Characterization of Escherichia coli from Captive Wild Animals for ESBL Production, Phylo-grouping and Virulence

Rahul Kolhe; Rahul Gondake; Vikas Waskar; Chandrashekhar Mote; Mrunalini Budhe; Shreyash Jaiswal

Authors

Rahul Kolhe KNP College of Veterinary Science, MAFSU Shirwal Maharashtra
Rahul Gondake
Vikas Waskar
Chandrashekhar Mote
Mrunalini Budhe
Shreyash Jaiswal

Keywords:

Diarrheagenic E. coli, ESBL Production, Phylogenetic Groups

Abstract

In this study, 59 fecal samples were collected from wild animals in captivity and 34 E. coli were isolated (57.62%). Out of 34 isolates, 12 (35.29%) were DEC strains belonging to ETEC and EPEC pathotypes. ETEC strains were detected in spotted deer, grey cockatiel, and an Indian gaur. While EPEC strains were detected in hippopotamus, jackals, barking deer, and nilgai. E. coli mainly belongs to B2 phylogroups. The study revealed the detection of multi-drug resistant as well as ESBL type of E. coli in zoo animals. E. coli were resistant to tetracycline (97.05%), ceftriaxone (94.11%), ceftazidime (88.23%), cefoxitin, and ceftazidime plus clavulanic acid (79.41%). However, sensitivity to ertapenem, imipenem, and colistin was recorded. E. coli isolated from jackal, nilgai and elephant were highly sensitive to almost all the used antimicrobials. About 38.23% of strains were ESBL-producing and detected from barking deer, spotted deer, penguins, tiger, jackal, blackbuck, chinkara, India gaur, hanuman langur, and elongated tortoise. Some strains also showed colistin and MBL + AmpC type of resistance as estimated by the Ezy MIC kit. ESBL-positive strains were also studied for the presence of beta-lactam genes, and only blaTEM was detected.

References

Adesiyun, A. A. (1999) Absence of Escherichia coli O157 in a survey of wildlife from Trinidad and Tobago. Journal of Wildlife Diseases, 35(1), 115-120.

Aktar, S., Saha, S., Sarder, M., Amin, M., Islam, M.H., Hassan, J. and Khan, M.F.R. (2015) Pathogenicity of E. coli in mice isolated from fecal samples of zoo animals. Bangladesh Livestock Journal, 1, 23-25.

Aranda, K.R., Fabbricotti, S.H., Fagundes-Neto, U. and Scaletsky I,C. (2007) Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxin-producing Escherichia coli strains in Brazilian children. FEMS Microbiology Letters, 267(2):145-150.

Bautista-Trujillo, G.U., Gutiérrez-Miceli, F.A., Mandujano-García, L., Oliva-Llaven, M.A., Ibarra-Martínez, C., Mendoza-Nazar, P., Ruiz-Sesma, B., Tejeda-Cruz, C., Pérez-Vázquez, L.C., Pérez-Batrez, J.E., Vidal, J.E. and Gutiérrez-Jiménez, J. (2020) Captive Green Iguana Carries Diarrheagenic Escherichia coli Pathotypes. Frontiers in Veterinary Science, 7, 99.

Bauwens, L., Meurichy, W. De. and Vercammen, F. (2000) Isolation of Escherichia coli O157 from zoo animals. Vlaams Diergeneeskundig Tijdschrift, 69, 76-79.

Carneiro, C., Araújo, C., Gonçalves, A., Vinué, L., Somalo, S., Ruiz, E., Uliyakina, I., Rodrigues, J., Igrejas, G., Poeta, P. and Torres, C. (2010) Detection of CTX-M-14 and TEM-52 extended-spectrum beta-lactamases in fecal Escherichia coli isolates of captive ostrich in Portugal. Foodborne Pathogens and Disease, 7(8):991-994.

Clermont, O., Bonacorsi, S. and Bingen, E. (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology, 66(10):4555-4558.

Clermont, O., Christenson, J.K., Denamur, E. and Gordon, D.M. (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, 5(1):58-65.

Clinical Laboratory Standard Institute (CLSI). Performance standards for antimicrobial susceptibility testing: twenty forth informational supplement (M 100-S 27). Wayne: CLSI; 2017.

