Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 26, Number 6—June 2020

Identifying and Interrupting Superspreading Events—Implications for Control of Severe Acute Respiratory Syndrome Coronavirus 2

Thomas R. Frieden1Comments to Author  and Christopher T. Lee1
Author affiliations: Resolve to Save Lives, New York, New York, USA

Main Article


Factors that increase the risk for superspreading events and implications for prevention and control of COVID-19*

Factor Disease Epidemiologic role Implications for control of COVID-19
Certain strains of Mycobacterium tuberculosis are more infectious, and patients ill with these strains should be prioritized for examination of a larger circle of contacts (21,22)
Continued monitoring for genetic change and for changes in the epidemiology of transmission
Viral shedding and risk for transmission among asymptomatic and presymptomatic persons can result in influenza transmission (23), particularly in closed settings with minimal ventilation (H. Nishiura et al., unpub. data,
Identification of factors associated with increased transmissibility and rapid intervention to prevent transmission from similar patients prospectively; further characterization of risk for asymptomatic transmission
Airborne transmission of SARS can result in environmental spread of disease in community (24) and healthcare settings (25)
Assess changes in plumbing and ventilation that may be needed to reduce risk for spread; increase social distancing; reduce mass gatherings in closed environments; ensure effective triage, isolation, and general infection control in healthcare facilities
Inaccurate perceptions of Ebola risk can result in behaviors that increase the probability of transmission (26,27)
Promote handwashing, cough etiquette, and safer care-seeking behavior, including mask-wearing by persons who are ill, and ensure that timely and accurate messaging about risk and behavioral preventive measures are tailored to and reach affected populations
Response MERS Timely implementation of control measures can reduce outbreak duration and number of transmission events (28) Rapidly identify and isolate cases to reduce transmission; implement large-scale NPIs in affected areas within 1 week

*COVID-19, coronavirus disease; MERS, Middle East respiratory syndrome; NPIs, nonpharmaceutical interventions; SARS, severe acute respiratory syndrome.

