Skip to main content

Advertisement

Log in

Cultural and Immunological Detection Methods for Salmonella spp. in Animal Feeds – A Review

  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Food-borne salmonellosis continues to be a major public health concern, and contamination with Salmonella spp. in pre-harvest animal production is considered a primary contributor to this problem. Animal feeds can easily become contaminated during primary production, feed mixing and processing as well as during feeding. Consequently, monitoring and surveillance of feeds and feed ingredients for Salmonella spp. contamination may be useful or necessary in the prevention and control of this organism. Cultural and immunological detection methods for salmonellae have been used or suggested as possible approaches for use in animal feeds. Cultural methods remain advantageous owing to their ability to detect viable bacterial cells, while immunological methods have the capability of detecting nonculturable bacterial cells. Advancements and improvements in both methodologies offer opportunities for eventual routine use of these detection technologies in animal feed assays.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

cfu:

colony-forming unit(s)

ELISA:

enzyme-linked immunosorbent assay

FDA:

US Food and Drug Administration

FSIS:

USDA Food Safety and Inspection Service

BG:

Brilliant green

HE:

Hektoen enteric

IgM:

immunoglobulin M

IMS:

immunomagnetic separation

MSRV:

modified semisolid RV

S.:

Salmonella

SC:

selenite cystine

RV:

Rappaport–Vassiliadis

TSA:

tryptic soy agar

TT:

tetrathionate

USDA:

US Department of Agriculture

XLD:

xylose lysine desoxycholate

References

  • Andrews, W.H., June, G.A., Sherrod, P.S., Hammack, T.S. and Amaguaña, R.M., 1995. Salmonella. In: Bacteriological Analytical Manual, 8th edn, (AOAC International, Gaithersburg, MD), 5.01–5.20

  • Angulo, F.J. and Swerdlow, D.L., 1998. Salmonella enteritidis infections in the United States. Journal of the Applied Veterinary Medicine Association, 213, 1729–1731

    CAS  Google Scholar 

  • Bäumler, A.J., Tsolis, R.M. and Heffron, F., 2000. Virulence mechanisms of Salmonella and their genetic basis. In: C. Wray and A. Wray (eds), Salmonella in Domestic Animals, (CAB International, Wallingford, UK), 52–57

  • Baylis, C.L., MacPhee, S. and Betts, R.P., 2000. Comparison of methods for the recovery and detection of low levels of injured Salmonella in ice cream and milk powder. Letters in Applied Microbiology, 30, 320–324;

    Article  PubMed  CAS  Google Scholar 

  • Bennett, A.R., MacPhee, S., Betts, R. and Post, D., 1999. Use of pyrrolidonyl peptidase to distinguish Citrobacter from Salmonella. Letters in Applied Microbiology, 28, 175–178

    Article  PubMed  CAS  Google Scholar 

  • Blais, B.W., Pietrzak, E., Oudit, D., Wilson, C., Phillippe, L.M. and Howlett, J., 1998. Polymacron enzyme immunoassay system for detection of naturally contaminating Salmonella in foods, feeds, and environmental studies. Journal of Food Protection, 61, 1187–1190

    PubMed  CAS  Google Scholar 

  • Bolton, F.J., Fritz, E. and Poynton, S., 2000. Rapid enzyme-linked immunoassay for detection of Salmonella in food and feed products: performance testing program. Journal of AOAC International, 83, 299–303

    PubMed  CAS  Google Scholar 

  • Braun, C., Kostka, V., Balks, E., Redmann, T. and Helmuth, R., 1998. Short communication: comparative studies of diagnostic bacteriological methods for the recovery of Salmonella from faecal samples from flocks of layers. Journal of Veterinary Medicine B, 45, 245–250

    Article  PubMed  CAS  Google Scholar 

  • Coleman, D.J., Chick, K.E. and Nye, K.J., 1995a. An evaluation of immunomagnetic separation for the detection of salmonellas in raw chicken carcasses. Letters in Applied Microbiology, 21, 152–154

    CAS  Google Scholar 

  • Coleman, D.J., Nye, K.J., Chick, K.E. and Gagg, C.M., 1995b. A comparison of immunomagnetic separation plus enrichment with conventional salmonella culture in the examination of raw sausages. Letters in Applied Microbiology 21, 249–251

