Abstract
Wildlife plays significant roles in the dissemination and zoonotic transmission of pathogens. The enterohaemorrhagic Escherichia coli (EHEC) are associated with complicated cases of food‑borne illnesses. This study investigated the presence of EHEC serogroups (O26, O45, O103, O145, O91, O111, O128, O121 and O157) in wildlife species: cane rats (Thryonomys swinderianus), royal antelope (Neotragus pygmaeus), African giant rats (Cricetomys gambianus) and waterbuck (Kobus ellipsiprymnus). EHEC and non‑EHEC isolates from these wildlife sources were tested for susceptibility to antimicrobial agents. Overall, 127 (83.0 %) out of 153 samples yielded E. coli. Nine (5.9%) samples were positive for EHEC belonging to three serogroups as follows: O26 (n = 2), O111 (n = 2) and O103 (n = 5). The EHEC isolates were from cane rats (n = 6) and royal antelope (n = 3) and possessed virulence‑associated genes stx1 (77.8%), stx2 (100.0%), eaeA (100.0%) and hlyA (100.0%). Overall, 127 E. coli isolates showed resistance to ampicillin (99.2%), ceftiofur (90.6%), tetracycline (90.0%), cephalexin (87.4%), cefotaxime (50.4%), streptomycin 42.5%, ceftazidime (41.7%), nalidixic acid (37.0%), ciprofloxacin (43.6%), amoxicillin/clavulanic acid (32.3%), gentamicin (27.6%), sulphamethoxazole/trimethoprim (25.2%), norfloxacin (17.3%) and chloramphenicol (11.0%). The role of wildlife in the dissemination and transmission of antimicrobial resistant and zoonotic bacteria should not be neglected for effective preventive and control strategies.
References
Chausson A.M., Rowcliffe J.M., Escouflaire L., Wieland M. & Wright J. H. 2019. Understanding the sociocultural drivers of urban bushmeat consumption for behavior change interventions in Pointe Noire, Republic of Congo. Hum Ecol , 47, 179 – 191.
Cizek A., Alexa P., Literak I., Hamrík J., Novák P. & Smola J. 1999. Shiga toxin-producing Escherichia coli O157 in feedlot cattle and Norwegian rats from a large-scale farm. Lett Appl Microbiol, 28, 435–439.
Dias D., Caetano T., Torres R.T., Fonseca C. & Mendo S. 2019. Shiga toxin-producing Escherichia coli in wild ungulates. Sci Total Environ, 651(Pt 1), 203-209.
Dolejska M. & Literak, I. 2019. Wildlife is overlooked in the epidemiology of medically important antibiotic-resistant bacteria. Antimicrob Agents Chemother, 63 (8), e01167-19.
Eichhorn I., Heidemanns K., Semmler T., Kinnemann B., Mellmann A., Harmsen D., Anjum M.F., Schmidt H., Fruth A., Valentin-Weigand P., Heesemann J., Suerbaum S., Karch H. & Wieler, L. H. 2015. Highly virulent non-O157 enterohemorrhagic Escherichia coli (EHEC) serotypes reflect similar phylogenetic lineages, providing new insights into the evolution of EHEC. Appl Environ Microbiol, 81, 7041–7047. doi:10.1128/AEM.01921-15
Ferens W.A. & Hovde C.J. 2011. Escherichia coli O157:H7: Animal Reservoir and Sources of Human Infection. Foodborne Pathog Dis, 8 (4), 465 – 487
Friant S., Paige S.B. & Goldberg T.L. 2015. Drivers of bushmeat hunting and perceptions of zoonoses in Nigerian hunting communities. PLoS Negl Trop Dis, 9 (5), e0003792.
Furness L.E., Campbell A., Zhang L., Gaze W.H. & McDonald R.A. 2017. Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res, 154, 28 – 34
Haindongo N., Nkandi J., Hamatui N., Larai A.A., Hemberger M.Y., Khaiseb S. & Molini U. 2018. The prevalence of non-O157:H7 shiga toxin-producing Escherichia coli in Namibian game meat. Vet Ital, 54 (3), 185 – 188.
