Occurrence, antibiogram, high-level vancomycin and aminoglycosides resistance and potential virulence factors of enterococci in dogs in Nigeria
Published:
Jan 21, 2023
Keywords:
aminoglycoside resistance canine enterococci vancomycin resistance virulence
Abstract
Abstract
This study was conducted to isolate enterococci from dogs in Nigeria, and to determine the potential virulence, antibiotic susceptibility, phenotypic vancomycin (VAN), high-level ampicillin (AMP) and aminoglycosides susceptibility profile of the isolates. Rectal swabs were collected from 295 randomly-selected, clinically-healthy dogs. The isolation of enterococci was done using Slanetz and Bartley enterococcal selective medium. The resistance of 150 non-repetitive isolates was determined using disc diffusion method. VAN resistance was assessed by high-level disc diffusion and agar-screening methods. High-level AMP and aminoglycosides (gentamicin and streptomycin) resistance was determined by agar-screening method. Potential virulence factors were assayed using phenotypic methods. Out of 295 samples, 234 (80.7%) gave positive growth. From these, 250 enterococcal isolates comprised 229 (91.6%) non-pigmented and 21 (8.4%) pigmented strains, were obtained. Resistance of the isolates was 89% to erythromycin, 92% to rifampicin, 77% to chloramphenicol, 83% to tetracycline, 64% to ciprofloxacin, 32.7% to VAN, 24.7% to high-level streptomycin (HLS) and 6% to high-level gentamicin (HLG). Among 150 non-repetitive resistant isolates, 144 (96%), including all the VAN-, HLS- and HLG-resistant strains, exhibited resistance to at least 3 classes of antibiotics. The mean multiple antibiotic resistance index was 0.54 (range = 0.22 – 0.89). Of these 150 isolates, 94 (62.7%), including all the VAN-, HLS- and HLG-resistant strains, displayed virulence potentials as biofilm (44.7%), surface-layer (13.8%), haemolysin (21.3%), gelatinase (40.4%), caesinase (10.6%) and deoxyribonuclease (12.8%) activities. This study showed that dogs in Nigeria are potential reservoirs and disseminators of potentially-virulent, multidrug-, VAN- and high-level aminoglycosides-resistant enterococci.Article Details
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Anyanwu, M., Eze, U., Nnamani, J., Ikenna-Ezeh, N., Akpa, P., Okorie-kanu, O., & Anene, B. (2023). Occurrence, antibiogram, high-level vancomycin and aminoglycosides resistance and potential virulence factors of enterococci in dogs in Nigeria. Journal of the Hellenic Veterinary Medical Society, 73(4), 4689–4696. https://doi.org/10.12681/jhvms.27783
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- Vol. 73 No. 4 (2022)
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- Research Articles
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References
Aasmäe B, Volkova J, Häkkinen L, Orro T, Tenson T, Kalmus P (2015). In vitro antimicrobial resistance of intestinal Escherichia coli and enterococci in clinically healthy dogs in Estonia. Veterinarija IR Zootechnika (Vet Med Zoot). T. 72 (94). 2015
Amaechi N., Nwankwo I.U. (2015) Evaluation of prevalence and antimicrobial resistance using enterococci isolates from pigs and poultry and birds in Abia State, Nigeria. Int. J. Curr. Microbiol. Appl. Sci., 4:825-833.
Anyanwu MU, Obetta TU (2015). Prevalence and antibiogram of generic enterococci in ready-to-slaughter beef cattle. Not Sci Biol, 7(4):390-399
Anyanwu MU, Okorie-Kanu OJ, Ogugua AJ, Ezenduka EV, Anidebe CO (2019). Occurrence, antibiogram and vancomycin resistance of generic enterococci in horses in Nigeria. Revue Méd. Vét., 170, 1-3, 46-52
Anyanwu MU, Ugwu IC, Ezekwelu MO, Okorafor ON (2017). Prevalence and antibiogram of generic extended-spectrum β-lactam-resistant enterobacteria in healthy dogs. Notulae Scientia Biologicae, 9(1): 22-33.
