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Systematic Review Open Access
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Abstract

Background

Outbreaks of norovirus gastroenteritis aboard cruise ships may affect a large number of people, debilitate vulnerable travellers, disrupt vacations and cause economic losses to the cruise ship industry.

Aim

We aimed to identify risk factors for norovirus outbreaks on cruise ships and assess the effectiveness of prevention and control measures.

Methods

We conducted a systematic literature review searching PubMed and Scopus databases as well as grey literature for articles and reports describing norovirus outbreaks on cruise ships between 1990 and 2020. We also performed a meta-analysis of norovirus prevalence in passengers and crew members.

Results

Data from 45 outbreaks on 26 cruise ships from 1990 to 2020 were identified in 13 articles and five reports, with a weighted average of prevalence (attack rate) for passengers of 7% (95% confidence interval (CI): 5.00–9.00) and for crew of 2% (95% CI: 0.00–3.00). Person-to-person was the most frequent mode of transmission in 35 of the 45 outbreaks (in 14 the only mode and in 21 as part of multiple transmission routes). Having an ill cabin mate (OR = 38.70; 95% CI: 13.51–110.86) was the most common risk factor. Six outbreak investigations reported poor hygiene, while four reported satisfactory hygiene in the cruise setting. Behavioural risk factors among travellers were investigated in three of the 13 studies.

Conclusions

The findings indicate a need for behavioural interventions to improve personal hygiene, symptom reporting and compliance with isolation measures, and for reconsidering current isolation policies where symptomatic and healthy individuals are isolated in the same cabin.

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/content/10.2807/1560-7917.ES.2024.29.10.2300345
2024-03-07
2024-11-09
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.10.2300345
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References

