Escherichia coli in Northern Tocantins horses and its relevance in public health

Authors

DOI:

https://doi.org/10.33448/rsd-v10i7.16383

Keywords:

AMR; Antibiogram; Horse; Bacterial isolation; Zoonosis.

Abstract

It is known that horses are potential reservoirs of zoonotic bacteria, such as Escherichia coli and Salmonella sp. However, there is little information on zoonotic bacteria as potential sources of infection and antibiotic resistance. Thus, the present study aimed to verify the prevalence of diarrheagenic E. coli (DEC) in horses from the northern region of Tocantins, Brazil and determine the microorganism’s susceptibility to the main antimicrobials used in horses and humans. By transrectal palpation, stool samples were taken from 72 horses health, and E. coli was identified by biochemical tests. To detect the main DEC serogroups, the slide agglutination technique was performed. The susceptibility to antimicrobials followed the methodology recommended by the Clinical and Laboratory Standards Institute (2011) and the National Committee for Clinical Laboratory Standards (2015). E. coli was detected in 39 of the studied animals and 68 different strains were identified, 32 (47.06%) of which were DEC. Of these, 26 (81.25%) were enteropathogenic, 5 (15.62%) enteroinvasive, and 1 (3.13%) enterohemorrhagic, which reflects the role of equines as reservoirs of pathogenic strains and as source infection to other animals and humans, representing an important threat to public health. Regarding antimicrobial resistance, the highest in vitro sensitivity and resistance was for Ciprofloxacin/Meropenem and Penicillin G, respectively. Multidrug-resistant isolates were also identified, with predominant resistance to ß-lactams, tetracyclines and sulfonamides. It is concluded that equines are potential reservoirs of pathogenic E. coli. An antibiogram is an important tool for the choice of an effective antimicrobial in cases the colibacillosis. People who have contact with equines should pay attention to the possible transmission of these pathogens during management.

References

Bardiau, M., Taminiau, B., DupreZ, J. N., Labrozzo, S. & Mainil, J. G. (2012). Comparison between a bovine and a human enterohaemorrhagic Escherichia coli strain of serogroup O26 by suppressive subtractive hybridization reveals the presence of atypical factors in EHEC and EPEC strains. FEMS Microbiology Letters. 330(2): 132-139. 10.1111/j.15746968.2012.02542.x

Bauer, A. W., Kirby, W. M. M., Sherris, J. C. & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disc method. American Journal of Clinical Pathology. 45(4): 493-496. 10.1093/ajcp/45.4_ts.493

Beuchat, L. R. (2002). Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes and Infection. 4(4): 413-423. 10.1016/s1286-4579(02)01555-1

Caprioli, A., Morabito, S., Brugère, H. & Oswald, E. (2005). Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Veterinary Research. 36(3): 289-311. 10.1051/vetres:2005002

Casasnovas, A. F., Ayuda, T. C. & Abenia, J. F. (2014). Manejo e Comportamento. In: Casasnovas A. F., Ayuda T. C. & Abenia, J. F. (Orgs). A exploração clínica do cavalo. 1ed. São Paulo: Editora MedVet, pp.23.

Chandran, A. & Mazumder, A. (2013). Prevalence of diarrhea-associated virulence genes and genetic diversity in Escherichia coli isolates from fecal material of various animal hosts. Applied Environmental Microbiology. 79(23): 7371-7380. 10.1128/AEM.02653-13

Chung, Y. S., Song, J. W., Kim, D. H., Shin, S., Park, Y. K., Yang, S. J., Lim, S. K., Park, K. T. & Park, Y. H. (2016). Isolation and characterization of antimicrobial-resistant Escherichia coli from national horse racetracks and private horse-riding courses in Korea. Journal of Veterinary Science. 17(2): 199-206. https://doi.org/10.4142/jvs.2016.17.2.199

Clinical and Laboratory Standards Institute (CLSI). (2011). Performance standards for Antimicrobial Susceptibility Testing; Twenty-first Informational Supplement. CLSI document M100-S21. 31(1). Wayne, PA: Clinical and Laboratory Standards Institute.

Croxen, M. A. & Finlay, B. B. (2010). Molecular mechanisms of Escherichia coli pathogenicity. Nature Reviews Microbiology. 8(1): 26-38. 10.1038/nrmicro2265

De Lagarde, M., Larrieu, C., Praud, K., Schouler, C., Doublet, B., Guillaume, S., Fairbrother, J. M. & Arsenau, T. J. (2019). Prevalence, risk factors, and characterization of multidrug resistant and extended spectrum -lactamase/AmpC -lactamase producing Escherichia coli in healthy horses in France in 2015. Journal of Veterinary Internal Medicine. 33(2): 902-911. http://10.1111/jvim.15415

Duijkeren, E. V., Van Asten, A. J. A. M. & Gaastra, W. (2000). Characterization of Escherichia coli isolated from adult horses with and without enteritis. Veterinary Quarterly. 22(3): 162-166. 10.1080/01652176.2000.9695048

European Food Safety Authority (EFSA). (2017). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2015. EFSA Journal. 15: 212.

