In a US study, they looked at two nursing homes in Washington state in early March.
A "facility-wide testing identified a 30.3% prevalence of infection among residents, indicating very rapid spread, despite early adoption of infection prevention and control measures. Approximately half of all residents with positive test results did not have any symptoms at the time of testing, suggesting that transmission from asymptomatic and presymptomatic residents, who were not recognized as having SARS-CoV-2 infection and therefore not isolated, might have contributed to further spread. Similarly, studies have shown that influenza in the elderly, including those living in SNFs, often manifests as few or atypical symptoms, delaying diagnosis and contributing to transmission (6–8). "
Another study in Singapore was posted. "Investigation of COVID-19 cases in Singapore identified seven clusters (clusters A–G) in which presymptomatic transmission likely occurred. These clusters occurred during January 19–March 12, and involved from two to five patients each (Figure). Ten of the cases within these clusters were attributed to presymptomatic transmission and accounted for 6.4% of the 157 locally acquired cases reported as of March 16."
This enforces the need for social distancing, handwashing, and frequent cleaning, but also tracing personal contact with people who are ill. As in this case with the nursing home, social distancing can be an issue in addition to having a population that is high at risk.
One interesting note sited in the MMWR report - "Speech and other vocal activities such as singing have been shown to generate air particles, with the rate of emission corresponding to voice loudness (7). News outlets have reported that during a choir practice in Washington on March 10, presymptomatic transmission likely played a role in SARS-CoV-2 transmission to approximately 40 of 60 choir members.*"
CDC MMWR
https://www.cdc.gov/mmwr/volumes/69/wr/mm6913e1.htm
Asymptomatic and Presymptomatic SARS-CoV-2 Infections in Residents of a Long-Term Care Skilled Nursing Facility — King County, Washington, March 2020
Early Release / March 27, 2020 / 69
Anne Kimball, MD1,2; Kelly M. Hatfield, MSPH1; Melissa Arons, MSc1,2; Allison James, PhD1,2; Joanne Taylor, PhD1,2; Kevin Spicer, MD1; Ana C. Bardossy, MD1,2; Lisa P. Oakley, PhD1,2; Sukarma Tanwar, MMed1,2; Zeshan Chisty, MPH1; Jeneita M. Bell, MD1; Mark Methner, PhD1; Josh Harney, MS1; Jesica R. Jacobs, PhD1,3; Christina M. Carlson, PhD1,3; Heather P. McLaughlin, PhD1; Nimalie Stone, MD1; Shauna Clark4; Claire Brostrom-Smith, MSN4; Libby C. Page, MPH4; Meagan Kay, DVM4; James Lewis, MD4; Denny Russell5; Brian Hiatt5; Jessica Gant, MS5; Jeffrey S. Duchin, MD4; Thomas A. Clark, MD1; Margaret A. Honein, PhD1; Sujan C. Reddy, MD1; John A. Jernigan, MD1; Public Health – Seattle & King County; CDC COVID-19 Investigation Team (View author affiliations)
Summary
What is already known about this topic?
Once SARS-CoV-2 is introduced in a long-term care skilled nursing facility (SNF), rapid transmission can occur.
What is added by this report?
Following identification of a case of coronavirus disease 2019 (COVID-19) in a health care worker, 76 of 82 residents of an SNF were tested for SARS-CoV-2; 23 (30.3%) had positive test results, approximately half of whom were asymptomatic or presymptomatic on the day of testing.
What are the implications for public health practice?
Symptom-based screening of SNF residents might fail to identify all SARS-CoV-2 infections. Asymptomatic and presymptomatic SNF residents might contribute to SARS-CoV-2 transmission. Once a facility has confirmed a COVID-19 case, all residents should be cared for using CDC-recommended personal protective equipment (PPE), with considerations for extended use or reuse of PPE as needed.
Older adults are susceptible to severe coronavirus disease 2019 (COVID-19) outcomes as a consequence of their age and, in some cases, underlying health conditions (1). A COVID-19 outbreak in a long-term care skilled nursing facility (SNF) in King County, Washington that was first identified on February 28, 2020, highlighted the potential for rapid spread among residents of these types of facilities (2). On March 1, a health care provider at a second long-term care skilled nursing facility (facility A) in King County, Washington, had a positive test result for SARS-CoV-2, the novel coronavirus that causes COVID-19, after working while symptomatic on February 26 and 28. By March 6, seven residents of this second facility were symptomatic and had positive test results for SARS-CoV-2. On March 13, CDC performed symptom assessments and SARS-CoV-2 testing for 76 (93%) of the 82 facility A residents to evaluate the utility of symptom screening for identification of COVID-19 in SNF residents. Residents were categorized as asymptomatic or symptomatic at the time of testing, based on the absence or presence of fever, cough, shortness of breath, or other symptoms on the day of testing or during the preceding 14 days. Among 23 (30%) residents with positive test results, 10 (43%) had symptoms on the date of testing, and 13 (57%) were asymptomatic. Seven days after testing, 10 of these 13 previously asymptomatic residents had developed symptoms and were recategorized as presymptomatic at the time of testing. The reverse transcription–polymerase chain reaction (RT-PCR) testing cycle threshold (Ct) values indicated large quantities of viral RNA in asymptomatic, presymptomatic, and symptomatic residents, suggesting the potential for transmission regardless of symptoms. Symptom-based screening in SNFs could fail to identify approximately half of residents with COVID-19. Long-term care facilities should take proactive steps to prevent introduction of SARS-CoV-2 (3). Once a confirmed case is identified in an SNF, all residents should be placed on isolation precautions if possible (3), with considerations for extended use or reuse of personal protective equipment (PPE) as needed (4).
Immediately upon identification of the index case in facility A on March 1, nursing and administrative leadership instituted visitor restrictions, twice-daily assessments of COVID-19 signs and symptoms among residents, and fever screening of all health care personnel at the start of each shift. On March 6, Public Health – Seattle and King County, in collaboration with CDC, recommended infection prevention and control measures, including isolation of all symptomatic residents and use of gowns, gloves, eye protection, facemasks, and hand hygiene for health care personnel entering symptomatic residents’ rooms. A data collection tool was developed to ascertain symptom status and underlying medical conditions for all residents.
