Outbreaks of illness determined to be caused by enterotoxigenic E. coli in persons who had not traveled outside the United States are not uncommon. In one outbreak, 47 airline passengers suffered from illness strongly associated with eating garden salad made from iceberg and romaine lettuce, endive, and shredded carrots (Beuchat 1996b). In another outbreak, 78 lodge guests became ill after consuming tossed salad as part of a buffet dinner. The salad contained several ingredients, including onions, carrots, zucchini, peppers, broccoli, mushrooms, and tomatoes (Beuchat, 1996, Center for Food Safety and Applied Nutrition, 2001)

Enterohemorrhagic E. coli O157:H7

Enterohemorrhagic E. coli O157:H7 is recognized as an important foodborne pathogen. The infectious dose is very low and sequelae to gastroenteritis can include bloody diarrhea (hemmorrhagic colitis) and hemolytic uremic syndrome. The latter is most common in young children (<5 years) and in the elderly. There have been very few surveys for the presence of the organism in raw produce. Surveys of lettuce or salad mixes in the United Kingdom and United States did not isolate the organism and, although originally included in an FDA imported produce study, it was later deleted because positive samples had not been identified (FDA 2001). However, a single survey in Mexico revealed very high isolation rates (19%) for this organism in mixed vegetables, cilantro, coriander, and celery. This single study was published as an abstract in 1995 and, to our knowledge, has not been published as a peer reviewed manuscript. Therefore, we were unable to review their methodology. (Center for Food Safety and Applied Nutrition, 2001)

Since cattle appear to be a primary reservoir, the vast majority of outbreaks of illness associated with E. coli O157:H7 have been associated with consuming undercooked beef and dairy products. However, outbreaks have also been linked to lettuce, un-pasteurized apple cider, cantaloupe, and sprouts. In outbreaks associated with cantaloupe and in some cases lettuce, contamination, particularly with raw beef juices, occurred during final preparation. (Center for Food Safety and Applied Nutrition, 2001)

Escherichia coli

Escherichia coli O157:H7 grows rapidly in several types of raw fruits and vegetables, particularly when stored at 12°C (53.6°F) or above. Packaging under modified atmosphere has little or no effect on the survival or growth of E. coli O157:H7. In addition, the infection dose of E. coli O157:H7 is low and can develop acid-resistance. (Center for Food Safety and Applied Nutrition, 2001)

Campylobacter

Category: Bacteria

Microorganism: Campylobacter

Other Names: C. Jujuni

Frequency of Occurrence: Common

Typical Incubation Period: 2 to 5 days typically, as long as 10 days

Typical Duration of Illness: 7 days

Infectious Dose (# cells): Not Known

Symptoms: Diarrhea, sometimes bloody, abdominal pain, fever and sometimes accompanied by nausea and vomiting

Source: Feces

Cruise Ship Notes: No confirmed ouotbreaks on cruise ships between 1994-2002 Campylobacter is one of the most common bacterial causes of diarrheal illness in the U.S.  Many cases go unreported and it’s estimated that it affects one million persons every year, or 0.5% of the population, or 4 out of every thousand.  While consumption of contaminated food of animal origin, particularly poultry, is largely responsible for infection, Campylobacter enteritis has also been associated with lettuce or salads.

Cross-contamination during food preparation was thought to be possible or probable, in one case with raw chicken juices. Cross-contamination of fresh produce with Campylobacter from poultry and other meats is a distinct possibility in delicatessen and other foodservice operations. Some studies have also shown its ability to survive on sliced watermelon and papaya. (Balch, 2000), (Center for Food Safety and Applied Nutrition, 2001)

Clostridium Botulinum (Botulism)

Category: Bacteria

Microorganism: Clostridium botulinum

Other Names: Botulism

Frequency of Occurrence: Rare

Typical Incubation Period: 12 to 48 hours, but may be as long as 10 days

Typical Duration of Illness: Up to 6-9 months

Infectious Dose (# cells): intoxication growth and toxin production in food

Symptoms: Nausea, vomiting, fatigue, dizziness, dryness of mouth and throat, muscle paralysis, difficulty swallowing, double or blurred vision, drooping eyelids, and breathing difficulties

Source: Soil, lakes, streams, decaying vegetation, reptiles

Cruise Ship Notes: No confirmed outbreaks on cruise ships between 1994-2002

Botulism can result in death due to respiratory failure and possible infection should not be taken lightly. Botulism is more closely related to cooked vegetables than to fresh produce. The organism enjoys a low acidic environment has been shown to grow on cabbage, asparagus, green beans, beets, butternut squash, sliced unions and corn in a contaminated environment. It has also been associated with garlic in oil, chili peppers, tomatoes and fermented fish. Visible signs of spoilage are not required.

