Detection and Isolation of Salmonella spp. in Animal Feeds from 2007-2011

Authors

  • Yi-Cheng Hsieh Office of the Texas State Chemist Texas A&M AgriLife Research
  • Kyung-Min Lee Office of the Texas State Chemist, Texas A&M AgriLife Research, Texas A&M University System, College Station, TX 77843, USA
  • Toni Poole Southern Plains Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, College Station, TX 77845 USA
  • Mick Runyon Office of the Texas State Chemist, Texas A&M AgriLife Research, Texas A&M University System, College Station, TX 77843, USA
  • Ben Jones
  • Timothy J Herrman Office of the Texas State Chemist, Texas A&M AgriLife Research, Texas A&M University System, College Station, TX 77843, USA

DOI:

https://doi.org/10.21423/JRS.REGSCI.2113

Keywords:

Salmonella, Animal feed, Food illness, Pathogen detection, Surveillance

Abstract

Salmonella species (spp.) are zoonotic pathogens that contaminate animal ingredients and finished feed and represent a significant hazard as identified by the Codex Animal Feed Taskforce. The United States (US) Food and Drug Administration (FDA) promulgated regulations prohibiting Salmonella contamination in feed and has since published a draft guidance document expressing their current strategy involving regulatory oversight of Salmonella contamination in feed. The Office of the Texas State Chemist (OTSC) initiated the broad surveillance of Salmonella spp. in 2007 in response of a Salmonella enterica serotype Typhimurium outbreak in frozen rodents, which are subject to the agency’s regulatory oversight as defined by the Texas Commercial Feed Control Act. From calendar years of 2007-2011, 2622 total feed samples were collected and subsequently evaluated for Salmonella contamination using multiple first-line methods, the accuracy of which was assessed with DNA-based polymerase chain reaction (PCR) and automated immunoanalysis. Three hundred and five out of 2622 tested samples with 78 different serotypes were identified as Salmonella-contaminated products. Results also indicated a steady increase in Salmonella incidence, along with a corresponding increase in Salmonella isolate and serotype diversity since 2007. This prevalence of Salmonella-contaminated feed stocks presents a potential risk to public health.

References

Akoachere J.F., Tanih N.F., Ndip L.M. and Ndip R.N. (2009). Phenotypic characterization of Salmonella typhimurium isolates from food-animals and abattoir drains in Buea, Cameroon. J Health Popul Nutr, 27, 612-8.

Aldridge K.E. and Hodges R.L. (1981). Correlation studies of entero-set 20, API 20E and conventional media systems for Enterobacteriaceae identification. J Clin Microbiol, 13, 120-5.

APHL. (2013). Disease Surveillance National Molecular Subtyping Network for Foodborne Pathogens. Pulsenet Disease Surveillance, 1-8.

Barton M.D. (2000). Antibiotic use in animal feed and its impact on human health. Nutrition Research Reviews, 13, 279-299.

Behravesh C.B., Ferraro A., Deasy M., 3rd, Dato V., Moll M., Sandt C., Rea N.K., Rickert R., Marriott C., Warren K., Urdaneta V., Salehi E., Villamil E., Ayers T., Hoekstra R.M., Austin J.L., Ostroff S. and Williams I.T. (2010).

Human Salmonella infections linked to contaminated dry dog and cat food, 2006-2008. Pediatrics, 126, 477-83.

Bird C.B., Miller R.L. and Miller B.M. (1999). Reveal for Salmonella test system. J AOAC Int, 82, 625-33.

Blackburn C.W. and McCarthy J.D. (2000). Modifications to methods for the enumeration and detection of injured Escherichia coli O157:H7 in foods. Int J Food Microbiol, 55, 285-90.

Blossom D., Noble-Wang J., Su J., Pur S., Chemaly R., Shams A., Jensen B., Pascoe N., Gullion J., Casey E., Hayden M., Arduino M., Budnitz D.S., Raad I., Trenholme G. and Srinivasan A. (2009). Multistate outbreak of Serratia marcescens bloodstream infections caused by contamination of prefilled heparin and isotonic sodium chloride solution syringes. Arch Intern Med, 169, 1705-11.

Bowen A.B., Kile J.C., Otto C., Kazerouni N., Austin C., Blount B.C., Wong H.N., Beach M.J. and Fry A.M. (2007). Outbreaks of short-incubation ocular and respiratory illness following exposure to indoor swimming pools. Environ Health Perspect, 115, 267-71.

