Articles Effects of the COVID-19 pandemic on maternal and perinatal outcomes: a systematic review and meta-analysis Barbora chilewst, Imogen Barat, Resemary Townsend Erkan Kala Jan van der Meuie, ek Gurol-Urganc Pot O'Brien Eaward Mets, Tim Draycott Shaka Thangeratnam, Kirsty Le Doar, Shame Ladhan Peter on Dadelszen, Laura Mage, Asma Khali Summary 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 ofthis effect has been undertaken. We aimed toassess 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 Jan1, 2020, to fan 8, 2021, for case-conteol 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 oF 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 stillbirth (pooled OR 1-28 95% C1 1-07-1-54]; =63%; 12 studies, 168 295 pregnancies during and 198 993 before the pandemic) and maternal death (1:37 [1-22-1-53; 12=0%, two studies [both from low-income and middle- income countries), 1237018 and 2224859 pregnancies) during versus before the pandemic. Preterm births before 37 weeks’ gestation were not significantly changed overall (0-94 [0-87-1-02}; P=75%; 15 studies, 170680 and 656423 pregnancies) but were decreased in highsincome countries (0-91 [0-84-0-99]; P=63%; 12 studies, 159987 and 635118 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, 2530 and 6517 pregnancies). Surgically managed ectopic pregnancies were increased during the pandemic (OR5:81 [2-16-15-6); 226%; 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 $ 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 lowsresource 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 Copyright © 2021 The Author(s). Published by Elsevier Ltd, This isan Open Access article under the CC BY 4.0 license Introduction also have affected the wellbeing of pregnant people and The SARS-CoV pandemic has had profound effects on health-care systems, societal structures, and the world economy: The adverse effects ofthe COVID-19 pandemic fon 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 meter sonvbncish Wal Jane 2023 their babies. “Emerging evidence suggests that rates of stillbirth and preterm birth might have changed substantially during the pandemic" A reduction in health-care-seeking behaviour, as well as reduced provision of maternity services, has been suggested as a possible cause* Robust estimates of the indirect maternal health effects of the @r® Thlactcomectgh os (Berman MSC DObttrasand racy, Une etl Tokay (Cran, Deparmereot lage obtiaand (Ponte, Urry Hap BHS {Emory norris (Po aetna Cenc fron ath (Pots angina waco,Articles asc logy Pasar beat Egan London, (ofstadan: prime Ure en Dusaletcoe Pre ageAC00) Forte sty patc ne Iipthyerco Psp crs 760 Researchin context Evidence before this study Before conducting this study we electronically searched. [MEDLINE snd Embe fram Jan 2,2020,t0 Jan 8, 2022, with no language restriction, to ident any previous systematic reviews and meta-analyses, Search terms included stillaith, perinatal mortality, maternalmortalty 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 kel ‘to requte intensive care treatment and experience preterm bint, Although individual tudes have eported pandemic assocated changes in pregnancy outcomes inthe general ‘maternity population, particular for preterm bith and stilsith, no global synthesis of ths kind has previously been reported. ‘Added value of this study “This review provides a comprehensive assessment ofthe global effects ofthe COVID-9 pandemic on maternal fetal. bith, pandemic can be derived from historical cohorts by examining the change in outcomes and calculating the excess event rate? This before-after approach applied to key pregnancy outcomes can be used to estimate the indirect effects of the COVID-19 pandemic. We aimed to assess the collateral effects on maternal, fetal, and neonatal outcomes of the global COVID-I9 pandemic. Methods Overview We did a systematic review and meta-analysis of studies fon the effects of the pandemic on maternal, fetal and neonatal outcomes. The review was registered with PROSPERO (CRD47020211753) and reported according to PRISMA guidelines.’ 