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Posted: June 29th, 2022

*A complete list of the investigators is included in the Supplementary

The new england
journal of medicine
n engl j med 382;22 nejm.org May 28, 2020 2081
established in 1812 May 28, 2020 vol. 382 no. 22
The authors’ full names, academic degrees, and affiliations are listed in the Appendix. Address reprint requests to Dr.
Jernigan at the Centers for Disease Control and Prevention, 1600 Clifton Rd.,
Mailstop A-31, Atlanta, GA 30333, or at
jqj9@cdc.gov.
*A complete list of the investigators is included in the Supplementary Appendix,
available at NEJM.org.
Ms. Arons and Ms. Hatfield contributed
equally to this article.
This article was published on April 24,
2020, at NEJM.org.
N Engl J Med 2020;382:2081-90.
DOI: 10.1056/NEJMoa2008457
Copyright © 2020 Massachusetts Medical Society.
BACKGROUND
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can spread
rapidly within skilled nursing facilities. After identification of a case of Covid-19
in a skilled nursing facility, we assessed transmission and evaluated the adequacy
of symptom-based screening to identify infections in residents.
METHODS
We conducted two serial point-prevalence surveys, 1 week apart, in which assenting
residents of the facility underwent nasopharyngeal and oropharyngeal testing for
SARS-CoV-2, including real-time reverse-transcriptase polymerase chain reaction
(rRT-PCR), viral culture, and sequencing. Symptoms that had been present during
the preceding 14 days were recorded. Asymptomatic residents who tested positive
were reassessed 7 days later. Residents with SARS-CoV-2 infection were categorized as symptomatic with typical symptoms (fever, cough, or shortness of breath),
symptomatic with only atypical symptoms, presymptomatic, or asymptomatic.
RESULTS
Twenty-three days after the first positive test result in a resident at this skilled nursing facility, 57 of 89 residents (64%) tested positive for SARS-CoV-2. Among 76 residents who participated in point-prevalence surveys, 48 (63%) tested positive. Of these
48 residents, 27 (56%) were asymptomatic at the time of testing; 24 subsequently
developed symptoms (median time to onset, 4 days). Samples from these 24 presymptomatic residents had a median rRT-PCR cycle threshold value of 23.1, and
viable virus was recovered from 17 residents. As of April 3, of the 57 residents with
SARS-CoV-2 infection, 11 had been hospitalized (3 in the intensive care unit) and
15 had died (mortality, 26%). Of the 34 residents whose specimens were sequenced,
27 (79%) had sequences that fit into two clusters with a difference of one nucleotide.
CONCLUSIONS
Rapid and widespread transmission of SARS-CoV-2 was demonstrated in this skilled
nursing facility. More than half of residents with positive test results were asymptomatic at the time of testing and most likely contributed to transmission. Infection-control strategies focused solely on symptomatic residents were not sufficient
to prevent transmission after SARS-CoV-2 introduction into this facility.
abstract
Presymptomatic SARS-CoV-2 Infections and Transmission
in a Skilled Nursing Facility
M.M. Arons, K.M. Hatfield, S.C. Reddy, A. Kimball, A. James, J.R. Jacobs, J. Taylor, K. Spicer, A.C. Bardossy,
L.P. Oakley, S. Tanwar, J.W. Dyal, J. Harney, Z. Chisty, J.M. Bell, M. Methner, P. Paul, C.M. Carlson,
H.P. McLaughlin, N. Thornburg, S. Tong, A. Tamin, Y. Tao, A. Uehara, J. Harcourt, S. Clark, C. Brostrom-Smith,
L.C. Page, M. Kay, J. Lewis, P. Montgomery, N.D. Stone, T.A. Clark, M.A. Honein, J.S. Duchin, and J.A. Jernigan,
for the Public Health–Seattle and King County and CDC COVID-19 Investigation Team*
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The new england journal o f medicine
The first reported case of coronavirus disease 2019 (Covid-19) in the United
States was diagnosed in a resident of Snohomish County, Washington, on January 20, 2020.1
In late February, an outbreak was identified in a
skilled nursing facility in neighboring King County; morbidity and mortality among residents were
high, straining the regional health care system.2,3
We report another outbreak of Covid-19 in a
separate skilled nursing facility in the same county.
