Cited by 66Antibiotic Resistance in BacteriaSalmonella and Campylobacter epidemiologyAntibiotic Use and Resistance

Longitudinal Study of Extended-Spectrum-β-Lactamase- and AmpC-Producing Enterobacteriaceae in Household Dogs

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Baede, Valérie O., Wagenaar, Jaap A., Broens, Els M., Duim, Birgitta, Dohmen, Wietske, Nijsse, Rolf, Timmerman, Arjen J., Hordijk, Joost·2015·Antimicrobial Agents and Chemotherapy

Abstract

A longitudinal study was performed to (i) investigate the continuity of shedding of extended-spectrum-beta-lactamase (ESBL)-producing Enterobacteriaceae in dogs without clinical signs, (ii) identify dominant plasmid-mediated ESBL genes, and (iii) quantify ESBL-producing Enterobacteriaceae in feces. Fecal samples from 38 dogs were collected monthly for 6 months. Additional samples were collected from 7 included dogs on a weekly basis for 6 weeks. Numbers of CFU per gram of feces for non-wild-type Enterobacteriaceae were determined by using MacConkey agar supplemented with 1 mg/liter cefotaxime (MCC), and those for total Enterobacteriaceae were determined by using MacConkey agar. Cefotaxime-resistant isolates were screened by PCR and sequence analysis for the presence of bla CTX-M , bla CMY , bla SHV , bla OXA , and bla TEM gene families. Bacterial species were identified by matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis. PCR-negative isolates were tested by a double-disk synergy test for enhanced AmpC expression. A total of 259 samples were screened, and 126 samples were culture positive on MCC, resulting in 352 isolates, 327 of which were Escherichia coli . Nine dogs were continuously positive during this study, and 6 dogs were continuously negative. Monthly or weekly shifts in fecal shedding were observed for 23 dogs. Genotyping showed a large variety of ESBL genes and gene combinations at single and multiple consecutive sampling moments. The ESBL genes bla CTX-M-1 , bla CTX-M-14 , bla CTX-M-15 , bla SHV-12 , and bla CMY-2 were most frequently found. The mean number of CFU of non-wild-type Enterobacteriaceae was 6.11 × 10 8 CFU/g feces. This study showed an abundance of ESBL-producing Enterobacteriaceae in dogs in the Netherlands, mostly in high concentrations. Fecal shedding was shown to be highly dynamic over time, which is important to consider when studying ESBL epidemiology.

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  • Two Dutch longitudinal studies reported associations between raw feeding and faecal E. coli from dogs showing ESBL resistance.

    “Two Dutch longitudinal studies reported associations between raw feeding and faecal E. coli from dogs showing ESBL resistance (Baede et al. 2015)”

    From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Baede et al. 2015

    The ‘Dogs and background information’ section reports that raw-meat feeding was positively associated with ESBL-producing E. coli in dogs (OR 2.08, 95% CI 1.22–3.57). The paper describes this as one Dutch longitudinal study; our copy does not establish that two such studies reported the association. (LLM, conf=0.88)

