Salmonellosis Outbreak among Yadamah Residents, Najran Region, Saudi Arabia, October 2022 ()
1. Introduction
Salmonella is one of the most crucial zoonotic bacteria involved in foodborne diseases related to food production systems [1]. It is a genus of Gram-negative, rod-shaped bacteria which belongs to the Enterobacteriaceae family. There are two species: Salmonella bongori and Salmonella enterica. The global health risk of these species, which are among the most common foodborne pathogens, affects millions of people annually and has the potential to be fatal in the most severe cases [2].
Salmonellosis becomes endemic, leading to high morbidity with various clinical symptoms such as diarrhea, nausea, abdominal cramps, vomiting, and fever [3]. Causing approximately 150 million illnesses and 60,000 deaths globally each year [4].
Food contamination can happen at multiple stages of production, delivery, and consumption, and it can be caused by environmental contamination like water, soil, or air pollution, as well as unsafe food storage and processing [5] [6]. Small foodborne outbreaks are typically characterized by a simultaneous occurrence of acute gastroenteritis among individuals with similar signs and symptoms who consumed a common food or meal [7]. These types of outbreaks can occur in locations where food is provided for people in groups, such as in companies, restaurants, hotels, hostels, hospitals, and others [8]. In the United States (US), according to the US Food and Drug Administration (FDA), the most common pathogens that cause foodborne illness are Escherichia coli, Salmonella, Listeria, norovirus, and hepatitis A virus [9]. Similar pathogens such as Salmonella spp., Shigella spp., Campylobacter jejuni, rotavirus, and hepatitis A virus have been reported to be responsible for most foodborne diseases in the Middle East [10].
In the Kingdom of Saudi Arabia (KSA), a national notifying policy for food poisoning incidents was established in 1984. Since then, food poisoning outbreaks have been reported from different regions of the country, mainly caused by Salmonella spp, exhibiting seasonal and regional variations [11]. Najran is one of the thirteen provinces in southwestern Saudi Arabia near the border with Yemen, with a population of approximately 608,467 [12]. The governorate of Yadamah is 182 kilometers from Najran City, with a population of approximately 16,889.
On Friday, October 7, 2022, the Field Epidemiology Training Program (FETP) knew about the outbreak through communication with the food safety program in the Ministry of Health (MOH) and, therefore, they were assigned to carry out investigations in the area and to participate for training purposes on inappropriate methods of containing and controlling this type of outbreaks. The outbreak started on October 7, 2022. The beginning was with seventeen cases reported by the emergency department of Yadamah Hospital in the early morning. The cases ate from the same restaurant in Yadamah City, which offered several types of fried chicken, shawarma, and pizza. Furthermore, the Najran Public Health team was notified, and the food safety program coordinator went to Yadamah Hospital and recorded 45 cases. On October 8, there were reports of the same common symptoms (fever, diarrhea, abdominal pain, nausea, vomiting, weakness, and headache) among different families. The restaurant was closed on the same day. The number of cases reached 100 by midnight.
On October 8, the FETP team arrived and immediately began preparations for fieldwork by building and communicating with authorized personnel. Administrative preparations such as official letters, logistical preparations such as residence and transportation, and scientific preparations were made by the Saudi FETP and the General Directorate of Health Affairs of Najran region. The FETP team started the field investigations on the same day and lasted for three days. Although the last case was detected at 1:00 AM on October 8, to ensure no more cases, the team needed to wait one maximum incubation period (IP), 72 hours after the suspected restaurant was closed. Then, the foodborne disease outbreak (FBDO) was over within three days, and the team announced its end on October 9, 2022.
A public source caused the current FBDO. Hence, it affected many residents over a broad area and added overwhelming pressure on healthcare facilities and providers in Yadamah City, thus requiring additional resources to investigate and manage the cases. This study aims to assess the severity and extent of the current FBDO, control it, and prevent similar FBDOs in Yadamah City, Najran Province.
