Effect of SARS-CoV-2 infection during pregnancy on maternal and perinatal mortality: a systematic review of cohort studies

Abstract

AimThe aim of this systematic review was to examine cohort studies investigating the association of this infection with maternal and perinatal mortality, especially stillbirth.MethodsAccording to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA 2020) guidelines, a search was conducted on 3 databases: PubMed, Scopus and ScienceDirect for cohort studies published up to 24 April 2022 in English or French. Studies comparing the incidence of maternal or perinatal mortality among infected and uninfected pregnant women were retained (PROSPERO registration number: CRD42022341500).ResultsInitially, 2818 articles were identified, and 24 cohort studies were included. The overall population was 1511875 pregnant women. Of seventeen studies addressing maternal mortality, six reported a significant increase in death incidence among the exposed group (RR ranging from 13.3 to 22.26). Although, three studies found no significant difference (p ≥ 0.05). Eight studies reported no maternal deaths, of which 7 were conducted in the first year of the epidemic and 5 in a single center. The association of SARS-CoV-2 infection with perinatal mortality and stillbirth was not significant in 9/17 studies. However, 6/17 studies reported a significant association (RR ranging from 1.2 to 4.7).
Factors that may influence outcomes included disease severity, body mass index, ethnicity, previous morbidities, and gestational age at the time of exposure.ConclusionThe association between SARS-CoV-2 infection and maternal mortality was contrasting. Single-center studies revealed a low risk, while larger studies indicated a high risk of death. Furthermore, the association with perinatal mortality was less strong.

Keywords

Introduction

Pregnant women were defined as a vulnerable population during the COVID-19 pandemic.¹
This is attributable to the physiological changes, which promote fetal development while reducing immunity and increasing the risk of infections.² Pregnant women are more likely than the general population to be admitted to intensive care units (ICUs) for infection by SARS-CoV-2.³ Disease severity is influenced by several factors such as maternal age, weight, comorbidities, parity, and ethnicity.⁴ The probability of vertical transmission is low. However, adverse fetal outcomes have been noted,⁵ and pregnant women were more likely to die from COVID-19 than non-pregnant.⁶
The probability of maternal death ranges from 0% to 15.78% in pregnant women infected with SARS-CoV-2.⁷ According to a living systematic review, they had an increased risk of maternal death (OR=6.09), and fetal death (OR=1.81) compared to pregnant women without the condition.⁴ Furthermore, maternal mortality and stillbirth rates have increased during the COVID-19 pandemic compared to the pre-pandemic period.⁸ This rise has varied among high-income countries and middle- and low-income countries.⁹
Although fetal mortality has reduced in high-income countries, it is considered a poor outcome in women with COVID-19.¹⁰ According to the World Association of Perinatal Medicine (WAPM), perinatal death occurred in 4.1% of women infected with SARS-CoV-2.^5,11 It occurs as a result of maternal or fetal complications.¹² SARS-CoV-2 induces placental vascular damage with episodes of hypoxia with a risk of adverse perinatal outcomes.¹⁰
Despite evidence of an increased risk of maternal and perinatal mortality associated with COVID-19 status, multiple studies have reported that the incidence of maternal and fetal death was not statically different among test-positive and test-negative women.¹³
The effect of SARS-CoV-2 infection on maternal and perinatal outcomes must be measured over the long term, given the emergence of new variants.¹⁴ Therefore, the World Health Organization has recommended in its generic protocol: COVID-19 and pregnancy, 2022 (available at the WHO website), to search for comparative data among infected and uninfected pregnant women. These studies should be longitudinal to ensure long-term monitoring.¹
Many published studies have reported data from infected cohorts of pregnant women without comparison groups.¹⁵ The primary objective of this systematic review is to examine comparative cohort studies that have investigated the association of SARS-CoV-2 infection status during pregnancy and the risk of maternal and perinatal mortality. The second objective is to identify factors that may influence this association.