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  1. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH. 2012. Extended- spectrum ␤-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on pub- lic health: a global perspective. Clin Microbiol Infect 18:646 -655. http: //dx.doi.org/10.1111/j.1469-0691.2012.03850.x. · DOI
  2. Hordijk J, Schoormans A, Kwakernaak M, Duim B, Broens E, Dierikx C, Mevius D, Wagenaar JA. 2013. High prevalence of fecal carriage of extended-spectrum ␤-lactamase/AmpC-producing Enterobacteriaceae in cats and dogs. Front Microbiol 4:242. http://dx.doi.org/10.3389/fmicb .2013.00242. · DOI
  3. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, Semmler T, Fruth A, Beutlich J, Guerra B, Wieler LH, Guenther S. 2010. Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta- lactamase-producing Escherichia coli among companion animals. J Anti- microb Chemother 65:651-660. http://dx.doi.org/10.1093/jac/dkq004. · DOI
  4. Ewers C, Bethe A, Stamm I, Grobbel M, Kopp PA, Guerra B, Stubbe M, Doi Y, Zong Z, Kola A, Schaufler K, Semmler T, Fruth A, Wieler LH, Guenther S. 2014. CTX-M-15-D-ST648 Escherichia coli from compan- ion animals and horses: another pandemic clone combining multiresis- tance and extraintestinal virulence? J Antimicrob Chemother 69:1224 - 1230. http://dx.doi.org/10.1093/jac/dkt516. · DOI
  5. Schwarz S, Silley P, Simjee S, Woodford N, van Duijkeren E, Johnson AP, Gaastra W. 2010. Editorial: assessing the antimicrobial susceptibility of bacteria obtained from animals. J Antimicrob Chemother 65:601-604. http://dx.doi.org/10.1093/jac/dkq037. · DOI
  6. Mulvey MR, Bryce E, Boyd DA, Ofner-Agostini M, Land AM, Simor AE, Paton S, Canadian Hospital Epidemiology Committee, Canadian Nosocomial Infection Surveillance Program, Health Canada. 2005. Mo- lecular characterization of cefoxitin-resistant Escherichia coli from Cana- dian hospitals. Antimicrob Agents Chemother 49:358 -365. http://dx.doi .org/10.1128/AAC.49.1.358-365.2005. · DOI
  7. Sun Y, Zeng Z, Chen S, Ma J, He L, Liu Y, Deng Y, Lei T, Zhao J, Liu J-H. 2010. High prevalence of blaCTX-M extended-spectrum ␤-lacta- mase genes in Escherichia coli isolates from pets and emergence of CTX- M-64 in China. Clin Microbiol Infect 16:1475-1481. http://dx.doi.org/10 .1111/j.1469-0691.2010.03127.x. · DOI
  8. O'Keefe A, Hutton TA, Schifferli DM, Rankin SC. 2010. 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. Antimi- crob Agents Chemother 54:3489 -3492. http://dx.doi.org/10.1128/AAC .01701-09. · DOI
  9. Shaheen BW, Nayak R, Foley SL, Kweon O, Deck J, Park M, Rafii F, Boothe DM. 2011. Molecular characterization of resistance to extended- spectrum cephalosporins in clinical Escherichia coli isolates from com- panion animals in the United States. Antimicrob Agents Chemother 55: 5666 -5675. http://dx.doi.org/10.1128/AAC.00656-11. · DOI
  10. So JH, Kim J, Bae IK, Jeong SH, Kim SH, Lim SK, Park YH, Lee K. 2012. Dissemination of multidrug-resistant Escherichia coli in Korean Longitudinal Study of ESBLs in Household Dogs June 2015 Volume 59 Number 6 aac.asm.org 3123 Antimicrobial Agents and Chemotherapy on April 20, 2016 by Universiteitsbibliotheek Utrecht http://aac.asm.org/ Downloaded from veterinary hospitals. Diagn Microbiol Infect Dis 73:195-199. http://dx.doi .org/10.1016/j.diagmicrobio.2012.03.010. · DOI
  11. Liao X-P, Liu B-T, Yang Q-E, Sun J, Li L, Fang L-X, Liu Y-H. 2013. Comparison of plasmids coharboring 16S rRNA methylase and extended- spectrum ␤-lactamase genes among Escherichia coli isolates from pets and poultry. J Food Prot 76:2018 -2023. http://dx.doi.org/10.4315/0362-028X .JFP-13-200. · DOI
  12. Huber H, Zweifel C, Wittenbrink MM, Stephan R. 2013. ESBL- producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland. Vet Microbiol 162:992-996. http://dx.doi.org/10.1016/j .vetmic.2012.10.029. · DOI
  13. Poirel L, Nordmann P, Ducroz S, Boulouis H-J, Arné P, Millemann Y. 2013. Extended-spectrum ␤-lactamase CTX-M-15-producing Klebsiella pneumoniae of sequence type ST274 in companion animals. Antimicrob Agents Chemother 57:2372-2375. http://dx.doi.org/10.1128/AAC.02622-12. · DOI
  14. Costa D, Poeta P, Briñas L, Sáenz Y, Rodrigues J, Torres C. 2004. Detection of CTX-M-1 and TEM-52 beta-lactamases in Escherichia coli strains from healthy pets in Portugal. J Antimicrob Chemother 54:960 - 961. http://dx.doi.org/10.1093/jac/dkh444. · DOI
  15. Costa D, Poeta P, Sáenz Y, Coelho AC, Matos M, Vinué L, Rodrigues J, Torres C. 2008. Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Vet Microbiol 127:97-105. http://dx.doi.org/10.1016/j.vetmic.2007.08.004. · DOI
  16. Carattoli A, Lovari S, Franco A, Cordaro G, Di Matteo P, Battisti A. 2005. Extended-spectrum beta-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003. Antimicrob Agents Chemother 49:833-835. http://dx.doi.org/10.1128/AAC.49.2.833-835.2005. · DOI
  17. Gandolfi-Decristophoris P, Petrini O, Ruggeri-Bernardi N, Schelling E. 2013. Extended-spectrum ␤-lactamase-producing Enterobacteriaceae in healthy companion animals living in nursing homes and in the commu- nity. Am J Infect Control 41:831-835. http://dx.doi.org/10.1016/j.ajic .2012.11.013. · DOI
  18. Harada K, Morimoto E, Kataoka Y, Takahashi T. 2011. Clonal spread of antimicrobial-resistant Escherichia coli isolates among pups in two ken- nels. Acta Vet Scand 53:11. http://dx.doi.org/10.1186/1751-0147-53-11. · DOI
  19. Benno Y, Nakao H, Uchida K, Mitsuoka T. 1992. Impact of the advances in age on the gastrointestinal microflora of beagle dogs. J Vet Med Sci 54:703-706. http://dx.doi.org/10.1292/jvms.54.703. · DOI
  20. Tamang MD, Nam H-M, Jang G-C, Kim S-R, Chae MH, Jung S-C, Byun J-W, Park YH, Lim S-K. 2012. Molecular characterization of ex- tended-spectrum-␤-lactamase-producing and plasmid-mediated AmpC ␤-lactamase-producing Escherichia coli isolated from stray dogs in South Korea. Antimicrob Agents Chemother 56:2705-2712. http://dx.doi.org /10.1128/AAC.05598-11. · DOI
  21. Harada K, Niina A, Nakai Y, Kataoka Y, Takahashi T. 2012. Prevalence of antimicrobial resistance in relation to virulence genes and phylogenetic origins among urogenital Escherichia coli isolates from dogs and cats in Japan. Am J Vet Res 73:409 -417. http://dx.doi.org/10.2460/ajvr.73.3.409. · DOI
  22. Lv L, Partridge SR, He L, Zeng Z, He D, Ye J, Liu J-H. 2013. Genetic characterization of IncI2 plasmids carrying blaCTX-M-55 spreading in both pets and food animals in China. Antimicrob Agents Chemother 57: 2824 -2827. http://dx.doi.org/10.1128/AAC.02155-12. · DOI
  23. Choi MJ, Lim SK, Jung SC, Ko KS. 2014. Comparisons of CTX-M- producing Escherichia coli isolates from humans and animals in South Korea. J Bacteriol Virol 44:44 -51. http://dx.doi.org/10.4167/jbv.2014.44 .1.44. · DOI
  24. Hou J, Huang X, Deng Y, He L, Yang T, Zeng Z, Chen Z, Liu J-H. 2012. Dissemination of the fosfomycin resistance gene fosA3 with CTX-M ␤-lactamase genes and rmtB carried on IncFII plasmids among Esche- richia coli isolates from pets in China. Antimicrob Agents Chemother 56:2135-2138. http://dx.doi.org/10.1128/AAC.05104-11. · DOI
  25. Tracz DM, Boyd DA, Hizon R, Bryce E, McGeer A, Ofner-Agostini M, Simor AE, Paton S, Mulvey MR, Canadian Nosocomial Infection Sur- veillance Program. 2007. ampC gene expression in promoter mutants of cefoxitin-resistant Escherichia coli clinical isolates. FEMS Microbiol Lett 270:265-271. http://dx.doi.org/10.1111/j.1574-6968.2007.00672.x. · DOI

