Norovirus transmission on cruise ship.
ABSTRACT An outbreak of norovirus gastroenteritis affected passengers on two consecutive cruises of ship X and continued on 4 subsequent cruises despite a 1-week sanitization. We documented transmission by food and person-to-person contact; persistence of virus despite sanitization onboard, including introductions of new strains; and seeding of an outbreak on land.
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ABSTRACT: Between July 1997 and June 2000, fecal specimens from 284 outbreaks of nonbacterial gastroenteritis were submitted to the Centers for Disease Control and Prevention for testing for "Norwalk-like viruses" (NLVs). Specimens were examined by reverse-transcription polymerase chain reaction and direct electron microscopy for the presence of NLVs. Adequate descriptive data were available from 233 of the outbreaks, and, of these, 217 (93%) were positive for NLVs. Restaurants and events with catered food were the most common settings, and contaminated food was the most common mode of transmission. Genogroup II (GII) strains were the predominant type (73%), with genogroup I strains causing 26% of all NLV-positive outbreaks. Certain GII clusters (GII/1,4,j) were more commonly associated with outbreaks in nursing home settings than with outbreaks in other settings. Strain diversity was great: one potential new sequence cluster was implicated in multiple outbreaks, and strains belonging to a tentative new genogroup were identified.The Journal of Infectious Diseases 08/2002; 186(1):1-7. · 5.85 Impact Factor
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ABSTRACT: Stool specimens from 156 Maryland nursing home residents, who became ill during 20 outbreaks of gastroenteritis from November 1987 through February 1988, were analyzed. All tested negative for astroviruses, enteroviruses, Group A rotaviruses, Sapporo-like caliciviruses, and enteric bacteria (i.e., Salmonella, Clostridium, and Shigella species). Eighty-two (52%) were positive for Norwalk-like viruses (NLVs), members of the family Caliciviridae. Six distinct genetic clusters within genogroups I and II of the NLVs were detected; a genogroup II (GII) virus closely related to the Camberwell virus in the NLV GII/4 genetic cluster was the predominant strain. Serologic evidence of infection with > or = 1 NLV was detected in 61 (56%) of 109 patients tested against 3 NLV antigens (i.e., Norwalk, Hawaii, and Toronto viruses). Sixteen (80%) outbreaks met the definition for an NLV outbreak. Taken together with a retrospective analysis of bacterial gastroenteritis in this same setting, these data support a major role for NLVs as etiologic agents of gastroenteritis in elderly persons.The Journal of Infectious Diseases 02/2002; 185(2):133-46. · 5.85 Impact Factor
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ABSTRACT: An explosive outbreak of gastroenteritis caused by a parvovirus-like (PVL) agent (Norwalk agent) affected 521 (64%) cruise ship passengers in 1977. The illness was characterized as mild-to-moderate and lasted one to two days. Principal symptoms experienced by ill passengers were nausea, vomiting, and diarrhea; fever was reported for approximately 25% of the patients. The outbreak was compatible with a common-source exposure, but no such exposure was identified. On the next four cruises, passengers experienced a similar gastrointestinal illness, but the outbreaks were less explosive, affected fewer persons, and symptoms appeared milder, on each subsequent cruise. No common source was identified, and person-to-person transmission may have occurred. The etiology of these outbreaks would have remained unknown were it not for the recent development of a specific radioimmunoassay (RIA) for the serologic identification of Norwalk virus and the measurement of antibody titers to the virus. A fourfold or greater rise in serum antibody titers to Norwalk antigen in serum from seven of eight ill passengers and the identification of Norwalk antigen in stool specimens from two ill passengers on the first cruise demonstrated that Norwalk virus caused this outbreak. The symptoms experienced by passengers on the four subsequent cruises suggest that a Norwalk agent probably also caused these outbreaks. In addition, a stool specimen from an ill passenger on cruise 3 contained Norwalk antigen.American Journal of Epidemiology 01/1981; 112(6):820-7. · 4.78 Impact Factor
Cruise S hip
Elmira T. Isakbaeva,* Marc-Alain Widdowson,*†
R. Suzanne Beard,* Sandra N. Bulens,*†
James Mullins,* Stephan S. Monroe,*
Joseph Bresee,* Patricia Sassano,‡
Elaine H. Cramer,* and Roger I. Glass*
An outbreak of norovirus gastroenteritis affected
passengers on two consecutive cruises of ship X and con-
tinued on 4 subsequent cruises despite a 1-week sanitiza-
tion. We documented virus transmission by food and
person-to-person contact, persistence of virus despite san-
itization onboard, introduction of new strains, and seeding
of an outbreak on land.
secutive cruises and the use of sequence analysis to
determine modes of virus transmission. Noroviruses
(NoV), are the most common cause of infectious acute
gastroenteritis and are transmitted feco-orally through
food and water, directly from person to person and by
environmental contamination (1). These viruses are often
responsible for protracted outbreaks in closed settings,
such as cruise ships, nursing homes, and hospitals (2,3).
