A Systematic Review and Meta-Analysis of the Campylobacter spp. Prevalence and Concentration in Household Pets and Petting Zoo Animals for Use in Exposure Assessments

Animal contact is a potential transmission route for campylobacteriosis, and both domestic household pet and petting zoo exposures have been identified as potential sources of exposure. Research has typically focussed on the prevalence, concentration, and transmission of zoonoses from farm animals to humans, yet there are gaps in our understanding of these factors among animals in contact with the public who don’t live on or visit farms. This study aims to quantify, through a systematic review and meta-analysis, the prevalence and concentration of Campylobacter carriage in household pets and petting zoo animals. Four databases were accessed for the systematic review (PubMed, CAB direct, ProQuest, and Web of Science) for papers published in English from 1992–2012, and studies were included if they examined the animal population of interest, assessed prevalence or concentration with fecal, hair coat, oral, or urine exposure routes (although only articles that examined fecal routes were found), and if the research was based in Canada, USA, Europe, Australia, and New Zealand. Studies were reviewed for qualitative synthesis and meta-analysis by two reviewers, compiled into a database, and relevant studies were used to create a weighted mean prevalence value. There were insufficient data to run a meta-analysis of concentration values, a noted study limitation. The mean prevalence of Campylobacter in petting zoo animals is 6.5% based on 7 studies, and in household pets the mean is 24.7% based on 34 studies. Our estimated concentration values were: 7.65x103cfu/g for petting zoo animals, and 2.9x105cfu/g for household pets. These results indicate that Campylobacter prevalence and concentration are lower in petting zoo animals compared with household pets and that both of these animal sources have a lower prevalence compared with farm animals that do not come into contact with the public. There is a lack of studies on Campylobacter in petting zoos and/or fair animals in Canada and abroad. Within this literature, knowledge gaps were identified, and include: a lack of concentration data reported in the literature for Campylobacter spp. in animal feces, a distinction between ill and diarrheic pets in the reported studies, noted differences in shedding and concentrations for various subtypes of Campylobacter, and consistent reporting between studies.

[1]  T. Cheasty,et al.  Verocytotoxin- producing Escherichia coli 0157 on a farm open to the public: outbreak investigation and longitudinal bacteriological study , 2000, Veterinary Record.

[2]  M. Eidson,et al.  Outbreaks of enteric disease associated with animal contact: not just a foodborne problem anymore. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[3]  M. Poore,et al.  Prevalence of and Risk Factors for Feline Tritrichomonas foetus and Giardia Infection , 2004, Journal of Clinical Microbiology.

[4]  N. Garrett,et al.  Campylobacteriosis in New Zealand: results of a case-control study. , 1997, Journal of epidemiology and community health.

[5]  J. House,et al.  Compendium of measures to prevent disease associated with animals in public settings, 2013. , 2013, Journal of the American Veterinary Medical Association.

[6]  P. Gerner-Smidt,et al.  Spatial distribution and registry-based case-control analysis of Campylobacter infections in Denmark, 1991-2001. , 2005, American journal of epidemiology.

[7]  A. Torralbo,et al.  Campylobacter spp., C. jejuni and C. upsaliensis infection-associated factors in healthy and ill dogs from clinics in Cordoba, Spain. Screening tests for antimicrobial susceptibility. , 2012, Comparative immunology, microbiology and infectious diseases.

[8]  J. Gray,et al.  The increasing application of multiplex nucleic acid detection tests to the diagnosis of syndromic infections , 2013, Epidemiology and Infection.

[9]  J. Weese,et al.  Pet husbandry and infection control practices related to zoonotic disease risks in Ontario, Canada , 2013, BMC Public Health.

[10]  N. Cave,et al.  Identification of Tritrichomonas foetus and Giardia spp. infection in pedigree show cats in New Zealand , 2010, New Zealand veterinary journal.

[11]  Compendium of measures to prevent disease associated with animals in public settings, 2005. , 2005, MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports.

[12]  R C Andrew Thompson,et al.  The zoonotic significance and molecular epidemiology of Giardia and giardiasis. , 2004, Veterinary parasitology.

[13]  J. Bono,et al.  Shiga-toxigenic Escherichia coli O157 in Agricultural Fair Livestock, United States , 2006, Emerging infectious diseases.

[14]  Kerrie Mengersen,et al.  Handbook of Meta-analysis in Ecology and Evolution , 2013 .

