The new england
\njournal of medicine
\nn engl j med 382;22 nejm.org May 28, 2020 2081
\nestablished in 1812 May 28, 2020 vol. 382 no. 22
\nThe authors\u2019 full names, academic degrees, and affiliations are listed in the Appendix. Address reprint requests to Dr.
\nJernigan at the Centers for Disease Control and Prevention, 1600 Clifton Rd.,
\nMailstop A-31, Atlanta, GA 30333, or at
\njqj9@cdc.gov.
\n*A complete list of the investigators is included in the Supplementary Appendix,
\navailable at NEJM.org.
\nMs. Arons and Ms. Hatfield contributed
\nequally to this article.
\nThis article was published on April 24,
\n2020, at NEJM.org.
\nN Engl J Med 2020;382:2081-90.
\nDOI: 10.1056\/NEJMoa2008457
\nCopyright \u00a9 2020 Massachusetts Medical Society.
\nBACKGROUND
\nSevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can spread
\nrapidly within skilled nursing facilities. After identification of a case of Covid-19
\nin a skilled nursing facility, we assessed transmission and evaluated the adequacy
\nof symptom-based screening to identify infections in residents.
\nMETHODS
\nWe conducted two serial point-prevalence surveys, 1 week apart, in which assenting
\nresidents of the facility underwent nasopharyngeal and oropharyngeal testing for
\nSARS-CoV-2, including real-time reverse-transcriptase polymerase chain reaction
\n(rRT-PCR), viral culture, and sequencing. Symptoms that had been present during
\nthe preceding 14 days were recorded. Asymptomatic residents who tested positive
\nwere reassessed 7 days later. Residents with SARS-CoV-2 infection were categorized as symptomatic with typical symptoms (fever, cough, or shortness of breath),
\nsymptomatic with only atypical symptoms, presymptomatic, or asymptomatic.
\nRESULTS
\nTwenty-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
\n48 residents, 27 (56%) were asymptomatic at the time of testing; 24 subsequently
\ndeveloped 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
\nviable virus was recovered from 17 residents. As of April 3, of the 57 residents with
\nSARS-CoV-2 infection, 11 had been hospitalized (3 in the intensive care unit) and
\n15 had died (mortality, 26%). Of the 34 residents whose specimens were sequenced,
\n27 (79%) had sequences that fit into two clusters with a difference of one nucleotide.
\nCONCLUSIONS
\nRapid and widespread transmission of SARS-CoV-2 was demonstrated in this skilled
\nnursing 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
\nto prevent transmission after SARS-CoV-2 introduction into this facility.
\nabstract
\nPresymptomatic SARS-CoV-2 Infections and Transmission
\nin a Skilled Nursing Facility
\nM.M. Arons, K.M. Hatfield, S.C. Reddy, A. Kimball, A. James, J.R. Jacobs, J. Taylor, K. Spicer, A.C. Bardossy,
\nL.P. Oakley, S. Tanwar, J.W. Dyal, J. Harney, Z. Chisty, J.M. Bell, M. Methner, P. Paul, C.M. Carlson,
\nH.P. McLaughlin, N. Thornburg, S. Tong, A. Tamin, Y. Tao, A. Uehara, J. Harcourt, S. Clark, C. Brostrom-Smith,
\nL.C. Page, M. Kay, J. Lewis, P. Montgomery, N.D. Stone, T.A. Clark, M.A. Honein, J.S. Duchin, and J.A. Jernigan,
\nfor the Public Health\u2013Seattle and King County and CDC COVID-19 Investigation Team*
\nThe New England Journal of Medicine
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\nCopyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\n2082 n engl j med 382;22 nejm.org May 28, 2020
\nThe new england journal o f medicine
\nThe first reported case of coronavirus disease 2019 (Covid-19) in the United
\nStates was diagnosed in a resident of Snohomish County, Washington, on January 20, 2020.1
\nIn late February, an outbreak was identified in a
\nskilled nursing facility in neighboring King County; morbidity and mortality among residents were
\nhigh, straining the regional health care system.2,3
\nWe report another outbreak of Covid-19 in a
\nseparate skilled nursing facility in the same county.