2. Methods
Establishment of the field investigation
The investigation team used the international FBDO definition, which states that two or more cases of a similar foodborne illness occur due to the consumption of a common food.
A case-series study design was applied. No controls represented the population at risk, as none of the controls consumed the food items, and all the exposed were ill, which resulted in the unveiled association.
Study population
The investigative team assumed in the beginning that the total population in Yadamah city was at risk of being exposed to the outbreak source and developing foodborne disease (FBD) during October 2022. Subsequently, study population was defined as all cases FBD who were exposed to outbreak source in Yadamah city, October 2022.
Identify and find cases
The cases were identified by passive surveillance through reports by Yadamah Hospital and Najran Health Directorate and by active surveillance through interviews with the cases and asking them if they knew more cases.
The cases were recognized by the previous data that was collected by Public Health team in General Health Directorate of Najran region. Since it was obvious from the beginning of our investigation that we were dealing with FBDO, we developed our case definition as follows: The possible case was defined as any case with gastrointestinal symptoms in Yadamah City in October 2022 to avoid missing cases. The probable case was defined as any case with one or more of the following symptoms: diarrhea, abdominal pain, fever, nausea, vomiting, and exposure to the outbreak source in Yadamah in Najran region, October 2022. The confirmed case was defined as any case with confirmed laboratory results of Salmonella enterica.
Data collection
Data were collected through a questionnaire for FBDO predesigned by the Ministry of Health (Appendix 1), which was filled out by a direct interview with the cases and guardians of the children at Yadamah Hospital. The questionnaire contained four sections that evaluated the socio-demographic and clinical features, consumed food items, and laboratory results. An outbreak was suspected when several individuals were hospitalized with gastrointestinal complaints after consuming food from a particular restaurant on October 6. Clinical history was collected through direct interviews with individuals who were still hospitalized when the outbreak investigation started. Data extracted from the questionnaires to line lists were developed in Excel (Appendix 2). Also, we used Najran health directorate data as they started before the FETP team.
Types of investigation
Three types of investigations (epidemiological, laboratory, and environmental) were conducted. The FETP team investigations also used Najran health directorate data because they started before the FETP team.
Epidemiological investigation
Descriptive epidemiology was intended to generate hypotheses about the determinants (causes, risk factors) of the outbreak by describing the outbreak. Descriptive epidemiology describes the distribution of cases by pattern (time, place, person) and frequency (number, proportion, or percentages). It described the time trend of the outbreak by onset of cases (x-axis) and number of cases (y-axis) and represented it by an epidemic curve. It described the persons (cases) by all the characteristics as in clinical medicine history taking (age, gender, nationality, occupation, address) and the clinical picture based on the case definition. These characteristics were presented in an epidemic table of cases.
Laboratory investigation
Laboratory investigation was conducted to confirm the diagnosis. A Total of 37 samples collected from the patients and food handlers included (stool cultures, blood cultures, and rectal swabs). Other samples were also collected from the food handlers (throat swab, nasal swab, and fingernail swab), which included 6 samples each. The samples isolated from the garlic sauce, Mayonnaise containers, and water used for cooking were also collected.
Samples were also taken from all ingredients involved in food production. Specimens were obtained from at least 10 to 20 individuals (ideally 15% to 20% of all cases) who manifest illnesses typical of the outbreak [8].
Environmental investigation
It was carried out to detect outbreak risk factors, and the team visited the restaurant from which the patients consumed the food to find out any contamination, proliferation, and survival contributing factors. The restaurant was closed with a red sign at that time as a precautionary closure. The team requested the municipality to reopen because it is the authorized member of quartet (MOH, Municipality, Ministry of Interior, Saudi Food and Drug Authority) to remove the red sign and open the restaurant. This is an authorized action to carry out the environmental investigation. The investigation was conducted in the presence of the authorized staff at the site, the restaurant owner, and the food handlers. The food handlers were examined, interviewed and observed on the food production processes, especially on the processes of the most likely involved food items. The team examined the structural and operational hygiene of the implicated restaurant. The sanitary investigation also searched for pests and insects. The team examines the equipment and utensils, including refrigerators, thermometers, blenders, and other items. No leftover food was found. But the team found raw food and how it was stored.
