Producing Salmonella-free pigs: a review focusing on interventions at weaning

Salmonella infection in pig production is typically endemic and largely asymptomatic. It is a cause of substantial concern among food safety bodies, prompting voluntary and legislative responses aimed at monitoring and reducing the number of Salmonella-infected animals entering the human food chain. Elimination of the problem at an early stage of production is highly desirable, and to this end the present review examines published evidence on the carriage of Salmonella by piglets before and after weaning, as well as evidence on the dynamics of Salmonella infection in the weaner and grower stages of pig production, the effects of maternal immunity, and risk factors for Salmonella excretion after weaning. Various interventions to reduce or eliminate Salmonella infection in young pigs have been tried, such as vaccination, competitive exclusion, treatments in feed and water, antibiotic administration, disinfection of animals, and segregated weaning to clean accommodation. The evidence on the effectiveness of these is considered, and the last is examined in some detail, as it appears currently to offer the best chance of eliminating Salmonella from growing stock.

[1]  Maja O’Connor.  LONGITUDINAL STUDY , 2013 .

[2]  Mark Breslin,et al.  Evaluation of commonly-used farm disinfectants in wet and dry models of Salmonella farm contamination , 2011, Avian pathology : journal of the W.V.P.A.

[3]  M. Donadeu,et al.  Comparative study of three porcine Salmonella ELISAs , 2010, Veterinary Record.

[4]  A. Rajić,et al.  Distribution of Salmonella serovars in breeding, nursery, and grow-to-finish pigs, and risk factors for shedding in ten farrow-to-finish swine farms in Alberta and Saskatchewan. , 2010, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[5]  J. Österberg.  Salmonella in Pigs Infection Dynamics of Different Serotypes , 2010 .

[6]  R. Davies,et al.  Longitudinal survey of the occurrence of Salmonella in pigs and the environment of nucleus breeder and multiplier pig herds in England , 2009, Veterinary Record.

[7]  F. Butler,et al.  Development and Application of a Stochastic Epidemic Model for the Transmission of Salmonella Typhimurium at the Farm Level of the Pork Production Chain , 2009, Risk analysis : an official publication of the Society for Risk Analysis.

[8]  J. Kamphues,et al.  Effects of dietary additives (potassium diformate/organic acids) as well as influences of grinding intensity (coarse/fine) of diets for weaned piglets experimentally infected with Salmonella Derby or Escherichia coli. , 2009, Journal of animal physiology and animal nutrition.

[9]  M. Arnold,et al.  Estimation of sample sizes for pooled faecal sampling for detection of Salmonella in pigs , 2009, Epidemiology and Infection.

[10]  A. Rajić,et al.  Distribution of Salmonella serovars in various pig production categories and risk factors for shedding in ten farrow-to-finish swine farms in western Canada. , 2009 .

[11]  D. Maes,et al.  Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. , 2008, Veterinary microbiology.

[12]  J. Pluske,et al.  Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs , 2008 .

[13]  G. Barigazzi,et al.  Longitudinal Study of Salmonella Infection in Italian Farrow‐To‐Finish Swine Herds , 2008, Zoonoses and public health.

[14]  M. Mazzoni,et al.  Antimicrobial effect of dietary nitrate in weaning piglets challenged or not with Salmonella enterica serovar typhimurium , 2008 .

[15]  P. E. Givisiez,et al.  Nose-to-nose transmission of Salmonella Typhimurium between weaned pigs. , 2007, Veterinary microbiology.

[16]  S. Martin,et al.  Multilevel analysis of risk factors for Salmonella shedding in Ontario finishing pigs , 2007, Epidemiology and Infection.

[17]  M. Kostrzynska,et al.  Approaches for reducing Salmonella in pork production. , 2007, Journal of food protection.

[18]  G. Reid,et al.  Effects on growth performance, feed efficiency, and health of weanling pigs fed fermented liquid whey inoculated with lactic acid bacteria that inhibit Escherichia coli in vitro , 2007 .

[19]  P. B. Lynch,et al.  Efficacy of cleaning and disinfection on pig farms in Ireland , 2007, Veterinary Record.

[20]  M. Stevens,et al.  Net Replication of Salmonella enterica Serovars Typhimurium and Choleraesuis in Porcine Intestinal Mucosa and Nodes Is Associated with Their Differential Virulence , 2007, Infection and Immunity.

