Prevalence and antibiotic resistance of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli in healthy dogs in Chiang Mai Jirapa

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Jirapa Thepmanee
Jutamart Rodroo
Nattakarn Awaiwanont
Montira Intanon
Kannika Na Lampang
Niyada Thitaram
Kriangkrai Thongkorn

Abstract

The aim of the present study was to investigate the prevalence and the antibiotic resistance of ESBL-producing Escherichia coli in healthy dogs in Chiang Mai. Fecal and oral biofilm samples were collected from eighty nine healthy dogs presented at Veterinary Teaching Hospital Chiang Mai University for received vaccination or health checking. All samples were inoculated on MacConkey agar plates containing 1ug/ml of cefotaxime and E. coli confirmation was performed by using MALDI TOF MS. ESBL producing E. coli confirmation was performed by combination disc test and the positive isolates were subjected to antibiotic susceptibility testing using 12 antibiotic discs by disc diffusion methods. The prevalence of ESBL producing E. coli of fecal samples was 25.84 %. On the other hand ESBL producing E. coli from oral biofilm samples was not detected. All ESBL producing E. coli isolates were highly antibiotic drug resistant, especially ampicillin, cefazolin, cephalexin and clindamycin (100% resistant). Furthermore, they had multi-drug resistance pattern. It is concluded that fecal ESBL producing E. coli can be found in healthy dogs and leads to the high antibiotic resistant rates. This information may increase awareness of animal-to-human or animal-to-animal transmission.

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Thepmanee, J., Rodroo, J., Awaiwanont, N., Intanon, M., Na Lampang, K., Thitaram, N., & Thongkorn, K. (2018). Prevalence and antibiotic resistance of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli in healthy dogs in Chiang Mai Jirapa. Veterinary Integrative Sciences, 16(3), 233–245. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/152432
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Research Articles

References

Belas, A., Salazar, A. S., Gama, L. T. da, Couto, N., & Pomba, C. (2014). Risk factors for faecal colonisation with Escherichia coli producing extended-spectrum and plasmid-mediated AmpC β-lactamases in dogs. The Veterinary Record, 175(8), 202. https://doi.org/10.1136/vr.101978

Ben Sallem, R., Ben Slama, K., Esfepa, V., Ould Cheikhna, E., Mint Mohamed, A., Chairat, S., Boudabous. (2015). Detection of CTX-M-15-producing Escherichia coli isolates of lineages ST410-A, ST617-A and ST354-D in faecal samples of hospitalized patients in a Mauritanian hospital. Journal of Chemotherapy (Florence, Italy), 27(2), 114–116. https://doi.org/10.1179/1973947814Y.0000000172

Boonyasiri, A., Tangkoskul, T., Seenama, C., Saiyarin, J., Tiengrim, S., & Thamlikitkul, V. (2014). Prevalence of antibiotic resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathogens and Global Health, 108(5), 235–245. https://doi.org/10.1179/2047773214Y.0000000148

Bradford, P. A. (2001). Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clinical Microbiology Reviews, 14(4), 933–951, table of contents. https://doi.org/10.1128/CMR.14.4.933-951.2001

Carattoli, A., Lovari, S., Franco, A., Cordaro, G., Di Matteo, P., & Battisti, A. (2005). Extended-Spectrum β-Lactamases in Escherichia coli Isolated from Dogs and Cats in Rome, Italy, from 2001 to 2003. Antimicrobial Agents and Chemotherapy, 49(2), 833–835. https://doi.org/10.1128/AAC.49.2.833-835.2005

Carvalho, A. C., Barbosa, A. V., Arais, L. R., Ribeiro, P. F., Carneiro, V. C., & Cerqueira, A. M. F. (2016). Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Brazilian Journal of Microbiology, 47(1), 150–158. https://doi.org/10.1016/j.bjm.2015.11.005

CDC | Antibiotic Resistance Threats in the United States. (2013). Retrieved March 26, 2018, from https://www.cdc.gov/drugresistance/threat-report-2013/index.html

Chung, Y. S., Park, Y. K., Park, Y. H., & Park, K. T. (2017). Probable secondary transmission of antimicrobial-resistant Escherichia coli between people living with and without pets. The Journal of Veterinary Medical Science, 79(3), 486–491. https://doi.org/10.1292/jvms.16-0585

CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 24th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2014.