Main Article

  1. World Health Organization. Coronavirus disease 2019 (COVID-19) situation reports, 2020 [cited 2020 Mar 8].
  2. Why 14 doctors in Wuhan were infected: no eyepieces and masks were worn during surgery Shanghai: Shanghai First Finance Media Limited, January 22, 2020 [cited 2020 Mar 8].
  3. Wang  D, Hu  B, Hu  C, Zhu  F, Liu  X, Zhang  J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020 [Epub ahead of print].
  4. South Korean city on high alert as coronavirus cases soar at ‘cult’ church. New York: The Guardian, February 20, 2020 [cited 2020 Mar 8].
  5. Wong  G, Liu  W, Liu  Y, Zhou  B, Bi  Y, Gao  GF. MERS, SARS, and Ebola: the role of super-spreaders in infectious disease. Cell Host Microbe. 2015;18:398401. DOIPubMedGoogle Scholar
  6. Lau  MS, Dalziel  BD, Funk  S, McClelland  A, Tiffany  A, Riley  S, et al. Spatial and temporal dynamics of superspreading events in the 2014-2015 West Africa Ebola epidemic. Proc Natl Acad Sci U S A. 2017;114:233742. DOIPubMedGoogle Scholar
  7. Wallinga  J, Teunis  P. Different epidemic curves for severe acute respiratory syndrome reveal similar impacts of control measures. Am J Epidemiol. 2004;160:50916. DOIPubMedGoogle Scholar
  8. Leavitt  J. Typhoid Mary: captive to the public’s health. Boston: Beacon Press; 1996.
  9. Marineli  F, Tsoucalas  G, Karamanou  M, Androutsos  G. Mary Mallon (1869-1938) and the history of typhoid fever. Ann Gastroenterol. 2013;26:1324.PubMedGoogle Scholar
  10. Prouty  AM, Schwesinger  WH, Gunn  JS. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun. 2002;70:26409. DOIPubMedGoogle Scholar
  11. Riley  RL, Mills  CC, O’Grady  F, Sultan  LU, Wittstadt  F, Shivpuri  DN. Infectiousness of air from a tuberculosis ward. Ultraviolet irradiation of infected air: comparative infectiousness of different patients. Am Rev Respir Dis. 1962;85:51125.PubMedGoogle Scholar
  12. Woolhouse  ME, Dye  C, Etard  JF, Smith  T, Charlwood  JD, Garnett  GP, et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci U S A. 1997;94:33842. DOIPubMedGoogle Scholar
  13. Shimizu  K, Kinoshita  R, Yoshii  K, Akhmetzhanov  AR, Jung  S, Lee  H, et al. An investigation of a measles outbreak in Japan and China, Taiwan, China, March-May 2018. Western Pac Surveill Response J. 2018;9:2531. DOIPubMedGoogle Scholar
  14. Shen  Z, Ning  F, Zhou  W, He  X, Lin  C, Chin  DP, et al. Superspreading SARS events, Beijing, 2003. Emerg Infect Dis. 2004;10:25660. DOIPubMedGoogle Scholar
  15. Chun  BC. Understanding and modeling the super-spreading events of the Middle East respiratory syndrome outbreak in Korea. Infect Chemother. 2016;48:1479. DOIPubMedGoogle Scholar
  16. Lloyd-Smith  JO, Schreiber  SJ, Kopp  PE, Getz  WM. Superspreading and the effect of individual variation on disease emergence. Nature. 2005;438:3559. DOIPubMedGoogle Scholar
  17. Liu  Y, Gayle  AA, Wilder-Smith  A, Rocklöv  J. The reproductive number of COVID-19 is higher compared to SARS coronavirus. J Travel Med. 2020;27:taaa021; Epub ahead of print. DOIPubMedGoogle Scholar
  18. Rocklöv  J, Sjödin  H, Wilder-Smith  A. COVID-19 outbreak on the Diamond Princess cruise ship: estimating the epidemic potential and effectiveness of public health countermeasures. J Travel Med. 2020;taaa030; Epub ahead of print. DOIPubMedGoogle Scholar
  19. Bauch  CT, Lloyd-Smith  JO, Coffee  MP, Galvani  AP. Dynamically modeling SARS and other newly emerging respiratory illnesses: past, present, and future. Epidemiology. 2005;16:791801. DOIPubMedGoogle Scholar
  20. Lloyd-Smith  JO, Galvani  AP, Getz  WM. Curtailing transmission of severe acute respiratory syndrome within a community and its hospital. Proc Biol Sci. 2003;270:197989. DOIPubMedGoogle Scholar
  21. Luo  T, Comas  I, Luo  D, Lu  B, Wu  J, Wei  L, et al. Southern East Asian origin and coexpansion of Mycobacterium tuberculosis Beijing family with Han Chinese. Proc Natl Acad Sci U S A. 2015;112:813641. DOIPubMedGoogle Scholar
  22. Holt  KE, McAdam  P, Thai  PVK, Thuong  NTT, Ha  DTM, Lan  NN, et al. Frequent transmission of the Mycobacterium tuberculosis Beijing lineage and positive selection for the EsxW Beijing variant in Vietnam. Nat Genet. 2018;50:84956. DOIPubMedGoogle Scholar
  23. 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 infections in the community. Clin Infect Dis. 2017;64:73642.PubMedGoogle Scholar
  24. Yu  IT, Li  Y, Wong  TW, Tam  W, Chan  AT, Lee  JH, et al. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N Engl J Med. 2004;350:17319. DOIPubMedGoogle Scholar
  25. Yu  IT, Xie  ZH, Tsoi  KK, Chiu  YL, Lok  SW, Tang  XP, et al. Why did outbreaks of severe acute respiratory syndrome occur in some hospital wards but not in others? Clin Infect Dis. 2007;44:101725. DOIPubMedGoogle Scholar
  26. Nielsen  CF, Kidd  S, Sillah  AR, Davis  E, Mermin  J, Kilmarx  PH; Centers for Disease Control and Prevention. Improving burial practices and cemetery management during an Ebola virus disease epidemic - Sierra Leone, 2014. MMWR Morb Mortal Wkly Rep. 2015;64:207.PubMedGoogle Scholar
  27. Faye  O, Boëlle  PY, Heleze  E, Faye  O, Loucoubar  C, Magassouba  N, et al. Chains of transmission and control of Ebola virus disease in Conakry, Guinea, in 2014: an observational study. Lancet Infect Dis. 2015;15:3206. DOIPubMedGoogle Scholar
