G.4.1 Faeces-Food-Water Cluster
Agents in this cluster are found in beverages, food, drinking water and on objects. Numerous outbreaks of gastrointestinal illness have been described, primarily from passenger ships. The main agents documented in outbreaks include Norovirus, E. coli spp, Salmonella typhi, Salmonella spp, Shigella spp, Vibrio spp, Staphylococcus aureus, Clostridium perfringens, Cylsospora spp, Giardia lamblia, Cryptosporidium sp, Trichinella spirali, Entamoeba histolytica, Enterobacter (1,2,3,4)
Dahl analysed gastrointestinal illness logs from 17 cruises in 2004. On average 590 passengers and 611 crew were present per day. During a 250 day period the percentage of GI cases per 7 days varied between 0.10% and 0.43% among passengers and between 0 and 0.29% among crew except for one cruise when percentage per 7 days reached 2.16% among passengers and 0.61% among crew (5).
Occurrence of gastrointestinal infections onboard passenger ships in the 1970´s to 1980´s led to a governmental inspection program in the United States, which is ongoing. The Centers for Disease Control and Prevention´s Vessel Sanitation Program web site lists 15 only outbreaks in 2008 but over 100 outbreaks of gastroenteritis from 1994 (6).
For prevention and control of food and waterborne infections on board ships detailed published recommendations include those of the World Health Organization, the Centers of Disease Control Vessel Sanitation Program (www.cdc.gov/nceh/vsp) (7) and the EU project ShipSan (www.ShipSAN.eu) (8,9).
Guidance documents from the World Health Organization on ship sanitation in general and food and water hygiene in particular are freely available at http://www.who.int/ihr.
The most relevant documents found on this website concerning food and water hygiene are
- Handbook for inspection of ships and issuance of ship sanitation certificates
- Guide to ship sanitation (third edition)
- Ship sanitation certificates
(1) World Health Organization. Guide to Ship Sanitation 3rd edition 2011 http://www.who.int/water_sanitation_health/publications/2011/ship_sanitation_guide/en/; last access14.2.2022
(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 Sep 24;70(6):1-19. doi: 10.15585/mmwr.ss7006a1. PMID: 34555008; PMCID: PMC8480991.
[3] Rooney RM, Cramer EH, Mantha S, Nichols G, Bartram JK, Farber JM, Benembarek PK. A review of outbreaks of foodborne disease associated with passenger ships: evidence for risk management. Public Health Rep 2004;119:427-434.
[4] Koo D, Maloney K, Tauxe R 1996. Epidemiology of diarrheal disease outbreaks on cruise ships, 1986 through 1993. J Am Med Ass 1996;275:545-547.
[5] Dahl E. Dealing with gastrointestinal illness on a cruise ship – Part 1: Description of sanitation measures, Part 2: An isolation study. Intern Marit Health 2004;55(1-4):19-29.
[6] Vessel Sanitation Program. Surveillance and outbreak information. www.cdc.gov/nceh/vsp. Last access 14.2.2022
[7] The VSP 2018 Operations Manual and updates are available at www.cdc.gov/nceh/vsp, last access 14.2.2022
(8) Mouchtouri VA, Verykouki E, Zamfir D, Hadjipetris C, Lewis HC, Hadjichristodoulou C; The Eu Shipsan Act Partnership. Gastroenteritis outbreaks on cruise ships: contributing factors and thresholds for early outbreak detection. Euro Surveill. 2017 Nov;22(45):16-00576. doi: 10.2807/1560-7917.ES.2017.22.45.16-00576. PMID: 29162205; PMCID: PMC5718393.
[9] ShipSan and ShipSanAct Joint Action https://www.shipsan.eu, Last access 14.2.2022
G.4.2 Norovirus
Norovirus circulates worldwide. The infection causes vomiting, fever and diarrhoea. Spread is via hand contact, inhalation of aerosols from vomit or diarrhoea and food. Infectivity is high and the infective dose is low. Index infections are often food or waterborne, secondary spread is often person-to-person. Most reports are from passenger ships, where outbreaks caused by Norovirus are showing an increased activity despite detailed infection control plans by most cruise companies.