Legionella

Category: Bacteria

Microorganism: Legionnella

Other Names:

Frequency of Occurrence: Not Common

Typical Incubation Period:

Typical Duration of Illness:

Infectious Dose (# cells): Unknowns

Symptoms: Bloody diarrhea, abdominal pain. Can lead to hemolytic uremic syndrome and kidney failure especially in children and the elderly.

Source: Animal feces, especially cattle, deer and human; cross contamination from raw meat

Cruise Ship Notes:

(Center for Food Safety and Applied Nutrition, 2001)

Salmonellellosis (Salmonella)

Category: Bacteria

Microorganism: Salmonella

Other Names:

Frequency of Occurrence: Frequent Infections

Typical Incubation Period: 6 to 24 hours

Typical Duration of Illness:

Infectious Dose (# cells): Unknown

Symptoms: Nausea, vomiting, abdominal cramps, diarrhea, fever, weakness

Source: Contaminated aerosols

Cruise Ship Notes: NONE Outbreak of typhoid fever (Salmonella typhi infections) followed possible cross-contamination between parallel sewer and water lines during maintenance procedures. (CDC, 1988, Balch, 2000)

Shingella spp.

Category: Bacteria

Microorganism: Shigella spp.

Other Names:

Frequency of Occurrence:

Typical Incubation Period: 1 to 3 d

Typical Duration of Illness:

Infectious Dose (# cells): ~10

Symptoms: Abdominal pain, diarrhea, fever, vomiting

Source: human feces

Cruise Ship Notes: An outbreak of Shigella sonnei infections was associated with drinking untreated well water at a summer camp. (CDC, 1988) The genus Shigella is composed of four species, Shigella dysenteriae, Shigella boydii, Shigella sonnei, and Shigella flexneri. All species are pathogenic to humans at a low dose of infection. Shigellosis is usually transmitted from person-to-person but may also occur by consumption of contaminated water and foods, including foods such as fruits or vegetables that have received little or no heat treatment. Several large outbreaks of shigellosis have been attributed to the consumption of contaminated raw vegetables. A lettuce processing facility was the common source of product responsible for outbreaks caused by S. sonnei that occurred simultaneously on two university campuses in Texas (Table O7). Ill students on both campuses had eaten salads from self-serve salad bars. Lettuce was the only produce item used in salads consumed by all students who became ill. (Center for Food Safety and Applied Nutrition, 2001)

In another outbreak of S. sonnei gastroenteritis was associated with eating shredded lettuce. All implicated restaurants received shredded lettuce from the same produce facility. An investigation suggested that a worker in the plant was the source of contamination and that the method of processing allowed contamination of the lettuce. (Center for Food Safety and Applied Nutrition, 2001)

Two mid-western United States outbreaks of S. flexneri infection have been linked to the consumption of fresh green onions (see Beuchat, 1996b). The onions were traced to shippers in California who obtained most of their green onions from a single farm in Mexico. It was concluded that contamination may have occurred in Mexico at harvest or during packing. (Center for Food Safety and Applied Nutrition, 2001)

Shigella sonnei can survive on lettuce at 5°C (41°F ) for 3 days without decreasing in number, and increased by more than 1000-fold at 22°C (71.6°F). Shigella can grow in shredded cabbage and chopped parsley stored at 24°C (75.2°F). Populations of S. sonnei, S. flexneri, and S. dysenteriae inoculated onto the surface of freshly cut cubes of papaya, jicama, and watermelon increased substantially within 4-6 h at 22-27°C (71.6-80.6°F). The pH values of the three fruits were 5.69, 5.97 and 6.81, respectively. (Center for Food Safety and Applied Nutrition, 2001)

Staphylococcal Aureua

Category: Bacteria

Microorganism: Staphylococcal aureua

Other Names:

Frequency of Occurrence: Common

Typical Incubation Period: 1 to 8 hours

Typical Duration of Illness:

Infectious Dose (# cells): Unknown

Symptoms: Nausea, vomiting, abdominal pain, diarrhea

Source: human skin

Cruise Ship Notes: Food poisoning

Staphylococcus aureus has been detected on fresh produce and ready-to-eat vegetable, salads, and is known to be carried by food handlers. However, enterotoxigenic S. aureus does not compete well with other microorganisms normally present on fresh produce, so incipient spoilage caused by nonpathogenic microbiota would likely precede the development of high populations of this pathogen. An outbreak of staphylococcal foodborne illness was linked to canned mushrooms. (Center for Food Safety and Applied Nutrition, 2001)

