DISCUSSION

In the present study we examined risk factors for Salmonella Infantis infection. Our analysis yielded no definitive risk factor that could explain the increase in S. Infantis cases occurring in Israel since 2008. S. Infantis is currently the most prevalent serotype nationwide, and its replacement of S. Enteritidis and S. Typhimurium as the leading serotype in Israel may be explained by the actions taken to reduce the prevalence of the latter in poultry [Reference Bassal8]. Those actions included tight surveillance of all breeding flocks and hatcheries, culling or treatment of all flocks infected with S. Enteritidis or S. Typhimurium, improvement of biosecurity and infrastructure, and systematic immunization against S. Typhimurium and S. Enteritidis initiated in 1994 and 1996, respectively [Reference Bassal8].

Our present study revealed significant protective factors for S. Infantis infection. Breastfeeding in infants aged ⩽1 year decreased the estimated risk for acquiring infection by fourfold. Breastfeeding had been found to be protective against Salmonella infections in several earlier studies [Reference Rowe9, Reference Jones10]. In one case-control study conducted by FoodNet sites for children aged <12 months, consumption of breast milk was found to be protective against Salmonella compared to the consumption of any other fluid (mOR 0·05, 95% CI 0·00–0·30). That study reported that breastfeeding could prevent as many as 74–100% of all Salmonella cases [Reference Rowe9]. Similar results were found in a case-control study that examined the association between sporadic Salmonella and different exposures, where the OR for breastfeeding was 0·5 (95% CI 0·3–0·6) [Reference Jones10]. The biological explanation for the beneficial effect of breastfeeding may be the presence of phagocytes as well as specific secretory IgA in the colostrum and breast milk [Reference Orlando11, Reference Johnson12]. Another explanation is that infants who are breastfed, are less likely to become exposed to contaminated food or bottled items.

Although larger families are usually of lower socioeconomic status, which is commonly considered a risk factor for enteric diseases [Reference Hasin13], we demonstrated that a large family size was protective in both age groups. A similar result was reported in a matched case-control study performed in children aged <5 years in Tanzania, where a large number of siblings was shown to be protective against diarrhoeal diseases [Reference Gascon14]. The researchers attributed the decrease in risk with increasing number of siblings to maternal experience affecting hygiene practices [Reference Gascon14]. A Danish study which examined the association between socio-demographic variables and enteric diseases due to Salmonella serotypes other than S. Typhimurium and S. Enteritidis in adults found that a large number of children in a household was protective against those diseases [Reference Simonsen, Frisch and Ethelberg15]. Those researchers proposed that when there are children at home, kitchen hygiene may become more important and the diet may contain fewer risky food items [Reference Simonsen, Frisch and Ethelberg15]. They also noted that the threshold for parents to seek medical care due to mild gastrointestinal symptoms may be higher with later-born than firstborn children [Reference Simonsen, Frisch and Ethelberg15]. If so, the lower risk in members of households with ⩾2 children may be, at least in part, the result of underreporting of disease in families with several children [Reference Simonsen, Frisch and Ethelberg15]. Our finding may also be explained in a number of ways: first, a large number of people in the household increases the chances of exposure to Salmonella and subsequent development of a high natural immunity against this bacterium as a result of a previous exposure. Second, there may be frequent exposures to low infective doses which do not cross the high threshold necessary to cause a disease but are sufficient to create natural immunity.

Consumption of eggs was a significant risk factor in our older age group. Previous studies demonstrated that consumption of improperly cooked eggs, such as scrambled and fried, were risk factors for infection with Salmonella serotypes [Reference Hedberg16, Reference Hennessy17]. Several reports on diarrhoeal outbreaks that were related to Salmonella serotypes were associated with the consumption of eggs [Reference Badrinath18, Reference Salmon19]. However, we could not identify an association with the method of preparation (scrambled, hardboiled, soft-boiled, omelette, fried), place of purchase (grocery, supermarket, private hutch, market) or amount of eggs that were consumed. Our finding was supported by data from the Central Salmonella Laboratory that reported in 2009 that 32·5% and 36·2% of human and animal Salmonella cases, respectively, were S. Infantis, and chickens were the main source of S. Infantis infection in animals (96·6%) [7].

Thawing chicken in water was a risk factor (with borderline significance) for S. Infantis infection in our cases. This way is quicker than thawing at room temperature and in the refrigerator [Reference Roberts20]. The outer layer of the chicken, especially that of a whole chicken, is defrosted more rapidly than the inner layer, and cooking a chicken which is not fully defrosted and at an insufficiently high temperature does not destroy Salmonella [Reference Roberts20]. It is also possible that using running water or still water in the thawing process may facilitate cross-contamination with Salmonella.

Our results revealed that eating carrots was protective against S. Infantis infection. The anti-bacterial activity of carrots is presumably due to apolar components. Free saturated fatty acid (dodecanoic acid) and methyl esters of saturated fatty acids (dodecanoic and pentadecanoic acids) were identified in purified active extracts of carrots and may be related to anti-bacterial activity [Reference Babic21]. Treatments with carrot extracts, especially the alcoholic extract, were reportedly efficient in inhibiting the growth of Pseudomonas aeruginosa [Reference Abdula Ali22]. However, the protective effect may be attributed to consumption of carrots and other vegetables which, as part of a healthy lifestyle, may prevent exposure to potential risk factors.

Observing a religious lifestyle was protective against S. Infantis infection. Religious Jews routinely separate dairy products and meat products, a practice that may prevent cross-contamination. However, another possibility for this finding is under-representation of observant individuals in the cases in our study because they are less likely to visit a physician. Another explanation, which was confirmed by our database, is the fact that religious families are larger than secular families [23].

Drinking tap water was found protective against S. Infantis compared to bottled water and filtered water. In Israel, 80% of tap water is supplied by one company [24]. Tap water is closely regulated for safety by the Ministry of Health from the production site to the customer's residence. Bottled water is regulated only at the manufacturer's plant. In addition, individuals who consume filtered water are recommended to replace the filters every 6 months (for a considerable amount of money), and there is no data as to how many comply with these recommendations. This may explain the advantage of drinking tap water.

Our study has a number of possible limitations. First, there may have been recall bias since cases were interviewed on an average of 34·6 days after obtaining the stool sample. Due to the long time interval elapsing, cases are less likely to remember their exposure. However, since the difference between cases and controls was only 5·6 days, we conclude that there is no reason to believe there was a differential misclassification between cases and controls. Matched ORs may thus be an underestimate of the true association. Second, controls were matched to cases by age, gender and neighbourhood. This may have led to overmatching, and important risk factors may have been obscured.

In conclusion, Salmonella infections may be prevented by good hygiene habits. Breastfeeding should be more vigorously encouraged by the Israeli public health authorities. The health authorities must raise the level of public awareness regarding the importance of hygienic care in the kitchen and of the importance of properly cooking eggs as well as of thawing chicken before preparation and cooking it properly.