Background
- On June 4, 2000, senior management officials from Disney Cruise Lines notified the staff of the Vessel Sanitation Program (VSP), National Center for Environmental Health (NCEH), Centers for Disease Control and Prevention (CDC), of an outbreak of gastroenteritis among passengers and crew aboard the Disney Magic cruise ship. In accordance with statutory requirements (Part 71, Section 215 of the Public Health Service (PHS) Act [Title 42, of the United States Code of Federal Regulations]), ship officials contacted VSP 24 hours before arriving at a U.S. port to report the total number of cases of gastroenteritis among passengers and crew members.
- The ship had embarked passengers in Port Canaveral, Florida, at approximately noon on June 2, 2000, and was scheduled to return to Port Canaveral on Monday, June 5, 2000, (Table 1). On June 4, 2000, the ship’s doctor reported that by the morning of the third day of the 4-day cruise, approximately 50 (1.9 %) of 2,601 passengers and 10 (1.1%) of 930 crew aboard the Disney Magic had reported to the ship infirmary with gastroenteritis, characterized primarily by diarrhea (three or more episodes of loose stools in 24 hours) and vomiting. By that evening, 50 more passengers had reported to the infirmary with gastroenteritis, totaling 100 (3.8%) of the 2,601 passengers ill.
- On the basis of these reports (greater than 3% of passengers and crew members ill with gastroenteritis), and the rapid rise in the number of cases, VSP initiated an epidemiologic and environmental investigation. The VSP medical epidemiologist flew to Florida to board the vessel on June 5, 2000, in Port Canaveral, the next port of the vessel's itinerary and the port of disembarkation for passengers. The VSP epidemiologist was accompanied on the investigation by three environmental health officials from Walt Disney World’s land-based environmental operations and several management officials.
- Objectives
- The objectives of the investigation were to 1) identify the etiologic agent(s) associated with the outbreak; 2) determine the source(s) of spread of illness among passengers and crew; 3) formulate interventional strategies to control the outbreak and prevent a recurrence.
Methods
- Epidemiologic Investigation
- Case Definition
- A case of gastroenteritis was defined as diarrhea (three or more episodes of loose stools in a 24-hour period) or vomiting in a passenger or crew member aboard the Disney Magic with onset on or after June 2, 2000. Well passengers or crew members were defined as people reporting no gastrointestinal symptoms during the 4-day cruise. People who reported symptoms but whose illness did not meet the case definition were classified as having indeterminate illness and were excluded from the cohort study.
- Case Interviews
- Several case-patients among passengers and all case-patients among crew members were interviewed in person by the ship medical staff to review exposure histories and identify individual risk factors for acquiring gastroenteritis before the onset of illness. Passengers who reported to the infirmary were asked to complete self-administered 48-hour food history questionnaires to further qualify exposure histories.
- Records Review
- The VSP epidemiologist reviewed an electronic copy of the ship's medical log for information about gastrointestinal symptoms among passengers and crew during the cruise and to verify attack rates. The medical doctor and nursing staff aboard the vessel maintained the log. On the evening of June 4, 2000, VSP generated a preliminary epidemic curve on the basis of entries in the medical log meeting the case definition, to determine the most likely period of exposure to illness. To generate a hypothesis, the epidemiologist reviewed self-administered food history questionnaires completed by ill passengers who were treated in the infirmary.
- Food Menus and Passenger Activities
- VSP obtained ship menus for the Disney Magic for the cruise of June 2-5, 2000, from Disney Cruise Line personnel. VSP staff interviewed the food and beverage manager and the executive chef, by telephone 1) to review food preparation and handling procedures 2) to identify all on-board restaurants and areas in which foods were served, and 3) to match items listed on menus with food-production records. VSP staff also reviewed water and ice handling procedures as well as daily passenger and crew activities.
