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Systematic review and critical evaluation of quality of clinical practice guidelines on the management of SARS-CoV-2 infection in pregnancy

  • Raffaella Di Girolamo
    Affiliations
    Center for Fetal Care and High-Risk Pregnancy, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy (Dr. Di Girolamo, Dr. Capannolo, Dr. Buca, Prof. Liberati, and Prof. D'Antonio)
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  • Asma Khalil
    Affiliations
    Fetal Medicine Unit, St George's Hospital, London, United Kingdom (Prof. Khalil)
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  • Giuseppe Rizzo
    Affiliations
    Department of Obstetrics and Gynaecology, Fondazione Policlinico Tor Vergata, Università degli studi di Roma Tor Vergata, Roma, Italy (Prof. Rizzo)
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  • Giulia Capannolo
    Affiliations
    Center for Fetal Care and High-Risk Pregnancy, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy (Dr. Di Girolamo, Dr. Capannolo, Dr. Buca, Prof. Liberati, and Prof. D'Antonio)
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  • Danilo Buca
    Affiliations
    Center for Fetal Care and High-Risk Pregnancy, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy (Dr. Di Girolamo, Dr. Capannolo, Dr. Buca, Prof. Liberati, and Prof. D'Antonio)
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  • Marco Liberati
    Affiliations
    Center for Fetal Care and High-Risk Pregnancy, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy (Dr. Di Girolamo, Dr. Capannolo, Dr. Buca, Prof. Liberati, and Prof. D'Antonio)
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  • Ganesh Acharya
    Affiliations
    Department of Clinical Science, Intervention and Technology, Karolinska Institute and Center for Fetal Medicine, Karolinska University Hospital, Stockholm, Sweden (Prof. Acharya)

    Women's Health and Perinatology Research Group, Department of Clinical Medicine, University of Tromsø – The Arctic University of Norway, Tromsø, Norway (Prof. Acharya)

    Department of Obstetrics and Gynecology, University Hospital of North Norway, Tromsø, Norway (Prof. Acharya)
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  • Anthony O. Odibo
    Affiliations
    Divisions of Maternal-Fetal Medicine and Clinical Research, Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO (Prof. Odibo)
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  • Francesco D'Antonio
    Correspondence
    Corresponding author: Francesco D'Antonio, MD, PhD.
    Affiliations
    Center for Fetal Care and High-Risk Pregnancy, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy (Dr. Di Girolamo, Dr. Capannolo, Dr. Buca, Prof. Liberati, and Prof. D'Antonio)
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      OBJECTIVE

      To systematically identify and critically assess the quality of clinical practice guidelines for the management of SARS-CoV-2 infection in pregnancy.

      DATA SOURCES

      Medline, Scopus, and ISI Web of Science databases were searched until February 15, 2022.

      STUDY ELIGIBILITY CRITERIA

      Inclusion criteria were clinical practice guidelines on the management of SARS-CoV-2 infection in pregnancy. The risk of bias and quality assessments of the included clinical practice guidelines were performed using the Appraisal of Guidelines for REsearch and Evaluation II tool, which is considered the gold standard for quality assessment of clinical practice guidelines. To define a clinical practice guideline as of good quality, we adopted the cutoff score proposed by Amer et al: if the overall clinical practice guideline score was >60%, it was recommended.

      METHODS

      The following clinical points related to the management of pregnant women with SARS-CoV-2 infection were addressed: criteria for maternal hospitalization, recommendations for follow-up fetal growth scan, specific recommendations against invasive procedures, management of labor, timing of delivery, postpartum care, and vaccination strategy.

      RESULTS

      A total of 28 clinical practice guidelines were included. All recommended hospitalization only for severe disease; 46.1% (6/13) suggested a fetal growth scan after SARS-CoV-2 infection, whereas 23.1% (3/13) did not support this practice. Thromboprophylaxis with low-molecular-weight heparin was recommended in symptomatic women by 77.1% (7/9) of the clinical practice guidelines. None of the guidelines recommended administering corticosteroids only for the presence of SARS-CoV-2 infection in preterm gestation, unless specific obstetrical indication exists. Elective induction of labor from 39 weeks of gestation was suggested by 18.1% (2/11) of the clinical practice guidelines included in the present review, whereas 45.4% (5/11) did not recommend elective induction unless other obstetrical indications coexisted. There were 27% (3/11) of clinical practice guidelines that suggested shortening of the second stage of labor, and active pushing was supported by 18.1% (2/11). There was general agreement among the clinical practice guidelines in not recommending cesarean delivery only for the presence of maternal infection and in recommending vaccine boosters at least 6 months after the primary series of vaccination. The Appraisal of Guidelines for REsearch and Evaluation II standardized domain scores for the first overall assessment of clinical practice guidelines had a mean of 50% (standard deviation±21.82%), and 9 clinical practice guidelines scored >60%.

      CONCLUSION

      A significant heterogeneity was found in some of the main aspects of the management of SARS-CoV-2 infection in pregnancy, as reported by the published clinical practice guidelines.

      Keywords

      Why was this study conducted?

      This systematic review wants to objectively evaluate the quality of the published clinical practice guidelines on the management of SARS-CoV-2 infection in pregnancy using the Appraisal of Guidelines for REsearch and Evaluation (AGREE) II tool.

      Key findings

      A general agreement in the criteria for maternal hospitalization, mode of delivery, and recommendation of vaccine booster was observed. Conversely, there was large heterogeneity in several other management aspects, including type and frequency of maternal assessment after infection, ultrasound scans, timing of delivery, and type of fetal monitoring during labor.

      What does this add to what is known?

      The results of this systematic review indicate the need for developing shared guidelines supported, endorsed, and promoted by national and international professional societies to make management of SARS-CoV-2 infection in pregnant women more homogeneous among different countries.
      The COVID-19 pandemic, caused by SARS-CoV-2 infection that was first identified in December 2019, still remains a major public health concern.
      • Mohamadian M
      • Chiti H
      • Shoghli A
      • Biglari S
      • Parsamanesh N
      • Esmaeilzadeh A.
      COVID-19: virology, biology and novel laboratory diagnosis.
      Pregnancy is an independent risk factor for adverse outcomes in women with SARS-CoV-2 infection, especially in the presence of several comorbidities such as diabetes mellitus or preeclampsia.
      WAPM (World Association of Perinatal Medicine) Working Group on COVID-19
      Maternal and perinatal outcomes of pregnant women with SARS-CoV-2 infection.
      ,
      • Di Mascio D
      • Buca D
      • Berghella V
      • et al.
      Counseling in maternal-fetal medicine: SARS-CoV-2 infection in pregnancy.
      The rapid spread of the pandemic and the higher risk of adverse maternal outcomes reported in women with SARS-CoV-2 infection underscore the importance of available evidence-based guidelines for the management of this infection in pregnancy.
      • Di Mascio D
      • Sen C
      • Saccone G
      • et al.
      Risk factors associated with adverse fetal outcomes in pregnancies affected by coronavirus disease 2019 (COVID-19): a secondary analysis of the WAPM study on COVID-19.

      Canadian Association of Emergency Physicians. Statement on COVID-19 vaccinations and pregnant and breastfeeding women. 2020. Available at:https://caep.ca/wp-content/uploads/2021/01/CAEPStatement-Vaccination-Pregnancy-COVID.pdf. Accessed February 18, 2022.

      Canadian Association of Perinatal and Women's Health Nurses. Suggestions for the care of the perinatal population. 2020. Available at:https://capwhn.ca/wp-content/uploads/2020/03/CAPWHN_COVID-19_Mar-25-2020.pdf. Accessed February 18, 2022.

