<scp>ISUOG</scp> Interim Guidance on coronavirus disease 2019 (COVID‐19) during pregnancy and puerperium: information for healthcare professionals – an update

Abstract

In response to the World Health Organization (WHO) statements and international concerns regarding the coronavirus disease 2019 (COVID-19) outbreak, the International Society of Ultrasound in Obstetrics and Gynecology (ISUOG) is issuing the following guidance for management during pregnancy and puerperium. Given the uncertainty regarding many aspects of the clinical course of COVID-19 in pregnancy, frequently updated information may help obstetricians and ultrasound practitioners in counseling pregnant women and further improve our understanding of the pathophysiology of COVID-19 in pregnancy. This statement, which is an update on our previous Interim Guidance1 (Appendix S1), is not intended to replace other previously published interim guidance on evaluation and management of COVID-19-exposed pregnant women and should be considered in conjunction with relevant advice from organizations such as: American College of Obstetricians and Gynecologists (ACOG): https://www.acog.org/clinical-information/physician-faqs/covid-19-faqs-for-ob-gyns-obstetrics Centers for Disease Control and Prevention (CDC): https://www.cdc.gov/coronavirus/2019-ncov/hcp/inpatient-obstetric-healthcare-guidance.html European Centre for Disease Prevention and Control (ECDC): https://www.ecdc.europa.eu Indicazioni ad interim della Societa Italiana di Neonatologia (SIN): https://www.sin-neonatologia.it/wp-content/uploads/2020/03/SIN.COVID19-10-maggio.V3-Indicazioni-1.pdf International Federation of Gynecology and Obstetrics (FIGO): https://obgyn.onlinelibrary.wiley.com/doi/epdf/10.1002/ijgo.13156 Ministry of Health, Brazil: https://www.conasems.org.br/wp-content/uploads/2020/03/guia_de_vigilancia_2020.pdf National Health Commission of the People's Republic of China: http://www.nhc.gov.cn Pan American Health Organization (PAHO): http://www.paho.org Perinatal Medicine Branch of Chinese Medical Association: https://mp.weixin.qq.com/s/11hbxlPh317es1XtfWG2qg Public Health England: https://www.gov.uk/guidance/coronavirus-covid-19-information-for-the-public Royal College of Obstetricians and Gynaecologists (RCOG): https://www.rcog.org.uk/en/guidelines-research-services/guidelines/coronavirus-pregnancy/ Santé Publique France: https://www.santepubliquefrance.fr/ Sociedad Española de Ginecología y Obstetricia (S.E.G.O.): https://mcusercontent.com/fbf1db3cf76a76d43c634a0e7/files/1abd1fa8-1a6f-409d-b622-c50e2b29eca9/RECOMENDACIONES_PARA_LA_PREVENCIO_N_DE_LA_INFECCIO_N_Y_EL_CONTROL_DE_LA_ENFERMEDAD_POR_CORONAVIRUS_2019_COVID_19_EN_LA_PACIENTE_OBSTE_TRICA.pdf Society for Maternal-Fetal Medicine: https://www.smfm.org/covidclinical World Health Organization (WHO): https://www.who.int/emergencies/diseases/novel-coronavirus-2019 Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), is a global public health emergency. Since the first case of COVID-19 pneumonia was reported in Wuhan, Hubei Province, China, in December 2019, the infection has spread rapidly to the rest of China and beyond2, 3. Coronaviruses are enveloped, non-segmented, positive-sense ribonucleic acid (RNA) viruses belonging to the family Coronaviridae, order Nidovirales4. The epidemics of the two β-coronaviruses, severe acute respiratory syndrome coronavirus (SARS-CoV) and Middle East respiratory syndrome coronavirus (MERS-CoV), have caused more than 10 000 cumulative cases in the past two decades, with mortality rates of 10% for SARS-CoV and 37% for MERS-CoV5-8. SARS-CoV-2 belongs to the same β-coronavirus subgroup and it has genome similarity of about 80% and 50% with SARS-CoV and MERS-CoV, respectively9. SARS-CoV-2 is spread by respiratory droplets and direct contact (when body fluids of an infected person touch another person's eyes, nose or mouth, or an open cut, wound or abrasion). It should be noted that SARS-CoV-2 has been found in a laboratory environment to be viable on plastic and stainless-steel surfaces for up to 72 h, whereas on copper and cardboard it is viable for up to 24 h10. SARS-CoV-2 also remains viable and infectious in aerosols for hours, raising the possibility of airborne transmission. The Report of the World Health Organization (WHO)-China Joint Mission on Coronavirus Disease 2019 (COVID-19)11 estimated a high R0 (reproduction number) of 2–2.5. The latest report from WHO12, on April 10th, estimated the global mortality rate of COVID-19 to be 6.1%. However, other reports, which utilized appropriate adjustment for the case ascertainment rate and the time lag between onset of symptoms and death, suggested the mortality rate to