- Passenger Survey
- A standardized passenger questionnaire, based on ship menus, food-preparation practices, daily activities, and the likely period of exposure to the suspected causal pathogens as determined by the epidemic curve (Figure 1), was faxed to the ship on the evening of June 4, 2000. Disney hotel staff placed one questionnaire under each of the 875 passenger cabin doors on the evening of June 4, 2000. Interviewees were asked about demographic information and risk factors for illness (e.g., shore excursions, food and water consumed) and were asked to select from a list of food items the foods they ate during the cruise. VSP staff used the questionnaires to characterize passenger demographics, timing of illness, attack rates, symptomatology, and risk factors for illness. Disney Cruise line staff collected the questionnaires on the morning of June 5, 2000, before passengers disembarked at Port Canaveral, Florida.
- Statistical Methods
- On June 6, 2000, under the supervision of the VSP epidemiologist, five Disney clerical staff entered questionnaire data into an electronic data base. The VSP epidemiologist analyzed data using Epi Info version 6.02 software.
- Analysis of disease onset was based on returned questionnaires from ill passengers who met the case definition. Descriptive and cohort analyses were based on the entire passenger data set. Baseline characteristics of ill and well passengers and crew (e.g., symptomatology and water, food, and ice consumption) were described by frequencies and percentiles for categorical variables (e.g., number of people with diarrhea), and ranges of values for continuous variables (e.g., age, time of onset of illness). Exposure variables were coded as dichotomous variables. In univariate analysis, VSP staff used risk ratios with 95% confidence intervals (CIs) to test for differences in illness risk between ill and well people.
- Laboratory Investigation
- From June 3-5, 2000, Disney medical staff collected stool samples from ill passengers and crew members for bacterial, viral, and parasitic testing. Whole stools were transported in specimen cups to the Centers for Disease Control and Prevention (CDC) on ice and were tested for small, round-structured virus (SRSV) using electron microscopy (EM) and for Norwalk-like virus using reverse transcriptase- polymerase chain reaction (RT-PCR) analysis using a "region B" primer set. Bacterial swabs of whole stool specimens were transported in Cary-Blair medium on ice to CDC and examined for bacterial pathogens (Campylobacter, Salmonella, Shigella, Vibrio parahaemolyticus, diarrheagenic Escherichia coli, and Yersinia enterocolitica). Split specimens obtained from whole stools were preserved in 10% formalin and were analyzed for antigens to Cryptosporidium oocysts and Giardia cysts and antibodies using a direct immunofluorescent antibody (FA) detection kit (Merifluor by Meridian Diagnostics, Inc., Cincinnati, OH). Epidemiologically implicated foods were cultured for enteric bacterial pathogens using standard methods.
- Environmental Investigation/Sanitation Inspection
- The investigative team conducted a review of environmental health factors aboard the ship that included housekeeping, food safety, and potable water-system chlorination procedures. The chef and food and beverage manager were interviewed in person while members of the investigative team were aboard the ship and were also interviewed during a conference call with VSP on June 7, 2000. A review of housekeeping procedures included evaluating infection-control measures, routine cabin and public space cleaning practices, and laundry facilities. A review of food safety measures included food storage, preparation, cleaning, and service practices in the galley. Areas of the ship where provisions were stored, thawed, prepared, and cooked were viewed, and procedures for preparing fish and seafood were reviewed in detail. VSP reviewed temperature logs for all food-refrigeration units and ship records of the free residual chlorine concentration in the potable-water holding tanks and the distribution system.
Results
- Epidemiologic Investigation
- Descriptive epidemiology
- Of the 875 passengers surveyed, 405 (46%) returned completed questionnaires. Because relatively few crew members were reported ill by active surveillance for illness conducted by medical and hotel staff and crew meals and living quarters were distinct from passenger quarters and meals, VSP did not survey the crew. Of passenger-respondents, 224 (55 %) reported having had symptoms that met the case definition of gastroenteritis; 9 (2.2 %) had indeterminate illness and were excluded from further analysis; 172 (42%) were well. Diarrhea was reported in 205 (93%) of cases, vomiting in 64 (30%), nausea in 142 (65%), headaches in 118 (55%), muscle aches in 58 (28%), bloody stools in 8 (4%), abdominal cramps in 170 (80%), and fever in 35 (18 %; [Table 2]). The duration of illness for 60 (60%) of 101 people who had recovered by the time the questionnaire was completed, the duration of illness was 2 days or more; 153 (72%) reported the onset of illness on June 3, 2000, the second day of the cruise. Dates of the onset of illness ranged from June 2, 2000 through June 5, 2000. The median age of ill passengers was 40 years (range 2-84 years); 112 (52%) of case subjects who responded were female. Seven passengers (2 males, 5 females; age 28-60 years) were hospitalized in the infirmary to receive intravenous fluids for rehydration. No crew members were diagnosed with or treated for dehydration.