Growth and toxin production occurred prior to processing the mushrooms, without significant visual degradation, possibly because the mushrooms were held under ambient conditions in plastic bags and with salt. Conditions within the bags rapidly became anaerobic and the normal spoilage microbiota may have been inhibited and S. aureus selected. Because the toxin is heat stable, it survived the thermal process. This suggests that raw produce-associated outbreaks due to S. aureus could potentially occur given the right conditions. S. aureus has been shown to grow on peeled Hamlin oranges stored at 24°C (75.2°F) or survived up to 14 d when stored at 4-8°C (39.2-46.4°F). (Center for Food Safety and Applied Nutrition, 2001)

Listeria Monocytogenes

Category: Bacteria

Microorganism: Listeria monocytogenes

Other Names:

Frequency of Occurrence: Rare

Typical Incubation Period: 14 to 28 days

Infectious Dose (# cells): Unknown dependent upon health of individual

Symptoms: Febrile gastroenteritis in healthy adults; may lead to spontaneous abortion or stillbirth in pregnant women; severe septicemia and meningitis in neonates and immunocompromised adults; mortality may be 20 to 40%

Source: soil, food-processing environments

While L. monocytogenes causes relatively mild gastroenteritis in healthy adults, the illness can be severe in susceptible individuals including pregnant women, neonates, and immune compromised individuals. The infective dose for this organism has not been clearly established, although it is thought to be relatively low among susceptible individuals. Listeria monocytogenes is widely distributed on raw fruits and vegetables and on plant material (Beuchat 1996b). However several studies with relatively large sample sizes failed to detect the organism. Factors affecting its presence or persistence have yet to be determined. Plants and plant parts used as salad vegetables play a role in disseminating the pathogen from natural habitats to the human food supply. This role may be indirect, for example by contaminating milk via forage or silage, or direct in the form of raw contaminated produce. In 1967, Blenden and Szatalowicz (1967) reported that 731 cases of human listeriosis had been documented between 1933 and 1966 in the United States. (Center for Food Safety and Applied Nutrition, 2001)

They stated that produce such as lettuce or other fresh vegetables contaminated with L. monocytogenes may have been responsible for some of these cases. However, documented outbreaks associated with this organism and linked to fresh produce have been limited. Ho and others (1986) reported an outbreak of L. monocytogenes infection that involved 23 patients from eight Boston hospitals in 1979. Three foods (tuna fish, chicken salad and cheese) were preferred by case patients more frequently than by control patients. However, the only common foods served with these foods were raw celery, tomatoes, and lettuce. It was concluded that consumption of these vegetables may have caused the listeriosis outbreak. No attempt was made to isolate L. monocytogenes from vegetables at the time of the outbreak. (Center for Food Safety and Applied Nutrition, 2001)

An outbreak of human infection due to L. monocytogenes occurred in 1981 in the Maritine provinces (Prince Edward Island, Nova Scotia and New Brunswick) in Canada. A case-control survey revealed that cases were more likely than controls to have consumed coleslaw during the three months before onset of illness. Ingestion of radishes was associated with coleslaw consumption but not with illness. Coleslaw obtained from the refrigerator of a patient was positive for L. monocytogenes serotype 4b, which was the epidemic strain and the strain isolated from the patient's blood. The coleslaw was commercially prepared with cabbage and carrots obtained from wholesalers and local farmers. Two unopened packages of coleslaw purchased from two different Halifax, Nova Scotia supermarkets yielded L. monocytogenes serotype 4b. The same processor produced both packages of coleslaw. An investigation of the sources of cabbage revealed one farmer who, in addition to raising cabbage, maintained a flock of sheep. Two of his sheep had died of listeriosis in 1979 and 1981. The farmer used composted and fresh sheep manure in fields in which cabbage were grown. From the last harvest in October through the winter and early spring, cabbage was kept in a cold-storage shed. A shipment of cabbage from that shed during the period of the outbreak was traced to the implicated coleslaw processor. This information strongly suggests that the vehicle of the 1981 Canadian outbreak of listerosis was coleslaw. (Center for Food Safety and Applied Nutrition, 2001

Listeria monocytogenes can grow on fresh produce stored at refrigerated temperature. Growth on fresh-cut fruit as well as asparagus, broccoli, butternut squash, coleslaw and cauliflower, rutabaga stored at 4°C (39.2°F), lettuce at 5°C (41°F) and chicory endive at 6.5°C (43.7°F) has been reported. Controlled atmosphere storage does not appear to influence growth rates. Carrot juice appears to be inhibitory towards this organism (Beuchat and Brackett 1990a; Nguyen-the and Lund 1991, 1992; Beuchat and others 1994; Beuchat and Doyle 1995). The antimicrobial properties are attributed to phytoalexins naturally present in carrots. The addition of carrot juice as a natural antimicrobial in other food products has been relatively unsuccessful (Beuchat and Doyle 1995). (Center for Food Safety and Applied Nutrition, 2001)

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