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Maternal mortality among women with coronavirus disease 2019 admitted to the intensive care unit

  • Matthew J. Blitz
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Southside Hospital, Northwell Health, 376 East Main St., Suite 202, Bay Shore, NY 11706
    Department of Obstetrics and Gynecology, Long Island Jewish Forest Hills Hospital, Northwell Health, Forest Hills, NY
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  • Burton Rochelson
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Katz Women’s Hospital, North Shore University Hospital, Northwell Health, Manhasset, NY
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  • Howard Minkoff
    Affiliations
    Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Maimonides Medical Center, Brooklyn, NY
    Department of Obstetrics and Gynecology, State University of New York Downstate Medical Center, Brooklyn, NY
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  • Natalie Meirowitz
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Katz Women’s Hospital, Long Island Jewish Medical Center, Northwell Health, New Hyde Park, NY
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  • Lakha Prasannan
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Katz Women’s Hospital, North Shore University Hospital, Northwell Health, Manhasset, NY
    Katz Women’s Hospital, Long Island Jewish Medical Center, Northwell Health, New Hyde Park, NY
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  • Viktoriya London
    Affiliations
    Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Maimonides Medical Center, Brooklyn, NY
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  • Timothy J. Rafael
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Department of Obstetrics and Gynecology, Long Island Jewish Forest Hills Hospital, Northwell Health, Forest Hills, NY
    Katz Women’s Hospital, North Shore University Hospital, Northwell Health, Manhasset, NY
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  • Shruti Chakravarthy
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Department of Obstetrics and Gynecology, Staten Island University Hospital, Northwell Health, Staten Island, NY
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  • Luis A. Bracero
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Southside Hospital, Northwell Health, Bay Shore, NY 11706
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  • Shane W. Wasden
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  • Sarah L. Pachtman Shetty
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  • Orlando Santandreu
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Long Island Jewish Forest Hills Hospital, Northwell Health, Forest Hills, NY
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  • Frank A. Chervenak
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Department of Obstetrics and Gynecology, Lenox Hill Hospital, Northwell Health, New York, NY
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  • Benjamin M. Schwartz
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Department of Obstetrics and Gynecology, Southside Hospital, Northwell Health, Bay Shore, NY
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  • Michael Nimaroff
    Affiliations
    Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
    Katz Women’s Hospital, North Shore University Hospital, Northwell Health, Manhasset, NY
    Katz Women’s Hospital, Long Island Jewish Medical Center, Northwell Health, New Hyde Park, NY
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      Objective

      Limited data are available on critically ill pregnant women hospitalized with coronavirus disease 2019 (COVID-19). Although maternal mortality has been reported,

      Vallejo V, Ilagan JG. A postpartum death due to coronavirus disease 2019 (COVID-19) in the United States. Obstet Gynecol 2020 [Epub ahead of print].

      • Hantoushzadeh S.
      • Shamshirsaz A.A.
      • Aleyasin A.
      • et al.
      Maternal death due to COVID-19.
      • Karami P.
      • Naghavi M.
      • Feyzi A.
      • et al.
      WITHDRAWN: mortality of a pregnant patient diagnosed with COVID-19: a case report with clinical, radiological, and histopathological findings.
      the frequency with which this devastating outcome occurs is unknown. The objective of this study was to determine the rate of maternal death among pregnant and postpartum women with COVID-19 admitted to the intensive care units (ICUs) in a large integrated health system in the New York metropolitan area. In this study, we described patient demographics, baseline comorbidities, clinical presentation, hospital course, and maternal outcomes.

      Study Design

      This case series evaluated all consecutively hospitalized pregnant and immediately postpartum women with laboratory-confirmed diagnosis of COVID-19 who were admitted to the ICUs at 10 hospitals within Northwell Health, the largest academic health system in New York, and Maimonides Medical Center, an affiliate of Northwell Health in Brooklyn, NY, from March 1, 2020, to May 6, 2020. Collectively, these hospitals perform approximately 40,000 deliveries per year, representing about 1 in 6 births in the state of New York and 1% of all births in the United States. Respiratory specimens were collected using nasopharyngeal swabs. Symptomatic patients who received positive test results for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) by polymerase chain reaction (PCR) assay were included. Admission to the ICU was at the discretion of the consulted critical care attending physician at each site. Patients who had a critical care consultation but were not directly managed by an intensivist were not included. Women who received positive test results for the virus but were admitted to the ICU for indications other than acute or impending hypoxemic respiratory failure were excluded (eg, postpartum hemorrhage). The Northwell Health Institutional Review Board approved this case series as minimal-risk research that used data collected for routine clinical practice and waived the requirement for informed consent. Some women in this study were included in previous publications characterizing COVID-19 hospitalizations within the Northwell Health system,
      • Richardson S.
      • Hirsch J.S.
      • Narasimhan M.
      • et al.
      Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City area.
      ,
      • Blitz M.J.
      • Grünebaum A.
      • Tekbali A.
      • et al.
      Intensive care unit admissions for pregnant and nonpregnant women with coronavirus disease 2019.
      whereas 1 maternal death was previously presented as a case report.