- Cohort study
- VSP’s unadjusted analysis showed that 196 (59%) of 331 passengers who ate the embarkation lunch on June 2, 2000, were 97% more likely to experience gastroenteritis than 12 (30 %) of 40 passengers who did not eat lunch (relative risk [RR] = 1.97;CI = 1.22,3.20; [Table 3]); 100 (76 %) of 131 passengers who consumed shrimp from the shrimp fountain served at the embarkation lunch buffet were 59% more likely to become ill compared with 93 (48%) of 194 who ate lunch, but who did not eat shrimp (RR = 1.59; CI = 1.34,1.90). Although the embarkation lunch buffet on June 2, 2000, was served at two restaurants (Topsider’s and Parrot Cay), the menus and foods for both restaurants were identical and were provided by the same galley. Because many passengers reported eating at both restaurants for lunch and were often unable to distinguish between the two buffet lines, the lunch buffet was treated as one variable. There were no statistically significant differences in gastroenteritis attack rates when VSP compared risks associated with any other meals or foods consumed, dining-seating or cabin assignments, or consumption of tap water aboard the ship.
- Laboratory Investigation
- Whole stool samples were collected from 14 ill people (10 passengers, 4 crew members ); swabs for bacterial analysis were obtained from each of the whole stools. Three swabs of fresh stool specimens obtained from two passengers and one crew member yielded enterotoxigenic E. coli. (ETEC). Two of these isolates obtained from one passenger and one crew member possessed the gene sequence for heat-stable toxin (ST) and were serogroup O25:NM. The other isolate possessed both the gene sequence for both the ST and heat-labile (LT) toxin (LT/ST), and were serogroup O6:H16. Two swabs obtained from stool specimens from two passengers yielded Salmonella (S.): two S. Newport and one S. Java. An isolate, forwarded from the Florida State Health Department Laboratories to the CDC laboratory yielded S. Lexington.
- None of the whole stool specimens was positive for small round-structured virus (SRSV) by electron microscopy or for Norwalk-like virus by RT-PCR with a "region B" primer set. Specimens were negative for Shigella spp., Vibrio spp., Campylobacter jejuni, Yersinia spp., and E. coli 0157: H7. One passenger specimen was positive for Giardia by antigen testing and by FA.
- A total of 83 food samples was obtained from foods stored in the dairy, pastry, seafood, fish, fresh meat, juice, and dry-store refrigerators and from the vegetable, seafood, and fish freezers in the ship’s galley and food preparation and stores areas. Specimens were shipped on dry ice to the CDC laboratory from the Disney Magic. A sample of cooked shrimp, which had been served at the embarkation lunch buffet on June 2, 2000, yielded S. Newport. A sample of the remaining supply of raw, frozen shrimp used to prepare the shrimp fountain yielded no bacteria when tested in the laboratory. Two samples of raw, frozen shrimp collected by Disney's environmental health department from the remaining supply used to prepare the shrimp fountain, tested in Disney laboratories and confirmed by CDC laboratory, both yielded Salmonella.
- Environmental Investigation
- Medical Record Keeping and Case Management
- Record keeping aboard the ship was good. The ship’s medical log accurately reflected the number of ill passengers and crew treated by medical staff in the ship’s infirmary. Self-administered food-history questionnaires were maintained with the gastrointestinal illness log. Ill crew members were quarantined in their cabins until they were symptom-free for 72 hours, and cabin mates of ill crew members who had duties in the galley were also asked to remain off of work for 48 hours until it was confirmed that they did not have gastroenteritis.
