Journal List > Obstet Gynecol Sci > v.66(4) > 1516083262

Jeong and Kim: The coronavirus disease 2019 infection in pregnancy and adverse pregnancy outcomes: a systematic review and meta-analysis

Abstract

The coronavirus disease 2019 (COVID-19) outbreak which started in December 2019 rapidly developed into a global health concern. Pregnant women are susceptible to respiratory infections and can experience adverse outcomes. This systematic review and meta-analysis compared pregnancy outcomes according to COVID-19 disease status. The MEDLINE, EMBASE, and Cochrane Library databases were searched for relevant articles published between December 1, 2019, and October 19, 2022. Main inclusion criterion was any population-based, cross-sectional, cohort, or case-control study that assessed pregnancy outcomes in women with or without laboratory-confirmed COVID-19. Sixty-nine studies including 1,606,543 pregnant women (39,716 [2.4%] diagnosed with COVID-19) were retrieved. COVID-19-infected pregnant women had a higher risk of preterm birth (odds ratio [OR], 1.59; 95% confidence interval [CI], 1.42–1.78), preeclampsia (OR, 1.41; 95% CI, 1.30–1.53), low birth weight (OR, 1.52; 95% CI, 1.30–1.79), cesarean delivery (OR, 1.20; 95% CI, 1.10–1.30), stillbirth (OR, 1.71; 95% CI, 1.39–2.10), fetal distress (OR, 2.49; 95% CI, 1.54–4.03), neonatal intensive care unit admission (OR, 2.33; 95% CI, 1.72–3.16), perinatal mortality (OR, 1.96; 95% CI, 1.15–3.34), and maternal mortality (OR, 6.15; 95% CI, 3.74–10.10). There were no significant differences in total miscarriage, preterm premature rupture of membranes, postpartum hemorrhage, cholestasis, or chorioamnionitis according to infection. This review demonstrates that COVID-19 infection during pregnancy can lead to adverse pregnancy outcomes. This information could aid researchers and clinicians in preparing for another pandemic caused by newly discovered respiratory viruses. The findings of this study may assist with evidence-based counseling and help clinicians manage pregnant women with COVID-19.

Introduction

Coronavirus disease 2019 (COVID-19) is a viral respiratory disease caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). It has been a global threat to public health owing to its high mortality and morbidity rates since the first outbreak in Wuhan, China, in December 2019. According to the World Health Organization, as of November 30, 2022, there were 639,132,486 confirmed cases of COVID-19 globally, including 6,614,082 deaths.
The experience of patients infected with COVID-19 varies significantly, ranging from asymptomatic to acute respiratory distress syndrome accompanied by high fever and severe respiratory symptoms, similar to those of the Middle East respiratory syndrome (MERS) and the SARS outbreak in 2003. Pregnant women undergo immunological and physiological changes that prevent fetal allograft rejection. These changes also increase their susceptibility to viral respiratory infections. The SARS outbreak in 2003 and MERS were associated with high fatality rates, with one-third of the infected pregnant women dying.
During the pandemic, pregnant women experienced considerable fear of the respiratory virus, besides anxiety regarding outcomes because it was unknown how the new viral outbreaks would affect pregnancy and neonatal prognosis, and vaccine safety has not been verified. Previous studies have reported increased rates of miscarriage, intrauterine growth retardation (IUGR), premature delivery, and fetal death during MERS. Furthermore, viral respiratory infections are a leading cause of maternal mortality [1,2].
The pregnancy and neonatal outcomes associated with COVID-19 are inconsistent and diverse. Some studies have indicated that SARS-CoV-2 infection is not associated with adverse pregnancy outcomes [3,4]. Large-scale data analyses have stressed the urgency of establishing strategies to help clinicians manage pregnancies and ensure safe maternal and childcare deliveries. This systematic review and meta-analysis were based on a thorough review of the existing literature. We investigated the association between COVID-19 infection during pregnancy and adverse pregnancy outcome to aid clinicians and researchers in managing pregnant women infected with COVID-19 currently and contribute to preparations for future respiratory virus outbreaks.