In the course of this outbreak investigation, Public
Health–Seattle and King County (PHSKC) and the
Centers for Disease Control and Prevention (CDC)
identified residents with asymptomatic SARSCoV-2 infection, which prompted further investigation. We performed serial point-prevalence surveys to assess the extent of transmission and to
evaluate the adequacy of symptom-based screening
of residents to identify infections. Initial findings
of this investigation were previously reported.4
Description of the Outbreak
On February 29, 2020, in response to increased
local awareness of Covid-19 in King County,
Washington, administrative leadership at Facility
A instituted enhanced infection-control measures.
Nursing staff assessed residents twice daily for
possible signs and symptoms of Covid-19, including fever (oral or temporal temperature measurement), cough, shortness of breath, and other
symptoms. Health care personnel were assessed
at the start of each shift with oral temperature
measurement and screening for symptoms, including cough, shortness of breath, sore throat,
or any other respiratory symptoms.
On March 1, one member of the health care
staff tested positive for SARS-CoV-2 after having
worked in a single unit (Unit 1) while symptomatic on February 26, the first day of symptoms,
and on February 28. On March 5, the facility was
informed that a hospitalized resident of Unit 1
(in whom symptoms had developed on March 2
and testing was done on March 3) had been diagnosed with Covid-19. Subsequently, all visitors
were restricted and communal activities were canceled. PHSKC and the CDC initiated an outbreak
investigation, and on March 6, provided on-site
infection prevention and control recommendations, including the recommendation that all
health care staff entering symptomatic residents’
rooms wear eye protection, a gown, gloves, and
a face mask (N95 respirators were not routinely
available).5
On March 8, the CDC and PHSKC
offered testing to all residents in Unit 1; 13 of
15 residents present were tested for SARS-CoV-2
(2 residents declined). A total of 6 residents tested
positive; of these, 4 had symptoms (e.g., fever,
cough, shortness of breath, or sore throat) and
2 had been asymptomatic during the preceding
14 days. On March 9, the facility implemented
Covid-19 transmission-based precautions for all
residents of Unit 1, regardless of symptoms or
infection status.
Methods
Study Population
Facility A is a 116-bed skilled nursing facility divided into four separate units with an equal mix of
short- and long-term residents in each unit. There
were 89 residents present at Facility A on March 3,
the date of the first positive test in a resident. Facility A provided a list of full-time health care personnel by occupation. Results of positive SARS-CoV-2
tests obtained during postmortem examination or
by outside health care providers during clinical
Assessment of symptomatic residents and staff were
provided to the CDC and PHSKC through March
26. All symptomatic health care personnel were
advised to be tested by their health care provider;
asymptomatic staff members were not tested as
part of this investigation.
Point-Prevalence Surveys
On two occasions, residents in the facility were
offered SARS-CoV-2 testing as part of a facilitywide point-prevalence survey. The first survey was
performed for all assenting residents, including
those who had previously tested positive, on March
13 (10 days after the first resident had tested
positive for SARS-CoV-2). Nasopharyngeal and
oropharyngeal swabs were collected in accordance
with CDC guidelines.6
A second survey was conducted 7 days later (March 19–20) for residents
who had had either a negative test result or a
positive result with atypical or no symptoms reported in the first survey.
Symptom Assessment
On the day of point-prevalence surveys, a standardized symptom-assessment form was completed by
nurses for each resident tested. Symptoms present during the preceding 14 days were recorded on
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n engl j med 382;22 nejm.org May 28, 2020 2083
Presymptomatic SARS-CoV-2 in a Nursing Facility
the basis of interview and review of medical records. Asymptomatic residents with a positive test
result were reassessed for symptoms 7 days later.