Norovirus is reported to be the predominant cause of diarrhea on cruise ships in many outbreak reports. Most programs focus on passenger safety, data on sickness in crew are often lacking (1,2,3,4).
On a US Navy aircraft carrier an outbreak of gastroenteritis occurred in 1997 during coastal exercises in Japan. A cross-sectional study showed an attack rate of 44% from the ship´s population of 4200 persons caused by Norovirus (5).
In one cruise ship from Florida to the Caribbean in 2002, Norovirus outbreaks occurred on six consecutive 7-day cruises despite aggressive sanitization after the second cruise. On cruise 1, 4% (84/2318) of passengers had gastroenteritis. On cruise 3, 8% of passengers (192/2456) and 2% (23/999) of crew had gastroenteritis (6).
In 2006 an increase of outbreaks on cruise ship sailing in Europe between January and August 2006 was recognized. The authors of the epidemiological study showed that the increase was possible due to an increased Norovirus activity in the community which coincided with the emergence of a new strain. 43 outbreaks were reported from 13 vessels. The highest attack rate was 48% for passengers and 19% for crew members. Two ferries showed higher attack rates in crew (13%) than in passengers (10%) (7).
In summer 2006 a Norovirus outbreak on a river cruise-ship was investigated. A retrospective cohort study among passengers and cruises of three successive voyages was performed. Attack rates for crew and passengers differed with a significant lower attack rates for crew (7%) as compared to passengers (47%) (8)
2002 an ongoing outbreak 6 consecutive cruises with Noroviruses (NoV) occured despite a 1-week sanitization (9).
(1) World Health Organization. Guide to Ship Sanitation 3rd edition 2011 http://www.who.int/water_sanitation_health/publications/2011/ship_sanitation_guide/en/; last access 2011
(2) Rooney RM, Cramer EH, Mantha S, Nichols G, Bartram JK, Farber JM, Benembarek PK. A review of outbreaks of foodborne disease associated with passenger ships: evidence for risk management. Public Health Rep 2004;119:427-434.
(3) Koo D, Maloney K, Tauxe R 1996. Epidemiology of diarrheal disease outbreaks on cruise ships, 1986 through 1993. J Am Med Ass 1996;275:545-547.
(4) Dahl E. Dealing with gastrointestinal illness on a cruise ship – Part 1: Description of sanitation measures, Part 2: An isolation study. Intern Marit Health 2004;55(1-4):19-29.
(5) Thornton S, Davies D, Chapman F, Farkas T, Wilton N, Doggett D, Jiang X. Detection of Norwalk-like virus infection aboard two U.S. Navy ships. Mil Med 2002;167:826-830.
(6) Corwin AL, Soderquist R, Edwards M, White A, Beecham J, Mills P, Larasati RP, Subekti D, Ansari T, Burans J, Oyofo B. Shipboard impact of a propable Norwalk virus outbreak from coastal Japan. Am J Trop Med Hyg 1999;61:898-903.
(7) Verhoef L, Depoortere E, Boxman I, Duizer E, van Duynhoven Y, Harris J, Johnsen C, Kroneman A, Le Guyader S, Lim W, Maunula L, Meldal H, Ratcliff R, Reuter G, Schreier E, Siebenga J, Vainio K, Varela C, Vennema H, Koopmans M. Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerg Infect Dis 2008;14:238-243.
(8) Verhoef L, Boxman IL, Duizer E, Rutjes SA, Vennema H, Friesema IHM, deRoda Husman AM, Koopmanns M. Multiple exposure during a Norovirus outbreak on a river-cruise sailing through Europe 2006. Eurosurveillance 2008;1 3(2)
(9) Isakbaeva ET, Widdowson MA, Beard RS, Bulens SN, Mullins J, Monroe SS, Bresee J, Sassano P, Cramer EH, Glass RI. Norovirus transmission on cruise ship. Emerg Infect Dis. 2005 Jan;11(1):154-8. doi: 10.3201/eid1101.040434. PMID: 15705344; PMCID: PMC3294347.