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 Mandatin. Abstracts and potentially relevant full texts were reviewed independently by three authors (BC, IB, and RT) with any conficts resolved by consensus. Case-control studies, cohort studies, and brief reports were eligible for inclusion, Case reports, stadies without comparison groups, narrative or systematic literature reviews, preprint andneanatal outcomes. We identified signifiantincreasesin ‘maternal and fetal morality (particuarlyis low-incomeand, middle-income countries [LMICs), ruptured ectopic pregnancies, and maternal symptoms of depression Moreover, ‘we fund a reduction n preterm birth n high-income counties during the pandemic epoch Implications of allthe available evidence The sruption cause by the COID-19 pandemichasledto avoidable deaths ofboth mothers and babes Policy makers and health-care leaders must urgent investigate robust strategies for preserving safe and respectful maternity care, ‘even during the ongoing global emergency. Our findings bighlight disproportionate impact on LMICs Immediate action is required to avoid roling back decades of investment in recicing mather and infant mortality in low-resoure settings. ‘Thereisabo an unprecedented opportunity to investigate the snecharisms underlying the observed reduction in preterm birth and generate novel preventive interventions 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 suum of adverse events in exch group were extracted for categorical outcomes (eg, stillbith, 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 [FPDS] scores) ‘Outcomes of interest inchaded 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 for resource-use changes without clinical outcomes, we excluded them from the analysis. Pandemic mitigation response measures were extracted from the Oxford COVID-I9 Goverament Response ‘Tracker? We recorded the maximum restrictions imple mented during the study timeframe, Quantitative assess: rent of the severity of mitigation measures was recorded according to the Government Response Stringency Index (GRSI} developed by the Blavatnik School of Government atthe University of Oxford (Oxford, UK)?" Quality assessment Each study was scored according to the Newcastle ‘Ottawa Scale” independently by two assessors (BC, 1B) mw helarctconbeeetgh Val Jupe2023Articles on thee ad characteristics: selection of study groups, bility of groups, and ascertainment of the outcome of interest Statistical analysis Quantitative meta-analysis war done for an outcome ‘when more than one study presented relevant dats, We excluded individual outcomes from studies reporting no adverse outcomes in one oF 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 randonveffects estimate of the pooled odés of each. outcome was generated with use of the Mantel-Haenszel method. Betweenstudy heterogeneity was explored Using the P statistic, with substantial heterogeneity defined as an 2 valve greater than 50%, Meta-regression analyses were done for outcomes with substantial heterogeneity to investigate the relative contribution of the WHO Healtheare Efficiency Index" and the strin- gency of lockdown measures (quantified with the GRSI).? 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 Eggers test and funnel plots for visual inspection when sufficient studies (n>10} were available Analyses were done with R software (version 40.2. Role of the funding source ‘There was no funding source for this study Results (F 3592 abstracts screened, 192 were relevant for full-text review and 40 met the inchision criteria for systematic review (figure 1)" A list of exchaded 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 77). OF the 40 included studies, 31 for which comparable outcomes were also reported in at least one other study were induded in the metaanalysis<™=morersnceno 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 messures among countries. No study reported data from countries in the lowest WHO Healthcare Efficiency Index quartile, and the majority (28 studicg)OMADAIMACAM FepOTted 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 =*noinsimmnesn The meter convbncish Wal Jone 2023 wk dd septs senses Deena Fiore: PSMA ow car. reported outcomes and outcome measures are listed with the relevant studies in the appendix (p 31). The majority ofthe 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 papers *=?