Tavuk Etlerinde Enterococcus spp. Prevelansı, Direnç Profilleri, VanA ve VanB Direnç Genlerinin Varlığı

Year 2022, , 381 - 389, 31.12.2022

Rabia Mehtap Tuncay , Yakup Can Sancak

https://doi.org/10.30607/kvj.1110734

Abstract

Türkiye’de Van ili piyasasından toplanan tavuk eti örneklerinde Enterococcus spp. prevelansı ve antibiyotik dirençliliği ve VanA ve VanB direnç genlerinin belirlenmesi amaçlandı. Çalışmada 100 adet tavuk eti örneği kullanıldı. Bunların 27’si (%27) Enterococcus spp. pozitif bulundu. Enterococcus spp. için pozitif olan 27 tavuk eti örneğinden toplam 67 izolat elde edildi. Bunlardan 53’ü (%79.10) E. faecalis, 14’ü (%20.90) ise E. faecium olarak tespit edildi. Antibiyotik dirençlilikleri incelenen analizler sonucunda Enterococcus spp. izolatlarının 48’sinin (%71.64) iki veya daha fazla antibiyotiğe dirençli olduğu, 19’sinin (%28.36) ise en az bir antibiyotiğe dirençli olduğu tespit edilmiştir. E. faecalis ve E. faecium suşlarının en az %50’si ampisilin, penisin, kloramfenol, vankomisin ve gentamisine duyarlı ve orta düzeyde olduğu tespit edildi. Ayrıca fenotipik olarak vankomisine dirençli ve orta düzeyde olan 13 izolatta VanA ve VanB geni varlığı PCR testi ile araştırıldı. PCR testi ile analizi yapılan izolatların hiçbirinde VanA ve VanB geni tespit edilemedi. Sonuç olarak, tavuk etlerinde Enterococcus spp. tespit edilmesi hijyenik koşullara dikkat edilmediğinin göstergesidir. Aynı zamanda bu gıdalardan elde edilen izolatlarda çoklu antibiyotik dirençliliğinin var olması ayrıca fenotipik olarak belirlenen dirençliliklerin halk sağlığını tehdit edebileceğini düşündürmektedir.

Keywords

Enterococcus spp., Tavuk eti, VanA, VanB

The Prevalence of Enterococcus spp., Resistance Profiles, the Presence of the VanA and VanB Resistance Genes in Chicken Meats

Abstract

The aim of the present study was to investigate the prevalence of Enterococcus spp., resistance profiles, and the presence of the VanA and VanB resistance genes in the chicken meat samples that were collected from the Van market, Turkey. A total of 100 chicken meat samples were used. Among the samples, 27 (27%) were Enterococcus spp. positive. A total of 67 isolates were obtained from 27 chicken meat samples, which were positive for Enterococcus spp. Among the 67 isolates, 53 (79.10%) were identified to be E. faecalis and 14 (20.90%) were identified to be E. faecium. The analysis of antibiotic resistance revealed that 48 isolates (71.74%) exhibited resistance to multiple antibiotics and 19 isolates (28.36%) were resistant to at least one antibiotic. At least 50% of the E. faecalis and E. faecium strains were intermediately sensitive to ampicillin, penicillin, chloramphenicol, vancomycin, and gentamicin. Moreover, the presence of the VanA and VanB genes in 13 strains that were phenotypically and intermediately resistant to vancomycin was examined by PCR test. The PCR analysis revealed that no isolate had the VanA and VanB genes. As a result, the detection of Enterococcus spp. in chicken meat is an indication of not paying attention to hygienic conditions. At the same time, the existence of multiple antibiotic resistance in isolates obtained from these foods also suggests that phenotypically determined resistances may threaten public health.