    CAS  Google Scholar 

  • Cox, N.A., 1988. Salmonella methodology update. Poultry Science, 67, 921–927

    PubMed  CAS  Google Scholar 

  • Cross, J.H., George, R.H., Booth, I.W. and Mayne, A.J., 1989. Life-threatening Salmonella enteritidis phage type 4 gastroenteritis in infancy. Lancet, 8638, 625–626

    Google Scholar 

  • Cudjoe, K.S. and Krona, R., 1997. Detection of Salmonella from raw food samples using Dynabeads anti-Salmonella and a conventional reference method. International Journal of Food Microbiology, 37, 55–62

    Article  PubMed  CAS  Google Scholar 

  • de Boer, E., 1998. Update on media for isolation of Enterobacteriaceae from foods. International Journal of Food Microbiology, 45, 43–53

    Article  PubMed  CAS  Google Scholar 

  • Devenish, J.A., Ciebin, B.W. and Brodsky, M.H., 1986. Novobiocin-brilliant green-glucose agar: new medium for isolation of salmonellae. Applied and Environmental Microbiology, 52, 539–545

    PubMed  CAS  Google Scholar 

  • Dill, K., Stanker, L.H. and Young, C.R., 1999. Detection of Salmonella in poultry using a silicon chip-based sensor. Journal of Biochemical and Biophysical Methods, 41, 61–67

    Article  PubMed  CAS  Google Scholar 

  • Ezaki, T., Kawamura, Y. and Yabuuchi, E., 2000. Recognition of nomenclatural standing of Salmonella typhi (Approved Lists 1980), Salmonella enteritidis (Approved Lists 1980) and Salmonella typhimurium (Approved Lists 1980), and conservation of the specific epithets enteritidis and typhimurium. International Journal of Systematic and Evolutionary Microbiology, 50, 945–947

    PubMed  Google Scholar 

  • Gaillot, O., Di Camillo, P., Berche, P., Courcol, R. and Savage, C., 1999. Comparison of CHROMagar Salmonella medium and Hektoen enteric agar for isolation of Salmonella spp. from stool samples. Journal of Clinical Microbiology, 37, 762–765

    PubMed  CAS  Google Scholar 

  • Gast, R.K., Porter, Jr., R.E. and Holt, P.S., 1997. Applying tests for specific yolk antibodies to predict contamination by Salmonella enteriditis in eggs from experimentally infected lying hens. Avian Diseases, 41, 195–202

    PubMed  CAS  Google Scholar 

  • Gast, R.K. and Holt, P.S., 1998. Application of flagella-based immunoassays for serologic detection of Salmonella pullorum infection in chickens. Avian Diseases, 42, 807–811

    PubMed  CAS  Google Scholar 

  • Gomez, J.R., Salinas, I.L., Salmerón, J.P., Cordoba, E.S. and Campos, L.M., 1998. Evaluation of methods for isolation of Salmonella species using modified semisolid Rappaport–Vassiliadis medium and Salmonella–Shigella agar. European Journal of Clinical Microbiology and Infectious Diseases, 17, 791– 793

    Google Scholar 

  • Gómez-Duarte, O.G., Lucas, B., Yan, Z.-X., Panthel, K., Haas, R. and Meyer, T.F., 1998. Protection of mice against gastric colonization by Helicobacter pylori by single oral dose immunization with attenuated Salmonella typhimurium producing urease subunits A and B. Vaccine, 16, 460–471

    PubMed  Google Scholar 

  • Grimont, P.A.D., Grimont, F. and Bouvet, P., 2000. Taxonomy of the genus Salmonella. In: C. Wray and A. Wray (eds), Salmonella in Domestic Animals, (CAB International, Wallingford, UK), 1–17

  • Guthrie, R.K., 1992. Microbiological methods for detection of Salmonella contamination. In:, (CRC Press, Boca Raton, FL), 131–156

  • Ha, S.D., Pillai, S.D. and Ricke, S.C., 1995a. Growth response of Salmonella spp. to cycloheximide amendment in media. Journal of Rapid Methods and Automation in Microbiology 4, 77–85

    CAS  Google Scholar 

  • Ha, S.D., Pillai, S.D., Maciorowski, K.G. and Ricke, S.C., 1995b. Cycloheximide as a media amendment for enumerating bacterial populations in animal feeds. Journal of Rapid Methods and Automation in Microbiology, 4, 95–105

    CAS  Google Scholar 

  • Hammack, T.S., Amaguaña, R.M., June, G.A., Sherrod, P.S. and Andrews, W.H., 1999. Relative effectiveness of selenite cystine broth, tetrathionate broth, and rappaport-vassiliadis medium for the recovery of Salmonella spp. from foods with a low microbial load. Journal of Food Protection 62, 16–21

