Carriage of Extended Spectrum Beta Lactamase-Producing Escherichia coli: Prevalence and Factors Associated with Fecal Colonization of Dogs from a Pet Clinic in Lower Saxony, Germany
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design and Inclusion of Participants
2.2. Questionnaire
2.3. Sample Collection and Laboratory Processing
2.4. Statistical Analysis
3. Results
3.1. Study Population
3.2. Status of ESBL-Carriage and Basic Questionnaire Variables
4. Discussion
4.1. Husbandry Conditions
4.2. Contact with Puppies
4.3. Feeding Customs
4.4. Antibiotic Treatment
4.5. Feeding Supplements
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tenaillon, O.; Skurnik, D.; Picard, B.; Denamur, E. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 2010, 8, 207–217. [Google Scholar] [CrossRef]
- Jang, J.; Hur, H.G.; Sadowsky, M.J.; Byappanahalli, M.N.; Yan, T.; Ishii, S. Environmental Escherichia coli: Ecology and public health implications-a review. J. Appl. Microbiol. 2017, 123, 570–581. [Google Scholar] [CrossRef] [PubMed]
- Tenaillon, O.; Barrick, J.E.; Ribeck, N.; Deatherage, D.E.; Blanchard, J.L.; Dasgupta, A.; Wu, G.C.; Wielgoss, S.; Cruveiller, S.; Médigue, C.; et al. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 2016, 536, 165–170. [Google Scholar] [CrossRef] [PubMed]
- Gronvold, A.M.; L’Abee-Lund, T.M.; Sorum, H.; Skancke, E.; Yannarell, A.C.; Mackie, R.I. Changes in fecal microbiota of healthy dogs administered amoxicillin. FEMS Microbiol. Ecol. 2010, 71, 313–326. [Google Scholar] [CrossRef] [PubMed]
- Guardabassi, L.; Schwarz, S.; Lloyd, D.H. Pet animals as reservoirs of antimicrobial-resistant bacteria. J. Antimicrob. Chemother. 2004, 54, 321–332. [Google Scholar] [CrossRef]
- Rantala, M.; Lahti, E.; Kuhalampil, J.; Pesonen, S.; Jarvinen, A.K.; Saijonmaa, K.; Honkanen-Buzalski, T. Antimicrobial resistance in Staphylococcus spp., Escherichia coli and Enterococcus spp. in dogs given antibiotics for chronic dermatological disorders, compared with non-treated control dogs. Acta Vet. Scand. 2004, 45, 37–45. [Google Scholar] [CrossRef] [PubMed]
- Leimbach, A.; Hacker, J.; Dobrindt, U. E. coli as an all-rounder: The thin line between commensalism and pathogenicity. Curr. Top Microbiol. Immunol. 2013, 358, 3–32. [Google Scholar] [CrossRef]
- Markey, B.; Leonard, F.; Archambault, M.; Cullinane, A.; Maguire, D. Clinical Veterinary Microbiology E-Book; Elsevier Health Sciences: Amsterdam, The Netherlands, 2013. [Google Scholar]
- O’Keefe, A.; Hutton, T.A.; Schifferli, D.M.; Rankin, S.C. First detection of CTX-M and SHV extended-spectrum beta-lactamases in Escherichia coli urinary tract isolates from dogs and cats in the United States. Antimicrob. Agents Chemother. 2010, 54, 3489–3492. [Google Scholar] [CrossRef]
- Wu, G.; Day, M.J.; Mafura, M.T.; Nunez-Garcia, J.; Fenner, J.J.; Sharma, M.; van Essen-Zandbergen, A.; Rodriguez, I.; Dierikx, C.; Kadlec, K.; et al. Comparative analysis of ESBL-positive Escherichia coli isolates from animals and humans from the UK, The Netherlands and Germany. PLoS ONE 2013, 8, e75392. [Google Scholar] [CrossRef]
- Damborg, P.; Broens, E.M.; Chomel, B.B.; Guenther, S.; Pasmans, F.; Wagenaar, J.A.; Weese, J.S.; Wieler, L.H.; Windahl, U.; Vanrompay, D.; et al. Bacterial Zoonoses Transmitted by Household Pets: State-of-the-Art and Future Perspectives for Targeted Research and Policy Actions. J. Comp. Pathol. 2016, 155, S27–S40. [Google Scholar] [CrossRef] [Green Version]
- Rubin, J.E.; Pitout, J.D. Extended-spectrum beta-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet. Microbiol. 2014, 170, 10–18. [Google Scholar] [CrossRef]
- Hernández, J.R.; Martínez-Martínez, L.; Cantón, R.; Coque, T.M.; Pascual, A. Nationwide study of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum beta-lactamases in Spain. Antimicrob. Agents Chemother. 2005, 49, 2122–2125. [Google Scholar] [CrossRef]
