Skip to main content
Log in

Herd- and individual-level prevalences of and risk factors for Salmonella spp. fecal shedding in dairy farms in Al-Dhulail Valley, Jordan

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Salmonellosis is an important disease frequently associated with diarrhea in calves. From January to September 2009, a cross-sectional study involving 91 dairy farms was conducted to determine the prevalence of Salmonella spp. infection in cattle in Al-Dhulail Valley, Jordan. A total of 910 calve and cow fecal samples were collected. Information on farm management practices was obtained through personal interviews using a standardized questionnaire and was tested as risk factors for Salmonella spp. positivity in farms by using logistic regression analysis. Standard conventional methods for Salmonella isolation and serotyping were used, and the disk agar diffusion test was used for antimicrobial testing. The herd-level prevalence of Salmonella spp. in calves, cows, and dairy farms was 12, 12, and 23 %, respectively, and the individual-level prevalence was 4 % for calves, cows, and dairy farms. Forty-six percent of the dairy farms had calf diarrhea, and 4 % had cow diarrhea. Seven (17 %) of the 42 farms with calf diarrhea had Salmonella. However, only 7 % (95 % CI: 4, 10) of the 221 diarrheic and 1 % (95 % CI: 0.2, 4) of the 234 of non-diarrheic calves had Salmonella. A total of 33 Salmonella isolates were obtained from the fecal samples: 12 isolates were Salmonella typhimurium, 6 were Salmonella montevideo, 6 were Salmonella anatum, 2 were Salmonella enteritidis, and 7 isolates were not serotyped. All isolates were susceptible to ciprofloxacin, trimethoprim–sulfamethoxazole, gentamycin, neomycin, colisitin, and amoxicillin at 100, 91, 85, 79, 79, and 70 %, respectively. Out of the 11 variables/categories, the frequency of cleaning every 2 months or more was associated with high odds of infection among calves (OR = 5.6) and farms (OR = 7.0).

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

References

  • Achá, S.J., Kühn, I., Jonsson, P., Mbazima, G., Katouli, M., and Möllby, R., 2004. Studies on Calf Diarrhea in Mozambique: Prevalence of Bacterial Pathogens. Acta Veterinaria Scandinavica, 45, 27-36

  • Alam, M.J., Renter, D.G., Ives, S.E., Thomson, D.U., Sanderson, M.W., Hollis, L.C., and Nagaraja, T.G., 2009. Potential associations between fecal shedding of Salmonella in feedlot cattle treated for apparent respiratory disease and subsequent adverse health outcomes. Veterinary Research, 40, 02

    Article  Google Scholar 

  • Anon., 2009; 2011. Annual reports of animal health, Ministry of Agriculture, Jordan.

  • Anon., 2007. SPSS Software, 16.0 Version. SPSS Inc.

  • Berge, A.C.B, Moore, D.A., and Sischo, W.M., 2006. Prevalence and antimicrobial resistance patterns of Salmonella enterica in preweaned calves from dairies and calf ranches. American Journal of Veterinary Research, 67, 1580-1588

    Article  CAS  PubMed  Google Scholar 

  • Boqvist, S., and Vågsholm, I., 2005. Risk factors for hazard of release from Salmonella-control restriction on Swedish cattle farms from 1993 to 2002. Preventive Veterinary Medicine, 71, 35-44

    Article  CAS  PubMed  Google Scholar 

  • Brichta-Harhay, D. M., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L., and Koohmaraie, M., 2011. Diversity of Multidrug-Resistant Salmonella enterica Strains Associated with Cattle at Harvest in the United States. Applied and Environmental Microbiology, 77, 1783–1796

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cannon, R.M., and Roe,s, R.T., 1982. Livestock Disease Surveys: A Field Manual For Veterinarians. Canberra: Australian Bureau of Animal Health

  • Carrique-Mas, J.J., Willmington, J.A., Papadopoulou, C., Watson, E.N., Davies, R.H, 2010. Salmonella infection in cattle in Great Britain, 2003 to 2008. The Veterinary Record, 167, 560-5