Search strategy

We searched the literature to identify articles that compared obstetrical and neonatal outcomes between COVID-19-infected and non-infected mothers. This systematic review and meta-analysis were conducted using the PROSPERO protocol (CRD42023402238). We performed a systematic online search of the MEDLINE, EMBASE, and Cochrane Library databases for relevant articles published until October 19, 2022. The databases were searched using a combination of Medical Subject Headings and text terms related to COVID-19 and pregnancy outcomes. The detailed search strategy used for each database is presented in Supplementary Table 1. Two reviewers (M.A.K. and Y.J.) independently selected studies. They first performed title and abstract screening and then assessed the full texts of the selected studies for eligibility according to the inclusion criteria. They cross-checked previously published review articles to identify additional studies that were missed during our online searches. Discrepancies were resolved by consensus-based discussions.

Study selection

We selected full-text articles that reported the impact of COVID-19 on obstetrical and neonatal outcomes by comparing infected and non-infected mothers and those that met the inclusion criteria as follows. 1) A population-based, cross-sectional, cohort, or case-control study design. 2) Inclusion of laboratory-confirmed non-infected pregnant women or pregnant women before the pandemic as a control group. 3) The study population included pregnant women with laboratory-confirmed COVID-19 infection at any stage of gestation, or pregnant women with assigned codes for COVID-19 based on the International classification of disease 10th version and related health problems. 4) Results included pregnancy or neonatal outcomes according to the COVID-19 infection status.
Outcomes, such as miscarriage, preterm birth, preeclampsia, cesarean section, intrauterine fetal death (IUFD) or stillbirth, preterm premature rupture of membranes (PPROM), placental abruption, placenta previa, postpartum hemorrhage, and maternal mortality were assessed as obstetric outcomes. IUGR, small for gestational age (SGA), low birth weight (LBW), neonatal intensive care unit (NICU) admission, and perinatal mortality were assessed as neonatal outcomes. Studies that met the following criteria were excluded: case reports, case series, review articles, editorials or letters to the editor, conference abstracts, lack of a control group, publications other than English, and inadequate information for data extraction.

Data extraction

We reviewed the full-text articles for complete data extraction and clarity if the details were not explicitly mentioned in the abstracts. The information extracted from each study included the first author’s name, publication year, journal name, study design, country, study period, inclusion and exclusion criteria, and the number of women included in the case and control groups.

Quality assessment

The Newcastle-Ottawa scale (NOS) was used to assess the quality of the included studies. The NOS evaluates studies from three perspectives: study group selection, group comparability, and exposure or outcome of interest for case-control or cohort studies. According to the NOS, each study was awarded a maximum of nine points with scores for various questions in each domain. Studies were considered of high quality if they had a NOS score ≥6.

Statistical analysis

This systematic review and meta-analysis were conducted according to the protocols established in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines and the Cochrane handbook for systematic reviews. We used a random-effects model to calculate the pooled odds ratios (ORs) and 95% confidence intervals (CIs) for adverse pregnancy outcomes experienced by women with or without COVID-19 infection. Heterogeneity was assessed using the I2 statistic; values of >25%, >50%, and >75% were considered evidence of low, moderate, and considerable statistical heterogeneity, respectively. A sensitivity analysis was conducted to evaluate the influence of individual studies on the meta-analysis by restricting the studies individually and assessing the effect on the main summary estimate. Significance levels were set at P<0.05 if the 95% CI did not include 1. All statistical analyses were performed using RevMan (version 5.4; The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark).

Study characteristics

The database search identified 4,279 citations, of which 4,108 were excluded from the title and abstract review. The remaining 171 citations were considered eligible for full-text screening, of which 69 met the inclusion criteria and were considered eligible for inclusion in the meta-analysis (Fig. 1). Table 1 presents the baseline characteristics of the 69 included studies. These studies included 39,716 pregnant women with COVID-19 and 1,566,827 pregnant women without COVID-19. Reverse transcriptase-polymerase chain reaction was used as a diagnostic method to confirm COVID-19 in most studies [3,571].

