Original Research ajog.

org

OBSTETRICS
Coronavirus disease 2019 in pregnant women: a report
based on 116 cases
Jie Yan, MD, PhD1; Juanjuan Guo, MD1; Cuifang Fan, MD1; Juan Juan, PhD1; Xuechen Yu, MD; Jiafu Li, MD; Ling Feng, MD;
Chunyan Li, MD; Huijun Chen, MD; Yuan Qiao, MD; Di Lei, MD; Chen Wang, MD, PhD; Guoping Xiong, MD; Fengyi Xiao,
MD; Wencong He, MD; Qiumei Pang, MD; Xiaoling Hu, MD; Suqing Wang, MD; Dunjin Chen, MD; Yuanzhen Zhang, MD;
Liona C. Poon, MD; Huixia Yang, MD

BACKGROUND: The coronavirus disease 2019, caused by spontaneous abortion. Of 99 patients, 21 (21.2%) who delivered had
severe acute respiratory syndrome coronavirus 2, is a global public pre- term birth, including 6 with preterm premature rupture of
health emergency. Data on the effect of coronavirus disease 2019 in membranes. The rate of spontaneous preterm birth before 37 weeks’
pregnancy are limited to small case series. gestation was 6.1% (6/
OBJECTIVE: To evaluate the clinical characteristics and outcomes in 99). One case of severe neonatal asphyxia resulted in neonatal
pregnancy and the vertical transmission potential of severe acute death. Furthermore, 86 of the 100 neonates tested for severe acute
respi- ratory syndrome coronavirus 2 infection. respiratory syndrome coronavirus 2 had negative results; of these, paired
STUDY DESIGN: Clinical records were retrospectively reviewed for amniotic fluid and cord blood samples from 10 neonates used to test
116 pregnant women with coronavirus disease 2019 pneumonia from 25 for severe acute respiratory syndrome coronavirus 2 had negative
hospitals in China between January 20, 2020, and March 24, 2020. results. CONCLUSION: Severe acute respiratory syndrome
Evidence of vertical transmission was assessed by testing for severe coronavirus 2 infection during pregnancy is not associated with an
acute respiratory syndrome coronavirus 2 in amniotic fluid, cord increased risk of spontaneous abortion and spontaneous preterm birth.
blood, and neonatal pharyngeal swab samples. There is no evi- dence of vertical transmission of severe acute
RESULTS: The median gestational age on admission was 38þ0 respiratory syndrome coronavirus 2 infection when the infection
(inter- manifests during the third trimester of pregnancy.
quartile range, 36þ0e39þ1) weeks. The most common symptoms were
fever (50.9%, 59/116) and cough (28.4%, 33/116); 23.3% (27/116) Key words: ascending infection, coronavirus, coronavirus disease
pa- tients presented without symptoms. Abnormal radiologic findings 2019, COVID-19, pandemic, pneumonia, pregnancy, pregnancy out-
were found in 96.3% (104/108) of cases. Of the 116 cases, there were
comes, pregnant women, preterm birth, PTB, SARS-CoV-2, severe acute
8 cases (6.9%) of severe pneumonia but no maternal deaths. One of 8
respiratory syndrome coronavirus 2, spontaneous abortion, spontaneous
patients who presented in the first trimester and early second trimester
preterm birth, spontaneous PTB, vertical transmission
had a missed

T he coronavirus disease 2019

(COVID-19), caused by severe
acute respiratory syndrome coronavirus
respiratory
(SARS-CoV)
syndrome
and
coronavirus severe pneumonia, because of the
Middle East physiological changes in the immune
respiratory syndrome coronavirus
2 (SARS-CoV-2), is a global public (MERS-CoV), have caused more than
health emergency. Since the first case of 10,000 cumulative cases in the past 2
COVID-19 pneumonia was reported in decades, with mortality rates of 10% for
Wuhan, Hubei Province, China, in 5e9
SARS-CoV and 37% for MERS-CoV.
December 2019, the infection has spread
Severe acute respiratory syndrome
rapidly to the rest of China and
1e3 coronavirus 2 belongs to the same b-
beyond. Coronaviruses are
coronavirus subgroup, and it has
enveloped, nonsegmented, positive-
genome similarity of about 80% and
sense RNA vi- ruses belonging to the
50% with SARS-CoV and MERS-CoV,
family Coronavir- idae, order 10
4 respectively. The latest report from
Nidovirales. The epidemics caused by
the World Health Organization (WHO)
2 b-coronaviruses, severe acute on March 3, 2020, estimated the global
mortality rate of COVID-19 to be
11
Cite this article as: Yan J, Guo J, Fan C, et al. Coro-
3.4%, although recent reports that
navirus disease 2019 in pregnant women: a report have used appropriate adjustment for
based on 116 cases. Am J Obstet Gynecol the case ascertainment rate and time
2020;XX:x.exex.ex. lag between symptoms onset and
0002-9378/$36.00
death suggest the mortality rate to be
12
ª 2020 Elsevier Inc. All rights reserved. lower at 1.4%.
https://doi.org/10.1016/j.ajog.2020.04.014
Pregnant women are especially sus-
ceptible to respiratory pathogens and
1.e1 American Journal of Obstetrics & Gynecology MONTH 2020 MONTH 2020 American Journal of Obstetrics & Gynecology 1.e1
and cardiopulmonary systems (eg,
diaphragm elevation, increased oxy-
gen consumption, and edema of the
respiratory tract mucosa), which can
render them intolerant to hypoxia.
The 1918 influenza pandemic caused
a mortality rate of 2.6% in the overall
population, but 37% among pregnant
13
women. In 2009, pregnant women
were reported to be at an increased
risk for complications from the
pandemic H1N1 2009 influenza virus
infection, with a higher estimated
rate of hospital admission than in the
14
general population. In 2003, it was
reported that approximately 50% of
pregnant women who received a
diagnosis for SARS-CoV were
admitted to the intensive care unit
(ICU), around 33% of pregnant
women with SARS-CoV required
mechanical ventilation, and the
mortality rate was as high as 25% for
15
these women.

