1887
Review Open Access
Like 0

Abstract

Background

Cruise ships provide an ideal setting for transmission of SARS-CoV-2, given the socially dense exposure environment.

Aim

To provide a comprehensive review of COVID-19 outbreaks on cruise ships.

Methods

PubMed was searched for COVID-19 cases associated with cruise ships between January and October 2020. A list of cruise ships with COVID-19 was cross-referenced with the United States Centers for Disease Control and Prevention’s list of cruise ships associated with a COVID-19 case within 14 days of disembarkation. News articles were also searched for epidemiological information. Narratives of COVID-19 outbreaks on ships with over 100 cases are presented.

Results

Seventy-nine ships and 104 unique voyages were associated with COVID-19 cases before 1 October 2020. Nineteen ships had more than one voyage with a case of COVID-19. The median number of cases per ship was three (interquartile range (IQR): 1–17.8), with two notable outliers: the Diamond Princess and the Ruby Princess, which had 712 and 907 cases, respectively. The median attack rate for COVID-19 was 0.2% (IQR: 0.03–1.5), although this distribution was right-skewed with a mean attack rate of 3.7%; 25.9% (27/104) of voyages had at least one COVID-19-associated death. Outbreaks involving only crew occurred later than outbreaks involving guests and crew.

Conclusions

In the absence of mitigation measures, COVID-19 can spread easily on cruise ships in a susceptible population because of the confined space and high-density contact networks. This environment can create superspreader events and facilitate international spread.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2022.27.1.2002113
2022-01-06
2022-01-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.1.2002113
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/27/1/eurosurv-27-1-6.html?itemId=/content/10.2807/1560-7917.ES.2022.27.1.2002113&mimeType=html&fmt=ahah

