key: cord-0725169-lw3oypbu
authors: Yang, Jie; D’souza, Rohan; Kharrat, Ashraf; Fell, Deshayne B.; Snelgrove, John W.; Murphy, Kellie E.; Shah, Prakesh S.
title: COVID‐19 pandemic and population‐level pregnancy and neonatal outcomes: a living systematic review and meta‐analysis
date: 2021-06-06
journal: Acta Obstet Gynecol Scand
DOI: 10.1111/aogs.14206
sha: e48f262536ee9a1f71fdbb73748f5e9b75021904
doc_id: 725169
cord_uid: lw3oypbu

INTRODUCTION: Conflicting reports of increases and decreases in rates of preterm birth (PTB) and stillbirth in the general population during the COVID‐19 pandemic have surfaced. The objective of our study was to conduct a living systematic review and meta‐analyses of studies reporting pregnancy and neonatal outcomes by comparing the pandemic and pre‐pandemic periods. MATERIAL AND METHODS: We searched PubMed and Embase databases, reference lists of articles published up until May 14, 2021 and included English language studies that compared outcomes between the COVID‐19 pandemic time period vs. pre‐pandemic time periods. Risk of bias was assessed using the Newcastle‐Ottawa scale. We conducted random‐effects meta‐analysis using the inverse variance method. RESULTS: Thirty‐seven studies with low‐to‐moderate risk of bias, reporting on 1,677,858 pregnancies during the pandemic period and 21,028,650 pregnancies during the pre‐pandemic period, were included. There was significant reduction in unadjusted estimates of PTB (28 studies, unadjusted odds ratio [uaOR] 0.94, 95% CI 0.91‐0.98) but not in adjusted estimates (6 studies, adjusted OR [aOR] 0.95, 95% CI 0.80‐1.13). The reduction was noted in studies from single centers/health areas (uaOR 0.90, 95% CI 0.86‐0.94) but not in regional/national studies (uaOR 0.99, 95% CI 0.95‐1.03). There was reduction in spontaneous PTB (5 studies, uaOR 0.89, 95% CI 0.82‐0.98) and induced PTB (4 studies, uaOR 0.90, 95% CI 0.81‐1.00). There was no reduction in PTB when stratified by GA <34, <32 or <28 weeks. There was no difference in stillbirths between the pandemic and pre‐pandemic time periods (21 studies, uaOR 1.08, 95% CI 0.94‐1.23 and 4 studies, aOR 1.06, 95% CI 0.81‐1.38). There was an increase in birth weight (6 studies, mean difference 17g, 95% CI 7‐28g) during the pandemic period. There was an increase in maternal mortality (4 studies, uaOR 1.15, 95% CI 1.05‐1.26), which was mostly influenced by one study from Mexico. There was significant publication bias for the outcome of PTB. CONCLUSIONS: The COVID‐19 pandemic time period may be associated with a reduction in PTB; however, referral bias cannot be excluded. There was no difference in stillbirth between pandemic and pre‐pandemic period.

While most pregnancies end with healthy mothers and healthy children, a small proportion result in adverse outcomes for the mother, fetus, or neonate. Among others, such outcomes include stillbirth, preterm birth (PTB), neonatal mortality, and maternal mortality -all of which can have devastating and long-lasting effects on families. [1] [2] [3] Preterm birth (birth before 37 weeks' gestation) is a major determinant of neonatal mortality and morbidity 4 with long-term adverse consequences during childhood and adulthood. 5 Medical, social, psychological, environmental, and economic factors have all been implicated in the etiopathogenesis of PTB and other adverse pregnancy outcomes.

The COVID-19 pandemic has had an unprecedented impact on society worldwide and provided a natural experiment allowing us to study the effects of these factors on adverse pregnancy outcomes.