1.e2 American Journal of Obstetrics & Gynecology MONTH 2020 MONTH 2020 American Journal of Obstetrics & Gynecology 1.e2
Original
ajog.org Research OBSTETRICS OBSTETRICS Original Research
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and radiologic findings, treatment mea-

AJOG at a Glance
sures, and outcome data were extracted
Why was this study conducted? from electronic medical records by a
To report maternal and neonatal outcome of coronavirus disease 2019 team of experienced clinicians and
(COVID-19) in pregnancy of 116 patients. curated with customized data collection
form. All laboratory testing and radio-
Key findings logic assessments, including chest CT,
There were 8 cases (6.9%, 8/116) of severe pneumonia but no maternal were performed according to the
deaths. clinical care needs of the patient.
One of 8 patients (12.5%, 1/8) who presented in the first trimester and early Laboratory assessments consisted of
second trimester had a missed spontaneous abortion. complete blood cell count, liver and
The rate of spontaneous preterm birth before 37 weeks’ gestation was 6.1% renal function, electrolytes, C-reactive
(6/ protein, and coagulation testing. We
99). determined the presence of a
Eighty-six of 100 neonates tested for severe acute respiratory syndrome radiologic abnormality based on the
coronavirus (SARS-CoV-2), had negative results. documentation or description in
medical charts. The date of onset of
What does this add to what is known? disease was defined as the day when the
SARS-CoV-2 infection during pregnancy is not associated with an increased symptoms were noticed. The intervals
risk of spontaneous abortion and spontaneous preterm birth. from onset of disease to hos- pital
There is no evidence of vertical transmission of SARS-CoV-2 infection admission and delivery were recorded.
when the infection manifests during the third trimester of pregnancy. Data on pregnancy and neonatal
outcome, including gestational
age at delivery, mode of delivery,
indi-
To date, data on the effect of COVID- collection, data analysis, or writing of
cation for cesarean delivery, complica-
19 in pregnancy are limited to small the report.
16e20 tions, neonatal birthweight, Apgar
case series. This multicenter study scores, and neonatal intensive care unit
aimed to evaluate the clinical character- Data collection (NICU) admission, were collected. The
istics and outcomes of 116 pregnant This was an expanded series from 4 date of data cutoff for outcomes was
women with COVID-19 pneumonia and 16,18e20
pre- vious small case series. March 24, 2020. The degree of severity
the vertical transmission potential of tained
We ob-the medical records and of
SARS-CoV-2 infection. compiled clinical and outcome data for COVID-19 pneumonia (severe vs non-
consecutive
pregnant women with COVID-19 pneu- severe) was defined by the Infectious
Materials and Methods monia from 25 hospitals (Supplemental Diseases Society of America/American
Thoracic Society guidelines for
Study design and participants Material) within and outside of Hubei community-acquired pneumonia.
25

This study was reviewed and approved Province between January 20, 2020, and Two study investigators (J.Y. and
by the Medical Ethics Committee of March 24, 2020. COVID-19 was diag- J.J.) independently reviewed the data
Zhongnan Hospital of Wuhan Univer- nosed on the basis of the New Corona- collec- tion forms to verify data
sity (reference 2020004) and Renmin virus Pneumonia Prevention and Complete epidemiologic history,
Hospital of Wuhan University (refer- Control Program published by the clinical symptoms or signs, laboratory
ence WDRY2020-K015, WDRY2020- National Health Commission of
K016). For the collection of clinical China.21e24 A laboratory-confirmed
data, verbal consent from pregnant case of COVID-19 was defined as a
women was obtained, and written positive result by quan- titative reverse
informed consent was waived consid- transcriptase polymerase chain reaction
ering the urgent need to collect data. (qRT-PCR) assay of maternal
Written informed consent was obtained pharyngeal swab specimens. At the
from pregnant women who agreed to peak of the COVID-19 outbreak within
the testing of biological samples and Hubei Province, China, cases with
neonatal pharyngeal swab samples. relevant symptoms, marked epidemio-
Data were analyzed and interpreted by logic history, and typical chest
the authors. All the authors reviewed computed tomography (CT) findings
the manuscript and vouched for the were clinically diagnosed as COVID-19
accuracy and completeness of the data pneumonia, whereas the viral nucleic
and for the adherence of the study to acid test was reported to have a false-
the protocol. The funding agencies did negative rate of
not participate in the study design, 30%.22
data
 Original Research
ajog.org
disagreement between them was
OBSTETRICS OBSTETRICS Original Research
ajog.org
resolved by consultation with a third
investigator (H.Y.).