On March 13, the symptom assessment tool was completed by facility A’s nursing staff members by reviewing screening records of residents for the preceding 14 days and by clinician interview of residents at the time of specimen collection. For residents with significant cognitive impairment, symptoms were obtained solely from screening records. A follow-up symptom assessment was completed 7 days later by nursing staff members. Nasopharyngeal swabs were obtained from all 76 residents who agreed to testing and were present in the facility at the time; oropharyngeal swabs were also collected from most residents, depending upon their cooperation. The Washington State Public Health Laboratory performed one-step real-time RT-PCR assay on all specimens using the SARS-CoV-2 CDC assay protocol, which determines the presence of the virus through identification of two genetic markers, the N1 and N2 nucleocapsid protein gene regions (5). The Ct, the cycle number during RT-PCR testing when detection of viral amplicons occurs, is inversely correlated with the amount of RNA present; a Ct value <40 cycles denotes a positive result for SARS-CoV-2, with a lower value indicating a larger amount of viral RNA.
Residents were assessed for stable chronic symptoms (e.g., chronic, unchanged cough) as well as typical and atypical signs and symptoms of COVID-19. Typical COVID-19 signs and symptoms include fever, cough, and shortness of breath (3); potential atypical symptoms assessed included sore throat, chills, increased confusion, rhinorrhea or nasal congestion, myalgia, dizziness, malaise, headache, nausea, and diarrhea. Residents were categorized as asymptomatic (no symptoms or only stable chronic symptoms) or symptomatic (at least one new or worsened typical or atypical symptom of COVID-19) on the day of testing or during the preceding 14 days. Residents with positive test results and were asymptomatic at time of testing were reevaluated 1 week later to ascertain whether any symptoms had developed in the interim. Those who developed new symptoms were recategorized as presymptomatic. Ct values were compared for the recategorized symptom groups using one-way analysis of variance (ANOVA) for all residents with positive test results for SARS-CoV-2. Analyses were conducted using SAS statistical software (version 9.4; SAS Institute).
On March 13, among the 82 residents in facility A; 76 (92.7%) underwent symptom assessment and testing; three (3.7%) refused testing, two (2.4%) who had COVID-19 symptoms were transferred to a hospital before testing, and one (1.2%) was unavailable. Among the 76 tested residents, 23 (30.3%) had positive test results.
Demographic characteristics were similar among the 53 (69.7%) residents with negative test results and the 23 (30.3%) with positive test results (Table 1). Among the 23 residents with positive test results, 10 (43.5%) were symptomatic, and 13 (56.5%) were asymptomatic. Eight symptomatic residents had typical COVID-19 symptoms, and two had only atypical symptoms; the most common atypical symptoms reported were malaise (four residents) and nausea (three). Thirteen (24.5%) residents who had negative test results also reported typical and atypical COVID-19 symptoms during the 14 days preceding testing.
One week after testing, the 13 residents who had positive test results and were asymptomatic on the date of testing were reassessed; 10 had developed symptoms and were recategorized as presymptomatic at the time of testing (Table 2). The most common signs and symptoms that developed were fever (eight residents), malaise (six), and cough (five). The mean interval from testing to symptom onset in the presymptomatic residents was 3 days. Three residents with positive test results remained asymptomatic.
Real-time RT-PCR Ct values for both genetic markers among residents with positive test results for SARS-CoV-2 ranged from 18.6 to 29.2 (symptomatic [typical symptoms]), 24.3 to 26.3 (symptomatic [atypical symptoms only]), 15.3 to 37.9 (presymptomatic), and 21.9 to 31.0 (asymptomatic) (Figure). There were no significant differences between the mean Ct values in the four symptom status groups (p = 0.3).
Discussion
Sixteen days after introduction of SARS-CoV-2 into facility A, facility-wide testing identified a 30.3% prevalence of infection among residents, indicating very rapid spread, despite early adoption of infection prevention and control measures. Approximately half of all residents with positive test results did not have any symptoms at the time of testing, suggesting that transmission from asymptomatic and presymptomatic residents, who were not recognized as having SARS-CoV-2 infection and therefore not isolated, might have contributed to further spread. Similarly, studies have shown that influenza in the elderly, including those living in SNFs, often manifests as few or atypical symptoms, delaying diagnosis and contributing to transmission (6–8). These findings have important implications for infection control. Current interventions for preventing SARS-CoV-2 transmission primarily rely on presence of signs and symptoms to identify and isolate residents or patients who might have COVID-19. If asymptomatic or presymptomatic residents play an important role in transmission in this population at high risk, additional prevention measures merit consideration, including using testing to guide cohorting strategies or using transmission-based precautions for all residents of a facility after introduction of SARS-CoV-2. Limitations in availability of tests might necessitate taking the latter approach at this time.
Although these findings do not quantify the relative contributions of asymptomatic or presymptomatic residents to SARS-CoV-2 transmission in facility A, they suggest that these residents have the potential for substantial viral shedding. Low Ct values, which indicate large quantities of viral RNA, were identified for most of these residents, and there was no statistically significant difference in distribution of Ct values among the symptom status groups. Similar Ct values were reported in asymptomatic adults in China who were known to transmit SARS-CoV-2 (9). Studies to determine the presence of viable virus from these specimens are currently under way.
SNFs have additional infection prevention and control challenges compared with those of assisted living or independent living long-term care facilities. For example, SNF residents might be in shared rooms rather than individual apartments, and there is often prolonged and close contact between residents and health care providers related to the residents’ medical conditions and cognitive function. The index patient in this outbreak was a health care provider, which might have contributed to rapid spread in the facility. In addition, health care personnel in all types of long-term care facilities might have limited experience with proper use of PPE. Symptom ascertainment and room isolation can be exceptionally challenging in elderly residents with neurologic conditions, including dementia. In addition, symptoms of COVID-19 are common and might have multiple etiologies in this population; 24.5% of facility A residents with negative test results for SARS-CoV-2 reported typical or atypical symptoms.
The findings in this report are subject to at least two limitations. First, accurate symptom ascertainment in persons with cognitive impairment and other disabilities is challenging; however, this limitation is estimated to be representative of symptom data collected in most SNFs, and thus, these findings might be generalizable. Second, because this analysis was conducted among residents of an SNF, it is not known whether findings apply to the general population, including younger persons, those without underlying medical conditions, or similarly aged populations in the general community.
This analysis suggests that symptom screening could initially fail to identify approximately one half of SNF residents with SARS-CoV-2 infection. Unrecognized asymptomatic and presymptomatic infections might contribute to transmission in these settings. During the current COVID-19 pandemic, SNFs and all long-term care facilities should take proactive steps to prevent introduction of SARS-CoV-2, including restricting visitors except in compassionate care situations, restricting nonessential personnel from entering the building, asking staff members to monitor themselves for fever and other symptoms, screening all staff members at the beginning of their shift for fever and other symptoms, and supporting staff member sick leave, including for those with mild symptoms (3). Once a facility has a case of COVID-19, broad strategies should be implemented to prevent transmission, including restriction of resident-to-resident interactions, universal use of facemasks for all health care personnel while in the facility, and if possible, use of CDC-recommended PPE for the care of all residents (i.e., gown, gloves, eye protection, N95 respirator, or, if not available, a face mask) (3). In settings where PPE supplies are limited, strategies for extended PPE use and limited reuse should be employed (4). As testing availability improves, consideration might be given to test-based strategies for identifying residents with SARS-CoV-2 infection for the purpose of cohorting, either in designated units within a facility or in a separate facility designated for residents with COVID-19. During the COVID-19 pandemic, collaborative efforts are crucial to protecting the most vulnerable populations.