On November 20, 2002, cruise ship X recorded an ele-
vated number of persons with acute gastroenteritis symp-
toms reporting to the ship’s infirmary (84 [4%] of 2,318
passengers) during a 7-day vacation cruise from Florida to
the Caribbean. According to federal regulations, when the
incidence of acute gastroenteritis among passengers and
crew exceeds 3%, an outbreak is defined and requires a for-
mal investigation (4). The outbreak continued on the subse-
quent cruise (cruise 2), after which the vessel was removed
from service for 1 week of aggressive sanitization. Despite
cleaning, gastroenteritis also developed in 192 (8%) of
2,456 passengers and 23 (2.3%) of 999 crew on the follow-
ing cruise (cruise 3). To determine the source of this contin-
uing outbreak and to better understand the mechanisms of
NoV transmission, we began an investigation on cruise 1
and collected stool specimens from persons with gastroen-
teritis on this cruise and the next 5 cruises.
e describe an investigation of a norovirus gastroen-
teritis outbreak aboard a cruise ship affecting 6 con-
We surveyed all 2,318 passengers on cruise 1 to deter-
mine dates of illness onset, symptoms, cabin locations,
activities, and food consumption. We also performed a
sanitary inspection of the ship. We suspected that initial
infection among passengers on cruise 1 originated from a
common food or water source and then continued to spread
from person to person. Therefore, we conducted a case-
control study with all passengers in whom illness devel-
oped early in the cruise (days 3 and 4) after embarkation
(defined as day 1) and also with passengers who became ill
later (day 5). Controls were systematically selected among
passengers who reported no symptoms of gastroenteritis
throughout the entire cruise. We continued to monitor the
number of cases of acute gastroenteritis on the subsequent
5 cruises and collected fecal specimens from ill persons on
all 6 cruises. During our shipboard investigation, we also
obtained stool specimens from ill persons in a long-term
care facility affected by an outbreak of acute gastroenteri-
tis, in which the index patient was a passenger who
returned ill to the facility after disembarking from cruise 1.
All stool specimens were tested for NoV by reverse tran-
scription–polymerase chain reaction, as previously
described (5). The positive amplicons were sequenced, and
sequences were compared for genetic diversity.
The outbreak began abruptly on day 2 of cruise 1 and
continued on cruise 2 with new passengers. Despite saniti-
zation of the ship for 1 week after cruise 2, illness was also
reported among passengers on cruise 3 (Figure 1). On the
subsequent cruises (4–6), the number of ill persons report-
ing to the infirmary remained above background levels but
below 3%. Of the 2,318 surveyed passengers on cruise 1,
1,276 (55%) returned questionnaires, of these, 212 case-
passengers and 265 control-passengers were enrolled in our
study. We identified that eating breakfast at restaurant Aon
154Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 1, January 2005
*Centers for Disease Control and Prevention, Atlanta, Georgia,
USA; †Atlanta Research and Education Foundation, Atlanta,
Georgia, USA; and ‡Bucks County Department of Health,
Doylestown, Pennsylvania, USA
Figure 1. Number (%) of cases of acute gastroenteritis among 513
passengers and 74 crew by date of symptom onset reported to the
infirmary on 6 consecutive cruises of ship X, November
2002–January 2003. Arrows indicate start and end of each cruise.
day 2 of the cruise was associated with illness among case-
passengers with onset of symptoms on day 3 (odds ratio
[OR] 4.04, p < 0.01) and that eating dinner at the same
restaurant on day 2 was a risk factor for illness among case-
passengers who became ill on day 4 (OR 2.8, p < 0.005).