Sample collection
Amniotic fluid samples from patients
with COVID-19 pneumonia were ob-
tained through direct needle syringe
aspiration at the time of cesarean de-
livery. Cord blood and neonatal
pharyngeal swab samples were
collected immediately after delivery in
the oper- ating or delivery room.
Evidence of ver- tical transmission was
evaluated by testing for the presence of
SARS-CoV-2 in these clinical samples.
In addition, vaginal secretion samples
were collected from the lower third of
the vagina on admission, and breast
milk samples were
collected at first lactation in Zhongnan cough in 28.4% (33/116), and fatigue 12.9% (15/116) of cases. In 23.3% (27/
Hospital of Wuhan University and in 116) of cases, there were no signs or
Renmin Hospital of Wuhan University. symptoms of the disease, 77.8% (21/27)
All samples were processed at the State of which were clinically diagnosed with
Key Laboratory of Virology, Institute of COVID-19 pneumonia. All these 21
Medical Virology, School of Basic Med- cases underwent investigations because
ical Sciences, Wuhan University, and of marked epidemiologic history.
Laboratory Medicine Center of Renmin Of note, there were 9 patients (7.8%,
Hospital of Wuhan University for 9/116) with gestational diabetes and 5
further testing. Sample collection, pro- (4.3%, 5/116) with hypertensive disor-
cessing, and laboratory testing complied ders, including 4 (3.4%, 4/116) with
26
with WHO guidance. All samples, as preeclampsia, and these pregnancy
described above, were tested for SARS- complications were unrelated to
CoV-2 using qRT-PCR with the Chi- COVID-19 pneumonia. There were 8
nese Center for Disease Control and patients (6.9%, 8/116) with severe
Preventionerecommended kit. pneumonia, all required ICU admission,
1 of whom (0.9%, 1/116) required plas-
Study outcomes mapheresis, 6 (5.2%, 6/116) received
The primary endpoint was admission to noninvasive ventilation, 2 (1.7%, 2/116)
ICU, use of mechanical ventilation, or received invasive mechanical ventilation,
death. Secondary endpoints were the and 1 (0.9%, 1/116) received extracor-
rates of spontaneous abortion, preterm poreal membrane oxygenation. Clinical
delivery, cesarean delivery, and neonatal details of severe pneumonia cases are
COVID-19. presented in the Supplemental Table. A
total of 76 (65.5%, 76/116) cases had
Statistical analysis been discharged. There were no cases of
Continuous variables were expressed as maternal death.
means (standard deviations [SDs]) or On admission, lymphocytopenia was
medians (interquartile ranges [IQRs]) present in 44.0% (51/116) of the patients
or simple ranges, as appropriate. and leukopenia was present in 24.1%
Categori- cal variables were (28/116) of patients, according to
summarized as numbers and pregnancy-specific reference ranges.
27

percentages. The results were Elevated levels of C-reactive protein

presented in the total study popu- were found in 44% of the patients. Pa-
lation and according to the methods of tients with severe disease had more
diagnosis for COVID-19 pneumonia. prominent laboratory abnormalities
The statistical software SPSS for Win- (including lymphocytopenia and leuko-
dows version 23 (SPSS, IL) was used penia) than those with nonsevere dis-
for data analyses. ease. In cases that underwent chest CT
scans at the time of admission, 96.3%
Results (104/108) revealed abnormal results. Of
Clinical characteristics note, all cases of clinically diagnosed
The characteristics and outcomes of the COVID-19 pneumonia exhibited
study population of 116 cases, including abnormal chest CT findings (Table 2).
65 cases of laboratory-confirmed and 51
cases of clinically diagnosed COVID-19 Pregnancy outcomes
pneumonia, are presented in Table 1. Of the 116 pregnant women with
The mean age was 30.8 (range 24e41) COVID-19 pneumonia, 8 cases pre-
years, and median gestational age on sented before 24 weeks’ gestation. One
þ0 þ0 þ1
admission was 38 (IQR 36 e39 ) case (12.5%, 1/8) was complicated with a
weeks. In 59.5% (69/116) of cases, missed spontaneous abortion at 5
þ2