[15]  E. Atwill,et al.  Cross-sectional study of faecal shedding of Giardia duodenalis and Cryptosporidium parvum among packstock in the Sierra Nevada Range. , 2010, Equine veterinary journal.

[16]  R. Chalmers,et al.  Cryptosporidium parvum infection in orphan lambs on a farm open to the public , 2007, Veterinary Record.

[17]  P. Kass,et al.  Evaluation of a routine diagnostic fecal panel for dogs with diarrhea. , 2002, Journal of the American Veterinary Medical Association.

[18]  E. Engvall,et al.  Isolation and Identification of Thermophilic Campylobacter Species in Faecal Samples from Swedish Dogs , 2003, Scandinavian journal of infectious diseases.

[19]  E. de Boer,et al.  Public farms: hygiene and zoonotic agents , 2007, Epidemiology and Infection.

[20]  B. Chaban,et al.  Multiple zoonotic pathogens identified in canine feces collected from a remote Canadian indigenous community. , 2010, The American journal of tropical medicine and hygiene.

[21]  M. Olson,et al.  Prevalence and diagnosis of Giardia infection in dogs and cats using a fecal antigen test and fecal smear. , 2010, The Canadian veterinary journal = La revue veterinaire canadienne.

[22]  J. Nicolet,et al.  Detection of Campylobacter upsaliensis in diarrheic dogs and cats, using a selective medium with cefoperazone. , 1992, American journal of veterinary research.

[23]  S. Villeneuve,et al.  Detection and characterization of Campylobacter spp. from 40 dairy cattle herds in Quebec, Canada. , 2014, Foodborne pathogens and disease.

[24]  L. Kreienbrock,et al.  Giardia in symptomatic dogs and cats in Europe--results of a European study. , 2010, Veterinary parasitology.

[25]  M. Evans,et al.  Hazards of Healthy Living: Bottled Water and Salad Vegetables as Risk Factors for Campylobacter Infection , 2003, Emerging infectious diseases.

[26]  S. Sheppard,et al.  Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. , 2009, Foodborne pathogens and disease.

[27]  P. McDonough,et al.  Prevalence of enteric zoonotic agents in cats less than 1 year old in central New York State. , 2001, Journal of veterinary internal medicine.

[28]  M. Woodward,et al.  Prevalence of attaching and effacing Escherichia coli serogroup O103 in orphan lambs on an open farm in eastern England , 2007, Veterinary Record.

[29]  D. Toney,et al.  An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm. , 2002, The New England journal of medicine.

[30]  S. Hemsworth,et al.  Pet ownership in immunocompromised children--a review of the literature and survey of existing guidelines. , 2006, European journal of oncology nursing : the official journal of European Oncology Nursing Society.

[31]  K. Jones,et al.  Cattle and sheep farms as reservoirs of Campylobacter , 2003, Journal of applied microbiology.

[32]  C. Panuska,et al.  Prevalence of and risk factors associated with shedding of Cryptosporidium felis in domestic cats of Mississippi and Alabama. , 2009, Veterinary parasitology.

[33]  L. J. Lund,et al.  Haemorrhagic colitis in child after visit to farm visitor centre , 1995, The Lancet.

[34]  S. Bunčić,et al.  Potential for the spread of Escherichia coli O157, Salmonella, and Campylobacter in the lairage environment at abattoirs. , 2002, Journal of food protection.

[35]  M. Cassidy,et al.  Exploring historical Canadian foodborne outbreak data sets for human illness attribution. , 2009, Journal of food protection.

[36]  Y. V. van Duynhoven,et al.  Escherichia coli O157 infection associated with a petting zoo , 2002, Epidemiology and Infection.

[37]  J. Weese,et al.  Reducing the risk of pet-associated zoonotic infections , 2015, Canadian Medical Association Journal.

[38]  M. Cormican,et al.  Prevalence of Gastrointestinal Bacterial Pathogens in a Population of Zoo Animals , 2008, Zoonoses and public health.

[39]  J. Lejeune,et al.  Outbreaks of zoonotic enteric disease associated with animal exhibits. , 2004, Journal of the American Veterinary Medical Association.

[40]  R. D. du Bois,et al.  Rare Diseases , 1946, Handbook Integrated Care.

[41]  G. Pinchbeck,et al.  A case–control study of pathogen and lifestyle risk factors for diarrhoea in dogs , 2011, Preventive Veterinary Medicine.