Braden C.R. (2006). Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis, 43, 512-7.

Butler D.A., Lobregat C.M. and Gavan T.L. (1975). Reproducibility of Analytab (Api 20e) System. J Clin Microbiol, 2, 322-326.

Carattoli A., Bertini A., Villa L., Falbo V., Hopkins K.L. and Threlfall E.J. (2005). Identification of plasmids by PCR-based replicon typing. J Microbiol Meth, 63, 219-228.

Cheung P.Y., Kwok K.K. and Kam K.M. (2007). Application of BAX system, Tecra Unique Salmonella test, and a conventional culture method for the detection of Salmonella in ready-to-eat and raw foods. J Appl Microbiol, 103, 219-27.

Crump J.A., Griffin P.M. and Angulo F.J. (2002). Bacterial contamination of animal feed and its relationship to human foodborne illness. Clinical Infectious Diseases, 35, 859-865.

D'Aoust J.Y., Pagotto F., Akhtar M., Bussey J., Cooper C., McDonald C., Meymandy M. and Tyler K. (2007). Evaluation of the BAX gel and fluorometric systems for the detection of foodborne Salmonella. J Food Prot, 70, 835-40.

Doyle T.J., Stark L., Hammond R. and Hopkins R.S. (2009). Outbreaks of noroviral gastroenteritis in Florida, 2006-2007. Epidemiol Infect, 137, 617-25.

Eriksson E. and Aspan A. (2007). Comparison of culture, ELISA and PCR techniques for salmonella detection in faecal samples for cattle, pig and poultry. BMC Vet Res, 3, 21.

FDA. (2009a). FDA Food Safety Modernization Act. 124 STAT. 3885-3973.

FDA. (2009b). SEC. 105. STANDARDS FOR PRODUCE SAFETY. FDA Food Safety Modernization Act, 124 STAT. 3899-3905.

FDA. (2009c). SEC. 108. National Agriculture and Food Defense Strategy.

FDA Food Safety Modernization Act, 124 STAT. 3910-3912.

FDA. (2013). Archive for Recalls, Market Withdrawals & Safety Alerts. Retrieved from http://www.fda.gov/Safety/Recalls/ArchiveRecalls/default.htm.

Goldman E. (2004). Antibiotic abuse in animal agriculture: Exacerbating drug resistance in human pathogens. Hum Ecol Risk Assess, 10, 121-134.

Gupta S.K., Nalluswami K., Snider C., Perch M., Balasegaram M., Burmeister D., Lockett J., Sandt C., Hoekstra R.M. and Montgomery S. (2007). Outbreak of Salmonella Braenderup infections associated with Roma tomatoes, northeastern United States, 2004: a useful method for subtyping exposures in field investigations. Epidemiol Infect, 135, 1165-73.

Harris J.R., Bergmire-Sweat D., Schlegel J.H., Winpisinger K.A., Klos R.F., Perry C., Tauxe R.V. and Sotir M.J. (2009). Multistate outbreak of Salmonella infections associated with small turtle exposure, 2007-2008. Pediatrics, 124, 1388-94.

Harris J.R., Neil K.P., Behravesh C.B., Sotir M.J. and Angulo F.J. (2010). Recent multistate outbreaks of human salmonella infections acquired from turtles: a continuing public health challenge. Clin Infect Dis, 50, 554-9.

Harrison T.M., Harrison S.H., Rumbeiha W.K., Sikarskie J. and McClean M. (2006). Surveillance for selected bacterial and toxicologic contaminants in donated carcass meat fed to carnivores. J Zoo Wildl Med, 37, 102-7.

Herrman T.J., Langemeier M.R. and Frederking M. (2007). Development and implementation of hazard analysis and critical control point plans by several U.S. feed manufacturers. J Food Prot, 70, 2819-23.

Hinton M.H. (2000). Infections and intoxications associated with animal feed and forage which may present a hazard to human health. Veterinary Journal, 159, 124-138.

Hochhut B., Jahreis K., Lengeler J.W. and Schmid K. (1997). CTnscr94, a conjugative transposon found in enterobacteria. Journal of Bacteriology, 179, 2097-2102.