References

  1. Li Q, Guan X, Wu P, Wang X, Zhou L, Tong Y, et al. Early transmission dynamics in Wuhan, China, of novel coronavirus–infected pneumonia. N Engl J Med. 2020;382(13):1199-207.  https://doi.org/10.1056/NEJMoa2001316  PMID: 31995857 
  2. Kasper MR, Geibe JR, Sears CL, Riegodedios AJ, Luse T, Von Thun AM, et al. An outbreak of Covid-19 on an aircraft carrier. N Engl J Med. 2020;383(25):2417-26.  https://doi.org/10.1056/NEJMoa2019375  PMID: 33176077 
  3. Pavli A, Maltezou HC, Papadakis A, Katerelos P, Saroglou G, Tsakris A, et al. Respiratory infections and gastrointestinal illness on a cruise ship: A three-year prospective study. Travel Med Infect Dis. 2016;14(4):389-97.  https://doi.org/10.1016/j.tmaid.2016.05.019  PMID: 27320130 
  4. Towers S, Chen J, Cruz C, Melendez J, Rodriguez J, Salinas A, et al. Quantifying the relative effects of environmental and direct transmission of norovirus. R Soc Open Sci. 2018;5(3):170602.  https://doi.org/10.1098/rsos.170602  PMID: 29657742 
  5. Zhang N, Miao R, Huang H, Chan EY. Contact infection of infectious disease onboard a cruise ship. Sci Rep. 2016;6(1):38790.  https://doi.org/10.1038/srep38790  PMID: 27929141 
  6. Cruise Line International Association (CLIA). State of the cruise industry outlook 2020. London: CLIA; 2020. Available from: https://cruising.org/-/media/research-updates/research/state-of-the-cruise-industry.ashx
  7. Moriarty LF, Plucinski MM, Marston BJ, Kurbatova EV, Knust B, Murray EL, et al. Public health responses to COVID-19 outbreaks on cruise ships—worldwide, February–March 2020. MMWR Morb Mortal Wkly Rep. 2020;69(12):347-52.  https://doi.org/10.15585/mmwr.mm6912e3  PMID: 32214086 
  8. Centers for Disease Prevention and Control (CDC). U.S. Department of Health and Human Services (HHS) Centers for Disease Control and Prevention (CDC). Order under sections 361 & 365 of the Public Health Service Act (42 U.S.C. 264, 286) and 42 code of federal regulations part 70 (interstate) and part 71 (foreign): Temporary extension & modification of framework for conditional sailing order. Atlanta: CDC; 2021. Available from: https://www.cdc.gov/quarantine/cruise/pdf/CDC-CSO-Extension-10-25-21-p.pdf
  9. Fox A. 2 MSC Cruises to resume sailing in Europe next week while princess cruises halts Asia voyages. New York City: Travel and Leisure; 10 Aug 2020. Available from: https://www.travelandleisure.com/cruises/msc-cruises-resume-sailing
  10. Cruise Industry News. MSC Cruises announces massive Europe restart program, 10 ships to sail this summer. New York City: Cruise Industry News; 15 Apr 2021. Available from: https://www.cruiseindustrynews.com/cruise-news/24788-msc-cruises-announces-massive-europe-restart-program-10-ships-to-sail.html
  11. Kordsmeyer AC, Mojtahedzadeh N, Heidrich J, Militzer K, von Münster T, Belz L, et al. Systematic Review on Outbreaks of SARS-CoV-2 on Cruise, Navy and Cargo Ships. Int J Environ Res Public Health. 2021;18(10):5195.  https://doi.org/10.3390/ijerph18105195  PMID: 34068311 
  12. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.  https://doi.org/10.1371/journal.pmed.1000097  PMID: 19621072 
  13. Blaskey S, Nehamas N, Dolven T. COVIDCRUISES_MIAMI_HERALD_DATA. Miami: Miami Herald; [Accessed: 10 Oct 2020]. Available from: https://docs.google.com/spreadsheets/d/1KTJj94nWd88Gml98AbTZKYZejbEJ8q4Xa7oE6g5r9ec/edit#gid=0
  14. Centers for Disease Control and Prevention (CDC). CDC’s role in helping cruise ship travelers during the COVID-19 pandemic 2020. Atlanta: CDC. [Accessed: 5 Oct 2020]. Available from: https://www.cdc.gov/coronavirus/2019-ncov/travelers/cruise-ship/what-cdc-is-doing.html
  15. Dolven T, Blaskey S, Nehamas N, Harris A. Cruise ships sailed on despite the coronavirus, thousands of people paid the price. Miami: Miami Herald; 2020. Available from: https://www.miamiherald.com/news/business/tourism-cruises/article241640166.html
  16. United States Centers for Disease Control and Prevention (CDC). Guidance for cruise ships on influenza-like illness (ili) management. Atlanta: CDC. [Accessed: 05 Oct 2020]. Available from: https://www.cdc.gov/quarantine/cruise/management/guidance-cruise-ships-influenza-updated.html
  17. Helderman RS, Sampson H, Bennett D, Tran AB. The pandemic at sea. Washington, DC: The Washington Post; 2020. Available from: https://www.washingtonpost.com/graphics/2020/politics/cruise-ships-coronavirus
  18. Yamagishi T, Kamiya H, Kakimoto K, Suzuki M, Wakita T. Descriptive study of COVID-19 outbreak among passengers and crew on Diamond Princess cruise ship, Yokohama Port, Japan, 20 January to 9 February 2020. Euro Surveill. 2020;25(23):2000272.  https://doi.org/10.2807/1560-7917.ES.2020.25.23.2000272  PMID: 32553062 