    Article  CAS  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention (CDC), 2013. Multistate Outbreak of Salmonella Montevideo and Salmonella Mbandaka Infections Linked to Tahini Sesame Paste. Salmonella homepage, http://www.cdc.gov/salmonella/montevideo-tahini-05-13/index.html. Accessed 8 Sep 2014

  • Cherry, B., Burns, A., Johnson, G.S., Pfeiffer, H., Dumas, N., Barrett, D., McDonough, P. L., and Eidson, M., 2004. Salmonella typhimurium outbreak associated with veterinary clinic. Emerging Infectious Diseases, 10, 2249-2251

    Article  PubMed Central  PubMed  Google Scholar 

  • Clinical and Laboratory Standards Institute, 2008. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals; Approved Standard—Third Edition. CLSI document M31-A3., Vol. 28, No. 8, Clinical and Laboratory Standards Institute, Wayne, PA

  • Cho, Y-il., and Yoon, K-Jin., 2014. An overview of calf diarrhea - infectious etiology, diagnosis, and intervention. Journal of Veterinary Science, 15, 1–17

    Article  PubMed Central  PubMed  Google Scholar 

  • Cummings, K.J., Warnick, L.D., Elton, M., Gröhn, Y.T., McDonough, P.L., and Siler, J.D., 2010. The effect of clinical outbreaks of salmonellosis on the prevalence of fecal Salmonella shedding among dairy cattle in New York. Foodborne Pathogens and Disease, 7, 815–823

    Article  PubMed Central  PubMed  Google Scholar 

  • Davison, H.C., Sayers, A.R., Smith, R.P., Pascoe, S.J., Davies, R.H., Weaver, J.P., and Evans, S.J., 2006. Risk factors associated with salmonella status of dairy farms in England and Wales. Veterinary Record, 159, 871-80

    CAS  PubMed  Google Scholar 

  • Dee, S., Deen, J., Burns, D., Douthit, G., and Pijoan, C., 2005. An evaluation of disinfectants for the sanitation of porcine reproductive and respiratory syndrome virus-contaminated transport vehicles at cold temperatures. Canadian Journal of Veterinary Research, 69, 64–70

    CAS  PubMed Central  PubMed  Google Scholar 

  • DEFRA, 2005. Veterinary Laboratories Report: Salmonella in Livestock Production in GB. (Also available at http://www.defra.gov.uk/corporate/vla/science/science-salm-rep04.htm)

  • DuPont, H.L., 2007. The growing threat of foodborne bacterial enteropathogens of animal origin. Clinical Infectious Diseases, 45, 1353-1361

    Article  PubMed  Google Scholar 

  • Ebuchi, S., Baba, A., Uryu, K., and Hiwaki, H., 2006. Two Outbreaks Caused by Salmonella Derby and S. Anatum at Grilled-Meat Restaurant in Fukuoka City. Japanese Journal of Infectious Diseases, 59, 405-406.

  • Ekdahl, K., de Jong, B., Wollin, R. and Andersson, Y., 2005. Travel-associated non-typhoidal salmonellosis: geographical and seasonal differences and serotype distribution. Clinical Microbiology and Infection, 11, 138-144

    Article  CAS  PubMed  Google Scholar 

  • Fraser, R.W., Williams, N.T., Powell, L.F., Cook, A.J.C., 2010. Reducing Campylobacter and Salmonella Infection: Two Studies of the Economic Cost and Attitude to Adoption of On-farm Biosecurity Measures R. W. Fraser et al. Farmer Attitudes and Control of Foodborne Zoonoses. Zoonoses & Public Health, 57, 109-115

  • Fossler, C.P., Wells, S.J., Kaneene, J.B., Ruegg, P.L., Warnick, L.D., Bender, J.B., Eberly, L.E., Godden, S.M., and Halbert, L.W., 2005. Herd-level factors associated with isolation of Salmonella in a multi-state study of conventional and organic dairy farms: II. Salmonella shedding in calves. Preventive Veterinary Medicine, 70: 279-291