women reported a history of relevant weeks at presentation with fever and fa-
environmental exposure, and 32.8% tigue. In the remaining 7 ongoing cases,
(38/ 4 had reached 20 weeks, and
116) had contact with infected persons. morphology scan revealed normal anat-
The most common symptoms at pre- omy and fetal growth. Ten cases
sentation were fever in 50.9% (59/116),
 þ6
presented between 24 and 33 weeks, neonate experienced severe
of which 7 cases are ongoing, 1 pneumonia and
delivered at term, and 2 cases (20%,
2/10) had iat- rogenic preterm delivery.
þ1
One had a ce- sarean delivery at 28
weeks on the same day of admission
for severe pneu- monia; 1 had a
þ6
cesarean delivery at 31 weeks on the
same day of admission for twin
pregnancy. Of the 22 cases pre-
þ6
sented between 34 and 36 weeks, 19
delivered preterm, 2 delivered at term,
and 1 case remained undelivered. There
were 27.3% (6/22) women who had
preterm premature rupture of mem-
branes (PPROM), 2 cases (33.3%, 2/6)
resulted in vaginal delivery; 4 cases
(66.7%, 4/6) required cesarean
delivery, with 3 cases indicated for
symptomatic COVID-19 pneumonia
and 1 because of history of previous
cesarean delivery. There are 16
ongoing pregnancies, with
1 patient with gestational diabetes mel-
litus and the other 15 patients with no
fetal or maternal complications reported
as of March 24, 2020.
A total of 99 pregnant women,
including 1 with twin pregnancy,
delivered their babies during hospitali-
zation, of whom 85.9% (85/99) under-
went cesarean delivery and 14.1% (14/
99) had a vaginal delivery (Table 3).
Cesarean delivery was indicated for
COVID-19 pneumonia in 38.8% (33/
85), previous cesarean delivery in
18.8% (16/85), fetal distress in 10.6%
(9/85), and failure to progress in 5.9%
(5/85) (Table 3). The rates of preterm
delivery before 34 weeks and 37
weeks were
2.0% (2/99) and 21.2% (21/99),
respectively (Table 3). Among the 21
preterm deliveries, 28.6% (6/21) had
PPROM, 2 of which resulted in vaginal
deliveries. There were no cases with
spontaneous onset of labor. The rate of
spontaneous preterm birth before 37
weeks was therefore 6.1% (6/99). No
cases of spontaneous preterm delivery
before 34 weeks were reported.
There were no cases of fetal deaths.
Among 100 neonates, there was 1 case
of severe neonatal asphyxia. There were
47.0% (47/100) neonates transferred to
the NICU for further treatment
(Table 3). There was 1 case of
neonatal death. The mother of this
TABLE 1
Demographics, baseline characteristics, and clinical outcomes of coronavirus disease 2019 infection in pregnant
women
Clinical characteristics All patients (n¼116) Laboratory confirmed (n¼65) Clinically diagnosed (n¼51)
Age, y
Mean SD 30.8 3.8 30.3 3.7 31.3 4.0
Range 24.0e41.0 24.0e40.0 24.0e41.0
Gestational age on admission, wk
Median (IQR) 38.0 (36.0, 39.1) 36.7 (33.8, 38.4) 39.0 (38.0, 39.4)
þ2 þ2
Range 5e41 5e41 30e41
<13þ6, n (%) 4 (3.4) 4 (6.2) 0
þ6
14e27 , n (%) 6 (5.2) 6 (9.2) 0
þ6
28e36 , n (%) 30 (25.9) 24 (36.9) 6 (11.8)
37, n (%) 76 (65.5) 31 (47.7) 45 (88.2)
Parity
Nulliparous, n (%) 64 (55.2) 37 (56.9) 27 (52.9)
Multiparous, n (%) 52 (44.8) 28 (43.1) 24 (47.1)
Epidemiologic history 107 (92.3) 65 (100) 42 (82.3)
Relevant environmental exposure, n (%) 69 (59.5) 39 (60.0) 30 (58.8)
Contact with infected person, n (%) 38 (32.8) 26 (40.0) 12 (23.5)
Symptoms
Fevera, n (%) 59 (50.9) 45(69.2) 14 (27.5)
Cough, n (%) 33 (28.4) 28 (43.1) 5 (9.8)
Fatigue, n (%) 15 (12.9) 13 (20.0) 2 (3.9)
Shortness of breath, n (%) 9 (7.8) 8 (12.3) 1 (2.0)
Sore throat, n (%) 10 (8.6) 10 (15.4) 0
Myalgia, n (%) 6 (5.2) 5 (7.7) 1 (2.0)
Dyspnea, n (%) 3 (2.6) 3 (4.6) 0
Diarrhea, n (%) 1 (0.9) 1 (1.5) 0
No symptoms, n (%) 27 (23.3) 6 (9.2) 21 (41.2)
Pregnancy complications
Gestational diabetes mellitus 9 (7.8) 3 (4.6) 6 (11.8)
Hypertensive disorders 5 (4.3) 2 (3.1) 3 (5.9)
Preeclampsia 4 (3.4) 1 (1.5) 3 (5.9)
Disease severity
Severe 8 (6.9) 6 (9.2) 2 (3.9)
Nonsevere 108 (93.1) 59 (90.8) 49 (96.1)
Treatment
Antibiotic therapy 109 (94.0) 58 (89.2) 51 (100)
Antiviral therapy 63 (54.3) 48 (73.8) 15 (29.4)
Use of corticosteroid 37 (31.9) 26 (40.0) 11 (21.6)
ICU admission 8 (6.9) 6 (9.2) 2 (3.9)
Noninvasive ventilation 6 (5.2) 6 (9.2) 0
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020. (continued)
 TABLE 1
Demographics, baseline characteristics, and clinical outcomes of coronavirus disease 2019 infection in pregnant
women (continued)
Clinical characteristics All patients (n¼116) Laboratory confirmed (n¼65) Clinically diagnosed (n¼51)
Invasive mechanical ventilation 2 (1.7) 2 (3.1) 0
ECMO 1 (0.9) 1 (1.5) 0
Plasmapheresis 1 (0.9) 0 1 (2.0)
Clinical outcomes
Remained in hospital 40 (34.5) 24 (36.9) 16 (31.4)
Discharged 76 (65.5) 41 (63.1) 35 (68.6)
Died 0 0 0
ECMO, extracorporeal membrane oxygenation; ICU, intensive care unit; IQR, interquartile range; SD, standard deviation.
a
Including postpartum fever cases. Data are expressed as n (%). Outcomes were followed up until March 24, 2020.
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020.

