Prevalence of Salmonella spp. and Escherichia coli O157 in a red deer herd (Cervus elaphus scoticus) in central Mexico



      The primary objective was to evaluate the prevalence of Salmonella spp. and Escherichia coli O157 in feces of Cervus elaphus scoticus during summer and winter of 2015 to 2017. Additionally, the seasonality and environmental conditions were evaluated to investigate association with pathogen shedding.

      Materials and Methods

      Preliminary evaluation of Salmonella spp. detection was achieved by PCR-amplification of the invA, spvR, and sopB genes, whereas for E. coli O157, the eae and rfbE genes were amplified. Candidate genes with low limit detection were not used to evaluate the prevalence of target pathogens.

      Results and Discussion

      Red deer fecal samples (n = 89) were evaluated to detect invA and rfbE genes. The results showed that E. coli O157 prevalence was 0%, due to rfbE being absent; nevertheless, Salmonella spp. prevalence identified through the invA gene amplification was 56.2%, with the least prevalence during winter 2017. A positive correlation was observed between bacterial prevalence, atmospheric humidity, and temperature.

      Implications and Applications

      The results showed that E. coli O157 was not detected in the stool of captive red deer; however, Salmonella spp. were present. Therefore, good practices in food handling and hygiene are indispensable to avoid the emergence of foodborne diseases.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Aboud O.A.A.
        • Adaska J.M.
        • Williams D.R.
        • Rossitto P.V.
        • Champagne J.D.
        • Lehenbauer T.W.
        • Atwill R.
        • Li X.
        • Aly S.S.
        Epidemiology of Salmonella sp. in California cull dairy cattle: Prevalence of fecal shedding and diagnostic accuracy of pooled enriched broth culture of fecal samples..
        PeerJ. 2016; 4 (e2386)
        • Akil L.
        • Ahmad H.A.
        • Reddy R.S.
        Effects of climate change on Salmonella infections..
        Foodborne Pathog. Dis. 2014; 11: 974-980
        • Alexander K.A.
        • Warnick L.D.
        • Cripps C.J.
        • McDonough P.L.
        • Grohn Y.T.
        • Wiedmann M.
        • Reed K.E.
        • James K.L.
        • Soyer Y.
        • Ivanek R.
        Fecal shedding of, antimicrobial resistance in, and serologic response to Salmonella Typhimurium in dairy calves..
        J. Am. Vet. Med. Assoc. 2009; 235: 739-748
        • Altschul S.F.
        • Gish W.
        • Miller W.
        • Myers E.W.
        • Lipman D.J.
        Basic local alignment search tool..
        J. Mol. Biol. 1990; 215: 403-410
        • Amini K.
        • Salehi T.Z.
        • Nikbakht G.
        • Ranjbar R.
        • Amini J.
        Molecular detection of invA and spv virulence genes in Salmonella Enteritidis isolated from human and animals in Iran..
        Afr. J. Microbiol. Res. 2010; 4: 2202-2210
        • Andino A.
        • Hanning I.
        Salmonella enterica: Survival, colonization, and virulence differences among serovars..
        Sci. World J. 2015; 2015: 1-16
        • Arnold T.
        • Scholz H.C.
        • Marg H.
        • Rösler U.
        • Hensel A.
        Impact of invA-PCR and culture detection methods on occurrence and survival of Salmonella in the flesh, internal organs and lymphoid tissues of experimentally infected pigs..
        J. Vet. Med. B. Infect. Dis. Vet. Public Health. 2004; 51: 459-463
        • Bai J.
        • Shi X.
        • Nagaraja T.G.
        A multiplex PCR procedure for the detection of six major virulence genes in Escherichia coli O157:H7..
        J. Microbiol. Methods. 2010; 82: 85-89
        • Bergmann G.T.
        • Craine J.M.
        • Robeson M.S.
        • Fierer N.
        Seasonal shifts in diet and gut microbiota of the American bison (Bison bison)..
        PLoS One. 2015; 10 (e0142409)
        • Berry E.D.
        • Wells J.E.
        Escherichia coli O157:H7: Recent advances in research on occurrence, transmission, and control in cattle and the production environment.
        Adv. Food Nutr. Res. 2010; 60: 67-117
        • Besser T.E.
        • Richards B.L.
        • Rice D.H.
        • Hancock D.D.
        Escherichia coli O157:H7 infection of calves: Infectious dose and direct contact transmission..
        Epidemiol. Infect. 2001; 127: 555-560
        • Blau D.M.
        • McCluskey B.J.
        • Ladely S.R.
        • Dargatz D.A.
        • Fedorka-Cray P.J.
        • Ferris K.E.
        • Headrick M.L.
        Salmonella in dairy operations in the United States: Prevalence and antimicrobial drug susceptibility..
        J. Food Prot. 2005; 68: 696-702
        • Branham L.A.
        • Carr M.A.
        • Scott C.B.
        • Callaway T.R.
        E. coli O157 and Salmonella spp. in white-tailed deer and livestock..
        Curr. Issues Intest. Microbiol. 2005; 6: 25-29
        • Cabal A.
        • Vicente J.
        • Alvarez J.
        • Barasona J.A.
        • Boadella M.
        • Dominguez L.
        • Gortazar C.