Ayeni F.A., Odumosu B.T., Oluseyi A.E., Ruppitsch W.: Identification and prevalence of tetracycline resistance in enterococci isolated from poultry in Ilishan, Ogun State, Nigeria. J. Pharm. Bioallied Sci., 2016, 8, 69-73.
Bertelloni F, Salvadori C, Lotti G, Cerri D, Ebani VV (2017) Antimicrobial resistance in Enterococcus strains isolated from healthy domestic dogs. Acta Microbiologica et Immunologica Hungarica 64 (3):301–312
Bertelloni F, Salvadori C, Lotti G, Cerri D, Ebani VV. (2017) Antimicrobial resistance in Enterococcus strains isolated from healthy domestic dogs. Acta Microbiologica et Immunologica Hungarica 64(3):301–312.
Beshiru A, Igbinosa IH, Omeje FI, Ogofure AG, Eyong MM, Igbinosa EO (2017) Multi-antibiotic resistant and putative virulence gene signatures in Enterococcus species isolated from pig farms environment. Microbial Pathogenesis 104 (2017) 90e96
Boynukara, B., Ekin, İ.H., Aksakal, A., Gulhan, T. (2002). Isolation and antibiotic susceptibility of enterococci from human, dog and cat faeces. Vet. Hek. Mikrobiyol. Derg., 2:37-42.
Cartwright CP, Stock F, Fahle GA, Gill VJ (1995) Comparison of pigment production and motility tests with PCR for reliable identification of intrinsically vancomycin-resistant enterococci. J Clin Microbiol. 33(7): 1931–1933.
Cinquepalmi V, Monno R, Fumarola L, Ventrella G, Calia C, Greco MF, Danila de Vito, and Soleo L. (2013) Environmental contamination by dog’s faeces: a public health problem? Int. J. Environ. Res. Public Health 2013, 10, 72-84; doi:10.3390/ijerph10010072
Clinical and Laboratory Standards Institute (CLSI). (2020). Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute.
Damborg P., Top J., Hendrickx A.P.A, Dawson S, Willems R.J.L, Guardabassi L (2009) Dogs are a reservoir of ampicillin-resistant Enterococcus faecium lineages associated with human infections. Applied and Environmental Microbiology, 75(8):, p. 2360–2365
De Graef, E.M., Decostere, A., Devriese, L.A. and Haesebrouck, F. (2004) Antibiotic resistance among fecal indicator bacteria from healthy individually owned and kennel dogs. Microb Drug Resist 10, 65–69.
De Leener E, Decostere A, De Graef EM, Moyaert H, Haesebrouck F (2005) Presence and mechanism of antimicrobial resistance among enterococci from cats and dogs. Microbial Drug Resistance, 11(4):395-403.
Delgado, M., Neto, I., Correia, J. H. and Pomba, C. (2007) Antimicrobial resistance and evaluation of susceptibility testing among pathogenic enterococci isolated from dogs and cats. Int. J. Antimicrob. Agents 30: 98–100.
Devriese, L. A., M. Ieven, H. Goossens, P. Vandamme, B. Pot, J. Hommez, and F. Haesebrouck. (1996). Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrob. Agents Chemother. 40:2285–2287.
Eze UU, Nwosu C, Dan-Jumbo SO, Ogbu KI, Anene BM, Okeke OS, Ogunkoya AB (2009). The role of dog markets in the spread of rabies in Enugu State, South Eastern Nigeria. Epizootiology and Animal Health in West Africa 5:35-42
Finisterra L, Duartea B, Peixe L, NovaiC, Freitas AR (2021). Industrial dog food is a vehicle of multidrug-resistant enterococci carrying virulence genes often linked to human infections. International Journal of Food Microbiology, https://doi.org/10.1016/j.ijfoodmicro.2021.109284
Ghosh A, Dowd SE, Zurek L (2011) Dogs leaving the ICU carry a very large multi-drug resistant enterococcal population with capacity for biofilm formation and horizontal gene transfer. PLoS ONE 6(7): e22451.