    PubMed  CAS  Google Scholar 

  • Heyndrickx, M., Vandekerchove, D., Herman, L., Rollier, I., Grijspeerdt, K. and De Zutter, L., 2002. Routes for salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 129, 253–265

    Article  PubMed  CAS  Google Scholar 

  • Hoffmans, C.M., Fung, D.Y.C. and Kastner, C.L., 1997. Methods and resuscitation environments for the recovery of heat-injured Listeria monocytogenes: a review. Journal of Rapid Methods and Automation in Microbiology, 5, 249–268

    Google Scholar 

  • Huang, H., Garcia, M.M., Brooks, B.W., Nielsen, K. and Ng, S.-P., 1999. Evaluation of culture enrichment procedures for use with Salmonella detection immunoassay. International Journal of Food Microbiology 51, 85–94

    Article  PubMed  CAS  Google Scholar 

  • Jones, F.T. and Ricke, S.C., 1994. Researchers propose tentative HACCP plan for feed mills. Feedstuffs, 66, 32, 36–37

    Google Scholar 

  • Kang, D.-H. and Fung, D.Y.C., 1999. Thin agar layer method for recovery of heat-injured Listeria monocytogenes. Journal of Food Protection 62, 1346–1349

    PubMed  CAS  Google Scholar 

  • Kang, D.-H. and Fung, D.Y.C., 2000. Application of thin agar layer method for recovery of injured Salmonella typhimurium. International Journal of Food Microbiology, 54, 127–32

    Article  PubMed  CAS  Google Scholar 

  • Keith, M., 1997. Evaluation of an automated enzyme-linked fluorescent immunoassay system for the detection of Salmonella in foods. Journal of Food Protection, 60, 682–685.

    Google Scholar 

  • Kim, M.L. and Slauch, J.M., 1999. Effect of acetylation (O-factor 5) on the polyclonal antibody response to Salmonella typhimurium O-antigen. FEMS Immunology and Medical Microbiology, 26, 83–92

    Article  PubMed  CAS  Google Scholar 

  • Lim, P.-L., Tam, F.C.H., Cheong, Y.-M. and Jegathesan, M., 1998. One-step 2-minute test to detect typhoid-specific antibodies based on particle separation in tubes. Journal of Clinical Microbiology, 36, 2271–2278

    PubMed  CAS  Google Scholar 

  • Lucore, L.A., Cullison, M.A. and Jaykus, L.-A., 2000. Immobilization with metal hydroxides as a means to concentrate food-borne bacteria for detection by cultural and molecular methods. Applied and Environmental Microbiology, 66, 1769–1776

    Article  PubMed  CAS  Google Scholar 

  • Mallinson, E.T., Miller, R.G., de Rezende, C.E., Ferris, K.E., deGraft-Hanson, J. and Joseph, S.W., 2000. Improved plating media for the detection of Salmonella species with typical and atypical hydrogen sulfide production. Journal of Veterinary Diagnostic Investigation, 12, 83–87

    PubMed  CAS  Google Scholar 

  • Manafi, M., 2000. New developments in chromogenic and fluorogenic culture media. International Journal of Food Microbiology, 60, 205–218

    Article  PubMed  CAS  Google Scholar 

  • Marriott, I., Hammond, T.G., Thomas, E.K. and Bost, K.L., 1999. Salmonella efficiently enter and survive within cultured CD11c+ dendritic cells initiating cytokine expression. European Journal of Immunology, 29, 1107–1115

    Article  PubMed  CAS  Google Scholar 

  • Massó, R. and Oliva, J, 1997. Technical evaluation of an automated analyser for the detection of Salmonella enterica in fresh meat products. Food Control, 8, 99–103

    Google Scholar 

  • McCleery, D.R. and Rowe, M.T., 1995. Development of a selective plating technique for the recovery of Escherichia coli O157:H7 after heat stress. Letters in Applied Microbiology, 21, 252–256

    PubMed  CAS  Google Scholar 

  • Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V., 1999. Food-related illness and death in the United States. Emerging Infectious Diseases, 5, 607–625

    PubMed  CAS  Google Scholar 

  • Meenakshi, M., Bakshi, C.S., Butchaiah, G., Bansal, M.P., Siddiqui, M.Z. and Singh, V.P., 1999. Adjuvanted outer membrane protein vaccine protects poultry against infection with Salmonella enteriditis. Veterinary Research Communications, 23, 81–90

