Bacterial-associated diarrhea in the dog: a critical appraisal

      Diarrhea in dogs is one of the most common maladies facing the small animal practitioner today, and bacterial enteropathogens play an important role in many of these cases [
      • Greene C.E.
      Enteric bacterial infections.
      ,
      • Guilford W.G.
      • Strombeck D.R.
      Gastrointestinal tract infections, parasites, and toxicosis.
      ]. Clinical signs can range in severity from a mild self-limiting diarrhea to a potentially fatal acute hemorrhagic diarrheal syndrome (AHDS) [
      • Cave N.J.
      • Marks S.L.
      • Kass P.H.
      • et al.
      Evaluation of a routine diagnostic fecal panel in dogs with diarrhea.
      ]. Despite this phenomenon, the clinical documentation of enteropathogenic bacteria causing diarrhea in dogs is clouded by the presence of many of these organisms existing as normal constituents of the indigenous intestinal flora. The bacteria most commonly incriminated in canine diarrhea include Clostridium perfringens, Clostridium difficile, Campylobacter spp, pathogenic Escherichia coli, and Salmonella spp [
      • Greene C.E.
      Enteric bacterial infections.
      ,
      • Guilford W.G.
      • Strombeck D.R.
      Gastrointestinal tract infections, parasites, and toxicosis.
      ,
      • Cave N.J.
      • Marks S.L.
      • Kass P.H.
      • et al.
      Evaluation of a routine diagnostic fecal panel in dogs with diarrhea.
      ]. It is important to appreciate that these bacterial species are but a small representation of putative pathogenic enteric bacteria and that additional studies are warranted to elucidate the role of less well-defined species, such as Anaerobiospirillum spp, Yersinia spp, and other yet uncharacterized organisms.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      PDF Download and 24 Hours Online Access
      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.
      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Veterinary Clinics: Small Animal Practice
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Greene C.E.
        Enteric bacterial infections.
        in: Infectious diseases of the dog and cat. WB Saunders, Philadelphia1998: 243-245
        • Guilford W.G.
        • Strombeck D.R.
        Gastrointestinal tract infections, parasites, and toxicosis.
        in: Guilford W.G. Center S.A. Strombeck’s small animal gastroenterology. WB Saunders, Philadelphia1996: 411-432
        • Cave N.J.
        • Marks S.L.
        • Kass P.H.
        • et al.
        Evaluation of a routine diagnostic fecal panel in dogs with diarrhea.
        J Am Vet Med Assoc. 2002; 221: 52-59
        • Smith L.
        • Williams B.L.
        Clostridium perfringens.
        in: Balows A. The pathogenic anaerobic bacteria. Charles C. Thomas, Springfield (IL)1984: 101-136
        • Kokai-Kun J.F.
        • Songer J.G.
        • Czeczulin J.R.
        • et al.
        Comparison of western immunoblots and gene detection assays for identification of potentially enterotoxigenic isolates of Clostridium perfringens.
        J Clin Microbiol. 1994; 32: 2533-2539
        • Songer J.G.
        • Meer R.R.
        Genotyping of Clostridium perfringens by polymerase chain reaction is a useful adjunct to diagnosis of Clostridial enteric disease in animals.
        Anaerobe. 1996; 2: 197-203
        • Van Damme-Jongsten M.
        • Wernars K.
        • Notermans S.
        Cloning and sequencing of the Clostridium perfringens enterotoxin gene.
        Antonie van Leeuwenhoek J Microbiol. 1989; 56: 181-190
        • Argenti L.
        • Coiro R.
        • Ciorba A.
        Enterite emorragica nel cane associata alla presenza di Clostridium perfringens tipo C.
        Summa. 1987; 4: 279-281
        • Meer R.R.
        • Songer J.G.
        Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens.
        Am J Vet Res. 1997; 58: 702-705
        • Marks S.L.
        • Kather E.J.
        • Kass P.H.
        • et al.
        Genotypic and phenotypic characterization of Clostridium perfringens and Clostridium difficile in diarrheic and healthy dogs.
        J Vet Intern Med. 2002; 16: 533-540
        • Meer R.R.
        • Songer J.G.
        • Park D.L.
        Human disease associated with Clostridium perfringens enterotoxin.
        Rev Environ Contam Toxicol. 1997; 150: 75-94
        • Sasaki J.
        • Goryo M.
        • Masatoshi A.
        • et al.
