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Letters

Tina Schaller, MD tion. A study conducted in New York City reported a 13.5%
Klaus Hirschbühl, MD prevalence of asymptomatic infection with severe acute
Katrin Burkhardt, MD respiratory syndrome coronavirus 2 (SARS-CoV-2) in women
Georg Braun, MD presenting for childbirth.1 On March 30, 2020, an initially
Martin Trepel, MD asymptomatic woman admitted to the Yale New Haven Health
Bruno Märkl, MD system developed cough and fever soon after childbirth; test-
Rainer Claus, MD ing confirmed SARS-CoV-2 infection. This event prompted the
development of a SARS-CoV-2 screening and testing program
Author Affiliations: Institute of Pathology and Molecular Diagnostics, of patients presenting for childbirth; we report the preva-
University Medical Center Augsburg, Augsburg, Germany (Schaller, Märkl);
Department of Hematology and Clinical Oncology, University Medical Center
lence detected in the first weeks of the program.
Augsburg, Augsburg, Germany (Hirschbühl, Trepel, Claus); Institute of
Laboratory Medicine and Microbiology, University Medical Center Augsburg, Methods | From April 2, 2020, to April 29, 2020, screening and
Augsburg, Germany (Burkhardt); Department of Gastroenterology, University
testing of patients admitted for childbirth was initiated at 3 Yale
Medical Center Augsburg, Augsburg, Germany (Braun).
New Haven Health hospitals in southern Connecticut. Screen-
Accepted for Publication: May 11, 2020.
ing consisted of questions related to travel, contacts, and symp-
Corresponding Author: Rainer Claus, MD, Department of Hematology and
Clinical Oncology, University Medical Center Augsburg, Stenglinstrasse 2, 86156
toms of COVID-19. All patients without a prior diagnosis of
Augsburg, Germany (rainer.claus@uk-augsburg.de). COVID-19 underwent SARS-CoV-2 polymerase chain reaction
Published Online: May 21, 2020. doi:10.1001/jama.2020.8907 (PCR) testing of nasopharyngeal swabs, with rapid testing avail-
Author Contributions: Drs Schaller and Claus had full access to all of the data in able. Patients scheduled for cesarean birth were screened and
the study and take responsibility for the integrity of the data and the accuracy tested at preoperative visits.
of the data analysis. Drs Schaller and Hirschbühl contributed equally as first Hospital policies recommended universal mask use on
authors. Drs Märkl and Claus contributed equally as senior authors.
Concept and design: Schaller, Hirschbühl, Braun, Trepel, Märkl, Claus.
clinical units by clinicians, patients, and support persons and
Acquisition, analysis, or interpretation of data: Schaller, Hirschbühl, Burkhardt, limited each patient to 1 support person visitor for childbirth.
Märkl, Claus. For patients with symptoms of COVID-19, clinicians wore N95
Drafting of the manuscript: Schaller, Hirschbühl, Braun, Trepel, Märkl, Claus.
respirators and appropriate personal protective equipment
Critical revision of the manuscript for important intellectual content: Schaller,
Hirschbühl, Burkhardt, Trepel, Märkl, Claus.
Statistical analysis: Claus.
Obtained funding: Braun. Table 1. Demographics and Characteristics of Patients Tested
Administrative, technical, or material support: Schaller, Hirschbühl, Burkhardt, for SARS-CoV-2 on Admission for Childbirtha
Trepel, Märkl.
Supervision: Claus. SARS-CoV-2 PCR result
Conflict of Interest Disclosures: None reported. Characteristics Positive (n = 30) Negative (n = 740)
Additional Contributions: We thank the physicians from the intensive care unit Age, y
(Michael Wittmann, MD, and Ulrich Jaschinski, MD), and the Department of <30 14 (46.7) 199 (26.9)
Radiology (Thomas Kröncke, MD) of the University Medical Center Augsburg. 30-34 10 (33.3) 310 (41.9)
We thank Jürgen Schlegel, MD, from the Department of Neuropathology,
School of Medicine, Institute of Pathology, Technical University Munich, for ≥35 6 (20.0) 231 (31.2)
sampling brain tissue. Technical support was provided by Alexandra Martin, Nulliparity 16 (53.3) 323 (43.7)
AMLT, Christian Beul, AMLT, and Elfriede Schwarz, AMLT, from the Institute of Site of hospital
Pathology and Molecular Diagnostics, University Medical Center Augsburg. No
compensation was received for their roles in the study. Greenwich 8 (26.7) 204 (27.6)

1. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 Bridgeport 11 (36.7) 129 (17.4)
novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. doi:10. New Haven 11 (36.7) 407 (55.0)
1016/S0140-6736(20)30183-5 Gestation <37 wk 0 62 (8.4)
2. Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients at birth
with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. Cesarean deliveryb 10 (33.3) 275 (37.2)
Published online February 7, 2020. doi:10.1001/jama.2020.1585 Apgar score
3. Hanley B, Lucas SB, Youd E, Swift B, Osborn M. Autopsy in suspected <7 At 1 min 0 40 (5.4)
COVID-19 cases. J Clin Pathol. 2020;73(5):239-242. doi:10.1136/jclinpath-2020-
206522 <7 At 5 min 0 12 (1.6)

4. Gu J, Korteweg C. Pathology and pathogenesis of severe acute respiratory Neonatal birth weight, 3370 (621) 3331 (568)
mean (SD), g
syndrome. Am J Pathol. 2007;170(4):1136-1147. doi:10.2353/ajpath.2007.061088
Neonatal SARS-CoV-2 positive 0
5. van den Brand JM, Smits SL, Haagmans BL. Pathogenesis of Middle East test resultc
respiratory syndrome coronavirus. J Pathol. 2015;235(2):175-184. doi:10.1002/
path.4458 Abbreviations: COVID-19, coronavirus disease 2019; PCR, polymerase chain
reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.
a
Data are expressed as No. (%) of participants unless otherwise indicated.
Prevalence of SARS-CoV-2 Among Patients Admitted Excludes patients diagnosed with COVID-19 prior to admission, including
for Childbirth in Southern Connecticut those considered recovered (defined as ⱖ14 days from onset of symptoms
Developing an approach to care for pregnancy and child- and ⱖ72 hours afebrile).
b
birth during the coronavirus disease 2019 (COVID-19) crisis Mode of birth was determined by routine obstetric indications.
c
is a priority to (1) provide safe care to pregnant women and Neonatal testing by PCR of nasopharyngeal swabs was performed at 24 hours
of age.
newborns and (2) protect health care workers from infec-

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Letters

Table 2. SARS-CoV-2 Test Results for Patients Tested at Admission for Childbirth, Stratified by Symptomsa

Patients screened, No. (%)b


Screening characteristic SARS-CoV-2 PCR result April 2-15, 2020 (n = 365) April 16-29, 2020 (n = 405) Total (n = 770)
Asymptomatic Positive 2 (0.5) 20 (4.9) 22 (2.9)
Negative 353 (96.7) 381 (94.1) 734 (95.3)
Symptomaticc Positive 5 (1.4) 3 (0.7) 8 (1.0)
Negative 5 (1.4) 1 (0.2) 6 (0.8)
c
Abbreviations: COVID-19, coronavirus disease 2019; PCR, polymerase chain Signs and symptoms of COVID-19 in patients with positive SARS-CoV-2 test
reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2. results were mild in 7 patients, including fever, headache, rhinorrhea, sore
a
Excludes patients diagnosed with COVID-19 prior to admission, including throat, myalgias, congestion, cough, anosmia/ageusia. One patient had severe
those considered recovered (defined as ⱖ14 days from onset of symptoms symptoms, including fever, myalgias, malaise, congestion, and shortness of
and ⱖ72 hours afebrile). breath. No mildly symptomatic patients developed COVID-19–related
b
complications. The severely symptomatic patient recovered from respiratory
Percentage is expressed as percentage of total patients tested during
insufficiency with critical care and oxygen support via nonrebreather mask.
the time period.

(PPE) until results returned, continuing use for patients with third highest death rate per capita from COVID-19, indicat-
positive test results. For patients without symptoms of COVID- ing a substantially affected region.2 The increasing preva-
19, clinicians followed usual precautions including wearing lence of positive SARS-CoV-2 test results in the asymptom-
masks. For the second stage of labor and cesarean or vaginal atic population, while the prevalence of symptomatic
birth, clinicians wore full PPE and N95 respirators for pa- infections decreased, may indicate that universal testing
tients without test results or with positive results. Excluded identifies patients in a convalescent period, in addition to
from universal testing were patients already diagnosed with those with subclinical active infection. Although performed
COVID-19 and patients not admitted for childbirth. The num- in mixed community and academic hospital settings, limita-
bers of positive PCR tests in patients with and without symp- tions of the findings include a short duration and a single
toms of COVID-19 were assessed over time. This quality im- geographic region.
provement project does not meet the definition of human Approaches to care that balance screening and testing of
subjects research; review by the institutional review board was patients combined with a rationalized approach to use of PPE
not required. should be considered for obstetric units.