™sH0e" reported on preterm birth, variation in the gestational age cutoffs and use of ranges limited their comparability ‘There were five reports from national registies,"°="* six regional reports*°**'* and four multicentre studies; "= the remaining 25 were single-centre studies UL studies"™™0020 had a comparison group from the equivalent period in 2019, the year preceding the 9 had & comparison group of annually matched periods from several preceding years (table 1}. 18 studiestamminaonenennce fad 3 ‘comparison group from immediately before che lock own period in the respective country. 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Ow Hise 6 42 ToL 555724 og1(oso10) om on secon 1 2 43 amtiodsag) ot A as scnorpot etme 35) Hohe snome cane lows dmieincn corras NAet apa PDS-Ednbigh Portal Deri Ss NLoreartalintee ce on Hando-ceseatrasbedly Mtl tal mob eign andre ara ctr eet teaser P95 ar (ean ere) Tale esate quatave hee table 3, appendix p 45). heterogeneity (table 3) was explained by neither WHO Healthcare Efficiency Index quartile nor GRSI score (appendix p 39. Quantitative synthesis was possible for gestat diabetes (OR 1-01 [95% Cl 0-86-1-19], A594)" and hypertensive disorders of pregnancy 1-79}; 81%), which were not significantly 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 parly explained by WHO Healthcare Efficiency Index quartile (p-D:023) but not GRSI score (p-0:89; appendix p 39) “Two studies" 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% Cl 0-87-1-19); 209%; table 3, appendix p 48) 11 studies reported on measures of maternal mental health." Assessment tools included the Generalised Anxiety and Depression Scale, EPDS, meter convhocish Wal 9 Jane 2023, The substantial statistical (L16 Generalised Anxiety Disorder 7 questionnaire, Inventory of Depression and Anxiety Symptoms (Expanded Form), Symptom Checklist 90 Revised, and Patient Health Questionnaire 9. Four studies*** gave mean EPDS || scores fon a scale of 0-30). One study violated the normality assumption and was excluded from quantitative synthesis." For the remaining three studies, the pooled ‘mean difference was 0-42 (95% CI 0:02-0:81; P-79%4; table 3, appendix p 49). There was significant statistical heterogeneity, not explained by either the WHO Healtheare Ffficiency 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 inerease in mean EPDS score in MICs (0:22 [0-21 to 0-23). OF the 11 studies reporting fon maternal mental health, seven reported a statistically significant increase in postnatal depression, maternal anxiety, or both. Tree stdies 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Articles Figr2: Foret plato est) seh), srg managerntot sctopcpregnaney (0, a0 preterm bith bore ay ests gestation) senate ited Martel aes eto. eighinare cout. rata “al ses estat ‘ivovtione el esse sro ether Co Wrote shay tt tor os A Pandemic Prepandemic Weight on (95% ace ne 0° a | sszrosears ntact” 59h raash tsa ste st = stints) ttt seemed agi OE Anas ato S ems Aeron aN pb gu IO {—_, 8 ce . 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Be aut ets come 4 ostporiaon case ne es sis aan A nog Scent ues 0 aya Helena stegeey -0033 9-187 0 pon cwnleand ‘aiks pokso 996 6563 se808 essorsen evjeny 00102552564) 5 Actes eon Po soa Pe wearer conbeeegh Val Jupe2023Articles [9596 CI 2-16-15.6], 2-269; table 3, figure 2C), most of Which were due to ruptured ectopic pregnancy. On the basis of 11 studies "30%" there was no significant change in the rate of spontaneous vaginal delivery (OR 0-98 [95% Cl 0-951-02} R=25%; appendix p St) during versus before the pandemic, 17 studies,snnccsnswe including 48550 preg- nancies during and 67442 before the pandemic, showed no significant change in caesarean section rate (1-03, |0-99-1-07); 46%; table 3, appendix p 52), with consistent findings when subdivided into HICs and IMICs. Additionally, on the basis of seven studies" rates of