        Hemorrhagic enteritis associated with Clostridium perfringens type A in a dog.
        J Vet Med Sci. 1999; 61: 175-177
        • Weese J.S.
        • Staempfli H.R.
        • Prescott J.F.
        • et al.
        The roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in diarrhea in dogs.
        J Vet Intern Med. 2001; 15: 374-378
        • Garmory H.S.
        • Chanter N.
        • French N.P.
        • et al.
        Occurrence of Clostridium perfringens B2-toxin amongst animals, determined using genotyping and subtyping PCR assays.
        Epidemiol Infect. 2000; 124: 61-67
        • Gibert M.
        • Jolivet-Renaud C.
        • Popoff M.R.
        Beta2 toxin, a novel toxin produced by Clostridium perfringens.
        Gene. 1997; 203: 65-73
        • Herholz C.
        • Miserez R.
        • Nicolet J.
        • et al.
        Prevalence of B2-toxigenic Clostridium perfringens in horses with intestinal disorders.
        J Clin Microbiol. 1999; 37: 358-361
        • Thiede S.
        • Goethe R.
        • Amtsberg G.
        Prevalence of B2 toxin gene of Clostridium perfringens type A from diarrhoeic dogs.
        Vet Rec. 2001; 149: 273-274
        • Bartlett M.L.
        • Walker H.W.
        • Ziprin R.
        Use of dogs as an assay for Clostridium perfringens enterotoxin.
        Appl Microbiol. 1972; 23: 193-197
        • Czeczulin J.R.
        • Collie R.E.
        • McClane B.A.
        Regulated expression of Clostridium perfringens enterotoxin in naturally cpe-negative type, A, B, and C isolates of C. perfringens.
        Infect Immun. 1996; 64: 3301-3309
        • Czeczulin J.R.
        • Hanna P.C.
        • McClane B.A.
        Cloning, nucleotide sequencing, and expression of the Clostridium perfringens enterotoxin gene in Escherichia coli.
        Infect Immun. 1993; 61: 3429-3439
        • Collie R.E.
        • McClane B.A.
        Evidence that the enterotoxin gene can be episomal in Clostridium perfringens isolates associated with non-food-borne human gastrointestinal diseases.
        J Clin Microbiol. 1998; 36: 30-36
        • Cornillot E.
        • Saint-Joanis B.
        • Daube G.
        • et al.
        The enterotoxin gene (cpe) of Clostridium perfringens can be chromosomal or plasmid-borne.
        Mol Microbiol. 1995; 15: 639-647
        • Miyamoto K.
        • Chakrabarti G.
        • Morino Y.
        • et al.
        Organization of the plasmid cpe locus in Clostridium perfringens type A isolates.
        Infect Immun. 2002; 70: 4261-4272
        • McClane B.A.
        New insights into the genetics and regulation of expression of Clostridium perfringens enterotoxin.
        Curr Top Microbiol Immunol. 1998; 225: 37-55
        • McClane B.A.
        The complex interactions between Clostridium perfringens enterotoxin and epithelial tight junctions.
        Toxicon. 2001; 39: 1781-1791
        • Kokai-Kun J.F.
        • McClane B.A.
        Evidence that a region(s) of the Clostridium perfringens enterotoxin molecule remains exposed on the external surface of the mammalian plasma membrane when the toxin is sequestered in small or large complexes.
        Infect Immun. 1996; 64: 1020-1025
        • McClane B.A.
        An overview of Clostridium perfringens enterotoxin.
        Toxicon. 1996; 34: 1335-1343
        • Sarker M.R.
        • Singh U.
        • McClane B.A.
        An update on Clostridium perfringens enterotoxin.
        J Nat Toxins. 2000; 9: 251-266
        • Wieckowski E.U.
        • Kokai-Kun J.F.
        • McClane B.A.
        Characterization of membrane-associated Clostridium perfringens enterotoxin following pronase treatment.
        Infect Immun. 1998; 66: 5897-5905
        • McDonel J.L.
        • Demers G.W.
        In vivo effects of enterotoxin from Clostridium perfringens type A in the rabbit colon: binding vs. biologic activity.
        J Infect Dis. 1982; 145: 490-494
        • McDonel J.L.
        • Duncan C.L.
        Regional localization of activity of Clostridium perfringens type A enterotoxin in the rabbit ileum, jejunum, and duodenum.