        Human influence and biotic homogenization drive the distribution of Escherichia coli virulence genes in natural habitats..
        MicrobiologyOpen. 2017; 6: 1-10
        • Callaway T.R.
        • Carr M.A.
        • Edrington T.S.
        • Anderson R.C.
        • Nisbet D.J.
        Diet, Escherichia coli O157:H7, and cattle: A review after 10 years..
        Curr. Issues Mol. Biol. 2009; 11: 67-79
        • Callaway T.R.
        • Dowd S.E.
        • Edrington T.S.
        • Anderson R.C.
        • Krueger N.
        • Bauer N.
        • Kononoff P.J.
        • Nisbet D.J.
        Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing..
        J. Anim. Sci. 2010; 88: 3977-3983
        • Carrillo-Del Valle M.D.
        • De la Garza-García J.A.
        • Díaz-Aparicio E.
        • Valdivia-Flores A.G.
        • Cisneros-Guzmán L.F.
        • Rosario C.
        • Manjarrez-Hernández Á.H.
        • Navarro A.
        • Xicohtencatl-Cortes J.
        • Maravilla P.
        • Hernández-Castro R.
        Characterization of Escherichia coli strains from red deer (Cervus elaphus) faeces in a Mexican protected natural area..
        Eur. J. Wildl. Res. 2016; 62: 415-421
        • Chaudhary J.H.
        • Nayak J.B.
        • Brahmbhatt M.N.
        • Makwana P.P.
        Virulence genes detection of Salmonella serovars isolated from pork and slaughterhouse environment in Ahmedabad, Gujarat..
        Vet. World. 2015; 8: 121-124
        • Choudhury M.
        • Borah P.
        • Sarma H.K.
        • Barkalita L.M.
        • Deka N.K.
        • Hussain I.
        • Hussain M.I.
        Multiplex-PCR assay for detection of some major virulence genes of Salmonella enterica serovars from diverse sources.
        Curr. Sci. 2016; 111: 1252-1258
        • Cummings K.J.
        • Warnick L.D.
        • Alexander K.A.
        • Cripps C.J.
        • Gröhn Y.T.
        • James K.L.
        • McDonough P.L.
        • Reed K.E.
        The duration of fecal Salmonella shedding following clinical disease among dairy cattle in the northeastern USA..
        Prev. Vet. Med. 2009; 92: 134-139
        • Davis M.A.
        • Hancock D.D.
        • Rice D.H.
        • Call D.R.
        • DiGiacomo R.
        • Samadpour M.
        • Besser T.E.
        Feedstuffs as a vehicle of cattle exposure to Escherichia coli O157:H7 and Salmonella enterica..
        Vet. Microbiol. 2003; 95: 199-210
        • Díaz-Sánchez S.
        • Sánchez S.
        • Herrera-León S.
        • Porrero C.
        • Blanco J.
        • Dahbi G.
        • Blanco J.E.
        • Mora A.
        • Mateo R.
        • Hanning I.
        • Vidal D.
        Prevalence of Shiga toxin-producing Escherichia coli, Salmonella spp. and Campylobacter spp. in large game animals intended for consumption: Relationship with management practices and livestock influence..
        Vet. Microbiol. 2013; 163: 274-281
        • Fornefeld E.
        • Schierstaedt J.
        • Jechalke S.
        • Grosch R.
        • Schikora A.
        • Smalla K.
        Persistence of Salmonella Typhimurium LT2 in soil enhanced after growth in lettuce medium..
        Front. Microbiol. 2017; 8: 1-8
        • Franz E.
        • van Diepeningen A.D.
        • de Vos O.J.
        • van Bruggen A.H.C.
        Effects of cattle feeding regimen and soil management type on the fate of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in manure, manure-amended soil, and lettuce..
        Appl. Environ. Microbiol. 2005; 71: 6165-6174
        • Gal-Mor O.
        • Boyle E.C.
        • Grassl G.A.
        Same species, different diseases: How and why typhoidal and non-typhoidal Salmonella enterica serovars differ..
        Front. Microbiol. 2014; 5: 1-10
        • Garrido A.
        • Chapela M.J.
        • Roman B.
        • Fajardo P.
        • Vieites J.M.
        • Cabado A.G.
        In-house validation of a multiplex real-time PCR method for simultaneous detection of Salmonella spp., Escherichia coli O157 and Listeria monocytogenes..
        Int. J. Food Microbiol. 2013; 164: 92-98
        • Halimi H.A.
        • Seifi H.A.
        • Rad M.
        Bovine salmonellosis in Northeast of Iran: Frequency, genetic fingerprinting and antimicrobial resistance patterns of Salmonella spp..
        Asian Pac. J. Trop. Biomed. 2014; 4: 1-7
        • Hall T.A.
        BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT..
        Nucleic Acids Symp. Ser. 1999; 41: 95-98
        • Hamzah A.M.
        • Hussein A.M.
        • Khalef J.M.
        Isolation of Escherichia coli O157:H7 strain from fecal samples of zoo animal..
        Hindawi Sci. World J. 2013; 2013 (843968)
        • Huston C.L.
        • Wittum T.E.
        • Love B.C.
        Persistent fecal Salmonella shedding in five dairy herds..
        J. Am. Vet. Med. Assoc. 2002; 220 (a): 650-655
        • Huston C.L.
        • Wittum T.E.
        • Love B.C.
        • Keen J.E.
        Prevalence of fecal shedding of Salmonella spp. in dairy herds..
        J. Am. Vet. Med. Assoc. 2002; 220 (b): 645-649
      1. International Business Machine Corporation. 2013. IBM SPSS Statistics for Windows, Version 22.0. IBM Corp., Armonk, NY.