During the early stages of the pandemic, reports emerged describing reduced PTB rates in Denmark 6 and Ireland. 7 However, these were followed by reports of increased PTB rates (births between 28-32 weeks' gestation) in Nepal 8 and no changes in PTB rates in the UK 9 and Sweden. 10 At the same time, increases in stillbirth rates were reported from the UK 9 and Nepal, 8 with or without changes in PTB rates, while no change in the stillbirth rate was reported from Ireland. 2 In light of these mixed reports, it is uncertain whether or not the COVID-19 pandemic has affected pregnancy outcomes at the population level. Inconsistency among conclusions from different studies and a lack of evidence to inform the creation of evidence-based population health guidance prompted us to undertake a comprehensive review of the influence of the COVID-19 pandemic on pregnancy outcomes. Our objective was to systematically review and meta-analyze studies reporting defined local, regional, or national population-based rates for maternal, fetal, and neonatal outcomes during the pandemic period compared to the pre-pandemic period.

The review was conducted using standardized methods for systematic reviews of observational studies and reported according to the Preferred Reporting Items in Systematic Reviews and Meta-analyses guidelines. 11 No ethical approval was obtained as all data used for these analyses were published previously. The review protocol was registered in PROSPERO (CRD42021234036). 12

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We searched PubMed and Embase databases, reference lists of included articles, and personal files for studies published up to May 14, 2021 . The search strategy used a combination of the MeSH terms "preterm" or "stillbirth" AND "Covid19" or "SARS-COV-2" and included any type of study design published in the English language (Supporting Information Appendix S1). Since this is a living systematic review, it will be updated 3-monthly for the duration of the pandemic, using the same search strategy. Studies were included if they compared pregnancy outcomes between the COVID-19 pandemic time period vs. pre-pandemic time periods and reported on any of the outcomes of interest. We excluded studies that only reported outcomes of pregnant women with COVID-19 infection. Screening of articles was conducted by two authors (PS and JY) and disagreements were resolved through discussion (JY, RD and PS) and consensus. Since we were interested in overall pregnancy outcomes, we did not restrict studies based on plurality (included singleton and multiple pregnancies).

In most studies, the pandemic period was defined as the period of time beginning from the date or month of the implementation of emergency lockdown measures in relevant countries or states or cities, or when there was an emergence of cases or a surge of cases in the population studied. Some studies assessed "post-lockdown" period which for the purpose of this study was included as "pandemic" period as we are still not out of pandemic yet. The pre-pandemic period was defined either as the period ending immediately before lockdown measures were implemented or before the emergence of the first case or high case numbers in the population, or as a historical period, such as births in the same population in previous year(s). The lengths of these periods varied across studies.

We included studies that reported outcomes of pregnancy in general population. The review was not designed to evaluate outcomes of pregnancies where only women were affected by SARS-CoV-2 infection were reported.

The primary outcomes in this study were rates of PTB and stillbirth. Secondary outcomes included mean birth weight (continuous) and rates of low birth weight (LBW), spontaneous PTB, medically

This article is protected by copyright. All rights reserved indicated PTB, and neonatal, perinatal, or maternal mortality. We contacted authors to obtain data on stillbirth and neonatal mortality when the outcomes were reported as 'intrauterine fetal death' (IUFD) and

'perinatal mortality'. The outcomes of IUFD and perinatal mortality, though specified in the protocol, were not included ultimately in review (deviation from protocol). Outcomes were defined as follows:

1. Preterm birth: Live births between 22 +0 and 36 +6 weeks' gestation were classified as PTB. Data on PTB at <28 weeks', <32 weeks', and <34 weeks' gestation were reported separately in some studies and were analyzed independently.

2. Stillbirth: Death before the complete expulsion or extraction from the parturient of a product of human conception at or after 20 weeks of gestation. 13 3. Birth weight: Infant weight in grams, measured as soon as possible after live birth. Birth weight <2500 grams was defined as LBW, birth weight <1500 grams was defined as very low birth weight (VLBW), and birth weight <1000 grams was defined as extremely low birth weight (ELBW).

