Bacteriological evaluation of vaccination against Salmonella Typhimurium with an attenuated vaccine in subclinically infected pig herds

https://doi.org/10.1016/j.prevetmed.2019.04.016Get rights and content

Abstract

Subclinical infections with Salmonella Typhimurium occur frequently in pigs. They constitute a risk for human salmonellosis and are difficult to control with currently available control measures. Vaccination against Salmonella Typhimurium in pigs can be an effective tool to control Salmonella infections at farm level.

In the present study, the efficacy of an attenuated Salmonella Typhimurium vaccine (Salmoporc®, IDT Biologika) to control Salmonella infections in pigs was evaluated in three subclinically infected pig herds. The effect on Salmonella excretion and the number of pigs positive for Salmonella Typhimurium field and vaccine strains in ileocecal lymph nodes at slaughter were evaluated using five different vaccination strategies: 1. vaccination of sows, 2. vaccination of sows and piglets, 3. vaccination of sows and fattening pigs, 4. vaccination of piglets, 5. vaccination of fattening pigs, which were all compared to a non-vaccinated control group (experimental group 6). Each vaccination strategy was implemented in each farm, during two consecutive production cycles of the same sows.

The prevalence of Salmonella Typhimurium field strain excretion was low; in total, 4% of the fecal and overshoe samples collected in the non-vaccinated control group were Salmonella Typhimurium field strain positive. The excretion of Salmonella Typhimurium field strain did not significantly differ between farms, production cycles and experimental groups. Applying vaccination in either sows and piglets, sows and fattening pigs, or in piglets only, resulted in a significantly reduced number of Salmonella Typhimurium field strain positive lymph nodes of slaughter pigs in the second production cycle, but not in the first production cycle. Vaccination of sows and piglets resulted in the most consistent reduction of Salmonella Typhimurium field strain positive lymph nodes at slaughter. The vaccine strain was detected in the lymph nodes of 13 pigs at slaughter, indicating the possible persistence of the vaccine strain until slaughter.

Because of limitations in the study design, and the variability between farms and production cycles, the results of the current observational study should be extrapolated with care. Nevertheless, the results provide evidence that applying vaccination against Salmonella Typhimurium in sows and piglets (preferred), sows and fattening pigs, and piglets only can support the control of Salmonella Typhimurium infections by decreasing the prevalence of Salmonella Typhimurium field strain positive lymph nodes at slaughter.

Introduction

Human salmonellosis is the second most reported foodborne zoonosis in Europe (EFSA, 2015b,a, 2016, 2017). Infections with Salmonella enterica subspecies enterica serovar Typhimurium (Salmonella Typhimurium) in pigs constitute a major risk for human salmonellosis. In 2016, pigs and pork were considered the source of 26.9% of the human infections caused by Salmonella Typhimurium and of 61.9% of the human infections caused by Salmonella Typhimurium monophasic variants (EFSA, 2017).

The high prevalence of subclinical infections with Salmonella Typhimurium in pig herds, together with the intermittent shedding pattern of infected pigs and the common occurrence of carriers and environmental reservoirs, hamper a proper control of infections at farm level (Gray and Fedorka-Cray, 1996; Funk et al., 2001; Pires et al., 2013; Lynch et al., 2018). Current on-farm control measures are mainly focused on biosecurity, cleaning and disinfection, all-in all-out management and acidification of feed and drinking water (Wales et al., 2011; Andres and Davies, 2015; Callegari et al., 2015; Hill et al., 2016). Vaccination against Salmonella in pigs can be an important tool to control Salmonella infections at farm level as well (Denagamage et al., 2007; de la Cruz et al., 2017; Wales and Davies, 2017).

