, 14, 15, 16, 19, 21, 22, 24, 26, 28, 30, 33, 34, 39, 41, 42, 47 adjusted for socioeconomic status, ethnic background, comorbidities, or other confounding factors.

A summary of the findings from included studies is shown in table 2. Meta-analysis was done for 21 outcomes for which more than one study was available for quantitative synthesis (table 3 ).

Table 3.

Results of the quantitative synthesis

Studies Pandemic
Pre-pandemic
Odds ratio or mean difference* p value I2
Events Pregnancies Events Pregnancies
Maternal and perinatal death
Stillbirth 12 1099 168 295 1325 198 993 1·28 (1·07–1·54) 0·0082 63%
HICs only 8 625 150 404 640 165 118 1·38 (0·94–2·02) 0·099 52%
LMICs only 4 474 17 891 685 33 875 1·29 (1·06–1·58) 0·012 64%
Neonatal death 3 62 13 214 120 22 570 1·01 (0·38–2·67) 0·98 85%
HICs only 1 5 2538 6 1262 0·41 (0·13–1·36) 0·14 NA
LMICs only 2 57 10 676 114 21 308 1·37 (0·42–4·46) 0·59 90%
Maternal death 2 530 1 237 018 698 2 224 859 1·37 (1·22–1·53) <0·0001 0%
HICs only 0 NA NA NA NA NA NA NA
LMICs only 2 530 1 237 018 698 2 224 859 1·37 (1·22–1·53) <0·0001 0%
Maternal morbidity and complications
Gestational diabetes 6 697 6946 954 10 137 1·01 (0·86–1·19) 0·85 45%
HICs only 5 667 6675 920 9826 1·02 (0·85–1·22) 0·86 56%
LMICs only 1 30 271 34 311 1·01 (0·60–1·71) 0·95 NA
Hypertensive disorders of pregnancy 6 293 6946 434 10 137 1·16 (0·75–1·79) 0·50 81%
HICs only 5 279 6675 431 9826 0·99 (0·67–1·46) 0·95 77%
LMICs only 1 14 271 3 311 5·59 (1·59–19·7) 0·0073 NA
EPDS score 3 NA 2330 NA 6517 0·42 (0·02–0·81) 0·038 79%
HICs only 1 NA 91 NA 101 2·16 (0·92–3·40) 0·0006 NA
LMICs only 2 NA 2239 NA 6416 0·22 (0·21–0·23) <0·0001 0%
Early pregnancy outcomes
Surgical treatment of ectopic pregnancy 3 27 37 73 272 5·81 (2·16–15·6) 0·0005 26%
HICs only 3 27 37 73 272 5·81 (2·16–15·6) 0·0005 26%
LMICs only 0 NA NA NA NA NA NA NA
Delivery outcomes
Spontaneous vaginal delivery 11 17 305 26 494 27 011 40 639 0·98 (0·93–1·02) 0·25 25%
HICs only 6 9675 14 632 11 288 16 362 0·99 (0·94–1·05) 0·80 4%
LMICs only 5 7630 11 862 15 723 24 277 0·96 (0·90–1·04) 0·33 37%
Caesarean section 17 15 304 48 550 20 656 67 442 1·03 (0·99–1·07) 0·14 46%
HICs only 11 10 091 33 161 10 824 36 956 1·01 (0·97–1·04) 0·76 10%
LMICs only 6 5213 15 389 9832 30 486 1·07 (0·99–1·16) 0·071 55%
Induction of labour 7 4860 16 459 5208 24 592 1·15 (0·81–1·64) 0·43 98%
HICs only 6 2578 9294 2950 11 403 1·03 (0·90–1·19) 0·64 76%
LMICs only 1 2282 7165 2258 13 189 2·26 (2·12–2·42) <0·0001 NA
Instrumental delivery 7 1045 16 287 1492 27 066 1·06 (0·97–1·15) 0·22 0%
HICs only 5 728 8168 740 10 300 1·07 (0·95–1·20) 0·88 0%
LMICs only 2 317 8119 752 16 766 1·02 (0·82–1·26) 0·25 0%
Preterm birth before 37 weeks' gestation 15 13 466 170 640 49 596 656 423 0·94 (0·87–1·02) 0·13 75%
HICs only 12 11 600 159 987 46 149 635 118 0·91 (0·84–0·99) 0·035 63%
LMICs only 3 1866 10 653 3447 21 305 1·05 (0·81–1·35) 0·73 88%
Preterm birth before 34 weeks' gestation 4 141 7039 210 9872 0·76 (0·42–1·36) 0·35 85%
HICs only 4 141 7039 210 9872 0·76 (0·42–1·36) 0·35 85%
LMICs only 0 NA NA NA NA NA NA NA
Preterm birth before 32 weeks' gestation 6 2297 152 422 6679 627 344 0·95 (0·64–1·39) 0·77 90%
HICs only 5 2198 148 974 6409 619 269 0·96 (0·61–1·52) 0·87 86%
LMICs only 1 99 3448 270 8075 0·85 (0·68–1·08) 0·18 NA
Preterm birth before 28 weeks' gestation 3 605 135 606 2603 586 189 0·84 (0·46–1·53) 0·56 57%
HICs only 3 605 135 606 2603 586 189 0·84 (0·46–1·53) 0·56 86%
LMICs only 0 NA NA NA NA NA NA NA
Iatrogenic preterm birth, any week 2 208 4204 358 6818 0·92 (0·77–1·10) 0·38 0%
HICs only 2 208 4204 358 6818 0·92 (0·77–1·10) 0·38 0%
LMICs only 0 NA NA NA NA NA NA NA
Spontaneous preterm birth, any week 2 192 4204 374 6818 0·81 (0·67–0·97) 0·020 0%
HICs only 2 192 4204 374 6818 0·81 (0·67–0·97) 0·020 0%
LMICs only 0 NA NA NA NA NA NA NA
Postpartum haemorrhage 2 603 3098 318 1978 1·02 (0·87–1·19) 0·82 0%
HICs only 2 603 3098 318 1978 1·02 (0·87–1·19) 0·82 0%
LMICs only 0 NA NA NA NA NA NA NA
Neonatal outcomes
5-min Apgar score <7 4 35 5701 45 9081 1·15 (0·62–2·15) 0·95 44%
HICs only 4 35 5701 45 9081 1·15 (0·62–2·15) 0·95 44%
LMICs only 0 NA NA NA NA NA NA NA
Birthweight <2500 g 3 919 9743 1510 14 492 0·99 (0·90–1·08) 0·75 0%
HICs only 1 144 2538 78 1262 0·91 (0·69–1·21) 0·53 NA
LMICs only 2 775 7205 1432 13 230 0·99 (0·91–1·09) 0·90 0%
NICU admission 7 446 8072 1604 37 557 0·90 (0·80–1·01) 0·084 0%
HICs only 6 413 7801 1555 37 246 0·91 (0·80–1·03) 0·14 0%
LMICs only 1 33 271 49 311 0·74 (0·46–1·19) 0·21 NA