For additional details on symptom assessment,
see the Supplementary Appendix, available with
the full text of this article at NEJM.org.
Residents were classified as symptomatic if
they had had at least one new or worsened typical or atypical symptom of Covid-19 in the preceding 14 days. Residents with subjective fever
or temperature greater than 100.0°F (37.8°C),
cough, or shortness of breath were classified as
symptomatic with typical symptoms.7
Residents
were classified as symptomatic with atypical symptoms if their symptoms included only chills, malaise, increased confusion, rhinorrhea, nasal congestion, sore throat, myalgia, dizziness, headache,
nausea, or diarrhea.
Asymptomatic residents were those who had
no symptoms or only stable chronic symptoms
(e.g., chronic cough without worsening). Presymptomatic residents were those who were asymptomatic at the time of testing but developed
symptoms within 7 days after testing. Residents
who did not develop symptoms in the 7 days after
testing remained classified as asymptomatic.
Laboratory Testing
The Washington State Public Health Laboratory
performed one-step real-time reverse transcriptase–polymerase chain reaction (rRT-PCR) on all
samples, using the SARS-CoV-2 CDC assay protocol; cycle threshold (Ct) values were reported
for two genetic markers: the N1 and N2 viral
nucleocapsid protein gene regions.8,9 Values below
40 cycles indicate a positive result for SARS-CoV-2.
All rRT-PCR–positive specimens from pointprevalence surveys were shipped to the CDC for
viral culture using Vero-CCL-81 cells. Cells showing cytopathic effect were used for SARS-CoV-2
rRT-PCR to confirm isolation and viral growth in
culture. Nucleic acid was extracted from rRT-PCR–
positive specimens and amplified for subsequent
sequencing (Oxford Nanopore MinION), with phylogenetic trees inferred with the neighbor-joining
method.10 Additional details on culture and sequencing methods are provided in the Supplementary Appendix.
Analyses
The daily proportions of residents with any known
positive test for SARS-CoV-2 (including those tested
as part of clinical management) were described
according to their unit in the facility. The daily
growth rate for the facility was estimated through
regression analysis, using the log-transformed
daily cumulative counts of all residents who were
positive for SARS-CoV-2 from March 3 through
March 20; doubling time was estimated by dividing the natural logarithm of 2 by the growth
rate. Similarly, doubling time was estimated for
all residents of King County, using case count
data reported through the PHSKC Covid-19 data
dashboard.11
All analyses were completed with SAS software,
version 9.4 (SAS Institute). Data were collected as
part of public health response and were deemed
non–human subjects research by the CDC.
Results
Residents
Of the 89 residents who lived in Facility A when
the first resident with confirmed Covid-19 was
tested, 57 (64%) had tested positive for SARSCoV-2 either during the point-prevalence surveys,
clinical Assessment, or postmortem examination
as of March 26. Seventy-six residents participated in the first point-prevalence survey on March
13 (Fig. 1). Of these 76 residents, 48 (63%) tested
positive in either the initial or subsequent pointprevalence surveys. Demographic characteristics,
coexisting conditions, and symptoms of surveyed
residents were similar, regardless of test result
(Table 1).
Of the 48 residents who tested positive from
the surveys, 17 (35%) reported typical symptoms,
4 (8%) reported only atypical symptoms, and 27
(56%) reported no new symptoms or changes in
chronic symptoms at the time of testing (Table 1
and Table S1). Among the 27 residents classified
as asymptomatic, 15 reported no symptoms and
12 reported only stable chronic symptoms. Fifteen (56%) residents who were asymptomatic at
the time of testing had documented cognitive
impairment; similar proportions were reported in
symptomatic residents (Table S2).
In the 7 days after their positive test, 24 of the
27 asymptomatic residents (89%) had onset of
symptoms and were recategorized as presymptomatic. The median time to symptom onset was
4 days (interquartile range, 3 to 5). The most common new symptoms were fever (71%), cough
(54%), and malaise (42%) (Table S3).