        • Ishaq S.L.
        • Wright A.-D.G.
        Insight into the bacterial gut microbiome of the North American moose (Alces alces)..
        BMC Microbiol. 2012; 12: 212
        • Jijón S.
        • Wetzel A.
        • LeJeune J.
        Salmonella enterica isolated from wildlife at two Ohio rehabilitation centers..
        J. Zoo Wildl. Med. 2007; 38: 409-413
        • Kongmuang U.
        • Luk J.M.C.
        • Lindberg A.A.
        Comparison of three stool-processing methods for detection of Salmonella serogroups B, C2, and D by PCR..
        J. Clin. Microbiol. 1994; 32: 3072-3074
        • Li Z.
        • Zhang Z.
        • Xu C.
        • Zhao J.
        • Liu H.
        • Fan Z.
        • Yang F.
        • Wright A.-E.
        • Li G.
        Bacteria and methanogens differ along the gastrointestinal tract of Chinese roe deer (Capreolus pygargus)..
        PLoS One. 2014; 9 (e114513)
        • Lillehaug A.
        • Bergsjø B.
        • Schau J.
        • Bruheim T.
        • Vikøren T.
        • Handeland K.
        Campylobacter spp., Salmonella spp., verocytotoxic Escherichia coli, and antibiotic resistance in indicator organisms in wild cervids..
        Acta Vet. Scand. 2005; 46: 23-32
        • Luo Z.
        • Gu G.
        • Ginn A.
        • Giurcanu M.C.
        • Adams P.
        • Vellidis G.
        • van Bruggen A.H.C.
        • Danyluk M.D.
        • Wright A.C.
        Distribution and characterization of Salmonella enterica isolates from irrigation ponds in the southeastern United States..
        Appl. Environ. Microbiol. 2015; 81: 4376-4387
        • Majowicz S.E.
        • Musto J.
        • Scallan E.
        • Angulo F.J.
        • Kirk M.
        • O’Brien S.J.
        • Jones T.F.
        • Fazil A.
        • Hoekstra R.M.
        The global burden of nontyphoidal Salmonella gastroenteritis..
        Clin. Infect. Dis. 2010; 50: 882-889
        • Malorny B.
        • Hoorfar J.
        • Bunge C.
        • Helmuth R.
        Multicenter validation of the analytical accuracy of Salmonella PCR: Towards an international standard multicenter..
        Appl. Environ. Microbiol. 2003; 69: 290-296
        • Mattiello S.
        Welfare issues of modern deer farming..
        Ital. J. Anim. Sci. 2009; 8: 205-217
      2. Mazerolle, M. J. 2019. Model Selection and Multimodel Inference Based on (Q)AIC(c) v. 2.2–2.