Data are n or point estimate (95% CI). HICs=high-income countries. LMICs=low-income and middle-income countries. NA=not applicable. EPDS=Edinburgh Postnatal Depression Scale. NICU=neonatal intensive care unit.

*

Random-effects estimates calculated by Mantel-Haenszel method for during versus before pandemic; all values are odds ratios, except the estimate for EPDS scores (mean difference).

Three studies13, 25, 27 included data on maternal death, all of which reported an increase during the pandemic compared with before the pandemic, although this increase was statistically significant in only one study.25 Two studies in which statistical analysis was done, from India and Mexico, were included in the meta-analysis (1 237 018 pregnancies during and 2 224 859 before the pandemic), which showed a significant increase in maternal death during the pandemic (OR 1·37 [95% CI 1·22–1·53]; I 2=0%; table 3, figure 2A ), with findings dominated by a single study.27

Figure 2.

Figure 2

Forest plot of pooled ORs for maternal death (A), stillbirth (B), surgical management of ectopic pregnancy (C), and preterm birth before 37 weeks' gestation (D)

ORs are random-effects estimates calculated by Mantel-Haenszel method. HIC=high-income country. LMIC=low-income and middle-income country. NA=not applicable. OR=odds ratio. *All studies investigating this outcome fell into a single subgroup (either LMIC or HIC); therefore, the subgroup totals are the same as the overall totals.