Preterm birth

Fifty studies reported the incidence of preterm births in 2,687 (10.3%) women with COVID-19 infection versus 58,203 (6.1%) women without the infection, demonstrating a significant difference (P<0.001). The risk of preterm birth was significantly (1.6-fold) higher among women with COVID-19 than those without (OR, 1.59; 95% CI, 1.42–1.78; I2=69%; Fig. 2A). Most studies did not accurately describe the indications for preterm birth. When only the eight studies that classified spontaneous preterm births were analyzed, the odds were 1.3-fold higher in women with COVID-19 than those without (OR, 1.33; 95% CI, 1.20–1.48; I2=22%; Fig. 2B).

Preeclampsia

Thirty-four studies reported that preeclampsia occurred in 2,214 of 27,732 women with COVID-19 (8.0%) versus 78,429 of 1,358,619 women without COVID-19 (5.8%), demonstrating a significant difference (OR, 1.41; 95% CI, 1.30–1.5; I2=31%; Fig. 3A).

Low birth weight

Twelve studies reported that 987 neonates had LBW, including 407 born to women with COVID-19 and 580 born to women without COVID-19. The risk of LBW was significantly higher among the offspring of women with COVID-19 infection than those born to women without the infection (OR, 1.52; 95% CI, 1.30–1.79; I2=6%; Fig. 3B).

Cesarean section

Fifty-seven studies reported the incidence of cesarean sections in 1,484,791 pregnant women. Women who experienced the COVID-19 infection during pregnancy were 1.2-fold more likely to deliver by a cesarean section than those without (OR, 1.20; 95% CI, 1.10–1.30; I2=79%; Fig. 4A).

IUFD or stillbirth

Twenty-seven studies reported the incidence of IUFD or stillbirth in 256 women with COVID-19 and 6,730 women without COVID-19. The odds of IUFD or stillbirth were higher in women with COVID-19 than those without (OR, 1.71; 95% CI, 1.39–2.10; I2=27%; Fig. 4B).

Fetal distress, NICU admission, and perinatal mortality

Seven studies reported the incidence of fetal distress in 169 women with COVID-19 and 577 women without COVID-19. We observed a statistically significant increase in fetal distress among women with COVID-19 than those without (OR, 2.49; 95% CI, 1.54–4.03; I2=69%; Fig. 5A). Thirty-one studies reported the NICU admissions of 12,397 neonates (1,187 with COVID-19 and 11,210 without COVID-19). The overall risk of NICU admission was significantly higher among women with COVID-19 infection than those without (OR, 2.33; 95% CI, 1.72–3.16; I2=89%; Fig. 5B). Perinatal mortality occurred in 27 of 4,123 (0.65%) cases with COVID-19 versus 105 of 14,474 (0.73%) cases without COVID-19 among a total of 21 studies (OR, 1.96; 95% CI, 1.15–3.34; I2=0%; Fig. 5C).

Maternal mortality

Twelve studies reported the incidence of maternal mortality in 39 of 9,633 women (0.40%) with COVID-19 versus 90 of 494,811 women (0.02%) without COVID-19, revealing a significant difference between the two (P<0.05). COVID-19 infection during pregnancy resulted in an increased risk of maternal mortality relative to those who were not infected (OR, 6.15; 95% CI, 3.74; I2=62%; Fig. 5D).