[42]  M. Sydney,et al.  Campylobacter upsaliensis: Another Pathogen for Consideration in the United States , 2002 .

[43]  R. Danila,et al.  Recurrent outbreaks of cryptosporidiosis associated with calves among students at an educational farm programme, Minnesota, 2003 , 2006, Epidemiology and Infection.

[44]  F. Mégraud,et al.  The seasonal distribution of campylobacter infection in nine European countries and New Zealand , 2002, Epidemiology and Infection.

[45]  J. Sargeant,et al.  Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae , 2014, BMC Public Health.

[46]  T. Cheasty,et al.  Escherichia coli O157 infection associated with a farm visitor centre. , 1995, Communicable disease report. CDR review.

[47]  A. Peregrine,et al.  Evaluation of the zoonotic potential of Giardia duodenalis in fecal samples from dogs and cats in Ontario. , 2011, The Canadian veterinary journal = La revue veterinaire canadienne.

[48]  S. Schleicher,et al.  Petting zoo-associated Escherichia coli 0157:h7--secondary transmission, asymptomatic infection, and prolonged shedding in the classroom. , 2004, Canada communicable disease report = Releve des maladies transmissibles au Canada.

[49]  Ainslie J Butler,et al.  Expert elicitation as a means to attribute 28 enteric pathogens to foodborne, waterborne, animal contact, and person-to-person transmission routes in Canada. , 2015, Foodborne pathogens and disease.

[50]  R. Shukla,et al.  Cryptosporidium spp. and other zoonotic enteric parasites in a sample of domestic dogs and cats in the Niagara region of Ontario. , 2006, The Canadian veterinary journal = La revue veterinaire canadienne.

[51]  Gaunt Mc,et al.  A survey of intestinal parasites in dogs from Saskatoon, Saskatchewan. , 2011 .

[52]  J. Dow,et al.  Outbreak of Escherichia coli 0157:H7 related to animal contact at a petting zoo. , 2002, The Canadian journal of infectious diseases = Journal canadien des maladies infectieuses.

[53]  D. Gow,et al.  Prevalence of Potentially Pathogenic Enteric Organisms in Clinically Healthy Kittens in the UK , 2009, Journal of feline medicine and surgery.

[54]  J. Wylie,et al.  Spatial analysis of campylobacter infection in the Canadian province of Manitoba , 2006, International journal of health geographics.

[55]  J. Weese,et al.  Factors related to Campylobacter spp. carriage in client-owned dogs visiting veterinary clinics in a region of Ontario, Canada , 2011, Epidemiology and Infection.

[56]  D. Lindsay,et al.  Prevalence of canine parasites based on fecal flotation , 1996 .

[57]  T. García,et al.  Determination of food authenticity by enzyme-linked immunosorbent assay (ELISA) , 2008 .

[58]  Y. Whitfield,et al.  Household pets and zoonoses , 2014 .

[59]  K. Heuner,et al.  Molecular characterization of Legionella pneumophila-induced interleukin-8 expression in T cells , 2010, BMC Microbiology.

[60]  T. Cheasty,et al.  Transmission of Vero cytotoxin producing Escherichia coli O157 infection from farm animals to humans in Cornwall and west Devon. , 1999, Communicable disease and public health.

[61]  P. Michel,et al.  The association between campylobacteriosis, agriculture and drinking water: a case-case study in a region of British Columbia, Canada, 2005–2009 , 2014, Epidemiology and Infection.

[62]  D. E. Johnston,et al.  The compendium on continuing education for the practicing veterinarian , 1984 .

[63]  J. Wood,et al.  Foal diarrhoea between 1991 and 1994 in the United Kingdom associated with Clostridium perfringens, rotavirus, Strongyloides westeri and Cryptosporidium spp. , 1996, Epidemiology and Infection.

[64]  R. Gilman,et al.  Transmission dynamics of Taenia solium and potential for pig-to-pig transmission. , 2006, Parasitology international.

[65]  R. Derlet,et al.  An analysis of human pathogens found in horse/mule manure along the John Muir Trail in Kings Canyon and Sequoia and Yosemite National Parks. , 2002, Wilderness & environmental medicine.

[66]  S. J. Billington,et al.  Potential virulence and antimicrobial susceptibility of Campylobacter jejuni isolates from food and companion animals. , 2004, Foodborne pathogens and disease.