Materials and Methods

1. Search StrategyThis systematic review was conducted in accordance with the PRISMA 2020 (preferred reporting items for systematic reviews and meta-analyses) guidelines.¹⁷ The protocol was registered and published on PROSPERO (registration number: CRD42022341500).
Two authors (K.O. and A.K.) independently queried three databases: Scopus, PubMed and ScienceDirect. Concerning Scopus and PubMed, the search for articles was done using two queries, first: (“COVID-19” or “SARS-CoV-2” or “Coronavirus” and “maternal mortality” or “maternal death”) and secondly: (“COVID-19” or “SARS-CoV-2” or “Coronavirus” and “perinatal mortality” or “perinatal death” or “stillbirth”). For ScienceDirect, the formula was as follows: ((“COVID-19” or “SARS-CoV-2” or “Coronavirus”) and (“maternal-death” or “maternal mortality” or “perinatal mortality” or “perinatal death” or “stillbirth”)).2. Selection ProcessWe included in this systematic review cohort studies published in English or French up to 24 April 2022. Initially, titles and abstracts were selected for relevant articles by 2 authors independently (K.O. and A.K.). Duplicate articles are eliminated using Zotero 6.0.18 (free version). A third reviewer (M.O.) was solicited to decide if there was disagreement between the two examiners. The included articles were retrieved in full text for further evaluation.3. Eligibility CriteriaArticles eligible for inclusion were comparative cohort studies that met the following criteria: 1) prospective or retrospective cohort studies; 2) studies that investigated the occurrence of maternal and/or perinatal death among pregnant women diagnosed with COVID-19 during pregnancy or at delivery (confirmed positive test) compared to pregnant women with negative test during the same investigation period.
Exclusion criteria were: 1) studies comparing the risk of mortality in SARS-CoV-2 infected pregnant women with that of pregnant women in the pre-pandemic period or non-pregnant women of childbearing age. 2) studies defined by their authors as cross-sectional, case-control, or cohort studies with no comparison group.4. Outcomes and Data Collection ProcessThis review compared SARS-CoV-2 infected and non-infected pregnant women with regard to the occurrence of the following outcomes:
a) maternal mortality: death of a woman, either during pregnancy or childbirth, from any cause related to or aggravated by pregnancy, or within 42 days of the end of pregnancy.¹⁸
b) perinatal mortality: incorporate stillbirth and early neonatal mortality (death of a child born alive and within the first 7 days of life).¹⁹
c) stillbirth: the birth of a baby without signs of life after 20 weeks of gestation.²⁰
The first author (K.O.) collected data from the included studies. The collected information was verified by another author (A.K.). A third author (M.O.) was asked to decide in case of disagreement.
The results were presented in three tables. The first lists the characteristics of the included studies. The second and third tables show the results of the maternal mortality studies and the perinatal mortality studies respectively. Quantitative data were expressed as numbers and proportions (N; %), odds ratios, relative and adjusted relative risks (with 95% CI). Results were considered statistically significant (p<0.05). A narrative synthesis of the findings was performed.Quality Assessment of StudiesThe quality assessment was conducted by two independent reviewers (K.O. and A.K.) using the JBI cohort study critical assessment checklist, 2017 (available at the jbi.global website). This checklist, approved by the Joanna Briggs Institute scientific committee, assesses the quality of cohort studies according to 11 items: 1) population and study groups; 2) and 3) similarity and validity of exposure measurement; 4) and 5) identification and managing of confounding factors; 6) and 7) validity of outcome measurement; 8) to 10) duration and continuity of follow-up; 11) statistical analysis quality. The checkboxes were: yes, no, unclear or not applicable.
Agreement between the examiners was assessed using the statistical coefficient kappa (κ).5. statistical AnalysisNot applicable.

