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Covid-19 in pregnancy.

March 22, 2020

Primary Sources in English. Updated April 6th.

This is not a source for advice on COVID-19. Neither professional nor lay.  For that, in the UK, visit the government website here, or the RCOG here. In the US, CDC advice is here and NIH research updates here.

Nor is this a place to report cases. UK cases should be reported to the UK Obstetric Surveillance System (UKOSS) (click here) via each NHS Trust’s local UKOSS reporter. Early pregnancy cases, including miscarriages & ectopic pregnancies, should also be reported there.  There also is an international registry here, and a US one here.

However, some of the primary sources are confusing, in that hospitals overlap and pre-prints appear before full publication; there must be a risk of double counting.  Many are also difficult to access. Below are links to, & brief notes on, the primary scientific reports in English on Covid-19 in pregnancy and the newborn. They are in, roughly, reverse order. I will update. Click here for running totals. I’ve excluded reports solely in news media; they are collected here.

6 April Update. No new scientific reports today. But obstetricians & midwives will enjoy reading the first newspaper report of a Covid-19 pregnancy and birth in France. Case 10 here. Better written and more detailed than many scientific reports.

5 April update. Study 26 added. The first report of puerperal Covid-19. Not added to running totals.

Study 26. The first case report of puerperal COVID-19

This baby developed COVID-19 symptoms at age 10 days and was admitted to Wuhan Children’s Hospital age 17 days on February 5, 2020.  Click here for the article in Chinese. What follows is based on Google translate. Both parents are reported to have had Covid-19 symptoms from three days before admission, i. e. day 14 after birth. This is therefore not a case of COVID infection in pregnancy or at birth, and therefore excluded from the running totals. However, the mother had puerperal Covid-19 and is, I believe, the first such case reported. The baby recovered and by implication, albeit not stated explicitly, so did the parents. The first author Zeng Lingkong shares a name with the first author of the series of 33 neonatal cases reported in JAMA Paediatrics, Study 8., but this is clearly not one of the three infected babies reported in that paper. Citation: Zeng Lingkong, Tao Xuwei, Yuan Wenhao, et al. The first neonatal coronavirus pneumonia in China [J]. Chinese Journal of Pediatrics, 2020,58 (04): 279-280. DOI: 10.3760 / cma.j.cn112140 -20200212-00081

4 April update Study 25 added belatedly.

Study 25. Report of the WHO-China Joint Mission on Coronavirus Disease 2019, 16-24 February 2020

Click here or who-china-joint-mission-on-covid-19-final-report for full text including annexes. (For Chinese version click here or who-china-joint-mission-on-covid-19-final-report chinese version. Annexe 6, page 32 of English version: “As opposed to Influenza A(H1N1)pdm09, pregnant women do not appear to be at higher risk of severe disease. In an investigation of 147 pregnant women (64 confirmed, 82 suspected and 1 asymptomatic), 8% had severe disease and 1% were critical.” Neither raw numbers, a citation, nor any further details are given. Assuming the percentages are of all 147, this would imply 12 women with severe disease, and one or two who were critical. In view of the high possibility of double counting – cases notified to the WHO team are likely to have also got reported elsewhere – I’ve left these out of the running total. Citation: Report of the WHO-China Joint Mission on Coronavirus Disease 2019 (COVID-19) 16-24 February 2020. Report submitted 28 February 2020

3 April update Studies 23 & 24 added. Study 23 is judged unreliable for reasons given below, and study 24 included no pregnancies. Neither have been included in the running totals.