Other outcomes

Pregnant women with COVID-19 had a higher risk of placental abruption (OR, 1.40; 95% CI, 1.02–1.92; I2=19%; 12 studies), IUGR or SGA (OR, 1.12; 95% CI, 1.0–1.26; I2=48%; 27 studies), gestational diabetes mellitus (OR, 1.13; 95% CI, 1.04–1.23; I2=45%; 40 studies), and congenital anomalies (OR, 1.45; 95% CI, 1.04–2.01; I2=0%; eight studies) (Supplementary Fig. 1). No significant differences were observed in the total miscarriage rates (OR, 1.04; 95% CI, 0.64–1.60; I2=74%; 13 studies), the incidences of PPROM (OR, 1.36; 95% CI, 0.96–1.93; I2=26%; 10 studies), postpartum hemorrhage (OR, 0.98; 95% CI, 0.78–1.24; I2=70%; 22 studies), cholestasis (OR, 1.34; 95% CI, 0.83–2.18; I2=0%; seven studies), or chorioamnionitis (OR, 1.26; 95% CI, 0.93–1.72; I2=38%; 14 studies) between women with and without the COVID-19 infection (Supplementary Fig. 2).

Conclusion

COVID-19 has spread rapidly worldwide and become a global health concern. It is associated with various complications, including high mortality and morbidity rates ranging from pulmonary distress to death. Pregnant women are susceptible to respiratory infections and can experience adverse outcomes. In this updated systematic review and meta-analysis, we described the obstetric and neonatal outcomes of COVID-19-infected versus non-infected pregnant women. We also investigated the effects of COVID-19 infection during pregnancy on adverse pregnancy outcomes by comparing the obstetric and neonatal outcomes of COVID-19-infected versus non-infected pregnant women.
Adverse pregnancy outcomes were more common in pregnant women with COVID-19 than in those without. This review revealed that COVID-19 during pregnancy is associated with an increased risk of cesarean delivery, preterm birth, preeclampsia, IUFD or stillbirth, gestational diabetes mellitus, IUGR or SGA, and LBW. Moreover, COVID-19 infection during pregnancy can lead to an increased risk of neonatal complications, such as fetal distress, NICU admission, and perinatal mortality. Furthermore, COVID-19 negatively affected maternal mortality.
These findings are consistent with those of previous studies [72]. Allotey et al. [2] reported that COVID-19 infection during pregnancy increases the risk of preterm birth, LBW, NICU admission, and stillbirth. Lassi et al. [73] reported a 2-fold increased risk of preterm birth in women with severe symptomatic COVID-19. Pathirathna et al. [74] suggested that pregnant women with COVID-19 have an increased risk of maternal death, preeclampsia, cesarean delivery, fetal distress, preterm birth, LBW, NICU admission, and stillbirth. In contrast, Huntley et al. [75], and Wei et al. [76] reported that COVID-19 infection during pregnancy did not increase the risk of cesarean delivery. Nevertheless, Wei et al. [77] reported that the risk of preterm birth, cesarean delivery, and preeclampsia increased with the presence and severity of COVID-19 symptoms.
Previous studies have reported that the most common obstetric complications associated with COVID-19 are PPROM, postpartum hemorrhage, cesarean delivery, and preterm birth [78,79]. The inflammatory reaction associated with infection can lead to the destruction of placental function and the subsequent development of adverse pregnancy outcomes [18,58,80]. Cesarean section is the preferred delivery route in COVID-19-positive pregnancies. The higher rate of cesarean sections compared to the current cesarean delivery rate of 30% could be due to changes in the obstetric management protocols influenced by the infectious disease management policy of the institution; this could also be attributed to disease progression caused by COVID-19. This finding is consistent with the results of another meta-analysis. Since most studies examined did not specify the indications for cesarean sections, this could not be accurately analyzed.
The present review demonstrates that COVID-19 infection during pregnancy is associated with an increased risk of preeclampsia. Pérez-López et al. [81] reported that preeclampsia and hypertensive disorders of pregnancy were more common in COVID-19-infected pregnant women regardless of the presence or severity of their symptoms. Other studies reported a positive association between preeclampsia and COVID-19 during pregnancy [74,77,82,83]. Multiple mechanisms are involved in the pathogenesis of preeclampsia in pregnant women with COVID-19. SARS-CoV-2 binds to cell membrane angiotensin-converting enzyme 2, which plays an important role in the renin-angiotensin system (RAS). RAS controls trophoblast proliferation, angiogenesis, and uteroplacental blood flow. COVID-19 can alter RAS function via its downregulation, which induces preeclampsia. Moreover, the infected placenta shows a decreased expression of angiotensin-conversing enzyme 2 receptors concurrent with increased production of soluble fms-like tyrosine kinase-1, which has been implicated in the pathogenesis of preeclampsia. Garrido-Pontnou et al. [84], and Hecht et al. [85] reported that infected COVID-19 term placentas demonstrated villous trophoblast necrosis, inflammatory infiltration, and fibrinoid deposition. The authors suggest that these placental mechanisms against infection could contribute to adverse pregnancy outcomes.