- Housekeeping Practices and the Potable Water System
- There were good procedures in place for cabin cleaning, public-area (surface) cleaning, and laundry practices. During the cruise, water was bunkered at Port Canaveral on July 2, 2000. From potable-water chlorine-analyzer records, we determined potable water chlorine levels were appropriate (between 1.0 and 4.0 ppm) at the distribution-system level during the entire cruise, never dropping below the 0.2 ppm minimum requirement. Analysis of samples collected and tested by the ship engineering staff from the potable-water distribution system, revealed appropriate chlorine concentrations in the potable-water holding tanks and distribution system and no evidence of coliforms or E. coli bacteria.
- Food Safety
- VSP staff reviewed with the executive chef, the food and beverage manager, and the seafood cooks the standard operating procedures for preparing shrimp used for the embarkation lunch buffet on June 2, 2000. Frozen, raw, shell-on shrimp was loaded into the freezers aboard the vessel on May 29, 2000. On the evening of June 1, 2000, shrimp was moved to the thaw room for thawing under running water in 100-125- pound batches. Fifty-pound portions of the thawed shrimp were transported in plastic bins from the thaw room to the seafood galley and were then boiled for approximately 5 minutes in two large steam kettles. This procedure was repeated four times until a total of approximately 450 pounds of shrimp had been prepared. The cooked product was transferred to stainless steel pans for 2 hours of rapid cooling in the crew galley blast chiller. Internal temperatures of the shrimp during cooking and upon removal from the blast chiller were not taken. The cooked shrimp were then transferred to plastic storage bins and transported to the seafood refrigerator in the seafood preparation area for storage overnight. Storage temperature records for all refrigerator units in the galley revealed consistent temperatures of between 35o F and 39o F.
- At 11:15 a.m. on June 2, 2000, the shrimp were placed on a total of six buffet lines in two restaurants (Topsider’s and Parrot Cay) for service at approximately 12:00 p.m. to approximately 3:30 p.m. The whole shrimp were served and displayed on each buffet line by being placed on a series of chipped ice-filled bowls, set inside each other, giving the appearance of a fountain. None of the food preparation workers who handled the shrimp for the buffet were reported ill. All food service workers were reported to have worn disposable gloves.
- Discussion
- A large outbreak of gastroenteritis caused by bacterial contamination of shrimp served at the embarkation lunch buffet on June 2, 2000, occurred among passengers on the cruise ship Disney Magic, during a cruise from June 2-5, 2000, that began at Port Canaveral, Florida. The epidemic curve among passengers, for this outbreak supports a common source of exposure, with the peak onset of illness on the second day of the cruise. Questionnaire data revealed a statistical association between eating shrimp from the shrimp fountain served at the embarkation lunch buffet on June 2, 2000, and illness among passengers. Laboratory analysis of the implicated shrimp revealed contamination with Salmonella. Clinical and laboratory findings are consistent with contamination of the shrimp with multiple bacteria. The one crew member who submitted an isolate which yielded ETEC was the chef de cuisine, who reported eating the implicated shrimp. The other crew member from India whose isolate yielded Giardia, was a server in the dining room and reported that he did not eat the shrimp.
- Salmonella and ETEC strains of Escherichia coli can both cause acute, self-limited gastroenteritis characterized by diarrhea, nausea, vomiting, abdominal cramps, muscle aches, and fever. In a series of ETEC outbreaks evaluated by CDC, the median incubation period for ETEC ranged from 21-68 hours, a duration that can make presentation of ETEC-related gastroenteritis clinically indistinguishable from salmonellosis. The clinical presentation by passengers with gastroenteritis resulting from this outbreak was compatible with illness caused by both of these bacterial pathogens.