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. The Journal of Antimicrobial Chemotherapy, 54(5), 960–961. https://doi.org/10.1093/jac/dkh444

Costa, D., Poeta, P., Sáenz, Y., Coelho, A. C., Matos, M., Vinué, L., … Torres, C. (2008). Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Veterinary Microbiology, 127(1–2), 97–105. https://doi.org/10.1016/j.vetmic.2007.08.004

Damborg, P., Morsing, M. K., Petersen, T., Bortolaia, V., & Guardabassi, L. (2015). CTX-M-1 and CTX-M-15-producing Escherichia coli in dog faeces from public gardens. Acta Veterinaria Scandinavica, 57. https://doi.org/10.1186/s13028-015-0174-3

David A. Crossley, Penman, S., & British Small Animal Veterinary Association. (1995). Manual of small animal dentistry. British Small Animal Veterinary Association. Retrieved from https://books.google.co.th/books?id=AS5qAAAAMAAJ

Espinosa-Gongora, C., Qaswar Ali Shah, S., Jessen, L. R., Bortolaia, V., Langebaek, R., Bjornvad, C. R., & Guardabassi, L. (2015). Quantitative assessment of faecal shedding of beta-lactam-resistant Escherichia coli and enterococci in dogs. Veterinary Microbiology, 181(3–4), 298–302. https://doi.org/10.1016/j.vetmic.2015.10.004

Ewers, C., Grobbel, M., Stamm, I., Kopp, P. A., Diehl, I., Semmler, T., … Guenther, S. (2010). Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta-lactamase-producing Escherichia coli among companion animals. The Journal of Antimicrobial Chemotherapy, 65(4), 651–660. https://doi.org/10.1093/jac/dkq004

Falagas, M. E., & Karageorgopoulos, D. E. (2009). Extended-spectrum beta-lactamase-producing organisms. The Journal of Hospital Infection, 73(4), 345–354. https://doi.org/10.1016/j.jhin.2009.02.021

Guardabassi, L., Schwarz, S., & Lloyd, D. H. (2004). Pet animals as reservoirs of antimicrobial-resistant bacteria. The Journal of Antimicrobial Chemotherapy, 54(2), 321–332. https://doi.org/10.1093/jac/dkh332

Hagman, R., & Kühn, I. (2002). Escherichia coli strains isolated from the uterus and urinary bladder of bitches suffering from pyometra: comparison by restriction enzyme digestion and pulsed-field gel electrophoresis. Veterinary Microbiology, 84(1–2), 143–153.

Hanhaboon, P., Kimprasit, T., Wajjwalku, W., & Amavisit, P. (2015). Extended Spectrum Beta-lactamase Producing Escherichia coli Isolated from Infected Canines. The Thai Journal of Veterinary Medicine, 45(2), 263–267.

Harada, K., Nakai, Y., & Kataoka, Y. (2012). Mechanisms of resistance to cephalosporin and emergence of O25b-ST131 clone harboring CTX-M-27 β-lactamase in extraintestinal pathogenic Escherichia coli from dogs and cats in Japan. Microbiology and Immunology, 56(7), 480–485. https://doi.org/10.1111/j.1348-0421.2012.00463.x

Huber, H., Zweifel, C., Wittenbrink, M. M., & Stephan, R. (2013). ESBL-producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland. Veterinary Microbiology, 162(2–4), 992–996. https://doi.org/10.1016/j.vetmic.2012.10.029

Lee, J. H., Bae, I. K., & Lee, S. H. (2012). New definitions of extended-spectrum β-lactamase conferring worldwide emerging antibiotic resistance. Medicinal Research Reviews, 32(1), 216–232. https://doi.org/10.1002/med.20210

Leite-Martins, L., Meireles, D., Beça, N., Bessa, L. J., de Matos, A. J. F., & Martins da Costa, P. (2015). Spread of multidrug-resistant Escherichia coli within domestic aggregates (humans, pets, and household environment). Journal of Veterinary Behavior: Clinical Applications and Research, 10(6), 549–555. https://doi.org/10.1016/j.jveb.2015.07.040

