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Salmonella Food Poisoning Outbreak in Riyadh, Saudi Arabia, 2001

On 21st June, 2001 several patients presented to the Emergency Room of Prince Salman Hospital, Riyadh, Saudi Arabia with symptoms of gastroenteritis. They all gave the history of having eaten food from a restaurant in Oraija Riyadh, the previous night. En response to notification to the health department, the Field Epidemiology Training Program assigned a team to investigate this outbreak, identify its source, assess its extent, and to suggest recommendations to prevent occurrence of similar outbreaks in future.
After initial interviews with the patients and review of hospital records, a case definition was developed. A case associated with the outbreak was defined as any individual who had developed diarrhea (more than three loose motions per (24 hours) along with any of the following symptoms: Abdominal pain, fever or vomiting; within three days of eating at the mentioned restaurant on 20th June, 2001. Hospitals, health centers and private polyclinics geographically related to the restaurant in Central and South-West of Riyadh were searched for cases including 4 government hospitals, two private hospitals and 8 private polyclinics. With the help of this health care record, interview of the cases and the driver of the restaurant; a list of people exposed to the restaurant's food on the stipulated day was prepared. All these patients and unaffected family members were interviewed about the food eaten from the restaurant using a structured questionnaire. The restaurant was also inspected for food hygiene. Routine preparation, source, transport, storage and handling of food was reviewed by interviewing the staff, who were in prison at the time of study. Stool samples of restaurant staff and most of the cases were collected for laboratory investigation.
A total of 147 individuals were interviewed, out of whom 139 (94.5%) were Saudis. 68 (46.3%) of interviewees developed the food poisoning symptoms. Among them, in addition to diarrhea (100%), common manifestations were fever (86.8%), abdominal pain (83.8%), vomiting (70.1%), nausea (61.7%) and chills (58.8%). All the cases recovered completely without any serious complication. The mean age of cases was 18.3 years (±13 years) with a male to female ratio of 1: 0.9. The median incubation period was 8 hours and the epidemic curve suggested a common point source outbreak. Out of 44 stool samples collected from cases, 42 (95 %) grew (Salmonella group D non-typhi). Further subtyping was not possible due to want of technical resources.
Among food and drink items served on June 21, very high attack rates of food poisoning symptoms were found among people who had eaten mayonnaise (98%), chicken, shawarma (97%) and potatoes (96%). However, when compared with people who had not eaten these food items, it was observed that the risk ratio for chicken shawarma was much higher (RR = 15.9, 95% CI= 6.8 — 37.2), as compared to mayonnaise (RR=5.2, 95% Cl =3.4-7.9) and potatoes (RR =5, 95% CI=3.3 — 7.7).
There was no history of recent diarrhea or isolation of salmonella from the food handlers, all of whom possessed a valid health certificate despite presence of multiple infected skin lesions over both hands of the shawarma cook, reflecting poor level of hygiene and personal care. However, the manager, who had also eaten shawarma that day developed food poisoning and had stool samples positive for salmonella. No Salmonella was isolated from any food item present in the restaurant at the time of study.
Review of chicken shawarma preparation procedure at the restaurant showed that chicken was exposed to above freezing temperature for about 9 hours during travel and marinating, followed by exposure to low heat during cooking for up to 10 hours, which support multiplication of salmonella in the meat.
This food borne Salmonella outbreak was most probably caused by chicken shawarma. Chicken was the most likely source of infection, while time-temperature abuse was the most important contributing factor leading to this outbreak.