Ethical considerations
No ethical approval is required in case of outbreaks as it is an emergency situation. The research team was careful to ensure justice and fairness in their dealings with all participants in this study. Firstly, it was ensured that all patients involved had equal access to medical care, and there was no discrimination among patients on any grounds (gender, age, nationality, ethnicity, etc.). Secondly, the investigation team gave a truthful declaration of the nature of the disease [13] [14].
3. Results
Descriptive analysis results
Distribution of cases by time
From October 7 to October 8, 2022, 100 cases were reported in Yadamah Hospital. The first exposure duration extended from October 6, 4:00 p.m. to 11:00 p.m., with 90 cases exposed. The last cases were on October 7, 2022, at 12:00 AM, with 10 cases exposed (Figure 1). The time distribution of cases shows that the outbreak started on October 7, 2:00 AM, when the index case started to have symptoms, and the last case was at 11:00 p.m. on the same day.
Most of the probable cases in the study showed symptoms of GIT illness on October 7, 2022 (Figure 2). The mean incubation period (IP) was 17:35 hours, median = 18 hours, mode = 24 hours. The minimum IP was 6 hours, and the maximum IP was 29 hours. The range of IP is 23 hours, and the standard deviation was 6 hours.
Distribution of cases by person
One hundred cases were included in the epidemiologic study. Among them, 58% were males, and 90% were Saudi (Figure 3, Figure 4). Forty-one patients were hospitalized, and there were no deaths. All the patients recovered.
The age of the cases ranged between 1 and 50. The mean age was 16, the median age was 13, and the mode of age was 10. More than half of the cases were between 5 and 19 years old (Figure 5).
Table 1 shows the symptoms. Fever was the most common (n = 99), followed by abdominal pain (n = 98), diarrhea (n = 95), and vomiting (n = 80). None of the cases reported bloody diarrhea.
Figure 1. Epidemic curve of food-borne Salmonella outbreak in Yadamah City, Najran region, Saudi Arabia October 2022, by the time of exposure (n = 100).
Figure 2. Epidemic curve of food-borne Salmonella outbreak in Yadamah City, Najran region, Saudi Arabia October 2022, by the onset of cases (n = 100).
Distribution of cases by place
All cases were from Yadamah city and were recognized in Yadamah hospital.
Laboratory results
A total of 32 rectal swab samples were taken from patients, 8 of which were positive for Salmonella enterica, while blood and stool samples were negative for FBDO
Figure 3. Gander distribution of food-borne Salmonella outbreak in Yadamah City, Najran region, Saudi Arabia October 2022 (n = 100).
Figure 4. Nationality wise distribution of food-borne Salmonella outbreak in Yadama City, Najran region, Saudi Arabia October 2022 (n = 100).
Figure 5. Distribution of cases by age groups of food-borne Salmonella outbreak in Yadamah City, Najran region, Saudi Arabia October 2022 (n = 100).
Table 1. Clinical characteristics among cases, salmonellosis outbreak, Yadama, Najran region, October 2022.
Signs & symptoms |
No. of cases (N = 100) |
proportion |
Diarrhea |
95 |
95% |
Vomiting |
80 |
80% |
Fever |
99 |
99% |
Abdominal pain |
98 |
98% |
Headache |
50 |
50% |
Nausea |
73 |
73% |
Weakness |
30 |
30% |
microbes. Five stool samples were taken from the food handlers, and one sample was positive. No organisms were detected in food and water samples.
Environmental investigation results
The food preparation room, floor, containers, and tables were clean. The storage refrigerator and freezer were working fine and within the range of the supposed degree of cooling. The ventilation window of the preparation room was not protected from insects by protective barrier mesh. The expiry dates of raw food items were valid. Five food handlers worked at the restaurant. The food handler with a positive result who was in direct contact with prepared chicken for shawarma could not provide the correct steps of thawing and handwashing in front of the investigation team.