  19. Kakimoto K, Kamiya H, Yamagishi T, Matsui T, Suzuki M, Wakita T. Initial investigation of transmission of COVID-19 among crew members during quarantine of a cruise ship—Yokohama, Japan, February 2020. MMWR Morb Mortal Wkly Rep. 2020;69(11):312-3.  https://doi.org/10.15585/mmwr.mm6911e2  PMID: 32191689 
  20. Expert Taskforce for the COVID-19 Cruise Ship Outbreak. Epidemiology of COVID-19 Outbreak on Cruise Ship Quarantined at Yokohama, Japan, February 2020. Emerg Infect Dis. 2020;26(11):2591-7.  https://doi.org/10.3201/eid2611.201165  PMID: 32822290 
  21. Rich M. We’re in a Petri dish’: How a coronavirus ravaged a cruise ship. New York Times. 22 Feb 2020. Available from: https://www.nytimes.com/2020/02/22/world/asia/coronavirus-japan-cruise-ship.html
  22. Lanz L, Feltault M. The Case of the Diamond Princess: Stranded at Sea in a Pandemic (Part 1). Boston. Boston University School of Hospitality Administration.30 Jun 2020. Available from: https://www.bu.edu/bhr/2020/07/08/the-case-of-the-diamond-princess-stranded-at-sea-in-a-pandemic/
  23. Critic C. When are cruise lines around the world expected to resume service? Pennington: Cruise Critic. [Accessed: 7 May 2021]. Available from: https://www.cruisecritic.co.uk/news/5206
  24. The Maritime Executive. European cruise lines plan to resume more sailings. Fort Lauderdale: The Maritime Executive; 17 Feb 2021. Available from: https://www.maritime-executive.com/article/european-cruise-lines-plan-to-resume-more-sailings
  25. Gallman S, Flores R. At least 13 crew members evacuated as cruise ships carrying people with flu-like symptoms sail off Florida. Atlanta: Cable News Network (CNN); 26 Mar 2020. Available from: https://edition.cnn.com/travel/article/cruise-ship-zaandam-flu-symptoms-florida/index.html
  26. Cruises P. Grand Princess Updates. Santa Clarita: Princess Cruises; 7 Apr 2020. Available from: https://www.princess.com/news/notices_and_advisories/notices/grand-princess-updates.html
  27. Fuller T, Gross J, Cowan J. Remember the Grand Princess? New York City: New York Times; 24 Mar 2020. Available from: https://www.nytimes.com/2020/03/19/us/grand-princess-cruise-passengers-coronavirus.html
  28. Webeck E. Coronavirus: 103 Grand Princess passengers test positive for coronavirus, amid questions over quarantine. San Jose: The Mercury News; 21 Mar 2020. Available from https://www.mercurynews.com/2020/03/26/coronavirus-first-known-deaths-from-stricken-grand-princess-cruise-ship-103-infected
  29. Chung L. Ruby Princess would be dealt with differently if it could be done again: NSW Health. Sydney: The Sydney Morning Herald; 5 May 2020. Available from: https://www.smh.com.au/national/nsw/decision-to-allow-ruby-princess-passengers-ashore-based-on-outdated-log-20200505-p54pyg.html
  30. British Broadcasting Corporation (BBC). Coronavirus: ‘Serious mistakes’ made over Ruby Princess outbreak. London: BBC; 17 Aug 2020. Available from: https://www.bbc.com/news/world-australia-53776285
  31. Alexander H, Koslowski M, Visentin L. Infected Ruby Princess passengers transmit virus to 19 people ashore. Sydney: The Sydney Morning Herald; 8 Apr 2020. Available from: https://www.smh.com.au/national/nsw/infected-ruby-princess-passengers-transmit-virus-to-19-people-ashore-20200407-p54hxg.html
  32. Browne A, St-Onge Ahmad S, Beck CR, Nguyen-Van-Tam JS. The roles of transportation and transportation hubs in the propagation of influenza and coronaviruses: a systematic review. J Travel Med. 2016;23(1):tav002.  https://doi.org/10.1093/jtm/tav002  PMID: 26782122 
  33. Rispens JR, Freeland A, Wittry B, Kramer A, Barclay L, Vinjé J, et al. Notes from the field: multiple cruise ship outbreaks of norovirus associated with frozen fruits and berries - United States, 2019. MMWR Morb Mortal Wkly Rep. 2020;69(16):501-2.  https://doi.org/10.15585/mmwr.mm6916a3  PMID: 32324722 
  34. Qian H, Miao T, Liu L, Zheng X, Luo D, Li Y. Indoor transmission of SARS-CoV-2. Indoor Air. 2021;31(3):639-45.  https://doi.org/10.1111/ina.12766  PMID: 33131151 
  35. Leclerc QJ, Fuller NM, Knight LE, Funk S, Knight GM, CMMID COVID-19 Working Group. What settings have been linked to SARS-CoV-2 transmission clusters? Wellcome Open Res. 2020;5:83.  https://doi.org/10.12688/wellcomeopenres.15889.2  PMID: 32656368 
  36. Taube JC, Miller PB, Drake JM. An open-access database of infectious disease transmission trees to explore superspreader epidemiology. medRxiv. 2021. Preprint.  https://doi.org/10.1101/2021.01.11.21249622 
  37. Nishiura H, Oshitani H, Kobayashi T, Saito T, Sunagawa T, Matsui T, et al. Closed environments facilitate secondary transmission of coronavirus disease 2019 (COVID-19). MedRxiv.2020; (Preprint).  https://doi.org/10.1101/2020.02.28.20029272 
