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Antimicrobial resistance and virulence profile of enterococci isolated from poultry and cattle sources in Nigeria

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An Erratum to this article was published on 10 March 2017

Abstract

This study investigated the occurrence, antimicrobial resistance and virulence of Enterococcus from poultry and cattle farms. Three hundred and ninety samples: cloacal/rectal swabs (n = 260) and manure (n = 130] were processed for recovery of Enterococcus species. Standard bacteriological methods were used to isolate, identify and characterize Enterococcus species for antimicrobial susceptibility and expression of virulence traits. Detection of antibiotic resistance and virulence genes was carried out by polymerase chain reaction. Enterococcus was recovered from 167 (42.8%) of the 390 samples tested with a predominance of Enterococcus faecium (27.7%). Other species detected were Enterococcus gallinarum, Enterococcus faecalis, Enterococcus hirae, Enterococcus raffinosus, Enterococcus avium, Enterococcus casseliflavus, Enterococcus mundtii and Enterococcus durans. All the isolates tested were susceptible to vancomycin, but resistance to tetracycline, erythromycin, ampicillin and gentamicin was also observed among 61.0, 61.0, 45.1 and 32.7% of the isolates, respectively. Sixty (53.1%) of the isolates were multidrug resistant presenting as 24 different resistance patterns with resistance to gentamicin-erythromycin-streptomycin-tetracycline (CN-ERY-STR-TET) being the most common (n = 11) pattern. In addition to expression of virulence traits (haemolysin, gelatinase, biofilm production), antibiotic resistance (tetK, tetL, tetM, tetO and ermB) and virulence (asa1, gelE, cylA) genes were detected among the isolates. Also, in vitro transfer of resistance determinants was observed among 75% of the isolates tested. Our data revealed poultry, cattle and manure in this area are hosts to varying Enterococcus species harbouring virulence and resistance determinants that can be transferred to other organisms and also are important for causing nosocomial infection.

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References

  • Abamecha, A., Wondafrash, B., Abdissa, A., 2015. Antimicrobial resistance profile of Enterococcus species isolated from intestinal tracts of hospitalized patients in Jimma, Ethiopia, BMC Research Notes, 8, 213

    Article  Google Scholar 

  • Adesokan, H.K., Akanbi, I.O., Akanbi, I.M., Obaweda, R.A., 2015. Pattern of antimicrobial usage in livestock animals in south-western Nigeria: The need for alternative plans, Onderstepoort Journal Veterinary Research, 82, 816

    Article  Google Scholar 

  • Ajayeoba, T.A., Atanda, O.O., Obadina, A.O., Bankole, M.O., Adelowo, O.O., 2016. The incidence and distribution of Listeria monocytogenes in ready-to-eat vegetables in South-western Nigeria, Food Science and Nutrition, 4, 59 – 66

    Article  PubMed  Google Scholar 

  • Ali, S.A., Hasan, K.A., Bin Asif, H., Abbasi, A., 2014. Environmental enterococci: I. Prevalence of virulence, antibiotic resistance and species distribution in poultry and its related environment in Karachi, Pakistan, Letters in Applied Microbiology, 58, 423 – 432.

  • Amaechi, N., Nwankwo, I.U., 2015. Evaluation of prevalence and antimicrobial resistance using enterococci isolates from pigs and poultry birds in Abia State, Nigeria, International Journal Current Microbiology Applied Science, 4, 825-833

    Google Scholar 

  • Anyanwu, M.U., Obetta, T.U., 2015. Prevalence and antibiogram of generic enterococci in ready-to-slaughter beef cattle, Notulae Scientia Biologicae, 7, 390 - 399

    Article  Google Scholar 

  • Arias, C.A., Contreras, G.A., Murray, B.E., 2010. Management of multidrug-resistant enterococcal infections, Clinical Microbiology and Infection, 16, 555 – 562.

    Article  CAS  PubMed  Google Scholar 

  • Ayeni, F.A., Odumosu, B.T., Oluseyi, A.E., Ruppitsch, W., 2016. Identification and prevalence of tetracycline resistance in enterococci isolated from poultry in IIishan, Ogun State, Nigeria, Journal of Pharmacy and Bioallied Sciences, 8, 69 – 73.

    Article  Google Scholar 

  • Ben Said, L., Klibi, N., Dziri, R., Borgo, F., Boudabous, A., Ben Slama, K., Torres, C., 2016. Prevalence, antimicrobial resistance and genetic lineages of Enterococcus spp. from vegetable food, soil and irrigation water in farm environments in Tunisia, Journal of Food and Agriculture, 96, 1627 -1633.