14 studies from nine countries provided data on the incidence of stillbirth during (168 295 births) and before the pandemic (165 118 births).4, 12, 15, 16, 19, 21, 24, 25, 30, 31, 32, 37, 47, 49 Two of these studies were excluded (Gu et al15 because no adverse outcomes were reported and Khalil et al4 because of cohort overlap with another larger study in the analysis37). Meta-analysis of the remaining 12 studies found a significant increase in the rate of stillbirth (pooled OR 1·28 [95% CI 1·07–1·54]; I 2=63%; table 3, figure 2B). A subgroup analysis according to study setting produced similar findings, but only the subgroup of low-income and middle-income countries (LMICs) reached statistical significance (1·29 [1·06–1·58]; I 2=64%), whereas HICs did not (1·38 [0·94–2·02]; I 2=52%). Funnel plot asymmetry testing did not show a significant publication bias effect (p=0·12; appendix p 42). One study reported on antepartum and intrapartum stillbirth separately and found no difference in the proportion of antenatally diagnosed stillbirth, despite an overall increase in stillbirth in this tertiary centre in India.24 One study excluded antepartum stillbirth by definition because only women carrying a live fetus at admission were enrolled.21

Three studies reported on neonatal death. The largest, from Nepal,21 found a statistically significant increase, but two smaller studies30, 47 identified no significant change. The pooled OR for studies included in the meta-analysis (detailing 13 214 births during and 22 570 before the pandemic) was 1·01 (95% CI 0·38–2·67; I 2=85%; table 3, appendix p 45). The substantial statistical heterogeneity (table 3) was explained by neither WHO Healthcare Efficiency Index quartile nor GRSI score (appendix p 39).

Quantitative synthesis was possible for gestational diabetes (OR 1·01 [95% CI 0·86–1·19]; I 2=45%)4, 15, 19, 31, 32, 34 and hypertensive disorders of pregnancy (1·16 [0·75–1·79]; I 2=81%),4, 15, 19, 31, 32, 34 which were not significantly different during the pandemic compared with before the pandemic (table 3, appendix p 48). The statistical heterogeneity in the meta-analysis of hypertensive disorders of pregnancy was partly explained by WHO Healthcare Efficiency Index quartile (p=0·023) but not GRSI score (p=0·89; appendix p 39).

Two studies19, 30 reported on post-partum haemorrhage. Meta-analysis (including 3098 pregnancies during and 1978 before the pandemic) found no significant difference associated with the pandemic (OR 1·02 [95% CI 0·87–1·19]; I 2=0%; table 3, appendix p 48).

11 studies reported on measures of maternal mental health.15, 18, 22, 29, 34, 36, 39, 41, 42, 43, 44 Assessment tools included the Generalised Anxiety and Depression Scale, EPDS, Generalised Anxiety Disorder 7 questionnaire, Inventory of Depression and Anxiety Symptoms (Expanded Form), Symptom Checklist 90 Revised, and Patient Health Questionnaire 9. Four studies18, 36, 41, 42 gave mean EPDS scores (on a scale of 0–30). One study violated the normality assumption and was excluded from quantitative synthesis.36 For the remaining three studies, the pooled mean difference was 0·42 (95% CI 0·02–0·81; I 2=79%; table 3, appendix p 49). There was significant statistical heterogeneity, not explained by either the WHO Healthcare Efficiency Index quartile (p=0·62) or GRSI score (p=0·057; appendix p 39). When subdivided according to country income status, there was a statistically significant increase in mean EPDS score in LMICs (0·22 [0·21 to 0·23]). Of the 11 studies reporting on maternal mental health, seven reported a statistically significant increase in postnatal depression, maternal anxiety, or both.

Three studies12, 40, 48 reported on the surgical management of ectopic pregnancy. Meta-analytical summary of three studies found increased odds for surgical treatment of ectopic pregnancy during the pandemic (OR 5·81 [95% CI 2·16–15·6]; I 2=26%; table 3, figure 2C), most of which were due to ruptured ectopic pregnancy.