Acknowledgments
Nursing and administrative leaders at facility A; Washington State Public Health Laboratory’s SARS-CoV-2 testing team.
Public Health – Seattle & King County
Atar Baer, Public Health – Seattle & King County; Leslie M. Barnard, Public Health – Seattle & King County; Eileen Benoliel, Public Health – Seattle & King County; Meaghan S. Fagalde, Public Health – Seattle & King County; Jessica Ferro, Public Health – Seattle & King County; Hal Garcia Smith, Public Health – Seattle & King County; Elysia Gonzales, Public Health – Seattle & King County; Noel Hatley, Public Health – Seattle & King County; Grace Hatt, Public Health – Seattle & King County; Michaela Hope, Public Health – Seattle & King County; Melinda Huntington-Frazier, Public Health – Seattle & King County; Vance Kawakami, Public Health – Seattle & King County; Jennifer L. Lenahan, Public Health – Seattle & King County; Margaret D. Lukoff, Public Health – Seattle & King County; Emily B. Maier, Public Health – Seattle & King County; Shelly McKeirnan, Public Health – Seattle & King County; Patricia Montgomery, Public Health – Seattle & King County; Jennifer L. Morgan, Public Health – Seattle & King County; Laura A. Mummert, Public Health – Seattle & King County; Sargis Pogosjans, Public Health – Seattle & King County; Francis X. Riedo, Public Health – Seattle & King County; Leilani Schwarcz, Public Health – Seattle & King County; Daniel Smith, Public Health – Seattle & King County; Steve Stearns, Public Health – Seattle & King County; Kaitlyn J. Sykes, Public Health – Seattle & King County; Holly Whitney, Public Health – Seattle & King County.
CDC COVID-19 Investigation Team
Hammad Ali, CDC; Michelle Banks, CDC; Arun Balajee, CDC; Eric J. Chow, CDC; Barbara Cooper, CDC; Dustin W. Currie, CDC; Jonathan Dyal, CDC; Jessica Healy, CDC; Michael Hughes, CDC; Temet M. McMichael, CDC; Leisha Nolen, CDC; Christine Olson, CDC; Agam K. Rao, CDC; Kristine Schmit, CDC; Noah G. Schwartz, CDC; Farrell Tobolowsky, CDC; Rachael Zacks, CDC; Suzanne Zane, CDC.
CDC MMWR
https://www.cdc.gov/mmwr/volumes/69/wr/mm6914e1.htm
Presymptomatic Transmission of SARS-CoV-2 — Singapore, January 23–March 16, 2020
Early Release / April 1, 2020 / 69
Wycliffe E. Wei, MPH1,2; Zongbin Li, MBBS1; Calvin J. Chiew, MPH1; Sarah E. Yong, MMed1; Matthias P. Toh, MMed2,3; Vernon J. Lee, PhD1,3
Early detection and isolation of symptomatic COVID-19 patients and tracing of close contacts is an important disease containment strategy; however, the existence of presymptomatic or asymptomatic transmission would present difficult challenges to contact tracing. Such transmission modes have not been definitively documented for COVID-19, although cases of presymptomatic and asymptomatic transmissions have been reported in China (1,2) and possibly occurred in a nursing facility in King County, Washington (3). Examination of serial intervals (i.e., the number of days between symptom onsets in a primary case and a secondary case) in China suggested that 12.6% of transmission was presymptomatic (2). COVID-19 cases in Singapore were reviewed to determine whether presymptomatic transmission occurred among COVID-19 clusters.
The surveillance and case detection methods employed in Singapore have been described (4). Briefly, all medical practitioners were required by law to notify Singapore’s Ministry of Health of suspected and confirmed cases of COVID-19. The definition of a suspected case was based on the presence of respiratory symptoms and an exposure history. Suspected cases were tested, and a confirmed case was defined as a positive test for SARS-CoV-2, using laboratory-based polymerase chain reaction or serologic assays (5). All cases in this report were confirmed by polymerase chain reaction only. Asymptomatic persons were not routinely tested, but such testing was performed for persons in groups considered to be at especially high risk for infection, such as evacuees on flights from Wuhan, China (6), or families that experienced high attack rates.
Patients with confirmed COVID-19 were interviewed to obtain information about their clinical symptoms and activity history during the 2 weeks preceding symptom onset to ascertain possible sources of infection. Contact tracing examined the time from symptom onset until the time the patient was successfully isolated to identify contacts who had interactions with the patient. All contacts were monitored daily for their health status, and those who developed symptoms were tested as part of active case finding.
Clinical and epidemiologic data for all 243 reported COVID-19 cases in Singapore during January 23–March 16 were reviewed. Clinical histories were examined to identify symptoms before, during, and after the first positive SARS-CoV-2 test.
Cluster A. A woman aged 55 years (patient A1) and a man aged 56 years (patient A2) were tourists from Wuhan, China, who arrived in Singapore on January 19. They visited a local church the same day and had symptom onset on January 22 (patient A1) and January 24 (patient A2). Three other persons, a man aged 53 years (patient A3), a woman aged 39 years (patient A4), and a woman aged 52 years (patient A5) attended the same church that day and subsequently developed symptoms on January 23, January 30, and February 3, respectively. Patient A5 occupied the same seat in the church that patients A1 and A2 had occupied earlier that day (captured by closed-circuit camera) (5). Investigations of other attendees did not reveal any other symptomatic persons who attended the church that day.
The possibility of presymptomatic transmission of SARS-CoV-2 increases the challenges of COVID-19 containment measures, which are predicated on early detection and isolation of symptomatic persons. The magnitude of this impact is dependent upon the extent and duration of transmissibility while a patient is presymptomatic, which, to date, have not been clearly established. In four clusters (A, B, F, and G), it was possible to determine that presymptomatic transmission exposure occurred 1–3 days before the source patient developed symptoms. Such transmission has also been observed in other respiratory viruses such as influenza. However, transmissibility by presymptomatic persons requires further study.