      Vallejo V, Ilagan JG. A postpartum death due to coronavirus disease 2019 (COVID-19) in the United States. Obstet Gynecol 2020 [Epub ahead of print].

      Clinical data were obtained from the electronic health record system. Subject records were reviewed manually. Data collected included demographics, medical comorbidities, duration of illness before hospitalization, laboratory and imaging results, ICU treatments, and clinical outcomes. No patients were postpartum at the time of hospital admission. The primary outcome was maternal death. Secondary outcomes included length of hospitalization and ICU stay, frequency and duration of invasive mechanical ventilation (ie, requiring endotracheal intubation), frequency of vasopressor administration, urgent or emergent delivery associated with acute respiratory decompensation, and discharge from the hospital. Descriptive statistics were used to characterize the data. Results are presented as means and standard deviations or medians and interquartile ranges, as appropriate. Categorical variables were expressed as numbers and percentages.

      Results

      Between March 1, 2020, and May 6, 2020, at the 11 included hospitals, there were 462 pregnant women who received positive test results for SARS-CoV-2, and 70 (15%) patients were classified as having severe or critical COVID-19 per National Institutes of Health (NIH) criteria. Out of these 70 patients, a total of 13 (19%) were admitted to the ICUs for acute or impending hypoxemic respiratory failure (Figure). Among this group, 2 (15%) died, and 11 (85%) were discharged from the hospital.
      Figure thumbnail gr1
      FigureIndividual patient outcomes
      A total of 13 pregnant or immediately postpartum women were admitted to the ICUs for COVID-19 and 8 required invasive mechanical ventilation. Although 2 patients (15%) died, 11 (85%) were discharged alive.
      COVID-19, coronavirus disease 2019; ICUs, intensive care units; SNF, skilled nursing facility.
      Blitz. Maternal mortality among intensive care unit admissions for coronavirus disease 2019. Am J Obstet Gynecol 2020.
      Women admitted to the ICUs had a mean maternal age of 33.8±5.2 years, and 69% were multiparous (Supplemental Table 1). Hispanic women constituted the largest racial or ethnic group (38%). The most common comorbidities were obesity (38%) and pulmonary conditions (23%) such as asthma and obstructive sleep apnea (OSA). However, nearly half of the patients (46%) had no baseline comorbidities. All pregnancies were singleton gestations. Most patients were tachycardic, tachypneic, and hypoxemic on initial evaluation, and few were febrile. Nearly all patients (92%) met the NIH criteria for severe COVID-19 at admission. Lymphopenia, elevated transaminases, and elevated inflammatory markers were common laboratory findings (Supplemental Table 2). The mean gestational age of pregnant women with COVID-19 at hospitalization was 33.3±5.3 weeks, and symptoms started 8±3 days before admission.
      The median length of hospitalization and ICU stay were 13 and 8 days, respectively (Supplemental Table 3). The duration of hospitalization before ICU admission and after ICU discharge were 2±2 and 3±3 days, respectively. Invasive mechanical ventilation was required in 8 (62%) cases (at initiation, 6 were postpartum and 2 were pregnant), and the median duration of therapy was 8 days. Among this group, 7 (88%) required vasopressors. One patient was extubated but remained ventilator dependent with a tracheostomy. All patients admitted to the ICUs received either prophylactic or therapeutic dose anticoagulation (100%); there were no known cases of venous thromboembolism. Most patients were administered hydroxychloroquine (85%) and antibiotics for community-acquired pneumonia (92%); some were enrolled in clinical trials for the antiviral drug remdesivir (23%), interleukin-6–receptor inhibitors (38%), or convalescent plasma therapy (15%).
      Of the 2 patients who died, 1 had a long, protracted course in the ICU, which was complicated by fetal demise at a periviable gestational age; she developed multiple organ failure and required renal replacement therapy, and after extensive counseling in the setting of a poor maternal prognosis, the family opted for no obstetrical intervention. She had a prepregnancy body mass index (BMI) greater than 40 kg/m2 and OSA. The second patient who died had a rapid clinical deterioration after delivery, which was complicated by severe respiratory distress, multiple organ failure, and cardiopulmonary arrest.

