Nesrin ÇAKICI, Nükhet Nilüfer DEMİREL ZORBA, Alper AKÇALI

Antibiotic resistance pattern and spa types of Staphylococcus aureus strains isolated from food business and hospital kitchen employees in Çanakkale, Turkey

Background/aim: The aim of this study was to determine antibiotic resistance profiles and spa types of Staphylococcus aureus strainsisolated from food business employees in Çanakkale, Turkey.Materials and methods: S. aureus isolates were collected from hand and nasal swabs of 300 individuals working in 17 food businessesand 9 hospital kitchens. All S. aureus isolates obtained from each carrier were typed by staphylococcal protein A (spa) typing method.Staphylococcal cassette chromosome mec (SCCmec) and multilocus sequence typing (MLST) of MRSA were performed by sequencingmethod.Results: Of the 300 individuals, 125 (41.6%) were found to be carriers of S. aureus, 215 isolates of which were obtained in total. Three(1.4%) of 215 isolates were identified as MRSA. Sixty spa types were identified among the 121 MSSA isolates, the most common beingt084 (9%). A novel spa type was discerned and added to the Ridom SpaServer database as t14963. The MLST type of the MRSA strainsidentified as spa type t786 was ST88 and as spa type t223 was ST22. All MRSA were determined to be SCCmec type IVa.Conclusion: spa typing can be performed to screen for transmission of S. aureus. t786, ST88, and SCCmec IVa MRSA strains wereidentified for the first time in Turkey

