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Salmonella in Imported Beef in French Food Poisoning Outbreak

03 December 2012

An outbreak of Salmonella at a school in Poitier, France was caused by contaminated imported beef burgers, according to a Eurodurveillance report carried out by the food safety agencies and health offices in France.

The outbreak of monophasic Salmonella Typhimurium 4,5,12:i:- was identified through the national disease notification system for food-borne illness.

Investigation by the Food Control Unit quickly identified the cause of the outbreak as beef burgers and all batches of the same date than the incriminated batch were rapidly withdrawn.

The impact of the consumption of the incriminated beef burgers was unknown at the time of outbreak notification as it occurred during school vacation.

The retrospective epidemiological investigation conducted in the four affected schools of Poitiers enabled us to identify 554 clinical cases among the 1,559 study participants who ate at school on the days the incriminated beef burgers were served. Twenty-one cases who participated in the study were biologically confirmed by the NRC by serotyping.

This multi-school outbreak is one of the biggest food-borne outbreaks due to monophasic Salmonella Typhimurium 4,5,12:i:- described in France, according to the research team of M E Raguenaud, S Le Hello, S Salah, F X Weill, A Brisabois, G Delmas and P Germonneau.

A previously described large outbreak of Salmonella enterica serotype 4,[5],12:i:- in France involved 337 identified cases and occurred nationwide between 31 October and 18 December 2011. Another nationwide epidemic involving the same Salmonella strain occurred in France between 1 August and 9 October 2011 with 682 cases reported.

In these two outbreaks, the investigations indicated dried pork sausage as being the most likely source of the outbreaks. The Poitiers school outbreak is the first large scale outbreak described in France of monophasic Salmonella enterica variants involving beef.

The overall attack rate of the Poitiers outbreak was higher than the average attack rate (seven per cent) observed in Salmonella food-borne outbreaks that occurred in school canteens in 2006–2008 in France. In the same period, no large-scale Salmonella outbreak was described in a school setting. The largest food outbreak described in schools in France occurred in 2008 and involved 1,137 identified cases with a global attack rate of 50 per cent and was of viral origin.

Although the Poitiers outbreak occurred two months before the annual winter peak of viral gastroenteritis, the researchers said they could not exclude that some of the cases identified in the survey were due to other gastrointestinal disease. The high attack rate observed in this outbreak could be explained by a particularly high initial concentration of bacterial inoculum. A meta-analysis by Teunis et al. [15] on food-borne outbreak data showed median infective dose (ID50) values ranging between 30 and 50 CFU/g for Salmonella.

The survey revealed an attack rate twice as high among adolescents as among adults. Moreover, the attack rate decreased with increasing age among adolescents. There are no obvious explanations for this finding other than the possibility that the younger students were served lunch at a different time than the others and thereby ate beef with a potentially different cooking time.

The outbreak showed signs of severity with about half of the cases, who sought medical care in a private practice or an emergency service, of which 31 of 554 (six per cent) were hospitalised for more than 24 hours.

Incubation for Salmonella infection is known to range from six to 72 hours with longer incubations (up to 16 days) documented. Two students with a positive stool culture and an incubation of nine and 10 days could be secondary cases contaminated by person-to-person spread.

The researchers observed that median incubation was shortest in the school with the highest attack rate (School B). Such negative correlation between attack rate and incubation has been documented in previous outbreaks and retrospective analysis of human outbreaks. This highlights the possibility that the infective dose was greater in beef burgers served in School B than in other schools, in particular School C.

Moreover, hospitalisation rate used as a proxy measure for disease severity in this context was 2.6 times greater among cases attending School B than among those attending School C. However, the possibility that frozen beef burgers were contaminated at different concentrations is unlikely because beef burgers supplied to schools were all from the same batch. One hypothesis for different attack rates observed between schools relates to different cooking practices.

Although the number of cases identified by the investigation is probably close to the real number of cases of salmonellosis due to ingestion of contaminated beef burgers, the number could be underestimated because of non exhaustive study participation (response rate 78 per cent), because of our assumption that all those who ate at the school consumed the beef, and because of errors in reporting disease onset for persons with clinical symptoms. Inversely, important local media attention before the conduct of the investigation could have induced a high participation rate of the ill student group and an over declaration of symptoms due to psychogenic-like effect. The two-week delay between the first cases and the questionnaire survey (due to school vacation) could have led to recall bias and errors, especially in date reporting. The risk of error for exposure was minimised by asking students about the date they ate lunch at school instead of asking them the specific food items they had eaten.

At the country’s departmental level, two other localised outbreaks of monophasic Salmonella Typhimurium 4,5,12:i:- occurred in October 2010, one in a retirement institution and another in a recreation centre associated with the consumption of beef burgers from the incriminated batch (18 cases, unpublished data).

Interviewing at each of the eighteen other institutions in the department that received frozen beef burgers with the same production date as the incriminated batch revealed that none was aware of cases of diarrhoea within their institution (as of 9 November 2010). Although distribution of potentially contaminated frozen beef burgers was widespread in France, no increase in food-borne outbreaks was detected through disease notification surveillance and no local increase in the serotype 4,5,12:i:- was detected by the NRC (as of 9 November 2010).

The international dimension of this outbreak in France is demonstrated by the fact that the beef was produced in an establishment in another EU Member State. The Rapid Alert System for Food and Feed (RASSF) was used to inform authorities of the manufacturer country and other EU countries likely to receive the products.

Only a French distributor received all the batches from this Member State manufacturer and sold them. Furthermore, no food-borne outbreaks caused by the monophasic Salmonella Typhimurium 4,5,12:i:- were reported in Europe at the time of the outbreak in Poitiers.

Monophasic Salmonella Typhimurium 4,5,12:i:- was associated with a severe outbreak, the largest Salmonella food-borne outbreak described in a school setting in France in recent years. Quick identification and withdrawal of incriminated food batch and respect of safe cooking practices for beef burgers were likely crucial to limit extension of outbreak. Informing other European countries was necessary as the incriminated beef was an imported food product.

Further Reading

You can view the full report by clicking here.
November 2012

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