The main goals of vaccination are to prevent clinical salmonellosis, to decrease shedding and colonization and to decrease the probability of contamination of carcasses (Haesebrouck et al., 2004; Meeusen et al., 2007; Boyen et al., 2008; Arguello et al., 2012; Wales and Davies, 2017). Several papers report beneficial effects of different vaccines against Salmonella infection in pigs, either under experimental or field conditions (Denagamage et al., 2007; de la Cruz et al., 2017; Wales and Davies, 2017). Most studies measured vaccine efficacy by comparing the presence of Salmonella in feces and/or organs between vaccinated and control groups (de la Cruz et al., 2017), additionally, the effect on weight gain is evaluated in several studies (Farzan and Friendship, 2010; De Ridder et al., 2014).

The attenuated histidine-adenine auxotrophic vaccine Salmoporc® (IDT Biologika) is currently the only Salmonella Typhimurium vaccine commercially available for pigs in Europe. The vaccine has previously been evaluated with promising results in sows and weaned piglets of three and six weeks of age (Lindner et al., 2007), in piglets of three and 24 days of age (Roesler et al., 2010; De Ridder et al., 2014), in weaned piglets of four and seven weeks of age (Theuß et al., 2017) and in sows and gilts (Davies et al., 2016; Smith et al., 2018). To our knowledge, the vaccine has not been evaluated in a field study applying several different vaccination strategies in one farrowing batch. Also, the vaccine has not yet been evaluated in fattening pigs at the start of the fattening period. Vaccination of fattening pigs may be beneficial compared to vaccination around weaning, as it avoids extra handling, stress and possible adverse reactions in the crucial transition period around weaning.

The general aim of the present study was to assess the effect of different vaccination strategies (1. vaccination of sows, 2. vaccination of sows and piglets, 3. vaccination of sows and fattening pigs, 4. vaccination of piglets, 5. vaccination of fattening pigs) with an attenuated Salmonella Typhimurium vaccine in subclinically infected pig herds. The specific objectives were: 1. to investigate the effect of the different vaccination strategies on the excretion of Salmonella Typhimurium field strains, 2. to investigate to which extent the different vaccination strategies reduce the number of pigs positive for Salmonella Typhimurium field strains in the ileocecal lymph nodes at slaughter, 3. to evaluate the possible persistence of the vaccine strain in ileocecal lymph nodes, 4. to evaluate the genetic variation between Salmonella Typhimurium isolates originating from vaccinated and non-vaccinated pigs and 5. to evaluate the effect of the different vaccination strategies on the daily weight gain during the fattening period.

Section snippets

Farm selection

Three Belgian pig farms (A, B, C) were selected based on the following criteria: 1. bacteriological detection of Salmonella Typhimurium on the farm and high Salmonella-specific antibody levels in fattening pigs (S/P-ratios ≥0.6) in the former Belgian Salmonella Surveillance Program, without clinical Salmonella infections during the year preceding the study, 2. a minimum of 72 sows per farrowing batch, 3. possibility to monitor the pigs from birth to slaughter, 4. willingness of the farmer to

Fecal and overshoe samples: sows

The bacteriological results of the fecal and overshoe samples from the sows are shown in Table 2. In total, 41/875 (4.7%) samples were Salmonella positive; 12/265 (4.5%), 24/299 (8.0%) and 5/311 (1.6%) samples from farm A, B and C, respectively. The vaccine strain was detected in 32/875 (3.7%) samples, collected in all three farms, both from vaccinated and from non-vaccinated sow groups. In total, 6/875 (0.69%) samples were Salmonella Typhimurium field strain positive; 1/265 (0.38%), 5/299

Discussion

The current study investigated the effect of different vaccination strategies against Salmonella Typhimurium with an attenuated vaccine on the excretion of Salmonella and the number of pigs positive for Salmonella in the ileocecal lymph nodes in three subclinically infected pig herds. In production cycle 2, the results showed a protective effect of vaccination on the number of Salmonella Typhimurium field strain positive lymph nodes when applying vaccination either in sows and piglets, sows and

Conclusion

The results of the current study should, because of limitations in the study design and the variability between the farms and production cycles, be extrapolated with care. Nevertheless, they provide evidence that applying vaccination against Salmonella Typhimurium in sows and piglets (preferred), sows and fattening pigs, and piglets only can support the control of Salmonella Typhimurium infections by decreasing the prevalence of Salmonella Typhimurium field strain positive lymph nodes at

Declaration of interest

None.