On the basis of 11 studies,14, 15, 18, 21, 26, 30, 31, 32, 33, 38, 46 there was no significant change in the rate of spontaneous vaginal delivery (OR 0·98 [95% CI 0·93–1·02]; I 2=25%; appendix p 51) during versus before the pandemic. 17 studies,6, 14, 15, 18, 19, 21, 25, 26, 30, 31, 32, 33, 38, 42, 45, 46, 49 including 48 550 pregnancies during and 67 442 before the pandemic, showed no significant change in caesarean section rate (1·03 [0·99–1·07]; I 2=46%; table 3, appendix p 52), with consistent findings when subdivided into HICs and LMICs. Additionally, on the basis of seven studies,14, 18, 19, 21, 30, 31, 32 rates of instrumental delivery did not differ during versus before the pandemic (1·06 [0·97–1·15]; I 2=0%; table 3, appendix p 53). The funnel plot asymmetry tests showed no significant publication bias in the included studies for vaginal birth (p=0·53) or caesarean section (p=0·61; appendix pp 64–65).

Seven studies,12, 14, 19, 21, 30, 31, 32 including 16 459 pregnancies during and 24 592 before the pandemic, showed no significant difference in the rate of induction of labour (OR 1·15 [95% CI 0·81–1·64]; I 2=98%; table 3, appendix p 54). The very high statistical heterogeneity was explained by WHO Healthcare Efficiency Index scores, with countries in the fourth quartile having lower induction rates (estimate −0·783, p<0·0001) than countries in the second quartile (appendix p 39). The only LMIC study21 included in the meta-analysis reported a significant increase in induction of labour (2·26 [2·12–2·42]).

There was a significant decrease in preterm birth in specific subgroups. Preterm birth was reported in 18 articles4, 5, 14, 15, 16, 17, 19, 20, 21, 26, 28, 30, 31, 32, 33, 38, 47, 49 with varying gestational age thresholds, and conflicting findings. Several large studies reported a local decrease in preterm birth, mostly in western European countries.5, 31, 33, 47, 49 One large study reported an increase in preterm birth in Nepal.21 Pooled analysis showed no overall effect for preterm birth before 37 weeks' gestation (OR 0·94 [95% CI 0·87–1·02]; I 2=75%; 15 studies; table 3, figure 2D). However, subgroup analysis of 12 studies (including 159 987 pregnancies during the pandemic and 635 118 pre-pandemic) suggested that there might be a significant decrease in HICs (0·91 [0·84–0·99]; I 2=63%). There was no overall effect on preterm birth before 34 weeks' gestation (0·76 [0·42–1·36]; I 2=85%; four studies), 32 weeks' gestation (0·95 [0·64–1·39]; I 2=90%; six studies) or 28 weeks' gestation (0·84 [0·46–1·53]; I 2=57%; three studies; table 3, appendix pp 55–57). In a meta-regression analysis for preterm birth before 37 weeks' gestation, neither WHO Healthcare Efficiency Index quartile (p=0·97) nor GRSI scores (p=0·17) adequately explained the statistical heterogeneity (appendix p 39). The funnel plot asymmetry test showed no significant publication bias in the included studies for preterm birth before 37 weeks' gestation (p=0·13; appendix p 66). Two studies reported on iatrogenic and spontaneous preterm birth before 37 weeks' gestation, both in HICs;16, 33 meta-analysis showed a significant decrease in spontaneous preterm birth (0·81 [0·67–0·97]; I 2=0%) but no difference in iatrogenic preterm birth (0·92 [0·77–1·10]; I 2=0%; table 3, appendix pp 59–60).

One study35 reported on the incidence of very low (<1500 g) and extremely low (<1000 g) birthweight as a proxy for preterm birth. This study reported a 73% reduction in very low birthweight infants, consistent with the reduction in preterm birth found in the meta-analysis. Three studies reported on the incidence of birthweight of less than 2500 g21, 30, 38 and found no significant difference associated with the pandemic (OR 0·99 [95% CI 0·90–1·08]; I 2=0%; table 3, appendix p 61).

Seven studies reported on neonatal intensive care unit admissions. Meta-analysis (including 8072 pregnancies during and 37 557 before the pandemic) found no overall difference in the rate of neonatal intensive care unit admissions (OR 0·90 [95% CI 0·80–1·01]; I 2=0%; table 3, appendix p 62).4, 14, 15, 19, 23, 31, 32