Results

1. Characteristics of Included Studies Initially, 2818 articles were identified. After removing duplicates, screening by title and abstract and then by full text was performed according to the eligibility criteria. Finally, 24 cohort studies were included for the systematic review (figure 1). The total duration of these studies extended from January 13, 2020, to July 4, 2021 (table 1). Eleven cohort studies had a prospective design.^20,30 Twelve studies were retrospective.^15,31,41 and there was one cohort with a retro-prospective design.⁴² Fourteen studies were multicenter.^{20,23,26,28,31,34,36,39,41} including a multinational study.²⁸ Ten studies were single-center.^{15,21,22,24,25,27,29,30,40,42} The overall population included in this review was 1,511,875 pregnant women, with 30,633 testing positive for SARS-CoV-2 infection and 1,481,242 testing negative. Five studies focused on maternal death.^{20,21,31,32,42} seven on perinatal death.^22,24,33,36 and twelve on both mortalities.^{15,25,30,37,40} 2. Assessment of the Quality of the Studies Included studies were assessed using the JBI cohort study critical assessment checklist. The results of the study assessment were detailed in supplementary material. For all studies, the study groups were recruited from the same population, and the exposure measure was similar and valid, with ambiguities in the two studies.^22,27 Confounding factors were identified in most studies (20/22), while strategies to address these confounders were indicated in 65% of these studies (13/20). The validity of outcomes measurement and duration of participant follow-up were overall appropriate. Regarding the statistical analysis, regression was used in 45% of the studies (11/24). The reviewers agreed that, in all, the included studies had a low risk of bias. The quality was considered “good” and the statistical coefficient of kappa was κ = 0.71. 3. Association of SARS-CoV-2 Infection During Pregnancy With the risk of Maternal Mortality As shown in table 2, eight studies reported no maternal mortality.^{20,25,27,29,30,32,40} In contrast, the occurrence of maternal death in pregnant women with SARS-CoV-2 was reported in nine cohort studies.^{15,21,28,31,37,39,41,42} Three of these studies concluded that there was a high association between SARS-CoV-2 exposure in pregnancy and the occurrence of maternal death.^29,38,39 However, a retrospective single-center study found no significant association between COVID-19 status and maternal mortality.¹⁵ Indeed, a multinational study including 18 countries showed that COVID-19 exposure during pregnancy was highly associated with an increased incidence of maternal mortality, with RR: 22.26 (2.88–172.11) (95% CI).²⁸ Similarly, based on analysis of data from 720 American hospitals, the risk of maternal death was 25.6 times higher among pregnant women with COVID-19 who delivered and 13.3 among all hospitalized pregnant women with COVID-19, including pregnancies that did not proceed to birth.³⁷ In addition, a cohort study conducted in 703 US hospitals found that women with a confirmed diagnosis of SARS-CoV-2 at the time of hospitalization for delivery had a 17-fold increased risk of death compared to the unexposed group.³⁸ Five cohort studies compared the incidence of maternal mortality among pregnant women exposed and unexposed to SARS-CoV-2 infection during pregnancy using the Chi2 test and/or the Fisher’s exact test.^{21,31,39,41,42} Of these, three studies found that there was an increased incidence of maternal death for pregnant women infected by the SARS-CoV-2.^21,39,41 However, two studies reported that the rates of maternal death in the exposed group were slightly higher than in the unexposed group, but this difference was not statistically significant.^31,42 To investigate factors influencing the association of SARS-CoV-2 infection during pregnancy with the risk of maternal mortality, four studies divided the study population into subgroups and assessed this association in each subgroup.^28,37,39,41 Stratification variables included severity of infection, maternal age, race/ethnicity, body mass index, previous morbidities, and gestational age at exposure (table 2). 4. SARS-CoV-2 Infection During Pregnancy and the risk of Perinatal Mortality As presented in table 3, seventeen cohort studies reported the occurrence of perinatal mortality in pregnant women diagnosed with COVID-19. Four of these studies reported a significant association between this exposure during pregnancy and the risk of stillbirth. This ranges from 1.2 to 4.7.^25,33,37,38 Also, a multicenter cohort study noted a significantly high incidence of stillbirths among the infected group (0.8%) compared with the matched uninfected group (0.1%), (p<0.05).³⁵ In addition, the multinational study by Villar et al. observed that newborns born to exposed mothers had a high perinatal morbidity and mortality index (PMMI) compared with those born to unexposed mothers (RR= 2.14). Using regression, three studies found an insignificant association between SARS-CoV-2 infection status during pregnancy and the risk of stillbirth.^22,34,36 In addition, five cohort studies concluded that there was no significant difference in fetal death incidence among the exposed and unexposed groups.^23,27,39,41 Also, the variation in stillbirth incidence between asymptomatic women with SARS-CoV-2 and uninfected pregnant women was not statistically significant (p>0.05).²⁶ Factors influencing the association between SARS-CoV-2 infection and the risk of perinatal mortality or stillbirth were assessed in eight studies.^{23,28,34,35,37,39,41} The risk of stillbirth was slightly higher in women aged ≥25 years, however, there was no significant difference between ethnic subgroups.³⁷ In addition, it was noted that symptomatic women and women with high body mass index or previous morbidities were more likely to have severe perinatal morbidity and mortality.²⁸ The influence of gestational age at infection on stillbirth incidence was discussed in four studies.^34,35,40,41 Finally, two single-center studies reported that there were no stillbirths in the study population.^24,30