4. Discussion
The outbreak of food poisoning among the residents of Yadamah was caused by S. enterica. This was consistent with the symptoms and incubation period reported and was further confirmed by the laboratory results from samples of cases. There were no deaths, but there were 41 admissions due to the outbreak, reflecting the severity of the disease. In the first epi curve, which represents the time of case exposure, the number of cases exposed continues from 4:00 pm, October 6 until 12 AM, October 7. The case’s exposure discontinued after 12 A.M, October 7, since the restaurant was open only in the evening period and the restaurant was closed by the municipality on the same day (Figure 1).
The epi curve constructed based on symptom onsets showed that, the illness onset was on October 7th, 2:00 A.M. The number of cases increased gradually, steeply, and decreased gradually to the end of day at 11 P.M. The incubation period ranged between 6 and 29 hrs. The minimum IP proved that the FBDO was caused by infections, not by toxins. That could have led the team to think of non-typhoid Salmonella serotypes and Shigella. However, as the minimum IP of Shigella is 24 hours, it was excluded from differential diagnoses. The approximate time to onset of symptoms of non-typhoid Salmonella serotypes IPs ranged from 6 - 96 hours (usually 1 - 3 days). That referred to a non-typhoid Salmonella serotype as the causative agent with high probability. Fever was the most common symptom, followed by abdominal cramps, diarrhea, vomiting, and headache [15].
The most common causative organism at the outbreak in Saudi Arabia was Salmonella species [16]. All the cases were linked to the same food source; no geographical risk factors could have resulted in the FBDO other than the suspected restaurant. That was, the restaurant was the only link between nonrelative patients. It referred to the fact that the restaurant was well known in Yadamah and that was the first time it had been a source of FBDO. That means there were some gaps in the food preparation process.
Nine clinical samples from ill individuals were positive for Salmonella enterica serotype Enteritidis, confirming the outbreak with salmonellosis of a food-borne nature. There are several explanations of the negative results from food handlers and food items samples:
1) Specimens may have been mishandled during collection, storage or transport.
2) Specimens may have been mishandled during processing.
3) Specimens may have been collected too late in the course of the patients’ illnesses.
4) The illness may be due to some agent not tested for by the laboratory.
5) The food handler may not be carrying out the test correctly [15].
Regarding environmental investigation, the key role played by food handlers in ensuring food safety and preventing the transmission of foodborne infections has been well established, as pathogens can enter foods if the correct procedures for producing, processing, and distributing foods are not strictly adhered to. One of the food handlers involved in preparing the shawarma and serving it to customers reported positive for Salmonella enterica. That was a strong contaminating factor. Although no Salmonella was isolated from food, this might have been due to reasons mentioned in laboratory investigation above. Food safety and hygiene awareness among restaurant employees should be promoted by means of compulsory attendance at education sessions and hands-on training.
5. Conclusion
This study highlights the processes undertaken to identify cases and causative pathogens of foodborne outbreaks. The results of the investigations and discussions indicated that the outbreak was a foodborne salmonellosis outbreak. Early implementation of control measures played a critical role in controlling the outbreak, as well as preventing future FBDOs.
Limitations
Delayed environmental sample collection by authorized personnel, which timing might have affected the test result and affected the support of the hypothesis, could be due to the restaurant being closed for days.
Recommendations
Restaurants must fully observe all practices prescribed by local authorities in the preparation of sauces and other foods.
Food safety and hygiene awareness among restaurant employees should be promoted by means of compulsory attendance at education sessions and hands-on training.
Frequent random visits by the food safety authority are critical to prevent similar outbreaks.
Acknowledgements
The authors would like to thank the General Directorate of Health Affairs in Najran and the health staff in Yadamah hospital and the Eastern Mediterranean Public Health Network (EMPHNET) for their invaluable support in the development of this project and manuscript.
Appendices
Appendix 1. MOH Questionnaire of FBDO Form in English and Arabic
Appendix 2. Line List of the Case