Ljungquist, O., Ljungquist, D., Myrenås, M., Rydén, C., Finn, M., & Bengtsson, B. (2016). Evidence of household transfer of ESBL-/pAmpC-producing Enterobacteriaceae between humans and dogs – a pilot study. Infection Ecology & Epidemiology, 6. https://doi.org/10.3402/iee.v6.31514

Macfarlane, G. T., & Macfarlane, S. (1997). Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scandinavian Journal of Gastroenterology. Supplement, 222, 3–9. https://doi.org/10.1080/00365521.1997.11720708

Moreno, A., Bello, H., Guggiana, D., Domínguez, M., & González, G. (2008). Extended-spectrum beta-lactamases belonging to CTX-M group produced by Escherichia coli strains isolated from companion animals treated with enrofloxacin. Veterinary Microbiology, 129(1–2), 203–208. https://doi.org/10.1016/j.vetmic.2007.11.011

Münnich, A., & Lübke-Becker, A. (2004). Escherichia coli infections in newborn puppies--clinical and epidemiological investigations. Theriogenology, 62(3–4), 562–575. https://doi.org/10.1016/j.theriogenology.2003.11.012

Ogeer-Gyles, J., Mathews, K. A., Sears, W., Prescott, J. F., Weese, J. S., & Boerlin, P. (2006). Development of antimicrobial drug resistance in rectal Escherichia coli isolates from dogs hospitalized in an intensive care unit. Journal of the American Veterinary Medical Association, 229(5), 694–699. https://doi.org/10.2460/javma.229.5.694

Okubo, T., Sato, T., Yokota, S., Usui, M., & Tamura, Y. (2014). Comparison of broad-spectrum cephalosporin-resistant Escherichia coli isolated from dogs and humans in Hokkaido, Japan. Journal of Infection and Chemotherapy: Official Journal of the Japan Society of Chemotherapy, 20(4), 243–249. https://doi.org/10.1016/j.jiac.2013.12.003

Oliveira, P. A. de, Moura, R. A., Rodrigues, G. V., Lopes, K. F. C., Zaniolo, M. M., Rubio, A. J., … Gonçalves, D. D. (2016). Detection of extended spectrum beta-lactamases and resistance in members of the Enterobacteriaceae family isolated from healthy sheep and dogs in Umuarama, Paraná, Brazil. Semina: Ciências Agrárias, Londrina, 37(2), 829–840. https://doi.org/10.5433/1679-0359.2016v37n2p829

Pitout, J. D. D., & Laupland, K. B. (2008). Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. The Lancet. Infectious Diseases, 8(3), 159–166. https://doi.org/10.1016/S1473-3099(08)70041-0

Puño-Sarmiento, J., Medeiros, L., Chiconi, C., Martins, F., Pelayo, J., Rocha, S., … Nakazato, G. (2013). Detection of diarrheagenic Escherichia coli strains isolated from dogs and cats in Brazil. Veterinary Microbiology, 166(3–4), 676–680. https://doi.org/10.1016/j.vetmic.2013.07.007

Rocha-Gracia, R. C., Cortés-Cortés, G., Lozano-Zarain, P., Bello, F., Martínez-Laguna, Y., & Torres, C. (2015). Faecal Escherichia coli isolates from healthy dogs harbour CTX-M-15 and CMY-2 β-lactamases. The Veterinary Journal, 203(3), 315–319. https://doi.org/10.1016/j.tvjl.2014.12.026

Rodríguez-Baño, J., Navarro, M. D., Retamar, P., Picón, E., & Pascual, Á. (2012). β-Lactam/β-Lactam Inhibitor Combinations for the Treatment of Bacteremia Due to Extended-Spectrum β-Lactamase–Producing Escherichia coli: A Post Hoc Analysis of Prospective Cohorts. Clinical Infectious Diseases, 54(2), 167–174. https://doi.org/10.1093/cid/cir790