      Vallejo V, Ilagan JG. A postpartum death due to coronavirus disease 2019 (COVID-19) in the United States. Obstet Gynecol 2020 [Epub ahead of print].

      She had a prepregnancy BMI less than 30 kg/m2 and no baseline comorbidities. Prone positioning to improve oxygenation during mechanical ventilation was used in the first case but not in the second because of the patient’s rapid clinical decline. These cases were critically reviewed by a multidisciplinary team; it was determined that the standard of care was met in both cases and that the outcomes were a consequence of the disease process.
      Of the 7 women (54%) who delivered during hospitalization for COVID-19, 5 (71%) were urgent or emergent cesarean deliveries in the setting of acute respiratory decompensation, whereas 1 was an emergent cesarean delivery for cord prolapse during induction of labor for worsening respiratory symptoms, and 1 presented in labor and delivered vaginally. There were 4 (57%) preterm births.

      Conclusion

      Maternal death occurred in 15% of patients admitted to the ICUs for COVID-19 and in 25% of those who required invasive mechanical ventilation. Delivery occurred in half of the patients with COVID-19 who were admitted to the ICUs and all patients who required invasive mechanical ventilation. Hispanic women constituted the largest racial or ethnic group in the study, which may reflect a disproportionate burden of disease among minority groups.
      Few studies have evaluated the characteristics and outcomes of critically ill pregnant women with COVID-19. Interestingly, and in contrast with our findings, no cases of maternal mortality were observed in the recent multicenter cohort study by Pierce-Williams et al
      • Pierce-Williams R.A.M.
      • Burd J.
      • Felder L.
      • et al.
      Clinical course of severe and critical COVID-19 in hospitalized pregnancies: a US cohort study. Am J Obstet Gynecol MFM 2020:100134.
      among pregnant women hospitalized with severe or critical COVID-19. At present, that study represents the largest report of such patients, but it is limited by the fact that half of the critically ill patients (11/20) were still hospitalized at the completion of data collection. In our study, approximately half of the women admitted to the ICUs had no baseline comorbidities, making it difficult to identify those who were at highest risk of respiratory failure and death. The patients were generally older, multiparous, and racial or ethnic minorities, which may reflect underlying disease prevalence (a product of various factors, including household size and ability to social distance) rather than intrinsic susceptibility to adverse outcomes. Larger studies are needed to determine which laboratory and imaging findings are most predictive of rapidly progressive respiratory failure in pregnancy. In our study, most patients were delivered in the setting of worsening disease; it is not known how autotransfusion and other physiological and immunologic changes immediately after delivery affect maternal outcomes.
      The strengths of this study include consecutive patient enrollment over a well-defined time interval, explicit inclusion and exclusion criteria, utilization of data from a single medical record system, and evaluation of clinically relevant outcomes. In addition, no patients remained hospitalized at study completion, allowing all in-hospital outcomes to be fully evaluated, without omission, further reducing the risk of bias. This study also has limitations. First, our sample size remains small because of the rarity of ICU admissions of pregnant women with COVID-19.
      • Blitz M.J.
      • Grünebaum A.
      • Tekbali A.
      • et al.
      Intensive care unit admissions for pregnant and nonpregnant women with coronavirus disease 2019.
      During the study, ICU bed availability was limited, and patients requiring considerable noninvasive respiratory support (eg, oxygen delivery by using a nasal cannula or face mask) were often managed on lower acuity units. Second, laboratory testing and radiologic imaging were not uniform. Third, treatment algorithms changed throughout the study period and were not identical for all patients. Finally, the true prevalence of COVID-19 among pregnant women in these communities is unknown; a SARS-CoV-2 testing strategy that only includes patients admitted to the hospital, predominantly for delivery, does no’t reflect this number. Universal testing for SARS-CoV-2 was implemented in the middle of the study period on our obstetrical units. Thus, determining an accurate risk of ICU admission or death among pregnant women infected with the virus is not possible.
      In summary, pregnant and postpartum women with COVID-19 admitted to the ICUs are at risk for maternal death, which may occur even in the absence of substantial baseline comorbidities. Longitudinal population-based cohort studies may offer more insights into mechanisms determining which patients infected with the virus are at highest risk.
      In addition, in the Figure, patients 1 to 7 and 9 were included in Richardson et al.
      • Richardson S.
      • Hirsch J.S.
      • Narasimhan M.
      • et al.
      Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City area.
      Patient 7 was included in Vallejo et al.

