1
Campylobacter and risk factors associated with dog ownership: a retrospective study in household and in shelter dogs
VetIt.2299.15789.1

Keywords

Campylobacter
Campylobacteriosis
Dogs
Risk factors
Shelter dogs
antibiotic resistance

How to Cite

Iannino, F., Di Donato, G., Salucci, S., Ruggieri, E., Vincifori, G., Danzetta, M. L., Dalla Villa, P., Di Giannatale, E., Lotti, G., & De Massis, F. (2022). Campylobacter and risk factors associated with dog ownership: a retrospective study in household and in shelter dogs. Veterinaria Italiana, 58(1), 59–66. https://doi.org/10.12834/VetIt.2299.15789.1

Abstract

Campylobacteriosis has been the most frequently reported zoonotic disease in humans in Europe. The scientific literature has reported that the role of dogs may be relevant. The objectives of this work are to improve the knowledge about Campylobacter spp. carriage, infection and antimicrobial resistance in household and shelter dogs in Italy, and to assess risk factors at the dog/human interface. During the 2015‑2016 period, rectal swabs were collected from 431 household vet‑visiting dogs and 173 dogs housed in shelters. A total of 3 veterinary clinics, located in three Italian regions (Abruzzo, Molise and Tuscany) and 10 shelters, five in Abruzzo and five in Molise, were included in the study. Relevant risk factors for the transmission of Campylobacter spp. from dogs to humans were assessed by means of a questionnaire administered to owners of household dogs. For Campylobacter spp. isolation, selective cultivation methods were used, followed by confirmation and species identification with the PCR method. Phenotypic antibiotic resistance profiles assayed using antimicrobial susceptibility testing were combined. Campylobacter spp. were isolated from 9 household dogs (2.1% CI 1.1% ‑ 3.9%) and from 13 shelter dogs (7.5 % CI 4.5% ‑ 12.4%). In household dogs C. jejuni was the most represented species (0.9%). In shelter dogs, the most common species was C. jejuni (5.2%). Campylobacter spp. isolates were resistant to ciprofloxacin (22.73%), nalidixic acid (22.73%), tetracyclines (27.27%), streptomycin (9.09%) and erythromycin (4.55%). The main C. jejuni Clonal Complex identified in dogs were CC21, CC45, CC206, CC403, CC42 and CC658. The risk of contracting Campylobacteriosis from dogs remains a concrete reality. This risk is increased in the presence of common habits, as shown by the data from the questionnaire. Prevalence control of Campylobacter spp. in household and shelter dogs would be important in order to reduce the transmission to humans.

https://doi.org/10.12834/VetIt.2299.15789.1
VetIt.2299.15789.1

References

Acke E., McGill K., Golden O., Jones B.R., Fanning S. & Whyte P. 2009. Prevalence of thermophilic campylobacter species in household cats and dogs in Ireland. Vet Rec, 164, 44–47.

Adak G.K., Meakins S.M., Yip H., Lopman B.A. & O'Brien S.J. 2005. Disease risks from foods, England and Wales, 1996-2000. Emerg Infect Dis, 11, 365–372.

Amar C., Kittl S., Spreng D., Thomann A., Korczak B. M., Burnens A. P. & Kuhnert P. 2014. Genotypes and antibiotic resistance of canine Campylobacter jejuni isolates. Vet Microbiol, 168, 124–130.

Andrzejewska M., Szczepańska B., Klawe J. J., Spica D. & Chudzińska M. 2013. Prevalence of Campylobacter jejuni and Campylobacter coli species in cats and dogs from Bydgoszcz (Poland) region. Pol J Vet Sci, 16, 115–120.

Berger J.O. 1985. Statistical Decision Theory and Bayesian Analysis. New York, Springer-Verlag.

Boya U.O., Dotson M.J. & Hyatt E.M. 2012. Dimensions of the dog–human relationship: a segmentation approach. J Target Meas Anal Mark, 20, 133–143.