Moreover, COVID-19 infection during pregnancy increases the risk of preterm birth. However, a previous study reported that the preterm birth rate during the pandemic was lower than that in the pre-pandemic era [86]. In this review, we did not address the causes of preterm birth, whether spontaneous or medically induced. Even when analyzing spontaneous preterm births, we observed that the risk of spontaneous preterm births was significantly higher in women with COVID-19 than in those without. Neonates born to women with COVID-19 had a higher NICU admission risk than those born to non-infected women. This finding is consistent with those of previous studies. Furthermore, COVID-19 increases the risk of fetal distress and perinatal mortality.
Pregnant women are categorized as immunosuppressed because they undergo immunological and physiological changes during pregnancy that prevent fetal allograft rejection [87]. Hence, pregnant women are more susceptible to respiratory infections than does the general population. Moreover, the physiological changes in the cardiopulmonary system in pregnant women can worsen the symptoms of respiratory infections. Furthermore, an elevated diaphragm, increased oxygen demand, and generalized edema, including that in the bronchial mucosa, experienced by pregnant women are risk factors for hypoxia [88,89]. Previously, influenza A subtype H1N1 virus, SARS-CoV, and MERS infections have demonstrated more systemic complications in pregnant women than in the general population [90,91]. However, unlike other respiratory viruses, the severity of COVID-19 remains relatively low. A previous study reported that the laboratory findings, clinical presentations, and radiological findings of pregnant women with COVID-19 were similar to those of non-pregnant women [11]. Several hypotheses have been proposed to explain these findings. One of them is that COVID-19 is caused by a novel ribonucleic acid mutation. Furthermore, concurrent with pregnancy, adaptive organ changes to offset fetal rejection may have resulted in a protective effect against the virus [92]. The process of immunological adaptation, which starts during pregnancy, may be the key to the milder symptoms of COVID-19 noted during pregnancy.
Vertical transmission was not considered in the present study. A previous review reported that vertical transmission of SARS-CoV-2 was rare and not detected in nasopharyngeal swabs of neonates, cord blood, or amniotic fluid [80]. Other studies have also reported very little evidence to support the vertical transmission of COVID-19 [81,83].
Although a few studies have investigated breastfeeding with COVID-19 infection, previous studies have reported conflicting results. Some researchers do not recommend breastfeeding when a nursing mother is infected, whereas others suggest that breastfeeding while wearing a mask should be practiced. Additionally, the virus is not believed to be transmitted through breast milk. However, further studies to confirm this hypothesis are warranted [80,9396].
This review has several strengths. As the studies included in this review were extracted from multiple countries, our findings can be generalized globally and interpreted regardless of race or country. The present systematic review compared the pregnancy outcomes of COVID-19-infected and non-infected pregnant women and did not investigate the general population. The selection bias was low owing to the high threshold of the inclusion criteria. This review also included a larger number of studies than previous reports. This review demonstrated that COVID-19 has a worse effect on outcomes, such as preterm birth, cesarean section, and placental abruption, compared with the outcomes reported in previous studies.
This study also has several limitations. First, the disease remains prevalent globally, causing additional alterations in public health restrictions. However, prospective randomized studies on viral infections are not applicable to pregnant women. Therefore, we included only retrospective, nonrandomized studies in this review. Second, the studies included in this report were conducted in multiple countries, and their baseline characteristics were highly heterogeneous including the types of COVID-19 variants. Third, we were unable to access the raw data analyzed in these studies. Fourth, this study did not analyze infections according to pregnancy trimesters. The pregnancy trimester at the infection time could be a significant factor in adverse pregnancy outcomes, as respiratory infections in early pregnancy can critically impact organogenesis. Fifth, this review did not assess indications for the delivery route.
As the global spread of COVID-19 continues, it is imperative to determine further its impact on pregnancy outcomes to prepare for future outbreaks. Pregnant women are particularly susceptible to respiratory infections, which can lead to high pregnancy morbidity and mortality rates. The findings of this review and meta-analysis provide sufficient information to enable evidence-based counseling and help clinicians manage pregnant women with COVID-19.