      Vallejo V, Ilagan JG. A postpartum death due to coronavirus disease 2019 (COVID-19) in the United States. Obstet Gynecol 2020 [Epub ahead of print].

      Patients 1 to 4, 6, and 8 to 10 were included in Blitz et al.
      • Blitz M.J.
      • Grünebaum A.
      • Tekbali A.
      • et al.
      Intensive care unit admissions for pregnant and nonpregnant women with coronavirus disease 2019.
      Patients 12 to 13 were included in London et al
      • London V.
      • McLaren Jr., R.
      • Atallah F.
      • et al.
      The relationship between status at presentation and outcomes among pregnant women with COVID-19.
      and McLaren et al.
      • McLaren Jr., R.A.
      • London V.
      • Atallah F.
      • et al.
      Delivery for respiratory compromise among pregnant women with COVID-19.
      Patients 3, 4, 6, 8, and 10 were included in Gulersen et al.

      Gulersen M, Blitz MJ, Rochelson B, et al. Clinical implications of SARS-CoV-2 infection in the viable preterm period. Am J Perinatol 2020 (in press).

      Acknowledgments

      We would like to acknowledge the contributions of the Northwell Health COVID-19 Research Consortium.

      Appendix

      Supplemental Table 1Clinical characteristics of the patients
      CharacteristicPatients (n=13)
      Demographics
      Maternal age, y33.8±5.2
       ≥356 (46)
      Race or ethnicity
       Hispanic or Latino5 (38)
       Non-Hispanic white4 (31)
       Non-Hispanic black1 (8)
       Asian3 (23)
      Multiparous9 (69)
       Parity of 3 or more6 (46)
      BMI prepregnancy, kg/m230.2±6.7
       ≥305 (38)
      Medical comorbidities
       Hypertension0 (0)
       Diabetes1 (8)
       Asthma2 (15)
       Obstructive sleep apnea1 (8)
      Pregnancy complications
       Gestational diabetes1 (8)
       Gestational hypertension or preeclampsia3 (23)
      COVID-19
      Duration of illness before hospitalization, d8±3
      Duration of hospitalization before ICU admission, d2±2
      Previous hospital visit for respiratory symptoms6 (46)
      Gestational age at positive PCR result for SARS-CoV-2, wk32.5±5.2
      Gestational age at hospitalization, wk33.3±5.3
      On admission
      Reported symptoms
       Fever, subjective or measured12 (92)
       Cough13 (100)
       Dyspnea10 (77)
       Myalgia6 (46)
       Fatigue or malaise3 (23)
      Obstetrical complaints
       Contractions2 (15)
       Decreased fetal movement3 (23)
      Vital signs
       Temperature, ≥100.4°F or 38°C2 (15)
       Heart rate, >100 beats per min10 (77)
       Respiratory rate, breaths per min27±12
      >303 (23)
       Systolic blood pressure, mm Hg122±18
       Oxygen saturation, %92±5
      ≤939 (69)
      Data are presented as n (%) and mean±standard deviation unless otherwise specified.
      BMI, body mass index; COVID-19, coronavirus disease 2019; PCR, polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.
      Blitz. Maternal mortality among intensive care unit admissions for coronavirus disease 2019. Am J Obstet Gynecol 2020.
      Supplemental Table 2Laboratory results and imaging findings
      VariablePatients (n=13)Reference ranges
      Reference range established for nonpregnant patients; many of these laboratory tests change by trimester
      On admission
      Defined as first test results available, typically within the first 24 hours of presentation
      White blood cell count, ×109/L7.9 (5.6–9.9)3.8–10.5
       >103 (23)
      Lymphocyte count, ×109/L0.8 (0.6–1.0)1.0–3.3
      Platelet count, ×103/μL204 (166–246)150–420
       <1502 (15)
      Aspartate aminotransferase, U/L81 (49–98)10–40
       >4010 (77)
      Alanine aminotransferase, U/L44 (21–67)10–45
       >408 (62)
      Venous lactate, mmol/L1.0 (0.8–1.4)0.7–2.0
       >1.53 (23)
      Serum creatinine, mg/dL0.6 (0.5–0.7)0.5–1.30
       >1.12 (15)
      Ferritin, ng/mL112 (95–246)15–400
      D-dimer, ng/mL613 (383–1169)0–229
       >10004 (31)
      C-reactive protein, mg/dL20.1 (11.3–33.1)0.0–0.40
      Procalcitonin, ng/mL0.8 (0.3–1.5)0.02–0.10
      Creatine kinase, U/L
      Data available for 9 patients.
      33 (33–128)25–200
      Troponin above test-specific upper limit of normal3/10 (30)