instrumental delivery did not differ during versus before the pandemic (1-06 [0-97-1-15}; P-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 sesarean section (p-0-61; appendix pp 64-63). Seven studies*9 including 16459 pregnancies during and 24592 before the pandemic, showed no significant difference in the rate of induction of labour (OR 1-15 [95% CI 0-81-1-64), 989%; table 5, appendix 54). The very high statistical heterogeneity was explained by WHO Healthcare Efficiency Index scores, with countries in the fourth quattile having lower induction rates (estimate -0-783, p<0-0001) than countries in the second quartile (appendix p 39). The only LMIC study included in the metaanalysis 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 artiles*2™0a1 80% with varying gestational age thresholds, and conflicting findings. Several large studies reported a local decrease in preterm birth, mostly in western European countries." One large study reported an increase in preterm birth in Nepal" Pooled analysis showed no overall effect for preterm birth before 37 weeks gestation (OR 0-94[95% CI 0-87-1- 02} 2=75%; 15 studies; table 3, figure 2D). However, subgroup analysis of 12 studies including 159987 pregnancies during the pandemic and 635118 pre-pandemic) suggested that there might be a significant decrease in HICs (0-91 [0-84-0-99), 2.6394) There was no overall effect on preterm birth before 34 weeks gestation (0:75 [o-42-1.36}, P85; four studies), 32 weeks’ gestation (0:95 [0,641.39]; 12-90%; six studies) or 28 weeks gestation (0-84[0-45-153], 12-57%; three studies; table 3, appendix pp 55-57). In a metaregression analysie for preterm birth before 37 week# gestation, neither WHO Healthcare Eificiency Index quartile (p-0-97) nor GRSI scores (p=0-17) adequately explained the statistical bacterogencity (appendix p 38). 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;* meta-analysis meter convbncish Wal Jone 2023 showed a significant decrease in spontaneous preterm birth (0-81 [0-67-0.97, P~0%) but no difference in iatrogenic preterm birth (0-92 0-77-1- 10} 0% table 3, appendix pp 59-60) ‘One sttidy” reported on the incidence of very low (<1500 g) snd extremely low (<1000 g) birthweight a= a proxy for preterm birth. ‘This study reported 2 78% 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 g°”" and found no significant difference associated with the pandemic (OR 0.99 [959% C1 0-90-1-08), 20%; table 3, appendix psy) Seven studies reported on neonatal intensive care unit admissions. Meta-analysis (including 8072 pregnancies uring and 37537 before the pandemic) found no overal difference in the rate of neonatal intensive cate unit admissions {OR 0-90 [95% CI 0-80-11]; P=0%; table 3, appendix p 62). ‘There were no significant differences in other neonatal cutcomes between pandemic and pre-pandemic cohorts (table ).justman and colleagues" 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 Ssmin Apgar scores (tables 1, 7). We excluded from the meta analysis the studies by Gu and colleagues" (scores reported as mean rather than binary [27 vs 27), Kugelman and colleagues” (no adverse events reported), and Sun and colleagues” (no statistical analysis done), Meta analysis of the remaining four studies" 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}; 124496; table 5, appendix p 63). Li and collesgues™ found no significant change in the proportion of pregnancies in which neonatal asphyxia was recorded (p=0-12). Meyer and colleagues" reported on a composite score for adverse neonatal outcomes and found no difference between pandemic and pre-pandemie cohorts (p=0-12), Discussion This systematic review summarises the available global data on the effects of the COVID-I9 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. Stilbirth might be particulasly increased in LMIC settings. There was no overall difference in preterm birth, but analyses of HIC data only suggested that both preterm bicth before 37 weeks gestation and spontancous 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 769oe their inability to cope with the pandemic, rather than by the stringency