Inatsu Y., Bari M.L., Kawasaki S. and Isshiki K. (2004). Survival of Escherichia coli O157:H7, Salmonella enteritidis, Staphylococcus aureus, and Listeria monocytogenes in Kimchi. J Food Prot, 67, 1497-500.

Johnson R., Mills J. and Colon-Reveles J. (2009). VIDAS Salmonella (SLM) assay method EasySLM with ChromID Salmonella (SM2) Agar. Performance Tested Method 020901. J Aoac Int, 92, 1861-4.

Kearney T.E., Larkin M.J., Frost J.P. and Levett P.N. (1993). Survival of pathogenic bacteria during mesophilic anaerobic digestion of animal waste. J Appl Bacteriol, 75, 215-9.

Kim J. and Jiang X. (2010). The growth potential of Escherichia coli O157:H7, Salmonella spp. and Listeria monocytogenes in dairy manure-based compost in a greenhouse setting under different seasons. J Appl Microbiol, 109, 2095-104.

Knight M.T., Wood D.W., Black J.F., Gosney G., Rigney R.O., Agin J.R., Gravens C.K. and Farnham S.M. (1990). Gram-negative identification card for identification of Salmonella, Escherichia coli, and other Enterobacteriaceae isolated from foods: collaborative study. J Assoc Off Anal Chem, 73, 729-33.

Koyuncu S., Andersson M.G. and Haggblom P. (2010). Accuracy and sensitivity of commercial PCR-based methods for detection of Salmonella enterica in feed. Appl Environ Microbiol, 76, 2815-22.

Lang M.M., Harris L.J. and Beuchat L.R. (2004). Survival and recovery of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes on lettuce and parsley as affected by method of inoculation, time between inoculation and analysis, and treatment with chlorinated water. J Food Prot, 67, 1092-103.

Lee K.M., McReynolds J.L., Fuller C.C., Jones B., Herrman T.J., Byrd J.A. and Runyon M. (2008). Investigation and characterization of the frozen feeder rodent industry in Texas following a multi-state Salmonella Typhimurium outbreak associated with frozen vacuum-packed rodents. Zoonoses Public Health, 55, 488-96.

Li A., Zhang H., Zhang X., Wang Q., Tian J., Li Y. and Li J. (2010). Rapid separation and immunoassay for low levels of Salmonella in foods using magnetosome-antibody complex and real-time fluorescence quantitative PCR. J Sep Sci, 33, 3437-43.

Li X., Bethune L.A., Jia Y., Lovell R.A., Proescholdt T.A., Benz S.A., Schell T.C., Kaplan G. and McChesney D.G. (2012). Surveillance of Salmonella Prevalence in Animal Feeds and Characterization of the Salmonella Isolates by Serotyping and Antimicrobial Susceptibility. Foodborne Pathogens and Disease, 9, 692-698.

Loharikar A., Briere E., Schwensohn C., Weninger S., Wagendorf J., Scheftel J., Garvey A., Warren K., Villamil E., Rudroff J.A., Kurkjian K., Levine S., Colby K., Morrison B., May A., Anderson S., Daly E., Marsden-Haug N., Erdman M.M., Gomez T., Rhorer A., Castleman J., Adams J.K., Theobald L., Lafon P., Trees E., Mitchell J., Sotir M.J. and Behravesh C.B. (2012). Four Multistate Outbreaks of Human Salmonella Infections Associated with Live Poultry Contact, United States, 2009. Zoonoses Public Hlth, 59, 347-354.

McMahon W.A., Schultz A.M. and Johnson R.L. (2004). Evaluation of VIDAS Immuno-Concentration Salmonella (ICS) plus selective plate method (Hektoen enteric, bismuth sulfite, Salmonella identification) for detection of Salmonella in selected foods (Method Modification 2001.07): collaborative study. J Aoac Int, 87, 380-4.

Medus C., Smith K.E., Bender J.B., Besser J.M. and Hedberg C.W. (2006). Salmonella outbreaks in restaurants in Minnesota, 1995 through 2003: evaluation of the role of infected foodworkers. J Food Prot, 69, 1870-8.

