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Food Borne Outbreak in Al-Hofuf, Saudi Arabia, June 2009.

On Tuesday 2/06/2009, an increased number of cases with food poisoning symptoms presented to the emergency department of King Fahad hospital in Al-Hofuf city, arriving after 10 pm and throughout the following two days. Two other hospitals (Al-Manaa, and Al-Hofuf maternity and pediatric hospitals) reported some cases at the same time. All were complaining of gastroenteritis symptoms including diarrhea, vomiting, abdominal pain, nausea and/or fever. All gave a history of eating a meal on the evening of Tuesday 2/06/2009 from one particular restaurant. The authorities closed the restaurant on Thursday 4/06/2009 and samples of the food leftovers were sent to the laboratory. The total number of cases was 50. A team from the Field Epidemiology Training Program investigated this outbreak.
The investigative team reviewed the case reports and available data in coordination with the Alahsa Directorate of health affairs. The team also reviewed the medical records of the three hospitals. A case-control study was conducted to identify factors responsible for the outbreak. A case was defined as any person who ate from the specified restaurant on the 2nd or 3rd of June 2009, and developed any gastrointestinal tract symptoms (diarrhea, vomiting, abdominal pain and fever) during the period of the outbreak. A control was defined as any person who ate from the same restaurant on the same dates and had not developed any symptoms.
We were able to trace and interview all the 50 cases. Another 50 individuals who had eaten food from the same restaurant and had not developed symptoms were selected as controls.
The outbreak occurred between Tuesday 2nd of June to Wednesday3rd of June, 2009. The time lapse between food consumption and appearance of symptoms ranged between 4.5 and 23 hours (median 10.5 hours). The mean time from eating the meal till appearance of symptoms was 11.82 hours. The epidemic curve is suggestive of a common point source outbreak. (Figure1).
Symptoms of the 50 cases were diarrhea 47 (94%), abdominal pain 38 (76%), fever 35 (70%), vomiting 31 (62%), nausea 15 (30%), and headache 17 (34%).
Among the cases, 31 were males (62%) and 19 were females (38%) with a male to female ratio of 1:1.63. Their ages ranged between 6 – 48 years (median 21 years). The majority of the cases were Saudis (98%).
Among the food items, there was a strong association of food poisoning with eating foods that contained mixed sauce (Odds Ratio (OR) = 44.59; 95% Confidence Interval (CI) = 11.82-168.1) and plate chicken shawarma (OR= 3.88; 95% Confidence Interval CI= 1.43-10.73). Other food items showed no association with food poisoning.
Salmonella enteritidis was isolated from 28 patients; 18 (36%) from stool culture, and 10 (20%) from rectal swabs. It was also isolated from the remnants of the mixed sauce. Stool cultures from the food handlers were negative.
The restaurant was small, with a total area of 56 m2. It was divided into two main sections, one for the cashier and dining area and the other for refrigerators and food preparation. The restaurant owner claimed that they purchased all of their supplies from nearby stores.
Inspection of the food preparation area showed that frozen chicken were thawed in a plastic tub, that was connected to the water supply system with a separate drainage tube connected to the restaurant drainage system. Another smaller plastic tub was found in a bathroom at the back of the restaurant. This bathroom was very dirty and there was a floating sewage closeby. There were four refrigerators, two of which were not clean and contained remnants of old vegetables and meats. The dining hall of the restaurant was clean, and the coolers were clean and working well.
Food handlers interviewed stated that they usually prepared about 1000-1500 different sandwiches daily. Preparation of chicken for shawarma usually started at 1:00 pm daily. Frozen chicken is thawed in the thawing tub until 3:00 pm, after which it is boiled for 20 minutes, then cut into small pieces, placed in several large plates and kept in the cooler in the dining hall in preparation for cooking in different amounts at separate times, according to clients’ demand. Meals are served from 4:00 pm until 1:00 am. The restaurant also supplies some colleges and schools with meals in the morning. These meals are prepared at night and reheated in the morning before delivery to the schools.
The mixed sauce is prepared daily at 1:00 pm by blending egg yolks, vegetable oil, cheese, salt, and vinegar in an electric mixer for about 10 minutes. After that it is placed in large plastic containers and kept in the fridge. It is taken out of the fridge at 4:00 pm and added to the sandwiches according to clients’ demand. The leftover of the mixed sauce may be used the next day.
Regarding the food handlers’ hygiene, their clothing was satisfactory, and their nails were short and clean.

Editorial note:

A food borne disease outbreak is the occurrence of two or more cases of a similar illness resulting

from the ingestion of a common food.1,2 It is obvious that Salmonella entiritidis was the cause of this outbreak, which is supported by the relatively short incubation period and isolation of the organism from patients.1
In Saudi Arabia, the total number of reported food poisoning outbreaks during the period from 1416 through 1425H was 3,877, with a total number of 26,707cases. Salmonella spp. was responsible for about 41.4% of these outbreaks.3 The main source of Salmonella infection is the chicken meat and eggs. Local studies have reported a large number of Salmonellosis outbreaks due to chicken shawarma, which has a great potential for food poisoning, since the meat is cooked very slowly by direct heat from a distance, which does not raise the meats’ temperature to an extent that can kill the bacteria. Inadequate storage, cross contamination and use of raw ingredients may be additional risk factors in these outbreaks.4
This food poisoning outbreak occurred in the early months of summer, as observed in the majority of other food poisoning outbreaks in the Kingdom. Over the years, a seasonal variation has been observed, with the peak occurring during the hot summer months of June to August.5 This period coincides with the summer holidays; during which families spend a substantial amount of time outside their homes and obtaining food from restaurants or other food outlets. The high temperature facilitates growth, multiplication and toxin production of microorganisms in the absence of hygienic practices.6
The mixed sauce and the chicken shawarma were the food items which could have been the source of this outbreak. One of the main ingredients of the mixed sauce was fresh eggs, a well known source of salmonella. The mixed sauce was kept at room temperature until serving which facilitated organism growth. However, eggs were not part of the chicken shawarma, which raises suspicion to the role of cross-contamination during the food preparation process. Unhygienic conditions at the restaurant and food preparation mechanisms clearly indicate a high risk environment for food poisoning.
It was recommended that raw food products be kept immediately after purchasing in clean refrigerators. Eggs, raw meat and chicken should not be kept over three hours outside the refrigerator before cooking.