Notes

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The study is not applicable to Institutional Review Board.

Patient consent

No informed consent was obtained from the patients because the study was retrospective.

Funding information

None.

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Fig. 1
Flowchart of the study selection process. COVID-19, coronavirus disease 2019.
ogs-22323f1.gif
Fig. 2
Forest plots of the summary crude odds ratios and 95% confidence intervals for the association between coronavirus disease 2019 and preterm delivery (A) and spontaneous preterm delivery (B). SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; CI, confidence interval.
ogs-22323f2.gif
Fig. 3
Forest plots of the summary crude odds ratios and 95% confidence intervals for the association between coronavirus disease 2019 and preeclampsia (A) and low birth weight (B). SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; CI, confidence interval.
ogs-22323f3.gif
Fig. 4
Forest plots of the summary crude odds ratios and 95% confidence intervals for the association between coronavirus disease 2019 and cesarean section (A) and IUFD or stillbirth (B). SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; CI, confidence interval; IUFD, intrauterine fetal death.
ogs-22323f4.gif
Fig. 5
Forest plots of the summary crude odds ratios and 95% confidence intervals for the association between coronavirus disease 2019 and fetal distress (A), NICU admission (B), perinatal mortality (C), and maternal mortality (D). SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; CI, confidence interval; NICU, neonatal intensive care unit.
ogs-22323f5.gif
Table 1
Baseline characteristics of included studies
Author Year Study design Study location Study period COVID test result (positive) Sample size COVID test method
Hanna M. Shepard 2022 Retrospective USA From 2020-03-01 to 2021-03-31 3,119 69,960 RT-PCR
Helga Vera von Bargen 2022 Prospective, cross-sectional Chile From 2020-04-15 to 2020-06-15 68 701 RT-PCR
Ian Griffin 2020 Prospective observational USA From 2020-04-21 to 2020-05-05 27 62 RT-PCR
Wei Liu 2020 Retrospective China From 2020-01-17 to 2020-03-04 32 48 Nasopharynx swab, chest CT
Oscar Martinez Perez 2020 Population-based, longitudital observational and anlaytic Spain From 2020-03-01 to 2020-05 246 1,009 RT-PCR
Amanda Dhyvetter 2021 Retrospective USA From 2020-04-12 to 2020-07-11 23 208 RT-PCR
Rong Yang 2020 Retrospective, population-based cohort China From 2020-01-13 to 2020-03 65 11,078 RT-PCR
Charles M’poca Charles 2022 Prospective cohort study Mozambique From 2020-10-20 to 2021-07-22 22 239 RT-PCR
Arun Harishchandra Nayak 2020 Restrospective observational analytical India From 2020-04-01 to 2020-05-15 141 977
Seyed-Abdolvahab 2021 Retrospective case-control Iran From 2020-03-01 to 2020-11-01 55 110
Jack Milln 2021 Retrospective cross-sectional UK From 2020-03-12 to 2020-04-22 32 1,316
Emily H. Adhikari 2020 Observational cohort USA From 2020-03-18 to 2020-08-22 252 3,374 RT-PCR
Mia Ahlberg 2020 Retrospective case-control Sweden From 2020-03-25 to 2020-07-24 155 759 RT-PCR
M Prabhu 2020 Prospective cohort study USA From 2020-03-22 to 2020-03-24 70 675 RT-PCR