[21]  J. S. Radcliffe,et al.  Effects of Acid LAC and Kem-Gest acid blends on growth performance and microbial shedding in weanling pigs. , 2007, Journal of animal science.

[22]  Moez Sanaa,et al.  Review of the Community Summary Report on Trends and Sources of Zoonoses, Zoonotic agents and Antimicrobial Resistance in the European Union in 2005 Scientific Opinion of the Scientific Panel on Biological Hazards (BIOHAZ) and Animal Health and Welfare (AHAW) , 2007 .

[23]  Robin C. Anderson,et al.  Influence of light exposure on horizontal transmission of Salmonella typhimurium in weaned pigs , 2007 .

[24]  S. Dowd,et al.  Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. , 2006, Current issues in intestinal microbiology.

[25]  A. Hensel,et al.  Immunization of sows in an integrated pig-breeding herd using a homologous inactivated Salmonella vaccine decreases the prevalence of Salmonella typhimurium infection in the offspring. , 2006, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[26]  S. S. Lewerin,et al.  Feed-borne Outbreak of Salmonella Cubana in Swedish Pig Farms: Risk Factors and Factors Affecting the Restriction Period in Infected Farms , 2006, Acta veterinaria Scandinavica.

[27]  K. Warriner,et al.  Prevalence of Salmonella spp. on Canadian pig farms using liquid or dry-feeding. , 2006, Preventive veterinary medicine.

[28]  R. Harvey,et al.  Low level nitrate or nitroethane preconditioning enhances the bactericidal effect of suboptimal experimental chlorate treatment against Escherichia coli and Salmonella Typhimurium but not Campylobacter in swine. , 2006, Foodborne pathogens and disease.

[29]  A. de Kruif,et al.  Distribution of salmonella strains in farrow-to-finish pig herds: a longitudinal study. , 2005, Journal of food protection.

[30]  A. de Kruif,et al.  Discrepancies between the isolation of Salmonella from mesenteric lymph nodes and the results of serological screening in slaughter pigs. , 2005, Veterinary research.

[31]  Dominiek Maes,et al.  Salmonella in sows: a longitudinal study in farrow-to-finish pig herds. , 2005, Veterinary research.

[32]  C. J. Oliveira,et al.  Experimental airborne transmission of Salmonella Agona and Salmonella Typhimurium in weaned pigs , 2005, Epidemiology and Infection.

[33]  A. Hensel,et al.  Effects of fluorequinolone treatment acidified feed, and improved hygiene measures on the occurrence of Salmonella Typhimurium DT104 in an integrated pig breeding herd. , 2005, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[34]  T. Crenshaw,et al.  Chlorate and disinfectant modify Salmonella enterica shedding in weaned pigs , 2005 .

[35]  A. Kruif,et al.  Dynamics of subclinical Salmonella infections in farrow-to-finish pig herds , 2005 .

[36]  A. Kruif,et al.  TRANSMISSION OF SALMONELLA FROM SOWS TO PIGLETS: A LONGITUDINAL STUDY , 2005 .

[37]  K-h,et al.  Effects of Fluorequinolone Treatment Acidified Feed , and Improved Hygiene Measures on the Occurrence of Salmonella Typhimurium DT 104 in an Integrated Pig Breeding Herd , 2005 .

[38]  A. Hensel,et al.  Oral vaccination of pigs with an invasive gyrA-cpxA-rpoB Salmonella Typhimurium mutant. , 2004, Vaccine.

[39]  A. Akkermans,et al.  Postnatal development of intestinal immune system in piglets: implications for the process of weaning , 2004 .

[40]  H. Stege,et al.  Herd-level risk factors for subclinical Salmonella infection in European finishing-pig herds. , 2004, Preventive veterinary medicine.

[41]  R H Davies,et al.  National survey for Salmonella in pigs, cattle and sheep at slaughter in Great Britain (1999–2000) , 2004, Journal of applied microbiology.

[42]  Y. Jung,et al.  Effect of Drinking-Water Administration of Experimental Chlorate Ion Preparations on Salmonella enterica serovar Typhimurium Colonization in Weaned and Finished Pigs , 2004, Veterinary Research Communications.

[43]  K. Richardson,et al.  Salmonella in commercially manufactured feeds. , 2004, Poultry science.

[44]  I. Charles,et al.  Oral vaccination , 2004, Antonie van Leeuwenhoek.

[45]  C Chauvin,et al.  Longitudinal serological responses to Salmonella enterica of growing pigs in a subclinically infected herd. , 2003, Preventive veterinary medicine.