\nIn the course of this outbreak investigation, Public
\nHealth\u2013Seattle and King County (PHSKC) and the
\nCenters for Disease Control and Prevention (CDC)
\nidentified residents with asymptomatic SARSCoV-2 infection, which prompted further investigation. We performed serial point-prevalence surveys to assess the extent of transmission and to
\nevaluate the adequacy of symptom-based screening
\nof residents to identify infections. Initial findings
\nof this investigation were previously reported.4
\nDescription of the Outbreak
\nOn February 29, 2020, in response to increased
\nlocal awareness of Covid-19 in King County,
\nWashington, administrative leadership at Facility
\nA instituted enhanced infection-control measures.
\nNursing staff assessed residents twice daily for
\npossible signs and symptoms of Covid-19, including fever (oral or temporal temperature measurement), cough, shortness of breath, and other
\nsymptoms. Health care personnel were assessed
\nat the start of each shift with oral temperature
\nmeasurement and screening for symptoms, including cough, shortness of breath, sore throat,
\nor any other respiratory symptoms.
\nOn March 1, one member of the health care
\nstaff tested positive for SARS-CoV-2 after having
\nworked in a single unit (Unit 1) while symptomatic on February 26, the first day of symptoms,
\nand on February 28. On March 5, the facility was
\ninformed that a hospitalized resident of Unit 1
\n(in whom symptoms had developed on March 2
\nand testing was done on March 3) had been diagnosed with Covid-19. Subsequently, all visitors
\nwere restricted and communal activities were canceled. PHSKC and the CDC initiated an outbreak
\ninvestigation, and on March 6, provided on-site
\ninfection prevention and control recommendations, including the recommendation that all
\nhealth care staff entering symptomatic residents\u2019
\nrooms wear eye protection, a gown, gloves, and
\na face mask (N95 respirators were not routinely
\navailable).5
\nOn March 8, the CDC and PHSKC
\noffered testing to all residents in Unit 1; 13 of
\n15 residents present were tested for SARS-CoV-2
\n(2 residents declined). A total of 6 residents tested
\npositive; of these, 4 had symptoms (e.g., fever,
\ncough, shortness of breath, or sore throat) and
\n2 had been asymptomatic during the preceding
\n14 days. On March 9, the facility implemented
\nCovid-19 transmission-based precautions for all
\nresidents of Unit 1, regardless of symptoms or
\ninfection status.
\nMethods
\nStudy Population
\nFacility A is a 116-bed skilled nursing facility divided into four separate units with an equal mix of
\nshort- and long-term residents in each unit. There
\nwere 89 residents present at Facility A on March 3,
\nthe 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
\ntests obtained during postmortem examination or
\nby outside health care providers during clinical
\nAssessment of symptomatic residents and staff were
\nprovided to the CDC and PHSKC through March
\n26. All symptomatic health care personnel were
\nadvised to be tested by their health care provider;
\nasymptomatic staff members were not tested as
\npart of this investigation.
\nPoint-Prevalence Surveys
\nOn two occasions, residents in the facility were
\noffered SARS-CoV-2 testing as part of a facilitywide point-prevalence survey. The first survey was
\nperformed for all assenting residents, including
\nthose who had previously tested positive, on March
\n13 (10 days after the first resident had tested
\npositive for SARS-CoV-2). Nasopharyngeal and
\noropharyngeal swabs were collected in accordance
\nwith CDC guidelines.6
\nA second survey was conducted 7 days later (March 19\u201320) for residents
\nwho had had either a negative test result or a
\npositive result with atypical or no symptoms reported in the first survey.
\nSymptom Assessment
\nOn the day of point-prevalence surveys, a standardized symptom-assessment form was completed by
\nnurses for each resident tested. Symptoms present during the preceding 14 days were recorded on
\nThe New England Journal of Medicine
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\nCopyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\nn engl j med 382;22 nejm.org May 28, 2020 2083
\nPresymptomatic SARS-CoV-2 in a Nursing Facility
\nthe basis of interview and review of medical records. Asymptomatic residents with a positive test
\nresult were reassessed for symptoms 7 days later.
