Determination of Multiple Antibiotic Resistance Profiles of Enterococcus Species Isolated From Fermented Meat Products CConsumed in Ankara

Yıl 2021, Cilt: 25 Sayı: 6, 1295 - 1303, 31.12.2021

Meryem Burcu Külahcı , Sumru Çıtak , Zehra Şahin

https://doi.org/10.16984/saufenbilder.999958

Öz

The aim of this study was to determine the multiple antibiotic resistance profiles of Enterococcus spp. isolated from the fermented meat products consumed in Ankara, Turkey. A total of 134 Enterococcus spp. were isolated and identified from 80 fermented meat samples. The highest prevalence of enterococci in the fermented food samples was found in sucuk (a Turkish fermented sausage) samples (50%), followed by sausage (25.4%), pastirma (a Turkish dry-cured meat product) (18.6%), and salami, respectively. Of a total of 134 Enterococcus isolates, 110 (82.1%) were found to be resistant to one or more of the antibiotics tested. Although the highest resistance rate was seen against rifampicin (73.2%), streptomycin (36.5%) and erythromycin (20.2%), 28 (20.9%) of Enterococcus isolates were resistant to multiple antibiotics. The presence of multiple antibiotic resistant Enterococcus in foods of animal origin raises alarm because of the risk of carrying these bacteria to humans via the food chain.

