J Korean Med Sci.  2020 Dec;35(48):e424. 10.3346/jkms.2020.35.e424.

COVID-19 Outbreak and Presymptomatic Transmission in Pilgrim Travelers Who Returned to Korea from Israel

• Park JH
• Jang JH
• Lee K
• Yoo SJ
• Shin H

• KMID: 2509529
• DOI: http://doi.org/10.3346/jkms.2020.35.e424

Abstract

Background
On February 21, 2020, 2 coronavirus disease 2019 (COVID-19) cases in pilgrim travelers from Korea to Israel were identified. We investigated the source of infection, clinical features of COVID-19, and transmission potential of presymptomatic and asymptomatic cases.
Methods
All 39 pilgrim travelers were aggressively tested for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Their clinical features and possible source of infection were investigated by interview and review of their medical records. Ten confirmed cases without symptoms at the first sampling dates were selected for follow-up reverse transcription polymerase chain reaction tests.
Results
Of the 39 pilgrim travelers, 30 (77%) were positive for SARS-CoV-2. Among the 30 positive COVID-19 cases, 4 (13%) were asymptomatic. Available follow-up cycle threshold values from 10 cases gradually increased over time and were lower during the presymptomatic period than during the postsymptomatic period. Out of 328 contacts related to the COVID-19 cases in the pilgrim travelers, 22 additional cases (7%) were confirmed with SARS-CoV-2 infections. Three tertiary cases were identified to be transmitted by presymptomatic secondary cases.
Conclusion
To prevent transmission of COVID-19, we need to focus on presymptomatic and asymptomatic cases, and massive testing for SARS-CoV-2 is required. More research about the possibility of presymptomatic transmission over 2 days before symptom onset is required.

Keyword

COVID-19; Severe Acute Respiratory Syndrome Coronavirus 2; Outbreaks; Transmission

Figure

• 

  Fig. 1 Epidemic curve of the outbreak in pilgrim travelers from Korea (symptomatic cases).

• 

  Fig. 2 Follow-up viral loads relative to sampling dates and days from symptom onset.Plots show the available Ct values relative to sampling dates for 10 cases from the upper respiratory tract specimens (nasopharyngeal plus oropharyngeal swabs; A) and 10 cases from the lower respiratory tract specimens (sputum; B). The available Ct values relative to days from symptom onset from the upper respiratory tract (C) and the lower respiratory tract (D) specimens for 6 symptomatic cases are shown. The circles are symptomatic cases and the squares are asymptomatic cases.Ct = cycle threshold.

• 

  Fig. 3 Contact diagram of coronavirus disease 2019 cases related to pilgrim travelers.The son of the primary case was not included in the result, considering the uncertainty of information on symptom onset.

Reference

1. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020; 382(8):727–733. PMID: 31978945.

2. World Health Organization. Coronavirus disease 2019 (COVID-19) weekly operational update 9 October 2020. Updated 2020. Accessed October 19, 2020. http://www.who.int/publications/m/item/weekly-update-on-covid-19-9-october-2020.

3. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020; 395(10229):1054–1062. PMID: 32171076.

4. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020; 382(18):1708–1720. PMID: 32109013.

5. Lipsitch M, Swerdlow DL, Finelli L. Defining the epidemiology of Covid-19 – studies needed. N Engl J Med. 2020; 382(13):1194–1196. PMID: 32074416.

6. Furukawa NW, Brooks JT, Sobel J. Evidence supporting transmission of severe acute respiratory syndrome coronavirus 2 while presymptomatic or asymptomatic. Emerg Infect Dis. 2020; 26(7):e201595.

7. Cheng HY, Jian SW, Liu DP, Ng TC, Huang WT, Lin HH, et al. Contact tracing assessment of COVID-19 transmission dynamics in Taiwan and risk at different exposure periods before and after symptom onset. JAMA Intern Med. 2020; 180(9):1156–1163. PMID: 32356867.

8. World Health Organization. Contact tracing in the context of COVID-19. Updated 2020. Accessed July 20, 2020. http://www.who.int/publications/i/item/contact-tracing-in-the-context-of-covid-19.

9. Kim SE, Jeong HS, Yu Y, Shin SU, Kim S, Oh TH, et al. Viral kinetics of SARS-CoV-2 in asymptomatic carriers and presymptomatic patients. Int J Infect Dis. 2020; 95:441–443. PMID: 32376309.

10. Korean Society of Infectious Diseases. Korean Society of Pediatric Infectious Diseases. Korean Society of Epidemiology. Korean Society for Antimicrobial Therapy. Korean Society for Healthcare-associated Infection Control and Prevention. Korea Centers for Disease Control and Prevention. Report on the epidemiological features of Coronavirus Disease 2019 (COVID-19) outbreak in the Republic of Korea from January 19 to March 2, 2020. J Korean Med Sci. 2020; 35(10):e112. PMID: 32174069.