of pandemic mitigation measures, ‘The strengths ofthis 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-stdy 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. Theze were fewer studies from LMIC settings than from HIC settings, which is concerning because ou analysis showed substantial variation in outcomes Detwieen 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 stilbirth. Finally, we could not exclude the risk of publication bias against studies reporting negative findings, although fanel plot asymmeny testing for such bias was negative Bary evidence suggested thatthe 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 bizth in HICs was reduced during the pandemic.” 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 4s, therefore, not likely to be explained by reduced iatrogenic delivery. It is more likely that changes in health-care delivery and population behaviours are conteibuting factors. Ifa decrease in preterm bigth has been achieved without a corresponding increase in fetal loss in some regions, theze are valuable lessons to be learned from understanding the mechanisms underlying this effect. ‘The observed increase in maternal death is based only fon data from LMICs. However, our findings are particulstly concerning because these areas already camry the majority of the global burden of maternal mortality ‘This finding ie supported by national data from Kenya not yet formally published” 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 (len associated with SARS-CoV.2) of an estimated 162344 births, corresponding to a maternal mortality rate of 9-9 per 100000," compared with 2 pre-pandemic rate of 9.7 per 100000 in 2016-18, ‘One proposed explanation for the increase in adverse pregnancy outcomes i that such outcomes could be linked t 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 routine" and unscheduled pregnancy care" This reduction could be driven by concern about the risk of acquiring COVID-19 in health-care setings, governmental advice to stay at hhome, or reduced public tansport and childcare access during lockdowns** 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-I9-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.” In LMICs, ‘where remote consultations are less feasible, people might simply miss out on preventive antenatal care entirely.” Im all settings, the impact is greatest on the most vulnerable individuals im the population: in Nepal, hospital deliveries decreased, most markedly among. disadvantaged groups.” and in the UK, 88% of pregnant women who died during the first wave of the pandemic ‘were from black and minority ethnic groups.” 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 UX, 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 luring the pandemic” and has already been highlighted" a a contributor to increased maternal mortally, Women hhave been disproportionately more likely to both become unemployed" and take on more childcare because of nursery and school closures. The resultant financial and time constraints are likely to have farreaching consequences for mothers’ physicsl, 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 moet conyboeetgh Val Jupe2023Articles messaging must emphasise the importance of antenatal ‘ate, and provide avenues of support for those at risk of intimate partner violence, National goveraments ens consider howto support financially wlnerable and socially isolated individuals, considering that each intersecting slnerabilty magnifies risk across all contets*** tis clear that pregnant individuals and babies have ‘been subjected to harm during the pandemic, and the ‘onus ison the academic community, health-care providers, and policymakers to learn from it. Women's Jnelthcare is often adversely afected in humanitarian disasters” 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 ahullenges to be faced as we work to end the grip ofthe pandemic on our glabal community. Rapid restrcturing of maternity cae has shown that high-quality remote care ‘an be facilitated, reductions in hospital stay can be achieved, and apparently intractable and entrenched