      American Academy of Family Physicians. Considerations for pregnancy, breastfeeding, and COVID-19. 2021. Available at: https://www.aafp.org/about/policies/all/breastfeeding-covid19.html. Accessed February 18, 2022.

      Canadian Paediatric Society. Breastfeeding and COVID-19. 2021. Available at:https://cps.ca/documents/position/breastfeeding-when-mothers-have-suspected-or-proven-covid-19. Accessed February 18, 2022.

      American Academy of Pediatrics. FAQs: Management of infants born to mothers with suspected or confirmed COVID-19. 2021. Available at:https://www.aap.org/en/pages/2019-novel-coronavirus-covid-19-infections/clinical-guidance/faqs-management-of-infants-born-to-covid-19-mothers/. Accessed February 18, 2022.

      Centers for Disease Control and Prevention. Care for breastfeeding people. 2020. Available at:https://www.cdc.gov/coronavirus/2019-ncov/hcp/care-for-breastfeeding-women.html. Accessed February 18, 2022.

      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).

      Elwood C, Poliquin V, Boucoiran I, et al. Committee Opinion No. 400: COVID-19 and pregnancy. 2021. Available at:https://sogc.org/common/Uploaded%20files/Covid%20Information/Committee%20Opinion%20No.%20400%20COVID-19%20and%20Pregnancy.Dec.17.2020.pdf. Accessed February 18, 2022.

      Centers for Disease Control and Prevention. COVID-19 vaccines while pregnant or breastfeeding. 2022. Available at:https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/pregnancy.html. Accessed February 18, 2022.

      The American College of Obstetricians and Gynecologists. COVID-19 vaccination considerations for Obstetric-Gynecologic care. 2020. Available at:https://www.acog.org/clinical/clinical-guidance/practice-advisory/articles/2020/12/covid-19-vaccination-considerations-for-obstetric-gynecologic-care. Accessed February 18, 2022.

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      The Royal Australian and New Zealand College of Obstetricians and Gynaecologists. Coronavirus disease (COVID-19) in pregnancy. 2020. Available at:https://ranzcog.edu.au/RANZCOG_SITE/media/RANZCOG-MEDIA/Women%27s%20Health/Global%20Health/RANZCOG-COVID-19-Guide-for-Resource-limited-Environments.pdf. Accessed February 18, 2022.

      International Federation of Gynecology and Obstetrics. Committee on the impact of pregnancy on long-term health. 2022. Available at:https://www.figo.org/what-we-do/figo-divisions-committees/committee-impact-pregnancy-longterm-health. Accessed February 18, 2022.

      New South Wales Health. Guidance for maternity, newborn care and infant feeding, Medicine management for pregnant patients with COVID-19. 2021. Available at:https://www.health.nsw.gov.au/Infectious/covid-19/communities-of-practice/Pages/maternity-and-newborn-care.aspx. Accessed February 18, 2022.

      Quebec Group. Guidelines for the management of the pregnant woman with COVID-19 admitted to the intensive care unit (ICU). 2021 . Available at:https://www.quebec.ca/en/health/health-issues/a-z/2019-coronavirus/information-for-pregnant-women-coronavirus-covid-19. Accessed February 18, 2022.

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      National Institute for Research in Reproductive Health
      Guidance for management of pregnant women in COVID-19 pandemic.
      • Bahtiyar MO
      • Baschat A
      • Deprest J
      • et al.
      Fetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy Network.
      • Martins I
      • Louwen F
      • Ayres-de-Campos D
      • Mahmood T.
      EBCOG position statement on COVID-19 vaccination for pregnant and breastfeeding women.
      • Donders GGG
      • Grinceviciene S
      • Haldre K
      • et al.
      ISIDOG consensus guidelines on COVID-19 vaccination for women before, during and after pregnancy.
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      • Bourne T
      • Kyriacou C
      • Coomarasamy A
      • et al.
      ISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2020-12-09-guidance-for-antenatal-screening-and-ultrasound-in-pregnancy-in-the-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for rationalising earlypregnancy services in the evolving coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2021-05-25-guidance-for-rationalising-early-pregnancy-services-in-the-evolving-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19) vaccination in pregnancy. 2021. Available at: https://www.rcog.org.uk/covid-vaccine. Accessed February 18, 2022.

      Healthcare improvement Scotland. COVID-19 position statement: maternal critical care provision. 2020. Available at:https://www.sign.ac.uk/media/1787/sg-maternal-critical-care-provision_v33.pdf. Accessed February 18, 2022.

      Italian Society of Gynecology and Obstetrics/ Association of Italian Hospital Obstetricians and Gynaecologists. Interim guidance on pregnancy, childbirth, breastfeeding and care of infants (0-2 years) in response to the COVID-19 emergency. 2021. Available at:https://www.iss.it/documents/5430402/0/Rapporto+ISS+COVID-19+2_2021_EN.pdf/421a0bc6-1933-aa77-6b39-a7860d866a16?t=1615472502820. Accessed February 18, 2022.

      Clinical Practice Guidelines (CPGs) are statements that include recommendations intended to optimize patient care. CPGs should follow a rigorous methodology to provide clinicians with the most up-to-date and objective clinical evidence. However, high-quality CPGs are methodologically complex to develop, which makes them relatively incompatible with emergency situations. Rapid Guidelines (RGs) are defined as CPGs that are developed in a 1- to 3-month time frame and are alternatives to comprehensive CPGs, providing guidance in response to an emergency.
      • Kowalski SC
      • Morgan RL
      • Falavigna M
      • et al.
      Development of rapid guidelines: 1. Systematic survey of current practices and methods.
      Since the beginning of the pandemic, a multitude of RGs reporting different aspects of the management of SARS-CoV-2 infection in pregnancy have been released. However, the methodological robustness of such guidelines has yet to be determined.
      • Butler A
      • Hall H
      • Copnell B.
      A guide to writing a qualitative systematic review protocol to enhance evidence-based practice in nursing and health care.
      The Appraisal of Guidelines for REsearch and Evaluation (AGREE) II tool is the most widely used tool for appraising the quality of CPGs, and it has been considered as the gold standard for CPG quality assessment.
      • Brouwers MC
      • Kho ME
      • Browman GP
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      The primary aim of this systematic review (SR) was to objectively evaluate the quality of the published CPGs on the management of SARS-CoV-2 infection in pregnancy using the AGREE II tool. The secondary aim was to assess and report the agreement or heterogeneity among the CPGs regarding different aspects of clinical management of SARS-CoV-2 infection.

      Methods

      Protocol, information sources, and literature search

      This review was performed according to a protocol recommended for SRs of clinical guidelines.
      • Liberati A
      • Altman DG
      • Tetzlaff J
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration.
      The review protocol was not designed a priori, given the rapid evolution of the pandemic and the speed of the evidence synthesis. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed (Table S1).
      • Liberati A
      • Altman DG
      • Tetzlaff J
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration.
      The literature search was conducted in the MEDLINE (PubMed), Scopus, and ISI Web of Science databases to identify all relevant CPGs published before February 15, 2022. Combinations of the following keywords and Medical Subject Headings (MeSH) search terms were used: (“management” OR “managing”) AND (“SARS-CoV-2” OR “COVID-19” OR “coronavirus”) AND (“pregnancy” OR “pregnant” OR “pregnant women” OR “during pregnancy” AND (“antenatal care” OR “prenatal” OR “vaccine” OR “ultrasound” OR “delivery”) AND (“guidelines”). No restrictions for geographic location were applied. The reference lists of relevant recommendations and considerations were also hand-searched to complement the database search. The search was restricted to guidelines published in English.
      Only CPGs including recommendations on the management of pregnant women with SARS-CoV-2 infection were considered eligible for this SR. Two reviewers (R.D.G., G.C.) independently evaluated titles and abstracts. Disagreements were resolved by discussion among authors, and if required, with the involvement of a third author (F.D.A.). When >1 version was available, the most updated version was included, considering newer versions methodologically as equivalent to previous versions, given that they were written using the same approach. Any CPGs on the organization of antenatal or postnatal services or information for healthcare professionals in the context of the COVID-19 pandemic were excluded.

