Mem Inst Oswaldo Cruz, Rio de Janeiro, VOLUME 117 | 2022
Research Articles

COVID-19 outbreaks among crew members in non-cruise vessels anchoring in Salvador, Brazil, 2021

Cristiane Wanderley Cardoso1,2,+, Mirela Maisa da Silva Souza1, Ana Claudia Venegeroles de Sá Teles3, Hernan Dario Argibay2, Olivete Borba dos Reis1, Felicidade Mota Pereira4, Marta Giovanetti5, Tereza Magalhaes6,7, Guilherme Sousa Ribeiro2,6

1Secretaria Municipal de Saúde de Salvador, Salvador, BA, Brasil
2Fundação Oswaldo Cruz-Fiocruz, Instituto Gonçalo Moniz, Salvador, BA, Brasil
3Agência Nacional de Vigilância Sanitária, Salvador, BA, Brasil
4Secretaria de Saúde do Estado da Bahia, Salvador, BA, Brasil
5Fundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Laboratório de Flavivírus, Rio de Janeiro, RJ, Brasil
6Universidade Federal da Bahia, Faculdade de Medicina, Salvador, BA, Brasil
7Colorado State University, Center for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Fort Collins, CO, USA

DOI: 10.1590/0074-02760220114
361 views 166 downloads
ABSTRACT

BACKGROUND The coronavirus disease 2019 (COVID-19) pandemic, caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has affected the maritime sector due to virus transmission onboard and traffic restrictions. However, reports of SARS-CoV-2 transmission on board have been mostly restricted to those occurring on cruise ships.
OBJECTIVES To report COVID-19 outbreaks in eight non-cruise vessels and discuss measures to prevent and control the onboard transmission of SARS-CoV-2.
METHODS We investigated outbreaks of COVID-19 on vessels anchoring in Baía de Todos-os-Santos, Salvador, Brazil, between February and November 2021.
FINDINGS Most vessels were cargo ships that had docked several times before anchoring in Salvador (five had docked in ≥ 9 ports). The crew ranged from 22 to 63 members. The infection attack rate on each vessel ranged from 9.7 to 88.9%. The risk of symptomatic infection largely varied among the crew of each vessel (0 to 91.6%). Overall, the risk of developing COVID-19 signs and symptoms was lower among crew members vaccinated (age-adjusted risk ratio: 0.19; 95% confidence interval 0.06-0.65). SARS-CoV-2 variants not previously identified in Salvador were detected (C.14, B.1.617.2 and B.1.351).
MAIN CONCLUSIONS Despite maritime guidelines to avert COVID-19 on board, outbreaks have happened. The multiple stopovers of non-cruise vessels during their routes may contribute to the spread of SARS-CoV-2 variants worldwide. Reducing the onboard transmission of SARS-CoV-2 depends on joint efforts by the crew and local health authorities and, equally important, achieving high vaccination coverage to prevent infections and illness.