problems can be transformed by the concerted application of finding, «cientfc enquiry, and politcal wil. We can Pioritise safe and accessible maternity care during the pandemic and the afermath, while planning fora ture of radically inclusive and equitable maternity care that will draw on the lessons ofthis pandemic to reduce preterm birth, stilbirth, and maternal mortality worldwide BOT RT EK and |AK patticipated in the éata curation, formal thay and vation LM, 1e-U BM, 1D, SE RUD ae SL parsed nthe vergon and viren yD and PO farted te iargen, alan sed vinulrtne ‘itr ppd inte coneptinnton,inbeatonand ‘hing soveving a ahing of te mone snd hove rad and Secdiote plated eon af hearse Alters al ‘css tall he aunt ya boil esponaiy fr the ‘co sub for pletion, BC 1, Rs Ek ected sd ‘sted he audrina Decastionot interes We didae n competing tres Data sang ‘All datasets gerzated ard aad inching the sty prota, seach ‘setegy ito he nlide ad acide tis, ata erated aml PHsne, quay aerearment and aseement ofthe pletion bis are Talal in the Artie ané pon request fom the crerponding autor Acdnowledgments ‘Wethenk Prt Prd Heath bis valuable ita appraisal the fetes 1 Gord Bank The plabal economic ouook during the COVID-9 pancemie's changed wal une 200 hp wr worden: glen nes etre/2020/06/08/thealabrheconomcoutonk Eiingthecovd 1 pandemicsshanged-wold cessed Nev is 200) 2. Bark 7 The indir impact of COVID-19 on women. ane Ife Di 2030 28 500-05 5 Rabenen T Caner ED, Cho VB, tal acy eeinate ofthe Indie eas of te COVID pandemic on mute and hd ‘aerully is lwincese and iddledaceme cots smedeing dy Lancet Gab Heath 2020 8301-08 46 Kal Aton Dadelzen F,DrayetT Ugwamads A OBrien? [ogee Change nthe inedence felts nd pete elery tng te COVIDI pandemic JAMA 2020328 03. nonelirctconyboegh Val 9 June 2023 0 2 % een JV, Burgos OchouL Berens LEM, Schoenmaes 8 ‘Stecges EAP, Ress IM. Impaceof COVIDAB magn seater onthe nice of preterm bch s ratond ess ‘periment dL Pal ea 200; 5604-1 Kili Avon Dadleren Kalai fetal. Change obeteic tendance and wes dig the COVIDA pandemic anc fet Di 2020, publ oaine Oe 5 He gh ol s73.s0592030799. ‘Wools, Chapman DA, abo RT, Weinberger DM. il ‘Tisor DDE: Exceee deste fom cone 8 sn ober sues ‘Marchjly 2020 JAMA 2020324 1562-64 ober D, Lb A. Teal), Asan DG. Prefered reporting fers fr syetemac eviews dd eee: the PRISMA ‘Siemens Med 200 100097 Dist cha of Goverment. Univer of Oxerd.Coonsirar {ovemmensesponercker Hipage sete ‘evearcheprojccorsanvgovertnenticspnsestaier [scene ot, 2020) ‘els GA, Shes 5, O'Connell D, a The Newasle Ota Sele (NOS) foraeesing the qui of nnrendorsee sade et "lye paca programejlied-xpederislogy nerds cessed Nev 16 200), Tangon A Mara Cl, Laker JA, Bans DB. Measuring vel ‘hl system prormance fr 1 counties. Geneva Weld Health {rgsniatin, 100 rps wn snt/bea inl papeso pal (feted Nov 1200, Del Ut ©. Manzoni, Cian Seal Fees 0 SARS-CoV2 ‘pdemicon he obtetica and gyeclopel emergeng serie ‘etses What apposed and wht shale ene Bom? Er) Obstet Gel Reprod Bil 2020 25406258. Goyal Singh? singh K, Sekar 5 Agrawal N. Mies 8. “The eet ofthe COVID«IS pandemic on maternal eth de9 day secng healthcare experience om aerny cee tnt) Choe bse 202152: 25%-35, (Greene NH, Klpatc ], Wong MS, Oxbmeh JA. Ng M Isp oor and delivery unt ply spodietion on mater nd onal ostcomes ring the arose dea 2039 endemic Arn] Obit Gel MEM 020, 2 10334, {Gu X%, Coen & YUH. Lng GY. Chea H, Shen Y. Hote present ‘nospill COVIDA9 infection and reasve women aout he ‘lt of pregnancy experience fos sobre certern Cn ine ed fern 48 0000520859557 Handley SC. Mali AM, Hot MA et a. Change in pete bith phenonpe ad lb 7 Papi hep dating he SaRS-Co\e2 pandemic, Mrchfune 2020 JANA 202 3258-88 ederana 6, Hedley PL, Baivad Hanser M, etal Danish premature bth rates Curing the COVID-Dlacdowe. Hs PW, Ma G, Seto MET, Cheung KW Ee’ of COVID-19 08 dcivery pars and postnatal depression: sores of pregnant Somes Hong Kong Mel 2020 publsked orlne Nov 3. [pr /deog/10 2809/2087 Justman W, Shaka G, Gute, al Lockdown with rice {heimpart af he COVID- 9 pandemic on pent care ad penta fuconcr ina trary cre ter fr ed e200 22 8037 Koga Tala