Research Article
Tüketime Hazır Bazı Gıdalarda Enterococcus spp. Prevalansı, Antibiyotik Dirençlilik ve Virülens Faktörlerinin Tespiti
Abstract
Bu çalışmada tüketime hazır bazı gıdalarda Enterokok türlerinin prevalansı, antibiyotik dirençliliği ve virülans faktörleri belirlendi. Analize alınan 187 gıda örneğinin 112 (%59,9)’sinde 114 Enterococcus spp. izole edildi. Et ürünlerinden 39 (%34,8), peynirlerden 42 (%37,5), salatalardan 25’i (%22,3) ve helva örneklerinden 8 (%7,1)’inde Enterococcus spp. izolatı elde edildi. Antibiyotik dirençlilik testi sonuçlarına göre, elde edilen Enterokok izolatlarının çalışmada kullanılan antibiyotiklerden en az dördüne dirençlilik gösterdiği tespit edildi. İzolatların hiçbirinde gelatinaz aktivitesi gözlenmezken, 36’sında (%31,6) hemolizin aktivitesi pozitif tespit edildi. Sonuç olarak starter kültür olarak kullanılabileceği ve insanlar için zararsız olduğu düşünülen bazı Enterokok türlerinin, virülens faktörler ve sahip olabilecekleri antimikrobiyal direnç bakımından halk sağlığı ve gıda güvenliği açısından bir risk oluşturabilmektedir. Bu nedenle gıda endüstrisinde starter olarak kullanılabilecek Enterokok türleri, patojenite özelliği bulunmayan ve antibiyotik direnç genlerine sahip olmayanlardan seçilmelidir.
References
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- 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.
- Ben-Omar N, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP. Functional and safety aspects of Enterococci isolated from different Spanish foods. Syst Appl Microbiol. 2004; 27: 118–130.
- Biendo M, Adjid´e C, Castelain S, Belmekki M, Rousseau F, Slama M, Ganry O, Schmit JL, Eb F. Molecular characterization of glycopeptide-resistant enterococci from hospitals of the Picardy Region (France). Int J Microbiol. 2010; doi:10.1155/2010/150464.
- Camargo CH, Bruder-Nascimento A, Lee, SH, Fernandes Júnior A, Kaneko R, Rall VL. Prevalence and phenotypic characterization of Enterococcus spp. isolated from food in Brazil. Braz J Microbiol. 2014; 45: 111-115.
- Chajęcka-Wierzchowska W, Zadernowska A, Nalepa B, Laniewska-Trokenheim L. Occurrence and antibiotic resistance of enterococci in ready-to-eat food of animal origin. Afr J Microbiol Res. 2012; 6: 6773- 6780.
- Charpentier E and Courvalin P. Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother. 1999; 43: 2103–2108.
- CLSI. Clinical Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement M100-S24, CLSI, Wayne, PA, USA, 2014.
- Comerlato CB, Resende MCC, De Caıerao J, D'azevedo PA. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Mem Inst Oswaldo Cruz. 2013; 108: 590-595.
- Dahlen G, Blomqvist S, Almstahl A, Carlen A. Virulence factors and antibiotic susceptibility in enterococci isolated from oral mucosal and deep infections. J Oral Microbiol. 2012; 4: 10855- DOI:10.3402/jom.v4i0.10855.
- De Fa´tima Silva Lopes M, Ribeiro T, Abrantes M, Figueiredo Marques JJ, Tenreiro R, Crespo MTB. Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int J Food Microbiol. 2005; 103: 191–198.
- EUCAST. European Committee on An icrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. Version 5.0, valid from (2015-01-01).
- Foulquié Moreno M, Sarantinopoulos P, Tsakalidou E, De Vuyst L. The role and application of enterococci in food and health. Int J Food Microbiol. 2006; 106: 1-24.
- Fracalanzza S, Scheidegger E, Santos P, Leite P, Teixeira L. Antimicrobial resistance profiles of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2007; 102: 853-859.
- Franz CM, Holzapfel WH, Stiles ME. Enterococci at the crossroads of food safety. Int J Food Microbiol. 1999; 47: 1–24.
- Gardin F, Martuscelli M, Caruso MC, Galgano F, Crudele MA, Favati F. Effects of pH, temperature and NaCl concentration on the growth kinetics, proteolytic activity and biogenic amine production of Enterococcus faecalis. Int J Food Microbiol. 2001; 64: 105– 117.
- Gelsomino R, Vancanneyt M, Condon S, Swings S, Cogan TM. Enterococcal diversity in the environment of an Irish cheddar-type cheesemaking factory. Int J Food Microbiol. 2001; 71: 177–188.
- Giraffa G. Enterococci from foods. FEMS Microbiol Rev. 2002; 26: 163-171.
- Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi LA, Franco BDGM, De Martinis ECP. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol. 2008; 25: 668–675.
- Hegstad K, Giske CG, Haldorsen B, Matuschek E, Schønning K, Leegaard TM, Kahlmeter G, Sundsfjord A, Nordicast VRE. Detection Study Group. Performance of the EUCAST disk diffusion method, the CLSI agar screen method, and the Vitek 2 automated antimicrobial susceptibility testing system for detection of clinical isolates of Enterococci with low- and medium-level VanB-type vancomycin resistance: a multicenter study. J Clin Microbiol. 2014; 52: 1582–1589.