G.4.3 Hepatitis A
Hepatitis A virus is spread by oral-faecal contact or ingestion of contaminated food. The infectious agent is found in faeces, reaches peak levels a week or two before the onset of symptoms and diminishes rapidly after jaundice or symptoms disappear.
Common sources of outbreaks have been related to contaminated water, food contaminated by infected food handlers, including food not cooked or handled after cooking, raw or undercooked molluscs harvested from contaminated waters and contaminated products such as lettuce and strawberries. Lifelong immunity occurs from vaccination or infection.
Risks of hepatitis A virus infection vary with age, country of origin and destination. Seroprevalence rates are highly correlated with socioeconomic status and access to clean water and sanitation. Adult Hepatitis A is a feature of travelers going from low-risk areas to high-risk areas. Inhabitants of high-risk areas are usually infected during childhood and acquire life-long immunity. Ships move between high and low prevalence areas accommodating seafarers with or without immunity in a semiclosed space. Most highly industrial countries are low prevalence regions, while infection rates are declining in the younger population in most Latin-American, Asian and Middle Eastern. Surveys from Africa indicate that infection rates remain high with no significant decline in rates (1).
A prevalence study among seafarers of US Navy vessels in 1989 showed that 10.1% (210 of 2072 male persons) had antibodies against hepatitis A. Immunity was independently associated with age, non-white racial/ethnic group, birth outside of the United States and prior Caribbean deployment (2).
A historical follow-up study based on record linkage of the research database on 24132 seamen who have been employed in Danish ships between 1986 and 1993 and the National Registry for Notifiable Infectious Diseases showed that the standardized incidence ratio for hepatitis A infection was 1.77 (0.91-3.10) as compared to the general population. The majority of the 15 cases reported an occupational exposure such as overseas travel or repair work of the ship’s sanitary installation (3).
One case report on hepatitis A infection from a cargo ship was published in 2008. The vessel carried a seafarer from the Philippines who was infected during a vacation in his country. Immunity could not be confirmed in fellow crew members by medical history or from documentation in their vaccination cards. As a consequence, post-exposure vaccination of the entire crew was performed by the Port Health Authority in Hamburg (4).
Mouchtouri et al. reported several cases of Hepatitis A infections on river boat cruises in Egypt and points to the importance of pre-tarvel vaccination for crew and passengers (5).
Given the high risk of acquiring the infection during sea travel, including common source infection (food, water) and person-to- person spread, pre-departure Hepatitis A vaccination of all seafarers from low incidence countries is necessary to avoid work-related disease and outbreaks on board. As an alternative to routine immunization, immunological screening can be performed. Cost-effectiveness of this measure must be assessed on the grounds of the country of origin of recruited sailors. Immunization of persons who have acquired natural immunity is not harmful, so routine vaccination of all crew without serological screening may be a cost-effective strategy for companies. Certainly the ship´s cook and engineers with responsibility for the on board sewage system must have highest priority for immunization.
Proper water and food sanitation on board and personal hygiene with special emphasis on hand washing are of prime importance. Maintaining a proper water treatment and distribution system on the ship is a key measure for prevention.
In case of an individual case of hepatitis A occurs on board, the infected person must be isolated in a cabin, with enteric precautions (do not share toilet, dishes, left-over food etc.) observed during the first 2 weeks of illness, but no more than 1 week after the onset of jaundice. Post-exposure prophylaxis with Hepatitis A vaccine, preferably simultaneously with IgG must be given to close contacts within 2 weeks of last exposure at separate injection sites. In the context of a ship, close contacts are all crew members working and living in the same area, thus all crew from a cargo ship. On a cruise ship this must be assessed in detail: Contacts may be persons sharing a cabin or wash rooms or working in the same areas Others to be considered are food handlers, those who work in a day-care center, with the water treatment or sewage and waste systems, or in spas or medical facilities.