Ferreira, A. J. P. & Knöbl, T. Colibacilose. In: Berchieri Jr., A., Silva, E., Di Fábio, J., Sesti, L. & Zuanaze, M. A. F. (Orgs). (2009). Doença das aves. 2ed. Campinas: Facta, pp.457-500.

Fontana, F. (2018). Técnicas de pesquisa. In Mazucato, T. (Org.). Metodologia da pesquisa e do trabalho científico (pp. 59-66). Penápolis, São Paulo: FUNEPE.

Gomes, T. A. T. & Hernandes, R. T. (2015). Escherichia coli Enteropatogênica (EPEC). In: Trabulsi L. R. & Alterthum F. (Eds). Trabulsi-Alterthum Microbiologia. 6ed. São Paulo: Atheneu, pp.303-10.

Guardabassi, L., Schwarz, S. & Lloyd, D. H. (2004). Pets animals as reservoirs of antimicrobial-resistant bacteria. Journal of Antimicrobial Chemotherapy. 54(2): 331-332. 10.1093/jac/dkh332

Gyles, C. L. (2007). Shiga toxin-producing Escherichia coli: an overview. Journal of Animal Science. 85(13): 45-62. 10.2527/jas.2006-508

Gyles, C. L. & Fairbrother, J. M. (2010). Escherichia coli. In: Gyles C.L, Prescott J.F., Songer J.G. & Thoen C.O. (Eds). Pathogenesis of Bacterial Infections in Animals. 4ed. Iowa: Blackwell Publishing, pp.231-265. 10.1002/9780470958209.ch15

Hernandes, R. T., Elias, W. P., Vieira, M. A. M. & Gomes, T. A. T. (2009). An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Letters. 297(2): 137-49. 10.1111/j.1574-6968.2009.01664.x

Huijbers, P. M. C., De Kraker, M., Graat, E. A. M., Van Hoek, A. H. A. M., Van Santen, M. G., De Jong, M. C. M., Van Duijkeren, E. & De Greef, S. C. (2013). Prevalence of extended-spectrum ß-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density. Clinical Microbiology and Infection. 19(6): 256-59. 10.1111/1469-0691.12150

Jokisalo, J., Bryan, J., Legget, B., Abbott, Y. & Katz, L. M. (2010). Multiple-drug resistant Acinetobacter baumannii bronchopneumonia in a colt following intensive care treatment. Equine Veterinary Education. 22(6): 281-286. 10.1111/j.2042-3292.2010.00071.x

Kaper, J. B., Nataro, J. D. & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology. 2(2): 123-140. https://doi.org/10.1038/nrmicro818

Klemm, P., Hancock, V. & Schembri, M. A. (2007). Mellowing Out: adaptation to commensalism by Escherichia coli asymptomatic bacteriuria strain 83972. Infection and Immunity. 75(8): 3688-3695. http://10.1128/IAI.01730-06

Knutton, S., Lloyd, D. R. & McNeish, A. S. (1987). Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and culture human intestinal mucosa. Infection and Immunity. 55(1): 69-77.

Krieg, N. R. & Holt, H. J. (1984). Facultatively anaerobic gram-negative rods: Family I. Enterobacteriaceae. In: Krieg N.R. & Holt H.J. (Eds). Bergey’s Manual of Systematic Bacteriology. 1ed. Baltimore: Williams & Wilkins, pp.408-420.

Lanz, R., Kuhnert, P. & Boerlin, P. (2003). Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Veterinary Microbiology. 91(1): 73-84. https://doi.org/10.1016/S0378-1135(02)00263-8

Laxminarayan, R., Sridhar, D., Blaser, M., Wang, M. & Woolhouse, M. (2016). Achieving global targets for antimicrobial resistance. Science. 353(6302): 874-875. https://doi.org/10.1126/science.aaf9286

Lengacher, B., Kline, T. R., Harpster, L., Williams, M. L. & Lejeune, J. T. (2010). Low prevalence of Escherichia coli O157:H7 in horses in Ohio, USA. Journal of Food Protection. 73(11): 2089-2092. 10.4315/0362-028X-73.11.2089