        J Infect Dis. 1977; 136: 661-666
        • Twedt D.C.
        Clostridium perfringens associated diarrhea in dogs.
        in: DeNova R. Proceedings of the Eleventh Annual Veterinary Medical Forum. American College of Veterinary Internal Medicine. Omni press, Madison (WI)1993: 121-125
        • Marks S.L.
        • Melli A.C.
        • Kass P.H.
        • et al.
        Evaluation of methods to diagnose Clostridium perfringens-associated diarrhea in dogs.
        J Am Vet Med Assoc. 1999; 214: 357-360
        • Twedt D.C.
        Clostridium perfringens-associated enterotoxicosis in dogs.
        in: Kirk R.W. Bonagura J.D. Current veterinary therapy XI: small animal practice. 11. WB Saunders, Philadelphia1992: 602-604
        • Berry P.R.
        • Rodhouse J.C.
        • Hughes S.
        • et al.
        Evaluation of ELISA, RPLA, and Vero cell assays for detecting Clostridium perfringens enterotoxin in fecal specimens.
        J Clin Pathol. 1988; 41: 458-461
        • Modi N.
        • Wilcox M.H.
        Evidence for antibiotic induced Clostridium perfringens diarrhoea.
        J Clin Pathol. 2001; 54: 748-751
        • Marks S.L.
        • Kather E.J.
        Antimicrobial susceptibilities of canine Clostridium difficile and Clostridium perfringens isolates to commonly utilized antimicrobial drugs.
        Vet Microbiol. 2003; 94: 39-45
      1. Kather EJ, Marks SL. Determination of the incidence of antimicrobial resistance genes in canine Clostridium perfringens. Presented at the Fourth International Conference on the Molecular Biology and Pathogenesis of the Clostridia, Woods Hole, MA. April 26–30, 2003.

        • Rood J.I.
        Transferable tetracycline resistance in Clostridium perfringens strains of porcine origin.
        Can J Microbiol. 1983; 29: 1241-1246
        • Shoemaker N.B.
        • Vlamakis H.
        • Hayes K.
        • et al.
        Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon.
        Appl Environ Microbiol. 2001; 67: 561-568
        • Hall J.C.
        • O'Toole E.
        Intestinal flora in newborn infants with description of a new pathogenic anaerobe, Bacillus difficilis.
        Am J Dis Child. 1935; 9: 390-402
        • Bartlett J.G.
        • Chang T.W.
        • Gurwith M.
        • et al.
        Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia.
        N Engl J Med. 1978; 298: 531-534
        • Kelly C.P.
        • Pothoulakis C.
        • LaMont J.T.
        Clostridium difficile colitis.
        N Engl J Med. 1994; 330: 257-262
        • Larson H.E.
        • Price A.B.
        • Honour P.
        • et al.
        Clostridium difficile and the aetiology of pseudomembranous colitis.
        Lancet. 1978; 1: 1063-1066
        • Jones R.L.
        • Adney W.S.
        • Alexander A.F.
        • et al.
        Hemorrhagic necrotizing enterocolitis associated with Clostridium difficile infection in four foals.
        J Am Vet Med Assoc. 1988; 193: 76-79
        • Kelly C.P.
        • LaMont J.T.
        Clostridium difficile infection.
        Annu Rev Med. 1998; 49: 375-390
        • Al-Barrak A.
        • Embil J.
        • Dyck B.
        • et al.
        An outbreak of toxin A negative, toxin B positive Clostridium difficile-associated diarrhea in a Canadian tertiary-care hospital.
        Can Commun Dis Rep. 1999; 25: 1-3
        • Barbut F.
        • Lalande V.
        • Burghoffer B.
        • et al.
        Prevalence and genetic characterization of toxin A variant strains of Clostridium difficile among adults and children with diarrhea in France.
        J Clin Microbiol. 2002; 40: 2079-2083
        • Kuijper E.J.
        • de Weerdt J.
        • Kato H.
        • et al.
        Nosocomial outbreak of Clostridium difficile-associated diarrhoea due to a clindamycin-resistant enterotoxin A-negative strain.
        Eur J Clin Microbiol Infect Dis. 2001; 20: 528-534
        • Riley T.V.
        • Adams J.E.
        • O'Neill G.L.
        • et al.
        Gastrointestinal carriage of Clostridium difficile in cats and dogs attending veterinary clinics.
        Epidemiol Infect. 1991; 107: 659-665
        • Struble A.L.