Given the safety, good tolerability, efficacy and long lasting protection (20-30 years) of the vaccine, pre- and post exposure hepatitis A vaccination in global seafaring is certainly an underused preventative measure.
[1] Jacobsen KH, Koopman JS. Declining hepatitis A seroprevalence: a global review and analysis. Epidemio. Infect 2004,132:1005-1022.
(2) Hawkins RE, Malone JD, Cloninger LA, Rozmajzl PJ, Lewis D, Butler J, Cross E, Gray S, Hyams KC. Risk of viral hepatitis among military personnel assigned to US Navy ships. J Infect Dis. 1992 Apr;165(4):716-9. doi: 10.1093/infdis/165.4.716. PMID: 1552201.
[3] Hansen HL. Occupation-related morbidity and mortality among merchant seafarers with particular reference to infectious diseases. Esbjerg: South Jutland University Press, 1996.
[4] Robert Koch Institut. Lamshöft M, Schlaich C. Riegelungsimpfungen gegen Hepatitis A auf einem Frachtschiff. Bericht aus der Tätigkeit des Hafen- und Flughafenärztlichen Dienstes. Epid Bull 2008;(39):338-339.
(5) Mouchtouri VA, Lewis HC, Hadjichristodoulou C; EU SHIPSAN ACT Joint Action Partnership. A Systematic Review for Vaccine-Preventable Diseases on Ships: Evidence for Cross-Border Transmission and for Pre-Employment Immunization Need. Int J Environ Res Public Health. 2019;16(15):2713. Published 2019 Jul 30. doi:10.3390/ijerph16152713
G.4.4 Hepatitis E
Hepatitis E infection is associated with travel to tropical or subtropical countries. It was first recognized 1980 as a cause of human disease. It can be an asymptomatic infection or induce clinical hepatitis, which may be severe or life-threatening, particularly for pregnant women. It is usually transmitted by the oral –faecal route with an incubation period of 15-60 days.
No reports on risk of hepatitis E infection in seafarers have yet been published.
In 2008, acute hepatitis E infection was confirmed in 4 passengers returning to the UK after a world cruise. A contact investigation of 2850 passengers revealed that 25% persons that provided blood samples were hepatitis E seropositive. Crew members were not examined, but the data pointed to a common source foodborne outbreak on board (1)
Another travel related outbreak wirth Hepatitis E was described in a German group of n= 5 (out of 24) travelers returning from India (2)
(1) Said B, Samreen I, Kafatos G et al. Hepatitis E outbreak on a cruise ship. Emerging Infectious Dis 2009, Vol 15, No 11.
(2) Pischke S, Schulze-Zur-Wiesch J, Lütgehetmann M, Kreuels B, Lueth S, Kapaun P, Benten D, Schmiedel S, Sterneck M, Lohse AW, Polywka S. High clinical manifestation rate in an imported outbreak of hepatitis E genotype 1 infection in a German group of travellers returning from India. Ann Hepatol. 2017 Jan-Feb;16(1):57-62. doi: 10.5604/16652681.1226815. PMID: 28051793.
G.4.5 Helicobacter pylori
Infection with Helicobacter pylori causes chronic gastritis and ulcer disease. The infection is epidemiologically linked with gastric adenocarcinoma. H. Pylori has an estimated rate of infection of up to 70% in developing countries and up to 20-30% in industrialized countries (1). H. pylori is a common bacterium, humans are the principal reservoir. The prevalence of H. pylori infection varies widely by geographic area, age, race and ethnicity. Rates appear to be higher in developing than in developed countries, with most of the infections occurring during childhood, and they seem to be decreasing with improvements in hygiene practices. Overall, inadequate sanitation practices, low social class, and crowded or high-density living conditions seem to be related to a higher prevalence of H. pylori infection. Recent studies in the United States have linked clinical H. pylori infection with consumption of H. pylori-contaminated well water (2).