  28. Lee  J, Chowell  G, Jung  E. A dynamic compartmental model for the Middle East respiratory syndrome outbreak in the Republic of Korea: A retrospective analysis on control interventions and superspreading events. J Theor Biol. 2016;408:11826. DOIPubMedGoogle Scholar
  29. Richard  M, Fouchier  RA. Influenza A virus transmission via respiratory aerosols or droplets as it relates to pandemic potential. FEMS Microbiol Rev. 2016;40:6885. DOIPubMedGoogle Scholar
  30. Tang  X, Wu  C, Li  X, Song  Y, Yao  X, Wu  X, et al. On the origin and continuing evolution of SARS-CoV-2. Natl Sci Rev. 2020;nwaa036; [Epub ahead of print]. DOIGoogle Scholar
  31. Yu  P, Zhu  J, Zhang  Z, Han  Y, Huang  L. A familial cluster of infection associated with the 2019 novel coronavirus indicating potential person-to-person transmission during the incubation period. J Infect Dis. 2020;jiaa077; Epub ahead of print. DOIPubMedGoogle Scholar
  32. Kupperscmidt  K. Study claiming new coronavirus can be transmitted by people without symptoms was flawed. Washington: American Association for the Advancement of Science, February 3, 2020 [cited 2020 Mar 8].
  33. Gu  J, Han  B, Wang  J. COVID-19: Gastrointestinal manifestations and potential fecal-oral transmission. Gastroenterology. 2020;Mar 3:pii: S0016-5085(20)30281-X. Epub ahead of print].
  34. Ong  SWX, Tan  YK, Chia  PY, Lee  TH, Ng  OT, Wong  MSY, et al. Air, surface environmental, and personal protective equipment contamination by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from a symptomatic patient. JAMA. 2020; Epub ahead of print. DOIPubMedGoogle Scholar
  35. Curran  KG, Gibson  JJ, Marke  D, Caulker  V, Bomeh  J, Redd  JT, et al. Cluster of Ebola virus disease linked to a single funeral—Moyamba District, Sierra Leone, 2014. MMWR Morb Mortal Wkly Rep. 2016;65:2025. DOIPubMedGoogle Scholar
  36. Kim  SW, Park  JW, Jung  HD, Yang  JS, Park  YS, Lee  C, et al. Risk factors for transmission of Middle East respiratory syndrome coronavirus infection during the 2015 outbreak in South Korea. Clin Infect Dis. 2017;64:5517.PubMedGoogle Scholar
  37. Zhao  S, Lin  Q, Ran  J, Musa  SS, Yang  G, Wang  W, et al. Preliminary estimation of the basic reproduction number of novel coronavirus (2019-nCoV) in China, from 2019 to 2020: A data-driven analysis in the early phase of the outbreak. Int J Infect Dis. 2020;92:2147. DOIPubMedGoogle Scholar
  38. Hellewell  J, Abbott  S, Gimma  A, Bosse  NI, Jarvis  CI, Russell  TW, et al.; Centre for the Mathematical Modelling of Infectious Diseases COVID-19 Working Group. Feasibility of controlling COVID-19 outbreaks by isolation of cases and contacts. Lancet Glob Health. 2020;8:e48896; Epub ahead of print. DOIPubMedGoogle Scholar
  39. Park  GE, Ko  JH, Peck  KR, Lee  JY, Lee  JY, Cho  SY, et al. Control of an outbreak of Middle East respiratory syndrome in a tertiary hospital in Korea. Ann Intern Med. 2016;165:8793. DOIPubMedGoogle Scholar
  40. World Health Organization. Clinical management of severe acute respiratory infection when novel coronavirus (2019-nCoV) infection is suspected: interim guidance, January 28, 2020 [cited 2020 Mar 8].
  41. Amer  H, Alqahtani  AS, Alzoman  H, Aljerian  N, Memish  ZA. Unusual presentation of Middle East respiratory syndrome coronavirus leading to a large outbreak in Riyadh during 2017. Am J Infect Control. 2018;46:10225. DOIPubMedGoogle Scholar
  42. Lee  CT, Hagan  JE, Jantsansengee  B, Tumurbaatar  OE, Altanchimeg  S, Yadamsuren  B, et al. Increase in infant measles deaths during a nationwide measles outbreak, Mongolia, 2015–2016. J Infect Dis. 2019;220:17719. DOIPubMedGoogle Scholar
  43. Frieden  TR, Sherman  LF, Maw  KL, Fujiwara  PI, Crawford  JT, Nivin  B, et al. A multi-institutional outbreak of highly drug-resistant tuberculosis: epidemiology and clinical outcomes. JAMA. 1996;276:122935. DOIPubMedGoogle Scholar
  44. Liang  W, Zhu  Z, Guo  J, Liu  Z, Zhou  W, Chin  DP, et al.; Beijing Joint SARS Expert Group. Severe acute respiratory syndrome, Beijing, 2003. Emerg Infect Dis. 2004;10:2531. DOIPubMedGoogle Scholar
  45. Riley  S, Fraser  C, Donnelly  CA, Ghani  AC, Abu-Raddad  LJ, Hedley  AJ, et al. Transmission dynamics of the etiological agent of SARS in Hong Kong: impact of public health interventions. Science. 2003;300:19616. DOIPubMedGoogle Scholar
  46. Centers for Disease Control and Prevention (CDC). Update: Outbreak of severe acute respiratory syndrome—worldwide, 2003. MMWR Morb Mortal Wkly Rep. 2003;52:2416, 248.PubMedGoogle Scholar
  47. Anderson  RM, Fraser  C, Ghani  AC, Donnelly  CA, Riley  S, Ferguson  NM, et al. Epidemiology, transmission dynamics and control of SARS: the 2002-2003 epidemic. Philos Trans R Soc Lond B Biol Sci. 2004;359:1091105. DOIPubMedGoogle Scholar
  48. Lai  S, Ruktanonchai  NW, Zhou  L, Prosper  O, Luo  W, Wesolowski  A, et al. Effect of nonpharmaceutical interventions for containing the COVID-19 outbreak: an observational and modelling study. World Population. 2020 Mar 4 [cited 2020 Mar 8].

Main Article

1These authors contributed equally to this article.

Page created: May 18, 2020
Page updated: May 18, 2020
Page reviewed: May 18, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.