- Baede, V.O.; Wagenaar, J.A.; Broens, E.M.; Duim, B.; Dohmen, W.; Nijsse, R.; Timmerman, A.J.; Hordijk, J. Longitudinal study of extended-spectrum-beta-lactamase- and AmpC-producing Enterobacteriaceae in household dogs. Antimicrob. Agents Chemother. 2015, 59, 3117–3124. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, Y.; Ikeda, F.; Kamimura, T.; Yokota, Y.; Mine, Y. Novel plasmid-mediated beta-lactamase from Escherichia coli that inactivates oxyimino-cephalosporins. Antimicrob. Agents Chemother. 1988, 32, 1243–1246. [Google Scholar] [CrossRef]
- Ewers, C.; Bethe, A.; Semmler, T.; Guenther, S.; Wieler, L.H. Extended-spectrum beta-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: A global perspective. Clin. Microbiol. Infect 2012, 18, 646–655. [Google Scholar] [CrossRef] [PubMed]
- Teshager, T.; Dominguez, L.; Moreno, M.A.; Saenz, Y.; Torres, C.; Cardenosa, S. Isolation of an SHV-12 beta-lactamase-producing Escherichia coli strain from a dog with recurrent urinary tract infections. Antimicrob. Agents Chemother. 2000, 44, 3483–3484. [Google Scholar] [CrossRef] [PubMed]
- Marques, C.; Belas, A.; Franco, A.; Aboim, C.; Gama, L.T.; Pomba, C. Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J. Antimicrob. Chemother. 2018, 73, 377–384. [Google Scholar] [CrossRef]
- Nienhoff, U.; Kadlec, K.; Chaberny, I.F.; Verspohl, J.; Gerlach, G.-F.; Schwarz, S.; Simon, D.; Nolte, I. Transmission of methicillin-resistant Staphylococcus aureus strains between humans and dogs: Two case reports. J. Antimicrob. Chemother. 2009, 64, 660–662. [Google Scholar] [CrossRef]
- Walther, B.; Tedin, K.; Lubke-Becker, A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet. Microbiol. 2017, 200, 71–78. [Google Scholar] [CrossRef]
- Hertz, F.B.; Schonning, K.; Rasmussen, S.C.; Littauer, P.; Knudsen, J.D.; Lobner-Olesen, A.; Frimodt-Moller, N. Epidemiological factors associated with ESBL- and non ESBL-producing E. coli causing urinary tract infection in general practice. Infect Dis. 2016, 48, 241–245. [Google Scholar] [CrossRef]
- Keshi, L.; Weiwei, X.; Shoulin, L.; Xiadong, L.; Hao, W.; Junhai, J.; Xiangwei, W.; Rui, W.; Pei, Z. Analysis of drug resistance of extended-spectrum beta-lactamases-producing Escherichia coli and Klebsiella pneumoniae in children with urinary tract infection. Saudi Med. J. 2019, 40, 1111–1115. [Google Scholar] [CrossRef] [PubMed]
- Tuuminen, T.; Osterblad, M.; Hamalainen, S.; Sironen, R. Relapsing sepsis episodes of Escherichia coli with CTX-M ESBL or derepressed ampC genes in a patient with chronic autoimmune pancreatitis complicated by IgG4 hypergammaglobulinaemia. New Microbes New Infect. 2016, 9, 50–53. [Google Scholar] [CrossRef]
- van Hout, D.; Verschuuren, T.D.; Bruijning-Verhagen, P.C.J.; Bosch, T.; Schurch, A.C.; Willems, R.J.L.; Bonten, M.J.M.; Kluytmans, J. Extended-spectrum beta-lactamase (ESBL)-producing and non-ESBL-producing Escherichia coli isolates causing bacteremia in the Netherlands (2014–2016) differ in clonal distribution, antimicrobial resistance gene and virulence gene content. PLoS ONE 2020, 15, e0227604. [Google Scholar] [CrossRef]
- CLSI Supplement M100; Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. Clinical and Laboratory Standartds Institute: Wayne, PA, USA, 2017.
- Waked, R.; Saliba, G.; Chehata, N.; Haddad, E.; Chedid, M.; Choucair, J. Extended spectrum beta lactamase producing Escherichia coli tricuspid valve endocarditis. IDCases 2020, 19, e00729. [Google Scholar] [CrossRef]
- Madigan, T.; Johnson, J.R.; Clabots, C.; Johnston, B.D.; Porter, S.B.; Slater, B.S.; Banerjee, R. Extensive Household Outbreak of Urinary Tract Infection and Intestinal Colonization due to Extended-Spectrum beta-Lactamase-Producing Escherichia coli Sequence Type 131. Clin. Infect Dis. 2015, 61, e5–e12. [Google Scholar] [CrossRef]
- Vet01SEd5; Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals. 5th ed. Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2020.