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.E.J. & Fèvre E.M. 2019. Clinically relevant antimicrobial resistance at the wildlife-livestock-human interface in Nairobi: an epidemiological study. Lancet Planet Health, 3 (6), e259 - e269. doi: 10.1016/S2542-5196(19)30083-X.
Ivbade A., Ojo O.E. & Dipeolu M.A. 2014. Shiga toxin-producing Escherichia coli O157:H7 in milk and milk products in Ogun State, Nigeria. Vet Ital, 50 (3), 185-191.
Kanayama A., Yahata Y., Arima Y., Takahashi T., Saitoh T., Kanou K., Kawabata K., Sunagawa T., Matsui T. & Oishi K. 2015. Enterohemorrhagic Escherichia coli outbreaks related to childcare facilities in Japan, 2010 – 2013. BMC Infect Dis, 15, 539.
Karp D.S., Gennet S., Kilonzo C., Partyka M., Chaumont N., Atwill E.R. & Kremen C. 2015. Comanaging fresh produce for nature conservation and food safety. Proc Natl Acad Sci, 112 (35), 11126 – 11131.
Kaspersen H. Urdahl A.N., Simm R., Slettemeås J.S., Lagesen K. & Norström M. 2018. Occurrence of quinolone resistant E. coli originating from different animal species in Norway. Vet Microbiol, 217, 25 – 31
Magwedere K., Dang H.A., Mills E.W., Cutter C.N., Roberts E.L. & DebRoy C. 2013. Incidence of shiga toxin-producing Escherichia coli strains in beef, pork, chicken, deer, boar, bison, and rabbit retail meat. J Vet Diagn Invest, 25 (2), 254 – 258.
Majowicz S.E., Scallan E., Jones-Bitton A., Sargeant J.M., Stapleton J., Angulo F.J., Yeung D.H. & Kirk M.D. 2014. Global incidence of human shiga toxin-producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis, 11, 447–455.
Mathusa E.C., Chen Y., Enache E. & Hontz L. 2010. Non-O157 shiga toxin-producing Escherichia coli in foods. J Food Prot, 73 (9), 1721 – 1736
Mikhail A.F.W., Jenkins C., Dallman T.J. Inns T., Douglas A., Martín A.I.C., Fox A., Cleary P., Elson R. & Hawker J. 2018. An outbreak of shiga toxin-producing Escherichia coli O157:H7 associated with contaminated salad leaves: epidemiological, genomic and food trace bac investigations. Epidemiol Infect, 146, 187-196.
Mo S.S., Urdahl A.M., Madslien K., Sunde M., Nesse L.L., Slettemeas J.S., Norström M. 2018. What does the fox say? Monitoring antimicrobial resistance in the environment using wild red foxes as an indicator. PLoS ONE, 13 (5), e0198019. doi:/10.1371/journal.pone.0198019.
Morsello C., Yagüe B., Beltreschi L., van Vliet N., Adams C., Schor T., Quiceno-Mesa M. P. & Cruz D. 2015. Cultural attitudes are stronger predictors of bushmeat consumption and preference than economic factors among urban Amazonians from Brazil and Colombia. Ecol Soc, 20 (4), 21. doi.org/10.5751/ES-07771-200421
Navarro-Gonzalez N., Porrero M.C., Mentaberre G., Serrano E., Mateos A., Domínguez L. & Lavín S. 2013. Antimicrobial resistance in indicator Escherichia coli isolates from free-ranging livestock and sympatric wild ungulates in a natural environment (Northeastern Spain). Appl Environ Microbiol, 79 (19), 6184 – 6186.