        • Tang Y.J.
        • Kass P.H.
        • et al.
        Fecal shedding of Clostridium difficile in dogs: a period prevalence survey in a veterinary medical teaching hospital.
        J Vet Diagn Invest. 1994; 6: 342-347
        • Baverud V.
        • Gustafsson A.
        • Franklin A.
        • et al.
        Clostridium difficile associated with acute colitis in mature horses treated with antibiotics.
        Equine Vet J. 1997; 29: 279-284
        • Brown E.
        • Talbot G.H.
        • Axelrod P.
        • et al.
        Risk factors for Clostridium difficile toxin-associated diarrhea.
        Infect Control Hosp Epidemiol. 1990; 11: 283-290
        • Ho M.
        • Yang D.
        • Wyle F.A.
        • et al.
        Increased incidence of Clostridium difficile-associated diarrhea following decreased restriction of antibiotic use.
        Clin Infect Dis. 1996; 23: S102-S106
        • Jones R.L.
        • Adney W.S.
        • Shideler R.K.
        Isolation of Clostridium difficile and detection of cytotoxin in the feces of diarrheic foals in the absence of antimicrobial treatment.
        J Clin Microbiol. 1987; 25: 1225-1227
        • Hammond G.A.
        • Johnson J.L.
        The toxigenic element of Clostridium difficile strain VPI 10463.
        Microb Pathog. 1995; 19: 203-213
        • Just I.
        • Fritz K.
        • Aktories K.
        • et al.
        Clostridium difficile toxin B acts on the GTP-binding protein rho.
        J Biol Chem. 1996; 269: 10706-10712
        • Just I.
        • Wilm M.
        • Selzer J.
        • et al.
        The enterotoxin from Clostridium difficile (Tox A) monoglucosylates the Rho proteins.
        J Biol Chem. 1995; 270: 13932-13936
        • Lyerly D.M.
        • Saum K.E.
        • MacDonald D.K.
        • et al.
        Effects of Clostridium difficile toxins given intragastrically to animals.
        Infect Immun. 1985; 47: 349-352
        • Mitchell T.J.
        • Ketley J.M.
        • Haslam S.C.
        • et al.
        Effect of toxin A and B of Clostridium difficile on rabbit ileum and colon.
        Gut. 1986; 27: 78-85
        • Lima A.A.
        • Lyerly D.M.
        • Wilkins T.D.
        • et al.
        Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro.
        Infect Immun. 1988; 56: 582-588
        • Libby J.M.
        • Donta S.T.
        • Wilkins T.D.
        Clostridium difficile toxin A in infants.
        J Infect Dis. 1983; 148: 606
        • Viscidi R.
        • Willey S.
        • Bartlett J.G.
        Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations.
        Gastroenterology. 1981; 81: 5-9
        • Perrin J.
        • Buogo C.
        • Gallusser A.
        • et al.
        Intestinal carriage of Clostridium difficile in neonate dogs.
        J Vet Med Ser B. 1993; 40: 222-226
        • Alfa M.J.
        • Kabani A.
        • Lyerly D.
        • et al.
        Characterization of toxin A-negative, toxin B-positive strain of Clostridium difficile responsible for a nosocomial outbreak of Clostridium difficile-associated diarrhea.
        J Clin Microbiol. 2000; 38: 2706-2714
        • Pituch H.
        • van den Braak N.
        • van Leeuwen W.
        • et al.
        Clonal dissemination of a toxin A-negative/toxin B-positive Clostridium difficile strain from patients with antibiotic-associated diarrhea in Poland.
        Clin Microbiol Infect. 2001; 7: 442-446
        • Gulke I.
        • Pfeifer G.
        • Liese J.
        • et al.
        Characterization of the enzymatic component of the ADP-ribosyltransferase toxin CDTa from Clostridium difficile.
        Infect Immun. 2001; 69: 6004-6011
        • Popoff M.R.
        • Rubin E.J.
        • Gill D.M.
        • et al.
        Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain.
        Infect Immun. 1988; 56: 2299-2306
        • Stubbs S.
        • Rupnik M.
        • Gibert M.
        • et al.
        Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile.
        FEMS Microbiol Lett. 2000; 186: 307-312
        • Braun M.
        • Herholz C.
        • Straub R.
        • et al.
        Detection of the ADP-ribosyltransferase toxin gene (cdtA) and its activity in Clostridium difficile isolates from Equidae.