\nFor additional details on symptom assessment,
\nsee the Supplementary Appendix, available with
\nthe full text of this article at NEJM.org.
\nResidents were classified as symptomatic if
\nthey had had at least one new or worsened typical or atypical symptom of Covid-19 in the preceding 14 days. Residents with subjective fever
\nor temperature greater than 100.0\u00b0F (37.8\u00b0C),
\ncough, or shortness of breath were classified as
\nsymptomatic with typical symptoms.7
\nResidents
\nwere classified as symptomatic with atypical symptoms if their symptoms included only chills, malaise, increased confusion, rhinorrhea, nasal congestion, sore throat, myalgia, dizziness, headache,
\nnausea, or diarrhea.
\nAsymptomatic residents were those who had
\nno symptoms or only stable chronic symptoms
\n(e.g., chronic cough without worsening). Presymptomatic residents were those who were asymptomatic at the time of testing but developed
\nsymptoms within 7 days after testing. Residents
\nwho did not develop symptoms in the 7 days after
\ntesting remained classified as asymptomatic.
\nLaboratory Testing
\nThe Washington State Public Health Laboratory
\nperformed one-step real-time reverse transcriptase\u2013polymerase chain reaction (rRT-PCR) on all
\nsamples, using the SARS-CoV-2 CDC assay protocol; cycle threshold (Ct) values were reported
\nfor two genetic markers: the N1 and N2 viral
\nnucleocapsid protein gene regions.8,9 Values below
\n40 cycles indicate a positive result for SARS-CoV-2.
\nAll rRT-PCR\u2013positive specimens from pointprevalence surveys were shipped to the CDC for
\nviral culture using Vero-CCL-81 cells. Cells showing cytopathic effect were used for SARS-CoV-2
\nrRT-PCR to confirm isolation and viral growth in
\nculture. Nucleic acid was extracted from rRT-PCR\u2013
\npositive specimens and amplified for subsequent
\nsequencing (Oxford Nanopore MinION), with phylogenetic trees inferred with the neighbor-joining
\nmethod.10 Additional details on culture and sequencing methods are provided in the Supplementary Appendix.
\nAnalyses
\nThe daily proportions of residents with any known
\npositive test for SARS-CoV-2 (including those tested
\nas part of clinical management) were described
\naccording to their unit in the facility. The daily
\ngrowth rate for the facility was estimated through
\nregression analysis, using the log-transformed
\ndaily cumulative counts of all residents who were
\npositive for SARS-CoV-2 from March 3 through
\nMarch 20; doubling time was estimated by dividing the natural logarithm of 2 by the growth
\nrate. Similarly, doubling time was estimated for
\nall residents of King County, using case count
\ndata reported through the PHSKC Covid-19 data
\ndashboard.11
\nAll analyses were completed with SAS software,
\nversion 9.4 (SAS Institute). Data were collected as
\npart of public health response and were deemed
\nnon\u2013human subjects research by the CDC.
\nResults
\nResidents
\nOf the 89 residents who lived in Facility A when
\nthe first resident with confirmed Covid-19 was
\ntested, 57 (64%) had tested positive for SARSCoV-2 either during the point-prevalence surveys,
\nclinical Assessment, or postmortem examination
\nas of March 26. Seventy-six residents participated in the first point-prevalence survey on March
\n13 (Fig. 1). Of these 76 residents, 48 (63%) tested
\npositive in either the initial or subsequent pointprevalence surveys. Demographic characteristics,
\ncoexisting conditions, and symptoms of surveyed
\nresidents were similar, regardless of test result
\n(Table 1).
\nOf the 48 residents who tested positive from
\nthe surveys, 17 (35%) reported typical symptoms,
\n4 (8%) reported only atypical symptoms, and 27
\n(56%) reported no new symptoms or changes in
\nchronic symptoms at the time of testing (Table 1
\nand Table S1). Among the 27 residents classified
\nas asymptomatic, 15 reported no symptoms and
\n12 reported only stable chronic symptoms. Fifteen (56%) residents who were asymptomatic at
\nthe time of testing had documented cognitive
\nimpairment; similar proportions were reported in
\nsymptomatic residents (Table S2).