- Findings from the laboratory and environmental investigations suggest contamination of the raw frozen shrimp may have occurred off-site at any stage of product preparation before the shrimp were loaded onto the vessel on May 29, 2000. As well, mishandling of shrimp by food preparation workers including the possibility of cross-contamination of the cooked shrimp with raw shrimp through usage of contaminated transport bins, and through concurrent handling of shrimp during the thawing process and subsequent handling of cooked shrimp in preparation for blast chilling, may have occurred. Because no internal food temperatures were taken by the cooks after the shrimp were boiled for an estimated 5 minutes, and because we do not know the levels of bacterial contamination of the raw shrimp, it is difficult to assess the relative contribution of these factors to the resultant gastroenteritis outbreak.
Recommendations and Follow-up Activities
- On June 7, 2000, VSP held a conference call with executives from Disney Cruise Lines and made the following recommendations for immediate implementation:
- General Recommendations
- 1. Continue to submit daily reports of all diarrheal illness over the next several cruises to monitor for cases of gastroenteritis.
- 2. Reinforce the importance of good hand washing to all officers, staff, and crew. Newly embarking crew members with galley duties should be instructed specifically about proper food-preparation techniques. Staff responsible for greeting passengers should be instructed to wash hands frequently.
- 3. Encourage both passengers and crew with diarrhea to immediately report illness to the infirmary. Passengers reporting illness should be attended to in their own cabins to encourage isolation.
- 4. Continue to conduct surveillance aboard the vessel by documenting cases of illness in the gastrointestinal illness logs. Recommended logs have been reviewed in detail with representatives of the Quality Assurance Department.
- 5. Exclude food handlers with vomiting and diarrhea or a history of vomiting or diarrhea until they are symptom free for 72 hours before returning to duty. Confined cabin mates of sick crew who experience no illness can return to work after 48 hours.
- 6. Continue to aggressively identify and disinfect cabins with a 1:10 concentration of chlorine bleach where sick passengers and crew reside and to disinfect public restrooms, hand rails, and other inanimate surfaces.
- 7. Protect ice from contamination both in transit and when dispersing to passenger cabins.
- 8. Thoroughly disinfect all passenger garbage receptacles and sanitize ice buckets. Use disposable plastic liners in ice buckets and trash cans in all cabins.
- 9. Thoroughly clean and sanitize the heating, ventilation, and air conditioning (HVAC) system.
- 10. Utilize detergent or sanitizer compounds for cleaning surfaces, such as carpeting, that might otherwise be bleached out by the use of chlorine.
- 11. Establish procedures for dealing with soiled passenger clothing and bed linens. Methods such as pre-soaking soiled items with a hospital-grade sanitizer (e.g., a phenolic acid compound containing a sanitizer and detergent) with the addition of an extra rinse cycle using bleach. Soiled items should be kept separate from noncontaminated items.
- 12. Discontinue use of sponges for sanitizing solutions. Use cotton cloths that can be easily laundered or disposable one-use cloths.
- Galley
- 13. Closely monitor temperatures of potentially hazardous foods from receipt, holding, and preparation to service. Document these temperatures with permanent records.
- 14. Use clearly marked, distinct bins for transport of raw and cooked foods to prevent cross-contamination of raw by ready-to-eat foods.
- 15. When preparing the shrimp fountain served on the embarkation buffet, time each segment of the entire process to ensure that the out-of-temperature time is not exceeded. Check internal temperatures of shrimp while thawing and when removed from the blast chiller. Shrimp should be boiled to an internal cooking temperature exceeding 140° F.
- 16. Maintain refrigerator holding temperatures of at 41° F or less. Internal food temperatures within refrigerators should be 45° F or less. To achieve rapid cooling blast, chiller temperatures should not exceed 30° F.
- 17. Mark normal temperature ranges on each refrigeration unit and maintain a separate, permanent log sheet on each unit, including the blast chiller. The blast chiller log should record the time that each food item was placed into and removed from the unit as well as the internal food temperature at the time of removal.
- 18. Sanitize all fresh fruits and vegetables in a 50 parts per million (mg/L) chlorinated water solution before serving.