There are few studies that evaluated the risk of H. pylori transmission on ships.
In a study to elucidate the route of transmission for Helicobacter pylori 64 German submarine crews who were investigated in comparison to air force staff showed a significantly higher antibody response. Crowding and limited sanitation aboard submarines seemed to facilitate person-person spread among crew members (3).
The prevalence of H. pylori in the crews of United States Navy nuclear submarines was 9.4% (47/451). The authors found this to be comparable to the United States general population (4).
Certainly these data support the importance of proper hygiene and living conditions on ships. The most likely mode of H. pylori transmission is from person to person, by either the oral-oral route (through vomitus or possibly saliva) or perhaps the faecal-oral route. The person-to-person mode of transmission is supported by the higher incidence of infection among institutionalized children and adults and the clustering of H. pylori infection within families. Waterborne transmission, probably due to faecal contamination is possible. As with many other infectious risks on ships, general food and water hygiene and avoidance of crowding on ships is effective to prevent disease transmission.
[1] Heyman DL ed. Control of Communicable Diseases Manual. American Public Health Association. WHO. 19th Edition 2008. ISBN 0-87553-034-6.
(2) Brown LM. Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev. 2000;22(2):283-97. doi: 10.1093/oxfordjournals.epirev.a018040. PMID: 11218379.
[3] Hammermeister I, Janus G, Schamarowski F, Rudolf M, Jacobs E, Kist M. Elevated risk of Helicobacter pylori infection in submarine crews. Eur J Clin Microbiol Infect Dis 1992;11:9-14.
[4] Jackman RP, Schlichting C, Carr W, Dubois A. Prevalence of Helicobacter pylori in United States Navy submarine crews. Epidemiol Infect 2006;134:460-464.
G.4.6 Enterotoxigenic E. coli
Enterotoxigenic E. coli (ETEC) is a common cause of travel associated diarrhoea.
In a review from the Word Health Organization 21 waterborne outbreaks were associated with ships. Enterotoxigenic E. coli was the pathogen most frequently associated with outbreaks. Contributing factors include contaminated source water, and failure in the disinfection system. No information on involvement of crew was given. Daniels et al. (1) investigated outbreaks of gastroenteritis caused by ETEC on three cruise ships. Attack rates in the first cruise was 2.6% in crew, 7.1% in passengers, in the second cruise 0.25% for crew and 2.5 % in passengers and in the 3rd cruise 2% for crew and 31% in passengers. Water taken in overseas ports was the likely source of disease (2).
In A Navy ship following a visit to Lima, Peru a conczúrrent outbreak of Borovirus and ETEC was described, n=65 out of 230 crew members fell sick.
[1] Daniels NA, Neimann J, Karpati A, Parashar UD, Greene KD, Wells JG, Srivastava A, Tauxe RV, Mintz ED, Quick R. Traveler´s diarrhea at sea: Three outbreaks of waterborne enterotoxigenic Escherichia coli on cruise ships. J Infect Dis 2000;181:1491-1495.
(2) Gonzaga VE, Ramos M, Maves RC, Freeman R, Montgomery JM. Concurrent outbreak of norovirus genotype I and enterotoxigenic Escherichia coli on a U.S. Navy ship following a visit to Lima, Peru. PLoS One. 2011;6(6):e20822. doi: 10.1371/journal.pone.0020822. Epub 2011 Jun 21. PMID: 21713034; PMCID: PMC3119660.
G.4.7 Shigella spp.
Outbreaks with Shigella – particular S. flexneri – are well documented from cruise and other ships. On a cruise from California to Mexico in 1994, 14% (72/512) of passengers and 3% (12/388) of crew fell ill.(1)
(1) Lew JF, Swerdlow DL, Dance ME, Griffin PM, Bopp CA, Gillenwater MJ, Mercatante T, Glass RI An outbreak of shigellosis aboard a cruise ship caused by a multiple-antibiotic-resistant strain of higella flexneri. Am J Epidemiol 1991;134:413-420.
