In Spain during August 1997, a monophasic S.Typhimurium (4,5,12:i:-) was isolated from human and food samples with affecting of 14 of the 17 Spanish Autonomous Communities. All positive food isolates corresponded to pork and pork products and it was indicated that this strain “has emerged and spread to human in Spain, probably with contaminated pork as the source”.1,2 From 1998 to 2000 in New York, a monophasic variant 4,5,12:i:- caused a food poisoning outbreak.3 In the Europe Union an increase of this monophasic variant of serovar Typhimurium has been observed over the last ten years, and the likely reservoir of infection, as in the Spanish case, is pigs.4,5

On April 5 2011, the Microbiology Laboratory of the General Hospital in Castellón (Spain) alerted the Epidemiology Division of the Public Health Center to a major increase of positive fecal culture S.Typhimurium in children with gastrointestinal symptoms. In this context, the aim of this study was to identify the cause of the infection and to take measures in order to control and prevention further spread of the disease.

The outbreak occurred during the local holydays, from March 26 to April 3 2011, in the city of Castellon, the capital of the province of Castellon with 170,000 inhabitants. A descriptive epidemiologic study was begun to considering the case definition and characteristics of patients: clinical symptoms, evolution and time and place of each case and potential risk factors of salmonellosis. All S.Typhimurium positive cases from the General Hospital of Castellon were investigated. Two incident matching case–control studies were then begun when the descriptive study generated a hypothesis relating to the sources of infection and before the serotyping and phage typing of the S.Typhimuriun were carried out. When the serotyping and phage typing were performed, positive cases of S.Typhimurium from the Microbiology Laboratory of the Hospital La Plana in Vila-real, a city of 50,000 inhabitants situated 6km from Castellon, were included in the study. Once these results had been obtained, two matched case–control studies were performed.

In the first incident matched case–control study, the definition of case was a patient during the period February to May 2011 with positive monophasic/biphasic S.Typhimurium phage type 138, S.Typhimurium phage type 193 or S.Derby isolated from fecal urine or blood cultures. In the second incident matched case–control study, the definition of case was a patient during the period February to May 2011 with positive S. Typhimurium phage type 104b, 21, U311, U302, 195, and un-typable phage types isolated from fecal cultures.

The matched case–control studies (1 case:2 controls), were matched by age (less than 1 year) and gender, and each control was chosen at random from the list of patients of the pediatrician or general practitioner who attended the case. Before contact was made with controls, their pediatrician or general practitioners were consulted and verbal consent was obtained. Verbal consent to participate was also obtained from the controls or their parents. An ad hoc questionnaire was used to obtain information on demographic characteristics and potential risk factors; the same questionnaire was used for cases and controls. Information on food exposure was obtained from questions about the consumption of the presumed source foods and other risk factors in a period of up to 15 days before the start of symptoms in the cases; for controls, enrolment was considered equivalent to the day symptoms started in the cases. If the control had suffered gastroenteritis in the 15 days before the interview, he or she was excluded. Information about cases was obtained through face to face or telephone interviews by the epidemiology division staff. Telephone interviews were used with the controls, and if contact had not been established after five telephone calls, another control was randomly chosen from the list.

The results indicated that the outbreak was caused by several isolates of S.Typhimurium and S.Derby, and the source of infection was brand X dried pork sausage and the microbiological surveillance alerted on the outbreak. The matched case–control studies allowed the food to be identified and the microbiologic results confirmed the source of infection. Following the intervention, to withdraw the implicated food, no new cases associated with the consumption of this food occurred.

The second matched case–control study found associations between the gastroenteritis and the consumption of brand X dried pork sausage together with contact with diarrhea patients, suggesting that all cases came from the same outbreak. The isolate of several Salmonella phage types in the brand X dried pork sausage also lens support to this claim. In addition, the time of occurrence and the clinical symptoms suggest the same source of infection.

The number of patients affected by the outbreak was probably higher than the number reported, considering that only the cases were the patients with a microbiological culture and probably with more severe symptoms. A study by the Epidemiology Division into the incidence of gastroenteritis patients in the General Hospital Emergency Service of Castellon found an increase in the number of patients in the period March-April 2012.In addition, 13 controls were excluded by gastroenteritis symptoms and 4 of whom had the consumption of brand X dried pork sausage as a risk factor. An incidence rate of 2.3%, 4 cases and 177 controls (164 included and 13 excluded) associated with this consumption, was estimated.