Brooks P. T., Brakel K.A., Bell J.A., Bejcek C.E., Gilpin T., Brudvig J. M. & Mansfield L.S. 2017. Transplanted human fecal microbiota enhanced Guillain Barré syndrome autoantibody responses after Campylobacter jejuni infection in C57BL/6 mice. Microbiome, 5(1), 1-22.

Brown C., Martin V. & Chitwood S. 1999. An outbreak of enterocolitis due to campylobacter spp. in a beagle colony. J Vet Diagn Invest, 11, 374–376.

Chaban B., Ngeleka M. & Hill J.E. 2010. Detection and quantification of 14 campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals. BMC Microbiol, 10, 73.

Charles N. 2016. Post-human families? Dog-human relations in the domestic sphere. Sociol Res Online, 21, 1–12.

Dingle K.E., Colles F.M., Wareing D.R., Ure R., Fox A.J., Bolton F.E., Bootsma H.J., Willems R.J., Urwin R. & Maiden M.C. 2001. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol, 39, 14–23.

Domingues A R., Pires S.M., Halasa T. & Hald T. 2012. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Epidemiol Infect, 140, 970–981.

Doorduyn Y., Van Den Brandhof W. E., Van Duynhoven Y.T.H.P., Breukink B.J., Wagenaar J.A. & Van Pelt W. 2010. Risk factors for indigenous Campylobacter jejuni and Campylobacter coli infections in The Netherlands: a case-control study. Epidemiol Infect, 138(10), 1391-1404.

Esan O.B., Pearce M., van Hecke O., Roberts N., Collins D., Violato M., McCarthy N., Perera R. & Fanshawe T. R. 2017. Factors associated with sequelae of Campylobacter and non-typhoidal Salmonella infections: a systematic review. EBioMedicine, 15, 100-111.

European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). 2018. The European union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2017. EFSA J, 16, 5500.

Fox J.G. 1990. Campylobacteriosis. In Infectious diseases of dog and cat. (Greene C.E. ed.) 2nd ed. Philadelphia, PA, WB Saunders, 226–248.

Gahamanyi N., Mboera L.E., Matee M.I., Mutangana D. & Komba E.V. 2020. Prevalence, Risk Factors, and Antimicrobial Resistance Profiles of Thermophilic Campylobacter Species in Humans and Animals in Sub-Saharan Africa: A Systematic Review. Int J Microbiol, 2092478.

Giacomelli M., Follador N., Coppola L.M., Martini M. & Piccirillo A. 2015. Survey of Campylobacter spp. in owned and unowned dogs and cats in Northern Italy. Survey of campylobacter spp. in owned and unowned dogs and cats in Northern Italy. Vet J, 204, 333–337.

Gras L.M., Smid J.H., Wagenaar J.A., Koene M.G.J., Havelaar A.H., Friesema I.H.M. & Busani L. 2013. Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets. Epidemiol Infect, 141(12), 2526-2535.

Guardabassi L Schwarz S Lloyd D. 2004. Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother, 54, 321–332.

Guest C.M., Stephen J.M. & Price C.J. 2007. Prevalence of campylobacter and four endoparasites in dog populations associated with hearing dogs. J Small Anim Pract, 48, 632–637.

Hellgren J., Hästö L.S., Wikström C., Fernström L.L. & Hansson I. 2019. Occurrence of Salmonella, Campylobacter, Clostridium and Enterobacteriaceae in raw meat-based diets for dogs. Vet Rec,184, 442.

Holmberg M., Rosendal T., Engvall E. O., Ohlson A. & Lindberg A. 2015. Prevalence of thermophilic Campylobacter species in swedish dogs and characterization of C. jejuni isolates. Acta Vet Scand, 57, 19.

Ibrahim J N., Eghnatio E., El Ro, A., Fardoun T. & Ghssein G. 2019. Prevalence, antimicrobial resistance and risk factors for campylobacteriosis in Lebanon. J Infect Dev Ctries, 13(01), 11-20.