septic shock after admission and of nonpregnant adults with COVID-19 of ground-glass opacity in the lungs.
required ICU admission for invasive pneumonia, as previously reported
28,29
; The rate of preterm delivery before 37
ventilation. The neonate (male) was (2) 23.3% (27/116) of pregnant patients weeks was 44%, and 94% of cases had
þ2
delivered at 35 weeks’ gestation by did not present with symptoms, but cesarean delivery. Our data were an
cesarean delivery, and severe neonatal most of these patients were diagnosed expanded series that included 33
16,18e20
asphyxia was reported. He had 1- as having COVID-19 pneumonia based published cases. We had
minute, 5-minute, and 10-minute on clinical criteria during the peak of reported clinical, laboratory, and
Apgar scores of 1, 1, and 1, respec- the outbreak in Hubei Province, China; radiologic characteristics that are
tively. He was treated with invasive (3) similar to published pregnant and
ventilation and died within 2 hours of 6.9% (8/116) of pregnant patients nonpregnant cases of COVID-19
birth. As of March 24, 2020, 76.0% (76/ experienced severe pneumonia that pneumonia.
28,29
Notably, our series
100) neonates had been discharged, required ICU admission and none died included cases of COVID-19 diagnosed
and as of March 24, 2020; (4) the rate of by clinical criteria. Most of these cases
23.0% (23/100) neonates remained in spontaneous abortion was 12.5% (1/8); presented at term, and all women
the hospital (Table 3). (5) the rate of preterm birth before 37 exhibited abnormal chest CT findings.
There were 86.0% (86/100) of weeks was 21.2% (21/99), one-third of During the peak of the COVID-19
neonates which had PPROM that resulted in outbreak, it was considered acceptable
who underwent testing for SARS-CoV- 6.1% (6/99) spontaneous preterm birth to not wait for repeated qRT-PCR
2 viral nucleic acid on pharyngeal rate; and (6) 86.0% (86/100) neonates testing to establish diagnosis. There
swab samples and the results were who were tested for SARS-CoV-2 viral were fewer cases of severe pneumonia
negative. Of these 86 neonates, paired nucleic acid on pharyngeal samples had in those who were diagnosed clinically
amniotic fluid and cord blood samples negative results; 10 of these 86
from 10 neonates tested for SARS-CoV- compared with laboratory-confirmed
16,20
neonates had paired amniotic fluid cases; cesarean delivery rate and
2 had negative re- sults. In and cord blood samples that also had neonatal outcome were similar between
addition, 6 patients con- sented and negative results for SARS-CoV-2. the 2 groups.
had their vaginal secretion samples
20 Normal pregnancy has been proposed
tested; the test results were negative. Clinical implications to be a state of physiological activation
Twelve patients had their breast milk To date, summarized data from 5 small of the innate limb of the immune
samples tested, and the test results series, with a total of 56 pregnant response. Pregnant women with acute
16,20
were negative. women
16e20
diagnosed as having infection were reported to display a
COVID-19 during the second and third more activated phenotype.
30
In our
Comments trimester, indicated that the most com- study, 8 of 116 (6.9%) pregnant women
Principal findings mon symptoms at presentation were fe- experienced severe COVID-19
We report clinical data from 116 preg- ver and cough; two-third of the patients pneumonia, which is similar to the rate
nant women with COVID-19 pneu- had lymphopenia and increased C- of severe disease that has been reported
monia. This descriptive study found that reactive protein, and 83% of cases had 28,29
(1) the clinical characteristics of these across China. This finding can be
chest CT scan revealing multiple attributed to our proac- tive and
patients with COVID-19 pneumonia patches
during pregnancy were similar to those
aggressive management of diagnosed
pregnant cases to minimize
 suggests that although the risk of any
TABLE 2
preterm birth before 37 weeks’
Laboratory and radiologic findings of pregnant women with
coronavirus disease 2019 on admission gestation is increased, COVID-19 is not
associated with an increased risk of
spontaneous
Laboratory Clinically preterm birth before 37 weeks. For the
All patients confirmed diagnosed 15 cases of iatrogenic preterm birth, ce-
Laboratory and radiologic findings (n¼116) (n¼65) (n¼51) sarean delivery was indicated for pneu-
Leucocytes (*109/L; reference rangea) monia (n¼5), twin pregnancy (n¼1),
Median (IQR) 7.9 (5.9, 10.6) 7.5 (5.2, 9.8) 8.9 (6.7, transverse lie with placenta previa
11.0) Decreased, n (%) 28 (24.1) 20 (30.8) 8 (n¼1), previous cesarean delivery
(n¼3), fetal distress (n¼3), preeclamp-
(15.7) Normal, n (%) 85 (73.3) 42 (64.6) 43
sia (n¼1), and poor obstetrical history
(84.3) Increased, n (%) 3 (2.6) 3 (4.6) 0 (n¼1).
9
Lymphocytes (*10 /L; reference range, 1.1e3.2)
Median (IQR) 1.2 (0.9, 1.6) 1.0 (0.8, 1.6) 1.3 (1.1, Research implications
One main focus of this study was to
1.6) Decreased, n (%) 51 (44.0) 38 (58.5) 13
investigate the possibility of vertical
(25.5) Normal, n (%) 64 (55.1) 26 (40.0) 38 transmission of SARS-CoV-2 infection.
(74.5) Increased, n (%) 1 (0.9) 1 (1.5) 0 We chose to evaluate amniotic fluid,
C-reactive protein concentration (mg/L; reference range, 0e10) cord blood, and neonatal pharyngeal
swab samples at birth to ascertain the
Median (IQR) 9.3 (3.3, 28.0) 16.6 (5.3, 37.9) 5.9 (2.6,
possi- bility of vertical transmission.
21.6) Increased, n (%) 51 (44.0) 32 (49.2) 19 Our results indicated that SARS-CoV-2
(37.3) Normal, n (%) 53 (45.7) 24 (36.9) 29 was negative in all of the above
(56.9) biological samples, suggesting that no
intrauterine fetal infection occurred
CT chest findings (n¼108) because of SARS-CoV-
Patchy shadowing or 104 (96.3) 53 (93.0) 51 (100%) 2 infection during the third trimester
ground-
glass opacity, n (%)
of pregnancy when the time interval
from
Negative finding, n (%) 4 (3.7) 4 (7.0) 0 clinical manifestation to delivery was
CT, computed tomography; IQR, interquartile range. up to 38 days. Our findings are in
a
Reference range in pregnancy: first trimester, 5.7e13.6 *109/L; second trimester, 5.6e14.8 *109/L; and third agreement with what was observed with
trimester, SARS-CoV.
5.9e16.9 *109 /L (from Williams Obstetrics 25th Edition27). Data are expressed as n (%). Increased means over the However, 2 recent research letters re-
upper
limit of the reference range and decreased means below the lower limit of the reference
range.
confirmed COVID-19 who tested
positive for immunoglobulin G and
immuno- globulin M antibodies
despite having a

the risk of disease progression. There monia in pregnant women is COVID-19 (n¼1462) have an increased
was a lack of clarity at the beginning associated with an increased risk of risk of preterm birth, FGR, and having a
of the COVID-19 outbreak, and we preterm birth, fetal growth restriction newborn with low birthweight and
31 Apgar score <7 at 5 minutes compared
could only base our practice on past (FGR), and perinatal mortality.
experience with SARS-CoV. As we Based on the nationwide population- with those without pneumonia
32
encountered more COVID-19 cases, based data, it has been indicated that (n¼7310). A case series of 12 pregnant
we adapted our man- agement, and pregnant women with viral women with SARS-CoV in Hong Kong,
care was provided by a pneumonia other than China, reported 3 maternal deaths; 4 of 7
multidisciplinary team including obste- patients (57%) who presented in the first
tricians, intensivists, obstetrical anes- trimester had spontaneous abortion, 4 of
thetists, virologists, microbiologists, 5 patients (80%) who presented after 24
neonatologists, and infectious-disease weeks had preterm birth, and 2 mothers
specialists. recovered without delivery but their
It has been reported that viral pneu- ongoing pregnancies were complicated
9
by FGR. Our study found reassuring
data suggesting that the risk of sponta- negative viral nucleic acid
34,35
neous abortion is not increased in result,
pregnant women with SARS-CoV-2 raising the possibility of vertical
infection from the background risk of trans- mission, but more data are
33
the general population. Our data also needed. In addition, this study
explored whether vaginal delivery
increases the risk of mother-to-
child transmission during delivery
by evaluating the vaginal se-
cretions of COVID-19 cases at
pre- sentation and these samples had
negative results. In this expanded
se- ries, our results further showed
nega- tive results for breast milk
samples from 12 mothers with
COVID-19 that were tested for
16
SARS-CoV-2.