Keywords

Chicken meat, Enterococcus spp., VanA, VanB

References

• Adams MR, Moss MO. Food Microbiology. 3th Ed., Royal Society of Chemistry Publishing, Cambridge, UK. 2008.
• Ahmed MO, Baptiste KE. Vancomycin-resistant enterococci: a review of antimicrobial resistance mechanisms and perspectives of human and animal health. Microbial Drug Resist. 2018; 24(5): 590-606.
• Anonymous. The Microbiology Manual. LABM Ltd, UK. 2015.
• Arthur M, Courvalin P. Genetics and mechanisms of glycopeptide resistance in Enterococci. Antimicrob Agents Chemother. 1993; 37(8): 1593-1571.
• Aslam M, Diarra MS, Checkley S, Bohaychuk V, Masson L. Characterization of antimicrobial resistance and virulence genes in Enterococcus spp. isolated from retail meats in Alberta, Canada. Int J Food Microbiol. 2012; 156(3): 222-230.
• Bauer RW, Kirby MDK, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966; 45:493-496.
• Bayram G, Delialioğlu N, Emekdaş G. Prevelance and identification of Enterococcus spp. from consumed Meats in Mersin city. Mersin University Journal of Health Sciences 2011; 4(2): 12-16.
• Boehm AB, Sassoubre LM. Enterococci as Indicators of Environmental Fecal Contamination, In: Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, Ed; Gilmore MS, Clewell DB, Ike Y, Shankar N, Massachusetts Eye and Ear Infirmary, Boston. 2014.
• Bonacina J, Suarez N, Hormigo R, Fadda S, Lechner M, Saavedra L. A genomic view of food-related and probiotic Enterococcus strains. Dna Research. 2017; 24(1): 11-24.
• Cetinkaya Y, Falk P, Mayhall CG. Vancomycin-resistant enterococci. Clin Microbiol Rev. 2000; 13(4): 686-707.
• Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria, VET08, 4th Ed., Clinical and Laboratory Standards Institute, USA. 2018; pp. 20-33.
• Çöleri A, Çökmüş C. Molecular mechanisms of resistance to glycopeptide antibiotics in Enterococcus species and modes of gene transfer. Turkish Bulletin of Hygiene and Experimental Biology 2008; 65(2): 87-96.
• Donado-Godoy P, Byrne BA, León M, Castellanos R, Vanegas C, Coral A, Arevalo A, Clavijo V, Vargas M, Zuñiga JJR, Tafur M, Pérez-Gutierrez E, Smith WA. Prevalence, resistance patterns, and risk factors for antimicrobial resistance in bacteria from retail chicken meat in Colombia. J Food Protect. 2015; 78(4): 751-759.
• Foulquié-Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. The role and application of enterococci in food and health. Int J Food Microbiol. 2006; 106(1): 1-24. Giraffa G. Enterococci from foods. FEMS Microbiol Rev. 2002; 26(2): 163-171.
• Gousia P, Economou V, Bozidis P, Papadopoulou C. Vancomycin-resistance phenotypes, vancomycin-resistance genes, and resistance to antibiotics of enterococci isolated from food of animal origin. Foodborne Pathog Dis, 2015; 12(3): 214-220.
• Gökmen M, Ektik N. Determination of Virulence Factors and Antibiotic Resistances of Enterococcus spp. Identified from Different Stages of Ripened (Classical) White Cheese Production. Kocatepe Veterinary Journal, 2022; 15(1): 120-127.
• Prieto AMG, van Schaik W, Rogers MR, Coque TM, Baquero F, Corander J, Willems RJL. Global emergence and dissemination of enterococci as nosocomial pathogens: attack of the clones? Front Microbiol.2016; 788(7): 1-15.
• Halkman AK (2019). Gıda Mikrobiyolojisi. Başak Matb.ve Tanıtım Hiz. Ltd, Ankara. PP: 648.
• Handwerger S, Perlman DC, Altarac D, McAuliffe V. Concomitant high-level vancomycin and penicillin resistance in clinical isolates of enterococci. Clin infect dis. 1992; 14(3): 655-661.
• Hayes JR, English LL, Carter PJ, Proescholdt T, Lee KY, Wagner DD, White DG. Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl Environ Microb. 2003; 69(12): 7153-7160.
• Hegstad K, Mikalsen T, Coque TM, Werner G, Sundsfjord A. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin Microbiol Infect. 2010; 16(6): 541-554.
• Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in enterococcus. Virulence 2012; 3(5): 421-433.
• Jackson CR, Lombard JE, Dargatz DA Fedorka-Cray PJ. Prevalence, species distribution and antimicrobial resistanceof enterococci isolated from US dairy cattle. Lett Appl Microbiol. 2011; 52(1): 41-48.
• Kasimoglu-Dogru A, Gencay YE, Ayaz ND. Prevalence and antibiotic resistance profiles of Enterococcus species in chicken at slaughter level; absence of vanA and vanB genes in E. faecalis and E. faecium. Res Vet Sci. 2010; 89(2): 153-158.