- 19. In the future, continue to preserve samples of suspicious food items in the event that a foodborne outbreak is suspected. Laboratory analysis of implicated foods can assist in identifying causal pathogens.
- Disney Cruise Lines cooperated fully with this investigation facilitating collection of passenger surveys and passenger and crew clinical specimens and providing copies of updated environmental and medical records. The microbiologist from Walt Disney World conducted food-sample collection. On June 12, 2000, VSP notified The Center for Food Safety and Applied Nutrition (CFSAN), United States Food and Drug Administration (FDA) of the findings of the epidemiologic, environmental, and laboratory portions of this investigation.
- Elaine H. Cramer, MD, MPH
- Medical Epidemiologist
- Vessel Sanitation Program
- National Center for Environmental Health
- Centers for Disease Control and Prevention
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Table 1 Itinerary of the Disney Magic on Which Passengers and Crew Became Ill, June 2-5, 2000 Date of Cruise Port of Call June 2, 2000 - Passenger Embarkation Port Canaveral, FL June 3, 2000 Nassau, Bahamas June 4, 2000 Castaway Cay, Bahamas June 5, 2000 Port Canaveral, FL - * n = 224 passengers
- 1 Defined as three loose stools in a 24-hour period
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Table 3. Unadjusted Gastroenteritis Attack Rates among Passengers Associated with Exposure to Selected Risk Factors Aboard the Cruise Ship Disney Magic, June 2-5, 2000 Risk Factor No. Ill / No. Exposed (%) No. Ill / No. Not Exposed (%) Risk Ratio (CI) p-value Bottled Water 48/87 (55) 47/78 (60) 0.92 (0.70, 1.19) 0.5107 Tap Water 34/58 (59) 43/76 (57) 1.04 (0.77, 1.39) 0.9519 Embarkation Lunch 196/331 (59) 12/40 (30) 1.97 (1.22, 3.20) 0.0008 Any Embarkation Dinner 187/331 (57) 20/33 (61) 0.93 (0.70. 1.25) 0.7869 Embarkation Dinner at Animator's 72/135 (53) 125/223 (56) 0.95 (0.78, 1.16) 0.6951 Embarkation Dinner at Parrot Cay 101/184 (55) 76/151 (50) 1.09 (0.89, 1.34) 0.4703 Embarkation Dinner at Lumiere's 125/224 (56) 69/133 (52) 1.08 (0.88, 1.32) 0.5420 Lettuce (lunch) 28/65 (43) 165/260 (64) 0.68 (0.51, 0.91) 0.0043 Pasta (lunch) 46/78 (59) 147/247 (60) 0.99 (0.80, 1.22) 0.9620 Shrimp fountain 100/131 (76) 93/194 (48) 1.59 (1.34, 1.90) 0.0000 Seafood Newburg 52/82 (63) 141/243 (58) 1.09 (0.90, 1.33) 0.4658 Rice (lunch) 49/99 (50) 144/226 (64) 0.78 (0.62, 0.97) 0.0226 Hamburger 17/32 (53) 176/293 (60) 0.88 (0.63, 1.24) 0.5688 Roast Beef 72/120 (60) 121/205 (59) 1.02 (0.84, 1.22) 0.9555
Investigation Summary: Outbreak of Gastroenteritis Illness Aboard the Cruise Ship, Disney Magic™, June 2 - 5, 2000
| Symptom | Ill Passengers / No. Responding (%) |
| Diarrhea | 205/220 (93) |
| Vomiting | 64/216 (30) |
| Nausea | 142/217 (65) |
| Abdominal Cramps | 170/212 (80) |
| Headache | 118/214 (55) |
| Fever | 35/193 (18) |
| Muscle Aches | 58/205 (28) |
| Bloody Stool | 8/203 (4) |
Centers for Disease Control and Prevention, 1600 Clifton Rd, Atlanta, GA 30333, U.S.A Tel: (404) 639-3311 • CDC Contact Center: 800-CDC-INFO • 888-232-6348 (TTY)