\nIn the 7 days after their positive test, 24 of the
\n27 asymptomatic residents (89%) had onset of
\nsymptoms and were recategorized as presymptomatic. The median time to symptom onset was
\n4 days (interquartile range, 3 to 5). The most common new symptoms were fever (71%), cough
\n(54%), and malaise (42%) (Table S3).
\nThe New England Journal of Medicine
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\nCopyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\n2084 n engl j med 382;22 nejm.org May 28, 2020
\nThe new england journal o f medicine 76 Were tested on March 13
\n89 Residents of Facility A on March 3
\n6 Were hospitalized (all tested positive for SARS-CoV-2 in hospital)
\n1 Was discharged home
\n23 Were positive 1 Who previously tested positive was negative
\n1 Had typical symptoms
\n52 Were negative
\n49 Were retested
\nMarch 19\u201320
\n12 Were asymptomatic 9 Had typical symptoms 2 Had atypical symptoms
\n15 Were asymptomatic 7 Had typical symptoms
\n2 Were asymptomatic 13 Were pre- symptomatic
\n2 Had atypical
\nsymptoms
\n1 Was asymptomatic 11 Were pre- symptomatic 24 Were positive 25 Were negative
\n82 Residents on March 13
\n2 Were hospitalized before testing (both were found to be positive
\nduring hospitalization)
\n1 Did not have data available
\n3 Declined to be tested (1 found to be positive postmortem)
\n3 Left facility before
\nMarch 19
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\nCopyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\nn engl j med 382;22 nejm.org May 28, 2020 2085
\nPresymptomatic SARS-CoV-2 in a Nursing Facility
\nCycle Threshold and Viral Culture
\nrRT-PCR Ct values for the N1 genetic markers for
\n47 residents ranged from 13.7 to 37.9; median Ct
\nvalues for the four symptom status groups were
\nsimilar (asymptomatic residents, 25.5; presymptomatic residents, 23.1; residents with atypical
\nsymptoms, 24.2; and residents with typical symptoms, 24.8) (Fig. 2). SARS-CoV-2 growth was identified from 31 of 46 rRT-PCR\u2013positive specimens
\n(Fig. 2). Viral growth was observed for specimens
\nobtained from 10 of 16 residents with typical
\nsymptoms, 3 of 4 with atypical symptoms, 17 of
\nTable 1. Demographic Characteristics and Reported Symptoms in Residents of Facility A at the Time of Testing.*
\nCharacteristics SARS-CoV-2 Test Results
\nPositive\u2020
\n(N=48)
\nNegative\u2021
\n(N=28)
\nOverall
\nPositive result during initial facility-wide cohort testing \u2014 no. (%) 23 (48) \u2014
\nMean age (\u00b1SD) \u2014 yr 78.6\u00b19.5 73.8\u00b111.5
\nLength of stay at Facility A <90 days before testing \u2014 no. (%) 23 (48) 14 (50)
\nCoexisting conditions \u2014 no. (%)
\nAny coexisting condition 47 (98) 28 (100)
\nChronic lung disease 18 (38) 8 (29)
\nDiabetes 18 (38) 11 (39)
\nCardiovascular disease 39 (81) 17 (61)
\nCerebrovascular accident 19 (40) 8 (29)
\nRenal disease 18 (38) 9 (32)
\nReceived hemodialysis 3 (6) 1 (4)
\nCognitive impairment 28 (58) 13 (46)
\nObesity 11 (23) 6 (21)
\nSymptoms during the past 14 days \u2014 no. (%)
\nIn symptomatic residents\u00a7 21 (44) 11 (39)
\nAt least one typical Covid-19 symptom 17 (35) 8 (29)
\nOnly atypical Covid-19 symptoms 4 (8) 3 (11)
\nIn asymptomatic residents 27 (56) 18 (64)
\nNo symptoms 15 (31) 14 (50)
\nOnly stable, chronic symptoms 12 (25) 3 (11)
\n* 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\u201320, 2020.