The high incidence in children, median 4 years, and old people may be associated with the possible low concentration of Salmonella in the food vehicle together with low body mass and the immature immunity in children and defective immunity in old people. The clinical symptoms were compatibles with severe gastroenteritis and the presence of blood in feces was frequent. The period of incubation was not calculated, however, it could have a range of 3 to 7 days. Antibiotic resistances of the Salmonella strains were small when comparisons with other S.Typhimurium were made.5

Our knowledge, this outbreak is the first of monophasic S.Typhimurium associate with the consumption of dried pork sausage reported in Spain and very recent an outbreak of monophasic S.Typhimurium phage type 138 with homemade chorizo as food vehicle of transmission was been occurred in Basque Country.10 In addition, consumption of chorizo like sausage, imported from Spain, has been implicated in an outbreak of S.Typhimurium in Denmark.11 In an international context, some S.Typhimurium outbreaks have been associated with the consumption of pork in the form of salami sticks in Great Britain,12 salami products in Denmark,13 Italian salami in Sweden,14 traditional pork salami in Italy,15 and pork meat in Denmark, Norway, and Sweden.16 These outbreaks have many similar characteristics to the outbreak reported here: the young medians age of patients’ age, the implicated food is ready to eat and it is consumed raw, the outbreaks tend to occur in spring, the severity of the infections with a high frequency of fever, presence of blood in stools, and frequent hospitalizations.

The Salmonella that caused the outbreak included monophasic S.Typhimurium phage type 138, S.Typhimurium phage type 193, and S.Derby; S.Wien was only isolated in food. The reservoir of these strains is the pig.17 In Europe, monophasic S.Typhimurium, is considered to be a potential and emergent risk for humans through the consumption of pork18 and some outbreaks of monophasic S.Typhimurium had been reported by several Europe Union countries such as France, where two outbreaks occurred with 447 patients and dried pork sausage as the likely vehicle of infections19–20 and Luxemburg with one outbreak and 133 patients with the consumption of pork meat as the suspected vehicle.21 In Germany outbreaks of this variant have been detected during 2006–2008.22 In France, an outbreak with 554 cases of the same variant in 4 schools was associated with the consumption of beef burger.23 In Italy, an outbreak of this variant was found associated with a cook pork product.24 It has been postulated that there are other animal reservoirs of this monophasic variant apart from pigs, such as chickens and turtles.25

The source of infection could find by the isolate of Salmonella in the brand X dry pork sausage and in samples from dried pork sausages in the warehouse of supermarket chain A. Monophasic and biphasic S.Typhimurium were isolated indicating that the contamination could have occurred at the factory during the dried pork sausage production, and that this contamination was elevated because three Salmonella strains were implicated. The production of brand X dried pork sausage was carried out in a town in Teruel province and the Aragon Health Authority found evidence of the cause of the outbreak in the producer. In addition, a recent study a herd-based survey of pigs in Aragon that including Teruel province, found Salmonella spp prevalence in the 31% of animals and in the 94% of herds.26 Samples were taken from mesenteric lymph nodes at the time of slaughter, and monophasic varaiant S.Typhimurium 4,[5], 12:i:- was the first prevalent serotype.26 Other serological survey in pigs in Aragon27 found high prevalence of the salmonellosis. The more important risk factors associated with the salmonellosis were farms without rodent control, long period of fattening, and farm with finishing pigs.26

The Surveillance of Salmonella was decisive detecting and controlling Salmonella outbreaks, considering that salmonellosis was not a notifiable disease in Spain in 2011. Pediatricians and generalist practitioners were unable to detect the outbreak. However, study of etiologic agents of gastroenteritis in fecal cultures, allowed the Microbiology Laboratory of Castellon General Hospital to detect the possibility of an outbreak in a short period of time. In addition, matched case–control studies found the source of the outbreak, and the characterization of the isolates by sero-typing, phage-typing and pulsed-field gel electrophoresis confirmed the source of the outbreak; the control measures were also effective. Several health institutions cooperated to control of the outbreaks (primary health care, microbiology laboratories, hospitals, and public health authorities).

The limitations of our study are as follows: the attack rate was not estimated, the magnitude of the outbreak could not be known, and the incubation period could not be estimated. In addition, some recall bias has occurred as a result of the study design, although reports about the outbreak appeared in the media once it was over. No chemical analyses of this food were carried out to learn how the Salmonella was able to survive in the food.12

Conclusions: The study revealed brand X dried pork sausage as the food vehicle of the outbreak and the cooperation of various health institutions enable it to be controlled and further spread prevented.

None conflict of interest by the authors.