    Article  PubMed  CAS  Google Scholar 

  • Micklewright, I.J. and Sartory, D.P., 1995. Evaluation of the BBL crystal enteric/nonfermenter kit for the identification of water-derived environmental Enterobacteriaceae. Letters in Applied Microbiology, 21, 160–163

    PubMed  CAS  Google Scholar 

  • Miller, R.G. and Mallinson, E.T., 2000. Improved detection of nontyphoid and typhoid Salmonella spp. with balanced agar formulations. Journal of Food Protection, 63, 1443–1446

    PubMed  CAS  Google Scholar 

  • Peng, H. and Shelef, L.A., 1999. Automated rapid screening of foods for the presence of Salmonella spp. Journal of Food Protection, 62, 1341–1345

    PubMed  CAS  Google Scholar 

  • Peplow, M.O., Correa-Prisant, M., Stebbins, M.E., Jones, F. and Davies, P., 1999. Sensitivity, specificity, and predictive values of three Salmonella rapid detection kits using fresh and frozen poultry environmental samples versus those of standard plating. Applied and Environmental Microbiology, 65, 1055–1060

    PubMed  CAS  Google Scholar 

  • Perry, J.D., Ford, M., Taylor, J., Jones, A.L., Freeman, R. and Gould, F.K., 1999. ABC medium, a new chromogenic agar for selective isolation of Salmonella spp. Journal of Clinical Microbiology, 37, 766–768

    PubMed  CAS  Google Scholar 

  • Poppe, C., Mann, E.D., Shaw, S., Warburton, D. and Sewell, A, 2004. Procedure for the isolation of Salmonella species by the modified semi-solid Rappaport Vassiliadis (MSRV) method. Laboratory Procedure MFLP-75, (Health Canada, Health Products and Food Branch. June 15, 2004)

  • Reeves, M.W., Evins, G.M., Heiba, A.A., Plikaytis, B.D. and Farmer III, J.J., 1989. Clonal nature of Salmonella typhi and its genetic relatedness to other Salmonella spp. as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. Journal of Clinical Microbiology, 27, 313–320

    PubMed  CAS  Google Scholar 

  • Restaino, L., Grauman, G.S., McCall, W.A. and Hill, W.M., 1977. Effects of varying concentrations of novobiocin incorporated into two Salmonella plating media on the recovery of four Enterobacteriaceae. Applied and Environmental Microbiology, 33, 585–589

    PubMed  CAS  Google Scholar 

  • Ricke, S.C., Pillai, S.D., Norton, R.A., Maciorowski, K.G. and Jones, F.T., 1998. Applicability of rapid methods for detection of Salmonella spp. in poultry feeds: a review. Journal of Rapid Methods and Automation in Microbiology, 6, 239–258

    Google Scholar 

  • Ricke, S.C. and Pillai, S.D., 1999. Conventional and molecular methods for understanding probiotic bacteria functionality in gastrointestinal tracts. Critical Reviews in Microbiology 25, 19–38

    Article  PubMed  CAS  Google Scholar 

  • Rijpens, N., Herman, L., Vereecken, F., Jannes, G., De Smedt, J. and De Zutter, L., 1999. Rapid detection of stressed Salmonella spp. in dairy and egg products using immunomagnetic separation and PCR. International Journal of Food Microbiology, 46, 37–44

    Article  PubMed  CAS  Google Scholar 

  • Ripabelli, G., Sammarco, M.L. and Grasso, G.M., 1999. Evaluation of immunomagnetic separation and plating media for recovery of Salmonella from meat. Journal of Food Protection, 62, 198–201

    PubMed  CAS  Google Scholar 

  • Roberts, T., 1988. Salmonellosis control: estimated economic costs. Poultry Science, 67, 936–943

    PubMed  CAS  Google Scholar 

  • Rose, B.E., 1998. Isolation and identification of Salmonella from meat, poultry, and egg products. In: USDA/FSIS Microbiology Laboratory Guidebook, 3rd edn, (Office of Public Health and Science, Microbial Division, US Department of Agriculture, Washington, DC)

  • Shaw, S.J., Blais, B.W. and Nundy, D.C., 1998. Performance of the Dynabeads anti-Salmonella system in the detection of Salmonella species in foods, animal feeds, and environmental samples. Journal of Food Protection, 61, 1507–1510.