- Roschanski, N.; Fischer, J.; Guerra, B.; Roesler, U. Development of a multiplex real-time PCR for the rapid detection of the predominant beta-lactamase genes CTX-M, SHV, TEM and CIT-type AmpCs in Enterobacteriaceae. PLoS ONE 2014, 9, e100956. [Google Scholar] [CrossRef]
- Aslantas, O.; Yilmaz, E.S. Prevalence and molecular characterization of extended-spectrum beta-lactamase (ESBL) and plasmidic AmpC beta-lactamase (pAmpC) producing Escherichia coli in dogs. J. Vet. Med. Sci. 2017, 79, 1024–1030. [Google Scholar] [CrossRef]
- Hering, J.; Hille, K.; Fromke, C.; von Munchhausen, C.; Hartmann, M.; Schneider, B.; Friese, A.; Roesler, U.; Merle, R.; Kreienbrock, L. Prevalence and potential risk factors for the occurrence of cefotaxime resistant Escherichia coli in German fattening pig farms--a cross-sectional study. Prev. Vet. Med. 2014, 116, 129–137. [Google Scholar] [CrossRef]
- Rabold, D.; Espelage, W.; Abu Sin, M.; Eckmanns, T.; Schneeberg, A.; Neubauer, H.; Möbius, N.; Hille, K.; Wieler, L.H.; Seyboldt, C.; et al. The zoonotic potential of Clostridium difficile from small companion animals and their owners. PLoS ONE 2018, 13, e0193411. [Google Scholar] [CrossRef]
- Rzewuska, M.; Stefanska, I.; Kizerwetter-Swida, M.; Chrobak-Cmiel, D.; Szczygielska, P.; Lesniak, M.; Binek, M. Characterization of Extended-Spectrum-beta-Lactamases Produced by Escherichia coli Strains Isolated from Dogs in Poland. Pol. J. Microbiol. 2015, 64, 285–288. [Google Scholar] [CrossRef]
- Wedley, A.L.; Maddox, T.W.; Westgarth, C.; Coyne, K.P.; Pinchbeck, G.L.; Williams, N.J.; Dawson, S. Prevalence of antimicrobial-resistant Escherichia coli in dogs in a cross-sectional, community-based study. Vet. Rec. 2011, 168, 354. [Google Scholar] [CrossRef]
- Wedley, A.L.; Dawson, S.; Maddox, T.W.; Coyne, K.P.; Pinchbeck, G.L.; Clegg, P.; Nuttall, T.; Kirchner, M.; Williams, N.J. Carriage of antimicrobial resistant Escherichia coli in dogs: Prevalence, associated risk factors and molecular characteristics. Vet. Microbiol. 2017, 199, 23–30. [Google Scholar] [CrossRef]
- Damborg, P.; Morsing, M.K.; Petersen, T.; Bortolaia, V.; Guardabassi, L. CTX-M-1 and CTX-M-15-producing Escherichia coli in dog faeces from public gardens. Acta Vet. Scand. 2015, 57, 83. [Google Scholar] [CrossRef]
- Gandolfi-Decristophoris, P.; Petrini, O.; Ruggeri-Bernardi, N.; Schelling, E. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in healthy companion animals living in nursing homes and in the community. Am. J. Infect. Control 2013, 41, 831–835. [Google Scholar] [CrossRef]
- Huber, H.; Zweifel, C.; Wittenbrink, M.M.; Stephan, R. ESBL-producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland. Vet. Microbiol. 2013, 162, 992–996. [Google Scholar] [CrossRef]
- Carattoli, A.; Lovari, S.; Franco, A.; Cordaro, G.; Di Matteo, P.; Battisti, A. Extended-spectrum beta-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003. Antimicrob. Agents Chemother. 2005, 49, 833–835. [Google Scholar] [CrossRef]
- Costa, D.; Poeta, P.; Saenz, Y.; Coelho, A.C.; Matos, M.; Vinue, L.; Rodrigues, J.; Torres, C. Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Vet. Microbiol. 2008, 127, 97–105. [Google Scholar] [CrossRef]
- Ewers, C.; Grobbel, M.; Stamm, I.; Kopp, P.A.; Diehl, I.; Semmler, T.; Fruth, A.; Beutlich, J.; Guerra, B.; Wieler, L.H.; et al. Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta-lactamase-producing Escherichia coli among companion animals. J. Antimicrob. Chemother. 2010, 65, 651–660. [Google Scholar] [CrossRef]
- Schaufler, K.; Bethe, A.; Lubke-Becker, A.; Ewers, C.; Kohn, B.; Wieler, L.H.; Guenther, S. Putative connection between zoonotic multiresistant extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli in dog feces from a veterinary campus and clinical isolates from dogs. Infect. Ecol. Epidemiol. 2015, 5, 25334. [Google Scholar] [CrossRef]