Study 24. No SARS-COV-2 in vaginas of non-pregnant women with severe Covid-19

Although not a study of pregnancy, this report of ten women with confirmed severe COVID-19 pneumonia in Tongji Zhongfa Hospital, Wuhan, China (click here or ciaa375) is reassuring for vaginal birth. None were positive for SARS-CoV-2 by RT-PCR assay in vaginal fluid. Citation: Lin Qiu, Xia Liu, Meng Xiao, Jing Xie, Wei Cao, Zhengyin Liu, Abraham Morse, Yuhua Xie, Taisheng Li, Lan Zhu. SARS-CoV-2 is not detectable in the vaginal fluid of women with severe COVID-19 infection. Clinical Infectious Diseases, ciaa375,  https://doi.org/10.1093/cid/ciaa375

Study 23. Three cases from Iran

This review (click here, full text here) from researchers in both Tehran and Shiraz, includes a report of the births of three infants from infected mothers, apparently not previously reported. The authors’ source was this Iranian ministry website (click here). All three babies were uninfected and survived, but two of the three mothers developed acute respiratory distress syndrome (ARDS) after delivery and died; presumably related to their Covid-19 infection. Citation: Mojgan Karimi-Zarchia, Hossein Neamatzadeh, Seyed Alireza Dastgheib, Hajar Abbasi, Seyed Reza Mirjalili, Thena Behforouz, Farzad Ferdosian, Reza Bahrami. Vertical Transmission of Coronavirus Disease 19 (COVID-19) from Infected Pregnant Mothers to Neonates: A Review. Fetal & Paed Pathol. https://doi.org/10.1080/15513815.2020.1747120 

Comment by Jim. Although these cases are reported in a scientific journal, the source is a website. The authors do not claim to have treated either the women nor the babies. The women are said to have delivered in Mazandaran and Zanjan provinces. None of the authors give these provinces as their address.  A google translation of the link provided reveals a report of a single case of a woman with COVID-19 who delivered at 36 weeks in Babol. Mother and baby doing well. Again none of the article authors came from Babol. It seems likely that the source of these three cases is the website alone. We have therefore excluded them from our running totals.

2 April update Thank you to Keelin O’Donoghue, Cork, for pointing me to Studies 18 & 19, which I had missed, and to Ganesh Acharya, Editor-in-Chief AOGS, for permission to upload a pre-publication version of Study 20.

Study 22. Case report from Korea

Delivered by Caesarean section at 37 weeks at Daegu Fatimal Hospital, Korea (click here). The baby was not infected. Mother and baby did well. Citation: Dong Hwan Lee, Jihyang Lee, Eunju Kim, Kyeongyoon Woo, Hak Youle Park, Jihyun An.  Emergency cesarean section on severe acute respiratory syndrome coronavirus 2 (SARS- CoV-2) confirmed patient. Korean J Anesthesiol. https://doi.org/10.4097/kja.20116    [Epub ahead of print]

Study 21. Case report from Washington DC

The patient had a normal vaginal delivery at 39 weeks at MedStar Washington Hospital Center (click here). Baby not infected. Both fine. Citation: Iqbal SN Rachael Overcash R, Neggin Mokhtari N,.
Haleema Saeed H, Gold S, Auguste T, Mirza M-U, Ruiz M-E, Chahine JJ, Waga M, Wortmann G. An Uncomplicated Delivery in a Patient with Covid-19 in the United States New Engl J Med April 1, 2020 DOI: 10.1056/NEJMc2007605

Study 20. Case report of twins from Stockholm

Twins born by Caesarean at 36 weeks in Southern General Hospital, Stockholm. Twins, breast milk & maternal vaginal secretions all Covid-19 negative. Pre-publication version here AOGS-20-0296_Proof_hi with permission of the editor, Ganesh Acharya. Link will follow. Citation: Gidlof S, Savchenko J, Brune, T, Josefsson H. COVID-19 in pregnancy with comorbidities: More liberal testing strategy is needed.  Acta Obstetricia et Gynecologica Scandinavica 

Study 19. Case report from Souzhou, China

Woman delivered by Caesarean at 30 weeks in the Affiliated Infectious Hospital of Soochow University, Souzhou, China. Although “no improvement was made on maximal ventilator support for four hours”, later “informed consent was obtained, an emergency cesarean section under combined spinal-epidural anesthesia was performed” and “uneventful perinatal course”.  Baby isolated and not infected. Both survived. Citation: Xiaotong Wang, Zhiqiang Zhou, Jianping Zhang, Fengfeng Zhu, Yongyan Tang, Xinghua Shen. A case of 2019 Novel Coronavirus in a pregnant woman with preterm delivery. Clinical Infectious Diseases, ciaa200, https://doi.org/10.1093/cid/ciaa200