Strengths and
limitations
This is the biggest pregnant series
to date. Unlike the other case series,
our data were collected using a
standardized methodology by a team
of experienced
 TABLE 3
Pregnancy and neonatal outcomes of coronavirus disease 2019
Outcome All deliveries (n¼99) Laboratory confirmed (n¼50) Clinically diagnosed (n¼49)
Mode of delivery
Cesarean delivery, n (%) 85 (85.9) 44 (88.0) 41 (83.7)
Vaginal delivery, n (%) 14 (14.1) 6 (12.0) 8 (16.3)
a
Indication of cesarean delivery
COVID-19 pneumonia, n (%) 33 (38.8) 19 (43.2) 14 (34.1)
Previous cesarean delivery, n (%) 16 (18.8) 8 (18.2) 8 (19.5)
Fetal distress, n (%) 9 (10.6) 7 (15.9) 2 (4.9)
Failure to progress, n (%) 5 (5.9) 3 (6.8) 2 (4.9)
Preeclampsia, n (%) 4 (4.7) 1 (2.3) 3 (7.3)
Abnormal fetal growth, n (%) 2 (2.4) 0 2 (4.9)
Placenta previa, n (%) 3 (3.5) 0 3 (7.3)
Others, n (%) 13 (15.3) 6 (13.6) 7 (17.1)
Onset of symptoms to delivery, d
Median (IQR) 2.5 (1.0, 6.7) 4.0 (1.0, 7.0) 4.0 (0.5, 8.5)
Range 0e38.0 0e38.0 0e22.0
Gestational age at delivery
Median (IQR) 38.4 (37.3, 39.4) 38.0 (36.6, 39.2) 39.0 (38.1, 39.4)
Range 28.1e41.3 28.1e41.3 31.9e41.0
<34 wk, n (%) 2 (2.0) 1 (2.0) 1 (2.0)
þ6
34e36 wk, n (%) 19 (19.2) 15 (30.0) 4 (8.2)
37 wk, n (%) 78 (78.8) 34 (68.0) 44 (89.8)
Preterm delivery before 34 wk, n (%) 2 (2.0) 1 (2.0) 1 (2.0)
Spontaneous labor-PPROM 0 0 0
Preterm delivery before 37 wk, n (%) 21 (21.2) 16 (32.0) 5 (10.2)
Spontaneous labor-PPROM 6 (6.1) 3 (6.1) 3 (6.1)
b
Clinical outcome of neonates (n¼100)
Neonatal birthweight (g) 3108 526 3087 504 3130 553
Apgar 1-min, median (IQR) 9 (8, 9) 9 (8, 9) 9 (9, 9)
Apgar 5-min, median (IQR) 10 (9, 10) 10 (9, 10) 10 (10, 10)
Severe neonatal asphyxia, n (%) 1 (1.0) 1 (2.0) 0
Transferred to NICU, n (%) 47 (47.0) 17 (34.0) 30 (60.0)
Remained in hospital, n (%) 23 (23.0) 13 (26.0) 10 (20.0)
Discharged, n (%) 76 (76.0) 36 (72.0) 40 (80.0)
Neonatal death, n (%) 1 (1.0) 1 (2.0) 0
COVID-19, coronavirus disease 2019; IQR, interquartile range; PPROM, preterm premature rupture of membranes; NICU, neonatal intensive care unit.
a
n (cesarean delivery)¼85; b including 1 pair of twins. Data are expressed as n (%). Outcomes were followed up until March 24, 2020.
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020.