    Article  CAS  PubMed  Google Scholar 

  • Hermesch, D., Thomson, D., Loneragan, G., Renter, D., and White, B., 2008. Effects of a commercially available vaccine against Salmonella enterica serotype Newport on milk production, somatic cell count, and shedding of Salmonella organisms in female dairy cattle with no clinical signs of salmonellosis. American Journal of Veterinary Research, 69, 1229–1234

    Article  PubMed  Google Scholar 

  • Izzo, M., Mohler, V., and House, J., 2011a. Antimicrobial susceptibility of Salmonella isolates recovered from calves with diarrhoea in Australia. Australian Veterinary Journal, 89, 402-8.

  • Izzo, M.M., Kirkland, P.D., Mohler, V.L., Perkins, N.R., Gunn, A.A., and House, J.K., 2011b. Prevalence of major enteric pathogens in Australian dairy calves with diarrhoea. Australian Veterinary Journal, 89,167-73.

  • Jones, F.T., 2011. A review of practical Salmonella control measures in animal feed. The Journal of Applied Poultry Research, 20, 102-113

    Article  Google Scholar 

  • Kagambèga, A., Lienemann, T., Aulu, L., Traoré, A.S., Barro, N., Siitonen, A., and Haukka, K., 2013. Prevalence and characterization of Salmonella enterica from the feces of cattle, poultry, swine and hedgehogs in Burkina Faso and their comparison to human Salmonella isolates. BMC Microbiology. 13, 1-16.

    Article  Google Scholar 

  • Levantesi, C., Bonadonna, L., Briancesco, R., Grohmann, E., Toze, S., and Tandoi, V., 2012. Salmonella in surface and drinking water: Occurrence and water-mediated transmission. Food Research International, 45, 587–602

    Article  Google Scholar 

  • Lombard, J.E., Beam, A.L., Nifong, E.M., Fossler, C.P., Kopral, C.A., Dargatz, D.A., Wagner, B.A., Erdman, M.M., Fedorka-Cray, P.J., 2012. Comparison of Individual, Pooled, and Composite Fecal Sampling Methods for Detection of Salmonella on U.S. Dairy Operations. Journal of Food Protection, 75, 1562-1571

  • Markey, B.K., 2013. Clinical veterinary microbiology, 2nd ed., Mosby/Elsevier, Edinburgh, Scotland.

    Google Scholar 

  • Martin, S.W., Meek, A.H., and Willberg, P., 1994. Veterinary Epidemiology: Principles and Methods. IOWA STATE UNIVERSITY PRESS / AMES.

  • McLaren, I., Wales, A., Breslin, M., and Davies, R., 2011. Evaluation of commonly-used farm disinfectants in wet and dry models of Salmonella farm contamination. Avian Pathology, 40, 33-42

    Article  CAS  PubMed  Google Scholar 

  • Moussa, I.M., Ashgan, M.H., Mohamed, M.S., Mohamed, K.H.F., Al-Doss, A.A., 2010. Rapid detection of Salmonella species in newborne calves by polymerase chain reaction. International Journal of Genetics and Molecular Biology, 2, 062-066

    CAS  Google Scholar 

  • Nielsen, L.R., Baggesen, D.L., Aabo, S., Moos, M.K., and Rattenborg, E., 2011. Prevalence and risk factors for Salmonella in veal calves at Danish cattle abattoirs. Epidemiology and Infection, 139, 1075-80

    Article  CAS  PubMed  Google Scholar 

  • Nielsen, L.R., Warnick, L.D., and Greiner, M., 2007. Risk Factors for Changing Test Classification in the Danish Surveillance Program for Salmonella in Dairy Herds. Journal of Dairy Science, 90, 2815-2824

    Article  CAS  PubMed  Google Scholar 

  • Okoro, C.K., Barquist, L., Connor, T.R., Harris, S.R., Clare, S., Stevens, M.P., Arends, M.J., Hale, C., Kane, L., Pickard, D.J., Hill, J., Harcourt, K., Parkhill, J., Dougan, G., and Kingsley, R.A., 2015. Signatures of Adaptation in Human Invasive Salmonella Typhimurium ST313 Populations from Sub-Saharan Africa. PLoS Neglected Tropical Diseases, 9: e0003611. doi: 10.1371/journal.pntd.0003611. eCollection.