1. Chin J. Control of Communicable Diseases Manual. 17th ed. Washington (DC): American Public Health Association; 2000. p.202-212,440.

2. Ayaz M, Nabutt NH. The toxic types of bacterial food poisoning. Saudi Med J 1984; (5):171.

3. Kurdi TS. Epidemiology of the food poisoning outbreaks in KSA during 1416-1425H. In: The HACCP, Food Safety and Hazards Analysis Critical Control Point System, Ed. 1, 2005:p211.

4.Center for Disease Control and Prevention/ National Center for Infectious Diseases/ Division of Bacterial and Mycotic Disease. Salmonella Enteritidis Infection, October 13, 2005.

5.Ministry of Health. Food Poisoning Accidents during the years 1421-1422. Annual Report. Riyadh (KSA): Food Poisoning Department, Ministry of Health; 2002.

6.Kurdi TS, Kamball AM, Muhammad MHA, Al-Zahrani MA. Manuals for worker for food poisoning accidents. Riyadh (KSA): Ministry of Health; 1998. p. 1-27.

فاشية تسمم غذائي، الهفوف، 1430 هـ (2009 م).

يصنف مرض التسمم الغذائي الذي تسببه بكتيريا السلمونيلا ضمن الأمراض التي تنتقل عن طريق الطعام الملوث. و ينتقل المرض غالبا من مصدر حيواني، مثل الدجاج والبيض النئ ومنتجات الألبان، أو عن طريق تداول الطعام بواسطة شخص مريض أو حامل للمرض.

في يوم الثلاثاء 9/6/1430هـ بدأت تصل إلى مكتب الطب الوقائي بالإحساء عدة بلاغات حول حالات تسمم غدائي من قبل عدة مستشفيات في مدينة الهفوف، حيث تم التبليغ عن إصابة (50) شخصاً أثر تناولهم الطعام من احد المطاعم المعروفة في مدينة الهفوف. وقد قامت بلدية الأحساء بإغلاق المطعم في يوم الخميس 11/6/1430هـ. تم تكليف فريق من برنامج الوبائيات الحقلي لعمل دراسة استقصائية عن أسباب ظهور الفاشية. قام فريق الدراسة بزيارة موقع المطعم ومقابلة بعض المرضى المنومون في المستشفيات والاطلاع على سجلاتهم ونتائجهم المخبرية، ومن ثم تم عمل دراسة ضابطة لتحديد حجم التسمم الغذائي و التعريف بمصدر العدوى كي يتم وضع التوصيات الوقائية المناسبة لتلافي حدوث مثل هذا التسمم الغذائي مستقبلا.

تم الوصول إلى (100) شخص بين أصحاء ومرضى و الحصول على المعلومات عن طريق المقابلة الشخصية او الهاتفية. تمت معاينة المطعم و أخذ مسحات (أنفية – حلقيه ـ شرجية ـ أظافر) من كل عامل بالمطعم. كما تم أخذ عينات من بقايا الطعام وإرسالها إلى المختبر. و قد أخذت عينات براز من المرضى بالمستشفيات.

أظهرت الدراسة الضابطة أن الخلطة التي كان يعدها المطعم محلياً ثم يقوم بإضافتها إلى أصناف الطعام الأخرى بالإضافة إلى شاورما الدجاج على الصاج أكثر الأصناف ارتباطا بحدوث المرض ( معامل خطورة 44.59 و 3.88 على التوالي). وكذلك أظهرت النتائج المخبريه عزل ميكروب السالمونيلا (D) من العينة التي أخذت من بقايا الخلطة التي كان يعدها المطعم، إضافة إلى عزل ميكروب السالمونيلا (D) من بعض عينات البراز التي أخذت من المرضى.

أظهر الاستقصاء الوبائي الوصفي أن العامل المسبب في وقوع هذه الفاشية من المحتمل أن يكون متماشياً مع الإصابة بداء السالمونيلا وقد تأكد ذلك بعد أن تم عزلها من المصابين و بقايا الطعام. وقد أظهرت الدراسة الضابطة أن الخلطة المحلية الصنع

والشاورما على الصاج كانتا مرتبطتا بوقوع الفاشية.

تمت التوصية علي التأكيد على تطبيق الأنظمة التي تمنع إعداد المايونيز داخل المطاعم و الإكتفاء بشرائه معلباً و جاهزاً، ومراقبة من يعده محلياً. التشديد على حفظ الأطعمة بعد شرائها مباشرة في ثلاجات نظيفة داخل المطعم، و تجنب إخراج البيض و اللحوم و الدجاج من الثلاجات قبل استخدامها لمدة تزيد على ثلاث ساعات.