Gulhan T, Aksakal A, Ekün UH, Savaþan S, Boynukara B (2006) Virulence factors of Enterococcus faecium and Enterococcus faecalis strains isolated from humans and pets. Turk. J. Vet. Anim. Sci. 30: 477-482
Igbinosa EO and Beshiru A (2019) Antimicrobial resistance, virulence determinants, and biofilm of Enterococcus species from ready-to-eat seafood. Front. Microbiol. 10:728.
Iseppi R, Messi P, Anacarso I, Bondi M, Sabia C, Condò C, de Niederhausern S (2015) Antimicrobial resistance and virulence traits in Enterococcus strains isolated from dogs and cats. New Microbiologica, 38:369-378.
Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Frye JG (2009) Prevalence, species distribution and antimicrobial resistance of enterococci isolated from dogs and cats in the United States. Journal of Applied Microbiology, 107:1269–1278
Kataoka Y, Ito C, Kawashima A, Ishii M, Yamashiro S, Harada K, Ochi H, Sawada T. (2013). Identification and antimicrobial susceptibility of enterococci isolated from dogs and cats subjected to differing antibiotic pressures. J. Vet. Med. Sci. 75(6): 749–753
Kirkan S, Ugur Parin1, Gamze Balat. (2019) Antimicrobial resistance of Enterococcus faecium isolated from the urinary system of dogs. Mac Vet Rev 2019; 42 (1): i-vii
Krumperman PH (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied Environmental Microbiology 46(1):165-170.
Leite-Martins L, Mahú MI, Costa AL, Bessa LJ, Vaz-Pires P, Loureiro L, Niza-Ribeiro J, de Matos AJF, Martins da Costa P. (2015) Prevalence of antimicrobial resistance in faecal enterococci from vet-visiting pets and assessment of risk factors. Vet. Rec. 176(26), 674 (2015).
Magiorakos A, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske C.G., Harbarth S., Hindler J.F., Kahlmeter G., Olsson-liljequist B., Paterson D.L., Rice L.B., Stelling J., Struelens M.J., Vatopoulos A., Weber J.T. Monnet D.L. Multidrug resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18: 268–281
Manero A, Blanch AR (1999) Identification of Enterococcus spp. with a Biochemical key. Applied and Environmental Microbiology, 65(10): 4425–4430.
Miranda C, Vanessa Silva, Gilberto Igrejas, Patrıcia Poeta (2021) Impact of European pet antibiotic use on enterococci and staphylococci antimicrobial resistance and human health. Future Microbiol. (2021) 16(3), 185–201.
Ngbede E.O., Raji M.A., Kwanashie C.N., Kwaga J.K.P (2017a). Antimicrobial resistance and virulence profile of enterococci isolated from poultry and cattle sources in Nigeria. Trop. Anim. Health Prod., 2017, 49, 451-458.
Ngbede E.O., Raji M.A., Kwanashie C.N., Kwaga J.K.P., Adikwu A.A., Maurice N.A., Adamu A.M (2017b) Characterization of high level ampicillin- and aminoglycoside enterococci isolated from non-hospital sources. J. Med. Microbiol., 2017, 66, 1027-1032.
Oguttu JW, Qekwana DN and Odoi A (2021) Prevalence and predictors of antimicrobial resistance among Enterococcus spp. from dogs presented at a veterinary teaching hospital, South Africa. Front. Vet. Sci. 7:589439.
Oliveira M, Tavares M, Gomes D, Touret T, São Braz B, 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.