REFERENCES
01. UNCTAD. COVID-19 and maritime transport: impact and responses. UNCTAD Policy Brief 75. 2021. Available from: https:// unctad.org/system/files/official-document/dtltlb2021d1_en.pdf
02. Stannard S. COVID-19 in the maritime setting: the challenges, regulations and the international response. Int Marit Health. 2020; 71: 85-90. http://doi.org/10.5603/IMH.2020.0016
03. Pacific Islands Forum Fisheries Agency. COVID-19 operating protocols for the fishing sector in the Pacific. 2021. Available from: https://www.ffa.int/covid19
04. European Maritime Safety Agency. COVID-19: EU Guidance for cruise ship operations. Guidance on the gradual and safe resumption of operations of cruise ships in the European Union in relation to the COVID-19 pandemic. 2020. Available from: https://www. ecdc.europa.eu/sites/default/files/documents/COVID-CRUISEGUIDANCE- revision-1-May-2021.pdf
05. International Chamber of Shipping. Coronavirus (COVID-19) – Guidance for ship operators for the protection of the health of seafarers. In: Shipping ICo. 5th ed. London: Marisec Publications, 2022.
06. Agência Nacional de Vigilância Sanitária. Protocolo para quarentena de embarcação com caso confirmado para COVID-19. In: Gerência‐Geral de Portos, Aeroportos, Fronteiras e Recintos Alfandegados (GGPAF). Brasília: ANVISA, 2020.
07. Willebrand KS, Pischel L, Malik AA, Jenness SM, Omer SB. A review of COVID-19 transmission dynamics and clinical outcomes on cruise ships worldwide, January to October 2020. Euro Surveill. 2022; 27: 1-13. http://doi.org/10.2807/1560-7917. ES.2022.27.1.2002113
08. Rocklov J, Sjodin 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; 27: 1-7. http://doi.org/10.1093/jtm/taaa030
09. Codreanu TA, Ngeh S, Trewin A, Armstrong PK. Successful control of an onboard COVID-19 outbreak using the cruise ship as a quarantine facility, Western Australia, Australia. Emerg Infect Dis. 2021; 27: 1279-87. http://doi.org/10.3201/eid2705.204142
10. Hung IF, Cheng VC, Li X, Tam AR, Hung DL, Chiu KH, et al. SARS-CoV-2 shedding and seroconversion among passengers quarantined after disembarking a cruise ship: a case series. Lancet Infect Dis. 2020; 20: 1051-60. http://doi.org/10.1016/S1473- 3099(20)30364-9
11. Maeda H, Sando E, Toizumi M, Arima Y, Shimada T, Tanaka T, et al. Epidemiology of coronavirus disease outbreak among crewmembers on cruise ship, Nagasaki City, Japan, April 2020. Emerg Infect Dis. 2021; 27: 2251-60. http://doi.org/10.3201/ eid2709.204596
12. 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): 1-8. Erratum in: Euro Surveill. 2020; 25(24). http://doi.org/10.2807/1560- 7917.ES.2020.25.23.2000272
13. Plucinski MM, Wallace M, Uehara A, Kurbatova EV, Tobolowsky FA, Schneider ZD, et al. Coronavirus disease 2019 (COVID-19) in Americans aboard the Diamond Princess cruise ship. Clin Infect Dis. 2021; 72: 1-23. http://doi.org/10.1093/cid/ciaa1180
14. Fanoy E, Ummels AE, Schokkenbroek V, van Dijk B, Wiegmans S, Veenstra T, et al. Outbreak of COVID-19 on an industrial ship. Int Marit Health. 2021; 72: 87-92. http://doi.org/10.5603/ IMH.2021.0016
15. Codreanu TA, Pingault N, O’Loughlin E, Armstrong PK, Scalley B. The healthy crew, clean vessel, and set departure date triad: successful control of outbreaks of COVID-19 on board four cargo vessels. Prehosp Disaster Med. 2021; 36: 611-20. http://doi. org/10.1017/S1049023X21000686
16. Companhia das Docas do Estado da Bahia. Estatísticas – Movimentações de cargas 2022. [accessed on 07 March 2022]. Available from: https://www.codeba.com.br/eficiente/sites/portalcodeba/ pt-br/porto_salvador.php?secao=porto_salvador_estatisticas
17. World Health Assembly. Revision of the International Health Regulations, WHA 58.3. [accessed on 28 June 2022]. Available from: http://www.who.int
18. Agência Nacional de Vigilância Sanitária. Protocolo – Detecção e atendimento de casos suspeitos da COVID-19 em portos, aeroportos e fronteiras. Atualizado em 30 de março de 2020. [accessed on 06 September 2022]. Available from: https://www.gov.br/anvisa/ pt-br/assuntos/paf/coronavirus/arquivos/protocolos/7098json-file-1
19. Agência Nacional de Vigilância Sanitária. Nota técnica Nº 5/2021/ SEI/GQRIS/GGPAF/DIRE5/ANVISA. 2020. Available from: https://static.poder360.com.br/2022/01/nota-tecnica-anvisa-cruzeiros. pdf
20. StataCorp. Stata Statistical Software: release 14. College Station (TX): StataCorp LP. [accessed on 30 September 2018]. Available from: https://www.stata.com
21. Morawska L, Tang JW, Bahnfleth W, Bluyssen PM, Boerstra A, Buonanno G, et al. How can airborne transmission of COVID-19 indoors be minimized? Environ Int. 2020; 142: 1-7. http://doi. org/10.1016/j.envint.2020.105832
22. Berry G, Parsons A, Morgan M, Rickert J, Cho H. A review of methods to reduce the probability of the airborne spread of COVID- 19 in ventilation systems and enclosed spaces. Environ. Res. 2022; 203: 1-12. https://doi.org/10.1016/j.envres.2021.111765
23. Kwok HF. Review of Covid-19 vaccine clinical trials – A puzzle with missing pieces. Int J Biol Sci. 2021; 17: 1461-8. http://doi. org/10.7150/ijbs.59170
24. Shao W, Chen X, Zheng C, Liu H, Wang G, Zhang B, et al. Effectiveness of COVID-19 vaccines against SARS-CoV-2 variants of concern in real-world: a literature review and meta-analysis. Emerg Microbes Infect. 2022; 11: 2383-92. http://doi.org/10.1080/ 22221751.2022.2122582
25. McCarthy CV, O’Mara O, van Leeuwen E, CMMID COVID-19 Working Group, Jit M, Sandmann F. The impact of COVID-19 vaccination in prisons in England and Wales: a metapopulation model. BMC Public Health. 2022; 22: 1-17. https://doi.org/10.1186/ s12889-022-13219-4
26. Flaherty GT, Hamer DH, Chen LH. Travel in the Time of COVID: a review of international travel health in a global pandemic. Curr Infect Dis Rep. 2022; 24: 129-45. http://doi.org/10.1007/s11908- 022-00784-3
27. Dinnes J, Deeks JJ, Berhane S, Adriano A, Berhane S, Taylor M, et al. Rapid, point-of-care antigen and molecular-based tests for diagnosis of SARS-CoV-2 infection. Cochrane Database Syst Rev. 2021; 3. http://doi.org/10.1002/14651858.CD013705.pub2
28. Mittal M, Battineni G, Goyal LM, Chhetri B, Oberoi SV, Chintalapudi N, et al. Cloud-based framework to mitigate the impact of COVID-19 on seafarers’ mental health. Int Marit Health. 2020; 71: 213-4. http://doi.org/10.5603/IMH.2020.0038. PMID: 33001435
29. Pauksztat B, Grech MR, Kitada M. The impact of the COVID-19 pandemic on seafarers’ mental health and chronic fatigue: beneficial effects of onboard peer support, external support and Internet access. Mar Policy. 2022; 137: 1-9. http://doi.org/10.1016/j. marpol.2021.104942

Financial support: CIEVS, SMS Salvador, Fiocruz, UFBA.
GSR received research scholarships (307450/2017-1; 311365/2021-3) from the CNPq.
+ Corresponding author: cristiane.cardoso@salvador.ba.gov.br
ORCID https://orcid.org/0000-0001-5432-1174
Received 15 May 2022
Accepted 10 October 2022

Our Location

Memórias do Instituto Oswaldo Cruz

Av. Brasil 4365, Castelo Mourisco 
sala 201, Manguinhos, 21040-900 
Rio de Janeiro, RJ, Brazil

Tel.: +55-21-2562-1222

This email address is being protected from spambots. You need JavaScript enabled to view it.

Support Program

ioc

fiocruz 
faperj cnpq capes