clinicians, curated with customized data notable limitations. First, there were trimester of pregnancy. There are 7
collection form, and verified indepen- only 8 cases of COVID-19 pneumonia cases with ongoing pregnancy, and we
dently by 2 investigators. There are during the first and early second do not have complete data on the
some risk of
congenital anomalies and FGR. The clinical characteristics of there is no evidence that pregnant
Further- more, 4 cases have reached 20 pregnant women with COVID-19 women with COVID-19 are more prone
weeks and a morphology scan has pneumonia are similar to those of to experience severe pneumonia than
revealed normal anatomy and fetal nonpregnant adults with COVID-19 nonpregnant patients. Reassuringly, the
growth. Because the COVID-19 pneumonia. Currently, risks of spontaneous abortion and
pandemic has reached a crit- ical stage, spontaneous preterm birth are not
we believe it is important to report increased. There is no evidence of verti-
our pregnant cases in relation to the cal transmission of SARS-CoV-2 when
risk of spontaneous abortion, preterm the infection manifests during the third
birth, and vertical transmission, trimester of pregnancy. Ongoing collec-
without waiting for complete outcome tion of clinical data and research is
data to be available. This would delay currently underway with the aim to
this publica- tion by several months. answer some of the questions in relation
Second, we included cases that were to the risk of congenital infection,
diagnosed on the basis of clinical criteria intrapartum management, and mode of
in this series. Ac- cording to the WHO, delivery. n
these cases would have been classified
as probable cases of COVID-19
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N Engl J Med 2020 [Epub ahead of print]. accepted April 17, 2020.
29. Wu Z, McGoogan JM. Characteristics of and This study was supported by the Science and Tech-
important lessons from the coronavirus disease Author and article information nology Department of Hubei Province, New Pneumonia
2019 (COVID-19) outbreak in China: summary of From the Department of Obstetrics and Gynecology, Emergency Science and Technology Project, perinatal
a report of 72 314 cases from the Chinese Peking University First Hospital, Beijing, China (Drs Yan, management strategies and mother-to-child trans-
Center for Disease Control and Prevention. Juan, Wang, and Yang); Department of Obstetrics and mission of pregnant women infected with 2019-nCoV
JAMA 2020 [Epub ahead of print]. Gynecology, Zhongnan Hospital of Wuhan University, (grant number 2020FCA011). The funding agencies
30. Naccasha N, Gervasi MT, Wuhan, China, Clinical Medicine Research Center of had no involvement in the study design, data collection,
Chaiworapongsa T, et al. Phenotypic and meta- Prenatal Diagnosis and Birth Health in Hubei Province, data analysis, data interpretation, writing of the report, or
bolic characteristics of monocytes and gran- Wuhan, China (Drs Guo, Yu, Li, Chen, Qiao, and Zhang); in the decision to submit the article for publication.
ulocytes in normal pregnancy and maternal Department of Obstetrics, Renmin Hospital of Wuhan The authors report no conflict of interest.
infection. Am J Obstet Gynecol 2001;185: University, Wuhan, China (Drs Fan, Li, and Lei); Depart- Corresponding author: Huixia Yang, MD. yanghuixia@
1118–23. ment of Obstetrics and Gynecology, Tongji Hospital, bjmu.edu.cn
1.e
10
SUPPLEMENTAL TABLE Or
Am
Clinical characteristics, pregnancy outcomes, and treatment for severe cases igi
eric Case 1 2 3 4 5 6 7 8 na
an
Jou
Clinical characteristics l
rnal Date of admission 2020/2/1 2020/1/28 2020/1/31 2020/2/17 2020/1/28 2020/1/26 2020/2/5 2020/2/2 Re
of
Ob
Age 32 35 34 33 28 30 35 32 se
stet Occupation / Nurse / Bank staff Company
employee
/ / /
ar
rics
& Gravidity 5 2 4 3 2 1 6 3 ch
O
Gy Parity 2 1 1 1 1 0 2 1 B
nec
Gestational age on 35þ2 34þ2 37þ6 36þ2 39þ0 39þ1 38þ2 28þ1
ST
olo
admission (wk) ET
gy
Residence Zhongshan, Wuhan, Hubei Zaoyang, Hubei Wuhan, Hubei Wuhan, Hubei Wuhan, Hubei Badong, Hubei Huangshi, Hubei RI
MO
Guangdong C
NTH
202 Epidemiologic history þ þ þ þ þ þ þ þ
0
Description of epidemiology Relevant Contacts with Contacts with Relevant Relevant Relevant Contacts with Relevant
environmental infected person person who came environmental environmental environmental person who came environmental
exposure back from Wuhan exposure (Wuhan, exposure exposure (Wuhan, back from Wuhan exposure (Wuhan,
(Xiaogan, Hubei) Hubei) (Wuhan, Hubei) Hubei) Hubei)
Other family members - - þ - - - þ -
affected
Onset to delivery (d) 4 Onset after delivery 0 10 Onset after Onset after 5 7
delivery delivery
Complications - PPROM Anemia; PPROM; elevated Anemia; Preeclampsia HBsAg (þ); Anemia
tachycardia aminotransferase hypothyroidism hypoproteinemia
Onset of symptoms
Fever/postpartum fever þ - þ þ þ þ þ þ
Cough þ þ - - - - þ þ
Fatigue - - þ - - - þ -
Shortness of breath - þ - - - - - -
Sore throat þ - - - - - - þ
Dyspnea - - þ - - - - -
Heart rate (bpm) 128 79 118 100 78 100 113 102
Respiratory rate (bpm) 23 30 20 20 20 20 28 25
Mean arterial pressure (mm 83 97 96 86 127 101 58 87
g.
Hg) or
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020. (continued)
g
 g.
SUPPLEMENTAL TABLE
Clinical characteristics, pregnancy outcomes, and treatment for severe cases (continued)
or
g
Case 1 2 3 4 5 6 7 8
Laboratory characteristics
White blood cell count (109/L) 6.80 7.10 10.65 11.67 14.95 11.50 4.00 13.16
Low or normal leukocyte þ þ þ þ þ þ þ þ
count
(<5.9e16.9 *109/L)
Lymphocyte count (109/L) 0.884 0.69 1.42 1.5 0.54 1.02 0.3 1.09
9
Lymphopenia (<1.1 *10 /L) þ þ - - þ þ þ þ
9
Neutrophil count (10 /L) / 6.01 8.87 9.83 4.78 7.41 / 10.64
9
Platelet count (10 /L) 160 184 269 282 202 274 146 271
CRP (mg/L) 60.8 73.63 102.8 41.2 152.4 52.74 94 41.98
Elevated CRP (>10 mg/L) þ þ þ þ þ þ þ þ
Prothrombin time (s) / 11.6 10.3 18.5 9.8 10.9 / 11.7
Activated partial / 30.7 33.4 40 31.7 24.5 / 32.5
thromboplastin time (s)
D-dimer (mg/L) / 3.93 1.28 / 1.31 1.94 6.54 0.68
Elevated aminotransferase þ þ þ þ - - þ -
(ALT<45U/L, AST<35U/L)
MO
NTH ALT (U/L) 142 51 72 181 17.6 6.9 90 17
202 AST (U/L) 235 22 50 213 28.2 12.6 59 28
0 OB
Creatine kinase (U/L) / 24 32.94 638 40.18 54.62 / 23
Am
Creatine kinase-MB (U/L) / 9 1.59 137 19.66 13.86 / 11
STE
eric
an Lactate dehydrogenase (U/L) / 452 322.7 638 196.3 195.5 / 276 TRI
Jou
Total bilirubin (mmol/L) / 7.8 19.78 123.1 6.1 1.8 19.2 14.8 CS
rnal
of Blood urea nitrogen (mmol/L) 2.3 3.4 1.52 5.5 4.21 3.35 4.44 1.24 Or
Ob
stet
Creatinine (mmol/L) 85 46.8 56.62 152.6 54.6 49.1 61.98 38 igi
rics Procalcitonin (ng/mL) 7.29 0.89 0.89 1.56 0.222 0.122 0.05 0.31 na
& Blood gas analysis l
Gy
nec
pH 7.41 7.27 7.41 / / / / 7.42 Re
olo Lactate (mmol/L) 4 3.4 / / / / / 1.8 se
gy
1.e
PaO2 (mm Hg) 60.5 117 66 / / / / 86
ar
11
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020. (continued)
ch
1.e
12 SUPPLEMENTAL TABLE
Or
Am Clinical characteristics, pregnancy outcomes, and treatment for severe cases (continued) igi
eric Case 1 2 3 4 5 6 7 8 na
an
Jou PaCO2 (mm Hg) 17.7 73 36.7 / / / / 24 l
rnal Confirmatory test þ þ þ - þ / þ þ Re
of
Ob
(SARS-CoV-2 by qRT-PCR) se
stet CT evidence of pneumonia ar
rics
&
Bilateral distribution of
patchy shadows or ground-
þ þ þ þ þ þ þ ch
O
Gy glass opacity
B
nec Local patchy shadows or þ ST
olo ground-glass opacity ET
gy
Mode of delivery CS Vaginal delivery CS Vaginal delivery CS CS Vaginal delivery CS RI
MO
C
NTH Indication for CS Previous CS / Previous CS / Previous CS Preeclampsia / Pneumonia
202 Pneumonia Pneumonia Pneumonia Pneumonia
0
Septic shock
Treatment
Oxygen support
(nasal cannula) þ þ þ þ þ þ þ þ