Study 18. Case report from Honduras, Central America

The woman went into preterm labour and delivered vaginally at 32 weeks. Baby not infected. Both doing well at time of report. Citation. Zambrano LI, Fuentes-Barahona IC, Bejarano-Torres DA, Bustillo C, Gonzales G, Vallecillo-Chinchilla G, Sanchez-Martínez FE,  Valle-Reconco JA, Sierra M, Bonilla-Aldana DK, Cardona-Ospina JA, Rodríguez-Morales AJ. A pregnant woman with COVID-19 in Central America. Travel Medicine and Infectious Disease. Online 25 March 2020. https://doi.org/10.1016/j.tmaid.2020.101639 

1 April update

Study 6a added (details below).

30th March update

Study 17. Five from Maternal & Child Hospital of Hubei Province, Tongji Medical College

Two Caesarean and three vaginal births delivered in the Maternal and Child Hospital of Hubei Province, Tongji Medical College (click here). Or siyu chen.  All mothers recovered. All babies well. According to Wikipaedia the MCH of HP is the 10th clinical college/hospital associated with Tongji Medical College. It is distinct from both Union hospital and Tongji hospital. These five births are therefore additional to those in the various Union Hospital reports, and to those in study 15. Citation: Chen S, Liao E, Shao Y. Clinical analysis of pregnant women with 2019 novel coronavirus pneumonia. J Med Virol. 2020 Mar 28. doi: 10.1002/jmv.25789. [Epub ahead of print] 

Study 16. Three non-cases from Shenzhen 2nd People’s Hospital.

Shenzen, a city of 13 million had had 420 confirmed cases of Covid-19, the second highest number outside Hubei, up to March 11th. Despite an annual birth rate in the city of 188,000, the 2nd People’s Hospital saw no COVID-19 infected pregnant women. Instead they report three suspected cases who, after barrier nursing, and in one case surgery for an ectopic pregnancy, were later confirmed negative. Citation: Yu Chen, Zhe Li, Yuan-Yuan Zhang, Wei-Hua Zhao, Zhi-Ying Yu. Maternal health care management during the outbreak of coronavirus disease 2019 (COVID-19) J Med Virol. 2020 Mar 26. doi: 10.1002/jmv.25787. [Epub ahead of print]

29th March – 3rd update

Study 15. Seven cases from Tongji in Lancet Respiratory Med

These seven cases (click here) delivered at Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology (Wuhan, China) between Jan 1 and Feb 8, 2020. All mothers had mild Covid-19 disease and all were delivered around term by Caesarean section. One baby (Patient 1) tested positive for Covid-19 by throat PCR at 36 hours and was transferred to Wuhan Children’s hospital. His mother’s age, gravidity, parity, lack of direct contact with Hunan seafood market and history of hypothyroidism all suggest this is the same mother/infant dyad as in report 11. Note however the reported birthweights differ 3250g v 3205g. No babies had any clinical symptoms and all (including the transferred one) were discharged home well. Wikipedia lists ten different hospitals/clinical colleges affiliated with Tongji Medical College in Wuhan. The 1st clinical college is called Wuhan Union Hospital. The 2nd clinical college is called Wuhan Tongji Hospital. This series is therefore unlikely to overlap with the various case series from Union Hospital Tongji. Citation: Nan Yu, Wei Li, Qingling Kang, Zhi Xiong, Shaoshuai Wang, Xingguang Lin, Yanyan Liu, Juan Xiao, Haiyi Liu, Dongrui Deng, Suhua Chen, Wanjiang Zeng, Ling Feng, Jianli Wu. Clinical features and obstetric and neonatal outcomes of pregnant patients with COVID-19 in Wuhan, China: a retrospective, single-centre, descriptive study. Lancet Infect Dis 2020 Published Online March 24, 2020 https://doi.org/10.1016/S1473-3099(20)30176-6

29th March – 2nd update.