We also found that eating dinner at restaurant B aboard ship
on day 3 was associated with illness among case-passen-
gers with onset on day 5 (OR 2.3, p < 0.05). Restaurants A
and B did not share a galley. Case-passengers with later
onset of illness on day 5 were more likely than controls to
have a cabin mate in whom gastroenteritis developed on
days 3 or 4 (OR 2.01, p = 0.01), which suggests either
infection by environmental contamination or by person-to-
Of 55 tested stool specimens from all 6 cruises, 25
(45%) were positive for NoV and belonged to 6 strains
(Table). Norovirus was detected in at least 1 stool sample
from all cruises, except cruise 4, where no stool samples
were found positive, and in 2 samples of ill persons from
the long-term care facility. The genetic sequences detect-
ed on cruises 1 and 2 were identical in regions B and C
and belonged to a lineage of NoV within genogroup II
(GII), cluster 4 (Figure 2), which has been provisionally
described as the Farmington Hills strain (6). Five of the 8
NoV-positive specimens on cruise 3, which sailed after
sanitization, contained 3 different sequences (X, Y, and
Z). Sequence X was found in 1 sample and was identical
to the sequence detected on cruises 1 and 2, which sug-
gested that this strain may have persisted onboard despite
cleaning. Sequence Y was found in 3 samples and differed
from sequence X by 3 nucleotides (nt) in region C, which
suggested that it was the predominant strain and probably
newly introduced by passengers or crew at the start of
cruise 3. Sequence Z was detected in 1 sample and
belonged to the same lineage of NoV as the strain found
on cruises 1 and 2 but to a different cluster (cluster 3),
which suggested that it was also newly introduced onto
cruise 3. Single stool samples from persons on cruises 5
and 6 contained a sequence that differed from the
Farmington Hills strain by 3 nt and 1 nt, respectively,
which suggested probable continuous reintroductions of
closely related viruses aboard the ship. A sequence
indistinguishable from that found on cruises 1 and 2 was
also detected in stool samples from 2 persons ill in the
outbreak that occurred in the long-term care facility,
which suggested that virus was possibly introduced by the
ill passenger from cruise 1. The environmental inspection
of the ship identified no major violations.
We report on a large outbreak of NoV-related gastroen-
teritis that affected 6 consecutive cruises on 1 ship and
recurred despite thorough sanitization after the second
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 1, January 2005155
Norovirus Transmission on Cruise Ship
Figure 2. Phylogram of 9 norovirus sequence types detected in
outbreaks on ship X, 4 reference sequences from GenBank, and
the Farmington Hills virus. The tree is based on a 277-nucleotide
region (region C) of the capsid gene and was created using uncor-
rected distances calculated by the DISTANCES program
(Genetics Computer Group, Madison, WI) and was constructed by
neighbor-joining using the GROWTREE program version 10.3
(Genetics Computer Group). Numbers in parenthesis indicate
number of samples with the identical sequence detected in a given
outbreak. Box highlights sequence types belonging to the
Farmington Hills virus that are indistinguishable in region C.
GenBank accession no. for reference strains include Bristol virus,
X76716; Toronto virus, U02030; Hawaii virus, U07611; and
Norwalk virus, M87661. Scale bar represents 10% divergence.
cruise. In the past, investigations of shipboard outbreaks of
viral gastroenteritis were limited by the lack of adequate
molecular methods for detecting and characterizing
viruses (7). In this investigation, epidemiologic analysis
suggested an initial foodborne source of infection with
subsequent secondary spread from person to person, while
molecular analysis provided several new insights into dis-
ease transmission. Application of genetic sequencing doc-
umented persistence of the same strain onboard between
cruises by detecting identical sequences in stool samples
from ill passengers before and after 1 week of the vessel’s
cleaning. Although these findings suggest that environ-
mental contamination may have helped perpetuate the out-
break, infected crew members could have also been a
reservoir of infection between cruises. Molecularly finger-
printing of detected viruses confirmed several introduc-
tions of new strains aboard, which underscores the
difficulty in controlling outbreaks of NoV on cruise ships.
Sequence analysis provided evidence that an outbreak of
NoV in the care facility was caused by a person returning
ill from an outbreak-affected cruise.
Like other outbreaks of viral gastroenteritis on cruise
ships (3,6,8–11), this outbreak affected several hundred
people, was transmitted by multiple modes, and recurred
on subsequent cruises. Multiple routes of NoV transmis-
sion have been documented in other reports, such as that of
an outbreak of gastroenteritis among football players, in
which initial foodborne transmission of virus and second-
ary person-to-person spread was demonstrated (12).
Outbreaks of gastroenteritis aboard cruise ships are similar
to those in other closed and crowded settings where iden-
tifying and interrupting multiple routes of transmission has
proved particularly challenging (2,13,14).
A limitation of this study was that the investigation on
cruise 1 started 7 days after the first cases were reported,
and because of logistic constraints, surveying was restrict-
ed to passengers in a short period before their disembarka-
tion. Thus, we were unable to investigate risk factors for
illness among crew and determine if any of the food-han-
dlers were ill. In addition, poor recall of exposures result-
ed in a lack of complete data for a detailed evaluation of
risk factors. We also did not perform a full investigation on
the subsequent cruises because the number of ill persons
did not exceed 3%.
Our investigation suggests that efforts to control gas-
troenteritis outbreaks on cruise ships should address all
possible modes of NoV transmission, including foodborne,
environmental persistence, and person-to-person spread.
