Outbreak of acute gastroenteritis in an air force base in Western Greece

Foodborne diseases are considered a major public health problem because they affect individuals of all ages and socioeconomic status [1]. Despite the use of HACCP programming and hygiene code to ensure the safe preparation of food, many outbreaks of gastroenteritis have been reported, caused by ingestion of pathogens or their toxins in contaminated food ingredients [2–4].

Numerous studies published recently, indicate that most outbreaks of acute gastroenteritis occur in places of mass feeding such as institutions, schools, restaurants and military units [3–8]. The Communicable Disease Surveillance Centre (CDSC) in England and Wales has operated a system of surveillance for general and foodborne outbreaks, according to which the most frequent aetiological agents are viruses (Rotaviruses, Noroviruses), Salmonella species, Clostridium perfringens, Escherichia coli strains, Campylobacter jejuni, Listeria, Yersinia as well as toxins of Staphylococcus aureus and Bacillus cereus [9–15]. Furthermore, 2004 data obtained from Centers for Disease Control and Prevention (CDC) in USA indicate declines in the incidence of foodborne infections caused by Campylobacter, Cryptosporidium, Shiga-toxin producing E. coli (STEC) O157, Listeria, Salmonella and Yersinia. As for the suspected food vehicles, these are usually dairy products, meat-based dishes, sauces and seafood [13–15].

In Greece, recording of outbreaks of foodborne gastroenteritis is limited and there is a considerable lack of recorded epidemiological data. Most cases are not reported, resulting in inadequate monitoring and evaluation of outbreak trends, based on aetiological agents, food vehicles and venues. Thus, prevention and control measures for food safety are difficult to establish.

The present study focused on a reported outbreak of gastroenteritis in an Air Force base in Western Greece, where during an operative training day, soldiers and staff experienced an outbreak of acute gastroenteritis. Following the assessment of descriptive epidemiology, we performed a case-control analytic approach. Using project-designed standardized questionnaires the main objective of the study was to determine the vehicle of the contamination. Furthermore, forced by a public health perspective and taking into account the possible malpractice of employees, we tried to develop control measures in order to prevent future contamination and underline the importance of adherence to high quality hygiene standards for food preparation.

The overall estimated attack rate was at least 60% among the approximately 1050 attendees. The outbreak started abruptly in the late afternoon on 20 September, peaked at midnight and ended about 25 hours later, as demonstrated by the epidemic curve (Figure 1). From the interviews and analysis thereof, it was established that lunch (beef, macaroni, tomato sauce and grated cheese) consumed several hours prior to the onset of the symptoms, was the likely source of the outbreak. The overall odds ratio of gastroenteritis among those who had lunch was 370 (95% CI: 48–7700) as compared to those who didn't eat lunch. Table 1 lists the odds ratio of lunch and dinner consumption.

The incubation time ranged from 3.5 to 19 h (mean 9 h) (Figure 2). The median duration of the gastrointestinal symptoms was 21 h, ranging from 3 to 141 h (Figure 3).

The results of the microbiological analyses showed that only S. aureus was detected in the sample of raw beef (2,000 cfu per g) and in the two samples of grated cheese. In total 7,800 cfu per g were detected in sample "c" (opened bag containing the rest of cheese that had been served to the subjects during lunch) and 3,000 cfu per g in sample "d" (unopened package purchased from the market).

All food samples cultured were negative for the presence of E. coli, Salmonella spp. and Colstridium spp. and HPC ranged in low levels, between 40 cfu and 1500 cfu per g. The analysis of water samples showed negative results for the parameters tested, indicating that the suspected vehicle of the pathogen was among the food items served to the subjects.

The outbreak of acute gastroenteritis, reported on 20 September 2005 on the Air Force base in Western Greece, was originally presumed to be caused by an enterotoxin-producing bacterium. This speculation was based on the short incubation period with abrupt onset, the symptomatology and the short, self-limiting nature of the illness. S. aureus was considered to be the most likely cause. Although mortality and longer-term morbidity are uncommon with food poisoning caused by enterotoxin-producing bacteria [18], this outbreak highlights its capacity to cause short term, moderately severe illness in a young and healthy population.