M, Oc D Preterm diver nd hypertensive de of pregnancy wer reed dung the COVID I pundesic Sale bsplbased ry J Ob Gynec er 2020 4 05 IKEA, Gurung R Kinney ta Efe fhe COVID 19 pandemic responce on nrapstam cae slit sd neonatal ‘nora otcomes in Nepal = prospective observational std nt Clb Hes 2030, RZD yar Hocilu M, Gna) 7 Yrdine OD, Turgut , Kathe A [Ant snd eprection septa the ste pregnant wores ‘elon nd daring the COVIDSS pare J Pernt Med 020" seca Kgehan N Lave 0, Asaf Wel. Changes nthe abe ‘merge department profile during te COVID#9 pandemic {Mato el Non! Me 2020 passed oline Nov Is ater a7058 202018672. Kosar M, Pat M, Yast 83 Sibi a he COVIOA pandemic looking eyone SARS-CoV nec. {nt Cyan Os 202, publaned olin Dec 3 pede onp0002) 6613504 omArticles om B 8 um V. Meda K Choudhary R. 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Stone Sth H, Thang K,Ramssy ME, Andrew edhe Sits ding the COViD+# pando a Engh. ‘petsjase 220, jana 2021925: 86-82 Sun SY, Gunzel CAF, de Mors LR ol fl of aye htc labor ere during the COVID.9pendemi on penta Sotomes ft} rac es 020 1 28S Sona 8Peyholgi tate ring the fet mimes of Dregnancy under the COVIDaDeplec a aan {Mater el Recall ted 020 pussed ole fly 2 bap: ono. 7058 202095398 Werner Kate A. Ceange in extopcprpnancy preenations {rng the COVID-IS pandemic at Pra 030 pubihed foline Dec 2 tps fetetg0jep13925. Ww ¥, Zhang, Ln H etal, Pecaclprtsve nd aety 2yespoms of pregnant women during the constr dea 2019 ure in Chins. Ae) Obes Gyecl 200, 2824019, anardaV Manghina ¥, Giier , Vetare M, Svein Statice © Pycologiel psc of COVID-9gusranne measures In nortbeaster tan motets the immed ate pep Deion J Gytcl Ose 200150 16-38 Xie M, Wang X Zhang. Wang ¥. lteation nthe pecs ‘tar ane fan emonment of pregnant worsen before sd ‘ang the COVIGS pander It} Gee bet 00 bled enn Jan 5p dig 1092) ige 19575 Bebelt N, Lamu R. Guor-Bisonnet ) DetinMazee Marl , Mande M. Uptend in ates sod poate ‘sraptaatalegy png wet ding rons dsc hs pandemic Act Ober Gye Sand 102098 34055 6 se a Bhan K Comb M,Bewlay A, a The fle f COVID9 on genera anastsa ales fr caste secon A cosssectanal ‘Sajas ef t heps othe errs of England: Ameena Borntinf, Coleeen M, Had G tal at perperam ‘acge sing the COVIDL pander J Pema Med 2070; ‘Canis EC Magos LE, ash etl. Medes reduction in dverse bith utameselawing tne COVID-I lockdown ‘am Obes Cyst 2020, pbliced online Dee ‘itp es ongt 0169 200012 158 Cannio F Youssef A, Aten A, Gamal NPG, Serco R Tnereed ut of ghee cape pega) ia COVIDSS ‘under anabes oe the Nerf aly. Urtound Obit nee De Cate M, Vln Pale A. 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Balin H, tal, atin nd provider perspectives of ne pret ear model inteducedn respons to {ecarnsrtu duce 209 pandemic Am J Obst Cyne 202° published online Oet Hpe/as ori (og 200 10.08 Ieganathan 5, rssnan 1, ise Ml) VabraN,Racelon 8 Mesowica :Adieeace and accepobliy of lee ppeimenss forkige osetia pabents rng be coronas dace 209 pander AmJ Obst Gy MF 2020; 210233. Tareas Rel S, Mage Lt Maternity zervie nthe UK {ting the corns ice 2019 pander ational suey of ‘modifeatenste stndnd ee BJO 7020, publibed eine Sep. tps: do.org/i0 1H Tar-sz8 6547 Holco D, Faucher MA, Sou. QuintBouzad M, Nedsos Duryea. Patetpespeines onset il prenatal te mi the seer see repo syndomecornatrar {SARS-Cav pandemic Oh Gynt 2000-196 37-2, Madden N, Eterm UN, Frc AM tal Teeth uptake Int preail cae and provide tides eutng se COVID-B pusdemc tn new jk city quanta nd quate alse Jr Pratl 2030 97 To08 4 Brey Ni. Parga A, Dllbouph K, Schneider Seah cate ratones esponsbiry tears toate parte valence else te COVID49 prdemics CMA 2020 19 E6090 ‘Gein V The carer cost of COVID9 io feerexeatcher, id [Row scence should serpone Notre 220°585 86259. Pér-Searila CunmingiarsK Morin VE. COVIDA9 and Iatral and chil food ané mutton accu = camoler fnderie Mate Chi utr 00 1:13, Botan N Homann 3, VeasCosseD The unegul pace ‘oronarts pandemic evidence from seenecn developing ‘ere, alah M, Clit CEM, King C, Bases to materal sth sevicer during the bal tren three Wert can unter alteratre een BMY lob Hah 2005: «0029 lancet conyhoeetgh Val Jupe2025