Ojo O.E., Ajuwape A.T.P., Otesile E.B., Owoade A.A., Oyekunle M.A. & Adetosoye A.I. 2010. Potentially zoonotic shiga toxin-producing Escherichia coli serogroups in the faeces and meat of food-producing animals in Ibadan, Nigeria. Intl J Food Microbiol, 142, 214 - 221.
Ojo O.E., Awoyomi O.J., Fabusoro E. & Dipeolu,M.A. 2017. Activities and influence of veterinary drug marketers on antimicrobial usage in livestock production in Oyo and Kaduna States, Nigeria. J Agric Rur Dev Trop Subtrop, 118 (2), 207–216.
Ojo O.E., Fabusoro E., Majasan A.A. & Dipeolu M.A. 2016. Antimicrobials in animal production: usage and practices among livestock farmers in Oyo and Kaduna States of Nigeria. Trop Anim Hlth Prod, 48, 189–197.
Ojo O.E., Schwarz S. & Michael G.B. 2016. Detection and characterization of extended-spectrum β-lactamase-producing Escherichia coli from chicken production chains in Nigeria. Vet Microbiol, 194, 62–68.
Paton A.W. & Paton J.C. 1998. Detection and characterization of shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic Escherichia coli hlyA, rfbO111, and rfbO157. J Clin Microbiol, 36, 598 – 602
Persad A.K. & LeJeune J.T. 2014. Animal reservoirs of shiga toxin-producing Escherichia coli. Microbiol Spectr, 2 (4), EHEC-0027-2014.*****(è proprio così)
Pruimboom-Brees I.M., Morgan T.W., Ackermann M.R., Nystrom E.D., Samuel J.E., Cornick N.A., & Moon H.W. 2000. Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc Natl Acad Sci, 97 (19), 10325–10329.
Rice D.H., Hancock D. D. & Besser, T.E. 2003. Faecal culture of wild animals for Escherichia coli O157:H7. Vet Rec, 152, 82 – 83.
Ritchie J.M., Thorpe C.M., Rogers A.B. & Waldor M.K. 2003. Critical Roles for stx2, eae, and tir in Enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun, 71, 7129–7139.
Rounds J.M., Rigdon C.E., Muhl L.J., Fordtner M., Danzeisen G.T., Koziol B.S., Taylor C., Shaw B.T., Short G.L. & Smith K.E. 2012. Non-O157 shiga toxin-producing Escherichia coli associated with venison. Emerg Infect Dis, 18 (2), 279 – 282.
Sánchez S., Martínez R., García A., Vidal D., Blanco J., Blanco M., Blanco J.E., Mora A., Herrera-León S., Echeita A., Alonso J.M. & Rey J. 2010. Detection and characterization of O157:H7 and non-O157 shiga toxin-producing Escherichia coli in wild boars. Vet Microbiol, 143, 420 - 423
Scaife H.R., Cowan D., Finney J., Kinghorn-Perry S.E. & Crook B. 2006. Wild rabbits (Oryctolagus cuniculus) as potential carriers of verocytotoxin-producing Escherichia coli. Vet Rec, 159, 175–178.
Stevens M.P., van Diemen P.M., Dziva F., Jones P.W. & Wallis T.S. 2002. Options for the control of enterohaemorrhagic Escherichia coli in ruminants. Microbiology 148: 3767–3778
Walz E., Wilson D., Stauffer J.C., Wanduragala D., Stauffer W.M., Travis D.A.& Alpern J.D. 2017. Incentives for bushmeat consumption and importation among West African immigrants, Minnesota, USA. Emerg Infect Dis, 23 (12), 2095 – 2097.
Zurfluh K., Albini S., Mattmann P., Kindle P., Nüesch-Inderbinen M., Stephan R. & Vogler B.R. 2019. Antimicrobial resistant and extended‐spectrum β‐lactamase producing Escherichia coli in common wild bird species in Switzerland. Microbiology open, 8 (11), e845. https:// doi.org/10.1002/mbo3.845. (****è proprio così)