The New England Journal of Medicine
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2084 n engl j med 382;22 nejm.org May 28, 2020
The new england journal o f medicine 76 Were tested on March 13
89 Residents of Facility A on March 3
6 Were hospitalized (all tested positive for SARS-CoV-2 in hospital)
1 Was discharged home
23 Were positive 1 Who previously tested positive was negative
1 Had typical symptoms
52 Were negative
49 Were retested
March 19–20
12 Were asymptomatic 9 Had typical symptoms 2 Had atypical symptoms
15 Were asymptomatic 7 Had typical symptoms
2 Were asymptomatic 13 Were pre- symptomatic
2 Had atypical
symptoms
1 Was asymptomatic 11 Were pre- symptomatic 24 Were positive 25 Were negative
82 Residents on March 13
2 Were hospitalized before testing (both were found to be positive
during hospitalization)
1 Did not have data available
3 Declined to be tested (1 found to be positive postmortem)
3 Left facility before
March 19
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Presymptomatic SARS-CoV-2 in a Nursing Facility
Cycle Threshold and Viral Culture
rRT-PCR Ct values for the N1 genetic markers for
47 residents ranged from 13.7 to 37.9; median Ct
values for the four symptom status groups were
similar (asymptomatic residents, 25.5; presymptomatic residents, 23.1; residents with atypical
symptoms, 24.2; and residents with typical symptoms, 24.8) (Fig. 2). SARS-CoV-2 growth was identified from 31 of 46 rRT-PCR–positive specimens
(Fig. 2). Viral growth was observed for specimens
obtained from 10 of 16 residents with typical
symptoms, 3 of 4 with atypical symptoms, 17 of
Table 1. Demographic Characteristics and Reported Symptoms in Residents of Facility A at the Time of Testing.*
Characteristics SARS-CoV-2 Test Results
Positive†
(N=48)
Negative‡
(N=28)
Overall
Positive result during initial facility-wide cohort testing — no. (%) 23 (48) —
Mean age (±SD) — yr 78.6±9.5 73.8±11.5
Length of stay at Facility A <90 days before testing — no. (%) 23 (48) 14 (50)
Coexisting conditions — no. (%)
Any coexisting condition 47 (98) 28 (100)
Chronic lung disease 18 (38) 8 (29)
Diabetes 18 (38) 11 (39)
Cardiovascular disease 39 (81) 17 (61)
Cerebrovascular accident 19 (40) 8 (29)
Renal disease 18 (38) 9 (32)
Received hemodialysis 3 (6) 1 (4)
Cognitive impairment 28 (58) 13 (46)
Obesity 11 (23) 6 (21)
Symptoms during the past 14 days — no. (%)
In symptomatic residents§ 21 (44) 11 (39)
At least one typical Covid-19 symptom 17 (35) 8 (29)
Only atypical Covid-19 symptoms 4 (8) 3 (11)
In asymptomatic residents 27 (56) 18 (64)
No symptoms 15 (31) 14 (50)
Only stable, chronic symptoms 12 (25) 3 (11)
* Results include all residents who were present in the facility on March 13 and assented to screening. Facility-wide cohort symptom screens and point-prevalence surveys were performed on March 13 and March 19–20, 2020.
† Residents categorized as positive include those with at least one positive test from facility-wide point-prevalence surveys on March 13 or March 19–20 and one resident who tested negative on March 13 but tested positive before March
13.
‡ Residents categorized as negative include 3 residents who had only one negative swab on March 13 and were not retested.
§ Typical symptoms include fever, cough, and shortness of breath. Atypical symptoms include chills, malaise, sore throat,
increased confusion, rhinorrhea or nasal congestion, myalgia, dizziness, headache, nausea, and diarrhea.
Figure 1 (facing page). Residents in Facility A on
March 3 through Two Point-Prevalence Surveys.
Shown are all 89 residents who lived in skilled nursing
facility A from March 3, when the first resident tested
positive for SARS-CoV-2. By March 13, the date of the
first point-prevalence survey, 82 residents remained in
the facility, and 76 were tested. By the second pointprevalence survey, 48 of the 76 residents tested in the
point-prevalence surveys had been identified as positive. Overall, 57 residents were positive as of March 26.