[67]  N. French,et al.  Prevalence and Genetic Diversity of Campylobacter spp. in Environmental Water Samples from a 100-Square-Kilometer Predominantly Dairy Farming Area , 2005, Applied and Environmental Microbiology.

[68]  J. Ellis,et al.  Exposure to infectious agents in dogs in remote coastal British Columbia: Possible sentinels of diseases in wildlife and humans. , 2011, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[69]  L. Wieler,et al.  Genomic Heterogeneity and O-Antigenic Diversity ofCampylobacter upsaliensis and Campylobacter helveticus Strains Isolated from Dogs and Cats in Germany , 2001, Journal of Clinical Microbiology.

[70]  C. Blackmore,et al.  Outbreak of Shiga toxin-producing Escherichia coli O157 infection associated with a day camp petting zoo--Pinellas County, Florida, May-June 2007. , 2009, MMWR. Morbidity and mortality weekly report.

[71]  S. Groft,et al.  Rare diseases epidemiology , 2010 .

[72]  R. Reporter,et al.  Campylobacter upsaliensis: Another pathogen for consideration in the United States. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[73]  P J Diggle,et al.  Spatio-temporal epidemiology of Campylobacter jejuni enteritis, in an area of Northwest England, 2000–2002 , 2010, Epidemiology and Infection.

[74]  T. Cheasty,et al.  Vero Cytotoxin–Producing Escherichia coli O157 Gastroenteritis in Farm Visitors, North Wales , 2003, Emerging infectious diseases.

[75]  J. Weese,et al.  Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoonotic potential. , 2011, The Veterinary clinics of North America. Small animal practice.

[76]  G. Duckworth,et al.  Escherichia coli O157 incident associated with a farm open to members of the public. , 1999, Communicable disease and public health.

[77]  D. Wells Comparison of two treatments for preventing dogs eating their own faeces , 2003, Veterinary Record.

[78]  P. Sockett,et al.  Enteric and foodborne disease in children: A review of the influence of food- and environment-related risk factors. , 2001, Paediatrics & child health.

[79]  A. Hofhuis,et al.  Two outbreaks of campylobacteriosis associated with the consumption of raw cows' milk. , 2009, International journal of food microbiology.

[80]  R. Christley,et al.  Risk factors for the carriage of Campylobacter upsaliensis by dogs in a community in Cheshire , 2009, Veterinary Record.

[81]  B. Blagburn,et al.  Prevalence of intestinal parasites in companion animals in Ontario and Quebec, Canada, during the winter months. , 2008, Veterinary therapeutics : research in applied veterinary medicine.

[82]  S. Sokolow,et al.  Epidemiologic evaluation of diarrhea in dogs in an animal shelter. , 2005, American journal of veterinary research.

[83]  I. Robertson,et al.  High prevalence of Giardia detected in cats by PCR. , 2003, Veterinary parasitology.

[84]  C. DebRoy,et al.  Screening Petting Zoo Animals for the Presence of Potentially Pathogenic Escherichia Coli , 2006, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[85]  R. Chalmers,et al.  Distribution of Cryptosporidium species in sheep in the UK. , 2008, Veterinary parasitology.

[86]  G. Pinchbeck,et al.  Detection of endoparasites with zoonotic potential in dogs with gastrointestinal disease in the UK. , 2008, Transboundary and emerging diseases.

[87]  J. Traub-Dargatz,et al.  The prevalence of Cryptosporidium/Giardia in the trail horse population utilizing public lands in Colorado , 1998, Journal of Equine Veterinary Science.

[88]  G. D. Inglis,et al.  Direct Quantification of Campylobacter jejuni and Campylobacter lanienae in Feces of Cattle by Real-Time Quantitative PCR , 2004, Applied and Environmental Microbiology.

[89]  M. Tobin-D'Angelo,et al.  Estimates of enteric illness attributable to contact with animals and their environments in the United States. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[90]  L. Hutwagner,et al.  An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. , 1998, The Journal of pediatrics.

[91]  B. Rechel,et al.  Investigation of a spatiotemporal cluster of verotoxin-producing Escherichia coli O157 infections in eastern England in 2007. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[92]  T. Graczyk,et al.  Equine Cryptosporidium parvum infections in western Poland , 2004, Parasitology Research.

[93]  H. Goossens,et al.  Campylobacter upsaliensis enteritis associated with canine infections , 1991, The Lancet.

[94]  N. Cohen,et al.  Prevalence of and risk factors for fecal shedding of Cryptosporidium parvum oocysts in horses. , 1998, Journal of the American Veterinary Medical Association.