Study 14. Seven pregnant women from New York Presbyterian

AJOG MFM Preprint (click here) or COVID_Early_Lessons_032620 NY presbyterian. via @neel_shah. The first reported cases outside China. Citation; Breslin N, Baptiste C, Miller R, Fuchs K, Goffman D, Gyamfi-Bannerman C, D’Alton M. COVID-19 in pregnancy: early lessons. Am J Obstet Gynecol. Available online 27 March 2020. https://doi.org/10.1016/j.ajogmf.2020.100111

29th March update. Four more primary reports including ten more cases. All previously unreported.

Study 13. Cord blood serology from six babies in Zhongnan Hospital, Wuhan

Six cases reported in JAMA (click here). All births by Caesarean. All mothers mild disease. All babies asymptomatic. Since they were born in a different hospital these are probably additional to the other 33 Wuhan neonates reported in JAMA.  Citation: Hui Zeng, Chen Xu, Junli Fan, Yueting Tang, Qiaoling Deng, Wei Zhang, Xinghua Long. Antibodies in Infants Born to Mothers With COVID-19 Pneumonia. JAMA. Published online March 26, 2020. doi:10.1001/jama.2020.4861

Study 12. Case report from Renmin Hospital Wuhan

Case report in JAMA of baby, born at Renmin Hospital, Wuhan, by Caesarean, 23 days after mother developed Covid-19, had IgM antibodies detected in cord blood (click here). This is additional to the two Remnin cases below, because the clinical details differ substantially. Citation: Lan Dong, Jinhua Tian, Songming He, Chuchao Zhu, Jian Wang, Chen Liu, Jing Yang. Possible Vertical Transmission of SARS-CoV-2 From an Infected Mother to Her Newborn. JAMA. Published online March 26, 2020. doi:10.1001/jama.2020.4621

Study 11. Caesarean birth & neonatal infection, Wuhan

Case report (click here) of a baby born by Caesarean to an infected mother at Wuhan Tongji Hospital.  The baby was separated from the mother at birth but became infected (pharyngeal PCR at 36 hours). Both mother and baby recovered. I believe this case report is additional to the 33 Wuhan neonatal cases reported in JAMA, because the details (e.g. birth weight) do not align. This is therefore the fourth infected baby born by Caesarean. Citation: Shaoshuai Wang, Lili Guo, Ling Chen, Weiyong Liu, Yong Cao, Jingyi Zhang, Ling Feng A Case Report of Neonatal 2019 Coronavirus Disease in China. Clinical Infectious Diseases, ciaa225, https://doi.org/10.1093/cid/ciaa225

Study 10. Two cases from Renmin Hospital, Wuhan

Two pregnant doctors with Covid-19 both delivered by Caesarean at term (click here). Also remnin two cases.  Babies separated and not infected. Probably additional to the 33 JAMA Wuhan neonates because neither neonate was transferred to Wuhan Children’s Hospital. Citation: Cuifang Fan, Di Lei, Congcong Fang, Chunyan Li, Ming Wang, Yuling Liu, Yan Bao, Yanmei Sun, Jinfa Huang, Yuping Guo, Ying Yu, Suqing Wang Perinatal Transmission of COVID-19 Associated SARS-CoV-2: Should We Worry?  Clinical Infectious Diseases, ciaa226, https://doi.org/10.1093/cid/ciaa226

28 March 2020 update. Three more more primary scientific reports.

Study 9. A Caesarean birth from Zhejiang

This case report is in Chinese but has an English abstract. Click here. It’s from the First Affiliated Hospital, College of Medicine, Zhejiang University School of Medicine, Hangzhou. There appears to be no overlap of the authors with the Zhejiang Caesarean below, so this may be a new case. The Caesarean is reported as being “successful” which presumably means both mother and baby survived.  Citation: Kang X, Zhang R, He H, Yao Y, Zheng Y, Wen X, Zhu S. Anesthesia management in cesarean section for a patient with coronavirus disease 2019. Zhejiang Da Xue Xue Bao Yi Xue Ban. 2020 May 25;49(1):0. Chinese. PMID: 32207592