be lower, at 1.4%13. Huang et al.14 first reported on a cohort of 41 patients with laboratory-confirmed COVID-19 pneumonia. They described the epidemiological, clinical, laboratory and radiological characteristics, as well as treatment and clinical outcome of the patients. Subsequent studies with larger sample sizes have shown similar findings15, 16. The most common symptoms reported are fever (88.5%) and cough (68.6%)17. Myalgia or fatigue (35.8%), expectoration (28.2%) and dyspnea (21.9%) are also reported17. Diarrhea (4.8%) and nausea and vomiting (3.9%) are less common17. Breslin et al.18 observed similar COVID-19 severity in pregnant patients (86.0% mild disease, 9.3% severe disease and 4.7% critical disease) to that reported in non-pregnant patients16. On admission, ground-glass opacity is the most common radiologic finding on computed tomography (CT) of the chest (56.4%)16. No radiographic or CT abnormality was found in 157 of 877 (17.9%) patients with non-severe disease and in five of 173 (2.9%) patients with severe disease. Lymphocytopenia was reported to be present in 64.5% of patients on admission17. Elevated C-reactive protein and lactic dehydrogenase were observed in 44.3% and 28.3% of patients, respectively. Breslin et al. screened asymptomatic pregnant patients admitted to the labor ward, and found that 32.6% of them tested positive; however, 71.4% of these patients developed symptoms during admission or early postpartum18. Universal testing for COVID-19 remains a topic of debate and its need is determined mainly by local protocol and prevalence of the disease. A recent study from New York, USA, reported that a relatively large proportion (13.5%) of patients without any symptoms admitted for delivery tested positive for SARS-CoV-219. Of these patients, 10% developed fever before discharge from the hospital. This indicates the potential problem with triaging patients based merely on symptoms in areas with widespread community infection. Pregnancy is a physiological state that predisposes women to respiratory complications of viral infection. Due to the physiological changes in their immune and cardiopulmonary systems, pregnant women are more likely to develop severe illness after infection with respiratory viruses20. In 2009, pregnant women accounted for 1% of patients infected with influenza A subtype H1N1 virus, but they accounted for 5% of H1N1-related deaths21. In addition, SARS-CoV and MERS-CoV are both known to be responsible for severe complications during pregnancy, including the need for endotracheal intubation, admission to an intensive care unit (ICU), renal failure and death8, 22. The case fatality rate of SARS-CoV infection among pregnant women is up to 25%8. Currently, however, there is no evidence that pregnant women are more susceptible to SARS-CoV-2 or that those with COVID-19 are more prone to developing severe pneumonia18, 23-28. Over and above the impact of COVID-19 on a pregnant woman, there are concerns relating to the potential effect on fetal and neonatal outcome; therefore, pregnant women require special attention in relation to prevention, diagnosis and management. Based on the limited information available as yet and our knowledge of other similar viral pulmonary infections, the following expert opinions are offered to guide clinical management. Case definitions are those included in the WHO's interim guidance, ‘Global surveillance for COVID-19 caused by human infection with COVID-19 virus’29. Note: for confirmed asymptomatic cases, the period of contact is measured from 2 days before to 14 days after the date on which the sample that led to confirmation was taken. A person with laboratory confirmation of COVID-19, irrespective of clinical signs and symptoms. Evidence suggests that a proportion of transmissions occur from cases with no or mild symptoms that do not provoke healthcare-seeking behavior30. Under these circumstances, in areas in which local transmission occurs, an increasing number of cases without a defined chain of transmission is observed and a lower threshold for suspicion in patients with severe acute respiratory infection may be recommended by health authorities31. Any suspected case should be tested for SARS-CoV-2 using available molecular tests, such as quantitative reverse transcription polymerase chain reaction (qRT-PCR). Lower-respiratory-tract specimens likely have a higher diagnostic value compared with upper-respiratory-tract specimens for detecting SARS-CoV-2. The WHO recommends that, if possible, lower-respiratory-tract specimens, such as sputum, endotracheal aspirate or bronchoalveolar lavage, be collected for SARS-CoV-2 testing32. If patients do not have signs or