[95]  M. Hänninen,et al.  Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. , 2008, Veterinary microbiology.

[96]  P. Chapman,et al.  Infection with verocytotoxin-producing Escherichia coli O157 during a visit to an inner city open farm , 2000, Epidemiology and Infection.

[97]  T. Nolan,et al.  Endoparasite prevalence and recurrence across different age groups of dogs and cats. , 2009, Veterinary parasitology.

[98]  Louise Matthews,et al.  Geographic determinants of reported human Campylobacter infections in Scotland , 2010, BMC public health.

[99]  J. D. Greig,et al.  Analysis of foodborne outbreak data reported internationally for source attribution. , 2009, International journal of food microbiology.

[100]  D. Bowman,et al.  Prevalence of Giardia in symptomatic dogs and cats throughout the United States as determined by the IDEXX SNAP Giardia test. , 2006, Veterinary therapeutics : research in applied veterinary medicine.

[101]  J. Reif,et al.  Prevalence of enteric zoonotic organisms in cats. , 2000, Journal of the American Veterinary Medical Association.

[102]  Evers Eg,et al.  Campylobacter source attribution by exposure assessment , 2008 .

[103]  A. Peregrine,et al.  Prevalence of zoonotic agents in dogs visiting hospitalized people in Ontario: implications for infection control. , 2006, The Journal of hospital infection.

[104]  David J Spiegelhalter,et al.  A re-evaluation of random-effects meta-analysis , 2009, Journal of the Royal Statistical Society. Series A,.

[105]  T. Hald,et al.  Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. , 2010, Foodborne pathogens and disease.

[106]  Richard Smith,et al.  Verocytotoxigenic Escherichia coli O157 in animals on public amenity premises in England and Wales, 1997 to 2007 , 2009, Veterinary Record.

[107]  L. Warnick,et al.  Prevalence of shiga toxin-encoding bacteria and shiga toxin-producing Escherichia coli isolates from dairy farms and county fairs. , 2006, Veterinary microbiology.

[108]  S. Giguère,et al.  Infectious Agents Detected in the Feces of Diarrheic Foals: A Retrospective Study of 233 Cases (2003–2008) , 2009, Journal of veterinary internal medicine.

[109]  J. Gerberding,et al.  Outbreaks of Escherichia coli O157:H7 associated with petting zoos--North Carolina, Florida, and Arizona, 2004 and 2005. , 2005, MMWR. Morbidity and mortality weekly report.

[110]  I. Connerton,et al.  Occurrence of campylobacters in small domestic and laboratory animals. , 1993, The Journal of applied bacteriology.

[111]  G. Markegard,et al.  Age, geographic, and temporal distribution of fecal shedding of Cryptosporidium parvum oocysts in cow-calf herds. , 1999, American journal of veterinary research.

[112]  Notes from the field: Escherichia coli O157:H7 gastroenteritis associated with a State Fair - North Carolina, 2011. , 2012, MMWR. Morbidity and mortality weekly report.

[113]  Steen Ethelberg,et al.  Spatio-temporal cluster analysis of the incidence of Campylobacter cases and patients with general diarrhea in a Danish county, 1995–2004 , 2009, International journal of health geographics.

[114]  R. Roberts,et al.  Modification of a Rapid Method for the Identification of Gene-Specific Polymorphisms inCryptosporidiumparvum and Its Application to Clinical and Epidemiological Investigations , 2001, Applied and Environmental Microbiology.

[115]  O. Rosef,et al.  Thermophilic campylobacters in surface water: A potential risk of campylobacteriosis , 2001, International journal of environmental health research.

[116]  A. Carr,et al.  A survey of intestinal parasites in dogs from Saskatoon, Saskatchewan. , 2011, The Canadian veterinary journal = La revue veterinaire canadienne.

[117]  B. Chaban,et al.  Detection and quantification of 14 Campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals , 2010, BMC Microbiology.

[118]  M. Lappin,et al.  Effect of the Probiotic Enterococcus faecium SF68 on Presence of Diarrhea in Cats and Dogs Housed in an Animal Shelter , 2011, Journal of veterinary internal medicine.

[119]  T. Christidis,et al.  A Comparative Exposure Assessment of Campylobacter in Ontario, Canada , 2017, Risk analysis : an official publication of the Society for Risk Analysis.