Editorial note:

Foodborne illnesses are important public health problems worldwide, affecting both developed as well as developing countries,[1] leading to substantial costs in public health terms and serious losses in terms of morbidity and mortality. [1] Salmonella species and Staph. aureus are the most commonly implicated organisms.[2] There has been a marked increase in the overall incidence of salmonellosis being reported worldwide, [1] particularly poultry associated. [3] In the U.S.A. for instance there was a 20% increase in incidence of Salmonellosis during 1999 compared to 1998, reaching up to 17.7 per 100,000 population.' Salmonellosis is commonly manifested by an acute enterocolitis with sudden onset of headache, abdominal pain, diarrhea, and fever. There are many different types of Salmonella, however, most cases are caused by two sereotypes: S. enteritidis and S. typhimurium. Salmonellosis in humans is contracted mainly through ingestion of contaminated food, water, or milk (raw and dry). Foods of animal origin such as poultry, eggs, and beef are the main source. Raw beef, salami and sausages have all been associated with Salmonella outbreaks in the USA. [3]
In 1984, a national policy for reporting, notifying and recording incidents of bacterial food poisoning in the Kingdom of Saudi Arabia was established.[4] Most outbreaks of food poisoning in Saudi Arabia have been attributed to Salmonella species, chicken shawarma sandwiches being repeatedly implicated as vehicle of transmission.[5,6] In a study conducted in the Eastern Province, Salmonella species were identified in 45 (33.6%) out of 134 food poisoning outbreaks occurring between 1991 — 1996. Salmonella organisms were isolated from 12% of shawarma samples.[5]
In this study, the absence of diarrheal illness in food handlers and their negative stool cultures also point to chicken shawarma as the likely source of Salmonella. The recovery of Salmonella from the manager's stool culture was probably due to his eating shawarma rather than an initial Salmonella infection. Clinical as well as laboratory data point to Salmonella group D non-typhi as the most likely causative agent of this outbreak and chicken shawarma as the most probable implicated food item. This is supported by the following epidemiological and laboratory findings; First, the median incubation period of 8 hours, and yielding of the organism from 42 cases out of 44 (95%) are consistent with salmonellosis; Second, a strong significant association of cases with chicken shawarma was demonstrated; and Third, serious time-temperature abuse during transportation and preparation of shawarma.
We suggest conduction of nationwide health education, and training programs that emphasize the importance of proper food handling practices, personal hygiene, and food sanitation.
References:
  1. Gomes T, Montarjemi Y, Miyagawa S. Foodborne Salmonello­sis. Wld Hlth Statist Quart 1997; 50: 81-89.
  2. Mead PS, Slutsker, Dietz V. Food related illness and death in the United States. Emerg infect Dis 1999; 5: 607-625.
  3. CDC. Preliminary • Food Net Data on the incidence of Food-borne illnesses Selected sites, U.S.A 1999. MMWR 2000; 49:10.
  4. Kurdi TS. MOH General Direc­torate of Health Prevention Guide­lines for Gastroenteritis Manage­ment. Environmental Health 1995; 1-14.
  5. Al Turki KA, El-Taper AH, BaBushait SA. Bacterial food poison­ing. Saudi Med J 1998; 19: 581-4.
  6. Jarallah JS, Khoja TA, Izmirly MA. Reports of bacterial food poi­soning in Riyadh region of Saudi Arabia: A one-year retrospective study. Saudi Medical J 1993; 14(1): 46-49.
Table 1: Attack rate by individual food items served at the restaurant during outbreak of food poisoning

Food item

ATE

DIDNOT EAT

RR

95%CI

 

Ill

Total

AR %

Ill

Total

AR %

Chicken shawarma

63

65

96.6

5

82

6.1

15.9

6.8-37.2

Mayonnaise

50

51

98

18

96

18.8

5.2

3.4-7.9

Potato

50

52

96.2

18.1

95

18.9

5

3.3-7.7

Cucumber

41

76

53

27

71

38

1.4

0.9-2.04

Tomato

46

79

59.2

22

68

32.4

1.8

1.2-2.7

Rice

6

79

7.6

62

68

91.2

0.08

0.4-0.18

Broasted chicken

1

5

20

67

142

47.2

0.4

0.07-2.5

Cocktail

0

2

0

68

145

46.9

0

-