\n\u2020 Residents categorized as positive include those with at least one positive test from facility-wide point-prevalence surveys on March 13 or March 19\u201320 and one resident who tested negative on March 13 but tested positive before March
\n13.
\n\u2021 Residents categorized as negative include 3 residents who had only one negative swab on March 13 and were not retested.
\n\u00a7 Typical symptoms include fever, cough, and shortness of breath. Atypical symptoms include chills, malaise, sore throat,
\nincreased confusion, rhinorrhea or nasal congestion, myalgia, dizziness, headache, nausea, and diarrhea.
\nFigure 1 (facing page). Residents in Facility A on
\nMarch 3 through Two Point-Prevalence Surveys.
\nShown are all 89 residents who lived in skilled nursing
\nfacility A from March 3, when the first resident tested
\npositive for SARS-CoV-2. By March 13, the date of the
\nfirst point-prevalence survey, 82 residents remained in
\nthe facility, and 76 were tested. By the second pointprevalence survey, 48 of the 76 residents tested in the
\npoint-prevalence surveys had been identified as positive. Overall, 57 residents were positive as of March 26.
\nCycle threshold values were available for 47 residents
\nwho tested positive in the point-prevalence surveys on
\nMarch 13 and March 19\u201320.
\nThe New England Journal of Medicine
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\n Copyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\n2086 n engl j med 382;22 nejm.org May 28, 2020
\nThe new england journal o f medicine
\n24 who were presymptomatic, and 1 of 3 who
\nremained asymptomatic.
\nWe observed no correlation between Ct values
\nand the number of days from the first evidence
\nof typical symptoms. Ct values consistent with a
\nhigh viral load were identified among residents
\nwho tested positive before typical symptom onset (median Ct value among 26 observations,
\n24.0; interquartile range, 20.4 to 28.5) and those
\nwho tested positive 7 or more days after typical
\nsymptom onset (median Ct value among 8 observations, 25.0; interquartile range, 21.3 to 28.2)
\n(Fig. 3, and Fig. S1). Viable virus was isolated from
\nspecimens collected 6 days before to 9 days after
\nthe first evidence of typical symptoms.
\n Prevalence and Transmission in the Facility
\nWe estimated the doubling time among residents
\nto be 3.4 days (95% confidence interval [CI], 2.5
\nto 5.3) (Table S4). The doubling time for the surrounding King County was 5.5 days (95% CI, 4.8
\nto 6.7). As of April 3, a total of 11 of the 57 residents with SARS-CoV-2 infection identified by
\nMarch 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
\nresident with SARS-CoV-2 infection lived (Unit 1)
\nhad the highest prevalence in the facility at the
\nend of the first point-prevalence survey. Although
\nother units identified SARS-CoV-2 infection in
\nresidents later, their prevalence also continued to
\nincrease (Fig. 4, and Fig. S4).
\nBy the time of the first point-prevalence survey, 11 of 138 full-time staff members (8%) had
\nhad a positive test for SARS-CoV-2. By March 26,
\nFigure 2. Cycle Threshold Values and Results of Viral Culture for Residents
\nwith Positive SARS-CoV-2 Tests According to Their Symptom Status.
\nShown are N1 target cycle threshold values and viral culture results for 47
\nresidents\u2019 first positive test for SARS-CoV-2 stratified by the resident\u2019s
\nsymptom status at the time of the test. One positive test was not assessed
\nfor culture growth. Typical symptoms include fever, cough, and shortness
\nof breath; atypical symptoms include chills, malaise, increased confusion,
\nrhinorrhea or nasal congestion, myalgia, dizziness, headache, nausea, and
\ndiarrhea.
\n10 15 20 25 30 35 40
\nCycle Threshold Values for N1 Target
\nPositive culture Negative culture No culture
\nTypical Symptoms
\n(N=16)
\nAtypical Symptoms
\n(N=4)
\nPresymptomatic
\n(N=24)
\nAsymptomatic
\n(N=3)
\nFigure 3. Cycle Threshold Values Relative to First Evidence of Fever, Cough, or Shortness of Breath.