There were no significant differences in other neonatal outcomes between pandemic and pre-pandemic cohorts (table 3). Justman and colleagues19 reported no difference in the proportion of pregnancies with shoulder dystocia (p=0·26) or umbilical arterial pH below 7·0 (p>0·99). Seven studies assessed 5-min Apgar scores (Table 1, Table 2).14, 15, 19, 23, 31, 32, 38 We excluded from the meta-analysis the studies by Gu and colleagues15 (scores reported as mean rather than binary [<7 vs ≥7]), Kugelman and colleagues23 (no adverse events reported), and Sun and colleagues38 (no statistical analysis done). Meta-analysis of the remaining four studies14, 19, 31, 32 showed no change in the proportion of pregnancies with 5-min Apgar scores of less than 7 (OR 1·15 [95% CI 0·62–2·15]; I 2=44%; table 3, appendix p 63). Li and colleagues26 found no significant change in the proportion of pregnancies in which neonatal asphyxia was recorded (p=0·12). Meyer and colleagues31 reported on a composite score for adverse neonatal outcomes and found no difference between pandemic and pre-pandemic cohorts (p=0·12).

Discussion

This systematic review summarises the available global data on the effects of the COVID-19 pandemic on maternal and perinatal outcomes. We found increased maternal mortality and stillbirth, maternal stress, and ruptured ectopic pregnancies during the pandemic compared with before the pandemic. Stillbirth might be particularly increased in LMIC settings. There was no overall difference in preterm birth, but analyses of HIC data only suggested that both preterm birth before 37 weeks' gestation and spontaneous preterm birth might be reduced. WHO Healthcare Efficiency Index explained some of the observed between-study heterogeneity, but GRSI scores did not. This finding suggests that the increased rate of adverse outcomes might be driven mainly by the inefficiency of health-care systems and their inability to cope with the pandemic, rather than by the stringency of pandemic mitigation measures.

The strengths of this review include the comprehensive search not restricted by language, and the inclusion and synthesis of a broad range of literature. We used meta-regression to adjust for between-study heterogeneity in important outcomes, and analysed HIC and LMIC settings separately to clarify the differential effects of the pandemic by country income.

The main limitations are the retrospective design of the included studies, as well as the heterogeneity of the study populations and the definitions and ways of measuring outcomes, thereby limiting the comparability of results. There were fewer studies from LMIC settings than from HIC settings, which is concerning because our analysis showed substantial variation in outcomes between high-income and low-income settings. With regard to stillbirth, only one study reported on antepartum and intrapartum stillbirth separately, limiting our ability to speculate on the probable mechanism of this change. Few studies reported both stillbirth and preterm birth in the same cohort, which would be necessary to ascertain whether the cost of a reduction in preterm birth was an increase in stillbirth. Finally, we could not exclude the risk of publication bias against studies reporting negative findings, although funnel plot asymmetry testing for such bias was negative.

Early evidence suggested that the pandemic period was marked by a substantial decrease in preterm birth. Our findings from HICs supported this decrease, whereas those from LMICs did not. The report of a significant reduction in very low birthweight birth in Ireland further supports the hypothesis that preterm birth in HICs was reduced during the pandemic.35 Although no significant overall difference in neonatal death was observed, the data suggested that neonatal death might be increased in LMICs and decreased in HICs, consistently with the observed trends in preterm birth, a leading cause of neonatal mortality. This reduction in HICs appears to be driven by a reduction in spontaneous preterm birth, and is, therefore, not likely to be explained by reduced iatrogenic delivery. It is more likely that changes in health-care delivery and population behaviours are contributing factors. If a decrease in preterm birth has been achieved without a corresponding increase in fetal loss in some regions, there are valuable lessons to be learned from understanding the mechanisms underlying this effect.

The observed increase in maternal death is based only on data from LMICs. However, our findings are particularly concerning because these areas already carry the majority of the global burden of maternal mortality. This finding is supported by national data from Kenya not yet formally published,50 and we call for further investigation of maternal mortality as a matter of urgency, particularly in LMIC settings. Data from the MBRRACE-UK rapid report show that; in the first wave of the pandemic (March–May, 2020), there were 16 maternal deaths (ten associated with SARS-CoV-2) of an estimated 162 344 births, corresponding to a maternal mortality rate of 9·9 per 100 000,51 compared with a pre-pandemic rate of 9·7 per 100 000 in 2016–18.