- Haenni, M.; Saras, E.; Metayer, V.; Medaille, C.; Madec, J.Y. High prevalence of blaCTX-M-1/IncI1/ST3 and blaCMY-2/IncI1/ST2 plasmids in healthy urban dogs in France. Antimicrob. Agents Chemother. 2014, 58, 5358–5362. [Google Scholar] [CrossRef] [Green Version]
- Belas, A.; Salazar, A.S.; Gama, L.T.; Couto, N.; Pomba, C. Risk factors for faecal colonisation with Escherichia coli producing extended-spectrum and plasmid-mediated AmpC beta-lactamases in dogs. Vet. Rec. 2014, 175, 202. [Google Scholar] [CrossRef]
- Suay-Garcia, B.; Galan, F.; Rodriguez-Iglesias, M.A.; Perez-Gracia, M.T. Detection and Characterization of Extended-Spectrum Beta-Lactamases-Producing Escherichia coli in Animals. Vector Borne Zoonotic Dis. 2018, 19, 115–120. [Google Scholar] [CrossRef]
- Hordijk, J.; Schoormans, A.; Kwakernaak, M.; Duim, B.; Broens, E.; Dierikx, C.; Mevius, D.; Wagenaar, J.A. High prevalence of fecal carriage of extended spectrum beta-lactamase/AmpC-producing Enterobacteriaceae in cats and dogs. Front. Microbiol. 2013, 4, 242. [Google Scholar] [CrossRef]
- Schmiedel, J.; Falgenhauer, L.; Domann, E.; Bauerfeind, R.; Prenger-Berninghoff, E.; Imirzalioglu, C.; Chakraborty, T. Multiresistant extended-spectrum beta-lactamase-producing Enterobacteriaceae from humans, companion animals and horses in central Hesse, Germany. BMC Microbiol. 2014, 14, 187. [Google Scholar] [CrossRef]
- Shaheen, B.W.; Nayak, R.; Foley, S.L.; Kweon, O.; Deck, J.; Park, M.; Rafii, F.; Boothe, D.M. Molecular characterization of resistance to extended-spectrum cephalosporins in clinical Escherichia coli isolates from companion animals in the United States. Antimicrob. Agents Chemother. 2011, 55, 5666–5675. [Google Scholar] [CrossRef]
- Rocha-Gracia, R.C.; Cortes-Cortes, G.; Lozano-Zarain, P.; Bello, F.; Martinez-Laguna, Y.; Torres, C. Faecal Escherichia coli isolates from healthy dogs harbour CTX-M-15 and CMY-2 beta-lactamases. Vet. J. 2015, 203, 315–319. [Google Scholar] [CrossRef]
- Yousfi, M.; Mairi, A.; Touati, A.; Hassissene, L.; Brasme, L.; Guillard, T.; De Champs, C. Extended spectrum beta-lactamase and plasmid mediated quinolone resistance in Escherichia coli fecal isolates from healthy companion animals in Algeria. J. Infect. Chemother. 2016, 22, 431–435. [Google Scholar] [CrossRef]
- Sallem, R.B.; Gharsa, H.; Slama, K.B.; Rojo-Bezares, B.; Estepa, V.; Porres-Osante, N.; Jouini, A.; Klibi, N.; Saenz, Y.; Boudabous, A.; et al. First detection of CTX-M-1, CMY-2, and QnrB19 resistance mechanisms in fecal Escherichia coli isolates from healthy pets in Tunisia. Vector Borne Zoonotic Dis. 2013, 13, 98–102. [Google Scholar] [CrossRef]
- So, J.H.; Kim, J.; Bae, I.K.; Jeong, S.H.; Kim, S.H.; Lim, S.K.; Park, Y.H.; Lee, K. Dissemination of multidrug-resistant Escherichia coli in Korean veterinary hospitals. Diagn. Microbiol. Infect. Dis. 2012, 73, 195–199. [Google Scholar] [CrossRef]
- Sun, Y.; Zeng, Z.; Chen, S.; Ma, J.; He, L.; Liu, Y.; Deng, Y.; Lei, T.; Zhao, J.; Liu, J.H. High prevalence of bla(CTX-M) extended-spectrum beta-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clin. Microbiol. Infect 2010, 16, 1475–1481. [Google Scholar] [CrossRef]
- Albrechtova, K.; Kubelova, M.; Mazancova, J.; Dolejska, M.; Literak, I.; Cizek, A. High prevalence and variability of CTX-M-15-producing and fluoroquinolone-resistant Escherichia coli observed in stray dogs in rural Angola. Microb. Drug Resist. 2014, 20, 372–375. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, V.M.; Pinchbeck, G.L.; Nuttall, T.; McEwan, N.; Dawson, S.; Williams, N.J. Antimicrobial resistance risk factors and characterisation of faecal E. coli isolated from healthy Labrador retrievers in the United Kingdom. Prev. Vet. Med. 2015, 119, 31–40. [Google Scholar] [CrossRef] [PubMed]
- Kuhnke, D. Occurrence of ESBL-producing Escherichia coli in healthy, living foodproducing animals in Europe: A systematic review. CAB Rev. 2020, 15, 1–13. [Google Scholar] [CrossRef]