[120]  L. Geue,et al.  Zoonotic Agents in Small Ruminants Kept on City Farms in Southern Germany , 2012, Applied and Environmental Microbiology.

[121]  G. Pinchbeck,et al.  Prevalence of Cryptosporidium, Giardia and Isospora species infections in pet cats with clinical signs of gastrointestinal disease , 2008, Journal of feline medicine and surgery.

[122]  R. Christley,et al.  Prevalence of Campylobacter spp. in a cross-sectional study of dogs attending veterinary practices in the UK and risk indicators associated with shedding. , 2010, Veterinary journal.

[123]  M. S. Patel,et al.  An introduction to meta-analysis. , 1989, Health Policy.

[124]  M Sandberg,et al.  Risk factors for Campylobacter infection in Norwegian cats and dogs. , 2002, Preventive veterinary medicine.

[125]  A. Maderner,et al.  Detection of Cryptosporidium species in feces or gastric contents from snakes and lizards as determined by polymerase chain reaction analysis and partial sequencing of the 18S ribosomal RNA gene , 2011, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[126]  J. Weese,et al.  Observation of practices at petting zoos and the potential impact on zoonotic disease transmission. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[127]  M. Madsen,et al.  Longitudinal Study of the Excretion Patterns of Thermophilic Campylobacter spp. in Young Pet Dogs in Denmark , 2004, Journal of Clinical Microbiology.

[128]  L. Glickman,et al.  Prevalence and risk factors for Giardia and coccidia species of pet cats in 2003–2004 , 2006, Journal of feline medicine and surgery.

[129]  J. Weese,et al.  Recurrent diarrhea associated with enterotoxigenic Clostridium perfringens in 2 dogs. , 2001, The Canadian veterinary journal = La revue veterinaire canadienne.

[130]  Andrea Nesbitt,et al.  Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. , 2013, Foodborne pathogens and disease.

[131]  S. Hajat,et al.  Climate variability and campylobacter infection: an international study , 2005, International journal of biometeorology.

[132]  M. Lappin,et al.  Prevalence of enteric pathogens in dogs of north-central Colorado. , 2003, Journal of the American Animal Hospital Association.

[133]  J. Arsenault Épidémiologie spatiale de la campylobactériose au Québec , 2011 .

[134]  J. Collins,et al.  Prevalence of thermophilic Campylobacter species in cats and dogs in two animal shelters in Ireland , 2006, Veterinary Record.

[135]  J. Line,et al.  Comparison of challenge models for determining the colonization dose of Campylobacter jejuni in broiler chicks. , 2008, Poultry science.

[136]  S. Marks,et al.  Prevalence of selected bacterial and parasitic agents in feces from diarrheic and healthy control cats from Northern California. , 2012, Journal of veterinary internal medicine.

[137]  M. Evans,et al.  A milk-borne campylobacter outbreak following an educational farm visit , 1996, Epidemiology and Infection.

[138]  M. Barton,et al.  Campylobacter species in cats and dogs in South Australia. , 1999, Australian veterinary journal.

[139]  OUTBREAKS OF ESCHERICHIA COLI O157:H7 INFECTIONS AMONG CHILDREN ASSOCIATED WITH FARM VISITS , 2001 .

[140]  J. Yang,et al.  A survey of the prevalence of Giardia in dogs presented to Canadian veterinary practices. , 2001, The Canadian veterinary journal = La revue veterinaire canadienne.

[141]  E. Rind,et al.  The spatial distribution of campylobacteriosis in New Zealand, 1997–2005 , 2010, Epidemiology and Infection.

[142]  M. Madsen,et al.  Healthy puppies and kittens as carriers of Campylobacter spp., with special reference to Campylobacter upsaliensis , 1997, Journal of clinical microbiology.

[143]  S. A. Shulman,et al.  Epidemiologic features of Campylobacter infection among cats in the upper midwestern United States. , 2005, Journal of the American Veterinary Medical Association.

[144]  C. Guest,et al.  Prevalence of Campylobacter and four endoparasites in dog populations associated with Hearing Dogs. , 2007, The Journal of small animal practice.

[145]  J. Dewulf,et al.  PCR detection of Campylobacter species in feces from dogs , 2008, Vlaams Diergeneeskundig Tijdschrift.

[146]  M. J. Nicholls,et al.  Prevalence of faecal excretion of verocytotoxigenic Escherichia coli 0157 in cattle in England and Wales , 2003, Veterinary Record.