Levandowski, R., Daroit, L. & Dos Santos, L. R. (2019). Escherichia coli: antimicrobial susceptibility monitoring 2015 - 2018 in the north region of the state of Rio Grande do Sul, Southern Brazil. Revista de Ciência Veterinária e Saúde Pública. 6(2): 251-261. 10.4025/revcivet.v6i2.47685

Lopes, E. S., Maciel, W. C., Teixeira, R. S. C., Albuquerque, A. H., Vasconcelos, R. H., Machado, D. N.; Bezerra, W. G. A. & Santos, I. C. L. (2016). Isolamento de Salmonella spp. e Escherichia coli de psittaciformes: relevância em saúde pública. Arquivo do Instituto Biológico. 83(e0602014): 1-10. 10.1590/1808-1657000602014

Maddox, T. W., Clegg, P. D., Diggle, P. J., Wedley, A. L., Dawson, S., Pinchbeck, G. L. & Williams N. J. (2012). Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 1: Prevalence of antimicrobial-resistant Escherichia coli and methicillin-resistant Staphylococcus aureus. Equine Veterinary Journal. 44(3): 289-296. 10.1111/j.2042-3306.2011.00441.x

Maddox, T. W., Clegg, P. D., Williams, N. J. & Pinchbeck, G. L. (2015). Antimicrobial resistance in bacteria from horses: epidemiology of antimicrobial resistance. Equine Veterinary Journal. 47(6): 756-765. https://doi.org/10.1111/evj.12471

Manning, S. D., Motiwala, A. S., Springman, A. C., Qi, W., Lacher, D. W., Ouellette, L. M.; Mladonicky, J. M., Somsel, P., Rudrik, J. T., Dietrich, S. E., Zhang, W., Swaminathan, B., Alland, D. & Whittam, T.S. (2008). Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proceedings of the National Academy of Sciences of the United States of America. 105(12): 4868-73. 10.1073/pnas.0710834105

Matamoros, S., Van Hattem, J. M., Arcilla, M. S., Willemse, N., Melles, D. C., Penders, J., Vinh, T. B., Hoa, N. T., Bootsma, M. C. J., Van Genderen, P. J., Goorhuis, A., Grobusch, M., Molhoek, N., Oude Lashof, A. M. L., Stobbering, E. E., Verbrug, H. A., De Jong, M. D. & Schultsz, C. (2017). Global phylogenetic analysis of Escherichia coli and plasmids carrying the mcr-1 gene indicates bacterial diversity but plasmid restriction. Scientific Reports. 7(15364): 1-9. 10.1038/s41598-017-15539-7

Mateu, E. & Martin, M. (2001). Why is anti-microbial resistance a veterinary problem as well? Journal of Veterinary Medicine Series B-Infectious Diseases and Veterinary Public Health. 48(8): 569-81. 10.1046/j.1439-0450.2001.00475.x

Mayrhofer, S., Paulsen, P., Smulders, F. J. M. & Hilbert, F. (2006). Antimicrobial resistance in commensal Escherichia coli isolated from muscle foods as related to the veterinary use of antimicrobial agents in food-producing animals in Austria. Microbial Drug Resistance. 12(4): 278-283. 10.1089/mdr.2006.12.278

Mazucato, T. (Org.). (2018). O projeto de pesquisa. In Mazucato, T. (Org.). Metodologia da pesquisa e do trabalho científico (pp. 45-47). FUNEPE.

Mazucato, T. (Org.). (2018). Métodos. In Mazucato, T. (Org.). Metodologia da pesquisa e do trabalho científico (pp. 58). Penápolis, São Paulo: FUNEPE.

McPeake, S. J. W., Smyth, J. A. & Ball, H. J. (2005). Characterization of avian pathogenic Escherichia coli (APEC) associated with colisepticaemia compared to faecal isolates from healthy birds. Veterinary Microbiology. 110(3-4): 245-253. 10.1016/j.vetmic.2005.08.001

Mehta, S. C., Samanta, M., Chow, D. C. & Palzkill, T. (2016). Avoiding the Carbapenem trap: KPC-2 β-lactamase sequence requirements for Carbapenem hydrolysis. The FASEB Journal. 30(S1) Suppl.: 1083.20-1083.20

Moyaert, H., De Graef, E. M., Haesebrouck, F. & Decostere, A. (2006). Acquired antimicrobial resistance in the intestinal microbiota of diverse cat populations. Research in Veterinary Science. 81(1): 1-7. 10.1016/j.rvsc.2005.10.004

Nataro J. P. & Kaper J. B. (1998). Diarrheagenic Escherichia coli. Clinical Microbiology Reviews. 11(1): 142-201.

National Committee for Clinical Laboratory Standards (NCCLS). (2015). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolates from animals. 3ed. CLSI supplement VET01S. Wayne, PA.