      Data extraction

      The main data extracted for the present review included publication ID (first author, a research consortium, or a professional society), year of publication, country, title, society, scope of the CPG, date of publication, number of revisions, and type of methodology adopted. The outcomes were extracted and reported in an online Google Sheets document for sharing among all authors.

      Risk of bias assessment and quality appraisal of guidelines

      The assessment of risk of bias and quality assessment of the included CPGs were performed using the AGREE II tool,35 which comprehends 23 items grouped into 6 quality domains: scope and purpose, stakeholder involvement, rigor of development, clarity of presentation, applicability, and editorial independence.
      Each of the 23 items targets various aspects of CPG quality, and was evaluated on a 7-point scale from 1 (strongly disagree) to 7 (strongly agree).
      A final overall assessment includes the rating of the overall quality of the CPG (OA1) and whether the CPG would be recommended for use in practice (OA2).
      To begin the appraisal process, it is recommended that at least 2 (preferably 4) appraisers review each CPG to increase the reliability of the assessment. The standardized domain score would be 0% if each appraiser gave a score of 1 for all the items included in this domain (https://www.agreetrust.org/resource-centre/agree-ii).
      • Brouwers MC
      • Kho ME
      • Browman GP
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      A consensus method for scoring the items was applied. After the review of the 23 items and the comprehensive evaluation by the reviewers, the CPGs were divided into 3 categories according to the AGREE II score: recommended, recommended after revision, and not recommended.

      Statistical analysis

      Statistical analysis was performed using descriptive statistics. We calculated frequencies and raw proportions to summarize the main recommendations for managing perinatal care of pregnant women with SARS-CoV-2 infection and their timing of delivery. In addition, we analyzed guidelines regarding other issues addressed, such as admission to hospital, vaccination policy, etc., and calculated proportions and percentages for each issue. Moreover, we calculated the quality of CPGs using AGREE II domain scores. Mean ± standard deviation (SD) was used to summarize the scores across all the guidelines per domain. The AGREE II tool does not provide any guidelines on how to define scores. To define a CPG as of good quality, we adopted the cutoff score proposed by Amer et al
      • Amer YS
      • Titi MA
      • Godah MW
      • et al.
      International alliance and AGREE-ment of 71 clinical practice guidelines on the management of critical care patients with COVID-19: a living systematic review.
      : if the overall CPG score was >60%, it was recommended; if the overall CPG score was 40% to 60%, it was recommended after modification; and if the CPG score was <40%, it was not recommended. The analysis was performed using Excel, version 16.57 (Microsoft Corporation, Redmond, WA).

      Outcome measures

      The following outcomes related to the management of pregnant women with SARS-CoV-2 infection were addressed: criteria for maternal hospitalization, recommendations for follow-up growth scan, specific recommendations against invasive procedures, use of supportive therapy (antenatal or maternal care), management of labor, indication for cesarean delivery, postpartum care, indication for vaccine booster.

      Results

      Study selection and characteristics

      A total of 20,798 articles were identified and screened; 38 were assessed with respect to their eligibility for inclusion, and 28 CPGs

      Canadian Association of Emergency Physicians. Statement on COVID-19 vaccinations and pregnant and breastfeeding women. 2020. Available at:https://caep.ca/wp-content/uploads/2021/01/CAEPStatement-Vaccination-Pregnancy-COVID.pdf. Accessed February 18, 2022.

      Canadian Association of Perinatal and Women's Health Nurses. Suggestions for the care of the perinatal population. 2020. Available at:https://capwhn.ca/wp-content/uploads/2020/03/CAPWHN_COVID-19_Mar-25-2020.pdf. Accessed February 18, 2022.

      American Academy of Family Physicians. Considerations for pregnancy, breastfeeding, and COVID-19. 2021. Available at: https://www.aafp.org/about/policies/all/breastfeeding-covid19.html. Accessed February 18, 2022.

      Canadian Paediatric Society. Breastfeeding and COVID-19. 2021. Available at:https://cps.ca/documents/position/breastfeeding-when-mothers-have-suspected-or-proven-covid-19. Accessed February 18, 2022.

      American Academy of Pediatrics. FAQs: Management of infants born to mothers with suspected or confirmed COVID-19. 2021. Available at:https://www.aap.org/en/pages/2019-novel-coronavirus-covid-19-infections/clinical-guidance/faqs-management-of-infants-born-to-covid-19-mothers/. Accessed February 18, 2022.

      Centers for Disease Control and Prevention. Care for breastfeeding people. 2020. Available at:https://www.cdc.gov/coronavirus/2019-ncov/hcp/care-for-breastfeeding-women.html. Accessed February 18, 2022.

      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).

      Elwood C, Poliquin V, Boucoiran I, et al. Committee Opinion No. 400: COVID-19 and pregnancy. 2021. Available at:https://sogc.org/common/Uploaded%20files/Covid%20Information/Committee%20Opinion%20No.%20400%20COVID-19%20and%20Pregnancy.Dec.17.2020.pdf. Accessed February 18, 2022.

      Centers for Disease Control and Prevention. COVID-19 vaccines while pregnant or breastfeeding. 2022. Available at:https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/pregnancy.html. Accessed February 18, 2022.

      The American College of Obstetricians and Gynecologists. COVID-19 vaccination considerations for Obstetric-Gynecologic care. 2020. Available at:https://www.acog.org/clinical/clinical-guidance/practice-advisory/articles/2020/12/covid-19-vaccination-considerations-for-obstetric-gynecologic-care. Accessed February 18, 2022.

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      The Royal Australian and New Zealand College of Obstetricians and Gynaecologists. Coronavirus disease (COVID-19) in pregnancy. 2020. Available at:https://ranzcog.edu.au/RANZCOG_SITE/media/RANZCOG-MEDIA/Women%27s%20Health/Global%20Health/RANZCOG-COVID-19-Guide-for-Resource-limited-Environments.pdf. Accessed February 18, 2022.

      International Federation of Gynecology and Obstetrics. Committee on the impact of pregnancy on long-term health. 2022. Available at:https://www.figo.org/what-we-do/figo-divisions-committees/committee-impact-pregnancy-longterm-health. Accessed February 18, 2022.

      New South Wales Health. Guidance for maternity, newborn care and infant feeding, Medicine management for pregnant patients with COVID-19. 2021. Available at:https://www.health.nsw.gov.au/Infectious/covid-19/communities-of-practice/Pages/maternity-and-newborn-care.aspx. Accessed February 18, 2022.

      Quebec Group. Guidelines for the management of the pregnant woman with COVID-19 admitted to the intensive care unit (ICU). 2021 . Available at:https://www.quebec.ca/en/health/health-issues/a-z/2019-coronavirus/information-for-pregnant-women-coronavirus-covid-19. Accessed February 18, 2022.

