SARS-CoV-2 in Pregnancy: A Comprehensive Summary of Current Guidelines

Since the declaration of the global pandemic of COVID-19 by the World Health Organization on 11 March 2020, we have continued to see a steady rise in the number of patients infected by SARS-CoV-2. However, there is still very limited data on the course and outcomes of this serious infection in a vulnerable population of pregnant patients and their fetuses. International perinatal societies and institutions including SMFM, ACOG, RCOG, ISUOG, CDC, CNGOF, ISS/SIEOG, and CatSalut have released guidelines for the care of these patients. We aim to summarize these current guidelines in a comprehensive review for patients, healthcare workers, and healthcare institutions. We included 15 papers from 10 societies through a literature search of direct review of society’s websites and their journal publications up till 20 April 2020. Recommendations specific to antepartum, intrapartum, and postpartum were abstracted from the publications and summarized into Tables. The summary of guidelines for the management of COVID-19 in pregnancy across different perinatal societies is fairly consistent, with some variation in the strength of recommendations. It is important to recognize that these guidelines are frequently updated, as we continue to learn more about the course and impact of COVID-19 in pregnancy.


Introduction
The World Health Organization (WHO) declared a global pandemic of COVID-19, caused by SARS-CoV-2 on 11 March 2020 [1]. The rapidly escalating numbers of individuals infected globally remain on the rise and little is still known about the course and outcomes of this serious infection in a vulnerable population of pregnant patients and their fetuses.
A variety of professional societies and institutions involved in the care of pregnant patients including Society for Maternal and Fetal Medicine (SMFM) [2,3] from United States, American College of Obstetrics and Gynecology (ACOG) [4,5] from United States, Royal College of Obstetrics and Gynecology (RCOG) [6] from United Kingdom, International Society for Ultrasound in Obstetrics and Gynecology (ISUOG) [7], United States Centers of disease control (CDC) [8,9]. In World Health Organization (WHO) [10], College National de Gynecologie et Obstetrique Francais (CNGOF) [11] from France, Istituto Superiore di Sanità/Società Italiana di Ecografia Ostetrico Ginecologica (ISS/SIEOG) [12,13] from Italy, and the Catalan Health Service (CatSalut) [14] from Spain have released independent guidelines for the assessment and care of pregnant patients from prenatal course to intrapartum to postpartum.
A paper published by Boelig et al. in March 2020 [3] to guide Maternal Fetal Medicine specialists on the care of SARS-Cov-2 pregnant patients urged healthcare providers and their institution to develop internal guidelines to have their unit ready to care for these patients.
In order to help institutions keep up with this rapidly evolving landscape. In authors of this paper aim to summarize and discuss all the current guidelines put forth by the aforementioned professional societies and institutions into one document. The goal is to allow institutions access to a comprehensive summary of guidelines related to the SARS-Cov-2 pandemic in pregnancies, which they can adapt to their practice environment and capabilities. The primary focus of all published guidelines is to design a model where patients and their families, as well as healthcare workers (HCW) in the frontline of the pandemic are protected and prepared.