Normanno, G., Corrente, M., La Salandra, G., Dambrosio, A., Quaglia, N. C., Parisi, A., Greco, G., Bellacicco, A. L., Virgilio, S. & Celano, G. V. (2007). Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. International Journal of Food Microbiology. 117(2): 219-22. 10.1016/j.ijfoodmicro.2007.04.006

Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C., Jones, R., Nightingale, C., Preston, R. & Waddell, J. (2004). Does the use of antibiotics in food animals pose a risk to human health? Journal of Antimicrobial Chemotherapy. 53(1): 28- 52. 10.1093/jac/dkg483

Porse, A., Gumpert, H., Kubicek-Sutherland, J. Z., Karami, N., Adlerberth, I., Wold, A. E.; Andersson, D. I., Sommer, M. O. A. (2017). Genome dynamics of Escherichia coli during antibiotic treatment: transfer, loss, and persistence of genetic elements in situ of the infant gut. Frontiers in cellular and infection microbiology. 7:126. 10.3389/fcimb.2017.00126

Robinson, N. E. & Sprayberry, K. A. (2009). Current therapy in equine medicine. 6ed. St Louis: Elsevier Saunders Co., pp.1104.

Rodríguez-Angeles, G. (2002). Principales características y diagnóstico de los grupos patógenos de Escherichia coli. Salud Pública de México. 44(5): 464-475

Sampaio, I. B. M. (2015). Estatística aplicada à experimentação animal. 4ed. Belo Horizonte: Fundação de Estudo e Pesquisa em Medicina Veterinária e Zootecnia (FEPMVZ), pp.265.

Souza, C. O., Melo, T. R. B., Melo, C. S. B., Menezes, E. M., De Carvalho, A. C. & Monteiro, L. C. R. (2016). Escherichia coli enteropatogênica: uma categoria diarreiogênica versátil. Revista Pan-Amazônica de Saúde. 7(2): 79-91. 10.5123/S2176-62232016000200010

Tenaillon, O., Skurnik, D., Picard, B. & Denamur, E. (2010). The population genetics of commensal Escherichia coli. Nature Reviews Microbiology. 8(3): 207-217. 10.1038/nrmicro2298

Trevena, W. B., Hooper, R. S., Wray, C., Willshaw, G. A., Cheasty, T. & Domingue, G. (1996). Vero cytotoxin–producing Escherichia coli O157 associated with companion animals. Veterinary Record. 138(16): 400.

Umber, J. K. & Bender, J. B. (2009). Pets and antimicrobial resistance. Veterinary Clinics of North America: Small Animal Practice. 39(2): 279-92. 10.1016/j.cvsm.2008.10.016

Van Spijk, J. N., Schmitt, S. & Schoster, A. (2017). Infections caused by multidrug-resistant bacteria in an equine hospital (2012–2015). Equine Veterinary Education. 31(12): 653-658. 10.1111/eve.12837

Vo, A. T. T., Van Duijkeren, E., Fluit, A. C. & Gaastra, W. (2007). Characteristics of extended-spectrum cephalosporin-resistant Escherichia coli and Klebsiella pneumoniae isolates from horses. Veterinary Microbiology. 124(3-4): 248-55. 10.1016/j.vetmic.2007.04.027

Williams, J. D. (1999). β-lactamases and β- lactamase inhibitors. International Journal of Antimicrobial Agents. 12(Suppl 1): 3-7. 10.1016/s0924-8579(99)00085-0

Williams, A. P., McGregor, K. A.; Killham, K. & Jones, D. L. (2008). Persistence and metabolic activity of Escherichia coli O157:H7 in farm animal faeces. FEMS Microbiology Letters. 287(2): 168-73. 10.1111/j.1574-6968.2008.01310.x

Wilson, R. S., Parker, J., Kovacs, D., Doohan, D. & Lejeune, J. (2009). Contamination prevention and response related to fresh and fresh-cut produce: an expert perspective on the farmer decision making process. Food Protection Trends. 29(8): 488-492.

World Health Organization (WHO). (2014). Antimicrobial resistance: global report on surveillance. pp.257.

Published

18/06/2021

How to Cite

NUNES, I. M. M.; MACIEL, K. A.; BARBOSA, S. M.; CARNEIRO, P. D.; ALMEIDA, K. de S.; SILVA, M. A. G. da. Escherichia coli in Northern Tocantins horses and its relevance in public health. Research, Society and Development, [S. l.], v. 10, n. 7, p. e17310716383, 2021. DOI: 10.33448/rsd-v10i7.16383. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/16383. Acesso em: 16 nov. 2024.

Issue

Section

Agrarian and Biological Sciences