Cycle threshold values were available for 47 residents
who tested positive in the point-prevalence surveys on
March 13 and March 19–20.
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24 who were presymptomatic, and 1 of 3 who
remained asymptomatic.
We observed no correlation between Ct values
and the number of days from the first evidence
of typical symptoms. Ct values consistent with a
high viral load were identified among residents
who tested positive before typical symptom onset (median Ct value among 26 observations,
24.0; interquartile range, 20.4 to 28.5) and those
who tested positive 7 or more days after typical
symptom onset (median Ct value among 8 observations, 25.0; interquartile range, 21.3 to 28.2)
(Fig. 3, and Fig. S1). Viable virus was isolated from
specimens collected 6 days before to 9 days after
the first evidence of typical symptoms.
Prevalence and Transmission in the Facility
We estimated the doubling time among residents
to be 3.4 days (95% confidence interval [CI], 2.5
to 5.3) (Table S4). The doubling time for the surrounding King County was 5.5 days (95% CI, 4.8
to 6.7). As of April 3, a total of 11 of the 57 residents with SARS-CoV-2 infection identified by
March 26 had been admitted to the hospital (including 3 in intensive care) and 15 had died (mortality, 26%). The unit where presumed introduction of infection took place and where the first
resident with SARS-CoV-2 infection lived (Unit 1)
had the highest prevalence in the facility at the
end of the first point-prevalence survey. Although
other units identified SARS-CoV-2 infection in
residents later, their prevalence also continued to
increase (Fig. 4, and Fig. S4).
By the time of the first point-prevalence survey, 11 of 138 full-time staff members (8%) had
had a positive test for SARS-CoV-2. By March 26,
Figure 2. Cycle Threshold Values and Results of Viral Culture for Residents
with Positive SARS-CoV-2 Tests According to Their Symptom Status.
Shown are N1 target cycle threshold values and viral culture results for 47
residents’ first positive test for SARS-CoV-2 stratified by the resident’s
symptom status at the time of the test. One positive test was not assessed
for culture growth. Typical symptoms include fever, cough, and shortness
of breath; atypical symptoms include chills, malaise, increased confusion,
rhinorrhea or nasal congestion, myalgia, dizziness, headache, nausea, and
diarrhea.
10 15 20 25 30 35 40
Cycle Threshold Values for N1 Target
Positive culture Negative culture No culture
Typical Symptoms
(N=16)
Atypical Symptoms
(N=4)
Presymptomatic
(N=24)
Asymptomatic
(N=3)
Figure 3. Cycle Threshold Values Relative to First Evidence of Fever, Cough, or Shortness of Breath.
Shown are N1 target cycle threshold values and viral culture results for each resident’s positive tests for SARS-CoV-2
shown by day since the first evidence of fever, cough, or shortness of breath (N=55). Dates of onset of typical symptoms were known for 43 residents; 12 residents with two specimens that were positive for SARS-CoV-2 are also included. One positive test was not assessed for culture growth. The relationship between the first test and the second test for residents who had two positive tests is shown in Figure S2.
−9 −8 −7 −6 −5 −4 −3 −2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Days from First Evidence of Fever, Cough, or Shortness of Breath
Cycle Threshold Values for N1 Target
15
10
20
25
35
30
40
Positive culture Negative culture No culture
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Presymptomatic SARS-CoV-2 in a Nursing Facility
a total of 55 of the 138 (40%) had reported symptoms, 51 (37%) had been tested, and 26 (19%) had
received a positive test result. Of the 26 staff members with positive tests, 17 were nursing staff and
9 had occupations that provided services across
multiple units during their shift (therapists, environmental services, dietary services). No staff
members with Covid-19 were hospitalized.