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      National Institute for Research in Reproductive Health
      Guidance for management of pregnant women in COVID-19 pandemic.
      • Bahtiyar MO
      • Baschat A
      • Deprest J
      • et al.
      Fetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy Network.
      • Martins I
      • Louwen F
      • Ayres-de-Campos D
      • Mahmood T.
      EBCOG position statement on COVID-19 vaccination for pregnant and breastfeeding women.
      • Donders GGG
      • Grinceviciene S
      • Haldre K
      • et al.
      ISIDOG consensus guidelines on COVID-19 vaccination for women before, during and after pregnancy.
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      • Bourne T
      • Kyriacou C
      • Coomarasamy A
      • et al.
      ISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2020-12-09-guidance-for-antenatal-screening-and-ultrasound-in-pregnancy-in-the-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for rationalising earlypregnancy services in the evolving coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2021-05-25-guidance-for-rationalising-early-pregnancy-services-in-the-evolving-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19) vaccination in pregnancy. 2021. Available at: https://www.rcog.org.uk/covid-vaccine. Accessed February 18, 2022.

      Healthcare improvement Scotland. COVID-19 position statement: maternal critical care provision. 2020. Available at:https://www.sign.ac.uk/media/1787/sg-maternal-critical-care-provision_v33.pdf. Accessed February 18, 2022.

      Italian Society of Gynecology and Obstetrics/ Association of Italian Hospital Obstetricians and Gynaecologists. Interim guidance on pregnancy, childbirth, breastfeeding and care of infants (0-2 years) in response to the COVID-19 emergency. 2021. Available at:https://www.iss.it/documents/5430402/0/Rapporto+ISS+COVID-19+2_2021_EN.pdf/421a0bc6-1933-aa77-6b39-a7860d866a16?t=1615472502820. Accessed February 18, 2022.

      were included in the qualitative analyses, whereas 19 were included in quantitative analysis (Tables 1 and 2; Figure). Main recommendations were extracted, synthesized, and reported in Table 3. The CPGs included in this SR were obtained from expert opinions, literature reviews, and expert panel consensus recommendations, and were representative of different countries (16 national, 10 international, and 2 local). The proportion of studies that were published in 2021 was 60.7% (17/28), and 7.1% (2/28) had more than 5 revisions.
      Table 1General characteristics of the clinical practice guidelines included in the quantitative analyses of systematic review
      Di Girolamo. Guidelines for SARS-CoV-2 infection in pregnancy. Am J Obstet Gynecol MFM 2022.
      First author or SocietyYearCountryTitleSocietyScopeDate of pubblicationNumber of revisionsMethod of development
      CAPWHN

      Canadian Association of Perinatal and Women's Health Nurses. Suggestions for the care of the perinatal population. 2020. Available at:https://capwhn.ca/wp-content/uploads/2020/03/CAPWHN_COVID-19_Mar-25-2020.pdf. Accessed February 18, 2022.

      2020CANADASuggestions for the care of the perinatal populationCanadian Association of Perinatal and Women's Health NursesNational20200Expert opinion, methods not reported
      D. CHAWLA
      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).
      2020INDIAPerinatal-Neonatal Management of COVID-19 InfectionFederation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP)National20200Review of literature, expert panel consensus, GRADE
      C. ELWOOD

      Elwood C, Poliquin V, Boucoiran I, et al. Committee Opinion No. 400: COVID-19 and pregnancy. 2021. Available at:https://sogc.org/common/Uploaded%20files/Covid%20Information/Committee%20Opinion%20No.%20400%20COVID-19%20and%20Pregnancy.Dec.17.2020.pdf. Accessed February 18, 2022.

      2020CANADACommittee Opinion No. 400: COVID-19 and PregnancyThe Society of Obstetricians and Gynaecologists of Canada (SOGC)National20212Review of literature, expert panel consensus, methods not reported
      CDC

      Centers for Disease Control and Prevention. COVID-19 vaccines while pregnant or breastfeeding. 2022. Available at:https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/pregnancy.html. Accessed February 18, 2022.

      2020USACOVID-19 Vaccines While Pregnant or BreastfeedingCenters for Disease Control and PreventionNational20213Methods not reported
      ACOG

      The American College of Obstetricians and Gynecologists. COVID-19 vaccination considerations for Obstetric-Gynecologic care. 2020. Available at:https://www.acog.org/clinical/clinical-guidance/practice-advisory/articles/2020/12/covid-19-vaccination-considerations-for-obstetric-gynecologic-care. Accessed February 18, 2022.

      2020USACOVID-19 Vaccination Considerations for Obstetric–Gynecologic CareAmerican College of Obstetricians and GynecologistsNational20213Review of literature, expert panel consensus, methods not reported
      E. Miller

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      2020UKSociety for Maternal-Fetal Medicine and Society for Obstetric and Anesthesia and Perinatology Labor and Delivery COVID-19 ConsiderationThe Society for Maternal-Fetal Medicine (SMFM)National20217Expert opinion, methods not reported
      RANZCOG

      The Royal Australian and New Zealand College of Obstetricians and Gynaecologists. Coronavirus disease (COVID-19) in pregnancy. 2020. Available at:https://ranzcog.edu.au/RANZCOG_SITE/media/RANZCOG-MEDIA/Women%27s%20Health/Global%20Health/RANZCOG-COVID-19-Guide-for-Resource-limited-Environments.pdf. Accessed February 18, 2022.

      2020AUSTRALIACoronavirus Disease (COVID-19) in Pregnancy A guide for resource-limited environmentsThe Royal Australian and New Zealand College of Obstetricians and GynaecologistsNational20203Review of literature, expert panel consensus, methods not reported
      NSW

      New South Wales Health. Guidance for maternity, newborn care and infant feeding, Medicine management for pregnant patients with COVID-19. 2021. Available at:https://www.health.nsw.gov.au/Infectious/covid-19/communities-of-practice/Pages/maternity-and-newborn-care.aspx. Accessed February 18, 2022.

      2020AUSTRALIAGuidance for maternity, newborn care and infant feeding, Medicine management for pregnant patients with COVID-19New South Wales government HealthLocal20213Review of literature, expert panel consensus, methods not reported
      QUEBEC GROUP

      Quebec Group. Guidelines for the management of the pregnant woman with COVID-19 admitted to the intensive care unit (ICU). 2021 . Available at:https://www.quebec.ca/en/health/health-issues/a-z/2019-coronavirus/information-for-pregnant-women-coronavirus-covid-19. Accessed February 18, 2022.

      2020CANADAGuidelines for the management of the pregnant woman with COVID-19 admitted to the intensive care unit (ICU)Quebec Maternal-Fetal. Medicine groupLocal20200Expert panel consensus, methods not reported
      Governament of India

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      2021INDIAGuidelines on operationalization of maternal health services during COVID-19 pandemicMaternal Health Division Ministry of Health & Family WelfareNational20210Methods not reported
      Indian Council of Medical Research

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      2020INDIAGuidance for Management of Pregnant Women in COVID-19 PandemicNational Institute for Research in Reproductive Health (ICMR)National20200Expert panel consensus, methods not reported
      M. O. Bahtiyar
      • Bahtiyar MO
      • Baschat A
      • Deprest J
      • et al.
      Fetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy Network.
      2021USAFetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy NetworkNorth American Fetal Therapy Network (NAFTN)National20210Expert opinion, methods not reported
      L. C. Poon
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      2020nsISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals – an updateInternational Society of Ultrasound in Obstetrics and Gynecology (ISUOG)International20201Review of literature, expert panel consensus, methods not reported
      T. Bourne
      • Bourne T
      • Kyriacou C
      • Coomarasamy A
      • et al.
      ISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2.
      2020nsISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2International Society of Ultrasound in Obstetrics and Gynecology (ISUOG)International20201Review of literature, expert panel consensus, methods not reported
      RCOG

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      2020UKGuidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemicRoyal College of Obstetricians and Gynaecologists (RCOG)National20211.2Review of literature, expert panel consensus, methods not reported
      RCOG

      Royal College of Obstetricians and Gynaecologists. Guidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2020-12-09-guidance-for-antenatal-screening-and-ultrasound-in-pregnancy-in-the-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      2021UKGuidance for rationalising early

      pregnancy services in the evolving coronavirus (COVID-19) pandemic
      Royal College of Obstetricians and Gynaecologists (RCOG)National20212Expert panel consensus, methods not reported
      RCOG

      Royal College of Obstetricians and Gynaecologists. Guidance for rationalising earlypregnancy services in the evolving coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2021-05-25-guidance-for-rationalising-early-pregnancy-services-in-the-evolving-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      2021UKCoronavirus (COVID-19) infection and pregnancyRoyal College of Obstetricians and Gynaecologists (RCOG)National202214.3Expert panel consensus, searching through literature
      HIS

      Healthcare improvement Scotland. COVID-19 position statement: maternal critical care provision. 2020. Available at:https://www.sign.ac.uk/media/1787/sg-maternal-critical-care-provision_v33.pdf. Accessed February 18, 2022.