Experimental Section
Perinatal guidelines that are frequently cited in the United States include publications by SMFM, ACOG, and ISUOG. However, to encompass a global picture and include guidelines that can be generalized to a larger patient population, we included some international guidelines from five countries (US, UK, Italy, Spain, and France). These were selected based on our collaboration with the co-authors from the respective countries to help with translation of documents or clinical application relevance; these societies include RCOG from United Kingdom, CNGOF from France, CatSalut from Spain, and ISS/SIEOG from Italy. Publications from outside of United States were selected by authors affiliated with that country, respectively. We also included WHO and CDC for their expertise in global health care and infectious diseases, respectively.
A literature search was performed through direct review of all the aforementioned society's website and journal publications and PubMed. Guidelines published between December 2019 and 20 April 2020, with selection of the most updated versions, were included. The search plan for SMFM, ACOG, and RCOG were arranged and done by two authors K.N. and E.I. with input from the study's principal investigator-R.R. RCOG publication was reviewed by author M.K. from the UK, CNFOG was reviewed, selected and translated by author O.P., CatSalut publication was reviewed, selected, and translated by authors R.E., A.S., E.C. from Spain, and ISS/SEIOG was reviewed, selected and translated by author G.T. from Italy-all applying the Preferred Reporting Items for Systematic Reviews and Meta Analyses (PRISMA) guidelines for the data extraction and quality assessment. Keywords used to search include COVID-19 and/or SARS-CoV-2 infection in pregnancy and the name of the society. Publications were included if they are an original document from the society, if they outline details on management of patients either during antepartum, intrapartum or postpartum, and if they were expert opinions or expert guidance. Exclusion criteria include case series, case reports, retrospective cohort studies, systematic reviews, or metanalyses. ACOG, SMFM, ISS, and CDC had two publications relevant to guidance for perinatal care and were all included. All other societies had one publication each. A total of 15 papers were identified from 10 societies and reviewed by two authors (K.N. and E.I.) who were in agreement. The list of publications included are summarized in (Table 1), arranged in ascending order of publication date. All the publications were thoroughly reviewed and important points of discussions were abstracted and summarized into antepartum, intrapartum, and postpartum management, as discussed in the next section. Not all publications addressed every aspect of care, but we summarized the most salient points in each publication in order to highlight the similarities and differences amongst these international guidelines.

Results
After reviewing all the publications, information was classified into antepartum, intrapartum, or postpartum management and was summarized in a systematic fashion into Tables 2-4, respectively.

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Prenatal and antepartum care (See Table 2): Reviewed guidelines support some form of screening of pregnant patients depending on symptoms and exposure, use of telehealth is encouraged for prenatal visits, while limiting face to face visits and ultrasounds only to those that are medically necessary. Prenatal appointments, lab work, and ultrasounds should be scheduled on the same day if possible. All ultrasound equipment and patient rooms should be appropriately cleaned after each use. The use of antenatal corticosteroids for fetal lung maturation can be continued till 34 weeks gestation, but the use of steroids in the late preterm period, >34 0/7 weeks gestation remains controversial.

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Intrapartum care (See Table 3): Reviewed guidelines recommend a designated area within the unit to care for SARS-CoV-2 positive pregnant patients or Person under investigation (PUI).
Timing and mode of delivery should follow routine obstetric indications. Cesarean section (CS) should be reserved for obstetric indications only; infection with SARS-CoV-2 is not an indication for cesarean delivery unless there is acute decompensation of mother or fetus. Only one consistent asymptomatic support person is allowed to be present at time of delivery. Patients and healthcare workers should be appropriately gowned, gloved, and have protective face masks; specifically, N95 should be used for aerosol generating procedures such as forceful expiration during pushing, use of oxygen for intrauterine resuscitation, or intubation. Use of operative delivery to shorten the second stage of labor can be considered for routine obstetric indications.
There is no contraindication to regional or general anesthesia if indicated, but appropriate personal protective equipment (PPE) use is encouraged.

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Postpartum care (See Table 4): Reviewed guidelines encourage early discharge from the hospital, one day for vaginal delivery and two days for cesarean delivery. This limits face to face exposure and increases bed availability. Separation of mother and baby or discouraging breastfeeding are not advised, unless the mother is acutely ill. However, mothers are encouraged to (1) practice respiratory hygiene during feeding, (2) wear a mask, (3) wash hands before and after touching the baby, and (4) routinely clean and disinfect surfaces they have touched. If breastpumping is used, all equipment should be cleaned thoroughly before and after each use. Postpartum visits should be performed over telehealth, unless face to face visit is essential to management.