4. Spontaneous PTB: Birth of a baby between 22 +0 and 36 +6 weeks' gestation following spontaneous preterm labor or preterm pre-labor rupture of membranes. 3 5. Medically indicated PTB: Preterm birth initiated by a healthcare provider for maternal or fetal indications. 3 6. Neonatal mortality: Death of a newborn due to any cause before 28 days of age. 7. Maternal mortality: Death of a woman either during pregnancy or childbirth from any cause related to or aggravated by pregnancy or its management, or within 42 days of end of pregnancy, irrespective of the duration and site of the pregnancy. 9

Data from the eligible studies were independently extracted by 2 authors (JY and PS) using a predefined, standardized extraction form. Disagreements between the authors were resolved by consensus and involving a third author (RD). The information extracted included details of the publication, study setting and size, pre-pandemic period definition, pandemic period definition, and rates of the reported outcomes in pre-pandemic and pandemic time periods. We relied only on published information.

We anticipated that primarily observational studies would be included in this review; thus, we used the Newcastle-Ottawa Scale 14 for cohort studies to assess risk of bias. This scale assesses risk of bias Accepted Article in domains of selection, comparability, and outcomes, and assigns a maximum score of 9. Studies with scores of 0 to 3 were considered to have high risk of bias, those with scores of 4 to 6 had moderate risk of bias, and those with scores of 7 to 9 had low risk of bias.

We planned for meta-analyses of studies that reported similar outcomes and were methodologically homogeneous. For binary outcomes, we calculated the summary unadjusted odds ratios (uaOR), adjusted OR (aOR) when available and 95% confidence intervals (CI), whereas for birth weight we calculated the mean difference (MD) and 95% CI. Statistical heterogeneity was assessed using the Cochran's Q statistic and quantified by calculating the I 2 values. We expected clinical and methodological heterogeneity between studies and thus planned a priori for random effect meta-analyses using the inverse variance method. We planned to meta-analyze adjusted estimates from studies that reported them, understanding that studies will have adjusted for different factors based on data availability and baseline differences. We also expected that the duration of the "pre-pandemic" period would vary across studies, thus, we conducted meta-regression on the variable "duration of the pre-pandemic period" as a covariate to explain any heterogeneity in the results. Post-hoc subgroup analyses were conducted for the 2 primary outcomes after dividing studies into single-center (or selected hospitals/centers in an area), regional (statewide or province-wide) or national in scope. Publication bias was assessed qualitatively, using funnel plots, and quantitatively, by calculating Egger's regression intercept when >10 studies were included in the meta-analyses. For the Egger test, values of <0.10 were considered indicative of publication bias.

Meta-analyses were conducted using STATA v11.0 (Stata, College Station, TX) and Review Manager v5.3 (Cochrane Collaboration).

Of 9,123 records in the initial search, 37 articles were eligible for inclusion, of which 36 were used in the quantitative synthesis 2, 6-10, 15-44 ( Figure 1 ). Eighteen full-text reports were excluded: reasons for the exclusions are provided in Supporting Information Appendix S2. For one study conducted in the Netherlands by Been et al, 45 data were presented using multiple cut-offs to define the pre-and post-Accepted Article pandemic periods, with several different comparisons, making it difficult to select one comparison that aligned well with the other studies; we, therefore, included this study in the systematic review but not in meta-analyses. Khalil et al 9 had overlapping data for stillbirth outcome with another study; however, preterm birth data were not overlapping, so only preterm birth data were used in this review. Study characteristics are reported in Table 1 : 6 studies were national in scope, 7 were regional, and 24 were local, including single-center studies. Across the included studies, totals of 1, 677, 858 pregnancies during the pandemic period (excluding numbers from Been et al 45 ) and 21, 028, 650 pregnancies during the prepandemic period were studied. Duration of the "pandemic period" studied varied from 4 weeks to 7 months, and duration of the "pre-pandemic period" studied varied from 2 months to 19 years. The risk of bias assessment scores for the included studies ranged from 5 to 9 ( Table 2) . Twenty studies had moderate risk of bias and 17 studies had low risk of bias. Twenty-nine studies included pregnant population from local/regional/national data which may have included those with COVID-19 infection, whereas 8 studies specifically excluded women with COVID-19 infection if it was known. However, it is difficult to be completely certain as testing on pregnant women was not universally applied in any of the studies.