- De Graef, E.M.; Decostere, A.; Devriese, L.A.; Haesebrouck, F. Antibiotic resistance among fecal indicator bacteria from healthy individually owned and kennel dogs. Microb. Drug Resist. 2004, 10, 65–69. [Google Scholar] [CrossRef]
- Harada, K.; Morimoto, E.; Kataoka, Y.; Takahashi, T. Clonal spread of antimicrobial-resistant Escherichia coli isolates among pups in two kennels. Acta Vet. Scand. 2011, 53, 11. [Google Scholar] [CrossRef] [PubMed]
- Rota, A.; Milani, C.; Corro, M.; Drigo, I.; Borjesson, S. Misuse of antimicrobials and selection of methicillin-resistant Staphylococcus pseudintermedius strains in breeding kennels: Genetic characterization of bacteria after a two-year interval. Reprod. Domest. Anim. 2013, 48, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Johnson, J.R.; Clabots, C.; Kuskowski, M.A. Multiple-host sharing, long-term persistence, and virulence of Escherichia coli clones from human and animal household members. J. Clin. Microbiol. 2008, 46, 4078–4082. [Google Scholar] [CrossRef]
- Johnson, J.R.; Stell, A.L.; Delavari, P. Canine feces as a reservoir of extraintestinal pathogenic Escherichia coli. Infect. Immun. 2001, 69, 1306–1314. [Google Scholar] [CrossRef]
- Low, D.A.; Braaten, B.A.; Ling, G.V.; Johnson, D.L.; Ruby, A.L. Isolation and comparison of Escherichia coli strains from canine and human patients with urinary tract infections. Infect. Immun. 1988, 56, 2601–2609. [Google Scholar] [CrossRef]
- Munnich, A.; Lubke-Becker, A. Escherichia coli infections in newborn puppies--clinical and epidemiological investigations. Theriogenology 2004, 62, 562–575. [Google Scholar] [CrossRef]
- Tamang, M.D.; Nam, H.M.; Gurung, M.; Jang, G.C.; Kim, S.R.; Jung, S.C.; Park, Y.H.; Lim, S.K. Molecular characterization of CTX-M beta-lactamase and associated addiction systems in Escherichia coli circulating among cattle, farm workers, and the farm environment. Appl. Environ. Microbiol. 2013, 79, 3898–3905. [Google Scholar] [CrossRef]
- van Hoek, A.; Dierikx, C.; Bosch, T.; Schouls, L.; van Duijkeren, E.; Visser, M. Transmission of ESBL-producing Escherichia coli between broilers and humans on broiler farms. J. Antimicrob. Chemother. 2019, 75, 543–549. [Google Scholar] [CrossRef]
- Davies, R.H.; Lawes, J.R.; Wales, A.D. Raw diets for dogs and cats: A review, with particular reference to microbiological hazards. J. Small Anim. Pract. 2019, 60, 329–339. [Google Scholar] [CrossRef]
- Weese, J.S.; Rousseau, J.; Arroyo, L. Bacteriological evaluation of commercial canine and feline raw diets. Can Vet. J. 2005, 46, 513–516. [Google Scholar]
- Strohmeyer, R.A.; Morley, P.S.; Hyatt, D.R.; Dargatz, D.A.; Scorza, A.V.; Lappin, M.R. Evaluation of bacterial and protozoal contamination of commercially available raw meat diets for dogs. J. Am. Vet. Med. Assoc. 2006, 228, 537–542. [Google Scholar] [CrossRef]
- Freeman, L.M.; Chandler, M.L.; Hamper, B.A.; Weeth, L.P. Current knowledge about the risks and benefits of raw meat-based diets for dogs and cats. J. Am. Vet. Med. Assoc. 2013, 243, 1549–1558. [Google Scholar] [CrossRef]
- Clark, C.; Cunningham, J.; Ahmed, R.; Woodward, D.; Fonseca, K.; Isaacs, S.; Ellis, A.; Anand, C.; Ziebell, K.; Muckle, A.; et al. Characterization of Salmonella associated with pig ear dog treats in Canada. J. Clin. Microbiol. 2001, 39, 3962–3968. [Google Scholar] [CrossRef]
- Morelli, G.; Catellani, P.; Miotti Scapin, R.; Bastianello, S.; Conficoni, D.; Contiero, B.; Ricci, R. Evaluation of microbial contamination and effects of storage in raw meat-based dog foods purchased online. J. Anim. Physiol. Anim. Nutr. 2019, 104, 690–697. [Google Scholar] [CrossRef]
- Pitout, J.D.; Reisbig, M.D.; Mulvey, M.; Chui, L.; Louie, M.; Crowe, L.; Church, D.L.; Elsayed, S.; Gregson, D.; Ahmed, R.; et al. Association between handling of pet treats and infection with Salmonella enterica serotype newport expressing the AmpC beta-lactamase, CMY-2. J. Clin. Microbiol. 2003, 41, 4578–4582. [Google Scholar] [CrossRef]
