Salmonella poisoning and chicken shawarmas, Western Riyadh, June 1997

On the morning of June 23, 1997, 36 patients from five different families sought emergency treatment at Prince Salman Hospital in Riyadh for abdominal cramps, diarrhea, fever or vomiting. All patients reported eating food purchased the previous evening from a small restaurant. The restaurant sold only shawarmas and hamburgers. An epidemiological investigation was initiated to determine both the magnitude of the outbreak and the food responsible.

A case was defined as any ill person who ate food from the restaurant and presented to any medical facility in Riyadh with loose stools (>3 times/ 24 hours) between June 22 and 25. A questionnaire was constructed and given to all persons in households with one or more cases. Hospitalized patients and family contacts were interviewed directly, and outpatients and family contacts by telephone.

We identified 142 cases. The median age of case-persons was 13 (range 1-61 years), both sexes were equally affected and 93% were Saudi nationals. Of the cases, 35% were admitted to four hospitals; the average hospitalization was 4.7 days (range 39). Salmonella (Group D) was isolated from rectal swabs of 82% of the case-persons. Most (98%) case-persons were seen at least once in a health institution and 96% (89 persons) received treatment with an antispasmodic, an anti-emetic and/or antibiotics. Onset of illness occurred over a 42-hour period after the food from the restaurant was eaten; the median incubation period was 9-12 hours (range 3-42 hours). All persons interviewed reported buying their food throughout the serving time for shawarmas (1600-2230) on June 22.

We interviewed and obtained full food histories for all persons in 22 family groups with one or more cases. These included 80 case-patients and 14 family contacts who also ate food from the restaurant on June 22 but did not become sick, giving an attack rate (AR) of 85% for eating from the restaurant on June 22. The AR for eating shawarma was 88%, compared with 0% for persons who did not eat a shawarma (Table 1). The AR for eating only hamburger was 0%, and the AR for eating both hamburger and shawarmas was 50%. Both hamburgers and shawarmas contained mayonnaise from conunon containers in the kitchen. No specific ingredient of the shawarma was alone associated with an excess risk of illness.

The restaurant made 154 to 184 shawarmas per day. Answers to the questionnaire indicated that each person ate an average of 1.0 (range=0.2-2.0) shawarma. Using the 88% AR, the estimate of total illness that developed during this outbreak ranged from 135 to 162.

On June 23, an intact chicken shawarma that had been purchased on June 22 and kept in a plastic bag inside one family's refrigerator was recovered: From it, the Riyadh Public Health Laboratory isolated Salmonella (group D), Escherichia colt and Vibrio cholerae non-01.

Food handlers reported that 22-23 frozen chickens were purchased daily. The chickens were left in a large con-tamer of tap water for three hours to thaw. They were then skimmed, cut, deboned and immersed all together in a marinade of garlic, spices and yogurt. This preparation process, beginning with the frozen chickens, required seven hours at room temperature. The chicken marinade mixture was put in a single large container in the refrigerator for 24 hours. The following day the chicken was built on the spit just before grilling. Grilling began at 1600 and ended at about 2230, when all the chicken from the spit had been consumed.

Three cooks prepared the hamburgers and the chicken sandwiches. None was sick. All were screened for asymptomatic carriage of pathogens (stool culture and rectal, nose and throat swabs), but no pathogens were recovered. The restaurant could not be inspected because the police closed it when the cases were first reported.

Both the epidemiology and the microbiologic evidence indicate that chicken shawarma sandwiches were responsible for this explosive outbreak of salmonellosis. Although the shawarmas also contained mayonnaise, salad, pickles and fried potato, the investigation indicates that infection and illness resulted from the chicken. Mayonnaise is made of raw eggs, which, like chicken, may be naturally infected with Salmonella. A recent outbreak in Abha was traced to mayonnaise. In the current outbreak, the same mayonnaise and salad were also used on hamburgers but did not cause illness. Furthermore, salad is unlikely as a source of the infection as it is not a good media for growth of Salmonella. Pickles and fried potatoes were only in the shawarma; however, Salmonella would not survive the pickling process or the frying (immersed in hot oil >100°C).

The high attack rates and short incubation point to heavy contamination of the implicated food. Only the chicken was exposed to ambient temperature (35-40°C) for sufficient time (seven hours) that would lead to heavy microbial growth. The correct preparation is to thaw chickens in the refrigerator at 4°C and immediately after deboning place the chicken back in the refrigerator and keep the marinade in the refrigerator. Refrigeration after marinating was also incorrect, since meat from 22 chickens placed in one container would require hours to reach refrigerator temperature. Warm foods must be refrigerated in small containers for rapid cooling.

Only the surface of the meat on a shawarma spit reaches temperatures sufficient to kill Salmonella. Salmonella could survive if the mass of meat extended above or below the heat source, if juices from the interior of the meat ran out onto the cooked meat, or if meat was cut too deeply from the cooked surface. Since the interior of the meat on the shawarma spit remained uncooked for several hours, Salmonella could continue to multiply during the grilling process.

During 1997 the Riyadh region received 38 reports of food poisoning, of which 10 were attributed to chicken shawarmas. Many more sporadic cases and unrecognized outbreaks may be occurring. Unsafe preparation and cooking of chicken shawarmas may be very common in Saudi Arabia. Accordingly, a safe method of preparation needs to be identified and instituted in all restaurants that prepare shawarmas.