The findings in this report are subject to at least three limitations. First, although these cases were carefully investigated, the possibility exists that an unknown source might have initiated the clusters described. Given that there was not widespread community transmission of COVID-19 in Singapore during the period of evaluation and while strong surveillance systems were in place to detect cases, presymptomatic transmission was estimated to be more likely than the occurrence of unidentified sources. Further, contact tracing undertaken during this period was extensive and would likely have detected other symptomatic cases. Second, recall bias could affect the accuracy of symptom onset dates reported by cases, especially if symptoms were mild, resulting in uncertainty about the duration of the presymptomatic period. Finally, because of the nature of detection and surveillance activities that focus on testing symptomatic persons, underdetection of asymptomatic illness is expected. Recall bias and interviewer bias (i.e., the expectation that some symptoms were present, no matter how mild), could have contributed to this.
The evidence of presymptomatic transmission in Singapore, in combination with evidence from other studies (9,10) supports the likelihood that viral shedding can occur in the absence of symptoms and before symptom onset. This study identified seven clusters of cases in which presymptomatic transmission of COVID-19 likely occurred; 10 (6.4%) of such cases included in these clusters were among the 157 locally acquired cases reported in Singapore as of March 16. Containment measures should account for the possibility of presymptomatic transmission by including the period before symptom onset when conducting contact tracing. These findings also suggest that to control the pandemic it might not be enough for only persons with symptoms to limit their contact with others because persons without symptoms might transmit infection. Finally, these findings underscore the importance of social distancing in the public health response to the COVID-19 pandemic, including the avoidance of congregate settings.
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Corresponding author: Vernon J. Lee, Vernon_Lee@moh.gov.sg.
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1Ministry of Health, Singapore; 2National Centre for Infectious Diseases, Singapore; 3Saw Swee Hock School of Public Health, Singapore.
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All authors have completed and submitted the International Committee of Medical Journal Editors form for disclosure of potential conflicts of interest. No potential conflicts of interest were disclosed.
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* https://www.latimes.com/world-nation/story/2020-03-29/coronavirus-choir-outbreak
external icon
Another study in Singapore was posted. "Investigation of COVID-19 cases in Singapore identified seven clusters (clusters A–G) in which presymptomatic transmission likely occurred. These clusters occurred during January 19–March 12, and involved from two to five patients each (Figure). Ten of the cases within these clusters were attributed to presymptomatic transmission and accounted for 6.4% of the 157 locally acquired cases reported as of March 16."
This enforces the need for social distancing, handwashing, and frequent cleaning, but also tracing personal contact with people who are ill. As in this case with the nursing home, social distancing can be an issue in addition to having a population that is high at risk.
One interesting note sited in the MMWR report - "Speech and other vocal activities such as singing have been shown to generate air particles, with the rate of emission corresponding to voice loudness (7). News outlets have reported that during a choir practice in Washington on March 10, presymptomatic transmission likely played a role in SARS-CoV-2 transmission to approximately 40 of 60 choir members.*"
CDC MMWR
https://www.cdc.gov/mmwr/volumes/69/wr/mm6913e1.htm
Asymptomatic and Presymptomatic SARS-CoV-2 Infections in Residents of a Long-Term Care Skilled Nursing Facility — King County, Washington, March 2020
Early Release / March 27, 2020 / 69
Anne Kimball, MD1,2; Kelly M. Hatfield, MSPH1; Melissa Arons, MSc1,2; Allison James, PhD1,2; Joanne Taylor, PhD1,2; Kevin Spicer, MD1; Ana C. Bardossy, MD1,2; Lisa P. Oakley, PhD1,2; Sukarma Tanwar, MMed1,2; Zeshan Chisty, MPH1; Jeneita M. Bell, MD1; Mark Methner, PhD1; Josh Harney, MS1; Jesica R. Jacobs, PhD1,3; Christina M. Carlson, PhD1,3; Heather P. McLaughlin, PhD1; Nimalie Stone, MD1; Shauna Clark4; Claire Brostrom-Smith, MSN4; Libby C. Page, MPH4; Meagan Kay, DVM4; James Lewis, MD4; Denny Russell5; Brian Hiatt5; Jessica Gant, MS5; Jeffrey S. Duchin, MD4; Thomas A. Clark, MD1; Margaret A. Honein, PhD1; Sujan C. Reddy, MD1; John A. Jernigan, MD1; Public Health – Seattle & King County; CDC COVID-19 Investigation Team (View author affiliations)
Summary
What is already known about this topic?
Once SARS-CoV-2 is introduced in a long-term care skilled nursing facility (SNF), rapid transmission can occur.
What is added by this report?
Following identification of a case of coronavirus disease 2019 (COVID-19) in a health care worker, 76 of 82 residents of an SNF were tested for SARS-CoV-2; 23 (30.3%) had positive test results, approximately half of whom were asymptomatic or presymptomatic on the day of testing.
What are the implications for public health practice?
Symptom-based screening of SNF residents might fail to identify all SARS-CoV-2 infections. Asymptomatic and presymptomatic SNF residents might contribute to SARS-CoV-2 transmission. Once a facility has confirmed a COVID-19 case, all residents should be cared for using CDC-recommended personal protective equipment (PPE), with considerations for extended use or reuse of PPE as needed.
Older adults are susceptible to severe coronavirus disease 2019 (COVID-19) outcomes as a consequence of their age and, in some cases, underlying health conditions (1). A COVID-19 outbreak in a long-term care skilled nursing facility (SNF) in King County, Washington that was first identified on February 28, 2020, highlighted the potential for rapid spread among residents of these types of facilities (2). On March 1, a health care provider at a second long-term care skilled nursing facility (facility A) in King County, Washington, had a positive test result for SARS-CoV-2, the novel coronavirus that causes COVID-19, after working while symptomatic on February 26 and 28. By March 6, seven residents of this second facility were symptomatic and had positive test results for SARS-CoV-2. On March 13, CDC performed symptom assessments and SARS-CoV-2 testing for 76 (93%) of the 82 facility A residents to evaluate the utility of symptom screening for identification of COVID-19 in SNF residents. Residents were categorized as asymptomatic or symptomatic at the time of testing, based on the absence or presence of fever, cough, shortness of breath, or other symptoms on the day of testing or during the preceding 14 days. Among 23 (30%) residents with positive test results, 10 (43%) had symptoms on the date of testing, and 13 (57%) were asymptomatic. Seven days after testing, 10 of these 13 previously asymptomatic residents had developed symptoms and were recategorized as presymptomatic at the time of testing. The reverse transcription–polymerase chain reaction (RT-PCR) testing cycle threshold (Ct) values indicated large quantities of viral RNA in asymptomatic, presymptomatic, and symptomatic residents, suggesting the potential for transmission regardless of symptoms. Symptom-based screening in SNFs could fail to identify approximately half of residents with COVID-19. Long-term care facilities should take proactive steps to prevent introduction of SARS-CoV-2 (3). Once a confirmed case is identified in an SNF, all residents should be placed on isolation precautions if possible (3), with considerations for extended use or reuse of personal protective equipment (PPE) as needed (4).