    Article  PubMed Central  PubMed  Google Scholar 

  • Popoff M.Y., Bockemühl J., Gheesling L.L., 2004. Supplement 2002 (no. 46) to the Kauffmann-White scheme. WHO Collaborating Centre for Reference and Research on Salmonella, Unité de Génétique des Bactéries Intracellulaires, Institut Pasteur, 75724 Paris Cedex 15, France. mypof@pasteur.fr, Research In Microbiology 155, 568-70.

    Article  PubMed  Google Scholar 

  • Schlundt, J., Toyofuku, H., Jansen, J., and Herbst, S.A., 2004. Emerging food-borne zoonoses. Revue scientifique et technique (International Office of Epizootics), 23, 513-533

    CAS  Google Scholar 

  • Seyfarth, A.M., H C Wegener, H.C., and Frimodt-Møller, N., 2014. Antimicrobial resistance in Salmonella enterica subsp. enterica serovar typhimurium from humans and production animals. Journal of Antimicrobial Chemotherapy, 40, 67-75

  • Shua, J.C., White, P.L., Lathrop, S.L., Solghan, S.M., Medus, C., McGlinchey, B.M., Tobin-D’Angelo, M., Marcus, R., and Mahon, B.E., 2012. Salmonella enterica Serotype Enteritidis: Increasing Incidence of Domestically Acquired Infections. Clinical Infectious Diseases, 54, S488- S497

    Article  Google Scholar 

  • Svensson, C. and Jensen, M.B., 2007. Short communication: Identification of diseased calves by use of data from automatic milk feeders. Journal Of Dairy Science, 90, 994-7

    Article  CAS  PubMed  Google Scholar 

  • Strawn, L.K., Danyluk, M.D., Worobo, R. W., and Wiedmann, M., 2014. Distributions of Salmonella Subtypes Differ between Two U.S. Produce-Growing Regions. Applied and Environmental Microbiology, 80, 3982–3991

    Article  PubMed Central  PubMed  Google Scholar 

  • Toth, J.D., Aceto, H.W., Rankin, S.C., Dou, Z., 2013. Short communication: Survey of animal-borne pathogens in the farm environment of 13 dairy operations. Journal of Dairy Science, 96, 5756-5761.

    Article  CAS  PubMed  Google Scholar 

  • Thrusfield, M., 2007. Veterinary Epidemiology. 3ed., Blackwell Science Ltd. London.

  • Vanselow, B.A., Hornitzky, M.A., Walker, K.H., Eamens, G.J., Bailey, G.D., Gill, P.A., Coates, K., Corney, B., Cronin, J.P., and Renilson, S., 2007. Salmonella and on-farm risk factors in healthy slaughter-age cattle and sheep in eastern Australia. Australian Veterinary Journal, 85, 498-502

    Article  CAS  PubMed  Google Scholar 

  • Youssef, A.I., and El-Haig, M.M., 2012. Herd problems and occupational zoonosis of Salmonella enterica serovars Typhimurium and Enteritidis infection in diarrheic cattle and buffalo calves in Egypt. Human & Veterinary Medicine, 4, 118-123. OPEN ACCESS, http://www.hvm.bioflux.com.ro/

Download references

Acknowledgments

This work received financial assistance from the Deanship of Research, Jordan University of Science and Technology.

Conflicts of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yaser H. Tarazi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tarazi, Y.H., Abo-Shehada, M.N. Herd- and individual-level prevalences of and risk factors for Salmonella spp. fecal shedding in dairy farms in Al-Dhulail Valley, Jordan. Trop Anim Health Prod 47, 1241–1248 (2015). https://doi.org/10.1007/s11250-015-0854-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-015-0854-z

Keywords

Navigation