      2020UKCOVID-19 position statement: Maternal critical care provisionHealthcare improvement Scotland (HIS)National20202Expert opinion, methods not reported
      SIGO/AOGOI

      Italian Society of Gynecology and Obstetrics/ Association of Italian Hospital Obstetricians and Gynaecologists. Interim guidance on pregnancy, childbirth, breastfeeding and care of infants (0-2 years) in response to the COVID-19 emergency. 2021. Available at:https://www.iss.it/documents/5430402/0/Rapporto+ISS+COVID-19+2_2021_EN.pdf/421a0bc6-1933-aa77-6b39-a7860d866a16?t=1615472502820. Accessed February 18, 2022.

      2021ItalyInterim guidance on pregnancy, childbirth, breastfeeding and care of infants (0-2 years) in response to the COVID-19 emergencyItalian Society of Gynaecology and Obstetrics/ Association of Italian Hospital Gynaecologists and ObstetriciansNational20212Review of literature, expert panel consensus, methods not reported
      Not specified (ns)
      Table 2AGREE-ment scores
      Di Girolamo. Guidelines for SARS-CoV-2 infection in pregnancy. Am J Obstet Gynecol MFM 2022.
      *A cut-off for high quality CPGs of 60% or more for all the 6 AGREE II domains were selected in consideration of the limitations associated with the Rapid Guidelines (RGs)’ development. The cut-offs for low and moderate quality are <40% (highlighted in red) and 40%–60% (highlighted in orange), respectively. The cut-offs for high quality are >60% (highlighted in green).
      CAEP.CA, Canadian Association of Emergency Physicians; AAFP, American Academy of Family Physicians; CPS, Canadian pediatric Society; AAP, American Academy of Pediatrics; CDC, Centers for Disease Control and Prevention; CAPWH, Canadian Association of Perinatal and Women's Health Nurses; FOGSI, Federation of Obstetric and Gynaecological Societies of India; NNF, National Neonatology Forum of India; IAP, Indian Academy of Pediatrics; SOGC, The Society of Obstetricians and Gynaecologists of Canada; CDC, Centers for Disease Control and Prevention; SMFM, The Society for Maternal-Fetal Medicine; RANZCOG, The Royal Australian and New Zealand College of Obstetricians and Gynaecologists; FIGO, International Federation of Gynacology and Obstetrics; NSW, New South Wales Government Health; QMFMG, Quebec Maternal-Fetal Medicine group; GOI, Government of India; ICMR, National Institute for Research in Reproductive Health; NAFTN, North American Fetal Therapy Network; ISIDOG, International Society of Infectious Diseases in Obstetrics and Gynecology; ISUOG, International Society of Ultrasound in Obstetrics and Gynecology; RCOG, Royal College of Obstetricians and Gynaecologists; JCV, Joined Commette Vaccination; RCOG, Royal College of Obstetricians and Gynaecologists; HIS, Healthcare improvement Scotland; SIGO/AOGOI, Italian Society of Gynaecology and Obstetrics/ Association of Italian Hospital Gynaecologists and Obstetricians; OA1, Overall Guideline Assessment 1; OA2, Overall Guideline Assessment 2; Y, Yes; YWM, Yes with modifications; N, No.
      Figure 1
      FigurePRISMA flowchart
      Di Girolamo. Guidelines for SARS-CoV-2 infection in pregnancy. Am J Obstet Gynecol MFM 2022.
      PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.
      Table 3Graphic description of issues addressed by eligible rapid guidelines for antenatal care management of pregnant women with COVID-19
      Di Girolamo. Guidelines for SARS-CoV-2 infection in pregnancy. Am J Obstet Gynecol MFM 2022.
      GuidelineCAPWHN

      Canadian Association of Perinatal and Women's Health Nurses. Suggestions for the care of the perinatal population. 2020. Available at:https://capwhn.ca/wp-content/uploads/2020/03/CAPWHN_COVID-19_Mar-25-2020.pdf. Accessed February 18, 2022.

      FOGSI, NNF, IAP
      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).
      SOGC

      Elwood C, Poliquin V, Boucoiran I, et al. Committee Opinion No. 400: COVID-19 and pregnancy. 2021. Available at:https://sogc.org/common/Uploaded%20files/Covid%20Information/Committee%20Opinion%20No.%20400%20COVID-19%20and%20Pregnancy.Dec.17.2020.pdf. Accessed February 18, 2022.

      CDC

      Centers for Disease Control and Prevention. COVID-19 vaccines while pregnant or breastfeeding. 2022. Available at:https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/pregnancy.html. Accessed February 18, 2022.

      ACOG

      The American College of Obstetricians and Gynecologists. COVID-19 vaccination considerations for Obstetric-Gynecologic care. 2020. Available at:https://www.acog.org/clinical/clinical-guidance/practice-advisory/articles/2020/12/covid-19-vaccination-considerations-for-obstetric-gynecologic-care. Accessed February 18, 2022.

      SMFM

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      RANZCOG

      The Royal Australian and New Zealand College of Obstetricians and Gynaecologists. Coronavirus disease (COVID-19) in pregnancy. 2020. Available at:https://ranzcog.edu.au/RANZCOG_SITE/media/RANZCOG-MEDIA/Women%27s%20Health/Global%20Health/RANZCOG-COVID-19-Guide-for-Resource-limited-Environments.pdf. Accessed February 18, 2022.

      NSW

      New South Wales Health. Guidance for maternity, newborn care and infant feeding, Medicine management for pregnant patients with COVID-19. 2021. Available at:https://www.health.nsw.gov.au/Infectious/covid-19/communities-of-practice/Pages/maternity-and-newborn-care.aspx. Accessed February 18, 2022.

      GMFMQ

      Quebec Group. Guidelines for the management of the pregnant woman with COVID-19 admitted to the intensive care unit (ICU). 2021 . Available at:https://www.quebec.ca/en/health/health-issues/a-z/2019-coronavirus/information-for-pregnant-women-coronavirus-covid-19. Accessed February 18, 2022.