Study 8. The 33 neonatal cases from Wuhan

A series of 33 neonates born to mothers who had Covid-19. All from Wuhan Children’s Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China. Reported in JAMA here. It seems possible that some or all of these infants are also included in the other Union Hospital Tongji series below.  Of the 26 neonates delivered by Caesarean three became infected. One born at 30 weeks and 2 days developed RDS, pneumonia and suspected sepsis, and required non-invasive ventilation. The authors speculate that some of his problems were related to prematurity rather than COVID-19. The other two neonates were healthy. All three survived. By inference, although this is not specifically stated in the paper, none of the seven infant born vaginally became infected.  Citation: Lingkong Zeng, Shiwen Xia, Wenhao Yuan, Kai Yan, Feifan Xiao, Jianbo Shao, Wenhao Zhou, Neonatal Early-Onset Infection With SARS-CoV-2 in 33 Neonates Born to Mothers With COVID-19 in Wuhan, China. JAMA Pediatr. Published online March 26, 2020. doi:10.1001/jamapediatrics.2020.0878

Study 7. The Quingdao case

This appears to be the first pregnancy case from  that city. Click here. The mother developed Covid-19 at 30 weeks but recovered and was discharged. At the time the report was written the pregnancy was ongoing. Citation: Rong Wen, Yue Sun, Quan-Sheng Xing A patient with SARS-CoV-2 infection during pregnancy in Qingdao, China Journal of Microbiology, Immunology and Infection Available online 10 March 2020 https://doi.org/10.1016/j.jmii.2020.03.004

22 March 2020 estimate. Assuming all the Union Hospital Tongji cases overlap, i.e. that Tongji has reported only 15 in total, there have been 38 published cases (39 babies) of Covid-19 infection in pregnancy. There have been no reports in the scientific literature of any maternal deaths, and all neonates have survived and not been infected. Four neonates remain undelivered.

Note 22 March 2020.  David A Schwarz (click here) in a review in Arch Pathol (preprint available March 21st) also makes the total 38 published cases.  However he includes a series published only in Chinese (his reference 17) Zhang I, Jiang Y, Wei M, Cheng BH, Zhou XC, Li J, et al. 湖北地区新型冠状病毒肺炎流行期间孕妇的 384 妊娠结局分析 [Analysis of the Pregnancy Outcomes in Pregnant Women With COVID-19 in Hubei Province]. Zhonghua Fu Chan Ke Za Zhi . 2020;55(0), E009. Available from: http://rs.yiigle.com/yufabiao/1184338.htm (accessed and translated 12 March 2020).  He reports this as including 16 cases.  For the moment I’ve not included this Hubei series, (but see Study 6a added 1 April).

Study 6a. 16 cases from Remnin

The cases included by David Schwarz on March 21 (see note above). English abstract (click here). Full text in Chinese here. Google translate used. The authors come from Remnin Hospital, but the paper reports that all 16 women were delivered by Caesarean at the Eastern Hospital of Wuhan University People’s Hospital.  Therefore assume no duplicates. Citation: Zhang Lu, Jiang Yan, Wei Min, et al. Analysis of pregnancy outcomes of pregnant women during the epidemic of new coronavirus pneumonia in Hubei [J / OL]. Chinese Journal of Obstetrics and Gynecology, 2020,55 (2020-03-08). http://rs.yiigle.com/yufabiao/1184338.htm. DOI: 10.3760 / cma.j.cn112141-20200218-00111. 

Study 6. The 15 Union hospital Tongji cases

A series of 15 pregnant women, of whom 11 had delivered and four remained undelivered from Union Hospital, Tongji Medical College, click here. These may include the four from the same hospital below and also possibly the 9 cases from the same hospital in Translational Paediatrics. Citation: Dehan Liu, Lin Li, Xin Wu, Dandan Zheng, Jiazheng Wang, Lian Yang and Chuansheng Zheng. Pregnancy and Perinatal Outcomes of Women With Coronavirus Disease (COVID-19) Pneumonia: A Preliminary Analysis American Journal of Roentgenology: 1-6. 10.2214/AJR.20.23072