Kaakoush N.O., Castaño-Rodríguez N., Mitchell H.M. & Man S.M. 2015. Global epidemiology of Campylobacter infection. Clin Microbiol Rev, 28(3), 687-720.

Kärenlampi R., Rautelin H., Schönberg-Norio D., Paulin L. & Hänninen M.L. 2007. Longitudinal study of finnish Campylobacter jejuni and C. coli isolates from humans, using multilocus sequence typing, including comparison with epidemiological data and isolates from poultry and cattle. Appl Environ Microbiol, 73, 148–155.

Keithlin J., Sargeant J., Thomas M.K. & Fazil A. 2014. Systematic review and meta-analysis of the proportion of campylobacter cases that develop chronic sequelae. BMC Public Health, 14, 1203.

Koene M.G., Houwers D.J., Dijkstra J.R., Duim B. & Wagenaar J.A. 2004. Simultaneous presence of multiple campylobacter species in dogs. J Clin Microbiol, 42, 819–821.

Kurnar R., Verma A.K., Kurnar A., Srivastava M., Lal H.P. 2012. Prevalence and antibiogram of campylobacter infections in dogs of Mathura, India. Asian J Anim Vet Adv, 7, 434–740.

Leonard E.K., Pearl D L., Janecko N., Weese J.S., Reid-Smith R.J., Peregrine A.S. & Finley R.L. 2011. Factors related to campylobacter spp. carriage in client-owned dogs visiting veterinary clinics in a region of Ontario, Canada. Epidemiol Infect, 139, 1531–1541.

World Organisation for Animal Health (OIE). 2008. Manual of diagnostic tests and vaccines for terrestrial animals. Chapter 2.9.3. Campylobacter jejuni and Campylobacter coli. OIE, Paris.

Mazick A., Ethelberg S., Møller Nielsen E., Mølbak K. & Lisby M. 2006.An outbreak of campylobacter jejuni associated with consumption of chicken, Copenhagen, 2005. Euro Surveill, 11, 137–139.

Mohan V. 2015. Faeco-prevalence of campylobacter jejuni in urban wild birds and pets in New Zealand. BMC Res Notes, 8, 1.

Siemer B.L., Harrington C.S., Nielsen E.M., Borck B., Nielsen N.L., Engberg J. & On S.L. 2004. Genetic relatedness among campylobacter jejuni serotyped isolates of diverse origin as determined by numerical analysis of amplified fragment length polymorphism (AFLP) profiles. J Appl Microbiol, 96, 795–802.

Strother K.O., Steelman C.D. & Gbur E.E. 2005. Reservoir competence of lesser mealworm (Coleoptera: Tenebrionidae) for campylobacter jejuni (Campylobacterales: Campylobacteraceae). J Med Entomol, 42 (1), 42–47.

Stull J W., Peregrine A S., Sargeant J. M. & Weese J.S. 2013. Pet husbandry and infection control practices related to zoonotic disease risks in Ontario, Canada. BMC Public Health, 13(1), 520.

Tam C.C., O'Brien S J., Adak G.K., Meakins S.M. & Frost J.A. 2003.Campylobacter coli - an important foodborne pathogen. J Infect, 47, 28–32.

Tenkate T.D. & Stafford R.J. 2001. Risk factors for campylobacter infection in infants and young children: a matched case-control study. Epidemiol Infect, 127, 399–404.

Wang G., Clark C.G., Taylor T.M., Pucknell C., Barton C., Price L., Woodward D.L. & Rodgers F.G. 2002. Colony multiplex PCR assay for identification and differentiation of campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol, 40, 4744–4747.

Copyright (c) 2022 Filomena Iannino, Guido Di Donato, Stefania Salucci, Enzo Ruggieri, Giacomo Vincifori, Maria Luisa Danzetta, Paolo Dalla Villa, Elisabetta Di Giannatale, Giulia Lotti, Fabrizio De Massis