Such measures should include extensive disinfection, good
food and water handling practices, isolating ill persons,
providing paid sick leave for ill crew, and promoting hand-
washing with soap and water among passengers and crew.
Developing strategies and incentives to dissuade sympto-
matic passengers from boarding may also minimize oppor-
tunities to introduce new strains aboard. Cruise ship out-
breaks with <3% of passengers reporting ill should be
considered for investigation because they may contribute
substantial information on the transmission and epidemio-
logic characteristics of NoV, which could be used to devel-
op control strategies and prevent future outbreaks on land
and at sea.
We thank Jaret Ames and Donald Ackerman for their assis-
tance during the investigation; passengers, crew members, and
representatives of the cruise line for their support; Susan Adams,
Leslie Hadley, Du-Ping Zheng, and Howard White for reverse
transcription–polymerase chain reaction testing performed at
CDC; Lenee Browne for assistance during the analysis; and
Claudia Chesley for excellent editorial comments.
The investigation was funded by CDC and by Bucks County
Dr. Isakbaeva was an officer with the Epidemic Intelligence
Service at the Centers for Disease Control and Prevention when
this investigation was conducted. She currently serves as a senior
adviser in the Department of Infectious Diseases Epidemiology
at the Norwegian Institute of Public Health in Oslo, Norway. Her
research interests focus on control of communicable diseases.
1. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS,
Parashar UD, et al. Epidemiologic and molecular trends of “Norwalk-
like viruses” associated with outbreaks of gastroenteritis in the
United States. J Infect Dis. 2002;186:1–7.
2. Green KY, Belliot G, Taylor JL, Valdesuso J, Lew JF, Kapikian AZ,
et al. A predominant role for Norwalk-like viruses as agents of epi-
demic gastroenteritis in Maryland nursing homes for the elderly. J
Infect Dis. 2002;185:133–46.
3. Gunn RA, Terranova WA, Greenberg HB, Yashuk J, Gary GW, Wells
JG, et al. Norwalk virus gastroenteritis aboard a cruise ship: an out-
break on five consecutive cruises. Am J Epidemiol. 1980;112:820–7.
4. Cramer EH, Gu DX, Durbin RE. Diarrheal disease on cruise ships,
1990–2000: the impact of environmental health programs. Am J Prev
5. Anderson AD, Heryford AG, Sarisky JP, Higgins C, Monroe SS,
Beard RS, et al. A waterborne outbreak of Norwalk-like virus among
snowmobilers—Wyoming, 2001. J Infect Dis. 2003;187:303–6.
6. 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;190:27–36.
7. Bresee JS, Widdowson MA, Monroe SS, Glass RI. Foodborne viral
gastroenteritis: challenges and opportunities. Clin Infect Dis.
8. Ho MS, Glass RI, Monroe SS, Madore HP, Stine S, Pinsky PF, et al.
Viral gastroenteritis aboard a cruise ship. Lancet. 1989;2:961–5.
9. 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;32:861–6.
156 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 1, January 2005
10. Khan AS, Moe CL, Glass RI, Monroe SS, Estes MK, Chapman LE,
et al. Norwalk virus-associated gastroenteritis traced to ice consump-
tion aboard a cruise ship in Hawaii: comparison and application of
molecular method-based assays. J Clin Microbiol. 1994;32:318–22.
11. McEvoy M, Blake W, Brown D, Green J, Cartwright R. An outbreak
of viral gastroenteritis on a cruise ship. Commun Dis Rep CDR Rev.
12. Becker KM, Moe CL, Southwick KL, MacCormack JN.
Transmission of Norwalk virus during football game. N Engl J Med.
13. Sharp TW, Hyams KC, Watts D, Trofa AF, Martin GJ, Kapikian AZ,
et al. Epidemiology of Norwalk virus during an outbreak of acute
gastroenteritis aboard a U.S. aircraft carrier. J Med Virol.
14. Kuusi M, Nuorti JP, Maunula L, Minh NN, Ratia M, Karlsson J, et al.
A prolonged outbreak of Norwalk-like calicivirus (NLV) gastroen-
teritis in a rehabilitation centre due to environmental contamination.
Epidemiol Infect. 2002;129:133–8.
Address for correspondence: Marc-Alain Widdowson, Centers for
Disease Control and Prevention, 1600 Clifton Rd NE, Mailstop A34,
Atlanta, GA 30333, USA; fax: 404-639-4960; email: MWiddowson@
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 1, January 2005 157
Norovirus Transmission on Cruise Ship
Use of trade names is for identification only and does not imply
endorsement by the Public Health Service or by the U.S.
Department of Health and Human Services.
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