Thirty-nine specimens from 34 residents were
sequenced. All sequences were identical or highly similar to sequences reported in previous analyses of Covid-19 cases in Washington (Fig. S3). Of
the 34 residents whose specimens were sequenced,
27 (79%) had sequences that fit into two clusters with one nucleotide difference (Fig. S4 and
Table S5).
Discussion
Twenty-three days after identifying the first resident with SARS-CoV-2 infection, Facility A had a
64% prevalence of Covid-19 among residents, with
a case fatality rate of 26% despite early adoption of
infection-control measures. In addition, Covid-19
was diagnosed in 26 members of the staff (19%).
These findings are strikingly similar to descriptions of the first Covid-19 outbreak in a U.S. skilled
nursing facility, which occurred in the same
county at nearly the same time.2
In the investigation reported here, more than half of the residents
with positive tests were asymptomatic at the time
of testing. Transmission from asymptomatic residents infected with SARS-CoV-2 most likely
contributed to the rapid and extensive spread of
infection to other residents and staff. Symptombased infection-control strategies were not sufficient to prevent transmission after the introduction of SARS-CoV-2 into this skilled nursing
facility.
Although we are unable to quantify the contributions of asymptomatic and presymptomatic
residents to transmission of SARS-CoV-2 in this
facility, evidence suggests that these residents
had the potential for substantial viral shedding.
Figure 4. Timeline Showing Prevalence, Notable Events, and Implementation of Infection Prevention and Control Measures at Facility A.
Dashed lines indicate the prevalence of Covid-19 based on test results obtained during clinical Assessment of symptomatic residents before a unit-wide or facility-wide point-prevalence survey (PPS); the dotted line indicates the prevalence based on results from a unit-specific point-prevalence survey; and solid lines indicate the prevalence based on results from clinical Assessment and a facility-wide pointprevalence survey. PPE denotes personal protective equipment. Percentage of Residents Positive for SARS-CoV-2
100
80
90
70
60
40
30
10
50
20
0
Feb. 25
Feb. 26
Feb. 27
Feb. 28
Feb. 29
March 1
March 2
March 3
March 4
March 5
March 6
March 7
March 8
March 9
March 10
March 11
March 12
March 13
March 14
March 15
March 16
March 17
March 18
March 19
March 20
Unit 1 Unit 2 Unit 3 Unit 4 Total
Suspected introduction
of SARS-CoV-2 from
symptomatic health care
personnel in Unit 1.
Temperature and
Covid-19 symptom
screening implemented
for all residents and
staff members.
Unit-wide testing
in Unit 1.
Covid-19–recommended
PPE implemented for
all of Unit 1.
Notification of PPS
test results.
Covid-19–recommended PPE implemented in all units.
Notification of first positive
test result in resident.
Covid-19–recommended
PPE implemented for
symptomatic residents.
Communal events canceled
and visitors restricted.
Initial facilitywide pointprevalence
survey. Follow-up
pointprevalence
survey.
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Ct values indicating large quantities of viral
RNA were identified, and viable SARS-CoV-2 was
isolated from specimens of asymptomatic and
presymptomatic residents. Evidence of transmission from presymptomatic persons has been
shown in epidemiologic investigations of SARSCoV-2.12-14
We estimated that the doubling time in this
facility was 3.4 days, which is faster than that of
the surrounding community, 5.5 days. The accelerated doubling time was likely to have been
due to inadequately controlled intrafacility transmission, which sequencing and spatiotemporal
data suggest was the primary driver of new infections. Shedding of high viral titers from the
respiratory tract, including shedding before the
onset of symptoms, might have led to droplet and
possibly aerosol transmission. Residents and staff
members with undetected SARS-CoV-2 infection
are likely to have contributed to transmission
through interactions between and among residents and staff. The contribution of indirect contact transmission in this outbreak is not known.
However, contaminated environmental surfaces
and shared medical devices could also have
played a role. Most of the early transmission appeared to have occurred in Unit 1, where the initial introduction of SARS-CoV-2 took place, several days before other units were involved. Early
recognition of initial SARS-CoV-2 introduction
combined with early interventions in all units
might prevent spread within a facility.