      Chest radiography
       Bilateral infiltrates11 (85)
       Pleural effusion0 (0)
      During ICU stay
      Highest serum creatinine, mg/dL0.7 (0.6–1.1)
       >2.52 (15)
      Lowest platelet count, ×103/μL152 (127–235)
       <1003 (23)
      Highest aspartate aminotransferase, U/L103 (81–141)
      Highest alanine aminotransferase, U/L97 (77–215)
      Aminotransferase, >1000 U/L3 (23)
      Highest D-dimer, ng/mL
       >30005 (38)
      Data are presented as n (%), mean±standard deviation, and median (interquartile range).
      ICU, intensive care unit.
      Blitz. Maternal mortality among intensive care unit admissions for coronavirus disease 2019. Am J Obstet Gynecol 2020.
      a Reference range established for nonpregnant patients; many of these laboratory tests change by trimester
      b Defined as first test results available, typically within the first 24 hours of presentation
      c Data available for 9 patients.
      Supplemental Table 3Clinical management and outcomes
      VariablePatients (n=13)
      ICU management
      Invasive mechanical ventilation8 (62)
       Duration, d8 (2–19)
       Extubated
      One patient was extubated but remained ventilator dependent with a tracheostomy
      6/8 (75)
       Prone positioning utilized4/8 (50)
      Extracorporeal membrane oxygenation0 (0)
      Vasopressors7 (54)
      Renal replacement therapy1 (8)
      Antiviral agent
       Hydroxychloroquine11 (85)
       Remdesivir3 (23)
      Antibiotics for community-acquired pneumonia12 (92)
      Anticoagulation, prophylactic or therapeutic13 (100)
      Immunomodulatory agent9 (69)
       Corticosteroid (for maternal indication)7 (54)
       Interleukin-1 inhibitor2 (15)
       Interleukin-6 inhibitor5 (38)
       Convalescent plasma2 (15)
      Maternal outcomes
      Length of stay, d
       In hospital13 (9–23)
       In ICU8 (4–15)
      Delivery during hospitalization7/13 (54)
       Cesarean delivery for acute respiratory decompensation5/7 (71)
       Cesarean delivery for obstetrical indication1/7 (14)
       Vaginal delivery1/7 (14)
      Died in hospital2 (15)
      Discharged from hospital11 (85)
       To home10 (77)
       To long-term care facility1 (8)
      Remained hospitalized at study completion0 (0)
      Neonatal outcomes
      Gestational age at delivery, wk36.9±2.0
      Birthweight, g2994±569
      Apgar scores
       1 min≤73/8 (38)
       5 min≤70/8 (0)
      Positive PCR result for SARS-CoV-2 on first day of life
      Results not available for 1 newborn.
      0/7 (0)
      Received antenatal corticosteroids5 (50)
      Gestational age at administration29.1±4.2
      Data are presented as n (%), mean±standard deviation, and median (interquartile range). Denominator is number of patients diagnosed as having COVID-19 at less than 37 weeks’ gestation.
      COVID-19, coronavirus disease 2019; ICU, intensive care unit; PCR, polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.
      Blitz. Maternal mortality among intensive care unit admissions for coronavirus disease 2019. Am J Obstet Gynecol 2020.
      a One patient was extubated but remained ventilator dependent with a tracheostomy
      b Results not available for 1 newborn.

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        • Aleyasin A.
        • et al.
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        • Naghavi M.
        • Feyzi A.
        • et al.
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        • Tekbali A.
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        Intensive care unit admissions for pregnant and nonpregnant women with coronavirus disease 2019.
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        • Pierce-Williams R.A.M.
        • Burd J.
        • Felder L.
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        Clinical course of severe and critical COVID-19 in hospitalized pregnancies: a US cohort study. Am J Obstet Gynecol MFM 2020:100134.
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        Delivery for respiratory compromise among pregnant women with COVID-19.
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