Anahtar Kelimeler

Enterococcus, fermented meat products, multiple antibiotic resistance

Kaynakça

• [1] A.M. Hammerum, “Enterococci of animal origin and their significance for public health,” Clinical Microbiology and Infection, vol.18, no.7, pp. 619-625, 2012.
• [2] L.M. Cintas, P. Casaus, L.S. Håvarstein, P.E. Hernandez, and I. Nes, “Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum,” Appl Environ Microbiol., vol. 63, no. 11, pp. 4321-4330, 1997.
• [3] H.L. Leavis, M.J. Bonten, and R.J. Willems, “Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance,” Current opinion in microbiology, vol. 5, pp. 454-460, 2006.
• [4] S. Ali, I. A. Mirza, S. Yaqoob, A. Hussain, I. Khan, and M. Y. Rafiq, “Antimicrobial susceptibility pattern of enterococcus species isolated from patients with urinary tract infection,” Gomal Journal of Medical Sciences, vol. 12, no. 1, pp. 11-14, 2014.
• [5] M. Sparo, L. Urbizu, M.V. Solana, G. Pourcel, A. Delpech, Confalonieri and S.F. Sanchez Bruni, High‐level resistance to gentamicin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota. Letters in applied microbiology, vol. 54, no. 2, pp. 119-125, 2012.
• [6] C. Vignaroli, G. Zandri, L. Aquilanti, S. Pasquaroli, and F. Biavasco, “Multidrug-resistant enterococci in animal meat and faeces and co-transfer of resistance from an Enterococcus durans to a human Enterococcus faecium,” Current microbiology, vol. 62, no. 5, pp. 1438-1447, 2011.
• [7] J. M. T. Hamilton-Miller, and S. Shah, “Identification of clinically isolated vancomycin-resistant enterococci: comparison of API and BBL Crystal systems,” Journal of Medical Microbiology, vol. 48, no. 7, pp. 695-696, 1999.
• [8] Clinical and Laboratory Standards Institute (CLSI), P. A. Wayne, M07-A9 Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard – ninth editio. 2012.
• [9] P. H. Krumperman, “Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods,” Applied and Environmental Microbiology, vol. 46, no. 1, pp. 165-170, 1983.
• [10] T. Elal Mus, F. Cetinkaya, R. Cibik, G. E. Soyutemiz, H. Simsek, and N. Coplu, “Pathogenicity determinants and antibiotic resistance profiles of enterococci from foods of animal origin in Turkey,” Acta Veterinaria Hungarica, vol. 65, no. 4, pp. 461-474, 2017.
• [11] S. Özmen Toğay, A. Çelebi Keskin, L. Açık, and A. Temiz, “Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods,” Journal of applied microbiology, vol. 109, no. 3, pp. 1084-1092, 2010.
• [12] M. Gökmen, N. Ektik, R. Kara, E. Torlak, and M. Metli, “Detection of prevalence, antibiotic resistance and virulence factors of Enterococcus spp. isolated from ready to eat foods,” Kocatepe Veteriner Dergisi, vol.10, no. 2, pp. 76-82, 2017.
• [13] M. Jahan, D. O. Krause, and R. A. Holley, “Antimicrobial resistance of Enterococcus species from meat and fermented meat products isolated by a PCR-based rapid screening method,” International journal of food microbiology, vol. 163, no. 2-3, pp. 89-95, 2013.
• [14] J. Barbosa, P.A. Gibbs, and P. Teixeira, “Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal,” Food Control, vol. 21, no. 5, pp. 651-656, 2010.
• [15] F. M. Aerestrup, Y. AgersØ, P. Ahrens, J. C. Østergaard Jørgensen, M. Madsen, and L. B. Jensen, “Antimicrobial susceptibility and presence of resistance genes in staphylococi from poultry,” Veterinary Microbiology, vol. 74, pp. 353–364, 2000.
• [16] N. Klibi, L. B. Said, A. Jouini, K.B. Slama, M. López, R. B. Sallem, and C. Torres, “Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia,” Meat science, vol. 93, no.3, pp. 675-680, 2013.
• [17] S. A. P. Fracalanzza, E. M. D. Scheidegger, P. F. D. Santos, P. C. Leite, and L. M. Teixeira, “Antimicrobial resistance profiles of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil,” Memórias do Instituto Oswaldo Cruz, vol. 102, no. 7, pp. 853-859, 2007.
• [18] G. Giraffa, “Enterococci from foods,” FEMS microbiology reviews, vol. 26, no. 2, pp. 163-171, 2002.
• [19] M. Hugas, M. Garriga, and M. T. Aymerich, “Functionality of enterococci in meat products,” International journal of food microbiology, vol. 88, no. 2-3, pp. 223-233, 2003.
• [20] B. Martin, M. Garriga, M. Hugas, and T. Aymerich, “Genetic diversity and safety aspects of enterococci from slightly fermented sausages,” Journal of Applied Microbiology, vol. 98, no. 5, pp. 1177-1190, 2005.
• [21] J. Barbosa, V. Ferreira, and P. Teixeira, “Antibiotic susceptibility of enterococci isolated from traditional fermented meat products,” Food Microbiology, vol. 26, no. 5, pp. 527-532, 2009.
• [22] L. Mannu, A. Paba, E. Daga, R. Comunian, S. Zanetti, I. Duprè, and L. A. Sechi, “Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin,” International journal of food microbiology, vol. 88, no. 2-3, pp. 291-304, 2003.
• [23] J. Peters, K. Mac, H. Wichmann-Schauer, G. Klein, and L. Ellerbroek, “Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany.” International journal of food microbiology, vol. 88, no. 2-3, pp. 311-314, 2003.
• [24] B. E. Murray, “The life and times of the Enterococcus,” Clinical microbiology reviews, vol. 3, no. 1, pp. 46-65, 1990.
• [25] V. Kak, and J. W. Chow, “Acquired antibiotic resistances in enterococci. In: The enterococci: pathogenesis, molecular biology, and antibiotic resistance,” ASM Press, pp. 355-383, 2002.
• [26] L. L. McGowan-Spicer, P.J. Fedorka-Cray, J. G. Frye, R. J. Meinersmann, J. B. Barrett, and C. R. Jackson, “Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food,” Journal of food protection, vol. 71, no. 4, pp. 760-769, 2008.
• [27] A. S. Valenzuela, N. B. Omar, H. Abriouel, R. L. López, E. Ortega, M. M. Cañamero, and A. Gálvez, “Risk factors in enterococci isolated from foods in Morocco: determination of antimicrobial resistance and incidence of virulence traits,” Food and chemical toxicology, vol. 46, no. 8, pp. 2648-2652, 2008.
• [28] World Health Organization (WHO). Critically important antimicrobials for human medicine-3rd revision. WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance (AGISAR), 978924 1504485, WHO Press, Geneva, Switzerland, 2011.
• [29] L. B. Rice, “Emergence of vancomycin-resistant enterococci,” Emerging infectious diseases, vol. 7, no.2, pp. 183, 2001.
• [30] K. Borgen, G. S. Simonsen, A. Sundsfjord, Y. Wasteson, Ø. Olsvik, and H. Kruse, “Continuing high prevalence of VanA‐type vancomycin‐resistant enterococci on Norwegian poultry farms three years after avoparcin was banned.” Journal of Applied Microbiology, vol. 89, no. 3, pp. 478-485, 2000.
• [31] P. Messi, E. Guerrieri, S. De Niederhaeusern, C. Sabia, and M. Bondi, “Vancomycin-resistant enterococci (VRE) in meat and environmental samples.” International journal of food microbiology, vol. 107, no. 2, pp. 218-222, 2006.
• [32] A. K. Olawale, R. J. Salako, A. O. Olawale, and O. Famurewa, “Antibiotic-Resistant Enterococcus faecalis isolated from food canteens in Osun States, Nigeria,” Microbiology Research Journal International, vol. 6, no. 4, pp. 196-206, 2015.
• [33] Son R, Nimita F, Rusul G, Nasreldin E, Samuel L, Nishibuchi M. Isolation and molecular characterization of vancomycin‐resistant Enterococcus faecium in Malaysia. Letters in applied microbiology, vol. 29, no. 2, pp. 118-122, 1999.
• [34] S. Citak, N. Yucel, and S. Orhan, “Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. International Journal of Dairy Technology, vol. 57, no.1, pp. 27-31, 2004.
• [35] S. M. McBride, V. A. Fischetti, D. J. LeBlanc, R. C. Moellering Jr, and M. S. Gilmore, “Genetic diversity among Enterococcus faecalis,” PloS one, vol. 2, no. 7, e582, 2007.
• [36] E. M. Carvalho, R. A. Costa, A. J. Araujo, F. A. C. Carvalho, S. P Pereira, O. V. Sousa, and R. H. Vieira, “Multiple antibiotic-resistance of Enterococcus isolated from coastal water near an outfall in Brazil,” African Journal of Microbiology Research, vol. 8, no. 17, pp. 1825-1831, 2014.
• [37] A. Bouymajane, F. R. Filali, S. Oulghazi, A. Ed-dra, F. Benhallam, A. El Allaoui, J. Anissi, K. Sendide, B. Ouhmidou, and M. Moumni, “Occurrence, molecular and antimicrobial resistance of Enterococcus spp. isolated from raw cow’s milk trade by street trading in Meknes city, Morocco,” Germs, vol. 8, no. 2, pp. 77, 2018.
• [38] E. Charpentier, and P. Courvalin, “Antibiotic resistance in Listeria spp.,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 9, pp. 2103-2108, 1999.
• [39] P. Linden, and C. Miller, “Vancomycin-resistant enterococci: the clinical effect of a common nosocomial pathogen,” Diagnostic microbiology and infectious disease, vol. 33, no. 2, pp. 113-120, 1999.
• [40] M. Y. Yoon, Y. J. Kim, and H.J. Hwang, “Properties and safety aspects of Enterococcus faecium strains isolated from Chungkukjang, a fermented soy product,” LWT-Food Science and Technology, vol. 41, no. 5, pp. 925-933, 2008.