- Leonard, E.K.; Pearl, D.L.; Janecko, N.; Finley, R.L.; Reid-Smith, R.J.; Weese, J.S.; Peregrine, A.S. Risk factors for carriage of antimicrobial-resistant Salmonella spp and Escherichia coli in pet dogs from volunteer households in Ontario, Canada, in 2005 and 2006. Am. J. Vet. Res. 2015, 76, 959–968. [Google Scholar] [CrossRef]
- van Bree, F.P.J.; Bokken, G.; Mineur, R.; Franssen, F.; Opsteegh, M.; van der Giessen, J.W.B.; Lipman, L.J.A.; Overgaauw, P.A.M. Zoonotic bacteria and parasites found in raw meat-based diets for cats and dogs. Vet. Rec. 2018, 182, 50. [Google Scholar] [CrossRef] [PubMed]
- Hellgren, J.; Hasto, L.S.; Wikstrom, C.; Fernstrom, L.L.; Hansson, I. Occurrence of Salmonella, Campylobacter, Clostridium and Enterobacteriaceae in raw meat-based diets for dogs. Vet. Rec. 2019, 184, 442. [Google Scholar] [CrossRef]
- Naziri, Z.; Derakhshandeh, A.; Firouzi, R.; Motamedifar, M.; Shojaee Tabrizi, A. DNA fingerprinting approaches to trace Escherichia coli sharing between dogs and owners. J. Appl. Microbiol. 2016, 120, 460–468. [Google Scholar] [CrossRef]
- Pfaller, M.A.; Segreti, J. Overview of the epidemiological profile and laboratory detection of extended-spectrum beta-lactamases. Clin. Infect. Dis. 2006, 42 (Suppl. S4), S153–S163. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, V.M.; Pinchbeck, G.; McIntyre, K.M.; Nuttall, T.; McEwan, N.; Dawson, S.; Williams, N.J. Routine antibiotic therapy in dogs increases the detection of antimicrobial-resistant faecal Escherichia coli. J. Antimicrob. Chemother. 2018, 73, 3305–3316. [Google Scholar] [CrossRef] [PubMed]
- van den Bunt, G.; van Pelt, W.; Hidalgo, L.; Scharringa, J.; de Greeff, S.C.; Schurch, A.C.; Mughini-Gras, L.; Bonten, M.J.M.; Fluit, A.C. Prevalence, risk factors and genetic characterisation of extended-spectrum beta-lactamase and carbapenemase-producing Enterobacteriaceae (ESBL-E and CPE): A community-based cross-sectional study, the Netherlands, 2014 to 2016. Eurosurveillance 2019, 24, 1800594. [Google Scholar] [CrossRef] [PubMed]
- Ruh, E.; Zakka, J.; Hoti, K.; Fekrat, A.; Guler, E.; Gazi, U.; Erdogmus, Z.; Suer, K. Extended-spectrum beta-lactamase, plasmid-mediated AmpC beta-lactamase, fluoroquinolone resistance, and decreased susceptibility to carbapenems in Enterobacteriaceae: Fecal carriage rates and associated risk factors in the community of Northern Cyprus. Antimicrob. Resist. Infect. Control 2019, 8, 98. [Google Scholar] [CrossRef]
- Van Aken, S.; Lund, N.; Ahl, J.; Odenholt, I.; Tham, J. Risk factors, outcome and impact of empirical antimicrobial treatment in extended-spectrum beta-lactamase-producing Escherichia coli bacteraemia. Scand. J. Infect. Dis. 2014, 46, 753–762. [Google Scholar] [CrossRef]
Factor (Time Period) | Category | Total | ESBL-pos | ESBL-neg | OR | CI | p | ||
---|---|---|---|---|---|---|---|---|---|
n | n | % | n | % | |||||
Demographic characteristics of the dogs | |||||||||
Gender of the dog | Male | 461 | 36 | 7.8 | 425 | 92.2 | 1 | ||
Female | 539 | 53 | 9.8 | 486 | 90.2 | 1.29 | 0.83–2.01 | 0.2635 | |
Origin | Germany | 774 | 56 | 7.2 | 718 | 92.8 | 1 | ||
Abroad | 225 | 33 | 14.7 | 192 | 85.3 | 2.2 | 1.39–3.49 | 0.0007 | |
Reason of visit | Prevention | 434 | 52 | 12.0 | 382 | 88.0 | 1.95 | 1.25–3.03 | 0.0031 |
Sick | 566 | 37 | 5.5 | 529 | 93.5 | 1 | |||
Husbandry conditions | |||||||||
Multidog household | No | 513 | 30 | 5.8 | 483 | 94.2 | 1 | ||
Yes | 487 | 59 | 12.1 | 428 | 87.9 | 2.22 | 1.40–3.51 | 0.0007 | |
More animals: small mammal | No | 863 | 65 | 7.5 | 798 | 92.5 | 1 | ||
Yes | 137 | 24 | 17.5 | 113 | 82.5 | 2.61 | 1.57–4.33 | 0.0002 | |
More animals: cat | No | 710 | 50 | 7.0 | 660 | 93.0 | 1 | ||
Yes | 290 | 39 | 13.5 | 251 | 86.5 | 2.05 | 1.32–3.2 | 0.0015 | |
More animals: horse | No | 830 | 61 | 7.3 | 769 | 92.7 | 1 | ||
Yes | 170 | 28 | 16.5 | 142 | 83.5 | 2.47 | 1.54–4.03 | 0.0002 | |