Results | Seven hundred eighty-two patients presenting for Katherine H. Campbell, MD, MPH
childbirth were screened; 1.5% (12/782) were previously diag- Jean M. Tornatore, MD
nosed with COVID-19. The remaining 770 patients were Kirsten E. Lawrence, MD
tested at admission (Table 1), and 30 of 770 (3.9%) tested Jessica L. Illuzzi, MD
positive for SARS-CoV-2 (Table 2). Twenty-two of the 30 who
L. Scott Sussman, MD
tested positive for SARS-CoV-2 (73.3%) were asymptomatic. Heather S. Lipkind, MD
The overall prevalence of positive test results among asymp- Christian M. Pettker, MD
tomatic patients was 2.9% (22/756). Prevalence of positive
test results among asymptomatic patients increased from
Author Affiliations: Department of Obstetrics, Gynecology, and Reproductive
0.6% (2/355) to 5% (20/401) from the first 2 weeks (April 2-15, Sciences, Yale School of Medicine, New Haven, Connecticut (Campbell,
2020) to the second 2 weeks (April 16-29, 2020), though the Lawrence, Illuzzi, Lipkind, Pettker); Department of Obstetrics and Gynecology,
prevalence of symptomatic patients who tested positive in Bridgeport Hospital, Bridgeport, Connecticut (Tornatore); Clinical Redesign,
Yale New Haven Health, New Haven, Connecticut (Sussman).
the total population admitted for childbirth decreased from
Corresponding Author: Katherine H. Campbell, MD, MPH, Department of
1.4% (5/365) to 0.7% (3/405) (Table 2). Fifty-seven percent
Obstetrics, Gynecology, and Reproductive Sciences, Yale School
(8/14) of patients with symptoms tested positive. No asymp- of Medicine, 330 Cedar St, FMB 302, New Haven, CT 06520-8063
tomatic patients who tested negative developed symptoms (katherine.campbell@yale.edu).
or required further testing. No health care workers on the Accepted for Publication: May 11, 2020.
obstetric units were removed from work due to SARS-CoV-2 Published Online: May 26, 2020. doi:10.1001/jama.2020.8904
exposure or disease from transmission from a known or pos- Author Contributions: Dr Campbell had full access to all of the data in the
sible contact with a patient. study and takes responsibility for the integrity of the data and the accuracy of
the data analysis.
Concept and design: Campbell, Illuzzi, Sussman, Lipkind, Pettker.
Discussion | These findings suggest a low (<3%) prevalence of Acquisition, analysis, or interpretation of data: Campbell, Tornatore, Lawrence,
positive SARS-CoV-2 test results among asymptomatic Illuzzi, Lipkind, Pettker.
patients in a pregnant population outside of the highly Drafting of the manuscript: Campbell, Illuzzi, Lipkind, Pettker.
Critical revision of the manuscript for important intellectual content: All authors.
endemic region of New York City. During this time period,
Statistical analysis: Illuzzi, Lipkind, Pettker.
these hospitals, with approximately 2200 licensed beds, Administrative, technical, or material support: Tornatore, Pettker.
experienced a peak (April 21, 2020) of 759 patients admitted Supervision: Lawrence, Lipkind, Pettker.
for COVID-19, and among US states, Connecticut had the Conflict of Interest Disclosures: None reported.