  38. Campbell M. The Carnival cruise ship that spread coronavirus around the world. New York City: Bloomberg Businessweek; 15 Sep 2020. Available from: https://www.bloomberg.com/news/features/2020-09-15/carnival-s-ruby-princess-cruise-ship-spread-coronavirus-around-the-world
  39. Raghavan S, Kornfield M. The tale of how a Nile cruise boosted the international coronavirus outbreak. Washington: The Washington Post; 14 Mar 2020. Available from: https://www.washingtonpost.com/world/middle_east/the-tale-of-a-nile-cruise-that-spawned-an-international-coronavirus-outbreak/2020/03/13/6ab633fc-6314-11ea-8a8e-5c5336b32760_story.html
  40. Edlund A, Poulisse A. Coronavirus: Hundreds of crew members stuck on cruise ship for 40 days off Florida coast. Seattle: KIRO 7; 25 Apr 2020. Available from: https://www.kiro7.com/news/trending/coronavirus-hundreds-crew-members-stuck-cruise-ship-40-days-off-florida-coast/FBULDCS5J5D7PKZW2WG75O3RJI
  41. McLaughlin K. A Florida man who tested positive for COVID-19 says he’s been stuck on a cruise ship in Italy for 8 weeks. New York City: Insider; 18 May 2020. Available from: https://www.insider.com/florida-man-covid-19-stuck-on-cruise-ship-for-weeks-2020-5
  42. Ritchie H, Ortiz-Ospina E, Beltekian D, Mathieu E, Hasell J, Macdonald B, et al. Mortality risk of COVID-19. Oxford: Our World In Data; 2020. Available from: https://ourworldindata.org/mortality-risk-covid#how-did-confirmed-deaths-and-cases-change-over-time
  43. Statista. Cruise industry in Europe – statistics and facts. New York: Statista. [Accessed: 27 Apr 2021]. Available from: https://www.statista.com/topics/4211/cruise-industry-in-europe
  44. Mapper C. Norwegian breakaway accidents and incidents. Cruise Mapper. [Accessed: 1 Oct 2020]. Available from: https://www.cruisemapper.com/accidents/Norwegian-Breakaway-584
  45. Peterson B. A doctor has died on the Norwegian Gem, two weeks after crew members saw another body loaded into an ambulance. New York City: Business Insider; 2020. Available from: https://www.businessinsider.com/norwegian-cruise-line-doctor-dies-on-gem-ship-2020-5
  46. European Maritime Safety Agency. COVID-19: EU Guidance for Cruise Ship Operations. Sweden: 12 May 2021 (Revision 1). Lisbon, Portugal. Available from: https://www.ecdc.europa.eu/en/publications-data/COVID-19-cruise-ship-guidance
  47. Celebritycruises.com. Healthy at sea. [Accessed: 18 Nov 2021]. Available from: https://www.celebritycruises.com/health-and-safety
  48. Royal Caribbean International. Healthy sail center. royalcaribbean.com. [Accessed: 18 Nov 2021]. Available from: https://www.royalcaribbean.com/the-healthy-sail-center
  49. Cruises P. CruiseHealth FAQ: Sailings from the United States. Princess Cruises. [Accessed: 18 Nov 2021]. Available from: https://www.princess.com/plan/cruise-with-confidence/cruise-health/frequently-asked-questions/us-cruises
  50. Princess Cruises. Health Protocols for Your Cruise. Santa Clarita: Princess Cruises. [Accessed: 18 Nov 2021]. Available from: https://www.princess.com/plan/cruise-with-confidence/cruise-health
  51. Norwegian Cruise Line. Sail Safe. Miami: Norwegian Cruise Line. [Accessed: 7 May 2021]. Available from: https://www.ncl.com/sail-safe
  52. Chang S, Pierson E, Koh PW, Gerardin J, Redbird B, Grusky D, et al. Mobility network models of COVID-19 explain inequities and inform reopening. Nature. 2021;589(7840):82-7.  https://doi.org/10.1038/s41586-020-2923-3  PMID: 33171481 
  53. Jenness SM, Willebrand KS, Malik AA, Lopman BA, Omer SB. Dynamic network strategies for SARS-CoV-2 control on a cruise ship. Epidemics. 2021;37:100488.  https://doi.org/10.1016/j.epidem.2021.100488  PMID: 34438256 
  54. Centers for Disease Control and Prevention (CDC). COVID-19 and Cruise Ship Travel. Atlanta: CDC. [Accessed 4 Jan 2022]. Available from: https://wwwnc.cdc.gov/travel/notices/covid-4/coronavirus-cruise-ship
  55. Centers for Disease Prevention and Control (CDC). Vessel Sanitation Program. Atlanta: CDC. [Accessed: 10 Dec 2021]. Available from: https://www.cdc.gov/nceh/vsp/pub/norovirus/norovirus.htm
  56. Jamaican Ministry of Health and Wellness. COVID-19 Update: 17 more recoveries, 4 new imported cases recorded. Kingston: Government of Jamaica; 5 June 2020. Available from: https://www.moh.gov.jm/covid-19-update-17-more-recoveries-4-new-imported-cases-recorded
  57. New Zealand Ministry of Health. COVID-19 Update on Ruby Princess and Celebrity Solstice cruises. Wellington: New Zealand Ministry of Health; 2020. Available from: https://www.health.govt.nz/news-media/media-releases/covid-19-update-ruby-princess-and-celebrity-solstice-cruises
/content/10.2807/1560-7917.ES.2022.27.1.2002113
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error