    Article  CAS  Google Scholar 

  • Ben Sallem, R., Klibi, N., Klibi, A., Ben Said, L., Dziri, R., Boudabous, A., Torres, C., Ben Slama, K., 2016. Antibiotic resistance and virulence of enterococci isolates from healthy humans in Tunisia, Annals of Microbiology, 66, 717 – 725.

    Article  CAS  Google Scholar 

  • Billington, E.O., Phang, S.H., Gregson, D.B., Pitout, J.D.D., Ross, T., Church, D.L., Laupland, K.D., Parkins, M.D. 2014. Incidence, risk factor, and outcomes for Enterococcus spp blood stream infections: A population-based study, International Journal of Infectious Diseases, 26, 76 - 82.

    Article  CAS  PubMed  Google Scholar 

  • Bourafa, N., Loucif, L., Boutenfnouchet, N., Rolain, J-M., 2015. Enterococcus hirae, an unusual pathogen in humans causing urinary tract infection in a patient with benign prostatic hyperplasia: first case report in Algeria, New Microbes New Infection, 8, 7 – 9.

    Article  CAS  Google Scholar 

  • Chaffenel, F., Charron-Bourgoin, F., Libante, V., Leblond-Bourget, N., Payot, S., 2015. Resistance genes and genetic elements associated with antibiotic resistance in clinical and commensal isolates of Streptococcus salivarius, Applied and Environmental Microbiology, 81, 4155 - 4163

    Article  Google Scholar 

  • Chung, Y.S., Kwon, K.H., Shin, S., Kim, J.H., Park, Y.H., Yoon, J.W., 2014. Characterization of veterinary hospital associated isolates of Enterococcus species in Korea, Journal of Microbiology and Biotechnology, 24, 386 – 393

    Article  CAS  PubMed  Google Scholar 

  • CLSI 2015. Clinical and Laboratory Standards Institute: Performance Standard for Antimicrobial Susceptibility Testing; Twenty-fifth Informational Supplement. Document M100-S25.Vol 35, No 3.Clinical and Laboratory Standards Institute, Wayne, PA, USA. pp 72

  • Comerlato, C.B., de Resende, M.C.C., Caierao, J., d’Azevedo, P.A., 2013. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin, Memorias do Instituto Oswaldo Cruz, 108, 590 – 595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daneil, D.S., Lee, S.M., Dykes, G.A., Rahman, S., 2015. Public health risks of multiple drug resistant Enterococcus spp. in Southeast Asia, Applied Environmental Microbiology, 81, 6090 – 6097.

    Article  Google Scholar 

  • Gabre, R.M., Shakir, A., 2016. Prevalence of some human enteroparasites in commonly consumed raw vegetables in Tabuk, Saudi Arabia, Journal of Food Protection, 79, 655 – 658

    Article  CAS  PubMed  Google Scholar 

  • Hammerum, A.H., 2012. Enterococci of animal origin and their significance for public health, Clinical Microbiology and Infection, 18, 619 – 625.

    Article  CAS  PubMed  Google Scholar 

  • Hermanosvska, L., Bardon, J., Cermak, P., 2016. Vancomycin-resistant enterococci—the nature of resistance and risk of transmission from animals to humans, Klinicka Mikrobiol Infekcni Lékařství, 22, 54 – 60.

    Google Scholar 

  • Hidano, A., Yamamoto, T., Hayama, Y., Muroga, N., Kobayashi, S., Nishida, T., Tsutsui, T. 2015. Unraveling antimicrobial resistance genes and phenotype patterns among Enterococcus faecalis isolated from retail chicken products in Japan, PLoS One, 10, e0121189.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ho, P-L., Lai, E., Chan, P-Y., Lo, W-U., Chow, K-H., 2013. Rare occurrence of vancomycin-resistant Enterococcus faecium among livestock animals in China, Journal of Antimicrobial Chemotherapy, 68, 2948-2949

    Article  CAS  PubMed  Google Scholar 

  • Hollenbeck, B.L., Rice, L.B., 2012. Intrinsic and acquired resistance mechanisms in Enterococcus, Virulence, 3, 421 - 569

    Article  PubMed  PubMed Central  Google Scholar 

  • Iseeepi, R., Messi, P., Anacarso, I., Bondi, M., Sabia, C., Condo, C., de Niederhausern, S., 2015. Antimicrobial resistance and virulence traits in Enterococcus strains isolated from dogs and cats, New Microbiology, 38, 369 – 378