Rota, A., Milani, C., Corrò, M., Drigo, I., & Börjesson, S. (2013). Misuse of antimicrobials and selection of methicillin-resistant Staphylococcus pseudintermedius strains in breeding kennels: genetic characterization of bacteria after a two-year interval. Reproduction in Domestic Animals = Zuchthygiene, 48(1), 1–6. https://doi.org/10.1111/j.1439-0531.2012.02012.x

Sallem, R. B., Gharsa, H., Slama, K. B., Rojo-Bezares, B., Estepa, V., Porres-Osante, N., … Torres, C. (2013). First detection of CTX-M-1, CMY-2, and QnrB19 resistance mechanisms in fecal Escherichia coli isolates from healthy pets in Tunisia. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 13(2), 98–102. https://doi.org/10.1089/vbz.2012.1047

Sancak, A. A., Rutgers, H. C., Hart, C. A., & Batt, R. M. (2004). Prevalence of enteropathic Escherichia coli in dogs with acute and chronic diarrhoea. The Veterinary Record, 154(4), 101–106.

Saonuam, P., Hiransuthikul, N., Suankratay, C., Malathum, K., & Danchaivijitr, S. (2010). Risk factors for nosocomial infections caused by extended-spectrum β-lactamase producing Escherichia coli or Klebsiella pneumoniae in Thailand. Asian Biomedicine (Research Reviews and News), 2(6), 485–491. https://doi.org/10.5372/929

Schaufler, K., Bethe, A., Lübke-Becker, A., Ewers, C., Kohn, B., Wieler, L. H., & Guenther, S. (2015). 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. Infection Ecology & Epidemiology, 5, 25334.

Schmidt, V. M., Pinchbeck, G. L., Nuttall, T., McEwan, N., Dawson, S., & Williams, N. J. (2015). Antimicrobial resistance risk factors and characterisation of faecal E. coli isolated from healthy Labrador retrievers in the United Kingdom. Preventive Veterinary Medicine, 119(1–2), 31–40. https://doi.org/10.1016/j.prevetmed.2015.01.013

Shaheen, B. W., Nayak, R., Foley, S. L., Kweon, O., Deck, J., Park, M., … Boothe, D. M. (2011). Molecular characterization of resistance to extended-spectrum cephalosporins in clinical Escherichia coli isolates from companion animals in the United States. Antimicrobial Agents and Chemotherapy, 55(12), 5666–5675. https://doi.org/10.1128/AAC.00656-11

Singh, F., Hirpurkar, S. D., Shakya, S., Rawat, N., Devangan, P., Khan, F. F., & Bhandekar, S. K. (2017). Presence of enterobacteria producing extended-spectrum β-lactamases and/or carbapenemases in animals, humans and environment in India. The Thai Journal of Veterinary Medicine, 47(1), 35–43.

Søraas, A., Olsen, I., Sundsfjord, A., Handal, T., Bjørang, O., & Jenum, P. A. (2014). Extended-spectrum beta-lactamase-producing bacteria are not detected in supragingival plaque samples from human fecal carriers of ESBL-producing Enterobacteriaceae. Journal of Oral Microbiology, 6. https://doi.org/10.3402/jom.v6.24026

Sun, Y., Zeng, Z., Chen, S., Ma, J., He, L., Liu, Y., … Liu, J.-H. (2010). High prevalence of bla(CTX-M) extended-spectrum β-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 16(9), 1475–1481.

Tamang, M. D., Nam, H.-M., Jang, G.-C., Kim, S.-R., Chae, M. H., Jung, S.-C., … Lim, S.-K. (2012). Molecular characterization of extended-spectrum-β-lactamase-producing and plasmid-mediated AmpC β-lactamase-producing Escherichia coli isolated from stray dogs in South Korea. Antimicrobial Agents and Chemotherapy, 56(5), 2705–2712. https://doi.org/10.1128/AAC.05598-11

Wadås, B., Kühn, I., Lagerstedt, A. S., & Jonsson, P. (1996). Biochemical phenotypes of Escherichia coli in dogs: comparison of isolates isolated from bitches suffering from pyometra and urinary tract infection with isolates from faeces of healthy dogs. Veterinary Microbiology, 52(3–4), 293–300.