In the present study our main concern was to determine the food vehicle of this reported foddborne gastroenteritis. For this purpose suspected food items were collected and examined. By that procedure we identified the aetiological agent and proceeded with the isolation and withdraw of the contaminated food item. Nevertheless, a limitation of this investigation was the fact that stool samples were not obtained for microbiological diagnosis. The reasons for this omission include the short duration of the symptoms and the overall lack of coordination in the military base, although they are important in suspected foodborne outbreaks, as reported [18]. The data collected from the questionnaires and microbiological analyses lead to the conclusion that S. aureus, detected in the cheese was the main aetiological agent of the reported outbreak. As far as the possible cause of the contamination is concerned, the most likely scenario is that the food-handler who packaged grated cheese into the bags in the market was the source, because the pathogen was detected in packaged cheese purchased directly from the market. S. aureus colonies were also detected in the beef sample, but that was probably due to cross-contamination from the cheese during lunch preparation.

According to epidemiological studies, a wide range of foods are sources of staphylococci food poisoning, resulting from enterotoxins produced primarily by S. aureus [19–21]. Focusing on dairy products, many studies state their association with S. aureus which survives well in cheese during production and handling processes [1, 16, 23, 24]. In general, high salt foods like cheese favour the growth of S. aureus over other bacteria [18]. The variety of toxins produced by S. aureus causes a wide array of disease symptoms, ranking staphylococcal enterotoxins as one of the most common causes of reported food-borne illnesses [16, 19, 21]. Staphylococcal food poisoning is a persistent cause of gastroenteritis worldwide, especially because Staphylococcal toxin is heat-stable and not destroyed by cooking.

In developed countries S. aureus may be more costly to treat than many other food-associated pathogens [21]. The chemical parameters of cheese together with poor hygienic quality favour S. aureus proliferation and contamination [23]. These data indicate the necessity of high quality hygienic conditions during manufacturing, storage and marketing. Another critical but often-unrecognised food safety factor is the temperature at which potentially hazardous foods are received [2].

On the other hand, S. aureus is an indicator of post process contamination by food handlers, which most likely occurred in our case. Humans are the main reservoir for staphylococci. Hands and the mucous membranes of the nasopharynx are predominant sites of colonization. High rates of carriage and large cells numbers are two major factors that explain the important role of food workers in the epidemiology of staphylococcal food poisoning outbreaks [20]. The majority of the staphylococci inhabiting the nasal fossae of food handlers belong to the species of S. epidermidis and S. aureus [25].

Reducing the number of foodborne outbreaks will require continued and coordinated efforts by many different agencies, including those of disease surveillance, consumer education and food handling, processing and marketing [26]. To begin with, certain measures should be implemented to correct the faulty food preparation and handling practices. This investigation highlights the importance and severity under which a hazard analysis critical control point (HACCP) system should be applied in all kinds of commercial food services followed by employee adherence. The HACCP system is a systematic approach to the identification, assessment and control of hazards that has been widely accepted as an effective means of ensuring food safety throughout the whole food chain and is compulsory in the European Union [20].

In Greece supervision authorities regarding foodservices are not fully developed and there is a considerable lack of epidemiological evidence, resulting in an unsatisfactory insight in the incident and pathogens of gastroenteritis caused by contaminated food. Thus, limited collected data of outbreaks do not allow the evaluation of outbreak trends and the proper surveillance by the Greek food-hygiene system.

Information obtained from the questionnaires with the results of microbiological analysis of food items led to the conclusion that the aetiological agent of this outbreak was S. aureus. The pathogen was detected and isolated from grated cheese, which served as food vehicle of transmission.

This outbreak highlights the capacity of enterotoxin-producing bacteria to cause short term, moderately-severe illness in a young and healthy population. Foodborne outbreaks like this one recorded in the present investigation should be reported to the associated authorities in order to accomplish appropriate monitoring in time. Thus, food-hygiene services could improve the surveillance of outbreaks, particularly those occurring in institutions or affecting the community at large and protect public health.