Na Li 2020 Restrospedtive case control China From 2020-01-24 to 2020-02-29 16 137 RT-PCR
Valerie J. Flaherman 2021 Prospective cohort study USA From 2020-03-22 to 2020-06-22 179 263 RT-PCR
Francesca Crovetto 2021 Prospective population-based cohort Spain From 2020-03-15 to 2020-05-31 317 2,225 RT-PCR
Andrea G. Edlow 2020 Propective cohort USA From 2020-04-02 to 2020-06-13 64 127 RT-PCR
Marta Rodriguez-Diaz 2021 Propective cohort Spain From 2020-03-23 to 2020-10-14 29 620 RT-PCR
Karola S. Jering 2020 Population-based, longitudital observational and anlaytic USA From 2020-04-01 to 2020-11-23 6,380 406,446 RT-PCR
Annette K. Regan 2021 National cohot study USA From 2020-04-30 to 2020-03-11 2,655 78,283 RT-PCR
Seyit A. Erol 2020 Prospective case-control Turkey From 2020-06-26 to 2020-08-27 60 99 RT-PCR
Carolina Loyola Prest Ferrugini 2022 Cross-sectional Brazil From 2020-07-01 to 2020-10-01 86 265 RT-PCR
Sumaya Binte Masud 2021 Group-comparison cross-sectional Bangladesh From 2020-03-01 to 2020-08-01 70 210 RT-PCR
Justin S. Brandt 2021 Matched case-control study USA From 2020-03-11 to 2020-06-11 61 183 RT-PCR
Najeh Hcini 2021 Observational prospective cohort France From 2020-06-16 to 2020-08-16 137 507 RT-PCR
Elizabeth T. Patberg 2021 Retrospective cohort study USA From 2020-03-31 to 2020-06-17 77 133 RT-PCR
Allie Sakowicz 2020 Retrospective cohort study USA From 2020-03-19 to 2020-05-31 101 1,418 RT-PCR
Beth L. Pineles 2020 Retrospective cohort study Houston, USA From 2020-04-22 to 2020-07-22 77 935 RT-PCR
Zaheera Saadia 2021 Observational study Pakistan From April to May 2020 48 94 RT-PCR
Pilar Diaz-Corvillon 2020 Cross-sectional Chile From 2020-04-27 to 2020-06-07 37 586 RT-PCR
Noga Fallach 2022 Retrospective large, population-based cohort study Israel From 2020-02-21 to 2021-07-02 2,753 43,061 RT-PCR
Desmond Sutton 2021 Retrospective cohort study USA From 2020-03-22 to 2020-04-18 79 454 RT-PCR
Darios Getahun 2022 Retrospective cohort study USA From 2020-04-06 to 2021-02-28 2,203 35,123 RT-PCR
Monica Cruz-Lemini 2021 Multicenter prospective study Spain From 2020-03-01 to 2020-05-31 174 604 RT-PCR
Sara Cruz Meguizo 2021 Multicenter prospective study Spain From 2020-03-01 to 2020-05-31 1,347 2,954 RT-PCR
Maria de Lourdes Benamor Teixeira 2021 Multicenter prospective study Spain From 2020-04-13 to 2020-06-17 33 115 RT-PCR
Michelle J. Wang 2020 Retrospective cohort study USA From 2020-04-01 to 2020-07-22 53 813 RT-PCR
Abedzadeh-Kalahroudi 2021 Cohort study Iran From March to November 2020 56 94 RT-PCR
Alipour 2021 Retrospective analytical cohort study Iran Between March 15, 2020 to November 15, 2020 133 165 RT-PCR
Bender 2020 Observational study USA Between April 13, 2020 and April 26, 2020 53 135 RT-PCR
Cardona-Pérez 2021 Retrospective case-control study Mexico Between April 22, 2020 and May 25, 2020 70 170 RT-PCR
Chornock 2021 Retrospective cohort study USA From 2020-04-08 to 2020-07-31 73 935 RT-PCR
Cosma 2021 Prospective, observational cohort study Italy Between April 16, 2020 and June 22, 2020 16 105 RT-PCR
Melguizo 2021 Multicenter prospective observational study Spain Between February 26, 2020 and November 5, 2020 1,347 1,607 PCR