Antibiotic therapy Piperacillin and

Moxifloxacin, Moxifloxacin, Moxifloxacin, Cefaxone/ Cefoperazone/ Azithromycin, Cefamandole,
sulbactam
cephalosporin, cefoperazone/ meropenem tazobactam sulbactam levofloxacin, ornidazole,
sodium,
imipenem, linezolid, sulbactam vancomycin cefmenoxime
imipenem
meropenem,
polymyxin B,
sulfanilamide
Antiviral therapy Oseltamivir Ganciclovir, arbidol,
Lopinavir, Arbidol Oseltamivir, Interferon Aciclovir, Arbidol
interferon
peramivir, arbidol, interferon oseltamivir,
interferon ribavirin, Interferon
Use of corticosteroid - Methylprednisolone,
prednisone Methylprednisolone Methylprednisolone - - - Methylprednisolone

Admitted to an ICU (d) þ 30 þ 14 6 3 16 15

Noninvasive ventilation (d) Withdrew
8 6 - 6 - 3 3
ventilation 36
Invasive mechanical 11 - - - - - -
ventilation (d) d after CS

ECMO (d) Withdrew ECMO - - - - - - - g.

26 d after CS
or
Plasmapheresis - - - þ - - - - g
Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020. (continued)
 g.
SUPPLEMENTAL TABLE
Clinical characteristics, pregnancy outcomes, and treatment for severe cases (continued)
or
g
Case 1 2 3 4 5 6 7 8
Duration of hospitalization (d) Remain in Remain in hospital 29 16 14 4 16 15
hospital
Pregnancy outcome
Gestational age at delivery 35þ2 34þ2 37þ6 36þ2 39þ1 39þ1 38þ3 28þ1
(wk)
Birthweight (g) 2700 2350 3500 2670 3750 3800 3200 1530
Preterm delivery þ þ - þ - - - þ
Low birthweight - þ - - - - - þ
Apgar score (1-min, 5-min) 1, 1 9, 10 9, 10 8, 9 10, 10 10, 10 9, 10 8, 9
Neonatal asphyxia þ - - - - - - -
Transferred to NICU þ - - þ - - - þ
Noninvasive ventilation - - - - - - - -
Invasive mechanical þ - - - - - - þ
ventilation
Neonatal death þ - - - - - - -
Neonatal outcomes Died Discharged Discharged Discharged Discharged Discharged Discharged Remained in
hospital
MO Fetal death or stillbirth - - - - - - - -
NTH Outcomes were followed up until March 22, 2020.
202 ALT, alanine transaminase; AST, aspartate aminotransferase; COVID-19, coronavirus disease 2019; CRP, C-reactive protein; CT, computed tomography; ECMO, extracorporeal membrane oxygenation; ICU, intensive care unit; NICU, neonatal intensive care unit;
0 PPROM, preterm premature rupture of membranes; qRT-PCR, quantitative reverse transcriptase polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2. OB
Am Yan et al. Coronavirus disease 2019 in pregnant women: 116 cases. Am J Obstet Gynecol 2020.
STE
eric
an TRI
Jou
CS
rnal
of Or
Ob
stet
igi
rics na
& l
Gy
nec Re
olo se
gy
1.e ar
13 ch
Original Research OBSTETRICS ajog.org

Supplemental Material Hanchuan People’s Hospital of Hubei Affiliated Taihe Hospital of Hubei
List of hospitals from which clinical re- Province University of Medicine
cords were retrospectively reviewed for Jiangnan Branch of the Yichang Cen- Badong County People’s Hospital in
116 pregnant women with coronavirus tral People’s Hospital Hubei Province
disease 2019 pneumonia Egang Hospital Xiangyang Central Hospital
Zhongnan Hospital of Wuhan Jianli County People’s Hospital Jingmen No. 1 People’s Hospital
University Zaoyang First People’s Hospital Jingzhou Maternal and Child Health
Renmin Hospital of Wuhan Xinglin Branch of the First Affiliated Hospital
University Hospital of Xiamen University The First People’s Hospital of
The Central Hospital of Wuhan Maternal and Child Hospital of Xianning
Tongji Hospital, Tongji Medical Hubei Huangshi Maternity and Children’s
Col- Province
lege, Huazhong University of Science The First People’s Hospital of Xiao- Health Hospital
and Technology chang County Yangxin People’s Hospital in Hubei
The Central Hospital of Suizhou Maternal and Child Health and Fam- Province
Yichang Central People’s Hospital ily Planning Service Center of Dawu Yan et al . Coronavirus disease 2019 in
Beijing YouAn Hospital County pregnant women: 116 cases. Am J Obstet
Anlu Pu’ai Hospital Gynecol 2020.

1.e14 American Journal of Obstetrics & Gynecology MONTH 2020