\nShown are N1 target cycle threshold values and viral culture results for each resident\u2019s positive tests for SARS-CoV-2
\nshown 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.
\n\u22129 \u22128 \u22127 \u22126 \u22125 \u22124 \u22123 \u22122 \u22121 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
\nDays from First Evidence of Fever, Cough, or Shortness of Breath
\nCycle Threshold Values for N1 Target
\n15
\n10
\n20
\n25
\n35
\n30
\n40
\nPositive culture Negative culture No culture
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\nn engl j med 382;22 nejm.org May 28, 2020 2087
\nPresymptomatic SARS-CoV-2 in a Nursing Facility
\na total of 55 of the 138 (40%) had reported symptoms, 51 (37%) had been tested, and 26 (19%) had
\nreceived a positive test result. Of the 26 staff members with positive tests, 17 were nursing staff and
\n9 had occupations that provided services across
\nmultiple units during their shift (therapists, environmental services, dietary services). No staff
\nmembers with Covid-19 were hospitalized.
\nThirty-nine specimens from 34 residents were
\nsequenced. All sequences were identical or highly similar to sequences reported in previous analyses of Covid-19 cases in Washington (Fig. S3). Of
\nthe 34 residents whose specimens were sequenced,
\n27 (79%) had sequences that fit into two clusters with one nucleotide difference (Fig. S4 and
\nTable S5).
\nDiscussion
\nTwenty-three days after identifying the first resident with SARS-CoV-2 infection, Facility A had a
\n64% prevalence of Covid-19 among residents, with
\na case fatality rate of 26% despite early adoption of
\ninfection-control measures. In addition, Covid-19
\nwas diagnosed in 26 members of the staff (19%).
\nThese findings are strikingly similar to descriptions of the first Covid-19 outbreak in a U.S. skilled
\nnursing facility, which occurred in the same
\ncounty at nearly the same time.2
\n In the investigation reported here, more than half of the residents
\nwith positive tests were asymptomatic at the time
\nof testing. Transmission from asymptomatic residents infected with SARS-CoV-2 most likely
\ncontributed to the rapid and extensive spread of
\ninfection 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
\nfacility.
\nAlthough we are unable to quantify the contributions of asymptomatic and presymptomatic
\nresidents to transmission of SARS-CoV-2 in this
\nfacility, evidence suggests that these residents
\nhad the potential for substantial viral shedding.
\nFigure 4. Timeline Showing Prevalence, Notable Events, and Implementation of Infection Prevention and Control Measures at Facility A.
\nDashed 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
\n100
\n80
\n90
\n70
\n60
\n40
\n30
\n10
\n50
\n20
\n0
\nFeb. 25
\nFeb. 26
\nFeb. 27
\nFeb. 28
\nFeb. 29
\nMarch 1
\nMarch 2
\nMarch 3
\nMarch 4
\nMarch 5
\nMarch 6
\nMarch 7
\nMarch 8
\nMarch 9
\nMarch 10
\nMarch 11
\nMarch 12
\nMarch 13
\nMarch 14
\nMarch 15
\nMarch 16
\nMarch 17
\nMarch 18
\nMarch 19
\nMarch 20
\nUnit 1 Unit 2 Unit 3 Unit 4 Total
\nSuspected introduction
\nof SARS-CoV-2 from
\nsymptomatic health care
\npersonnel in Unit 1.
\nTemperature and
\nCovid-19 symptom
\nscreening implemented
\nfor all residents and
\nstaff members.
\nUnit-wide testing
\nin Unit 1.
\nCovid-19\u2013recommended
\nPPE implemented for
\nall of Unit 1.
\nNotification of PPS
\ntest results.
\nCovid-19\u2013recommended PPE implemented in all units.
\nNotification of first positive
\ntest result in resident.
\nCovid-19\u2013recommended
\nPPE implemented for
\nsymptomatic residents.
\nCommunal events canceled
\nand visitors restricted.
\nInitial facilitywide pointprevalence
\nsurvey. Follow-up
\npointprevalence
\nsurvey.