    PubMed  CAS  Google Scholar 

  • Shelef, L.A. and Tan, W., 1998. Automated detection of hydrogen sulfide release from thiosulfate by Salmonella spp. Journal of Food Protection, 61, 620–622

    PubMed  CAS  Google Scholar 

  • Smith, J.L., 1994. Arthritis and foodborne bacteria. Journal of Food Protection, 57, 935–941

    Google Scholar 

  • Tauxe, R.V., 1991. Salmonella: a postmodern pathogen. Journal of Food Protection, 54, 563–568

    Google Scholar 

  • Ten Bosch, C., Van der Plas, J., Havekes, M., Geurts, J., van der Palen, C., Huis in 'T Veld, J.H.J. and Hofstra, H., 1992. Salmonella PCR: implementation of a screening method in meat and meat products. In: Reports and Communications: Salmonella and Salmonellosis, (Ploufragan, Saint-Brieuc, France)

  • Uyttendaele, M., Vanwildemeersch, K. and Debevere, J., 2003. Evaluation of real-time PCR vs automated ELISA and a conventional culture method using a semi-solid medium for detection of Salmonella. Letters in Applied Microbiology, 37, 386–391

    Article  PubMed  CAS  Google Scholar 

  • Weenk, G.H., 1992. Microbiological assessment of culture media: comparison and statistical evaluation of methods. International Journal of Food Microbiology, 17, 159–181

    PubMed  CAS  Google Scholar 

  • Westerman, R.B., He, Y., Keen, J.E., Littledike, E.T. and Kwang, J., 1997. Production and characterization of monoclonal antibodies specific for the lipopolysaccharide of Escherichia coli O157. Journal of Clinical Microbiology, 35, 679–684

    PubMed  CAS  Google Scholar 

  • Williams, J.E., 1981a. Salmonellas in poultry feeds – a worldwide review. Part I: Introduction. World's Poultry Science Journal, 37, 6–19

    Google Scholar 

  • Williams, J.E., 1981b. Salmonellas in poultry feeds – a worldwide review. Part II: Methods in isolation and identification. World's Poultry Science Journal, 37, 19–25

    Google Scholar 

  • Williams, J.E., 1981c. Salmonellas in poultry feeds – a worldwide review. Part III. Methods in control and elimination. World's Poultry Science Journal, 37, 97–105

    Google Scholar 

  • Withanage, G.S.K., Sasai, K., Fukata, T., Miyamoto, T. and Baba, E., 1999. Secretion of Salmonella-specific antibodies in the oviducts of hens experimentally infected with Salmonella enteriditis. Veterinary Immunology and Immunopathology, 67, 185–193

    Article  PubMed  CAS  Google Scholar 

  • Wiuff, C., Jauho, E.S., Stryhn, H., Andresen, L.O., Thaulov, K., Boas, U., Jakobsen, M.H. and Heegaard, P.M.H., 2000. Evaluation of a novel enzyme-linked immunosorbent assay for detection of antibodies against Salmonella, employing a stable coating of lipopolysaccharide-derived antigens covalently attached to polystyrene microwells. Journal of Veterinary Diagnostic Investigation, 12, 130–135

    PubMed  CAS  Google Scholar 

  • Zamora, B.M., Hartung, M. and Hildebrandt, G. 1999a. Simplified preparation of a specific S. enteritidis antigen for ELISA and other immunological techniques. Journal of Veterinary Medicine B, 46, 1–7

    CAS  Google Scholar 

  • Zamora, B.M., Hartung, M., Hildebrandt, G. and Käsbohrer, W., 1999b. Detection of antibodies to S. enteritidis in broilers by means of indirect ELISA and chemiluminescent immunoassay (CLIA). Journal of Veterinary Medicine B, 46, 9–23

    CAS  Google Scholar 

  • Ziprin, R.L., 1994. Salmonella. In: Y.H. Hui, J.R. Gorham, K.D. Murrell and D.O. Cliver (eds), Foodborne Disease Handbook: Diseases Caused by Bacteria, vol. 1, (Marcel Dekker, New York)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. C. Ricke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maciorowski, K.G., Herrera, P., Jones, F.T. et al. Cultural and Immunological Detection Methods for Salmonella spp. in Animal Feeds – A Review. Vet Res Commun 30, 127–137 (2006). https://doi.org/10.1007/s11259-006-3221-8

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-006-3221-8

Keywords

Navigation