symptoms of lower-respiratory-tract disease or specimen collection for lower-respiratory-tract disease is clinically indicated but collection is not possible, upper-respiratory-tract specimens of combined nasopharyngeal and oropharyngeal swabs should be collected. If initial testing is negative in a patient who is strongly suspected of having COVID-19, the patient should be resampled, with a sampling time interval of at least 1 day, and specimens collected from multiple respiratory-tract sites (nose, sputum, endotracheal aspirate). Additional specimens, such as blood, urine and stool, may be collected to monitor the presence of virus and the shedding of virus from different body compartments. When qRT-PCR analysis is negative for two consecutive tests, COVID-19 can be ruled out. The WHO has provided guidance on the rational use of PPE for COVID-1933. When conducting aerosol-generating procedures (e.g. tracheal intubation, non-invasive ventilation, cardiopulmonary resuscitation, manual ventilation before intubation), healthcare workers are advised to use respirators (e.g. fit-tested N95, FFP2 or equivalent standard) with their PPE33, 34. The Centers for Disease Control and Prevention (CDC) additionally considers procedures that are likely to induce coughing (e.g. sputum induction, collection of nasopharyngeal swabs and suctioning) as aerosol-generating procedures and CDC guidance includes the option of using a powered air-purifying respirator34, 35. Chest imaging, especially CT scan, is essential for evaluation of the clinical condition of a pregnant woman with COVID-1936-38. Fetal growth restriction (FGR), microcephaly and intellectual disability are the most common adverse effects from high-dose (> 610 mGy) radiation exposure39, 40. According to the American College of Radiology and American College of Obstetricians and Gynecologists, when a pregnant woman undergoes a chest the radiation to the is which is the radiation to the is from a chest CT or CT pulmonary Chest CT has high for diagnosis of In a pregnant woman with suspected COVID-19, a chest CT may be considered as a for the of COVID-19 in should be and a radiation the of the in a CT on patients, and the need for of the CT unit after a COVID-19 a chest is an to a CT A CT pulmonary is in to a on clinical suspicion of pulmonary and should not be during pregnancy. the COVID-19 it has been that ultrasound of the of a pregnant woman with suspected COVID-19 be at the same time as the scan, in order to the of radiation as well as the clinical of these patients. This of also be considered when chest and CT are not However, management should be determined by the clinical and severity of the disease, and not be based merely on diagnostic A guide on to ultrasound in pregnant women with suspected COVID-19 was published In the ultrasound can be using any of and any of and guidance regarding of ultrasound and in the of COVID-19 has been provided in the on of and and in of On are the of the When the but is not it different and of When the of the is ultrasound a in which are as an and A and these can be found in the the ultrasound with the patient in a the can the from the to the the and areas of the The should the pulmonary from to areas of the and can be in order to a the patient in a or the of the should be from to areas or to the to of pregnant patients who have COVID-19 is of in order to the of for patients and healthcare workers up a the and is for and (Appendix for symptoms (e.g. and on contact and should be When is about a potential COVID-19 to symptoms a should be on the patient and should be from other patients, in an COVID-19 workers should appropriate PPE for the management of pregnant women with to 3. and confirmed cases of COVID-19 should be by with and cases should be in and confirmed cases should be in a when COVID-19 can help spread by patients with should up a and a neonatal the and neonatal should have When it is not to up ventilation for it is to with the it is appropriate to their should PPE N95, FFP2 or and and when care for confirmed cases of However, in areas with widespread local transmission of the disease, health may be to such of care to or confirmed COVID-19 women with a mild clinical may not require admission, and can be provided that is and that of the condition can be If are not patients should be in or COVID-19 has been of confirmed cases, the should PPE and and their patient a of 2 or from any without When an has confirmed COVID-19, is of for of not yet in COVID-19 pregnant patients, a early can be to early of critical is provided in When the condition should not be to pregnancy. for to an in the pulmonary need for and of with respiratory failure should be