[46]  R. Harvey,et al.  Competitive exclusion of Salmonella from the gut of neonatal and weaned pigs. , 2003, Journal of food protection.

[47]  M. Rostagno,et al.  Impact of commercial preharvest transportation and holding on the prevalence of Salmonella enterica in cull sows. , 2003, Journal of food protection.

[48]  Yasmine Ghafir,et al.  Salmonella contamination of pigs and pork in an integrated pig production system. , 2003, Journal of food protection.

[49]  B. White,et al.  Fermentable fiber reduces recovery time and improves intestinal function in piglets following Salmonella typhimurium infection. , 2003, The Journal of nutrition.

[50]  L. Alban,et al.  Longitudinal Study of Salmonella enterica Serotype Typhimurium Infection in Three Danish Farrow-to-Finish Swine Herds , 2003, Journal of Clinical Microbiology.

[51]  T. Y. Guan,et al.  Pathogen survival in swine manure environments and transmission of human enteric illness--a review. , 2003, Journal of environmental quality.

[52]  G. Bilkei,et al.  EFFECT OF HIGHLY FERMENTABLE DIETARY FIBER ON PIG PERFORMANCE IN A LARGE UNIT, INFECTED WITH ENDEMIC SWINE DYSENTERY , 2003 .

[53]  R. Isaacson,et al.  Distribution of Salmonella in swine production ecosystems. , 2002, Journal of food protection.

[54]  R. Scheidegger,et al.  Incidence of Reinfections with Mycoplasma hyopneumoniae and Actinobacillus pleuropneumoniae in Pig Farms Located in Respiratory-Disease-Free Regions of Switzerland – Identification and Quantification of Risk Factors , 2002, Acta veterinaria Scandinavica.

[55]  J. Funk,et al.  Longitudinal study of Salmonella enterica in growing pigs reared in multiple-site swine production systems. , 2001, Veterinary microbiology.

[56]  A. Wingstrand,et al.  Bacteriological and serological examination and risk factor analysis of Salmonella occurrence in sow herds, including risk factors for high Salmonella seroprevalence in receiver finishing herds. , 2001, Berliner und Munchener tierarztliche Wochenschrift.

[57]  P. Wallgren,et al.  Eradication of Salmonella Yoruba in an integrated pig herd. , 2001, Berliner und Munchener tierarztliche Wochenschrift.

[58]  J. M. Roe,et al.  Effects of stressors on immune parameters and on the faecal shedding of enterotoxigenic Escherichia coli in piglets following experimental inoculation. , 2001, Research in veterinary science.

[59]  B. B. Jensen,et al.  Effect of pelleting and use of lactic acid in feed on Salmonella prevalence and productivity in weaners , 2001 .

[60]  J. Dahl,et al.  Effect on Salmonella prevalence by feeding sows meal or pelleted feed. , 2001 .

[61]  E. Eveno,et al.  Development of a complete ELISA using Salmonella lipopolysaccharides of various serogroups allowing to detect all infected pigs. , 2000, Veterinary research.

[62]  M. Jenkins,et al.  Serovar Typhimurium Enterica Salmonella Virulent but Not Attenuated Antibody Is Required for Protection Against , 2000 .

[63]  S. Kaufmann,et al.  Immune response to infection with Salmonella typhimurium in mice , 2000, Journal of leukocyte biology.

[64]  J. Funk,et al.  Fecal shedding of Salmonella by gilts before and after introduction to a swine breeding farm , 2000 .

[65]  S. Messier,et al.  Assessment of various treatments to reduce carriage of Salmonella in swine. , 2000, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[66]  S. Messier,et al.  Distribution of Salmonella in swine herds in Québec. , 1999, Veterinary microbiology.

[67]  R. Harvey,et al.  Effect of competitive exclusion treatment on colonization of early-weaned pigs by Salmonella serovar Choleraesuis , 1999 .

[68]  R. Harvey,et al.  Experimental and natural infection of early weaned pigs with Salmonella choleraesuis. , 1998, Research in veterinary science.

[69]  M. Chengappa,et al.  Preventing Salmonella infection in pigs with offsite weaning , 1998 .

[70]  D. Baggesen,et al.  Elimination of Salmonella typhimurium infection by the strategic movement of pigs , 1997, Veterinary Record.

[71]  P. Siba,et al.  The incidence of swine dysentery in pigs can be reduced by feeding diets that limit the amount of fermentable substrate entering the large intestine. , 1996, The Journal of nutrition.