Acknowledgements

The research that yielded these results was funded by the Belgian Federal Public Service of Health, Food Chain Safety and Environment through the contract [SUSALVAC; RT14/3].

We thank the farmers for their motivation and help with this study. Also, we are grateful to the veterinarians of the farms, the slaughterhouse employees and all colleagues and students for their assistance during the study. The lab personnel, especially Nathalie Van Rysselberghe, is greatly appreciated for the help during

References (55)

  • H.S. Hurd et al.

    The effect of lairage on Salmonella isolation from market swine

    J. Food Prot.

    (2001)
  • J.D. Kich et al.

    Prevalence, distribution, and molecular characterization of Salmonella recovered from swine finishing herds and a slaughter facility in Santa Catarina, Brazil

    Int. J. Food Microbiol.

    (2011)
  • J.-S. Lin et al.

    Development and use of polymerase chain reaction for the specific detection of Salmonella Typhimurium in stool and food samples

    J. Food Prot.

    (1999)
  • C. Magistrali et al.

    Contamination of Salmonella spp. in a pig finishing herd, from the arrival of the animals to the slaughterhouse

    Res. Vet. Sci.

    (2008)
  • N. Nollet et al.

    Distribution of Salmonella strains in farrow-to-finish pig herds: a longitudinal study

    J. Food Prot.

    (2005)
  • A. Rajiċ et al.

    Longitudinal study of salmonella species in 90 Alberta swine finishing farms

    Vet. Microbiol.

    (2005)
  • J. Ruggeri et al.

    Inactivated Salmonella enterica serovar Typhimurium monophasic variant (S. Typhimurium 1, 4,[5], 12: i-) in sows is effective to control infection in piglets under field condition

    Vet. Microbiol.

    (2015)
  • H. Salmon et al.

    Humoral and cellular factors of maternal immunity in swine

    Dev. Comp. Immunol.

    (2009)
  • D. Sandvang et al.

    Persistence of a Salmonella enterica serotype Typhimurium clone in Danish pig production units and farmhouse environment studied by pulsed field gel electrophoresis (PFGE)

    FEMS Microbiol. Lett.

    (2000)
  • R.S. Singer et al.

    Do microbial interactions and cultivation media decrease the accuracy of Salmonella surveillance systems and outbreak investigations?

    J. Food Prot.

    (2009)
  • B.J. Wilhelm et al.

    Interventions to reduce non-typhoidal Salmonella in pigs during transport to slaughter and lairage: systematic review, meta-analysis, and research synthesis based infection models in support of assessment of effectiveness

    Prev. Vet. Med.

    (2017)
  • V.M. Andres et al.

    Biosecurity measures to control Salmonella and other infectious agents in pig farms: a review

    Compr. Rev. Food Sci. Food Saf.

    (2015)
  • H. Arguello et al.

    Salmonella Control Measures at Farm in Swine Production. Salmonella-Distribution, Adaptation, Control Measures and Molecular Technologies

    (2012)
  • T. Blaha et al.

    The Early Colonization Pattern of S. Typhimurium in Pigs after Oral Intake

    (1997)
  • C. Boland

    Development of New Molecular Tools for Characterizing Salmonella spp. Strains Isolated in Belgium, With New Insights into Monophasic Variants of Serovar Typhimurium

    (2014)
  • N. Botteldoorn et al.

    Phenotypic and molecular typing of Salmonella strains reveals different contamination sources in two commercial pig slaughterhouses

    Appl. Environ. Microbiol.

    (2004)
  • C. Boughton et al.

    Quantitative examination of Salmonella spp. in the lairage environment of a pig abattoir

    Foodborne Pathogens Dis.

    (2007)
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