Immediately upon identification of the index case in facility A on March 1, nursing and administrative leadership instituted visitor restrictions, twice-daily assessments of COVID-19 signs and symptoms among residents, and fever screening of all health care personnel at the start of each shift. On March 6, Public Health – Seattle and King County, in collaboration with CDC, recommended infection prevention and control measures, including isolation of all symptomatic residents and use of gowns, gloves, eye protection, facemasks, and hand hygiene for health care personnel entering symptomatic residents’ rooms. A data collection tool was developed to ascertain symptom status and underlying medical conditions for all residents.
On March 13, the symptom assessment tool was completed by facility A’s nursing staff members by reviewing screening records of residents for the preceding 14 days and by clinician interview of residents at the time of specimen collection. For residents with significant cognitive impairment, symptoms were obtained solely from screening records. A follow-up symptom assessment was completed 7 days later by nursing staff members. Nasopharyngeal swabs were obtained from all 76 residents who agreed to testing and were present in the facility at the time; oropharyngeal swabs were also collected from most residents, depending upon their cooperation. The Washington State Public Health Laboratory performed one-step real-time RT-PCR assay on all specimens using the SARS-CoV-2 CDC assay protocol, which determines the presence of the virus through identification of two genetic markers, the N1 and N2 nucleocapsid protein gene regions (5). The Ct, the cycle number during RT-PCR testing when detection of viral amplicons occurs, is inversely correlated with the amount of RNA present; a Ct value <40 cycles denotes a positive result for SARS-CoV-2, with a lower value indicating a larger amount of viral RNA.
Residents were assessed for stable chronic symptoms (e.g., chronic, unchanged cough) as well as typical and atypical signs and symptoms of COVID-19. Typical COVID-19 signs and symptoms include fever, cough, and shortness of breath (3); potential atypical symptoms assessed included sore throat, chills, increased confusion, rhinorrhea or nasal congestion, myalgia, dizziness, malaise, headache, nausea, and diarrhea. Residents were categorized as asymptomatic (no symptoms or only stable chronic symptoms) or symptomatic (at least one new or worsened typical or atypical symptom of COVID-19) on the day of testing or during the preceding 14 days. Residents with positive test results and were asymptomatic at time of testing were reevaluated 1 week later to ascertain whether any symptoms had developed in the interim. Those who developed new symptoms were recategorized as presymptomatic. Ct values were compared for the recategorized symptom groups using one-way analysis of variance (ANOVA) for all residents with positive test results for SARS-CoV-2. Analyses were conducted using SAS statistical software (version 9.4; SAS Institute).
On March 13, among the 82 residents in facility A; 76 (92.7%) underwent symptom assessment and testing; three (3.7%) refused testing, two (2.4%) who had COVID-19 symptoms were transferred to a hospital before testing, and one (1.2%) was unavailable. Among the 76 tested residents, 23 (30.3%) had positive test results.
Demographic characteristics were similar among the 53 (69.7%) residents with negative test results and the 23 (30.3%) with positive test results (Table 1). Among the 23 residents with positive test results, 10 (43.5%) were symptomatic, and 13 (56.5%) were asymptomatic. Eight symptomatic residents had typical COVID-19 symptoms, and two had only atypical symptoms; the most common atypical symptoms reported were malaise (four residents) and nausea (three). Thirteen (24.5%) residents who had negative test results also reported typical and atypical COVID-19 symptoms during the 14 days preceding testing.
One week after testing, the 13 residents who had positive test results and were asymptomatic on the date of testing were reassessed; 10 had developed symptoms and were recategorized as presymptomatic at the time of testing (Table 2). The most common signs and symptoms that developed were fever (eight residents), malaise (six), and cough (five). The mean interval from testing to symptom onset in the presymptomatic residents was 3 days. Three residents with positive test results remained asymptomatic.
Real-time RT-PCR Ct values for both genetic markers among residents with positive test results for SARS-CoV-2 ranged from 18.6 to 29.2 (symptomatic [typical symptoms]), 24.3 to 26.3 (symptomatic [atypical symptoms only]), 15.3 to 37.9 (presymptomatic), and 21.9 to 31.0 (asymptomatic) (Figure). There were no significant differences between the mean Ct values in the four symptom status groups (p = 0.3).
Discussion
Sixteen days after introduction of SARS-CoV-2 into facility A, facility-wide testing identified a 30.3% prevalence of infection among residents, indicating very rapid spread, despite early adoption of infection prevention and control measures. Approximately half of all residents with positive test results did not have any symptoms at the time of testing, suggesting that transmission from asymptomatic and presymptomatic residents, who were not recognized as having SARS-CoV-2 infection and therefore not isolated, might have contributed to further spread. Similarly, studies have shown that influenza in the elderly, including those living in SNFs, often manifests as few or atypical symptoms, delaying diagnosis and contributing to transmission (6–8). These findings have important implications for infection control. Current interventions for preventing SARS-CoV-2 transmission primarily rely on presence of signs and symptoms to identify and isolate residents or patients who might have COVID-19. If asymptomatic or presymptomatic residents play an important role in transmission in this population at high risk, additional prevention measures merit consideration, including using testing to guide cohorting strategies or using transmission-based precautions for all residents of a facility after introduction of SARS-CoV-2. Limitations in availability of tests might necessitate taking the latter approach at this time.
Although these findings do not quantify the relative contributions of asymptomatic or presymptomatic residents to SARS-CoV-2 transmission in facility A, they suggest that these residents have the potential for substantial viral shedding. Low Ct values, which indicate large quantities of viral RNA, were identified for most of these residents, and there was no statistically significant difference in distribution of Ct values among the symptom status groups. Similar Ct values were reported in asymptomatic adults in China who were known to transmit SARS-CoV-2 (9). Studies to determine the presence of viable virus from these specimens are currently under way.
SNFs have additional infection prevention and control challenges compared with those of assisted living or independent living long-term care facilities. For example, SNF residents might be in shared rooms rather than individual apartments, and there is often prolonged and close contact between residents and health care providers related to the residents’ medical conditions and cognitive function. The index patient in this outbreak was a health care provider, which might have contributed to rapid spread in the facility. In addition, health care personnel in all types of long-term care facilities might have limited experience with proper use of PPE. Symptom ascertainment and room isolation can be exceptionally challenging in elderly residents with neurologic conditions, including dementia. In addition, symptoms of COVID-19 are common and might have multiple etiologies in this population; 24.5% of facility A residents with negative test results for SARS-CoV-2 reported typical or atypical symptoms.