The CDC and PHSKC confirmed Covid-19
infection in 26 symptomatic staff members associated with this skilled nursing facility as of
March 26; these staff members most likely contributed to intrafacility transmission. A concurrent study of King County health care personnel
with Covid-19 showed that 65% worked while
symptomatic and that 17% of symptomatic
health care personnel initially had mild, nonspecific symptoms and no fever, cough, shortness
of breath, or sore throat.15 The potential for viral
shedding from staff members with SARS-CoV-2
infection during either the presymptomatic or
the mildly symptomatic phase of the illness reinforces current recommendations for expanded
symptom screening for health care personnel
and universal use of face masks for all health
care staff in long-term care facilities.5
Current interventions for preventing SARSCoV-2 transmission in health care settings rely
primarily on the presence of signs and symptoms to identify and isolate residents and staff
who might have Covid-19. The data presented
here suggest that sole reliance on symptombased strategies may not be effective to prevent
introduction of SARS-CoV-2 and further transmission in skilled nursing facilities. Impaired
immune responses associated with aging and
the high prevalence of underlying conditions,
such as cognitive impairment and chronic cough,
make it difficult to recognize early signs and
symptoms of respiratory viral infections in this
population.16 Studies have shown that in the elderly, including those living in skilled nursing
facilities, influenza often manifests with few or
atypical symptoms, delaying diagnosis and contributing to transmission.17,18 Furthermore, symptom-based cohorting strategies could inadvertently increase the risk of SARS-CoV-2 exposure
for uninfected residents, given that typical symptoms were common in those who tested negative.
Our investigation demonstrated a poor correlation between symptom onset and viral shedding that was potentially due to the difficulty of
ascertaining precise dates of symptom onset or
to differences in viral shedding in this population.
Studies in other populations show that SARSCoV-2 shedding is highest early in the illness.19,20
Our investigation shows that some facility residents shed virus for more than 7 days after
symptom onset, a finding seen in some other
populations.21 These data support current recommendations preferring a test-based strategy
to discontinue transmission-based precautions for
residents of skilled nursing facilities.22 If a non–
test-based strategy is used, these data support
extending the duration of transmission-based
precautions.22
Because asymptomatic or presymptomatic
residents might play an important role in transmission in this high-risk population, additional
prevention measures merit consideration, including using testing to guide the use of transmission-based precautions, isolation, and cohorting strategies. The ability to test large numbers of
residents and staff with rapid turn-around times
may expedite cohorting of residents and staff in
locations designated for the care of those with
SARS-CoV-2 infection either in different locations
within individual facilities or in separate facilities.
This investigation has several limitations.
First, challenges in symptom ascertainment may
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Presymptomatic SARS-CoV-2 in a Nursing Facility
have resulted in misclassification of symptom
grouping for some residents. However, multiple
sources of symptom data were used to minimize
such misclassification. The accuracy of symptom
ascertainment for this investigation is likely to
be equivalent to, if not exceed, symptom screening in most skilled nursing facilities, and thus,
these findings should be generalizable to this setting. Second, because this analysis was conducted
among residents of a skilled nursing facility, it is
not known whether the findings apply to the
general population, including younger persons,
those without underlying medical conditions, or
similarly aged populations in the general community or in other long-term care settings. Third,
asymptomatic staff members were not tested;
therefore, we are unable to document their role in
transmission in this facility.
SARS-CoV-2 can spread rapidly after introduction into skilled nursing facilities, resulting in
substantial morbidity and mortality and increasing the burden on regional health care systems.