Discussion

In the present review, six cohort studies showed that there was a high association between SARS-CoV-2 infection during pregnancy and the incidence of maternal death. According to a living systematic review and meta-analysis of eight studies, the probability of all-cause mortality in pregnant women with COVID-19 was higher compared to pregnant women without the disease.⁴ Another meta-analysis indicated that the probability of maternal death related to SARS-CoV-2 infection is high (pooled OR: 7.05.^2,41,20,65 ).⁴³ In contrast, a meta-analysis of six comparative studies showed that there was no significant difference in maternal mortality rates in relation to COVID-19 status (p=0.23).¹³
Eight included studies found no maternal deaths in pregnant women with SARS-CoV-2. Of these, seven were conducted during the first year of the pandemic and the majority were monocentric. Maternal death is an uncommon event requiring a large study population and a follow-up until six weeks after delivery to obtain valid results. Furthermore, the absence of symptoms may explain this finding; an included single-center study with no deaths indicated that 86.24% of infected women were asymptomatic.²⁰ Other systematic reviews reported that no maternal deaths occurred among infected women.^43,45 Similarly, a meta-analysis of data of the early pandemic revealed no deaths among 348 cases recorded.⁴⁶
In the current review, countries concerned by the increase in maternal deaths related to COVID-19 were the USA in four studies,^37,39,41 Romania,²¹ and eighteen countries included in a multinational study.²⁸ A meta-analysis of recent studies conducted in low-resource countries showed an increased incidence of death in pregnant women who tested positive.⁴⁷ Among the countries suffering most from this issue, Brazil recorded high maternal mortality rates during the outbreak.⁴⁸
Regarding the determinants of the association between SARS-CoV-2 infection and maternal mortality risk, symptomatic pregnant women or those with a history of morbidity or overweight had a high incidence of maternal death.²⁸ Similarly, a meta-analysis found that all 153 pregnant and postpartum women who died due to COVID-19 were symptomatic and suffered from morbidities such as diabetes, overweight, cardiovascular diseases, and asthma.⁹ A systematic review of 14 articles showed that high BMI or comorbidities were risk factors for mortality associated with SARS-CoV-2 infection.⁴⁹ In our review, maternal age over 35 years increased the risk of maternal death.³⁷ In another systematic review, 41.7% of died infected mothers were older than 35 years.⁹
In terms of perinatal death, six studies in this review found a significant association between SARS-CoV-2 infection during pregnancy and the risk of stillbirth. This is consistent with many systematic and meta-analyses, which have reported high odds ratio values (OR=2.70),⁵⁰ (pooled OR 1.46),⁴³ (OR=2.11),⁵¹ and (OR=2.36).⁵² In the opposite, nine included cohort studies revealed that SARS-CoV-2 exposure did not significantly influence the incidence of stillbirth. In agreement, this incidence was 1.1% in both groups according to a meta-analysis of six comparative studies.¹³ Another meta-analysis found that the risk of fetal death from COVID-19 was extremely low.⁵³
In the current review, the probability of stillbirth was slightly higher among women over 25 years.³⁷ However, a discrepancy has been observed regarding the effect of severity of infection, gestational age, and weight on this probability. Indeed, an included multinational cohort study noted that symptomatic women with a high body mass index were more likely to have a perinatal death.²⁸ The fetal death rate was higher in asymptomatic or mildly affected women,³⁹ and was not correlated with either BMI or gestational age.⁴⁰ Besides, the incidence of stillbirth was higher in women infected within 30 days of delivery.⁴¹ While, it was higher among women infected in the first or second trimester.³⁵ This discrepancy can be explained by sample size limitations in monocentric studies and retrospective data collection, mainly under-recording of patient information.
Most studies in this review involved pregnant women infected at or near the time of delivery. A review of maternal and fetal outcomes related to COVID-19 showed that the third trimester was the most vulnerable period for infection.⁵⁴Strengths and Limitations of the StudyThis systematic review had several strengths and limitations. It included comparative cohort studies allowing for follow-up of outcomes in and without the exposure. In addition, cohort studies comparing outcomes with the pre-pandemic period were eliminated to avoid confounding the impact of the COVID-19 pandemic on healthcare services. However, the unavailability of some data or full-text articles reduced the number of included studies.
The overall study period was from the beginning of the pandemic until July 2021, which provided a large study population (1,511,875 pregnant women). However, the data collected did not cover new variants such as Omicron, which appeared for the first time on 9 November 2021. In addition, the influence of vaccination status was not studied because the SARS-CoV-2 vaccine was contraindicated for pregnant women during the early pandemic.
The retrospective design of many cohort studies did not provide a real-time follow-up of outcomes related to SARS-CoV-2 infection. Nevertheless, there were more prospective than retrospective studies.
Therefore, meta-analyses of recent large-sample multicenter studies are recommended to compare the effect of infection with different variants of SARS-CoV-2 and vaccine coverage on maternal and fetal outcomes, including maternal and perinatal mortality.

Conclusion

The findings of included cohort studies regarding the association of SARS-CoV-2 infection during pregnancy with the risk of maternal and perinatal mortality varied.
Studies covering the early months of the pandemic noted that the risk of maternal mortality was low. However, larger studies reported that women exposed to SARS-CoV-2 infection during pregnancy have a higher risk of maternal mortality than those unexposed. Factors that may influence this association include the severity of COVID-19 disease, co-morbidities, overweight, maternal, gestational age, and ethnicity. On the other hand, according to findings of studies that have addressed perinatal mortality, the association of SARS-CoV-2 infection and the risk of stillbirth was lower than the association of this condition with maternal death.

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