The findings in this report are subject to at least two limitations. First, accurate symptom ascertainment in persons with cognitive impairment and other disabilities is challenging; however, this limitation is estimated to be representative of symptom data collected in most SNFs, and thus, these findings might be generalizable. Second, because this analysis was conducted among residents of an SNF, it is not known whether findings apply to the general population, including younger persons, those without underlying medical conditions, or similarly aged populations in the general community.
This analysis suggests that symptom screening could initially fail to identify approximately one half of SNF residents with SARS-CoV-2 infection. Unrecognized asymptomatic and presymptomatic infections might contribute to transmission in these settings. During the current COVID-19 pandemic, SNFs and all long-term care facilities should take proactive steps to prevent introduction of SARS-CoV-2, including restricting visitors except in compassionate care situations, restricting nonessential personnel from entering the building, asking staff members to monitor themselves for fever and other symptoms, screening all staff members at the beginning of their shift for fever and other symptoms, and supporting staff member sick leave, including for those with mild symptoms (3). Once a facility has a case of COVID-19, broad strategies should be implemented to prevent transmission, including restriction of resident-to-resident interactions, universal use of facemasks for all health care personnel while in the facility, and if possible, use of CDC-recommended PPE for the care of all residents (i.e., gown, gloves, eye protection, N95 respirator, or, if not available, a face mask) (3). In settings where PPE supplies are limited, strategies for extended PPE use and limited reuse should be employed (4). As testing availability improves, consideration might be given to test-based strategies for identifying residents with SARS-CoV-2 infection for the purpose of cohorting, either in designated units within a facility or in a separate facility designated for residents with COVID-19. During the COVID-19 pandemic, collaborative efforts are crucial to protecting the most vulnerable populations.
Acknowledgments
Nursing and administrative leaders at facility A; Washington State Public Health Laboratory’s SARS-CoV-2 testing team.
Public Health – Seattle & King County
Atar Baer, Public Health – Seattle & King County; Leslie M. Barnard, Public Health – Seattle & King County; Eileen Benoliel, Public Health – Seattle & King County; Meaghan S. Fagalde, Public Health – Seattle & King County; Jessica Ferro, Public Health – Seattle & King County; Hal Garcia Smith, Public Health – Seattle & King County; Elysia Gonzales, Public Health – Seattle & King County; Noel Hatley, Public Health – Seattle & King County; Grace Hatt, Public Health – Seattle & King County; Michaela Hope, Public Health – Seattle & King County; Melinda Huntington-Frazier, Public Health – Seattle & King County; Vance Kawakami, Public Health – Seattle & King County; Jennifer L. Lenahan, Public Health – Seattle & King County; Margaret D. Lukoff, Public Health – Seattle & King County; Emily B. Maier, Public Health – Seattle & King County; Shelly McKeirnan, Public Health – Seattle & King County; Patricia Montgomery, Public Health – Seattle & King County; Jennifer L. Morgan, Public Health – Seattle & King County; Laura A. Mummert, Public Health – Seattle & King County; Sargis Pogosjans, Public Health – Seattle & King County; Francis X. Riedo, Public Health – Seattle & King County; Leilani Schwarcz, Public Health – Seattle & King County; Daniel Smith, Public Health – Seattle & King County; Steve Stearns, Public Health – Seattle & King County; Kaitlyn J. Sykes, Public Health – Seattle & King County; Holly Whitney, Public Health – Seattle & King County.
CDC COVID-19 Investigation Team
Hammad Ali, CDC; Michelle Banks, CDC; Arun Balajee, CDC; Eric J. Chow, CDC; Barbara Cooper, CDC; Dustin W. Currie, CDC; Jonathan Dyal, CDC; Jessica Healy, CDC; Michael Hughes, CDC; Temet M. McMichael, CDC; Leisha Nolen, CDC; Christine Olson, CDC; Agam K. Rao, CDC; Kristine Schmit, CDC; Noah G. Schwartz, CDC; Farrell Tobolowsky, CDC; Rachael Zacks, CDC; Suzanne Zane, CDC.
CDC MMWR
https://www.cdc.gov/mmwr/volumes/69/wr/mm6914e1.htm
Presymptomatic Transmission of SARS-CoV-2 — Singapore, January 23–March 16, 2020
Early Release / April 1, 2020 / 69
Wycliffe E. Wei, MPH1,2; Zongbin Li, MBBS1; Calvin J. Chiew, MPH1; Sarah E. Yong, MMed1; Matthias P. Toh, MMed2,3; Vernon J. Lee, PhD1,3
Summary
What is already known about this topic?
Preliminary evidence indicates the occurrence of presymptomatic transmission of SARS-CoV-2, based on reports of individual cases in China.
What is added by this report?
Investigation of all 243 cases of COVID-19 reported in Singapore during January 23–March 16 identified seven clusters of cases in which presymptomatic transmission is the most likely explanation for the occurrence of secondary cases.
What are the implications for public health practice?
The possibility of presymptomatic transmission increases the challenges of containment measures. Public health officials conducting contact tracing should strongly consider including a period before symptom onset to account for the possibility of presymptomatic transmission. The potential for presymptomatic transmission underscores the importance of social distancing, including the avoidance of congregate settings, to reduce COVID-19 spread.
Article Metrics
Presymptomatic transmission of SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), might pose challenges for disease control. The first case of COVID-19 in Singapore was detected on January 23, 2020, and by March 16, a total of 243 cases had been confirmed, including 157 locally acquired cases. Clinical and epidemiologic findings of all COVID-19 cases in Singapore through March 16 were reviewed to determine whether presymptomatic transmission might have occurred. Presymptomatic transmission was defined as the transmission of SARS-CoV-2 from an infected person (source patient) to a secondary patient before the source patient developed symptoms, as ascertained by exposure and symptom onset dates, with no evidence that the secondary patient had been exposed to anyone else with COVID-19. Seven COVID-19 epidemiologic clusters in which presymptomatic transmission likely occurred were identified, and 10 such cases within these clusters accounted for 6.4% of the 157 locally acquired cases. In the four clusters for which the date of exposure could be determined, presymptomatic transmission occurred 1–3 days before symptom onset in the presymptomatic source patient. To account for the possibility of presymptomatic transmission, officials developing contact tracing protocols should strongly consider including a period before symptom onset. Evidence of presymptomatic transmission of SARS-CoV-2 underscores the critical role social distancing, including avoidance of congregate settings, plays in controlling the COVID-19 pandemic.
What is already known about this topic?
Preliminary evidence indicates the occurrence of presymptomatic transmission of SARS-CoV-2, based on reports of individual cases in China.