Unrecognized asymptomatic and presymptomatic
infections most likely contribute to transmission
in these settings. During the current Covid-19
pandemic, skilled nursing facilities and all longterm care facilities should take proactive steps to
prevent introduction of SARS-CoV-2. These steps
include restricting visitors and nonessential personnel from entering the building, requiring
universal use of face masks by all staff for source
control while in the facility, and implementing
strict screening of staff. Our data suggest that
symptom-based strategies for identifying residents
with SARS-CoV-2 are insufficient for preventing
transmission in skilled nursing facilities. Once
SARS-CoV-2 has been introduced, additional strategies should be implemented to prevent further
transmission, including use of recommended personal protective equipment, when available, during
all resident care activities regardless of symptoms.5
Consideration should be given to test-based strategies for identifying residents and staff with SARSCoV-2 infection for the purpose of excluding infected staff and cohorting residents, either in
designated units within a facility or in a separate
facility designated for residents with Covid-19.
The findings and conclusion in this report are those of the
authors and do not necessarily represent the official position of
the Centers for Disease Control and Prevention.
Disclosure forms provided by the authors are available with
the full text of this article at NEJM.org.
We thank the facility residents; the staff of Facility A for their
ongoing efforts to provide care in the face of these challenges;
staff at the local and state health departments responding to
this public health emergency; staff at the Washington State Department of Health Public Health Laboratories; CDC staff at the
Emergency Operations Center; and members of the Covid-19
response teams at the local, state, and national levels for their
unwavering commitment in the face of this global public health
emergency.
Appendix
The authors’ full names and academic degrees are as follows: Melissa M. Arons, R.N., Kelly M. Hatfield, M.S.P.H., Sujan C. Reddy,
M.D., Anne Kimball, M.D., Allison James, Ph.D., Jesica R. Jacobs, Ph.D., Joanne Taylor, Ph.D., Kevin Spicer, M.D., Ana C. Bardossy,
M.D., Lisa P. Oakley, Ph.D., Sukarma Tanwar, M.Med., Jonathan W. Dyal, M.D., Josh Harney, M.S., Zeshan Chisty, M.P.H., Jeneita M.
Bell, M.D., Mark Methner, Ph.D., Prabasaj Paul, Ph.D., Christina M. Carlson, Ph.D., Heather P. McLaughlin, Ph.D., Natalie Thornburg,
Ph.D., Suxiang Tong, Ph.D., Azaibi Tamin, Ph.D., Ying Tao, Ph.D., Anna Uehara, Ph.D., Jennifer Harcourt, Ph.D., Shauna Clark, R.N.,
Claire Brostrom-Smith, M.S.N., Libby C. Page, M.P.H., Meagan Kay, D.V.M., James Lewis, M.D., Patty Montgomery, M.P.H., Nimalie D.
Stone, M.D., Thomas A. Clark, M.D., Margaret A. Honein, Ph.D., Jeffrey S. Duchin, M.D., and John A. Jernigan, M.D.
The authors’ affiliations are as follows: the Centers for Disease Control and Prevention COVID-19 Emergency Response (M.M.A.,
K.M.H., S.C.R., A.K., A.J., J.R.J., J.T., K.S., A.C.B., L.P.O., S. Tanwar, J.W.D., J. Harney, Z.C., J.M.B., M.M., P.P., C.M.C., H.P.M.L.,
N.T., S. Tong, A.T., Y.T., A.U., J. Harcourt, N.D.S., T.A.C., M.A.H., J.A.J.), and the Epidemic Intelligence Service (M.M.A., A.K., A.J.,
J.T., A.C.B., L.P.O., S. Tanwar, J.W.D.) and the Laboratory Leadership Service (J.R.J., C.M.C.), Centers for Disease Control and Prevention — all in Atlanta; and Public Health — Seattle & King County (S.C., C.B.-S., L.C.P., M.K., J.L., J.S.D.) and the University of Washington, Department of Medicine (J.S.D.), Seattle, the Washington State Public Health Laboratory, Shoreline (J.S.D.), and the Washington
State Department of Health, Tumwater (P.M.) — all in Washington.
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Copyright © 2020 Massachusetts Medical Society.
receive immediate notification when an article
is published online first
To be notified by email when Journal articles
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The New England Journal of Medicine
Downloaded from nejm.org on June 21, 2020. For personal use only. No other uses without permission.
Copyright © 2020 Massachusetts Medical Society. All rights reserved.

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