  1. World Health Organization (WHO). International travel and health. Geneva: WHO; 2019. Available from: https://www.who.int/publications/i/item/9789241580472
  2. Jenkins KA, Vaughan GH Jr, Rodriguez LO, Freeland A. Acute gastroenteritis on cruise ships - maritime illness database and reporting system, United States, 2006-2019. MMWR Surveill Summ. 2021;70(6):1-19.  https://doi.org/10.15585/mmwr.ss7006a1  PMID: 34555008 
  3. Launders NJ, Nichols GL, Cartwright R, Lawrence J, Jones J, Hadjichristodoulou C. Self-reported stomach upset in travellers on cruise-based and land-based package holidays. PLoS One. 2014;9(1):e83425.  https://doi.org/10.1371/journal.pone.0083425  PMID: 24427271 
  4. de Graaf M, Villabruna N, Koopmans MP. Capturing norovirus transmission. Curr Opin Virol. 2017;22:64-70.  https://doi.org/10.1016/j.coviro.2016.11.008  PMID: 28056379 
  5. Gunn RA, Terranova WA, Greenberg HB, Yashuk J, Gary GW, Wells JG, et al. Norwalk virus gastroenteritis aboard a cruise ship: an outbreak on five consecutive cruises. Am J Epidemiol. 1980;112(6):820-7.  https://doi.org/10.1093/oxfordjournals.aje.a113054  PMID: 7457473 
  6. EU SHIPSAN ACT Joint Action (20122103). European manual for hygiene standards and communicable disease surveillance on passenger ships. 2nd ed. ISBN 978-960-99647-3-9. Brussels: European Commission; 2016. Available from: https://www.shipsan.eu/Home/EuropeanManual.aspx
  7. HEALTHY SAILING. Prevention, mitigation, management of infectious diseases on cruise ships and passenger ferries. HORIZON-CL5-2021-D6-01. Larissa: HEALTHY SAILING. [Accessed: 14 Jun 2023]. Available from: https://healthysailing.eu
  8. Florida-Caribbean Cruise Association (FCCA). Cruise industry overview - 2013. Pembroke Pines: FCCA; Available from: https://www.f-cca.com/downloads/2013-cruise-industry-overview.pdf
  9. World Maritime News. CLIA: cruise passengers top 22 million mark in 2014. Piraeus: Maritimes; 2015. Available from: https://maritimes.gr/en/clia-cruise-passengers-top-22-million-mark-in-2014
  10. Cruise Lines International Association (CLIA). 2019 cruise trends & industry outlook. Washington: CLIA; 2019. Available from: https://cruising.org/-/media/eu-resources/pdfs/CLIA%202019-Cruise-Trends--Industry-Outlook
  11. Phocuswright. U.S. cruise market report 2021-2025. Rutherford: Phocuswright; 2022. Available from: https://www.phocuswright.com/Travel-Research/Market-Overview-Sizing/US-Cruise-Market-Report-2021-to-2025
  12. Khan AS, Moe CL, Glass RI, Monroe SS, Estes MK, Chapman LE, et al. Norwalk virus-associated gastroenteritis traced to ice consumption aboard a cruise ship in Hawaii: comparison and application of molecular method-based assays. J Clin Microbiol. 1994;32(2):318-22.  https://doi.org/10.1128/jcm.32.2.318-322.1994  PMID: 8150941 
  13. Verhoef L, Boxman IL, Duizer E, Rutjes SA, Vennema H, Friesema IH, et al. Multiple exposures during a norovirus outbreak on a river-cruise sailing through Europe, 2006. Euro Surveill. 2008;13(24):18899.  https://doi.org/10.2807/ese.13.24.18899-en  PMID: 18761943 
  14. Bert F, Scaioli G, Gualano MR, Passi S, Specchia ML, Cadeddu C, et al. Norovirus outbreaks on commercial cruise ships: a systematic review and new targets for the public health agenda. Food Environ Virol. 2014;6(2):67-74.  https://doi.org/10.1007/s12560-014-9145-5  PMID: 24838574 
  15. Centers for Disease Control and Prevention (CDC). Vessel Sanitation Program 2018 operations manual. U.S. Department of Health and Human Services. Atlanta: CDC; 2018. Available from: https://www.cdc.gov/nceh/vsp/docs/vsp_operations_manual_2018-508.pdf
  16. Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention. Updated norovirus outbreak management and disease prevention guidelines. MMWR Recomm Rep. 2011;60(RR-3):1-18. PMID: 21368741 
  17. Nikolakopoulou A, Mavridis D, Salanti G. How to interpret meta-analysis models: fixed effect and random effects meta-analyses. Evid Based Ment Health. 2014;17(2):64.  https://doi.org/10.1136/eb-2014-101794  PMID: 24778439 
  18. Veroniki AAJD, Jackson D, Viechtbauer W, Bender R, Bowden J, Knapp G, et al. Methods to estimate the between-study variance and its uncertainty in meta-analysis. Res Synth Methods. 2016;7(1):55-79.  https://doi.org/10.1002/jrsm.1164  PMID: 26332144 
  19. Balduzzi S, Rücker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health. 2019;22(4):153-60.  https://doi.org/10.1136/ebmental-2019-300117  PMID: 31563865 
  20. Centers for Disease Control and Prevention (CDC). Outbreaks of gastroenteritis associated with noroviruses on cruise ships--United States, 2002. MMWR Morb Mortal Wkly Rep. 2002;51(49):1112-5. PMID: 12530708 