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\n2088 n engl j med 382;22 nejm.org May 28, 2020
\nThe new england journal o f medicine
\nCt values indicating large quantities of viral
\nRNA were identified, and viable SARS-CoV-2 was
\nisolated from specimens of asymptomatic and
\npresymptomatic residents. Evidence of transmission from presymptomatic persons has been
\nshown in epidemiologic investigations of SARSCoV-2.12-14
\nWe estimated that the doubling time in this
\nfacility was 3.4 days, which is faster than that of
\nthe surrounding community, 5.5 days. The accelerated doubling time was likely to have been
\ndue to inadequately controlled intrafacility transmission, which sequencing and spatiotemporal
\ndata suggest was the primary driver of new infections. Shedding of high viral titers from the
\nrespiratory tract, including shedding before the
\nonset of symptoms, might have led to droplet and
\npossibly aerosol transmission. Residents and staff
\nmembers with undetected SARS-CoV-2 infection
\nare likely to have contributed to transmission
\nthrough interactions between and among residents and staff. The contribution of indirect contact transmission in this outbreak is not known.
\nHowever, contaminated environmental surfaces
\nand shared medical devices could also have
\nplayed 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
\nrecognition of initial SARS-CoV-2 introduction
\ncombined with early interventions in all units
\nmight prevent spread within a facility.
\nThe CDC and PHSKC confirmed Covid-19
\ninfection in 26 symptomatic staff members associated with this skilled nursing facility as of
\nMarch 26; these staff members most likely contributed to intrafacility transmission. A concurrent study of King County health care personnel
\nwith Covid-19 showed that 65% worked while
\nsymptomatic and that 17% of symptomatic
\nhealth care personnel initially had mild, nonspecific symptoms and no fever, cough, shortness
\nof breath, or sore throat.15 The potential for viral
\nshedding from staff members with SARS-CoV-2
\ninfection during either the presymptomatic or
\nthe mildly symptomatic phase of the illness reinforces current recommendations for expanded
\nsymptom screening for health care personnel
\nand universal use of face masks for all health
\ncare staff in long-term care facilities.5
\nCurrent interventions for preventing SARSCoV-2 transmission in health care settings rely
\nprimarily on the presence of signs and symptoms to identify and isolate residents and staff
\nwho might have Covid-19. The data presented
\nhere suggest that sole reliance on symptombased strategies may not be effective to prevent
\nintroduction of SARS-CoV-2 and further transmission in skilled nursing facilities. Impaired
\nimmune responses associated with aging and
\nthe high prevalence of underlying conditions,
\nsuch as cognitive impairment and chronic cough,
\nmake it difficult to recognize early signs and
\nsymptoms of respiratory viral infections in this
\npopulation.16 Studies have shown that in the elderly, including those living in skilled nursing
\nfacilities, influenza often manifests with few or
\natypical symptoms, delaying diagnosis and contributing to transmission.17,18 Furthermore, symptom-based cohorting strategies could inadvertently increase the risk of SARS-CoV-2 exposure
\nfor uninfected residents, given that typical symptoms were common in those who tested negative.
\nOur investigation demonstrated a poor correlation between symptom onset and viral shedding that was potentially due to the difficulty of
\nascertaining precise dates of symptom onset or
\nto differences in viral shedding in this population.
\nStudies in other populations show that SARSCoV-2 shedding is highest early in the illness.19,20
\nOur investigation shows that some facility residents shed virus for more than 7 days after
\nsymptom onset, a finding seen in some other
\npopulations.21 These data support current recommendations preferring a test-based strategy
\nto discontinue transmission-based precautions for
\nresidents of skilled nursing facilities.22 If a non\u2013
\ntest-based strategy is used, these data support
\nextending the duration of transmission-based
\nprecautions.22
\nBecause asymptomatic or presymptomatic
\nresidents might play an important role in transmission in this high-risk population, additional
\nprevention 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
\nresidents and staff with rapid turn-around times
\nmay expedite cohorting of residents and staff in
\nlocations designated for the care of those with
\nSARS-CoV-2 infection either in different locations
\nwithin individual facilities or in separate facilities.
\nThis investigation has several limitations.
