Sixteen culture confirmed cases of enteric infection with Salmonella enterica serotype Oranienburg were detected between August 10 and September 29 1999 in Tyrol (Austria). Ten of them suffered bloody diarrhoea and six were asymptomatic carriers. Interviews with 11 of the 16 cases linked the outbreak to an alpine farm and to eating locally produced cow milk cheese. Environmental sampling in faecal specimens collected from the chicken coop at the farm identified S. Oranienburg. Chickens had roamed near the cheese producing area and had access to it.

Before 1999 only isolated cases of Salmonella enterica serotype Oranienburg were confirmed in the province of Tyrol. In 1996 and 1997 two human cases infected with S. Oranienburg were documented; in 1998 only one. In 1999, however, S. Oranienburg was documented as an initial isolate in 18 cases. This paper presents the results of the epidemiological investigation of this outbreak.

From 10 August to 29 September 1999, 17 initial isolates of S. Oranienburg were cultured from human stool specimens; two of the initial isolates, found during official source screening, were from the same person (a mistake in spelling the surname).

The only isolate of S. Oranienburg found in 1999 unconnected to this outbreak was from a stool specimen taken from a 16 month old girl in the district of Kitzbuehel on 21 October. The girl was treated in hospital for diarrhoea. The consumption of milk products from her Turkish homeland was postulated as a possible risk factor, but to our knowledge such products are not known to be contaminated with S. Oranienburg.

Ten of the 16 people infected in the outbreak (4 male, 6 female) had diarrhoea, six were asymptomatic (four relations of the patients sent in stool specimens through their general practitioners; in two cases stool specimens were obtained through the local district authorities during compulsory source screening). The mean age of infected people was 34 years (range: 11-70; median: 34). Nine of the 16 cases (56%) were female.

Figure 1 shows the time course of the outbreak, by date of receipt of positive stool specimens. Onset of illness was known was known for only six cases; an average of 16 days passed between onset of sickness and receipt of specimen (range: 5-32; median: 10.5).

In the alpine dairy farm cow’s milk cheese was made daily using milk from cows that spend the summer months at the Alpe Lorain. The morning milk was used immediately and the evening milk was cooled overnight to be processed the next morning with the fresh morning milk. Four people worked in cheese production. The cultures were added to unrefined milk for 40 minutes at about 32°C, and then heated to 46°- 48°C. The cheese was put in a cold cellar for five to six weeks to ripen at about 8°C. The floor of this cellar was flushed daily with hot water to increase the humidity. The matured cheese was sold there, as whole cheeses or in pieces. About 450 litres of milk were produced each day, a little more at the beginning of summer. About 14 litres of milk are needed to produce 1 kg of cheese. Hence about 35 kg of cheese were produced every day; a whole cheese weighed about 5 kg.

In the 39th calendar week of 1999 S. Oranienburg was found in the following products from the Alpe Lorain: four of five samples of ‘whole fat alpine cheese,’ four of five samples of ‘3/4 fat alpine cheese,’ three of all those samples of ‘1/2 fat alpine cheese,’ and one sample of ‘skimmed milk alpine cheese.’ Samples of starting cultures (n=1), and drinking water (n=2) taken from the Alpe Lorain were free of S. Oranienburg. So were milk samples from cows that had been on the Alpe Lorain pasture until week 38, or were free of salmonella.

Specimens were taken from animals and the surroundings at the Alpe Lorain in week 39. Mouse excrement (from the feeding troughs), one sample of supplemented feed, three dust samples (from the doormat at the entrance of the dairy hut, the ramp leading to the milking stand, the windowsill), and samples of cow urine and liquid manure were all free of salmonella. Stool specimens from 44 cows and one collective sample of chicken droppings (the latter without any contact to the Alpe Lorain for 12 days) were also negative.

Only one stool sample from a pigsty situated 60 m to 80 m from the working quarters of the Alpe Lorain yielded S. Oranienburg. Pigs were no longer in the sty when samples were taken. The pigs had been fed daily with whey (a waste product of cheese making) through a pipeline (plastic hose) connected to the feeding trough.

On 20 October (week 42) the authorities issued an official warning about the consumption of the products involved. Altogether about three tonnes of alpine cheese with different fat contents were produced at the Alpe Lorain between 3 July and 18 September 1999. At the time of the official investigation about 1200 kg of cheese were still in storage.

In week 43 three collective stool samples were taken from the empty chicken coop of the Alpe Lorain. S. Oranienburg was found in this stool and also in a swab sample from the floor of the dairy room. According to the tenant of the alpine pasture, chickens had been allowed to roam freely and also had had repeated access to the alpine dairy room. The lack of hygienic partition between the coop and the dairy room was noted as a serious structural shortcoming.

Thus, without performing a case control study and without using molecular methods to compare patients and food isolates, we identified locally produced alpine cheese epidemiologically and through culture as the vehicle of this outbreak of S. Oranienburg infection.

Transmission of salmonella through milk or infected cattle is unlikely because we found no evidence that the cattle was infected. It appeared that the infection of the pigs was a result of their being fed with whey and other contaminated waste products from the cheese making process. They seemed to have had no relation with human infections.

Alpine cheese is seldom found to cause salmonella infections, and in this case, the epidemiological outbreak investigation was triggered by the appearance of an atypical serotype, not previously found in humans in Tyrol.

An outbreak of S. Oranienburg that affected 11 cases in Minnesota (United States) in 1992 was attributed to industrially produced mozzarella cheese (1). S. Oranienburg infections are rare in humans; a large outbreak in Japan in 1999 appeared to be due to industrially produced dried octopus (2).

In May 2000, the alpine dairyman of the Alpe Lorain was charged with violating food legislation and given a suspended sentence of an 84 000 Austrian Schillings (6104.5 Euro) fine. The possible consequences of criminal proceedings may hinder epidemiological outbreak investigations. Investigating the chain of infection is essential to implement specific preventive measures and therefore indispensable in view of public health, but may carry unforeseen legal consequences for those involved. People with S. Oranienburg infection who refused to cooperate actively justified their refusal by saying the investigation might have negative consequences for the alpine dairy business.

1. Hedberg CW, Korlath JA, D’Aoust JY, White KE, Schell WL, Miller MR, et al. A multistate outbreak of Salmonella javiana and Salmonella oranienburg infections due to consumption of contaminated cheese. JAMA 1992; 268: 3203-7.

2. Okumara T, Suzuki K, Mii H, Kimura F, Ito J, Kumada K, et al. Sepsis due to Salmonella Oranienburg – a case report. Kansenshogaku-Zasshi 1999; 73: 787-91.