What is added by this report?
Investigation of all 243 cases of COVID-19 reported in Singapore during January 23–March 16 identified seven clusters of cases in which presymptomatic transmission is the most likely explanation for the occurrence of secondary cases.
What are the implications for public health practice?
The possibility of presymptomatic transmission increases the challenges of containment measures. Public health officials conducting contact tracing should strongly consider including a period before symptom onset to account for the possibility of presymptomatic transmission. The potential for presymptomatic transmission underscores the importance of social distancing, including the avoidance of congregate settings, to reduce COVID-19 spread.
Article Metrics
Presymptomatic transmission of SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), might pose challenges for disease control. The first case of COVID-19 in Singapore was detected on January 23, 2020, and by March 16, a total of 243 cases had been confirmed, including 157 locally acquired cases. Clinical and epidemiologic findings of all COVID-19 cases in Singapore through March 16 were reviewed to determine whether presymptomatic transmission might have occurred. Presymptomatic transmission was defined as the transmission of SARS-CoV-2 from an infected person (source patient) to a secondary patient before the source patient developed symptoms, as ascertained by exposure and symptom onset dates, with no evidence that the secondary patient had been exposed to anyone else with COVID-19. Seven COVID-19 epidemiologic clusters in which presymptomatic transmission likely occurred were identified, and 10 such cases within these clusters accounted for 6.4% of the 157 locally acquired cases. In the four clusters for which the date of exposure could be determined, presymptomatic transmission occurred 1–3 days before symptom onset in the presymptomatic source patient. To account for the possibility of presymptomatic transmission, officials developing contact tracing protocols should strongly consider including a period before symptom onset. Evidence of presymptomatic transmission of SARS-CoV-2 underscores the critical role social distancing, including avoidance of congregate settings, plays in controlling the COVID-19 pandemic.
Early detection and isolation of symptomatic COVID-19 patients and tracing of close contacts is an important disease containment strategy; however, the existence of presymptomatic or asymptomatic transmission would present difficult challenges to contact tracing. Such transmission modes have not been definitively documented for COVID-19, although cases of presymptomatic and asymptomatic transmissions have been reported in China (1,2) and possibly occurred in a nursing facility in King County, Washington (3). Examination of serial intervals (i.e., the number of days between symptom onsets in a primary case and a secondary case) in China suggested that 12.6% of transmission was presymptomatic (2). COVID-19 cases in Singapore were reviewed to determine whether presymptomatic transmission occurred among COVID-19 clusters.
The surveillance and case detection methods employed in Singapore have been described (4). Briefly, all medical practitioners were required by law to notify Singapore’s Ministry of Health of suspected and confirmed cases of COVID-19. The definition of a suspected case was based on the presence of respiratory symptoms and an exposure history. Suspected cases were tested, and a confirmed case was defined as a positive test for SARS-CoV-2, using laboratory-based polymerase chain reaction or serologic assays (5). All cases in this report were confirmed by polymerase chain reaction only. Asymptomatic persons were not routinely tested, but such testing was performed for persons in groups considered to be at especially high risk for infection, such as evacuees on flights from Wuhan, China (6), or families that experienced high attack rates.
Patients with confirmed COVID-19 were interviewed to obtain information about their clinical symptoms and activity history during the 2 weeks preceding symptom onset to ascertain possible sources of infection. Contact tracing examined the time from symptom onset until the time the patient was successfully isolated to identify contacts who had interactions with the patient. All contacts were monitored daily for their health status, and those who developed symptoms were tested as part of active case finding.
Clinical and epidemiologic data for all 243 reported COVID-19 cases in Singapore during January 23–March 16 were reviewed. Clinical histories were examined to identify symptoms before, during, and after the first positive SARS-CoV-2 test.
Records of cases that were epidemiologically linked (clusters) were reviewed to identify instances of likely presymptomatic transmission. Such clusters had clear contact between a source patient and a patient infected by the source (a secondary patient), had no other likely explanations for infection, and had the source patient’s date of symptom onset occurring after the date of exposure to the secondary patient who was subsequently infected. Symptoms considered in the review included respiratory, gastrointestinal (e.g., diarrhea), and constitutional symptoms. In addition, the source patient’s exposure had to be strongly attributed epidemiologically to transmission from another source. This reduced the likelihood that an unknown source was involved in the cases in the cluster.
Seven Clusters of COVID-19 Cases Suggesting Presymptomatic Transmission
Investigation of COVID-19 cases in Singapore identified seven clusters (clusters A–G) in which presymptomatic transmission likely occurred. These clusters occurred during January 19–March 12, and involved from two to five patients each (Figure). Ten of the cases within these clusters were attributed to presymptomatic transmission and accounted for 6.4% of the 157 locally acquired cases reported as of March 16.
Seven Clusters of COVID-19 Cases Suggesting Presymptomatic Transmission
Investigation of COVID-19 cases in Singapore identified seven clusters (clusters A–G) in which presymptomatic transmission likely occurred. These clusters occurred during January 19–March 12, and involved from two to five patients each (Figure). Ten of the cases within these clusters were attributed to presymptomatic transmission and accounted for 6.4% of the 157 locally acquired cases reported as of March 16.
Cluster A. A woman aged 55 years (patient A1) and a man aged 56 years (patient A2) were tourists from Wuhan, China, who arrived in Singapore on January 19. They visited a local church the same day and had symptom onset on January 22 (patient A1) and January 24 (patient A2). Three other persons, a man aged 53 years (patient A3), a woman aged 39 years (patient A4), and a woman aged 52 years (patient A5) attended the same church that day and subsequently developed symptoms on January 23, January 30, and February 3, respectively. Patient A5 occupied the same seat in the church that patients A1 and A2 had occupied earlier that day (captured by closed-circuit camera) (5). Investigations of other attendees did not reveal any other symptomatic persons who attended the church that day.
Cluster B. A woman aged 54 years (patient B1) attended a dinner event on February 15 where she was exposed to a patient with confirmed COVID-19. On February 24, patient B1 and a woman aged 63 years (patient B2) attended the same singing class. Two days later (February 26), patient B1 developed symptoms; patient B2 developed symptoms on February 29.
Cluster C. A woman aged 53 years (patient C1) was exposed to a patient with confirmed COVID-19 on February 26 and likely passed the infection to her husband, aged 59 years (patient C2) during her presymptomatic period; both patients developed symptoms on March 5.
Cluster D. A man aged 37 years (patient D1) traveled to the Philippines during February 23–March 2, where he was in contact with a patient with pneumonia who later died. Patient D1 likely transmitted the infection to his wife (patient D2), aged 35 years, during his presymptomatic period. Both patients developed symptoms on March 8.
