Risk factors for Salmonella spp in Portuguese breeding pigs using a multilevel analysis

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Abstract

Salmonella is the second most frequent cause of foodborne illness in the European Union (EU), so EU enforced legislation to achieve a reduction in Salmonella prevalence in the swine sector. To set the reduction target each country carried out a baseline survey to estimate Salmonella prevalence. The aim of our study was to identify risk factors for the presence of Salmonella in breeding pigs based on the data of the Baseline Study for Salmonella in Breeding Pigs in Portugal. In total, 1670 pen fecal samples from 167 herds were tested by culture and 170 samples tested positive. Along with the collection of the samples a survey was applied to collect information about the herd management and potential risk factors. Multilevel analysis was applied to the data using generalized linear mixed models and a logit link function. The outcome variable was the presence/absence of Salmonella in the pen fecal samples. The first level was assigned to the pen fecal samples and the second level to the herds. The results showed significant associations between Salmonella occurrence and the factors (p < 0.05): maternity pens versus mating pens (OR = 0.39, 95%CI: 0.24–0.63), feed from external or mixed source versus home source (OR = 2.81, 95%CI: 1.19–6.61), more than 10 animals per pen versus 10 animals per pen (OR = 2.02, 95%CI: 1.19–3.43), North Region versus Alentejo Region (OR = 3.86, 95%CI: 1.08–13.75), rodents control (OR = 0.23, 95%CI: 0.090–0.59), more than 90% of boars homebred or no boars versus more than 90% of boars from an external source (OR = 0.54, 95%CI: 0.3–0.97), semen from another herd versus semen from insemination centers (OR = 4.47, 95%CI: 1.38–14.43) and herds with a size of 170 or more sows (OR = 1.82, 95%CI: 1.04–3.19). This study offers very relevant information for both the Portuguese veterinary authorities and the pig farmers currently developing control programmes for Salmonella. This is the first study providing evidence for semen and boars source as risk factors for Salmonella in breeding pigs.

Introduction

Salmonella has been reported as the second most frequent cause of foodborne illness in the European Union (EU) in the past ten years (EFSA, 2010). The contribution of pork products to the total burden of human salmonellosis cases varies between countries but it is estimated to be around 10% (Pires et al., 2010). The EU Regulation (EU Regulation No 2160/2003) imposes to the Member States (MS) implementation of a control programme to reduce the prevalence in food production species including pigs. To set the reduction target each MS carried out baseline surveys to estimate the Salmonella spp. prevalence in some food production animals. The objective of the surveys was to obtain comparable data for all MS through harmonized sampling and testing schemes. In pigs the baseline study was done at abattoir level (collection of lymph nodes of pigs slaughtered) and at herd level (collection of pen fecal samples of breeding pigs). These cross-sectional studies also collected information regarding herd management practices and potential risk factors linked to this agent. After the specification of the reduction target each MS will have the responsibility to establish an effective national control programme adjusted for the country-specific characteristics, such as the risk factors, the disease prevalence and the financial implications for stakeholders.

It was expected that the baseline surveys supplied enough data to enable the identification and quantification of potential risk factors to be used in the development of programmes and procedures that reduces Salmonella shedding in pig herds economically and effectively. It is important that this information is available before Salmonella reduction programmes are implemented at the herd level to enable farmers to make informed choices, enhance public health and avoid unnecessary costs (Bahnson et al., 2006).

Some of the known risk factors already identified were linked to: (1) biosecurity measures (Baptista et al., 2010) such as potential biological vectors (as rodents) (Letellier et al., 1999, Meerburg and Kijlstra, 2007, Skov et al., 2008), hygiene of hands, equipment and facilities (Lo Fo Wong et al., 2004), purchase of animals from different suppliers (Lo Fo Wong et al., 2004), (2) herd management, such as herd size (Poljak et al., 2008), batch production system (Funk and Gebreyes, 2004), housing – type of floor (partial slatted floor) (Nollet et al., 2004, Rossel et al., 2006), type of pen separations (Lo Fo Wong et al., 2004), (3) feeding practices such as dry feed (Bahnson et al., 2006), purchase of feed (Benschop et al., 2008), adding organic acids to feed (Funk and Gebreyes, 2004), (4) the use of antibiotics (Beloeil et al., 2007, Funk et al., 2007), parasite infestations (van der Wolf et al., 2001, Beloeil et al., 2004), and health status of the herd (Funk and Gebreyes, 2004) among others (Fosse et al., 2009).

The data used in the present study were collected as part of the Baseline Survey on the Prevalence of Salmonella in Breeding Pigs in Portugal. The aim of the study was to identify risk factors for the presence of Salmonella in herds with breeding pigs.

Section snippets

Sampling and samples collection and analysis

The data used in this study were transferred to the authors by the Portuguese Veterinary Authorities (PVA) and they are derived from the baseline study for Salmonella in Breeding Pigs in Portugal. This study was carried out by the PVA in the context of the Commission Decision 2008/55/EC. The authors were not involved in the baseline study and the data collection methodology described below is of the entire responsibility of the PVA.

The sampling frame, the diagnostic testing methods, the sample

Results

A total of 1670 fecal pen samples (level 1) belonging to 167 herds (level 2), that responded to the questionnaire, were tested. Among the samples tested 170 from 76 herds were positive to Salmonella. Salmonella Typhimurium, followed by Salmonella Rissen were the most frequent serotypes found in the positive samples.

In the 167 herds there were 33 breeding holdings (45.45% had at least one sample positive to Salmonella, CI: 37.9–53.1%) and 134 productions holdings (45.45% had at least one sample

Discussion

In this study a representative sample of the herds with breeding pigs in Portugal was used. The herds sampled were obtained using a sampling frame assembled by the PVA. The sample was representative of the country and took into consideration the different number of herds per region. The herds were randomly allocated to the study. The risk factors were assessed using data from a questionnaire filled by the herd veterinarian which were also responsible for the collection of the feces samples. The

Conclusion

The risks highlighted in this study are epidemiologically and biologically consistent and they are representative of the breeding pigs system currently used in Portugal. It is noticeable the identification of risks associated with semen and boars purchasing: this reinforces that attention should be paid to these factors when conceiving herd biosecurity programmes; also noticeable and important is the fact that these risk factors have not been highlighted before. Our findings are of high

Acknowledgments

We would like to thank FCT for the PhD scholarship (SFRH/BD/40932/2007) and the Portuguese official veterinary authority (DGV) for supplying the data from the Baseline Survey on the Prevalence of Salmonella in Breeding Pigs.

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