        FEMS Microbiol Lett. 2000; 184: 29-33
        • Perelle S.
        • Gibert M.
        • Bourlioux P.
        • et al.
        Production of a complete binary toxin (actin-specific ADP-ribosyltransferase) by Clostridium difficile CD196.
        Infect Immun. 1997; 65: 1402-1407
        • Fekety R.
        Guidelines for the diagnosis and management of Clostridium difficile-associated diarrhea and colitis. American College of Gastroenterology, Practice Parameters Committee.
        Am J Gastroenterol. 1997; 92: 739-750
        • Landry M.L.
        • Topal J.
        • Ferguson D.
        • et al.
        Evaluation of biosite triage Clostridium difficile panel for rapid detection of Clostridium difficile in stool samples.
        J Clin Microbiol. 2001; 39: 1855-1858
        • Alfa M.J.
        • Swan B.
        • VanDekerkhove P.
        • et al.
        The diagnosis of Clostridium difficile-associated diarrhea: comparison of triage C. difficile panel, EIA for Tox A/B/ and cytotoxin assays.
        Diagn Microbiol Infect Dis. 2002; 43: 257-263
        • O'Connor D.
        • Hynes P.
        • Cormican M.
        • et al.
        Evaluation of methods for detection of toxins in specimens of feces submitted for diagnosis of Clostridium difficile-associated diarrhea.
        J Clin Microbiol. 2001; 39: 2846-2849
        • Gumerlock P.H.
        • Tang Y.J.
        • Weiss J.B.
        • et al.
        Specific detection of toxigenic strains of Clostridium difficile in stool specimens.
        J Clin Microbiol. 1993; 31: 507-511
        • Wolfhagen M.J.
        • Fluit A.C.
        • Torensma R.
        • et al.
        Rapid detection of toxigenic Clostridium difficile in fecal samples by magnetic immuno PCR assay.
        J Clin Microbiol. 1994; 32: 1629-1633
        • Hosie B.D.
        • Nicolson T.B.
        • Henderson D.B.
        Campylobacter infections in normal and diarrhoeic dogs.
        Vet Rec. 1979; 105: 80
        • Malik R.
        • Love D.N.
        The isolation of Campylobacter jejuni/coli from pound dogs and canine patients in a veterinary hospital.
        Aust Vet Pract. 1989; 19: 16-18
        • McOrist S.
        • Browning J.W.
        Carriage of Campylobacter jejuni in healthy and diarrhoeic dogs and cats.
        Aust Vet J. 1982; 58: 33-34
        • Engvall E.O.
        • Brandstrom B.
        • Gunnarsson A.
        • et al.
        Validation of a polymerase chain reaction/restriction enzyme analysis method for species identification of thermophilic campylobacters isolated from domestic and wild animals.
        J Appl Microbiol. 2002; 92: 47-54
        • Steinhauserova I.
        • Fojtikova K.
        • Klimes J.
        The incidence and PCR detection of Campylobacter upsaliensis in dogs and cats.
        Lett Appl Microbiol. 2000; 31: 209-212
        • Bourke B.
        • Chan V.L.
        • Sherman P.
        Campylobacter upsaliensis: waiting in the wings.
        Clin Microbiol Rev. 1998; 11: 440-449
        • Labarca J.A.
        • Sturgeon J.
        • Borenstein L.
        • et al.
        Campylobacter upsaliensis: another pathogen for consideration in the United States.
        Clin Infect Dis. 2002; 34: E59-E60
        • Prescott J.F.
        • Karmali M.A.
        Attempts to transmit Campylobacter enteritis to dogs and cats.
        Can Med Assoc J. 1978; 119: 1001-1002
        • Prescott J.F.
        • Barker I.K.
        • Manninen K.I.
        • et al.
        Campylobacter jejuni colitis in gnotobiotic dogs.
        Can J Comp Med. 1981; 45: 377-383
        • Sandstedt K.
        • Ursing J.
        • Walder M.
        Thermotolerant Campylobacter with no or weak catalase activity isolated from dogs.
        Curr Microbiol. 1983; 8: 209-213
        • Goossens H.
        • Vlaes L.
        • Butzler J.P.
        • et al.
        Campylobacter upsaliensis enteritis associated with canine infections.
        Lancet. 1991; 337: 1486-1487
        • Olson P.
        • Sandstedt K.