Cluster E. A man aged 32 years (patient E1) traveled to Japan during February 29–March 8, where he was likely infected, and subsequently transmitted the infection to his housemate, a woman aged 27 years (patient E2), before he developed symptoms. Both developed symptoms on March 11.
Cluster F. A woman aged 58 years (patient F1) attended a singing class on February 27, where she was exposed to a patient with confirmed COVID-19. She attended a church service on March 1, where she likely infected a woman aged 26 years (patient F2) and a man aged 29 years (patient F3), both of whom sat one row behind her. Patient F1 developed symptoms on March 3, and patients F2 and F3 developed symptoms on March 3 and March 5, respectively.
Cluster G. A man aged 63 years (patient G1) traveled to Indonesia during March 3–7. He met a woman aged 36 years (patient G2) on March 8 and likely transmitted SARS-CoV-2 to her; he developed symptoms on March 9, and patient G2 developed symptoms on March 12.
Investigation of these clusters did not identify other patients who could have transmitted COVID-19 to the persons infected. In four clusters (A, B, F, and G), presymptomatic transmission exposure occurred 1–3 days before the source patient developed symptoms. For the remaining three clusters (C, D, and E), the exact timing of transmission exposure could not be ascertained because the persons lived together, and exposure was continual.
Discussion
This investigation identified seven clusters of COVID-19 in Singapore in which presymptomatic transmission likely occurred. Among the 243 cases of COVID-19 reported in Singapore as of March 16, 157 were locally acquired; 10 of the 157 (6.4%) locally acquired cases are included in these clusters and were attributed to presymptomatic transmission. These findings are supported by other studies that suggest that presymptomatic transmission of COVID-19 can occur (1–3). An examination of transmission events among cases in Chinese patients outside of Hubei province, China, suggested that 12.6% of transmissions could have occurred before symptom onset in the source patient (3).
Presymptomatic transmission might occur through generation of respiratory droplets or possibly through indirect transmission. Speech and other vocal activities such as singing have been shown to generate air particles, with the rate of emission corresponding to voice loudness (7). News outlets have reported that during a choir practice in Washington on March 10, presymptomatic transmission likely played a role in SARS-CoV-2 transmission to approximately 40 of 60 choir members.*
Environmental contamination with SARS-CoV-2 has been documented (8), and the possibility of indirect transmission through fomites by presymptomatic persons is also a concern. Objects might be contaminated directly by droplets or through contact with an infected person’s contaminated hands and transmitted through nonrigorous hygiene practices.
Investigation of these clusters did not identify other patients who could have transmitted COVID-19 to the persons infected. In four clusters (A, B, F, and G), presymptomatic transmission exposure occurred 1–3 days before the source patient developed symptoms. For the remaining three clusters (C, D, and E), the exact timing of transmission exposure could not be ascertained because the persons lived together, and exposure was continual.
Discussion
This investigation identified seven clusters of COVID-19 in Singapore in which presymptomatic transmission likely occurred. Among the 243 cases of COVID-19 reported in Singapore as of March 16, 157 were locally acquired; 10 of the 157 (6.4%) locally acquired cases are included in these clusters and were attributed to presymptomatic transmission. These findings are supported by other studies that suggest that presymptomatic transmission of COVID-19 can occur (1–3). An examination of transmission events among cases in Chinese patients outside of Hubei province, China, suggested that 12.6% of transmissions could have occurred before symptom onset in the source patient (3).
Presymptomatic transmission might occur through generation of respiratory droplets or possibly through indirect transmission. Speech and other vocal activities such as singing have been shown to generate air particles, with the rate of emission corresponding to voice loudness (7). News outlets have reported that during a choir practice in Washington on March 10, presymptomatic transmission likely played a role in SARS-CoV-2 transmission to approximately 40 of 60 choir members.*
Environmental contamination with SARS-CoV-2 has been documented (8), and the possibility of indirect transmission through fomites by presymptomatic persons is also a concern. Objects might be contaminated directly by droplets or through contact with an infected person’s contaminated hands and transmitted through nonrigorous hygiene practices.
The possibility of presymptomatic transmission of SARS-CoV-2 increases the challenges of COVID-19 containment measures, which are predicated on early detection and isolation of symptomatic persons. The magnitude of this impact is dependent upon the extent and duration of transmissibility while a patient is presymptomatic, which, to date, have not been clearly established. In four clusters (A, B, F, and G), it was possible to determine that presymptomatic transmission exposure occurred 1–3 days before the source patient developed symptoms. Such transmission has also been observed in other respiratory viruses such as influenza. However, transmissibility by presymptomatic persons requires further study.
The findings in this report are subject to at least three limitations. First, although these cases were carefully investigated, the possibility exists that an unknown source might have initiated the clusters described. Given that there was not widespread community transmission of COVID-19 in Singapore during the period of evaluation and while strong surveillance systems were in place to detect cases, presymptomatic transmission was estimated to be more likely than the occurrence of unidentified sources. Further, contact tracing undertaken during this period was extensive and would likely have detected other symptomatic cases. Second, recall bias could affect the accuracy of symptom onset dates reported by cases, especially if symptoms were mild, resulting in uncertainty about the duration of the presymptomatic period. Finally, because of the nature of detection and surveillance activities that focus on testing symptomatic persons, underdetection of asymptomatic illness is expected. Recall bias and interviewer bias (i.e., the expectation that some symptoms were present, no matter how mild), could have contributed to this.
The evidence of presymptomatic transmission in Singapore, in combination with evidence from other studies (9,10) supports the likelihood that viral shedding can occur in the absence of symptoms and before symptom onset. This study identified seven clusters of cases in which presymptomatic transmission of COVID-19 likely occurred; 10 (6.4%) of such cases included in these clusters were among the 157 locally acquired cases reported in Singapore as of March 16. Containment measures should account for the possibility of presymptomatic transmission by including the period before symptom onset when conducting contact tracing. These findings also suggest that to control the pandemic it might not be enough for only persons with symptoms to limit their contact with others because persons without symptoms might transmit infection. Finally, these findings underscore the importance of social distancing in the public health response to the COVID-19 pandemic, including the avoidance of congregate settings.
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Corresponding author: Vernon J. Lee, Vernon_Lee@moh.gov.sg.
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1Ministry of Health, Singapore; 2National Centre for Infectious Diseases, Singapore; 3Saw Swee Hock School of Public Health, Singapore.
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All authors have completed and submitted the International Committee of Medical Journal Editors form for disclosure of potential conflicts of interest. No potential conflicts of interest were disclosed.
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* https://www.latimes.com/world-nation/story/2020-03-29/coronavirus-choir-outbreak
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