Cited by

Sorted by citations

Authors
Baede, V. O., Wagenaar, J. A., Broens, E. M., Duim, B., Dohmen, W., Nijsse, R., Timmerman, A. J., & Hordijk, J.
Affiliations
Utrecht University (NL)
Venue
Antimicrobial Agents and Chemotherapy
Published
2015-06
Volume
59
Issue
6
Pages
3117-3124
ISSN
  • 0066-4804 (ISSN-L)
  • 1098-6596
OpenAlex
W1759586988
Cited by
66
References
0
Citations by year
2026: 1 · 2024: 7 · 2023: 3 · 2022: 15 · 2021: 12 · 2020: 3 · 2019: 8 · 2018: 9 · 2017: 4 · 2016: 2 · 2015: 2
FWCI
2.36
Type
journal article
Language
en
Open access
Locations
  • Antimicrobial Agents and Chemotherapy (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Socio-Environmental Systems Modeling (acceptedVersion)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Keywords
extended-spectrum beta-lactamase, AmpC beta-lactamase, Enterobacteriaceae, dogs, fecal shedding, Escherichia coli, blaCTX-M, blaSHV, blaCMY, blaOXA, blaTEM, plasmid-mediated antibiotic resistance, zoonotic transmission, antimicrobial resistance epidemiology
MeSH terms
Animals, Bacterial Proteins, beta-Lactamases, Dogs, Enterobacteriaceae, Enterobacteriaceae Infections, Genotype, Longitudinal Studies, Microbial Sensitivity Tests

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