More animals: pig | No | 918 | 75 | 8.2 | 843 | 91.8 | 1 | ||
Yes | 82 | 14 | 17.1 | 68 | 82.9 | 2.31 | 1.24–4.3 | 0.0082 | |
Keeping form | Indoor | 874 | 65 | 7.4 | 809 | 92.6 | 1 | ||
Outdoor | 121 | 24 | 19.8 | 97 | 80.2 | 3.08 | 1.84–5.15 | <0.0001 | |
Dog contact with: | Small animals | 739 | 65 | 8.8 | 674 | 91.2 | 1.36 | 0.73–2.5 | 0.33 |
Other animals | 58 | 11 | 19.0 | 47 | 81 | 3.3 | 1.39–7.82 | 0.0069 | |
No contact | 196 | 13 | 6.6 | 183 | 93.4 | 1 | |||
Dog contact with cat | No | 720 | 53 | 7.4 | 667 | 92.6 | 1 | ||
Yes | 280 | 36 | 12.9 | 244 | 87.1 | 1.86 | 1.83–2.91 | 0.0068 | |
Contact with puppy (12 months) | No | 658 | 41 | 6.2 | 617 | 93.8 | 1 | ||
Yes | 321 | 47 | 4.6 | 274 | 85.4 | 2.46 | 1.57–3.82 | <0.0001 | |
Lick owners face (12 months) | Never/rare | 680 | 49 | 7.2 | 631 | 92.8 | 1 | ||
Regularly | 97 | 7 | 7.2 | 90 | 92.8 | 1.00 | 0.44–2.28 | 0.997 | |
Daily | 180 | 32 | 17.8 | 148 | 82.2 | 2.79 | 1.72–4.50 | <0.0001 | |
Stay in Shelter (12 months) | No | 848 | 67 | 7.9 | 781 | 92.1 | 1 | ||
Yes | 122 | 22 | 18.0 | 100 | 82.0 | 2.57 | 1.52–4.33 | 0.0004 | |
Feeding: raw meat | No | 728 | 54 | 7.4 | 674 | 92.6 | 1 | ||
Yes | 246 | 34 | 13.8 | 212 | 86.2 | 2.00 | 1.27–3.16 | 0.0029 | |
Feeding: food residues | No | 66 | 7.9 | 766 | 92.1 | 1 | |||
Yes | 142 | 22 | 15.5 | 120 | 84.5 | 2.13 | 1.27–3.58 | 0.0044 | |
Feeding: treat | No | 305 | 43 | 14.1 | 262 | 85.9 | 2.30 | 1.48–3.58 | 0.0002 |
Yes | 675 | 45 | 6.7 | 630 | 93.3 | 1 | |||
Feeding: supplements | No | 754 | 78 | 10.3 | 676 | 89.7 | 1 | ||
Yes | 201 | 10 | 5.0 | 191 | 95.0 | 0.45 | 0.23–0.89 | 0.0223 | |
Medical history dog | |||||||||
Acute disease | No | 662 | 70 | 10.6 | 592 | 89.4 | 1 | ||
Yes | 299 | 19 | 6.4 | 280 | 93.6 | 0.57 | 0.34–0.97 | 0.0387 | |
Antibiotic treatment (3 months) | No | 797 | 60 | 7.5 | 737 | 92.5 | 1 | ||
Yes | 176 | 29 | 16.5 | 147 | 83.5 | 2.42 | 1.50–3.91 | 0.0003 | |
Contact with any diarrhea patient (12 months) | No | 413 | 27 | 6.5 | 386 | 93.5 | 1 | ||
Yes | 231 | 39 | 16.9 | 192 | 83.1 | 2.90 | 1.73–4.89 | <0.0001 | |
Unknown | 256 | 23 | 6.5 | 333 | 94.5 | 0.99 | 0.57–1.76 | 0.9656 | |
Contact with human with diarrhea (12 months) | No | 931 | 77 | 8.3 | 854 | 91.7 | 1 | ||
Yes | 69 | 12 | 17.4 | 57 | 83.6 | 2.34 | 1.20–4.54 | 0.0124 | |
Contact with animals with diarrhea (12 months) | No | 823 | 60 | 7.3 | 763 | 92.7 | 1 | ||
Yes | 177 | 29 | 16.4 | 148 | 83.6 | 2.49 | 1.55–4.02 | 0.0002 | |
Demographic characteristics and medical history owner | |||||||||
Living environment | Small city | 229 | 11 | 4.8 | 218 | 95.2 | 1 | ||
Rural area | 693 | 74 | 10.7 | 619 | 89.3 | 2.37 | 1.23–4.55 | 0.0095 | |
Large city | 58 | 4 | 6.9 | 54 | 93.1 | 1.47 | 0.45–4.79 | 0.5246 | |
Gender | Male | 233 | 12 | 5.1 | 221 | 94.9 | 1 | ||
Female | 723 | 74 | 10.2 | 649 | 89.8 | 2.1 | 1.12–3.94 | 0.0207 | |
Profession | Other | 631 | 41 | 6.5 | 590 | 93.5 | 1 | ||
No Profession | 200 | 23 | 11.5 | 177 | 88.5 | 1.87 | 1.09–3.20 | 0.0225 | |
Agricultural sector | 128 | 24 | 18.8 | 104 | 81.2 | 3.32 | 1.93–5.73 | <0.0001 | |
Unknown | 41 | 1 | 2.4 | 40 | 97.6 | 0.36 | 0.05–2.68 | 0.3187 | |
Contact with diarrhea patient (12 months) | No | 257 | 15 | 5.8 | 242 | 94.2 | 1 | ||
Yes | 320 | 46 | 14.4 | 274 | 85.6 | 2.71 | 1.48–4.97 | 0.0013 | |
Unknown | 423 | 28 | 6.6 | 395 | 93.4 | 1.14 | 0.6–2.19 | 0.6844 | |
Contact with human with diarrhea (12 months) | No | 891 | 74 | 8.3 | 817 | 9.69 | 1 | ||
Yes | 109 | 15 | 13.8 | 94 | 86.24 | 1.76 | 0.97–3.19 | 0.0619 | |
Contact with animal with diarrhea (12 months) | No | 762 | 55 | 7.2 | 707 | 92.8 | 1 | ||
Yes | 238 | 34 | 14.29 | 204 | 85.71 | 2.14 | 1.36–3.38 | 0.001 | |
Suffered from diarrhea (4 weeks) | No | 902 | 73 | 8.1 | 829 | 91.9 | 1 | ||
Yes | 49 | 8 | 16.3 | 41 | 83.7 | 2.22 | 1.00–4.90 | 0.0496 | |
Unknown | 49 | 8 | 16.3 | 41 | 83.7 | 2.22 | 1.00–4.90 | 0.0496 | |
Antibiotic treatment (2 months) | No | 912 | 73 | 8 | 839 | 92 | 1 | ||