admitted to the as as care or respiratory is can similar to those of severe COVID-19 (e.g. pulmonary and the changes of pregnancy may management (e.g. changes in respiratory appropriate attention should be to and should be for with signs using and should be to analysis should be chest (when should be should be with and testing and The to treatment and surveillance is the same as for is should be to the of is the first of to be Currently, there is no treatment for COVID-19 patients, a number of are in patients with severe symptoms. regarding and treatment should be in conjunction with local and with the advice on potential or fetal effects of any treatment A of potential including and is provided in In non-pregnant COVID-19 patients, such as or to the for to severe disease, with clinical it is to monitor pregnant patients with these and to be of The of severity of COVID-19 pneumonia is defined by the Society of Society for pneumonia (Appendix pneumonia is with a high and mortality there therefore, a for including with and chest The case should be in a in the with the woman in a or prone if should be provided by a appropriate treatment in with treatment should be when there is suspected or confirmed following with and in patients without should be can in severe disease without In patients with and are to an and a 2 The of care is a and to initial care for This of is provided in The WHO of in the first as a should be to should be to patients with and the of ventilation should be to the condition and following guidance from the and in pregnancy is possible, to and The should be of a higher of and of during pregnancy. indicated delivery should be considered by the on a delivery may ventilation, for prone ventilation if in confirmed COVID-19 patients, other for should be It has been reported that viral pneumonia in pregnant women is with an of and Based on from it was that pregnant women with viral pneumonia an of and having a with and at compared with those without pneumonia A case of pregnant women with SARS-CoV in China, reported that of patients who in the first of five patients who after 24 and two without delivery but their were by Currently, there are limited regarding the impact on the of SARS-CoV-2 infection. is an of but not of therefore, is not is common in COVID-19 patients. have that fever in early pregnancy can the and other However, a study of pregnant women reported that the rate of fever in early pregnancy was the of fetal in was the viable with collected at of in the pregnant women with a reported days in early pregnancy, compared to those without a fever in early pregnancy, the of fetal was not studies have reported no evidence of infection with and there are no on the of when SARS-CoV-2 infection is during the first or early of If advice or to patients with COVID-19 can be When the patient has to be in early and should be healthcare workers these patients should appropriate PPE33, 35. in a is advised for confirmed However, if is not a from which any has been is between patients, to local is especially of admission be for pregnant patients with COVID-19, of the disease or for A of should be for these patients, with for confirmed This should use such as or ultrasound This should not be from the without appropriate by if is advised for these if a patient is in an ward, and care with remains be considered for pregnant women who are as especially in those with severe disease, delivery is The Royal College of Obstetricians and Gynaecologists for pregnant women admitted with COVID-19, and should also be considered in patients on a to However, if the patient a analysis should be regarding the of to concerns regarding its use in conjunction with for fetal at an appropriate to local should be as well as ultrasound of fetal growth and with if In severe COVID-19 cases, the fetal can be the patient is should appropriate PPE when the ultrasound of ultrasound and should be before further women with confirmed SARS-CoV-2 infection who are or from mild should be with ultrasound of fetal growth and with if When the infection is in the first or early of pregnancy, a at of is and these should be after The pregnancy should be to the clinical of the of infection during pregnancy. clinical for should be in with local should be by 14 days or positive two consecutive negative are on to ultrasound are provided in to 3. COVID-19 is not an for there is a need to improve and confirmed cases of COVID-19, delivery should be in a The and of delivery should be mainly on the clinical of the and fetal In the that an infected woman has onset of labor with can be to fetal and is essential in these patients. for care as well as for the of the evidence of