1. Preterm birth and its subgroups: Twenty eight studies including 300, 117 women during the pandemic period and 1, 268, 708 women in the pre-pandemic period reported PTB <37 weeks' gestation; there was a reduction in unadjusted odds of PTB during the pandemic period compared with the prepandemic period (pooled uaOR 0.94, 95% CI 0.91-0.98, I 2 = 62%, Figure 2 ). However, subgroup analyses revealed no differences in odds of PTB during pandemic period in national or regional studies (uaOR 0.99, 95% CI 0.94-1.03, I 2 = 76%), but there was a reduction in odds of PTB in single center studies (uaOR 0.90, 95% CI 0.86-0.94, I 2 = 12%, subgroup differences P = 0.005, Figure 2 ). Six of these studies reported adjusted estimates (with different factors adjusted, reported in Table 1 ) and pooled analyses did not show significant differences in PTB rate (pooled aOR 0.95, 95% CI 0.80-1.13; I 2 =92%; Figure 3 ). There was no reduction in unadjusted odds of PTB <34 weeks' ( 

This article is protected by copyright. All rights reserved studies of medically-indicated PTB revealed reduction in unadjusted odds of PTB during pandemic period (Table 3 , Supporting Information Appendix S7).

While most of the studies presented data for the entire pregnant population, some studies categorically excluded individuals with a known confirmed diagnosis of COVID-19. When such studies were included in meta-analyses, we identified no difference in PTB or stillbirth (for PTB: Subgroup analyses also revealed no difference in stillbirth during the pandemic period vs the prepandemic period in single-center studies and regional/national studies ( Figure 4 ). Meta-analysis of adjusted estimates from 4 studies revealed no difference in stillbirth between groups (aOR 1.06, 95% CI 0.81-1.38; I 2 =72%; Supporting Information Appendix S8).

3. Birth weight: Seven studies of 13,871 women during the pandemic period and 49,152 women in the pre-pandemic period reported birth weight. There was an increase in mean birth weight during the pandemic compared to the pre-pandemic period [(pooled mean difference 17g, 95% CI 7-28gm, I 2 =0%) Table 3 , Supporting Information Appendix S9]. There was no difference in odds of low birth weight (Table 3 , Supporting Information Appendix S10), very low birth weight (Table 3 , Supporting Information Appendix S11) or extremely low birth weight (Table 3 , Supporting Information Appendix S12).

4. Neonatal mortality: Six studies of 90, 976 neonates during the pandemic period did not show any difference in the rate of neonatal mortality between the pandemic and pre-pandemic periods (uaOR 1.34, 95% CI 0.71-2.55, I 2 =96%, Table 3 , Supporting Information Appendix S13), however, the heterogeneity of results across studies was very high. One national study from nine hospitals in Nepal 8 reported a higher neonatal mortality rate during the pandemic period that may reflect significant local impact on access to care during the lockdown period.

5. Maternal mortality: Four studies reported on maternal mortality. Three studies reported no significant difference in maternal mortality; however, one study from Mexico 34 reported significant increase in Accepted Article maternal mortality during pandemic ( Figure 5 ). The study from Mexico contributed to 98.7% weight in this analysis and it also reported that significant portion of excess mortality was due to respiratory infections including COVID-19.

In meta-regression analyses, duration of the pre-pandemic period did not emerge as a significant covariate for any outcome (P >0.05 for all outcomes). We found evidence of publication bias for PTB (Egger's P = 0.001, Supporting Information Appendix S14) but not for stillbirth (Supporting Information Appendix S15), with fewer studies reporting higher rates of PTB during the pandemic period.