Fang, H., Ataker, F., Hedin, G. and Dornbusch, K. (2008) Molecular epidemiology of extended-spectrum beta-lactamases among Escherichia coli isolates collected in a Swedish hospital and its associated health care facilities from 2001 to 2006. Journal of Clinical Microbiology, 46(2), 707–712.

Gopee, N. V., Adesiyun, A.A. and Caesar, K. (2000) Longitudinal study of Escherichia coli strains isolated from captive mammals, birds, and reptiles in Trinidad. Journal of Zoo and Wild Medicine, 31(3), 353-60.

Gruel, G., Sellin, A., Riveiro, H., Pot, M., Breurec, S., Guyomard-Rabenirina, S., Talarmin, A. and Ferdinand, S. (2021) Antimicrobial use and resistance in Escherichia coli from healthy food-producing animals in Guadeloupe. BMC veterinary research, 17(1), 116.

Hassell, J. M., Ward, M. J., Muloi, D., Bettridge, J. M., Robinson, T. P., Kariuki, S., Ogendo, A., Kiiru, J., Imboma, T., Kang'ethe, E. K., Öghren, E. M., Williams, N. J., Begon, M., Woolhouse, M. and Fèvre, E. M. (2019) Clinically relevant antimicrobial resistance at the wildlife-livestock-human interface in Nairobi: an epidemiological study. The Lancet. Planetary Health, 3(6), e259–e269.

Milton, A., Agarwal, R. K., Priya, G. B., Aravind, M., Athira, C. K., Rose, L., Saminathan, M., Sharma, A. K. and Kumar, A. (2019) Captive wildlife from India as carriers of Shiga toxin-producing, Enteropathogenic and Enterotoxigenic Escherichia coli. The Journal of Veterinary Medical Science, 81(2), 321–327.

Moawad, A. A., Hotzel, H., Neubauer, H., Ehricht, R., Monecke, S., Tomaso, H., Hafez, H. M., Roesler, U. and El-Adawy, H. (2018) Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli. Gut Pathogens, 10, 39.

Oludairo, O. O., Kwaga, J., Dzikwi, A. and Kabir, J. (2016) Isolation and prevalence of Escherichia coli in wild animals at the national zoological garden Jos, Nigeria. Bangladesh Journal of Veterinary Medicine, 14(2), 233-236.

Radhouani, H., Silva, N., Poeta, P., Torres, C., Correia, S. and Igrejas, G. (2014) Potential impact of antimicrobial resistance in wildlife, environment and human health. Frontiers in Microbiology, 5, 23.

Steger, L., Rinder, M. and Korbel, R. (2020). Phenotypical antibiotic resistances of bacteriological isolates originating from pet, zoo and falconry birds. Veterinary Practice Ausg K Small Animals Pets, 48(04): 260-269.

Taneja, N. and Sharma, M. (2019) Antimicrobial resistance in the environment: The Indian scenario. The Indian Journal of Medical Research, 149(2), 119–128.

Vale AP, Cousins C, Tzora A, McCarron MT, Green A, Molloy S, Bainbridge J. and Leonard F. (2020) Molecular characterization of fecal Escherichia coli isolated from zoo animals. Journal of Zoo and Wildlife Medicine, 50(4), 813-821.

Vadnov, M., Barbič, D., Žgur-Bertok, D. and Erjavec, M. S. (2017) Escherichia coli isolated from feces of brown bears (Ursus arctos) have a lower prevalence of human extraintestinal pathogenic E. coli virulence-associated genes. Canadian Journal of Veterinary Research, 81(1), 59–63.

Wang, Y., He, T., Han, J., Wang, J., Foley, S.L., Yang, G., Wan, S., Shen, J. and Wu, C. (2012) Prevalence of ESBLs and PMQR genes in fecal Escherichia coli isolated from the non-human primates in six zoos in China. Veterinary Microbiology, 159(1-2):53-59.

Zaidi, S., Gahlot, K., Diwakar., Anjum, F. and Kataria, A. K. (2020) Characterization of Escherichia coli recovered from wild animals kept at Bikaner zoo for their antibiotic resistance. Journal of Pharmaceutical Research International, 32(3),1-8.

Zanardi, G., Iemmi, T., Spadini, C., Taddei, S., Cavirani, S. Cabassi, C.S. (2020) Wild micromammals as bioindicators of antibiotic resistance in ecopathology in Northern Italy. Animals, 10(7):1184.