  21. Chimonas MA, Vaughan GH, Andre Z, Ames JT, Tarling GA, Beard S, et al. Passenger behaviors associated with norovirus infection on board a cruise ship--Alaska, May to June 2004. J Travel Med. 2008;15(3):177-83.  https://doi.org/10.1111/j.1708-8305.2008.00200.x  PMID: 18494695 
  22. Herwaldt BL, Lew JF, Moe CL, Lewis DC, Humphrey CD, Monroe SS, et al. Characterization of a variant strain of Norwalk virus from a food-borne outbreak of gastroenteritis on a cruise ship in Hawaii. J Clin Microbiol. 1994;32(4):861-6.  https://doi.org/10.1128/jcm.32.4.861-866.1994  PMID: 8027335 
  23. Isakbaeva ET, Widdowson MA, Beard RS, Bulens SN, Mullins J, Monroe SS, et al. Norovirus transmission on cruise ship. Emerg Infect Dis. 2005;11(1):154-8.  https://doi.org/10.3201/eid1101.040434  PMID: 15705344 
  24. Khan AS, Moe CL, Glass RI, Monroe SS, Estes MK, Chapman LE, et al. Norwalk virus-associated gastroenteritis traced to ice consumption aboard a cruise ship in Hawaii: comparison and application of molecular method-based assays. J Clin Microbiol. 1994;32(2):318-22.  https://doi.org/10.1128/jcm.32.2.318-322.1994  PMID: 8150941 
  25. McEvoy M, Blake W, Brown D, Green J, Cartwright R. An outbreak of viral gastroenteritis on a cruise ship. Commun Dis Rep CDR Rev. 1996;6(13):R188-92. PMID: 8990576 
  26. Neri AJ, Cramer EH, Vaughan GH, Vinjé J, Mainzer HM. Passenger behaviors during norovirus outbreaks on cruise ships. J Travel Med. 2008;15(3):172-6.  https://doi.org/10.1111/j.1708-8305.2008.00199.x  PMID: 18494694 
  27. Qi L, Xiang X, Xiong Y, Ling H, Shen H, Deng W, et al. Outbreak of acute gastroenteritis caused by norovirus genogroup ii attributed to contaminated cold dishes on a cruise ship in Chongqing, China, 2017. Int J Environ Res Public Health. 2018;15(12):2823.  https://doi.org/10.3390/ijerph15122823  PMID: 30544983 
  28. Vivancos R, Keenan A, Sopwith W, Smith K, Quigley C, Mutton K, et al. Norovirus outbreak in a cruise ship sailing around the British Isles: investigation and multi-agency management of an international outbreak. J Infect. 2010;60(6):478-85.  https://doi.org/10.1016/j.jinf.2010.03.018  PMID: 20359496 
  29. Wang X, Yong W, Shi L, Qiao M, He M, Zhang H, et al. An outbreak of multiple norovirus strains on a cruise ship in China, 2014. J Appl Microbiol. 2016;120(1):226-33.  https://doi.org/10.1111/jam.12978  PMID: 26481457 
  30. Widdowson MA, Cramer EH, Hadley L, Bresee JS, Beard RS, Bulens SN, et al. Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus--United States, 2002. J Infect Dis. 2004;190(1):27-36.  https://doi.org/10.1086/420888  PMID: 15195240 
  31. Wikswo ME, Cortes J, Hall AJ, Vaughan G, Howard C, Gregoricus N, et al. Disease transmission and passenger behaviors during a high morbidity Norovirus outbreak on a cruise ship, January 2009. Clin Infect Dis. 2011;52(9):1116-22.  https://doi.org/10.1093/cid/cir144  PMID: 21429864 
  32. Centers for Disease Control and Prevention (CDC). Outbreak investigation reports. Atlanta: CDC. [Accessed: 22 Jul 2014]. Available from: https://www.cdc.gov/nceh/vsp/surv/gilist.htm
  33. Centers for Disease Control and Prevention (CDC). Outbreaks of gastroenteritis associated with noroviruses on cruise ships--United States, 2002. MMWR Morb Mortal Wkly Rep. 2002;51(49):1112-5. PMID: 12530708 
  34. Mouchtouri VA, Verykouki E, Zamfir D, Hadjipetris C, Lewis HC, Hadjichristodoulou C, et al. Gastroenteritis outbreaks on cruise ships: contributing factors and thresholds for early outbreak detection. Euro Surveill. 2017;22(45):16-00576.  https://doi.org/10.2807/1560-7917.ES.2017.22.45.16-00576  PMID: 29162205 
  35. Taylor CJ. Gastroenteritis outbreaks on cruise ships: are sanitation inspection scores a true index of risk? Int Marit Health. 2018;69(4):225-32.  https://doi.org/10.5603/IMH.2018.0037  PMID: 30589061 
  36. Cramer EH, Blanton CJ, Blanton LH, Vaughan GH Jr, Bopp CA, Forney DL, et al. Epidemiology of gastroenteritis on cruise ships, 2001-2004. Am J Prev Med. 2006;30(3):252-7.  https://doi.org/10.1016/j.amepre.2005.10.027  PMID: 16476642 
  37. Centers of Disease Control and Prevention (CDC). Outbreak updates for international cruise ships. Atlanta: CDC; 2023. Available from: https://www.cdc.gov/nceh/vsp/surv/gilist.htm
  38. World Health Organization (WHO). Behavioural sciences for better health. Geneva: WHO. [Accessed: 18 Jun 2023]. Available from: https://www.who.int/initiatives/behavioural-sciences
  39. 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 
  40. Barker TH, Migliavaca CB, Stein C, Colpani V, Falavigna M, Aromataris E, et al. Conducting proportional meta-analysis in different types of systematic reviews: a guide for synthesisers of evidence. BMC Med Res Methodol. 2021;21(1):189.  https://doi.org/10.1186/s12874-021-01381-z  PMID: 34544368 
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