      GOI

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      ICMR
      National Institute for Research in Reproductive Health
      Guidance for management of pregnant women in COVID-19 pandemic.
      NAFTN
      • Bahtiyar MO
      • Baschat A
      • Deprest J
      • et al.
      Fetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy Network.
      ISUOG
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      ISUOG
      • Bourne T
      • Kyriacou C
      • Coomarasamy A
      • et al.
      ISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2.
      RCOG

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      RCOG

      Royal College of Obstetricians and Gynaecologists. Guidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2020-12-09-guidance-for-antenatal-screening-and-ultrasound-in-pregnancy-in-the-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      RCOG

      Royal College of Obstetricians and Gynaecologists. Guidance for rationalising earlypregnancy services in the evolving coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2021-05-25-guidance-for-rationalising-early-pregnancy-services-in-the-evolving-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      HIS

      Healthcare improvement Scotland. COVID-19 position statement: maternal critical care provision. 2020. Available at:https://www.sign.ac.uk/media/1787/sg-maternal-critical-care-provision_v33.pdf. Accessed February 18, 2022.

      SIGO

      Italian Society of Gynecology and Obstetrics/ Association of Italian Hospital Obstetricians and Gynaecologists. Interim guidance on pregnancy, childbirth, breastfeeding and care of infants (0-2 years) in response to the COVID-19 emergency. 2021. Available at:https://www.iss.it/documents/5430402/0/Rapporto+ISS+COVID-19+2_2021_EN.pdf/421a0bc6-1933-aa77-6b39-a7860d866a16?t=1615472502820. Accessed February 18, 2022.

      Year2020202020202020202020202020202020202021202020212020202020202021202220202021
      Maternal hospitalization criteria for COVID-19XXXXXX
      Maternal hospitalization criteria for Obstetric conditionsXXXXXX
      Ultrasound scan soon after recoveryXXXXXX
      Monthly surveillance during pregnancy after recoveryXXXXX
      Specific recommendations against invasive proceduresX
      Use of antenatal anticoagulation with LMWH

      XXXXXXXX
      Send placenta to histopathologyX
      Corticosteroids for COVID-19 symptomsXXXXX
      Other Supportive therapies

      during labor
      XXXXXXXXXXXX
      Continuous fetal electronic monitoringXXXXXXX
      Induction of labor at 39 weeksXX
      Indication for CS for COVID-19 symptomsXXX
      Shortening of the second stage of laborXX
      Active pushingX
      Post-partum care: is use LMWH encouraged?X
      Vaccine boosterXXXXX
      CS, Cesarean section; LMWH, low molecular weight heparin; CAPWH, Canadian Association of Perinatal and Women's Health Nurses; FOGSI, Federation of Obstetric and Gynaecological Societies of India; NNF, National Neonatology Forum of India; IAP, Indian Academy of Pediatrics; SOGC, The Society of Obstetricians and Gynaecologists of Canada; CDC, Centers for Disease Control and Prevention; SMFM, The Society for Maternal-Fetal Medicine; RANZCOG, The Royal Australian and New Zealand College of Obstetricians and Gynaecologists; NSW, New South Wales Government Health; QMFMG, Quebec Maternal-Fetal Medicine group; GOI, Government of India; ICMR, National Institute for Research in Reproductive Health; NAFTN, North American Fetal Therapy Network; ISUOG, International Society of Ultrasound in Obstetrics and Gynecology; RCOG, Royal College of Obstetricians and Gynaecologists; HIS, Healthcare improvement Scotland; SIGO/AOGOI, Italian Society of Gynaecology and Obstetrics/ Association of Italian Hospital Gynaecologists and Obstetricians.

      Synthesis of results

      All the CPGs included in the SR did not recommend maternal hospitalization only for SARS-CoV-2 infection, and there was general agreement that admission to hospital should be restricted to women with severe infection. Fifty percent of the included guidelines specifically stated the criteria for maternal admission, including respiratory distress, respiratory rate >22/min, O2 saturation <95%, or rapid deterioration in respiratory status.
      The 46.1% (6/13) of CPGs suggested to perform a fetal growth scan after SARS-CoV-2 infection (generally after 2 weeks); 23.1% (3/13) did not support this practice, whereas the remaining 30.8% (4/13) did not address this point. The proportion of CPGs included in the present review suggesting monthly maternal assessment after the infection was 38.4% (5/13). The large majority of CPGs (80%, 4/5) did not report any contraindication in case the patient should undergo invasive procedures, whereas one suggested delaying chorionic villus sampling and opting for amniocentesis.
      Thromboprophylaxis with low-molecular-weight heparin (LMWH) was recommended for symptomatic women in 77.7% (7/9) of CPGs. None of the CPGs recommended administering corticosteroids only for the presence of SARS-CoV-2 infection in preterm gestation, unless specific obstetrical indication coexists, because such corticosteroid therapy is specifically for fetal lung maturity. Management of labor in women with SARS-CoV-2 infection was addressed by 11 CPGs. Elective induction of labor (IOL) at 39 weeks of gestation was recommended by 18.1% (2/11) of the CPGs, whereas 45.4% (5/11) did not recommend elective induction unless other obstetrical indications coexist with maternal infection. Oxygen support was suggested by 75% of CPGs (9/12), and continuous fetal electronic monitoring by 58.3 % (7/12). There were 27.2% (3/11) of CPGs that recommended shortening of the second stage of labor, mainly with iatrogenic rupture of the membranes or oxytocin infusion, and active pushing was supported by 18.1% (2/11). A general agreement was recorded among the CPGs in not recommending cesarean delivery only for the presence of maternal infection, although 77.7% (7/9) of the guidelines suggested considering it in the case of severe maternal SARS-CoV-2 infection with worsening of maternal conditions. The need for postpartum thromboprophylaxis with LMWH was mentioned in only one CPG out of those included, as well as the need for sending placenta specimens to histopathology for examination. Finally, there was general agreement in recommending completion of vaccine series at least 6 months after the primary vaccine (Table 4), and 88.9% (8/9) of the included CPGs did not report any specific restrictions with regard to the gestational age at vaccination.
      Table 4Description of issues addressed by eligible rapid guidelines for antenatal care management of pregnant women with COVID-19
      Di Girolamo. Guidelines for SARS-CoV-2 infection in pregnancy. Am J Obstet Gynecol MFM 2022.
      Issues (guidelines total=19)N (%)
      • Criteria for hospital admission (12)
      Admission in case of severe disease (not specified)6/12 (50)
      Specific criteria for admission (respiratory distress >22/min, O2 saturation <95%, rapid deterioration in respiratory status)6/12 (50)
      • Ultrasound assessment (13)
      Ultrasound scan soon after recovery
       Recommend6/13 (46.1)
       Recommend against1/13 (7.6)
       No recommendation for or against6/13 (46.1)
      Monthly surveillance during pregnancy after recovery
       Recommend5/13 (38.4)
       Recommend against3/13 (23.0)
       No recommendation for or against4/13 (30.7)
      • Specific recommendations against invasive procedures (5)
       Recommend1/5 (20)
       Recommend against4/5 (80)
      • Use of anticoagulation with LMWH (9)
       Recommend when patient has COVID-19 symptoms7/9 (77.7)
       Recommend against1/9 (11.1)
       Recommend ever1/9 (11.1)
      • Corticosteroids for COVID-19 symptoms (8)
       Recommend, preferably using those not passing placenta4/8 (50.0)
       No recommendation for or against, but still suggested for obstetrical indications as usual4/8 (50.0)
      • Management of labor (12)
       Fluids3/12 (25.0)
       Oxygen9/12 (75.0)
       Continuous fetal electronic monitoring7/12 (58.3)
      Induction of labor at 39 wk (11)
       Recommend2/11 (18.1)
       Recommend against5/11 (45.4)
       Shortening the second stage of labor3/11 (27.2)
      Active pushing2/11 (18.1)
      • Send placenta to histopathology (19)
       No recommendation for or against18/19 (94.7)
       Recommend1/19 (5.2)
      • Indication for CD in case of symptomatic COVID-19 (9)
       Recommend against, but consider in severe or worsening course of the disease7/9 (77.7)
       Recommend against2/9 (22.2)
      • Postpartum care: is use of LMWH recommended? (19)
       No recommendation for or against18/19 (94.7)
       Recommend1/19 (5.2)
      • Vaccine booster (5)
       Recommend, pregnant women at increased risk1/5 (20)
       Recommend, 6 mo after their Pfizer/Moderna primary series4/5 (80)
      CD, cesarean delivery; LMWH, low-molecular-weight heparin.