G.4.8 Vibrio cholerae
Cholera is an acute diarrhoeal infection caused by eating or drinking food or water that is contaminated with the bacterium Vibrio cholerae.
It takes between 12 hours and 5 days for a person to show symptoms after consuming contaminated food or water. The main manifestation of cholera is severe, very watery (rice-water) diarrhoea, not accompanied by fever that can cause dehydration. However, most infections in healthy adults are inapparent or mild (90%). Most people infected with Vibrio cholerae do not develop any symptoms, although the bacteria are present in their faeces for 1-10 days after infection.
No severe disease was described in seafarers in the last decades. Cholera is often predictable and preventable. It can ultimately be eliminated where access to clean water and sanitation facilities is given.
Effective vaccines are available. Cholera is nit a mandatory or recommended vaccination for seafarers, unless there are special circumstances (e.g, sewage work in affected aresas, refugee work etc.).
G.4.9 Salmonella spp
Other agents of waterborne or foodborne disease including Salmonella typhi and non-typhi, Cryptosporidium, Vibrio parahaemolyticus, Entamoeba histolytica, Yersinia enterocolitica and Giardia lamblia in passengers of cruise ships are documented, but no data are available for risk of infection in seafarers.
Though no data are published on salmonellosis in seafarers, the infection is of special relevance to the seafaring profession. It is a bacterial disease commonly manifested by acute enterocolitis, with sudden onset of headache, abdominal pain, diarrhoea, nausea and sometimes vomiting. Fever is almost always present. It can also cause severe sepsis. In cases of enterocolitis, faecal excretion usually persist for several days or weeks beyond the acute phase, administration of antibiotics may not decrease this duration.
Salmonellosis is commonly transmitted by food of animal origin. The incubation period is usually 12-36 hours. Cases may occur sporadically or in outbreaks, commonly from contaminated food or water.
If an outbreak aboard a ship occurs, the water system must inspected, including sampling. Food handling aboard needs to be critically reviewed.
Basic food handling hygiene for eggs and egg products, milk, meat and poultry is important. Appropriate training of the ship´s cook and trusted sources of food in ports aboard are key. All food handlers aboard must be educated about the importance of hand washing before, during and after food preparation, in thoroughly cooking all food stuff from animal sources, and avoiding recontamination within the kitchen after cooking is completed. Maintaining a sanitary kitchen and protecting prepared food against rodent and insect contamination are also essential pars of this education.
The source of infection may also be an infected food handler. Thus the cooks must be instructed to report symptoms of enterocolitis. The shipmaster MUST exclude the cook and other helpers who have symptoms of diarrhea and vomiting from food handling.
G.4.10 Typhoid Fever (Enteric Fever, Typhus abdominalis) and Paratyphoid Fever
Typhoid and paratyphoid fevers are systemic bacterial diseases caused by two closely related bacteria of the Salmonella group. The clinical picture varies from mild illness with low-grade to severe clinical disease with abdominal discomfort and multiple complications. The disease occurs worldwide, but most of the burden of the disease is in the developing world. Reservoirs are humans. Transmission is by ingestion of contaminated food or water. Incubation time usually is 8-14 days.
Preventative measures, as with other salmonella infections, concern general hygiene, water treatment aboard and food handling.
Few patients become chronic carriers of typhoid organisms. Typhoid carriers should be excluded from handling food until three consecutive negative cultures are obtained from faecal specimens at least 1 months apart and at least 48 hours after antimicrobial therapy has stopped. Ciprofloxacin treatment 400 mg twice daily for a full month is successful in treating most carriers.
A vaccine for typhoid fever is available and recommended for seafarers from non-endemic areas, especially food-handlers. Persons from endemic areas carry a relatively~ specific immunity after childhood infection.