In this systematic review and meta-analysis, we identified a reduction in the unadjusted odds of PTB in pandemic compared with pre-pandemic time periods, especially spontaneous PTB and medicallyindicated PTB. However, in subgroup analyses, a significant reduction in PTB was only observed in single-center studies, not in regional or national studies. Moreover, we identified no difference in odds of PTB in analysis of studies that reported adjusted estimates, although factors adjusted for, varied across the individual studies. We identified no difference in any other fetal/neonatal outcomes including stillbirths and neonatal mortality, and only a marginal increase of 17grams in mean birthweight during the pandemic period as compared with the pre-pandemic period. The increased incidence of maternal mortality noted in our meta-analysis, was mostly driven by one study from Mexico 34 which included deaths due to COVID-19, which emerged as the leading cause of maternal mortality during the pandemic period.

This review was designed to evaluate the impact of the COVID-19 pandemic time period on pregnancy and neonatal outcomes and not to evaluate studies that report only on maternal COVID-19 infection itself, which has been discussed in other reviews 46-48 . We specifically excluded studies which only reported outcomes of pregnant population infected with COVID-19. We identified conflicting evidence from the included studies based on whether they were single-center or regional/national studies.

There could be a number of reasons for this. In addition to potential referral bias, other potential explanations include variation in sample sizes, outcome definitions, lengths of the pandemic and prepandemic periods, differences in timing and enforcement of lockdown orders, failure of some studies to account for natural variation in pregnancy outcomes over time, and dissimilarities among COVID-19

This article is protected by copyright. All rights reserved mitigation strategies. 8, 10, 17, 24, 38 Moreover, the study populations were heterogeneous; for example, baseline PTB rates ranged from 4.8% to 16.7% during pre-pandemic period across the included studies; however, the change in PTB rate between periods was not baseline rate dependent. Although we didn't observe any differences in subgroups of PTB using different gestational age cut-offs (i.e., <34, <32, and <28 weeks), not all studies contributed to these analyses.

Recently, Chmielewska 49 and an increase in stillbirth (12 studies, uaOR 1.28, 95% CI 1.07-1.54) and maternal mortality. With availability of data from 13 more studies on PTB and 9 more studies for stillbirth, the results have remarkably changed, although this could also partly relate to minor differences in study inclusion criteria and data extraction. The larger number of subjects included in pooled analyses in our review has improved the precision of pooled estimates, thus increasing confidence in the findings particularly for less common secondary outcomes; however, this is the main reason for conducting this as a living systematic review so the information can be updated regularly.

The effects of lockdowns and mitigation strategies had contrasting effects in high-versus lowand middle-income countries. 49 Reports from low-resource settings described increased fear and stress among pregnant individuals, reluctance to access in-hospital care during a pandemic, financial or employment issues, childcare or home schooling challenges, maternity staff shortages, reduced access to in-hospital care, and perceived or actual reductions in available obstetric services, resulting in a significant reduction in institutional births. 8, 9, 17, 30, 31 Some reports noted a reduction in PTB and attributed this to a number of social and health behaviors associated with the pandemic, 2, 7 including decreased physical and mental stress due to better work-life balance, 6, 16, 37 better support systems and financial assistance, 16, 28 improved nutrition, better hygiene, 8, 12 reduced physical activity, 6, 16, 28, 33 reduced exposure to infection, 8, 16 , 37, 50 lower incidence of smoking and drug use due to reduced access and being indoors, 16 lower pollution exposure and levels in environment, 16, 51 and fewer medical interventions secondary to reduced antenatal surveillance. 7, 16, 37, 45 The differences in PTB findings between single-center/adjacent hospitals studies and national/regional studies could reflect a change in referral patterns due to reduced access or the fact that pregnant individuals opted to give birth in hospitals with lower prevalence of COVID-19 or in non-COVID designated hospitals. 27 Future studies are needed to explore these differences.