Cuñarro-López 2020 Observational, analytic, retrospective cohort study Spain From 2020-03-10 to 2020-05-12 43 68 RT-PCR
Farghaly 2020 Retrospective cohort study USA From March to May 2020 15 64 RT-PCR
Gulersen 2020 Retrospective cohort study USA From 2020-04-09 to 2020-04-27 50 50 RT-PCR
Gupta 2021 Retrospective cohort study India Between September 1, 2020 and November 30, 2020 108 3,057 RT-PCR
Gurol-Urganci 2021 Population-based cohort study England Between May 29, 2020 and January 31, 2021 3,527 338,553 RT-PCR
Smithgall 2020 Retrospective cohort study USA From 2020-03-23 to 2020-04-29 51 25 RT-PCR
Katz 2021 Retrospective cohort study USA From 2020-03-19 to 2020-05-31 490 964 RT-PCR
Ko 2021 Retrospective cohort study USA From March to September 2020 6,550 482,921 ICD-10-CM code U07.1 (COVID-19, virus identified)
Laresgoiti-Servitje 2021 Retrospective case-control study Mexico From mid-April 2020 to mid-September 2020 298 828 RT-PCR
Liao 2020 Retrospective analysis China Between January 20, 2020 and March 2, 2020 10 53 RT-PCR
Liu 2021 Retrospective cohort study USA From 2020-04-10 to 2020-06-10 56 279 RT-PCR
Norman 2021 Nationwide, prospective cohort study Sweden Between March 11, 2020, and January 31, 2021 2,286 84,719 RT-PCR
Papageorghiou 2021 Large, longitudinal, prospective, unmatched diagnosed and not-diagnosed observational study 18 countries Between March 2, 2020 and February 2, 2021 725 1,401 RT-PCR
Pirjani 2020 Prospective cohort study Iran From 2020-03-01 to 2020-09-01 66 133 RT-PCR
Ríos-Silva 2020 Retrospective cohort study Mexico From the beginning of the epidemic in Mexico until May 25, 2020 448 17,942 RT-PCR
Rosenbloom 2021 Retrospective cohort study USA From 2020-06-01 to 2020-11-30 83 166 RT-PCR
Ruggiero 2021 Prospective cohort study Italy Between April 7, 2020 to May 6, 2020 28 287 RNA PCR, anti-envelope anti-nucleoprotein
Savirón-Cornudella 2021 Observational cohort study Spain Between March 31, 2020 and September 30, 2020 22 1,146 PCR test and by detection of serum immunoglobulins G and M.
SOTO-TORRES 2021 Retrospective case-control study USA Between May 1, 2020 and August 31, 2020 106 103 RNA PCR, rapid antigen tests
Steffen 2021 Prospective cohort study USA Between May 1, and September 2020 61 939 RT-PCR
Timircan 2021 Prospective cohort study Romania Between August 30, 2020 and January 31, 2021 101 938 RT-PCR
Trahan 2021 Prospective Canada Between March 22, 2020 and July 31, 2020 45 225 RT-PCR
Villar 2021 Prospective, longitudinal, observational study 18 countries From March to October 2020 706 1,424 Real-time polymerase chain reaction and antibody tests
Vousden 2021 National, prospective cohort study UK From 2020-03-01 to 2020-08-31 722 694 Not mentioned
Yadav 2020 Retrospective comparative study India Between March 23, 2020 till July 23, 2020 28 112 RT-PCR

RT-PCR, reverse transcriptase–polymerase chain reaction; CT, computed tomography; ICD-10-CM, international classification of diseases, tenth revision, clinical modification; COVID-19, coronavirus disease 2019; RNA, ribonucleic acid.

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