Yes | 43 | 8 | 18.6 | 35 | 81.4 | 2.63 | 1.77–5.88 | 0.0185 |
Factor | Category | Final Multivariable Model | ||
---|---|---|---|---|
OR | CI | p | ||
Husbandry conditions | ||||
Keeping form | Household | 0.0001 | ||
Other | 3.00 | 1.50–6.00 | 0.0019 | |
Contact with puppy last 12 months | No | 0.0001 | ||
Yes | 2.43 | 1.32–4.46 | 0.0044 | |
Feeding: raw meat | No | 0.0001 | ||
Yes | 2.28 | 1.21–4.31 | 0.0110 | |
Feeding: Food residues | No | 0.0001 | ||
Yes | 2.31 | 1.18–4.53 | 0.0151 | |
Feeding: supplements | No | 0.0001 | ||
yes | 0.426 | 0.18–0.96 | 0.0487 | |
Medical history dog | ||||
Antibiotic treatment last 3 months | No | 0.0001 | ||
Yes | 3.03 | 1.62–5.68 | 0.0005 | |
Medical history owner | ||||
Antibiotic treatment last 2 months | No | 0.0001 | ||
Yes | 2.74 | 1.04–7.19 | 0.041 |
Country | % | Reference | Year | Study Details |
---|---|---|---|---|
European Studies | ||||
Cheshire, UK | 0.5 | [34] | 2011 | n = 183, dogs in a semi-rural community |
UK | 1.9 | [35] | 2017 | n = 580, dogs visiting a veterinary practice |
Denmark | 1.9 | [36] | 2015 | n = 209, fecal samples from public garden |
Switzerland | 2.9 | [37] | 2013 | n = 174, nursing homes and vet practice, Enterobacteriaceae |
Poland | 3.4 | [33] | 2015 | n = 119, veterinary faculty, diseased dogs |
Switzerland | 3.4 | [38] | 2013 | n = 59 dogs, urinary samples |
Italy | 4 | [39] | 2005 | n = 298, dog/cat/rat, healthy, diseased, dead |
Portugal | 7.8 | [40] | 2008 | n = 39, healthy pets |
Germany | 10,7 | [41] | 2010 | n = 84 diseased dogs, mainly German samples |
Germany | 12 | [42] | 2015 | n = 100, fecal sample from veterinary faculty and neighborhood |
France | 12.8 | [43] | 2014 | n = 368, healthy dogs, veterinary clinic |
Portugal | 13.2 | [44] | 2014 | n = 151 vet. clinic, not infected dogs, Lisbon |
Turkey | 16.8 | [30] | 2017 | n = 428, healthy dogs, veterinary clinic |
Spain | 17.8 | [45] | 2018 | n = 140 dogs, samples from laboratories, 25 positive samples, no further patient data |
Netherland | 50 | [46] | 2013 | n = 40, 50% diarrhea patients, ESBL/AmpC |
Germany | 52.2 | [47] | 2014 | n = 67 dogs, infected patients |
Non-European Studies | ||||
USA | 3 | [48] | 2011 | n = 944, dogs and cats, samples from veterinary practitioners |
Mexico | 6 | [49] | 2015 | n = 53, healthy dogs in a public area |
Algeria | 14.7 | [50] | 2016 | n = 102 healthy dogs, veterinary practice |
Tunisia | 19.5 | [51] | 2013 | n = 41, veterinary clinic, healthy dogs |
USA | 26.7 | [9] | 2010 | n = 150, dogs and cats, samples from UTI |
Korea | 33.3 | [52] | 2012 | n = 63 hospitalized dogs |
China | 41.3 | [53] | 2010 | n = 240 dog/cat, veterinary clinics/pet shop |
Angola | 75 | [54] | 2014 | n = 17, stray dogs, no medical history known |
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Werhahn Beining, M.; Hartmann, M.; Luebke-Becker, A.; Guenther, S.; Schaufler, K.; Hille, K.; Kreienbrock, L. Carriage of Extended Spectrum Beta Lactamase-Producing Escherichia coli: Prevalence and Factors Associated with Fecal Colonization of Dogs from a Pet Clinic in Lower Saxony, Germany. Animals 2023, 13, 584. https://doi.org/10.3390/ani13040584
Werhahn Beining M, Hartmann M, Luebke-Becker A, Guenther S, Schaufler K, Hille K, Kreienbrock L. Carriage of Extended Spectrum Beta Lactamase-Producing Escherichia coli: Prevalence and Factors Associated with Fecal Colonization of Dogs from a Pet Clinic in Lower Saxony, Germany. Animals. 2023; 13(4):584. https://doi.org/10.3390/ani13040584
Chicago/Turabian StyleWerhahn Beining, Marco, Maria Hartmann, Antina Luebke-Becker, Sebastian Guenther, Katharina Schaufler, Katja Hille, and Lothar Kreienbrock. 2023. "Carriage of Extended Spectrum Beta Lactamase-Producing Escherichia coli: Prevalence and Factors Associated with Fecal Colonization of Dogs from a Pet Clinic in Lower Saxony, Germany" Animals 13, no. 4: 584. https://doi.org/10.3390/ani13040584