This article is protected by copyright. All rights reserved While we did not observe an overall change in the odds of stillbirth during the pandemic period, several individual studies, mostly single-center in scope, reported increased odds of stillbirth compared to pre-pandemic time periods. The increase in stillbirth reported by these studies was attributed to reduced antenatal surveillance, a reluctance to access in-hospital care due to increased stress and anxiety, 9, 18, 30, 33, 39 or missed appointments due to rapid changes in maternity services during the pandemic. 50 These reasons may also explain an increase in maternal mortality identified in Mexico 34 ; however, according to authors the data from government website were preliminary in scope and may change as more data are available. This could be a signal to be vigilant in attending the mother-fetus dyad during difficult public health emergency situations.

We did not find any significant differences between the pandemic and pre-pandemic periods for other outcomes, except for a marginal difference in birth weight. Since these data came from only 5 studies, further studies are needed to clarify this association, as a difference of 17 grams is unlikely to be of clinical significance. Other factors that could be responsible for the differences between study findings include variations in the etiology of adverse pregnancy outcomes in different countries, 2, 17 initiatives by local governments to provide support to those at risk for higher stress, 7 and changes to national legislation on pregnancy termination during the study period potentially influencing the incidences of stillbirth and PTB. 2, 7 A key strength of our review was the inclusion of large populations from 18 countries, mainly arising from national or state or provincial data. Most included studies came from registries or similar types of datasets. In addition, we only included studies that reported on temporal changes in outcomes in the overall population, and not data specifically from women affected by COVID-19. However, our study has limitations. There may be other relevant studies that are not yet published (and thus, not included) as the pandemic is still ongoing and many countries are facing a second or third wave of infections and associated public health restrictions. There was clinical and methodological heterogeneity across studies regarding pandemic and pre-pandemic period definitions, population bases (single-center/adjacent hospitals vs regional/national), and choices of statistical methodologies. To overcome these limitations, we planned a priori to include pre-pandemic duration in meta-regression analyses, and we conducted posthoc subgroup analyses on type of studies. We were able to explain statistical heterogeneity to an extent for both of our primary outcomes. Some studies included the entire population of pregnant women, comprising of those who did and did not have COVID-19 infection in their sample. When studies that

This article is protected by copyright. All rights reserved categorically excluded women with COVID-19 infection were included in our review, we identified no difference in PTB or stillbirth. Finally, there were insufficient studies to assess some of the pre-specified outcomes, including maternal mortality.

The COVID-19 pandemic has affected many countries with very high case numbers, such as India, Brazil, the UK, and Italy, yet large, population-based estimates on pregnancy outcomes from these countries were lacking in this review. National registries from these and other countries would be ideally suited to investigate the impact of the pandemic on perinatal health at a population level. A harmonization of methodological approaches would also facilitate the assessment of the effects of the pandemic period on fetal, neonatal, and maternal outcomes, as high methodological heterogeneity makes direct comparisons challenging. One important point to consider going forward will be that the rates of these outcomes fluctuate with natural variation over time. We hope to capture these fluctuations through three-monthly updates of this living systematic review. Future investigations should use approaches than can elucidate whether any fluctuation observed in a particular setting during the pandemic period is outside the range of expected natural variation.

In pooled analyses, we observed reductions in the unadjusted odds of PTB between the pandemic and pre-pandemic periods; especially spontaneous PTB. However, this finding was driven by singlecenter studies. There was no difference in analyses of adjusted estimates of PTB or within subgroups of PTB. Although we did not observe meaningful differences in other outcomes, including odds of stillbirth, the data were more limited and precluded a robust assessment. Higher maternal mortality reported from Mexico indicates that further studies from low-and middle-income regions highly affected by COVID-19 are needed where drastic changes in the healthcare access, healthcare availability, and personal, social and environmental factors contributed disproportionately to adverse pregnancy outcomes. Since the findings are changed between review published recently and current review, there is a need for such living systematic review which can be updated regularly. 

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This article is protected by copyright. All rights reservedWe thank Heather McDonald Kinkaid, PhD, for editorial support in preparing this manuscript. Dr.

Sinai Hospital in Toronto, Ontario, Canada, and receives a salary for her work. MiCare is supported by Sinai Health and the participating hospitals, and in turn provides organizational support for the Canadian Preterm Birth Network.