• Ke D, Picard FJ, Martineau F, Ménard C, Roy PH, Ouellette M, Bergeron MG. Development of a PCR assay for rapid detection of enterococci. J Clin Microbiol, 1999; 37(11): 3497-3503.
• Kilonzo-Nthenge A, Brown A, Nahashon SN, Long D. Occurrence and antimicrobial resistance of enterococci isolated from organic and conventional retail chicken. J Food Protect, 2015; 78(4): 760-766.
• Kim YB, Seo KW, Jeon HY, Lim SK, Sung HW, Lee YJ. Molecular characterization of erythromycin and tetracycline-resistant Enterococcus faecalis isolated from retail chicken meats. Poultry Sci. 2019; 98(2): 977-983.
• Kim YJ, Park JH, Seo KH. Comparison of the loads and antibiotic-resistance profiles of Enterococcus species from conventional and organic chicken carcasses in South Korea. Poultry Sci. 2018: 97(1): 271-278.
• Kirst HA, Thompson DG, Nicas TI. Historical yearly usage of vancomycin. Antimicrob Agents Ch. 1998; 42(5): 1303-1304.
• Korten V. Enterokoklar, In: Infeksiyon Hastalıkları ve Mikrobiyolojisi, Ed; Willke TA, Söyletir G, Doganay M, 2nd Ed., Nobel Tıp Kitabevleri, Istanbul. 2002; pp. 1497-1506.
• Lawlwy R, Curtis L and Davis J. The food safety hazard guidebook. The Royal Society of Chemistry, London, UK. 2012.
• Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A, Mazumdar V, Corander J, Cheng L, Saif S, Young S, Zeng Q, Wortman J, Birren B, Willems RJ, Earl AM, Gilmore MS. Emergence of epi-demic multidrug-resistant Enterococcus faecium fromanimal and commensal strains. MBio. 2013; 4(4): 1-10.
• Manson AL, Van Tyne D, Straub TJ, Clock S, Crupain M, Rangan U, Gilmore MS, Earl AM. Chicken meat-associated enterococci: influence of agricultural antibiotic use and connection to the clinic. Appl Environ Microb. 2019; 85(22): 1-10.
• Moellering RC. Enterococcus species, Streptococcus bovis and Leuconostoc species, In: Principles And Practice of Infectious Diseases, Ed; Mandell GL, Bennett JE, Dolin R, 5th Ed., Churchill Livingstone, New York. 2005; pp. 2411-2421.
• Molechan C, Amoako DG, Abia ALK, Somboro AM, Bester LA, Essack SY. Molecular epidemiology of antibiotic-resistant Enterococcus spp. from the farm-to-fork continuum in intensive poultry production in KwaZulu-Natal, South Africa. Sci Total Environ. 2019; 692: 868-878.
• Nieto-Arribas P, Seseña S, Poveda JM, Chicón R, Cabezas L, Palop L. Enterococcus populations in artisanal Manchego cheese: Biodiversity, technological and safety aspects. Food Microbiol. 2011; 28(5): 891-899.
• Onaran B, Göncüoğlu M, Bilir-Ormancı FS. Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Univ Vet Fak Derg. 2019; 66(4): 331-336.
• Pesavento G, Calonico C, Ducci B, Magnanini A, Nostro AL. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol. 2014; 41: 1-7.
• Robredo B, Singh KV, Baquero F, Murray BE, Torres C. Vancomycin-resistant enterococci isolated from animals and food. Int J Food Microbiol, 2010; 54(3): 197-204. Saha B, Singh AK, Ghosh A, Bal M. Identification and characterization of a vancomycin-resistant Staphylococcus aureus isolated from Kolkata (South Asia). J Med Microbiol. 2008; 57(1): 72-79.
• Sanlibaba P, Tezel BU, Senturk E. Antimicrobial resistance of Enterococcus species isolated from chicken in Turkey. Korean J Food Sci An. 2018; 38(2): 391-402.
• Semedo-Lemsaddek T, Tenreiro R, Alves PL, Crespo MTB. Enterococcus, In: Molecular Detection of Foodborne Pathogens, Ed; Liu D, CRC Press, London. 2010.
• Švec P, Devriese LA. Enterococcus, In: Bergey’s Manual Trust, John Wiley & Sons, Inc. 2015.
• Şentürk E. Molecular identi̇fi̇cati̇on of anti̇mi̇crobi̇al enterococcus spp. and determi̇nati̇on of anti̇bi̇oti̇c resi̇stance level. MSc Thesis, Ankara University Institute of Science, Ankara, 2017.
• Van Schaik W, Willems, RJ. Genome-based insights into the evolution of enterococci. Clin Microbiol Infect. 2010; 16(6): 527-532.
• Vidal-Carou MC, Latorre-Moratalla ML, Bover-Cid S. Biogenic Amines, In: Safety Analysis of Foods of Animal Origin, Ed; Nollet LM, Toldrá F, CRC Press, London. 2011; pp. 400-440.
• Yüksel M, Çetin B, Selahattin S (2013). Erzurum’da satışa sunulan tavuk ciğer ve etlerinin mikrobiyolojik kalitesi. Akademik Gıda, 11: 58-62.