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- Jamet E, Akary E, Poisson MA, Chamba JF, Bertrand X, Serror P. Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 2012; 31: 191-198.
- Kayser FH. Safety aspects of enterococci from the medical point of view. Int J Food Microbiol. 2003; 88: 255–262.
- Klibi N, Said LB, Jouini A, Slama KB, López M, Sallem RB, Boudabous A, Torres C. Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia. Meat Sci. 2013; 93: 675–680.
- Lopez-Diaz TM, Santos JA, Gonzales CJ, Moreno B, Garcia ML. Bacteriological quality of a traditional Spanish blue cheese. Milchwiss. 1995; 50: 503–504.
- Maietti L, Bonvini B, Huys G, Giraffa G. Incidence of antibiotic resistance and virulence determinants among Enterococcus italicus isolated from dairy products. Syst Appl Microbiol. 2007; 30: 509-517.
- Marra A, Dib-Hajj F, Lamb L, Kaczmarek F, Shang W, Beckius G, Millici A.J, Medina I, Gootz TD. Enterococcal virulence determinants may be involved in resistance to clinical therapy. Diagn Microbiol Infect Dis. 2007; 58: 59-65.
- Michel M and Gutmann L. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: therapeutic realities and possibilities. Lancet. 1997; 349: 1901–1906. 2000; 13: 513– 522.
- Pesavento G, Calonico C, Ducci B, Magnanini A, Lo Nostro A. 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.
- Ristori CA, Rowlands REG, Bergamini AMM, Lopes GISL, Paula AMR, Oliveira MA. Prevalence and antimicrobial susceptibility profile of Enterococcus spp. isolated from frozen chicken carcasses. Rev Inst Adolfo Lutz São Paulo.2012; 71: 237–243.
- Sadowsky MJ and Whitman RL (Eds.). The fecal bacteria. Washington DC: ASM Press. 2011.
- Trivedi K, Cupakova S, Karpiskova R. Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Veterinarni Medicina. 2011; 56: 352–357.
- Vergis EN, Shankar N, Chow JW, Hayden MK, Snydman DR, Zervos MJ. Association between the presence of enterococcal virulence factors gelatinase, hemolysin, and enterococcal surface protein and mortality among patients with bacteremia due to Enterococcus faecalis. Clin Infect Dis. 2002; 35: 570–575.
Detection of Prevalence, Antibiotic Resistance and Virulence Factors of Enterococcus spp. Isolated From Ready to Eat Foods
Abstract
In this study, we identified the prevalence of Enterococcus spp., antibiotic resistance and several virulence factors of some ready-to-eat foods. Totally 114 Enterococcus spp. were isolated in 112 (59.90 %) of the 187 food samples analysed. Enterococcus spp. isolates were obtained from 39 samples of meat products (34.80 %), 42 samples of cheese brands (37.50 %), 25 samples of salads (22.30 %) and eight samples of halva (7.10 %). According to the results of the antibiotic resistance test, the Enterococci isolates obtained were determined to show resistance to at least 4 of the antibiotics used in the study. While no gelatinase activity was observed in any of the isolates, haemolysin activity was observed to be positive in 36 of them (31.60 %). As a result, having been regarded for years as harmless and reported likely to be used as a starter culture, some Enterococcus spp. pose a risk to public health and to food safety since they have virulence factors and strong antimicrobial resistance. For this reason, the Enterococcus spp. to be used as a starter in the food industry should be chosen from among those that don’t have pathogenicity and antibiotic resistance genes.
References
- Aslam M, Diarra M.S, 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: 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.
- Ben-Omar N, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP. Functional and safety aspects of Enterococci isolated from different Spanish foods. Syst Appl Microbiol. 2004; 27: 118–130.
- Biendo M, Adjid´e C, Castelain S, Belmekki M, Rousseau F, Slama M, Ganry O, Schmit JL, Eb F. Molecular characterization of glycopeptide-resistant enterococci from hospitals of the Picardy Region (France). Int J Microbiol. 2010; doi:10.1155/2010/150464.
- Camargo CH, Bruder-Nascimento A, Lee, SH, Fernandes Júnior A, Kaneko R, Rall VL. Prevalence and phenotypic characterization of Enterococcus spp. isolated from food in Brazil. Braz J Microbiol. 2014; 45: 111-115.
- Chajęcka-Wierzchowska W, Zadernowska A, Nalepa B, Laniewska-Trokenheim L. Occurrence and antibiotic resistance of enterococci in ready-to-eat food of animal origin. Afr J Microbiol Res. 2012; 6: 6773- 6780.
- Charpentier E and Courvalin P. Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother. 1999; 43: 2103–2108.
- CLSI. Clinical Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement M100-S24, CLSI, Wayne, PA, USA, 2014.
- Comerlato CB, Resende MCC, De Caıerao J, D'azevedo PA. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Mem Inst Oswaldo Cruz. 2013; 108: 590-595.