Osman, K. M., Badr, J., Orabi, A., Elbehiry, A., Saad, A., Ibrahim, M. D. S., et al. (2019). Poultry as a vector for emerging multidrug resistant Enterococcus spp.: first report of vancomycin (van) and the chloramphenicol–florfenicol (cat-fex-cfr) resistance genes from pigeon and duck faeces. Microb. Pathog. 128, 195–205.
Ossiprandi MC, Zerbini L. (2015) Antimicrobial susceptibility of enterococcal species isolated from Italian dogs. IntechOpen http://dx.doi.org/10.5772/61778
Pillay S., Zishiri O.T, Adeleke MA(2018). Prevalence of virulence genes in Enterococcus species isolated from companion animals and livestock. Onderstepoort J Vet Res., 85(1):1583.
Pillay, S., Zishiri, O.T, Adeleke M.A., (2018). Prevalence of virulence genes in Enterococcus species isolated from companion animals and livestock. Onderstepoort Journal of Veterinary Research 85(1):a1583.
Poeta, P, Costa D, Rodrigues J, Torres, C (2006). Antimicrobial resistance and the mechanisms implicated in faecal enterococci from healthy humans, poultry and pets in Portugal. Inter. J. Antimicrob. Agents 27, 131–137.
Ramnath L, Sithole B, Govinden R (2017) Identification of lipolytic enzymes isolated from bacteria indigenous to Eucalyptus wood species for application in the pulping industry. Biotechnol Rep (Amst). 15:114-124.
Rodrigues, J., Poeta, P., Martins, A. and Costa, D. (2002) The importance of pets as reservoirs of resistant Enterococcus strains, with special reference to vancomycin. J Vet Med B Infect Dis Vet Public Health 49, 278–280.
Said L, Dziri R, Sassi N, Lozano C, Ben Slama K, Ouzari I, Torres C, Klibi N (2017) Species distribution, antibiotic resistance and virulence traits in canine and feline enterococci in Tunisia. Acta Vet Hung, 65(2):173-184.
Solati SM, Tajbakhsh E, Khamesipour F, Gugnani HC (2015) Prevalence of virulence genes of biofilm producing strains of Staphylococcus epidermidis isolated from clinical samples in Iran. AMB Express, 5(1):134
Torres C., Alonso C.A., Ruiz-Ripa L., Leónsampedro R., Del Campo R., Coque T.M. (2018) Antimicrobial resistance in Enterococcus spp. of animal origin. Microbiol. Spectr., 2018, 6, doi:10.1128/ microbiolspec.ARBA-0032-2018.
Turkyilmaz S, Erdem V, Bozdoğan B (2010) Investigation of antimicrobial susceptibility for enterococci isolated from cats and dogs and the determination of resistance genes by polymerase chain reaction. Turk. J. Vet. Anim. Sci. 34(1): 61-68
Vu J, Carvalho J, Quiloan MLG (2012). Enterococcus faecalis can be distinguished from Enterococcus faecium via differential susceptibility to antibiotics and growth and fermentation characteristics on mannitol salt agar. Front Biol, 7(2):167-177.
Wada Y, Harun AB., Yean CY, Zaidah AR (2020). Vancomycin-resistant enterococci (VRE) in Nigeria: the first systematic review and meta-analysis. Antibiotics 9:565.
Wada Y, Irekeola A.A, E.A.R. E.N.S, Yusof W, Lih Huey L, Ladan Muhammad S, Harun A, Yean C.Y, Zaidah A.R. (2021). Prevalence of vancomycin-resistant Enterococcus (VRE) in companion animals: the first meta-analysis and systematic review. Antibiotics, 10:138.
World Health Organization (WHO) (2017). Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics http://www.who.int/medicines/publications/WHOPPL-Short_Summary_25FebET_NM_WHO.pdf.
Zhao J, W Xie, X Lin, AR Baloch and X Zhang. (2012). Antimicrobial resistance in enterococci isolates from pet dogs in Xi’an, China. Pak Vet J., 32(3): 462-464.