Discussion
The summary of the reviewed guidelines for the management of COVID-19 in pregnancy across different professional societies and institutions is consistent, with some variation in the strength of recommendations. Global societies such as WHO and CDC have a similar approach to their guideline publication, keeping their recommendations broad so it can be utilized across all shapes and sizes of healthcare institutions. Many of their recommendations overlap with those for the general population and they provide great resources to guide readers to perinatal societies for more specific questions.
International perinatal societies, including ACOG, RCOG, SMFM, ISUOG, CNGOF, ISS/SIEOG, and public institution CatSalut, all share similar recommendations answering questions that are very specific to the care of pregnant patients-from prenatal screening, antepartum care, details of intrapartum care during different stages of labor in emergency and non-emergency settings to postpartum care and follow up. The guidelines put forth by SMFM (United States) are most specific to the care of high risk pregnancies, given their expertise in this field. ACOG (United States) and RCOG (United Kingdom) summarize recommendations that are suitable for lower risk pregnant patients. CNGOF (France) and ISS/SIEOG (Italy) and CatSalut (Barcelona) give some practical recommendations for the management of infected pregnant women. ISUOG (International) provides more information specific to managing and cleaning ultrasound equipment-an essential tool in the care of pregnant patients, which could be a vector for disease transmission if sanitization is not a priority.
The consensus amongst all perinatal societies encourages all institutions to transition to telehealth when appropriate and limit the number of face to face visits. Ultrasounds and antenatal surveillance should be performed only if medically indicated. The use of antenatal steroids for fetal lung maturation for patients at high risk of preterm birth within seven days should still be performed if pregnancy is between 24 0/7 to 33 6/7 weeks gestation, but use during late preterm of 34 0/7 to 36 6/7 weeks gestation is still controversial. All institutions should set up a designated screening area, labor and delivery rooms, and operating rooms for SARS-CoV-2 infected patients. All patients should be screened for symptoms, travel history, contact history, and follow the appropriate algorithm provided to guide need for performing real time PCR tests. If elective procedures or induction of labor is scheduled, patients should first be screened and triaged over the phone, followed by a nasopharyngeal swab for SARS-CoV-2 infection. This screening should be done within a time frame to allow the test results to return before the scheduled procedure date. For urgent or emergent obstetric conditions, screening for SARS-CoV-2 should be performed right away, but procedures should not be delayed for results to return; patients should be treated as a PUI and managed as presumptive positive.
As the numbers of testing sites and resources have increased over the past few weeks, there should be consideration for screening every pregnant patient being admitted, regardless of exposure, history or symptoms. Societies recommend only one consistent support person to be present during delivery. Mode and timing of delivery should still be performed on the basis of routine obstetric indications, and delivery should be expedited with cesarean delivery in the event of maternal deterioration due to severe COVID-19 disease or fetal distress. Aerosol generating procedures such as the use of supplemental oxygen, intubation, and forceful pushing should be avoided to protect everyone in the delivery room. Appropriate PPE should be donned by patients and healthcare workers during all interactions. N95 should be worn during aerosol generating procedures.
Currently, there is no definitive evidence to suggest vertical transmission of SARS-CoV-2. As a result, mother and baby separation and discouraging breastfeeding are not advised unless the mother is acutely ill. Mothers who are acutely ill with SARS-CoV-2 infection are advised the option for breast pumping, and to wash hands before handling baby or touching pumps or bottle, avoid coughing while baby is feeding, and consider wearing a face mask while feeding or handling baby. If a breast pump is used, clean properly after each use and routinely clean all surfaces that are touched. The length of hospital stay should be decreased to one day for vaginal delivery and two days for cesarean delivery to limit time of exposure for patients and healthcare workers in the hospital while also increasing bed capacity. Once discharged, patients are advised to continue social distancing, and routine postpartum visits can be conducted using telehealth. The method of telehealth should be individualized based on institution resources and availability.

Conclusions
The present manuscript summarizes the guidelines for Obstetrical and perinatal management of pregnant women during the SARS-CoV-2 pandemic, which can be an overall reference for Obstetricians all over the world. Many similarities are identified amongst these guidelines. All of the international professional societies and institutions discussed in this paper, including ACOG, RCOG, SMFM, ISUOG, WHO, CNGOF, ISS/SIEOG, CatSalut and CDC, continue to work tirelessly to put forth updated information for the care of pregnant patients and beyond. This manuscript also provides the summary of the source for continuous updates. It is imperative for readers to continue to use the most updated guidelines available as we continue to learn more about the impacts of the SARS-Cov-2 pandemic in pregnancy.