    Google Scholar 

  • Iweriebor, B.C., Obi, L.C., Okoh, A.I., 2015. Virulence and antimicrobial resistance factors of Enterococcus spp. isolated from fecal samples from piggery farms in Eastern Cape, South Africa, BMC Microbiology, 15, 136

  • Iweriebor, B.C., Obi, L.C., Okoh, A.I., 2016. Macrolide, glycopeptide resistance and virulence genes in Enterococcus species isolates from dairy cattle, Journal of Medical Microbiology, 65, 641-648,

    Article  CAS  PubMed  Google Scholar 

  • Jackson, C.R., Lombard, J.E., Dargatz, D.A., Fedorka-Cray, P.J., 2011. Prevalence, species distribution and antimicrobial resistance of enterococci isolated from US dairy cattle, Letters in Applied Microbiology, 52, 41 – 48.

    Article  CAS  PubMed  Google Scholar 

  • Jurado-Rabadan, S., de la Fuente, R., Ruiz-Santa-Quiteria, J.A., Orden, J.A., de Vries, L.E., Agerso, Y., 2014. Detection and linkage to mobile genetic elements of tetracycline resistance gene tet(M) in Escherichia coli isolates from pigs. BMC Veterinary Research, 10, 155

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaiser, T.D.L., Pereira, E.M., dos Santos, K.R.N., Maciel, E.L.N., Schuenck, R.P., Nunes, A.P.F., 2013. Modification of the Congo red agar method to detect biofilm production by Staphylococcus epidermidis, Diagnostic Microbiology and Infectious Disease,75, 235 - 239.

    Article  CAS  PubMed  Google Scholar 

  • Kajihara, T., Nakamura, S., Iwanaga, N., Oshime, K., Takazono, T., Wiyazaki, T., Izumikawa, K., Yanagihar, K., Kohno, N., Kohno, S., 2015. Clinical characteristics and risk factors of enterococcal infections in Nagasaki, Japan: A retrospective study, BMC Infectious Diseases, 15, 426.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan, H.A., Ahmad, A., Mehboob, R., 2015. Nosocomial infections and their control strategies, Asian Pacific Journal of Tropical Biomedicine, 5, 509 - 514

    Article  Google Scholar 

  • Kim, D.H., Chung, Y.S., Park, Y.K., Yang, S-J., Lim, S.K., Park, H.Y., Park, K.T., 2016. Antimicrobial resistance and virulence profiles of Enterococcus spp. isolated from horses in Korea, Clinical Immunology, Microbiology and Infectious Disease, 48, 6 - 13

    Article  Google Scholar 

  • Klibi, A., Ben Lagha, A., Ben Slama, K., Boudabous, A., Torres, C., 2013. Faecal enterococci from camels in Tunisia: species, antibiotic resistance and virulent genes, Veterinary Records, 172, 213.

    Article  CAS  Google Scholar 

  • Klibi, N., Aouini, R., Borgo, F., BenSaid, L., Ferrario, C., Dziri, R., Boudabous, A., Torres, C., Ben Slama, K., 2015. Antibiotic resistance and virulence of faecal enterococci isolated from food-producing animals in Tunisia, Annals of Microbiology, 65, 695 - 702.

    Article  CAS  Google Scholar 

  • Kwon, K.H., Hwang, S.Y., Moon, B.Y., Park, Y.K., Shin, S., Hwang, C-Y., Park, Y.H., 2012. Occurrence of antimicrobial resistance and virulence genes, and distribution of enterococcal clonal complex 17 from animals and human beings in Korea, Journal of Veterinary Diagnostic Investigation, 24, 924 – 931.

    Article  PubMed  Google Scholar 

  • Laird, P.W., Ziderveld, A., Linders, K., Rudnicki, M.A. Jaenish, R., Berns, A., 1991. Simplified mammalian DNA isolation procedure, Nucleic Acids Research, 19, 4293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., Liu, K., Lai, J., Wu, C., Shen, J., Wang, Y., 2012. Prevalence and antimicrobial resistance of Enterococcus species of food animal origin from Beijing and Shandong Province, China, Journal of Applied Microbiology, 114, 555 – 563.