Study 5. The 9 Union Hospital Tongji cases

Published in Translational Paediatrics (click here). Nine mothers, ten neonates. Citation: Huaping Zhu, Lin Wang, Chengzhi Fang, Sicong Peng, Lianhong Zhang, Guiping Chang, Shiwen Xia, Wenhao Zhou. Clinical analysis of 10 neonates born to mothers with 2019-nCoV pneumonia. Translational Pediatrics Vol 9, No 1 (February 2020)  

Study 4. The Zeijang case

From the First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China (click here) Caesarean for unclear indication. Baby not infected. Citation: Yang Li, Ruihong Zhao, Shufa Zheng, Xu Chen, Jinxi Wang, Xiaoli Sheng, Jianying Zhou, Hongliu Cai, Qiang Fang, Fei Yu, Jian Fan, Kaijin Xu, Yu Chen and Jifang Sheng Lack of Vertical Transmission of Severe Acute Respiratory Syndrome Coronavirus 2, China. Emerging Infectious Diseases. 2020 Apr [date cited]. https://doi.org/10.3201/eid2606.200287 DOI: 10.3201/eid2606.200287

Study 3. The Sun Yat Sen series

These 13 cases were reported from the First Affiliated Hospital of Sun Yat-sen University, Guangzhou 510080, Province. Guangdong, P.R. China. (click here). Also pre-publication text 10.1016@j.jinf.2020.02.028). They included 3 patients from Zhejiang, 3 from other cities of Hubei and 1 each from Fujian, Shanxi, Beijing, Guangdong, Jiangxi, Heilongjiang and Anhui.   No infected neonates but one mother seriously ill on ECMO.  Citation: Yangli Liu, Haihong Chen, Kejing Tang, Yubiao Guo. Clinical manifestations and outcome of SARS-CoV-2 infection during pregnancy J Infect. https://doi.org/10.1016/j.jinf.2020.02.028

Study 2. The first Union Hospital Tongji series

From Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan. The original abstract here, described three cases and linked to an original paper in Chinese. These may overlap with four cases later published in Frontiers click here. There is also a pre-print of three cases from Tongji, (Click here or preprints202002.0373.v1) which includes some authors from the Liverpool School of Tropical Medicine & Hygiene. Again these may overlap, or even be the same cases.

Study 2a. Citations: Chen S, Huang B, Luo DJ, Li X, Yang F, Zhao Y, Nie X, Huang BX. Pregnant women with new coronavirus infection: a clinical characteristics and placental pathological analysis of three cases. Zhonghua Bing Li Xue Za Zhi. 2020 Mar 1;49(0):E005. doi: 10.3760/cma.j.cn112151-20200225-00138.

Study 2b. Liu, W.; Wang, Q.; Zhang, Q.; Chen, L.; Chen, J.; Zhang, B.; Lu, Y.; Wang, S.; Xia, L.; Huang, L.; Wang, K.; Liang, L.; Zhang, Y.; Turtle, L.; Lissauer, D.; Lan, K.; Feng, L.; Yu, H.; Liu, Y.; Sun, Z. Coronavirus Disease 2019 (COVID-19) During Pregnancy: A Case Series. Preprints 2020, 2020020373

Study 2c. Yan Chen, Hua Peng, Lin Wang, Yin Zhao, Lingkong Zeng, Hui Gao and Yalan Liu.      Infants Born to Mothers With a New Coronavirus (COVID-19)  Front. Pediatr., 16 March 2020 | https://doi.org/10.3389/fped.2020.00104

Study 1. The original Lancet nine

All from Zhongnan Hospital of Wuhan University, Wuhan, click hereCitation: Huijun Chen, Juanjuan Guo, Chen Wang, Fan Luo, Xuechen Yu, Wei Zhang, Jiafu Li, Dongchi Zhao, Dan Xu, Qing Gong, Jing Liao, Huixia Yang, Wei Hou, Yuanzhen Zhang. Clinical characteristics and intrauterine vertical transmission potential of COVID-19 infection in nine pregnant women: a retrospective review of medical records. Lancet. Volume 395, Issue 10226, 7–13 March 2020, Pages 809-815.

Jim Thornton

 

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