One proposed explanation for the increase in adverse pregnancy outcomes is that such outcomes could be linked to reduced access to care. Although maternal anxiety was consistently shown to be increased during the pandemic, health-care providers around the world have reported reduced attendance for routine6, 13, 15, 52, 53, 54, 55 and unscheduled pregnancy care.6, 12, 13, 15, 19, 56 This reduction could be driven by concern about the risk of acquiring COVID-19 in health-care settings, governmental advice to stay at home, or reduced public transport and childcare access during lockdowns.13, 52 In HICs, much of routine care was rapidly restructured and delivered remotely using diverse models, including telephone or video-based appointments. Although technology can provide a COVID-19-secure path to continuity of antenatal care, there remains inequality of access for people without regular access to high-speed internet or privacy in their living space.57, 58 In LMICs, where remote consultations are less feasible, people might simply miss out on preventive antenatal care entirely.13, 53 In all settings, the impact is greatest on the most vulnerable individuals in the population: in Nepal, hospital deliveries decreased, most markedly among disadvantaged groups;21 and in the UK, 88% of pregnant women who died during the first wave of the pandemic were from black and minority ethnic groups.51

Reduced access to care is not the sole factor to consider in our continuing response to this global emergency. During its peak prevalence, maternity staff have been redeployed to support critical care and medical teams, reducing the staffing available for maternity care. Following the first wave in the UK, the Royal College of Obstetricians and Gynaecologists argued strongly for excluding maternity staff from redeployment wherever possible. We strongly recommend the prioritisation of safe staffing for maternity services throughout all phases of the pandemic response and in response to future health system shocks.

Wider societal changes are also echoed in observed changes in maternal health. Intimate-partner violence, already a leading cause of maternal death, has increased during the pandemic59 and has already been highlighted51 as a contributor to increased maternal mortality. Women have been disproportionately more likely to both become unemployed60 and take on more childcare because of nursery and school closures. The resultant financial and time constraints are likely to have far-reaching consequences for mothers' physical, emotional, and financial health during pregnancy and in the future.

Health-care providers planning for service delivery in the ongoing pandemic must consider how to establish robust antenatal care pathways that explicitly reach out to vulnerable individuals and communities. Public health messaging must emphasise the importance of antenatal care, and provide avenues of support for those at risk of intimate-partner violence. National governments must consider how to support financially vulnerable and socially isolated individuals, considering that each intersecting vulnerability magnifies risk across all contexts.51, 61, 62

It is clear that pregnant individuals and babies have been subjected to harm during the pandemic, and the onus is on the academic community, health-care providers, and policy-makers to learn from it. Women's health-care is often adversely affected in humanitarian disasters63 and our findings highlight the central importance of planning for robust maternity services in any emergency response.

There remain opportunities to be seized as well as challenges to be faced as we work to end the grip of the pandemic on our global community. Rapid restructuring of maternity care has shown that high-quality remote care can be facilitated, reductions in hospital stay can be achieved, and apparently intractable and entrenched problems can be transformed by the concerted application of funding, scientific enquiry, and political will. We can prioritise safe and accessible maternity care during the pandemic and the aftermath, while planning for a future of radically inclusive and equitable maternity care that will draw on the lessons of this pandemic to reduce preterm birth, stillbirth, and maternal mortality worldwide.

This online publication has been corrected. The corrected version first appeared at thelancet.com/lancetgh on May 18, 2021

Data sharing

All datasets generated and analysed, including the study protocol, search strategy, list of the included and excluded studies, data extracted, analysis plans, quality assessment, and assessment of the publication bias, are available in the Article and upon request from the corresponding author.

Declaration of interests

We declare no competing interests.

Acknowledgments

Acknowledgments

We thank Prof Paul Heath for his valuable critical appraisal of the systematic review.

Contributors

BC, IB, RT, EK, and AK participated in the data curation, formal analysis, and validation. LM, JvdM, IG-U EM, TD, ST, KLD, and SL participated in the investigation and visualisation. PvD and PO'B participated in the investigation, validation, and visualisation. All authors participated in the conceptualisation, visualisation, and writing, reviewing, and editing of the manuscript, and have read and agreed to the published version of the manuscript. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. BC, IB, RT, and EK accessed and verified the data underlying the study.

Supplementary Material

Supplementary appendix
mmc1.pdf (2.9MB, pdf)

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Associated Data

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

Supplementary Materials

Supplementary appendix
mmc1.pdf (2.9MB, pdf)

Data Availability Statement

All datasets generated and analysed, including the study protocol, search strategy, list of the included and excluded studies, data extracted, analysis plans, quality assessment, and assessment of the publication bias, are available in the Article and upon request from the corresponding author.


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