11. Ministry of Health - State of Israel. Coronavirus patients summary announcement. Updated 2020. Accessed July 20, 2020. http://www.health.gov.il/English/News_and_Events/Spokespersons_Messages/Pages/28022020_4.aspx.

12. Ministry of Health - State of Israel. Investigation findings update on patient no. 7 from Italy. Updated 2020. Accessed July 20, 2020. http://www.health.gov.il/English/News_and_Events/Spokespersons_Messages/Pages/29022020_2.aspx.

13. Central Disease Control Headquarters. Coronavirus disease 2019 response guidelines for local governments in South Korea, edition 6. Updated 2020. Accessed September 17, 2020. http://www.gidcc.or.kr/epvbr/코로나바이러스감염증-19covid-19.

14. Central Disease Control Headquarters. Coronavirus disease 2019 response guidelines for local governments in South Korea, edition 7-4. Updated 2020. Accessed September 17, 2020. http://www.gidcc.or.kr/epvbr/코로나바이러스감염증-19covid-19.

15. Hong KH, Lee SW, Kim TS, Huh HJ, Lee J, Kim SY, et al. Guidelines for laboratory diagnosis of Coronavirus Disease 2019 (COVID-19) in Korea. Ann Lab Med. 2020; 40(5):351–360. PMID: 32237288.

16. Central Disease Control Headquarters. Coronavirus disease 2019 response guidelines for local governments in South Korea, edition 7. Updated 2020. Accessed September 17, 2020. http://www.gidcc.or.kr/epvbr/코로나바이러스감염증-19covid-19.

17. Jing QL, Liu MJ, Zhang ZB, Fang LQ, Yuan J, Zhang AR, et al. Household secondary attack rate of COVID-19 and associated determinants in Guangzhou, China: a retrospective cohort study. Lancet Infect Dis. 2020; 20(10):1141–1150. PMID: 32562601.

18. Kimball A, Hatfield KM, Arons M, James A, Taylor J, Spicer K, et al. Asymptomatic and presymptomatic SARS-CoV-2 infections in residents of a long-term care skilled nursing facility – King County, Washington, March 2020. MMWR Morb Mortal Wkly Rep. 2020; 69(13):377–381. PMID: 32240128.

19. Mizumoto K, Kagaya K, Zarebski A, Chowell G. Estimating the asymptomatic proportion of coronavirus disease 2019 (COVID-19) cases on board the Diamond Princess cruise ship, Yokohama, Japan, 2020. Euro Surveill. 2020; 25(10):200180.

20. Ip DK, Lau LL, Leung NH, Fang VJ, Chan KH, Chu DK, et al. Viral shedding and transmission potential of asymptomatic and paucisymptomatic influenza virus infection in the community. Clin Infect Dis. 2017; 64(6):736–742. PMID: 28011603.

21. Zou L, Ruan F, Huang M, Liang L, Huang H, Hong Z, et al. SARS-CoV-2 viral load in the upper respiratory specimens of infected patients. N Engl J Med. 2020; 382(12):1177–1179. PMID: 32074444.

22. Arons MM, Hatfield KM, Reddy SC, Kimball A, James A, Jacobs JR, et al. Presymptomatic SARS-CoV-2 infections and transmission in a skilled nursing facility. N Engl J Med. 2020; 382(22):2081–2090. PMID: 32329971.

23. Backer JA, Klinkenberg D, Wallinga J. Incubation period of 2019 novel coronavirus (2019-nCoV) infections among travellers from Wuhan, China, 20–28 January 2020. Euro Surveill. 2020; 25(5):2000062.

24. Kang YJ. Lessons learned from cases of COVID-19 infection in South Korea. Disaster Med Public Health Prep. 2020; 1–8.

25. Park SY, Kim YM, Yi S, Lee S, Na BJ, Kim CB, et al. Coronavirus disease outbreak in call center, South Korea. Emerg Infect Dis. 2020; 26(8):1666–1670. PMID: 32324530.

26. Qian GQ, Yang NB, Ding F, Ma AH, Wang ZY, Shen YF, et al. Epidemiologic and clinical characteristics of 91 hospitalized patients with COVID-19 in Zhejiang, China: a retrospective, multi-centre case series. QJM. 2020; 113(7):474–481. PMID: 32181807.

27. Eldin C, Lagier JC, Mailhe M, Gautret P. Probable aircraft transmission of Covid-19 in-flight from the Central African Republic to France. Travel Med Infect Dis. 2020; 35:101643. PMID: 32247016.