        Campylobacter in the dog: a clinical and experimental study.
        Vet Rec. 1987; 121: 99-101
        • Prescott J.F.
        • Bruin-Mosch C.W.
        Carriage of Campylobacter jejuni in healthy and diarrheic animals.
        Am J Vet Res. 1981; 42: 164-165
        • Bruce D.
        • Zochowsky W.
        • Fleming G.A.
        Campylobacter infections in cats and dogs.
        Vet Rec. 1980; 107: 200-201
        • Torre E.
        • Tello M.
        Factors influencing fecal shedding of Campylobacter jejuni in dogs without diarrhea.
        Am J Vet Res. 1993; 54: 260-262
        • Fox J.G.
        • Moore R.
        • Ackerman J.I.
        Campylobacter jejuni-associated diarrhea in dogs.
        J Am Vet Med Assoc. 1983; 183: 1430-1433
        • Skirrow M.B.
        Campylobacter enteritis in dogs and cats: a ‘new’ zoonosis.
        Vet Res Commun. 1981; 5: 13-19
        • Robinson D.A.
        Infective dose of Campylobacter jejuni in milk.
        BMJ (Clin Res Ed). 1981; 282: 1584-1585
        • Butzler J.P.
        • Skirrow M.B.
        Campylobacter enteritis.
        Clin Gastroenterol. 1979; 8: 737-765
        • Burnens A.P.
        • Nicolet J.
        Detection of Campylobacter upsaliensis in diarrheic dogs and cats, using a selective medium with cefoperazone.
        Am J Vet Res. 1992; 53: 48-51
        • Aspinall S.T.
        • Wareing D.R.
        • Hayward P.G.
        • et al.
        A comparison of a new campylobacter selective medium (CAT) with membrane filtration for the isolation of thermophilic campylobacters including Campylobacter upsaliensis.
        J Appl Bacteriol. 1996; 80: 645-650
        • Boosinger T.R.
        • Dillon A.R.
        Campylobacter jejuni infections in dogs and the effect of erythromycin and tetracycline therapy on fecal shedding.
        J Am Anim Hosp Assoc. 1992; 28: 33-38
        • Monfort J.D.
        • Donahoe J.P.
        • Stills H.F.
        • et al.
        Efficacies of erythromycin and chloramphenicol in extinguishing fecal shedding of Campylobacter jejuni in dogs.
        J Am Vet Med Assoc. 1990; 196: 1069-1072
        • Pai C.H.
        • Gillis G.
        • Toumanen E.
        • et al.
        Erythromycin in treatment of Campylobacter enteritis in children.
        Am J Dis Child. 1983; 137: 286-288
        • Davies A.P.
        • Gebhart C.J.
        • Meric S.A.
        Campylobacter-associated chronic diarrhea in a dog.
        J Am Vet Med Assoc. 1984; 184: 469-471
        • Mead P.S.
        • Slutsker L.
        • Dietz V.
        • et al.
        Food-related illness and death in the United States.
        Emerg Infect Dis. 1999; 5: 607-625
        • Fukata T.
        • Naito F.
        • Yoshida N.
        • et al.
        Incidence of Salmonella infection in healthy dogs in Gifu Prefecture, Japan.
        J Vet Med Sci. 2002; 64: 1079-1080
        • Kwaga J.K.
        • Adesiyun A.A.
        • Abdullahi S.U.
        • et al.
        Prevalence of salmonellae, shigellae and Plesiomonas shigelloides in dogs in Zaria, Nigeria.
        Br Vet J. 1989; 145: 174-177
        • Sato Y.
        • Kuwamoto R.
        A case of canine salmonellosis due to Salmonella infantis.
        J Vet Med Sci. 1999; 61: 71-72
        • van Duijkeren E.
        • Houwers D.
        Salmonella enteritis in dogs, not relevant?.
        Tijdschr Diergeneeskd. 2002; 127: 716-717
        • Joffe D.J.
        • Schlesinger D.P.
        Preliminary assessment of the risk of Salmonella infection in dogs fed raw chicken diets.
        Can Vet J. 2002; 43: 441-442
        • Bäumler A.J.
        • Tsolis R.M.
        • Heffron F.
        Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium.
        Infect Immun. 1996; 64: 1862-1865
        • Francis C.L.
        • Ryan T.A.
        • Jones B.D.
        • et al.
        Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria.