presence of the virus in and the of healthcare workers to use PPE during the should be the by delivery can be as a may be for the woman to to a pregnant woman without a diagnosis of COVID-19, but who be a of the virus, regarding the of a as it is if there is an of to any healthcare the delivery without may the of a in the spread of the virus by respiratory should be especially when to its should be in an such as of labor can be considered when the is but there should be a threshold to the delivery when there is fetal in labor in acute failure or fetal should delivery if before fetal PPE is and may the but it is and their should be about which may be of in and can be on the clinical condition of the patient and after with the is considered an aerosol-generating is When an early should be considered for a woman with confirmed the presence of a during to local It is to the asymptomatic a and they However, when the is they in and the cases delivery between 24 and of regarding the use of or for fetal in a can clinical condition and the of the delivery that is for management of the especially when there is a need to improve The use of should be considered to analysis and in with and the use of in women at for delivery and of analysis and should be to the use of in women with and of COVID-19 pregnant women should be as infectious and should be of it is there is a of transmission of SARS-CoV-2. In two with a combined of 10 pregnant women with COVID-19 in the and neonatal tested negative for there was no evidence of transmission in women who developed COVID-19 pneumonia in in the study by et tested negative for SARS-CoV-2 a to a pregnant woman with COVID-19 tested positive for SARS-CoV-2 in the sample after but it was confirmed that qRT-PCR testing of the and was negative for that transmission not have studies the possibility of transmission of SARS-CoV-2 in a combined of by testing for and and in neonatal that SARS-CoV-2 be in was based on the presence of by developed in from following However, for cases, the neonatal respiratory tested negative for SARS-CoV-2 In the study of et the observed 14 of in the with a in strongly suggests that neonatal were from the and not by the neonatal In order to further the possibility of transmission of including blood, and should be collected after using from women with A neonatal can also be collected. If possible, testing for SARS-CoV-2 of the of COVID-19 pregnant women should be In to testing for SARS-CoV-2 by testing be an in order to the of transmission of the for of to COVID-19 women should be neonatal management of and confirmed cases of COVID-19, the should be and the should be to the for by the should be different healthcare workers care of the and the in order to the of is evidence regarding the of infection to the direct In in which is should should be is also evidence regarding the of and the need for If the is or to be the with to in order to there should be a and the should be to the after If the patient is asymptomatic or and can be considered by the in with healthcare or may be if Since the is that the virus may be by respiratory droplets than should their and a before the In case of the should be at least 2 from the and a such as a or may be The need to with COVID-19 from their with the that they are to may early as well as of for in the well as for their should the of these appropriate and when the time of there are no or to should be considered in order to the of the This Interim was of Obstetrics and The Chinese of of Obstetrics and China of and and of of Obstetrics and and of Gynecology of New of of Obstetrics and Royal of Gynecology and Medical of and of Obstetrics and of Obstetrics and The Chinese of of Obstetrics and of Wuhan, China of Obstetrics and The of Medical China of and of This Interim should be as: Interim on coronavirus disease 2019 (COVID-19) during pregnancy and information for healthcare Ultrasound 1 for of coronavirus disease 2019 (COVID-19) in computed quantitative reverse transcription polymerase chain severe acute respiratory syndrome coronavirus contact and 2 of symptoms and contact and on healthcare including to healthcare PPE including and to use on healthcare PPE including fit-tested N95, FFP2 or and and to susceptible healthcare workers from use for management of with computed intensive care severe acute respiratory syndrome coronavirus early with from for of on after and before to of after and of or monitor of changes from previous Interim Guidance1 for treatment of COVID-19 in pregnant Society of Society for severe of The is not responsible for the or of any information by the Any than should be to the for the

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