    Article  PubMed  Google Scholar 

  • Lozano, C., Gonzalez-Barrio, D., Camacho, M.C., Lima-Barbero, F.J., de la Puente, J., Hofle, U., Torres, C., 2015a. Characterization of fecal vancomycin-resistant enterococci with acquired and intrinsic resistance mechanisms in wild animals, Spain, Microbial Ecology, 72, 813 - 820

    Article  Google Scholar 

  • Lozano, C., Gonzalez-Barrio, D., Garcia, J.T., Ceballos, S., Olea, P.P., Ruiz-Fons, F., Torres, C., 2015b. Detection of vancomycin-resistant Enterococcus faecalis ST6-vanB2 and E. faecium ST915-vanA in faecal samples of wild Rattus rattus in Spain, Veterinary Microbiology, 177, 168 – 174

    Article  CAS  PubMed  Google Scholar 

  • Manero, A., Blanch, A.R., 1999. Identification of Enterococcus spp. with a biochemical key, Applied and Environmental Microbiology, 65, 4425 - 4430.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martins, E., Novais, C., Freitas, A.R., Dias, A.R.,Ribeiro, T.G., Antunes, P., Peixe, L., 2015. Filling the map for antimicrobial resistance in sub-Saharan Africa: ampicillin-resistant Enterococcus from non-clinical sources in Angola, Journal of Antimicrobial Chemotherapy, 70, 2914 - 2916.

    Article  CAS  PubMed  Google Scholar 

  • Ng, L.K., Martin, I., Alfa, M., Mulvev, M., 2001. Multiplex PCR for the detection of tetracycline resistant genes, Molecular and Cellular Probes, 15, 209 - 215.

    Article  CAS  PubMed  Google Scholar 

  • Nisson, O., 2012. Vancomycin resistant enterococci in farm animals-occurrence and importance, Infection EcologyEpidemiology,2:

  • O’Driscoll, T., Crank, C.W., 2015. Vancomycin-resistant enterococcal infections: epidemiology, clinical manifestation and optimal management, Infection and Drug Resistance, 8, 217 – 230

  • Oguntoyinbo, F.A., Okueso, O., 2013. Prevalence, distribution and antibiotic resistance pattern among enterococci species in two traditional fermented dairy foods, Annals of Microbiology, 63, 55.

    Article  Google Scholar 

  • Oliveira, M., Tavares, M., Gomes, D., Touret, T., Braz, B.S., Tavares, L., Semedo-Lemsaddek, T., 2016. Virulence traits and antibiotic resistance among enterococci isolated from dogs with periodontal disease, Comparative Immunology, Microbiology and Infectious Diseases, 46, 27 -31.

    Article  PubMed  Google Scholar 

  • Olonitola, O.S., Fahrenfeld, N., Pruden, A., 2015. Antibiotic resistance profile among mesophilic aerobic bacteria in Nigerian chicken litter and associated antibiotic resistance genes, Poultry Science, 94, 867 – 874.

    Article  CAS  PubMed  Google Scholar 

  • Oluwasile, B.B., Agbaje, M., Ojo, O.E., Dipeolu, M.A., 2014. Antibiotic usage pattern in selected poultry farms in Ogun state, Sokoto Journal of Veterinary Science, 12, 45 - 50.

    Article  Google Scholar 

  • Osman, K.M., Ali, M.N., Radwan, I., ElHofy, F., Abed, A.H., Orabi, A., Fawzy, N.M., 2016 Dispersion of the vancomycin resistance genes vanA and vanC of Enterococcus isolated from Nile Tilapia on retail sale: A public health hazard. Frontiers in Microbiology, 7, 1354.

    PubMed  PubMed Central  Google Scholar 

  • Pruksakom, C., Pimam, C., Boonsoongnem, A., Narongsak, W., 2016. Detection and phenotypic characterization of vancomycin-resistant Enterococcus in pigs in Thailand, Agriculture and Natural Resources, 50, 199 – 203

    Article  Google Scholar 

  • Ristori, C.A., Rowlands, R.E.G., Bergamini, M.M., Lopes, G.I.S.L., de Paula, M.R., de Olivera, M.A., Lima, M., Tegani, L.S., Watanabe, A.H., Jakabi, M., Zanella, R.C., 2012. Prevalence and antimicrobial susceptibility profile of Enterococcus species isolated from frozen chicken carcasses. Revista do Instituto Adolfo Lutz (Impresso), 71, 237 - 243

    CAS  Google Scholar 

  • Schwaiger, K., Schmied, E.M.V., Bauer, J., 2010. Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany, Zoonoses and Public Health, 57, 171 - 180.