        Nature. 1993; 364: 639-642
        • Choudhary S.P.
        • Kalimuddin M.
        • Brasad G.
        • et al.
        Observations on natural and experimental salmonellosis in dogs.
        J Diarrhoeal Dis Res. 1985; 3: 149-153
        • Day H.H.
        • James E.
        • Heather C.D.
        Salmonellosis in the dog.
        Am J Vet Res. 1963; 24: 156-158
        • Wolf M.K.
        Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli.
        Clin Microbiol Rev. 1997; 10: 569-584
        • Beutin L.
        • Geier D.
        • Steinruck H.
        • et al.
        Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals.
        J Clin Microbiol. 1993; 31: 2483-2488
        • Hammermueller J.
        • Kruth S.
        • Prescott J.
        • et al.
        Detection of toxin genes in Escherichia coli isolated from normal dogs and dogs with diarrhea.
        Can J Vet Res. 1995; 59: 265-270
        • Starcic M.
        • Johnson J.R.
        • Stell A.L.
        • et al.
        Haemolytic Escherichia coli isolated from dogs with diarrhea have characteristics of both uropathogenic and necrotoxigenic strains.
        Vet Microbiol. 2002; 85: 361-377
        • Hart C.A.
        • Batt R.M.
        • Saunders J.R.
        Diarrhea caused by Escherichia coli.
        Ann Trop Paediatr. 1993; 13: 121-131
        • Alexander T.J.L.
        Neonatal diarrhoea in pigs.
        in: Gyles C.L. Escherichia coli in domestic animals and humans. CAB International, Guilford, UK1994: 151-170
        • Olson O.
        • Hedhammer A.
        • Faris A.
        • et al.
        Enterotoxigenic Escherichia coli (ETEC) and Klebsiella pneumoniae isolated from dogs with diarrhea.
        Vet Microbiol. 1985; 10: 577-589
        • Sears C.L.
        • Kaper J.B.
        Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion.
        Microbiol Rev. 1996; 60: 167-215
        • Richter T.
        • Grund S.
        • Hellmann E.
        Occurrence of enterotoxic E. coli in the young dog. Description of probable pathogenicity factors.
        Berl Muench Tierarztl Wochenschr. 1984; 97: 37-43
        • Drolet R.
        • Fairbrother J.M.
        • Harel J.
        • et al.
        Attaching and effacing and enterotoxigenic Escherichia coli associated with enteric colibacillosis in the dog.
        Can J Vet Res. 1994; 58: 87-92
        • Beutin L.
        • Geier D.
        • Zimmermann S.
        • et al.
        Virulence markers of Shiga-like toxin-producing Escherichia coli strains originating from healthy domestic animals of different species.
        J Clin Microbiol. 1995; 33: 631-635
        • Prada J.
        • Baljer G.
        • De Rycke J.
        • et al.
        Characteristics of alpha-hemolytic strains of Escherichia coli isolated from dogs with gastroenteritis.
        Vet Microbiol. 1991; 29: 59-73
        • Turk J.
        • Maddox C.
        • Fales W.
        • et al.
        Examination for heat-labile, heat stable, and Shiga-like toxins and for the eaeA gene in Escherichia coli isolates obtained from dogs dying with diarrhea: 122 cases (1992–1996).
        J Am Vet Med Assoc. 1998; 212: 1735-1736
        • Donnenberg M.S.
        Enteropathogenic Escherichia coli.
        in: Blaser M.J. Raudin J.I. Greenberg H.B. Guerrant R.L. Infections of the gastrointestinal tract. Raven Press, New York1995: 709-726
        • Jerse A.E.
        • Yu J.
        • Tall B.D.
        • et al.
        A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells.
        Proc Natl Acad Sci USA. 1990; 87: 7839-7843
        • Penteado A.S.
        • Aidar L.
        • Pestana de Castro A.F.
        • et al.
        eae-negative attaching and effacing Escherichia coli from piglets with diarrhea.
        Res Microbiol. 2001; 152: 75-81
        • Konowalchuk J.
        • Speirs J.I.
        • Stavric S.
        Vero response to a cytotoxin of Escherichia coli.
        Infect Immun. 1977; 18: 775-779
        • O'Brian A.D.
        • LaVeck G.D.
        • Thompson M.R.
        Production of Shigella dysenteriae type I-like cytotoxin by Escherichia coli.
        J Infect Dis. 1982; 146: 763-769
        • Calderwood S.B.