- Dahlen G, Blomqvist S, Almstahl A, Carlen A. Virulence factors and antibiotic susceptibility in enterococci isolated from oral mucosal and deep infections. J Oral Microbiol. 2012; 4: 10855- DOI:10.3402/jom.v4i0.10855.
- De Fa´tima Silva Lopes M, Ribeiro T, Abrantes M, Figueiredo Marques JJ, Tenreiro R, Crespo MTB. Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int J Food Microbiol. 2005; 103: 191–198.
- EUCAST. European Committee on An icrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. Version 5.0, valid from (2015-01-01).
- Foulquié Moreno M, Sarantinopoulos P, Tsakalidou E, De Vuyst L. The role and application of enterococci in food and health. Int J Food Microbiol. 2006; 106: 1-24.
- Fracalanzza S, Scheidegger E, Santos P, Leite P, Teixeira L. Antimicrobial resistance profiles of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2007; 102: 853-859.
- Franz CM, Holzapfel WH, Stiles ME. Enterococci at the crossroads of food safety. Int J Food Microbiol. 1999; 47: 1–24.
- Gardin F, Martuscelli M, Caruso MC, Galgano F, Crudele MA, Favati F. Effects of pH, temperature and NaCl concentration on the growth kinetics, proteolytic activity and biogenic amine production of Enterococcus faecalis. Int J Food Microbiol. 2001; 64: 105– 117.
- Gelsomino R, Vancanneyt M, Condon S, Swings S, Cogan TM. Enterococcal diversity in the environment of an Irish cheddar-type cheesemaking factory. Int J Food Microbiol. 2001; 71: 177–188.
- Giraffa G. Enterococci from foods. FEMS Microbiol Rev. 2002; 26: 163-171.
- Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi LA, Franco BDGM, De Martinis ECP. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol. 2008; 25: 668–675.
- Hegstad K, Giske CG, Haldorsen B, Matuschek E, Schønning K, Leegaard TM, Kahlmeter G, Sundsfjord A, Nordicast VRE. Detection Study Group. Performance of the EUCAST disk diffusion method, the CLSI agar screen method, and the Vitek 2 automated antimicrobial susceptibility testing system for detection of clinical isolates of Enterococci with low- and medium-level VanB-type vancomycin resistance: a multicenter study. J Clin Microbiol. 2014; 52: 1582–1589.
- Hugas M, Garriga M, Aymerich MT. Functionalty of enterococci in meat products. Int J Food Microbiol. 2003; 88: 223-233.
- Jamet E, Akary E, Poisson MA, Chamba JF, Bertrand X, Serror P. Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 2012; 31: 191-198.
- Kayser FH. Safety aspects of enterococci from the medical point of view. Int J Food Microbiol. 2003; 88: 255–262.
- Klibi N, Said LB, Jouini A, Slama KB, López M, Sallem RB, Boudabous A, Torres C. Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia. Meat Sci. 2013; 93: 675–680.
- Lopez-Diaz TM, Santos JA, Gonzales CJ, Moreno B, Garcia ML. Bacteriological quality of a traditional Spanish blue cheese. Milchwiss. 1995; 50: 503–504.
- Maietti L, Bonvini B, Huys G, Giraffa G. Incidence of antibiotic resistance and virulence determinants among Enterococcus italicus isolated from dairy products. Syst Appl Microbiol. 2007; 30: 509-517.
- Marra A, Dib-Hajj F, Lamb L, Kaczmarek F, Shang W, Beckius G, Millici A.J, Medina I, Gootz TD. Enterococcal virulence determinants may be involved in resistance to clinical therapy. Diagn Microbiol Infect Dis. 2007; 58: 59-65.
- Michel M and Gutmann L. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: therapeutic realities and possibilities. Lancet. 1997; 349: 1901–1906. 2000; 13: 513– 522.
- Pesavento G, Calonico C, Ducci B, Magnanini A, Lo Nostro A. 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.
- Ristori CA, Rowlands REG, Bergamini AMM, Lopes GISL, Paula AMR, Oliveira MA. Prevalence and antimicrobial susceptibility profile of Enterococcus spp. isolated from frozen chicken carcasses. Rev Inst Adolfo Lutz São Paulo.2012; 71: 237–243.
- Sadowsky MJ and Whitman RL (Eds.). The fecal bacteria. Washington DC: ASM Press. 2011.
- Trivedi K, Cupakova S, Karpiskova R. Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Veterinarni Medicina. 2011; 56: 352–357.
- Vergis EN, Shankar N, Chow JW, Hayden MK, Snydman DR, Zervos MJ. Association between the presence of enterococcal virulence factors gelatinase, hemolysin, and enterococcal surface protein and mortality among patients with bacteremia due to Enterococcus faecalis. Clin Infect Dis. 2002; 35: 570–575.
There are 33 citations in total.
Details
| Journal Section | RESEARCH ARTICLE |
|---|---|
| Authors | |
| Publication Date | March 1, 2017 |
| Acceptance Date | May 3, 2017 |
| Published in Issue | Year 2017 Volume: 10 Issue: 2 |
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