    Article  CAS  PubMed  Google Scholar 

  • Shirin, K., Mohsen, E., Javad, S., Gholamreza, I., Nour, A., Malihe, T., 2016. Detection of virulence genes in enterococci isolated from the human normal flora by multiplex-polymerase chain reaction, Infectious Diseases in Clinical Practice, 24, 227 - 230

    Article  Google Scholar 

  • Steoien-Pysniak, D., Marek, A., Banach, T., Adaszek, L., Pysik, E., Wilczyrisk, J., Winiarcyk, S., 2016. Prevalence and antibiotic resistance of Enterococcus strains isolated from poultry, Acta Veterinaria Hungarica, 64: doi: 10.1556/004.2016.016

  • Sutcliffe, J., Grebe, T., Tait-Kamradt, A., Wondrack, L., 1996. Detection of erythromycin-resistant determinants by PCR, Antimicrobial Agents and Chemotherapy, 40, 2562 - 2566.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tremblay, C-L., Letellier, A., Quessy, S., Daignault, D., Archambault, M., 2012. Antibiotic-resistant Enterococcus faecalis in abattoir pigs and plasmid colocalization and cotransfer of tet(M) and erm(B) genes, Journal of Food Protection, 75, 1595 - 1602

    Article  CAS  PubMed  Google Scholar 

  • Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D., Goossens, H., 2004. Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hylgenes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium, Journal of Clinical Microbiology, 42, 4473 - 4479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventola, L.C., 2015. The antibiotic resistance crisis. Part I: causes and threats, Pharmacy and Therapeutics, 40, 1- 3

    Google Scholar 

  • von Wintersdorff, C.J.H., Penders, J., van Niekerk, J.M., Mills, N.D., Majumder, S., van Alphen, L.B., Savelkoul, P.H.M., Wolffs, P.F.G., 2016. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer, Frontiers in Microbiology, 7, 173

    Google Scholar 

  • Woolhouse, M., Ward, M., van Bunnik, B., Farrar, J., 2015. Antimicrobial resistance in humans, livestock and the wider environment, Philosophical Transactions of the Royal Society B, 370, 20140083

    Article  Google Scholar 

  • Wurster, J.I., Saavedra, J.T., Gilmore, M.S., 2016.Impact of antibiotic use on the evolution of Enterococcus faecium, Journal of Infectious Diseases, 213, 1862 – 1865.

    Article  PubMed  Google Scholar 

  • Yilmaz, E.S., Aslantas, O., Onen, S.P., Turkylmaz, S., Kurekci, C., 2016. Prevalence, antimicrobial resistance and virulence traits in enterococci from food of animal origin in Turkey, LWT - Food Science and Technology, 66, 20 – 26

    Article  CAS  Google Scholar 

  • Zischka, M., Kunne, C.T., Blom, J., Wobser, D., Saknc, T., Schmidt-Hohagen, K., Dabrowski, P.W., Nitsche, A., Hübner, J., Hain, T., Chakraborty, T., Linke, B., Goesmann, A., Voget, S., Daniel, R., Schomburg, D., Hauck, R., Hafez, H.M., Tielen, P., Jahn, D., Solheim, M., Sadowy, E., Larsen, J., Jensen, L.B., Ruiz-Garbajosa, P., Pérez, D.Q., Mikalsen, T., Bender, J., Steglich, M., Nubel, U., Witte, W., Werner, G., 2015. Comprehensive molecular, genomic and phenotypic analysis of a major clone of Enterococcus faecalis MLST ST40, BMC Genomics, 16, 175

    Article  PubMed  PubMed Central  Google Scholar 

  • Yusuf, T.M., Tiamiyu, S.A., Aliu, R.O. 2016. Financial analysis of poultry production in Kwara State, Nigeria, African Journal of Agricultural Research, 11, 718 - 723

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to Prof Frank Møller Aarestrup and Dr. Susanne Karlsmose Pedersen of the WHO Center for Antimicrobial Resistance in Foodborne Pathogens, EU Reference laboratory for Antimicrobial Resistance, National Food Institute, Technical University of Denmark, for providing the control strain used in this study.

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Correspondence to Emmanuel Ochefije Ngbede.

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An erratum to this article is available at http://dx.doi.org/10.1007/s11250-017-1261-4.

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Ngbede, E.O., Raji, M.A., Kwanashie, C.N. et al. Antimicrobial resistance and virulence profile of enterococci isolated from poultry and cattle sources in Nigeria. Trop Anim Health Prod 49, 451–458 (2017). https://doi.org/10.1007/s11250-016-1212-5

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