        • Acheson D.W.K.
        • Keusch T.
        • et al.
        Proposed new nomenclature for SLT (VT) family.
        ASM News. 1994; 62: 118-119
        • Beutin L.
        • Montenegro M.
        • Orskov I.
        • et al.
        Close association of verotoxin (shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli.
        J Clin Microbiol. 1989; 27: 2559-2564
        • Boyce T.G.
        • Swerdlow D.L.
        • Griffin P.M.
        Escherichia coli O157 and the hemolytic-uremic syndrome.
        N Engl J Med. 1995; 333: 364-368
        • Trevena W.B.
        • Hooper S.
        • Wray C.
        • et al.
        Vero cytotoxin-producing Escherichia coli O157 associated with companion animals.
        Vet Rec. 1996; 138: 400
        • Pohl P.
        • Oswald E.
        • Van Muylem K.
        • et al.
        Escherichia coli producing CNF1 and CNF2 cytotoxins in animals with different disorders.
        Vet Res. 1993; 24: 311-315
        • Nataro J.P.
        • Kaper J.B.
        Diarrheogenic Escherichia coli.
        Clin Microbiol Rev. 1998; 11: 142-201
        • Pass M.A.
        • Odedra R.
        • Batt R.M.
        Multiplex PCRs for identification of Escherichia coli virulence genes.
        J Clin Microbiol. 2000; 38: 2001-2004
        • Jertborn M.
        • Svennerholm A.M.
        Enterotoxin-producing bacteria isolated from Swedish travellers with diarrhoea.
        Scand J Infect Dis. 1991; 23: 473-479
        • Olive D.M.
        Detection of enterotoxigenic Escherichia coli after polymerase chain reaction amplification with a thermostable DNA polymerase.
        J Clin Microbiol. 1989; 27: 261-265
        • Pollard D.R.
        • Johnson W.M.
        • Lior H.
        • et al.
        Rapid and specific detection of verotoxin genes in Escherichia coli by the polymerase chain reaction.
        J Clin Microbiol. 1990; 28: 540-545
        • Monaghan C.
        • Tierney U.
        • Colleran E.
        Antibiotic resistance and R-factors in the fecal coliform flora of urban and rural dogs.
        Antimicrob Agents Chemother. 1981; 19: 266-270
        • Wong C.S.
        • Brandt J.R.
        Risk of hemolytic uremic syndrome from antibiotic treatment of Escherichia coli O157:H7 colitis.
        JAMA. 2002; 288: 3111-3112
        • Aranda-Michel J.
        • Giannella R.A.
        Acute diarrhea: a practical review.
        Am J Med. 1999; 106: 670-676
        • Baljer G.
        • Hinsch F.
        • Mayr B.
        Clinical experience with kennel-specific E. coli oral vaccines in dogs.
        Tierarztl Prax. 1990; 18: 65-68
        • Malnick H.
        • Thomas M.
        • Lotay H.
        • et al.
        Anaerobiospirillum species isolated from humans with diarrhoea.
        J Clin Pathol. 1983; 36: 1097-1101
        • Malnick H.
        Anaerobiospirillum thomasii sp. nov., an anaerobic spiral bacterium isolated from the feces of cats and dogs and from diarrheal feces of humans, and emendation of the genus Anaerobiospirillum.
        Int J Syst Bacteriol. 1997; 47: 381-384
        • Malnick H.
        • Williams K.
        • Phil-Ebosie J.
        • et al.
        Description of a medium for isolating Anaerobiospirillum spp., a possible cause of zoonotic disease, from diarrheal feces and blood of humans and use of the medium in a survey of human, canine, and feline feces.
        J Clin Microbiol. 1990; 28: 1380-1384
        • Fenwick S.G.
        • Madie P.
        • Wilks C.R.
        Duration of carriage and transmission of Yersinia enterocolitica biotype 4, serotype 0:3 in dogs.
        Epidemiol Infect. 1994; 113: 471-477
        • Hayashidani H.
        • Kaneko K.
        • Sakurai K.
        • et al.
        Experimental infection with Yersinia enterocolitica serovar 0:8 in beagle dogs.
        Vet Microbiol. 1995; 47: 71-77
        • Tiwary B.K.
        • Prasad L.B.
        Enteric infection in livestock and poultry caused by Salmonellae and Shigellae.
        Vet Rec. 1972; 91: 510-513