\nFirst, challenges in symptom ascertainment may
\nThe New England Journal of Medicine
\nDownloaded from nejm.org on June 21, 2020. For personal use only. No other uses without permission.
\n Copyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.
\nn engl j med 382;22 nejm.org May 28, 2020 2089
\nPresymptomatic SARS-CoV-2 in a Nursing Facility
\nhave resulted in misclassification of symptom
\ngrouping for some residents. However, multiple
\nsources of symptom data were used to minimize
\nsuch misclassification. The accuracy of symptom
\nascertainment for this investigation is likely to
\nbe equivalent to, if not exceed, symptom screening in most skilled nursing facilities, and thus,
\nthese findings should be generalizable to this setting. Second, because this analysis was conducted
\namong residents of a skilled nursing facility, it is
\nnot known whether the findings apply to the
\ngeneral population, including younger persons,
\nthose without underlying medical conditions, or
\nsimilarly aged populations in the general community or in other long-term care settings. Third,
\nasymptomatic staff members were not tested;
\ntherefore, we are unable to document their role in
\ntransmission in this facility.
\nSARS-CoV-2 can spread rapidly after introduction into skilled nursing facilities, resulting in
\nsubstantial morbidity and mortality and increasing the burden on regional health care systems.
\nUnrecognized asymptomatic and presymptomatic
\ninfections most likely contribute to transmission
\nin these settings. During the current Covid-19
\npandemic, skilled nursing facilities and all longterm care facilities should take proactive steps to
\nprevent introduction of SARS-CoV-2. These steps
\ninclude restricting visitors and nonessential personnel from entering the building, requiring
\nuniversal use of face masks by all staff for source
\ncontrol while in the facility, and implementing
\nstrict screening of staff. Our data suggest that
\nsymptom-based strategies for identifying residents
\nwith SARS-CoV-2 are insufficient for preventing
\ntransmission in skilled nursing facilities. Once
\nSARS-CoV-2 has been introduced, additional strategies should be implemented to prevent further
\ntransmission, including use of recommended personal protective equipment, when available, during
\nall resident care activities regardless of symptoms.5
\nConsideration 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
\ndesignated units within a facility or in a separate
\nfacility designated for residents with Covid-19.
\nThe findings and conclusion in this report are those of the
\nauthors and do not necessarily represent the official position of
\nthe Centers for Disease Control and Prevention.
\nDisclosure forms provided by the authors are available with
\nthe full text of this article at NEJM.org.
\nWe thank the facility residents; the staff of Facility A for their
\nongoing efforts to provide care in the face of these challenges;
\nstaff at the local and state health departments responding to
\nthis public health emergency; staff at the Washington State Department of Health Public Health Laboratories; CDC staff at the
\nEmergency Operations Center; and members of the Covid-19
\nresponse teams at the local, state, and national levels for their
\nunwavering commitment in the face of this global public health
\nemergency.
\nAppendix
\nThe authors\u2019 full names and academic degrees are as follows: Melissa M. Arons, R.N., Kelly M. Hatfield, M.S.P.H., Sujan C. Reddy,
\nM.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,
\nM.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.
\nBell, M.D., Mark Methner, Ph.D., Prabasaj Paul, Ph.D., Christina M. Carlson, Ph.D., Heather P. McLaughlin, Ph.D., Natalie Thornburg,
\nPh.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.,
\nClaire 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.
\nStone, M.D., Thomas A. Clark, M.D., Margaret A. Honein, Ph.D., Jeffrey S. Duchin, M.D., and John A. Jernigan, M.D.
\nThe authors\u2019 affiliations are as follows: the Centers for Disease Control and Prevention COVID-19 Emergency Response (M.M.A.,
\nK.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.,
\nN.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.,
\nJ.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 \u2014 all in Atlanta; and Public Health \u2014 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
\nState Department of Health, Tumwater (P.M.) \u2014 all in Washington.
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\nCopyright \u00a9 2020 Massachusetts Medical Society.
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\n Copyright \u00a9 2020 Massachusetts Medical Society. All rights reserved.<\/p>\n","protected":false},"excerpt":{"rendered":"
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