      Methodological quality of clinical practice guidelines

      The AGREE II domains are summarized in Table 2. The average AGREE II standardized score for each domain is reported below (mean±SD).
      The cutoff for CPGs of high quality was >60%, represented in green (Table 2). Medium quality (with 40%–59% cutoff) was represented in yellow and low quality in red.
      Only 1 CPG
      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).
      reported the use of the Grading of Recommendations, Assessment, Development and Evaluation (GRADE) approach.
      The AGREE II standardized domain scores for the first overall assessment (OA1) had a mean of 50% (SD±21.0%). Nine CPGs scored >60%

      Centers for Disease Control and Prevention. Care for breastfeeding people. 2020. Available at:https://www.cdc.gov/coronavirus/2019-ncov/hcp/care-for-breastfeeding-women.html. Accessed February 18, 2022.

      ,
      • Chawla D
      • Chirla D
      • Dalwai S
      • et al.
      Perinatal-neonatal management of COVID-19 infection - guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).
      ,

      Centers for Disease Control and Prevention. COVID-19 vaccines while pregnant or breastfeeding. 2022. Available at:https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/pregnancy.html. Accessed February 18, 2022.

      ,

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      ,
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      ,

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for antenatal screening and ultrasound in pregnancy in the coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2020-12-09-guidance-for-antenatal-screening-and-ultrasound-in-pregnancy-in-the-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Guidance for rationalising earlypregnancy services in the evolving coronavirus (COVID-19) pandemic. 2021. Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/2021-05-25-guidance-for-rationalising-early-pregnancy-services-in-the-evolving-coronavirus-covid-19-pandemic.pdf. Accessed February 18, 2022.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19) vaccination in pregnancy. 2021. Available at: https://www.rcog.org.uk/covid-vaccine. Accessed February 18, 2022.

      and revealed a consensus agreement between the reviewers on recommending their use.

      Discussion

      Summary of the main findings

      The findings of this SR of CPGs showed that significant heterogeneity and disagreement were assessed in several aspects of clinical management of SARS-CoV-2 infection in pregnancy as reported by the published CPGs. There was a general agreement in the criteria for maternal hospitalization, mode of delivery, and recommendation for vaccine booster. Conversely, a large heterogeneity was observed in several other management aspects, including type and frequency of maternal assessment after the infection, ultrasound scans, timing of delivery, and type of fetal monitoring during labor.

      Strengths and limitations

      This SR of CPGs on SARS-CoV-2 infection in pregnancy used a recognized tool (AGREE II) for evaluating medical guidelines. Other strengths included the thorough literature search and assessment of the multitude of management aspects of pregnancies with SARS-CoV-2 infection. The main weakness of the present review is the methodological quality of some of the included CPGs, as indicated by their low AGREE II scores.
      Of note, the methods of guideline development were not reported for most of the included CPGs, making the assessment of Domain 3 with AGREE II challenging, thus limiting an objective evaluation of the included CPGs. It has been suggested that Domains 3 and 5 (applicability), in addition to domain 6 (editorial independence), may have had the greatest effect on the results of the 2 overall assessments of the CPGs. These guidelines were developed as an acute response to a period of crisis, which partially explains the lack of detailed methodological descriptions for some of the included guidelines. However, a positive sign in CPG development methodology was the application of GRADE in some of the more recent CPGs, indicating improvements in their quality and trustworthiness.

      Interpretation of the study findings, clinical and research implications

      The rapid spread of the pandemic has made the availability of objective evidence-based guidelines on the management of SARS-CoV-2 infection in pregnancy critical. Pregnancy represents an independent risk factor for severe SARS-CoV-2 infection, and infected women are at higher risk of adverse maternal outcomes, including mechanical ventilation, admission to the intensive care unit, and even death, compared with nonpregnant infected women.
      • Carbone L
      • Esposito R
      • Raffone A
      • Verrazzo P
      • Carbone IF
      • Saccone G.
      Proposal for radiologic diagnosis and follow-up of COVID-19 in pregnant women.
      • Di Mascio D
      • D'Antonio F
      Perinatal mortality and morbidity of SARS-COV-2 infection during pregnancy in European countries: findings from an international study.
      • Jamieson DJ
      • Rasmussen SA
      An update on COVID-19 and pregnancy.
      Several risk factors have been associated with an increased risk of symptomatic infection, including obesity, hypertension, underlying respiratory disorder, and Black or Asian race.
      • Hawkins D.
      Differential occupational risk for COVID-19 and other infection exposure according to race and ethnicity.
      ,
      • Gao YD
      • Ding M
      • Dong X
      • et al.
      Risk factors for severe and critically ill COVID-19 patients: a review.
      In view of such associations, all pregnant women with SARS-CoV-2 infection should be closely monitored for the development of symptoms and signs of severe COVID-19 disease. Importantly, some of the clinical manifestations of COVID-19 overlap with symptoms of normal pregnancy (ie, fatigue, shortness of breath, nasal congestion, nausea or vomiting), which should be considered during the evaluation of afebrile symptomatic women. Nevertheless, 75% of women will experience an asymptomatic infection, not requiring hospitalization.
      • Khan DSA
      • Hamid LR
      • Ali A
      • et al.
      Differences in pregnancy and perinatal outcomes among symptomatic versus asymptomatic COVID-19-infected pregnant women: a systematic review and meta-analysis.
      In the present review, there was general agreement on the criteria for maternal hospital admission in those with SARS-CoV-2 infection, with all the included CPGs recommending hospitalization only for severe disease. Moreover, although pregnant women still show hesitancy toward COVID-19 vaccines,
      • Carbone L
      • Mappa I
      • Sirico A
      • et al.
      Pregnant women's perspectives on severe acute respiratory syndrome coronavirus 2 vaccine.
      • Mappa I
      • Luviso M
      • Distefano FA
      • Carbone L
      • Maruotti GM
      • Rizzo G.
      Women perception of SARS-CoV-2 vaccination during pregnancy and subsequent maternal anxiety: a prospective observational study.
      • Carbone L
      • Di Girolamo R
      • Mappa I
      • et al.
      Worldwide beliefs among pregnant women on SARS-CoV-2 vaccine: a systematic review.
      CPGs already declared the safety and efficacy of available messenger RNA vaccines against SARS-CoV-2 infection, and also the usefulness of the booster dose in reducing the rate of complications during pregnancy (Tables 3 and 4). The association between SARS-CoV-2 variants and maternal or perinatal outcomes represents another particular issue given that the risk of adverse outcomes may vary according to virus variants, thus affecting the recommendations provided by CPGs. Most of the reported data on the association between SARS-CoV-2 infection and maternal outcomes come from the early stages of the pandemic when wild-type SARS-CoV-2 predominated. A recent study carried out through the UK Obstetric Surveillance System, including over 4000 pregnant women, reported that the Alpha and Delta variants have been associated with more severe disease in pregnancy than the wild-type variant.

      Vousden N, Ramakrishnan R, Bunch K, et al. Severity of maternal infection and perinatal outcomes during periods of SARS-CoV-2 wildtype, alpha, and delta variant dominance in the UK: prospective cohort study. 2022. Available at: https://bmjmedicine.bmj.com/content/1/1/e000053.info. Accessed February 18, 2022.