[72]  B. R. Berends,et al.  Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. , 1996, Journal of food microbiology.

[73]  M. Tokach,et al.  Growth and microbial flora of nonmedicated, segregated, early weaned pigs from a commercial swine operation. , 1996, Journal of the American Veterinary Medical Association.

[74]  P. Fedorka-Cray,et al.  Natural transmission of Salmonella choleraesuis in swine , 1996, Applied and environmental microbiology.

[75]  D. Baggesen,et al.  The serological response to Salmonella serovars typhimurium and infantis in experimentally infected pigs. The time course followed with an indirect anti-LPS ELISA and bacteriological examinations. , 1995, Veterinary microbiology.

[76]  H. A. Vahl,et al.  A survey of the incidence of Salmonella species and Enterobacteriaceae in poultry feeds and feed components , 1995, Veterinary Record.

[77]  E. Telemo,et al.  Effect of early weaning on the development of immune cells in the pig small intestine. , 1995, Veterinary immunology and immunopathology.

[78]  M. Tokach,et al.  Evaluation of segregated early weaning to control salmonellosis and proliferative enteritis. , 1995 .

[79]  R. Isaacson,et al.  Transmission of Salmonella typhimurium to swine. , 1994, Veterinary microbiology.

[80]  J. Lumsden,et al.  Immune response of pigs to parenteral vaccination with an aromatic-dependent mutant of Salmonella typhimurium. , 1992, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[81]  R. Rose,et al.  Populations of Salmonella typhimurium in internal organs of experimentally infected carrier swine. , 1992, American journal of veterinary research.

[82]  Wilkie Bn,et al.  Resistance to fecal shedding of salmonellae in pigs and chickens vaccinated with an aromatic-dependent mutant of Salmonella typhimurium. , 1991 .

[83]  R. Rose,et al.  Experimental establishment of persistent infection in swine with a zoonotic strain of Salmonella newport. , 1991, American journal of veterinary research.

[84]  M. Tokach,et al.  Kansas State University Swine Day 1999. Report of Progress 841. , 1991 .

[85]  J. Lumsden,et al.  Resistance to fecal shedding of salmonellae in pigs and chickens vaccinated with an aromatic-dependent mutant of Salmonella typhimurium. , 1991, American journal of veterinary research.

[86]  A. Pospischil,et al.  Distribution of persistent Salmonella typhimurium infection in internal organs of swine. , 1989, American journal of veterinary research.

[87]  H. L. Thacker,et al.  Studies on the pathogenesis of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf infection in weanling pigs. , 1986, American journal of veterinary research.

[88]  H. L. Thacker,et al.  Studies on the pathogenesis of Salmonella heidelberg infection in weanling pigs. , 1985, American journal of veterinary research.

[89]  A. Lindberg,et al.  Salmonella typhimurium infection in calves: cell-mediated and humoral immune reactions before and after challenge with live virulent bacteria in calves given live or inactivated vaccines , 1983, Infection and immunity.

[90]  A. Lindberg,et al.  Salmonella typhimurium infection in calves: protection and survival of virulent challenge bacteria after immunization with live or inactivated vaccines , 1983, Infection and immunity.

[91]  D. Williams,et al.  Observations on the occurrence of Salmonella cholerae-suis and other salmonellas in two herds of feeder pigs , 1981, Journal of Hygiene.

[92]  G. Boon,et al.  Medicated early weaning to obtain pigs free from pathogens endemic in the herd of origin , 1980, Veterinary Record.

[93]  P. Vanderwal.  Salmonella Control of Feedstuffs by Pelleting or Acid Treatment , 1979 .

[94]  W. R. Mitchell,et al.  Salmonella investigation in an Ontario feed mill. , 1978, Canadian journal of comparative medicine : Revue canadienne de medecine comparee.

[95]  F. J. Bourne.  Humoral immunity in the pig , 1976, Veterinary Record.

[96]  F. J. Bourne.  The immunoglobulin system of the suckling pig , 1973, Proceedings of the Nutrition Society.

[97]  G. Tullock,et al.  Competitive Exclusion. , 1960, Science.

[98]  K. Newell,et al.  Salmonellosis in Northern Ireland, with special reference to pigs and salmonella-contaminated pig meal , 1959, Journal of Hygiene.

[99]  金潤,et al.  SALMONELLOSIS , 1974 .