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Letters

1. Sutton D, Fuchs K, D’Alton M, Goffman D. Universal screening for SARS-CoV-2 nential growth function to cumulative hospitalization data
in women admitted for delivery. N Engl J Med. Published online April 13, 2020. in each state for dates up to and including the median effec-
doi:10.1056/NEJMc2009316
tive date of that state’s stay-at-home order. We computed
2. Connecticut coronavirus map and case count. New York Times. Published
95% prediction bands on the exponential fit line to deter-
April 16, 2020 (updated daily). Accessed April 16, 2020. https://www.nytimes.
com/interactive/2020/us/coronavirus-us-cases.html mine if the observed number of hospitalizations fell within
the interval. We then examined whether the observed
cumulative hospitalizations for dates after the median
Association of Stay-at-Home Orders With COVID-19 effective date deviated from the projected exponential
Hospitalizations in 4 States growth in cumulative hospitalizations. In an additional
In analyses of the effectiveness of response measures to analysis, a linear growth function was fit to cumulative hos-
the outbreak of coronavirus disease 2019 (COVID-19), pitalization data for dates up to and including the median
most studies have used the number of confirmed cases or effective date, and goodness of fit was assessed with an R2
deaths. However, case count is a conservative estimate of comparison. All analyses were performed using Microsoft
the actual number of infected individuals in the absence Excel version 14.1.
of community-wide serologic testing. Death count is a lag-
ging metric and insufficient for proactive hospital capacity Results | In all 4 states, cumulative hospitalizations up to and
planning. A more valuable metric for assessing the effects of including the median effective date of a stay-at-home order
public health interventions on the health care infrastructure closely fit and favored an exponential function over a linear
is hospitalizations.1 As of April 18, 2020, governors in 42 fit (R2 = 0.973 vs 0.695 in Colorado; 0.965 vs 0.865 in Min-
states had issued statewide executive “stay-at-home” nesota; 0.98 vs 0.803 in Ohio; 0.994 vs 0.775 in Virginia)
orders to help mitigate the risk that COVID-19 hospitaliza- (Table). However, after the median effective date, observed
tions would overwhelm their state’s health care infrastruc- hospitalization growth rates deviated from projected expo-
ture. This study assessed the association between these nential growth rates with slower growth in all 4 states.
orders and hospitalization trends. Observed hospitalizations consistently fell outside of the
95% prediction bands of the projected exponential growth
Methods | In March 2020, we began collecting data on cumu- curve (Figure).
lative confirmed COVID-19 hospitalizations from each For example, Minnesota’s residents were mandated to
state’s department of health website on a daily basis. 2 stay at home starting March 28. On April 13, 5 days after the
Among states issuing a statewide stay-at-home order, we median effective date, the cumulative projected hospitaliza-
identified states with at least 7 consecutive days of cumula- tions were 988 and the actual hospitalizations were 361.
tive hospitalization data for COVID-19 (including patients In Virginia, projected hospitalizations 5 days after the
currently hospitalized and those discharged) before the median effective date were 2335 and actual hospitalizations
stay-at-home order date and at least 17 days following were 1048.
the order date. Because the median incubation period of
COVID-19 was reported to be 4 to 5.1 days3,4 and the median Discussion | In 4 states with stay-at-home orders, cumulative hos-
time from first symptom to hospitalization was found to be pitalizations for COVID-19 deviated from projected best-fit ex-
7 days,5 we hypothesized that any association between stay- ponential growth rates after these orders became effective. The
at-home orders and hospitalization rates would become evi- deviation started 2 to 4 days sooner than the median effective
dent after 12 days (median effective date). States included in date of each state’s order and may reflect the use of a median
this sample were Colorado, Minnesota, Ohio, and Virginia. incubation period for symptom onset and time to hospitaliza-
Among the 4 states meeting the inclusion criteria, the earli- tion to establish this date. Other factors that potentially de-
est date with data on hospitalizations was March 10. All creased the rate of virus spread and subsequent hospitaliza-
states were observed through April 28. We fit the best expo- tions include school closures, social distancing guidelines, and

Table. Cumulative Hospitalizations Due to COVID-19 in Colorado, Minnesota, Ohio, and Virginia, March 10 Through April 28, 2020

Cumulative hospitalizations Best exponential fit: ln(y) = ln(a) + bt Linear fit: y = ct


Fitting Stay-at-home Median On first day
State perioda issue date effective date of reporting On April 28 ln(a) (95% CI) b (95% CI) R2 c (95% CI) R2
Colorado March March 26 April 6 2 2671 1.28 0.24 0.973 30.89 0.695
10-April 6 (1.02-1.54) (0.22-0.25) (25.28-36.5)
Minnesota March March 28 April 8 7 912 2.02 0.19 0.965 9.993 0.865
19-April 8 (1.8-2.24) (0.17-0.21) (8.86-11.12)
Ohio March March 24 April 4 17 3340 2.94 0.23 0.98 38.23 0.803
17-April 4 (2.75-3.13) (0.21-0.24) (32.78-43.67)
Virginia March March 30 April 10 19 2165 2.77 0.178 0.994 23.31 0.775
19-April 10 (2.69-2.85) (0.172-0.184) (19.74-26.9)

Abbreviation: COVID-19, coronavirus disease 2019.


a
Fitting period consists of observed data from the first day of reporting up to and including the median effective date of the state’s stay-at-home order.

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