Mody R.K., Greene S.A., Gaul L., Sever A., Pichette S., Zambrana I., Dang T., Gass A., Wood R., Herman K., Cantwell L.B., Falkenhorst G., Wannemuehler K., Hoekstra R.M., McCullum I., Cone A., Franklin L., Austin J., Delea K., Behravesh C.B., Sodha S.V., Yee J.C., Emanuel B., Al-Khaldi S.F., Jefferson V., Williams I.T., Griffin P.M. and Swerdlow D.L. (2011). National outbreak of Salmonella serotype saintpaul infections: importance of Texas restaurant investigations in implicating jalapeno peppers. PLoS One, 6, e16579.

Murray P.R. (1978). Standardization of Analytab Enteric (Api-20e) System to Increase Accuracy and Reproducibility of Test for Biotype Characterization of Bacteria. J Clin Microbiol, 8, 46-49.

Nicholson F.A., Groves S.J. and Chambers B.J. (2005). Pathogen survival during livestock manure storage and following land application. Bioresour Technol, 96, 135-43.

Oliveira M., Usall J., Vinas I., Solsona C. and Abadias M. (2011). Transfer of Listeria innocua from contaminated compost and irrigation water to lettuce leaves. Food Microbiol, 28, 590-6.

Olson E.D. (2011). Protecting food safety: more needs to be done to keep pace with scientific advances and the changing food supply. Health Aff (Millwood), 30, 915-23.

Oosterom J. (1991). Epidemiologic Studies and Proposed Preventive Measures in the Fight against Human Salmonellosis. International Journal of Food Microbiology, 12, 41-52.

Perry H.N., McDonnell S.M., Alemu W., Nsubuga P., Chungong S., Otten M.W., Jr., Lusamba-dikassa P.S. and Thacker S.B. (2007). Planning an integrated disease surveillance and response system: a matrix of skills and activities. BMC Med, 5, 24.

Silbernagel K., Jechorek R., Carver C., Barbour W.M. and Mrozinski P. (2003). Evaluation of the BAX system for detection of Salmonella in selected foods: collaborative study. J AOAC Int, 86, 1149-59.

Skjerve E. and Olsvik O. (1991). Immunomagnetic separation of Salmonella from foods. Int J Food Microbiol, 14, 11-7.

Smith K.E., Medus C., Meyer S.D., Boxrud D.J., Leano F., Hedberg C.W., Elfering K., Braymen C., Bender J.B. and Danila R.N. (2008). Outbreaks of salmonellosis in Minnesota (1998 through 2006) associated with frozen, microwaveable, breaded, stuffed chicken products. J Food Prot, 71, 2153-60.

Sotir M.J., Ewald G., Kimura A.C., Higa J.I., Sheth A., Troppy S., Meyer S., Hoekstra R.M., Austin J., Archer J., Spayne M., Daly E.R. and Griffin P.M. (2009). Outbreak of Salmonella Wandsworth and Typhimurium infections in infants and toddlers traced to a commercial vegetable-coated snack food. Pediatr Infect Dis J, 28, 1041-6.

Swanson E.C. and Collins M.T. (1980). Use of the API 20E system to identify veterinary Enterobacteriaceae. J Clin Microbiol, 12, 10-4.

Swanson S.J., Snider C., Braden C.R., Boxrud D., Wunschmann A., Rudroff J.A., Lockett J. and Smith K.E. (2007). Multidrug-resistant Salmonella enterica serotype typhimurium associated with pet rodents. New Engl J Med, 356, 21-28.

Tate J.E., Bunning M.L., Lott L., Lu X., Su J., Metzgar D., Brosch L., Panozzo C.A., Marconi V.C., Faix D.J., Prill M., Johnson B., Erdman D.D., Fonseca V., Anderson L.J. and Widdowson M.A. (2009). Outbreak of severe respiratory disease associated with emergent human adenovirus serotype 14 at a US air force training facility in 2007. J Infect Dis, 199, 1419-26.

Taylor M.R. (2011). Will the Food Safety Modernization Act Help Prevent Outbreaks of Foodborne Illness? New England Journal of Medicine, 365:e18.

Tice G., Andaloro B., Fallon D. and Wallace F.M. (2009). DuPont Qualicon BAX System polymerase chain reaction assay. Performance Tested Method 100201. J Aoac Int, 92, 1902-5.

Ukita M. and Prasertsan P. (2002). Present state of food and feed cycle and accompanying issues around Japan. Water Sci Technol, 45, 13-21.

Downloads

Published

2014-12-19

Issue

Section

Scientific Articles

Most read articles by the same author(s)

1 2 > >>