      After adjustment for potential confounding factors, both Alpha and Delta were independently associated with admission to the intensive care unit. Conversely, no difference was found in the risk of perinatal outcomes (mainly stillbirth) between wild-type, Alpha, and Delta variants. The effect of the Omicron variant on maternal and perinatal outcomes is more difficult to assess because most studies included fully vaccinated women. Birol Ilter et al
      • Birol Ilter P
      • Prasad S
      • Berkkan M
      • et al.
      Clinical severity of SARS-CoV-2 infection among vaccinated and unvaccinated pregnancies during the Omicron wave.
      reported that fully vaccinated pregnant women infected with SARS-CoV-2 during the Omicron wave had milder illness and were less likely to require oxygen supplementation and intensive care than their unvaccinated counterparts. Despite the apparently lower risk of adverse maternal outcomes reported in vaccinated pregnant women with SARS-CoV-2 infection, it is not possible to provide specific guidelines for women infected with the Omicron variant for various reasons. First, viral sequencing is not extensively undertaken. Second, the studies reporting the outcomes of pregnant women infected with the Omicron variant include mainly vaccinated women, thus potentially biasing their findings. Last, pregnancy represents an independent risk factor for adverse outcomes in SARS-CoV-2 infection, and COVID-19–positive women should be thoroughly followed up because the course of the infection may be unpredictable.
      Recent studies and SRs have reported that a large proportion of pregnancies complicated by SARS-CoV-2 infection have placental histopathologic abnormalities consistent with placental inflammation and hypoperfusion. Although there is no standard definition of placental SARS-CoV-2 infection and no definite COVID-19–specific placental changes, the association between infection and placental signs of the disease raises the question of whether these pregnancies should undergo more intensive surveillance to identify placenta-related complications such as preeclampsia or fetal growth restriction. Indeed, it should be recommended to send placental tissue of all SARS-CoV-2–infected pregnant women to histopathology.
      • Di Girolamo R
      • Khalil A
      • Alameddine S
      • et al.
      Placental histopathology after SARS-CoV-2 infection in pregnancy: a systematic review and meta-analysis.
      A recent meta-analysis of observational studies reported 62% higher odds of developing preeclampsia among infected patients. Furthermore, preeclampsia with severe features, eclampsia, HELLP syndrome, and preterm birth are also reported to be increased in pregnant women with SARS-CoV-2 infection, whereas the association with preterm birth is less established. Likewise, there is emerging evidence on the increased risk of stillbirth in pregnant women with SARS-CoV-2 infection. A recent report from the United States including 1.2 million births reported that the risk of stillbirth was 1.26% in infected women vs 0.64% in noninfected women. The risk of stillbirth increased with the presence of comorbidities such as chronic hypertension, multiple gestation, cardiac disease, placental abruption, acute respiratory distress syndrome, and mechanical ventilation, and was mainly due to the Delta virus variant.
      • DeSisto CL
      • Wallace B
      • Simeone RM
      • et al.
      Risk for stillbirth Among women with and Without COVID-19 at delivery hospitalization - United States, March 2020-September 2021.
      In the present review, there was no general agreement on the need for increased maternal and fetal surveillance after the infection, with nearly half of the CPGs suggesting increased fetal surveillance starting from 15 days following maternal infection. (Tables 3 and 4)
      Another important dilemma in the management of SARS-CoV-2 infection in pregnancy is the timing of birth. The recently published ARRIVE (A Randomized Trial of Induction Versus Expectant Management) trial reported that elective IOL at 39 weeks of gestation results in a significantly lower frequency of cesarean delivery in healthy pregnancies.
      • Grobman WA
      • Rice MM
      • Reddy UM
      • et al.
      Labor Induction versus Expectant Management in Low-Risk Nulliparous Women.
      Since the beginning of the pandemic, elective delivery of women with asymptomatic or nonsevere SARS-CoV-2 infection at 39 weeks of gestation has been suggested by several authors to decrease the risk of worsening maternal status before the onset of spontaneous labor.
      • Boelig RC
      • Manuck T
      • Oliver EA
      • et al.
      Labor and delivery guidance for COVID-19.
      Elective IOL at 39 weeks of gestation was suggested by only 2 CPGs,

      Society for Maternal-Fetal Medicine. Coronavirus (COVID-19). 2022. Available at: https://www.smfm.org/covid19. Accessed February 18, 2022.

      ,

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      whereas the remaining CPGs did not specifically recommend this practice. Conversely, in severely symptomatic women, delivery could be indicated by the worsening of maternal clinical conditions and may be considered by 32 to 34 weeks’ gestation.

      Maternal Health Division Ministry of Health & Family Welfare. Guidelines on operationalization of maternal health services during COVID-19 pandemic. 2021. Available at:https://covid19.india.gov.in/document/guidelines-on-operationalization-of-maternal-health-services-during-the-covid-19-pandemic/. Accessed February 18, 2022.

      National Institute for Research in Reproductive Health
      Guidance for management of pregnant women in COVID-19 pandemic.
      • Bahtiyar MO
      • Baschat A
      • Deprest J
      • et al.
      Fetal interventions in the setting of the coronavirus disease 2019 pandemic: statement from the North American Fetal Therapy Network.
      • Martins I
      • Louwen F
      • Ayres-de-Campos D
      • Mahmood T.
      EBCOG position statement on COVID-19 vaccination for pregnant and breastfeeding women.
      • Donders GGG
      • Grinceviciene S
      • Haldre K
      • et al.
      ISIDOG consensus guidelines on COVID-19 vaccination for women before, during and after pregnancy.
      • Poon LC
      • Yang H
      • Dumont S
      • et al.
      ISUOG Interim Guidance on coronavirus disease 2019 (COVID-19) during pregnancy and puerperium: information for healthcare professionals - an update.
      • Bourne T
      • Kyriacou C
      • Coomarasamy A
      • et al.
      ISUOG Consensus Statement on rationalization of early-pregnancy care and provision of ultrasonography in context of SARS-CoV-2.

      Royal College of Obstetricians and Gynaecologists. Coronavirus (COVID-19), pregnancy and women's health. 2020. Available at:https://www.rcog.org.uk/coronavirus-pregnancy. Accessed February 18, 2022.

      It is the collective authors’ opinion that, despite the coverage offered by the COVID-19 vaccines, women with SARS-CoV-2 infection should be strictly followed up to detect early signs of severe infection. Risk stratification is crucial when assessing these mothers because some particular medical conditions, mainly preeclampsia and diabetes mellitus, represent additional independent risk factors for the development of severe infection. In this scenario, women with such additional risk factors should undergo a closer follow-up. A growth scan within a month from the infection is advisable in view of the association between SARS-CoV-2 infection and placenta-related disorders, mainly fetal growth restriction. Last, timing of IOL should be carefully evaluated. Although elective IOL at 39 weeks’ gestation in women with current or previous SARS-CoV-2 infection is not the common clinical practice in any of the authors’ affiliated institutions, a closer follow-up of these women is commonly considered because of the association between infection and placenta-related disorders. This allows the identification of pregnancies at higher risk of adverse perinatal outcomes, which may benefit from elective IOL.

      Conclusions

      A significant heterogeneity was found in some of the main aspects of clinical management of SARS-CoV-2 infection in pregnancy, as suggested by the published CPGs, especially regarding follow-up after the infection and timing of delivery. The findings from this SR highlight the need for developing shared guidelines supported, endorsed, and promoted by national and international professional societies to make the management of SARS-CoV-2 infection in pregnant women more homogeneous among different countries.

      Appendix. Supplementary materials

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