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1. Hiramatsu K, Katayama Y, Yuzawa H, Ito T. Molecular genetics of methicillin-resistant Staphylococcus aureus. Int J Med Microbiol 2002; 292: 67-74.
2. Yılmaz S, Kılıç A, Karagöz A, Bedir O, Üsküdar Güçlü A, Başustaoğlu AC. Investigation of various virulence factors among the hospital and community-acquired Staphylococcus aureus isolates by Real-Time PCR. Microbiol Bul 2012; 46: 532-545 (in Turkish with abstract in English).
3. Kırca Yılmaz S, Acuner IC, Strommenger B, Bek Y, Witte W. Infectivity-resistotype-genotype clustering of methicillinresistant Staphylococcus aureus strains in the central Blacksea Region of Turkey. Microbiol Bul 2014; 48: 14-27 (in Turkish with abstract in English).
4. O’Hara FP, Suaya JA, Ray GT, Baxter R, Brown ML, Mera RM, Close NM, Thomas E, Amrine-Madsen H. spa typing and multilocus sequence typing show comparable performance in a macroepidemiologic study of Staphylococcus aureus in the United States. Microb. Drug Resist 2016; 22: 88-96.
5. Al-Tam F, Brunel AS, Bouzinbi N, Corne P, Banuls AL, Shahbazkia HR. DNAGear—a free software for spa type identification in Staphylococcus aureus. BMC Research Notes 2012; 5: 642.
6. Harmsen D, Claus H, Witte W, Rothganger J, Claus H. Turnwald D. Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41: 5442- 5448.
7. Strommenger B, Braulke C, Heuck D, Schmidt C, Pasemann B, Nübel U, Witte W. spa typing of Staphylococcus aureus as a frontline tool in epidemiological typing. J Clin Microbiol 2008; 46: 574-581.
8. Sabat AJ, Budimir A, Nashev D, Sa-Leao R, van Dijl JM, Laurent F, Grundmann H, Friedrich AW. Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveillance 2013; 18: 20380.
9. Hallin M, Friedrich AW, Struelens MJ. spa typing for epidemiological surveillance of Staphylococcus aureus. Methods Mol Biol 2009; 551: 189-202.
10. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disc Susceptibility Testing; Twenty-Second Informational Supplement, M100-S22. Wayne, PA, USA: CLSI; 2012.
11. Choi SM, Kim SH, Kim HJ, Lee DG, Choi JH, Yoo JH, Kang JH, Shin WS, Kang MW. Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among staphylococcus species. J Korean Med Sci 2003; 18: 631-636.
12. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 1988; 26: 2465-2466.
13. Oliveira DC, Lencastre HD. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2002; 46: 2155-2161.
14. Zhang K, McClure J, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2005; 43: 5026-5033.
15. Bozdoğan B, Yıldız Ö, Oryaşın E, Kırdar S, Gülcü B, Aktepe O, Arslan U, Bayramoğlu G, Çoban AY, Coşkuner SA et al. t030 is the most common spa type among methicillin-resistant Staphylococcus aureus strains isolated from Turkish hospitals. Microbiol Bul 2013; 47: 571-581 (in Turkish with abstract in English).
16. Sepin Özen N, Tuğlu Ataman Ş, Seyman D, Aldağ H, Emek M. Investigation of nasal Staphylococcus aureus carriage and methicillin resistance rates with three different methods in food handlers working in Antalya. Turkish Bulletin of Hygiene and Experimental Biology 2013; 70: 51-58 (in Turkish with abstract in English).
17. Pala K, Özakın C, Akış N, Sınırtaş M, Gedikoğlu S. Asymptomatic carriage of bacteria in food workers in Nilüfer District. Turk J Med Sci 2010; 40: 133-139.
18. Erdoğan H, Arslan H. Nasal and pharyngeal carriage of Staphylococcus aureus among hotel staff and risk assessment. Klimik Dergisi 2011; 24: 90-93 (in Turkish with abstract in English).
19. Alp E, Klaassen C, Doğanay M, Klaassen CHW, Doğanay M, Altoparlak U, Aydın K, Engin A, Kuzucu C, Özakın C et al. MRSA genotypes in Turkey: persistence over 10 years of a single clone of ST239. J Infect 2009; 58: 433-438.
20. Ergon MC, Biçmen M, Gülay Z. Dokuz Eylül Üniversitesi Hastanesi’ndeki dominant metisiline dirençli Staphylococcus aureus suşunun moleküler yöntemlerle tiplendirilmesi. ANKEM 2010; 24: 65-70 (in Turkish).
21. Erdem Z, Türkyılmaz S. Molecular typing of methicillinresistant Staphylococcus aureus strains isolated from cows and farm workers. Journal of the Faculty of Veterinary Medicine of Kafkas University 2013; 19: 963-968 (in Turkish with abstract in English).
22. Dündar D, Willke A, Sayan M, Koç MM, Akan OA, Sümerkan B, Saltoğlu N, Yaman A, Ayaz C, Köksal İ. Epidemiological and molecular characteristics of methicillin-resistant Staphylococcus aureus in Turkey: a multicenter study. J Global Antimicrob Resist 2016; 6: 44-49.
23. Oksuz L, Dupieux C, Tristan A, Bes M, Etienne J, Gurler N. The high diversity of MRSA clones detected in a university hospital in Istanbul. Int J Med Sci 2013; 10: 1740-1745.
24. Aqel AA, Alzoubia HM, Vickers A, Pichon B, Kearns AM. Molecular epidemiology of nasal isolates of methicillinresistant Staphylococcus aureus from Jordan. Journal of Infection and Public Health 2015; 8: 90–97.
25. Al-Bakri AG, Al-Hadithi H, Kasabri V, Othman G, Kriegeskorte A, Becker K. The epidemiology and molecular characterization of methicillin-resistant staphylococci sampled from a healthy Jordanian population. Epidemiol Infect 2013; 141: 2384-2391.
26. Biber A, Abuelaish I, Rahav G, Raz M, Cohen L, Valinsky L, Taran D, Goral A, Elhamdany A, Regev-Yochay G. A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza Strip. PLoS One 2012; 7: e42864.
27. Abou Shadya HM, Bakr AEA, Hashad ME, Alzohairyd MA. Staphylococcus aureus nasal carriage among outpatients attending primary healthcare centers: a comparative study of two cities in Saudi Arabia and Egypt. Branz J Infect Dis 2015; 19: 68-76.
28. Gostev V, Kruglov A, Kalinogorskaya O, Dmitrenko O, Khokhlova O, Yamamoto T, Lobzin Y, Ryabchenko I, Sidorenko S. Molecular epidemiology and antibiotic resistance of methicillin-resistant Staphylococcus aureus circulating in the Russian Federation. Infect Genet Evol 2017; 53: 189-194.
29. Geraci DM, Bonura C, Giuffre M, Aleo A, Saporito L, Graziano G, Valenti RM, Mammina C. tst1-positive ST22 MRSA-IVa in healthy Italian preschool children. Infection 2014: 42; 535–538.
30. Larsson AK, Gustafsson E, Johansson PJH, Odenholt I, Petersson AC, Melander E. Epidemiology of MRSA in southern Sweden: strong relation to foreign country of origin, healthcare abroad and foreign travel. Eur J Clin Microbiol Infect Dis 2014; 33: 61-68.
31. Conceiçao T, Coelho C, Lencastre H, Aires-de-Sousa M. Frequent occurrence of oxacillin-susceptible mecApositive Staphylococcus aureus (OS-MRSA) strains in two African countries. J Antimicrob Chemother 2015; 70: 3200- 3204.
32. Kock R, Brakensiek L, Mellmann A, Kipp F, Henderikx M, Harmsen D, Daniels-Heardt I, Von Eliff C, Becter K, Hendrix MG et al.. Cross-border comparison of the admission prevalence and clonal structure of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2009; 71: 320-326.
33. Mithoe D, Rijnders MIA, Roede BM, Stobberingh E, Möller AVM. Prevalence of community-associated methicillinresistant Staphylococcus aureus and Panton-Valentine leucocidin-positive S. aureus in general practice patients with skin and soft tissue infections in the northern and southern regions of the Netherlands. Eur J Clin Microbiol Infect Dis 2012; 31: 349-356.
34. Senn L, Basset P, Greub G, Prod’hom G, Frei R, Zbinden R, Gaia V, Balmelli C, Pfyffer GE, Muhlemann K et al.. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Switzerland: sampling only invasive isolates does not allow a representative description of the local diversity of clones. Clin Microbiol Infect 2013; 19: 288-290.
35. Ho J, O’Donoghue MM, Boost MV. Occupational exposure to raw meat: a newly-recognized risk factor for Staphylococcus aureus nasal colonization amongst food handlers. International Journal Hygiene Environmental Health 2014; 217: 347-353.
36. Skramm I, Moen AE, Bukholm G. Nasal carriage of Staphylococcus aureus: frequency and molecular diversity in a randomly sampled Norwegian community population. APMIS 2011; 119: 522-528.
37. Jimenez JN, Velez LA, Mediavilla JR, Ocampo AM, Vanegas JM. Livestock-associated methicillin-susceptible Staphylococcus aureus ST398 infection in woman, Colombia. Emerg Infect Dis 2011; 17: 1970-1971.