        • McWhorter A.R.
        • Chousalkar K.K.
        Comparative phenotypic and genotypic virulence of Salmonella strains isolated from Australian layer farms..
        Front. Microbiol. 2015; 6: 1-14
        • Money P.
        • Kelly A.F.
        • Gould S.W.J.
        • Denholm-Price J.
        • Threlfall E.J.
        • Fielder M.D.
        Cattle, weather and water: Mapping Escherichia coli O157:H7 infections in humans in England and Scotland..
        Environ. Microbiol. 2010; 12: 2633-2644
      3. New South Wales Department of Primary Industries. 2017 Collection of Faeces. Accessed Aug. 31, 2017.

        • Priyanka B.
        • Patil R.
        • Dwarakanath S.
        A review on detection methods used for foodborne pathogens..
        Indian J. Med. Res. 2016; 144: 327
        • Qian W.
        • Li Z.
        • Ao W.
        • Zhao G.
        • Li G.
        • Wu J.
        Bacterial community composition and fermentation in the rumen of Xinjiang brown cattle (Bos taurus), Tarim red deer (Cervus elaphus yarkandensis), and Karakul sheep (Ovis aries)..
        Can. J. Microbiol. 2017; 63: 375-383
      4. R Core Team. 2019. R: A language and environment for statistical computing. R Found. Stat. Comput., Vienna, Austria. Software.

        • Renter D.G.
        • Sargeant J.M.
        • Hygnstorm S.E.
        • Hoffman J.D.
        • Gillespie J.R.
        Escherichia coli O157:H7 in free-ranging deer in Nebraska..
        J. Wildl. Dis. 2001; 37: 755-760
        • Sargeant J.M.
        • Hafer D.J.
        • Gillespie J.R.
        • Oberst R.D.
        • Flood S.J.
        Prevalence of Escherichia coli O157:H7 in white-tailed deer sharing rangeland with cattle..
        J. Am. Vet. Med. Assoc. 1999; 215: 792-794
      5. Secretaría de Salud. 2017. Boletín Epidemiológico. Accessed Aug. 20, 2017.

      6. Smith, J. L., P. M. Fratamico, and N. W. Gunther. 2014. Shiga toxin-producing Escherichia coli. Pages 145–197 in Advances in Applied Microbiology. 1st ed. Elsevier Inc., Amsterdam, the Netherlands.10.1016/B978-0-12-800262-9.00003-2.

        • Soumet C.
        • Ermel G.
        • Rose V.
        • Rose N.
        • Drouin P.
        • Salvat G.
        • Colin P.
        Identification by a multiplex PCR-based assay of Salmonella Typhimurium and Salmonella Enteritidis strains from environmental swabs of poultry houses..
        Lett. Appl. Microbiol. 1999; 29: 1-6
        • Stone G.G.
        • Oberst R.D.
        • Hays M.P.
        • Mcvey S.
        • Chengappa M.M.
        Detection of Salmonella serovars from clinical samples by enrichment broth cultivation-PCR procedure..
        J. Clin. Microbiol. 1994; 32: 1742-1749
      7. Weather Underground. 2017. Accessed Aug. 22, 2017.