The Prevalence and Antibiotic Resistance of Methicillin-Resistant Staphylococcus aureus (MRSA) in Milk and Dairy Products in Balikesir, Turkey

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DOI: https://doi.org/10.12681/jhvms.16062
NISANUR EKTIK
Department of Food Hygiene and Technology, Institute of Health Science, Balikesir University
MUKADDERAT GÖKMEN
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Balikesir University
RECEP ÇIBIK
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Uludağ University
Resumen
Methicillin-Resistant Staphylococcus aureus is an important pathogen that causes severe infections in humans and animals. The aim of this study was to determine the prevalence and the antimicrobial profile of methicillin-resistant S. aureus (MRSA) in cow bulk tank milk and dairy products in the region of Balikesir in Turkey. Of 175 milk and dairy products’ samples, 26 were found to be positive for coagulase-positive staphylococci and 3 (2 samples from cow bulk tank milk and 1 sample from tulum cheese) were MRSA phenotypically being resistant against both oxacillin and cefoxitin. Among these, 17 were confirmed as S. aureus by the detection of nuc gene and one as MRSA carrying the mecA gene. All MRSA isolates were found to be also resistant against ampicillin, penicillin and sulfamethoxazole-trimethoprim. Consequently, even though the prevalence of MRSA in cow bulk tank milk and dairy productswas relatively low (1.70%), it may pose serious risks in terms of food safety and public health. In order to prevent the prevalence of MRSA in dairy products, hygienic measures, especially in terms of personal hygiene and disinfection of equipment in all stages of dairy production, should be taken, and HACCP and GMP regulations should be implemented.
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Ağalar C, Göçmen JS, Kılıç D, Kaygusuz S, Karabıçak Ç (2012) Üçüncü basamak bir referans hastanesinde izole edilen metisilin dirençli stafilokok suşlarında duyarlılık. J Clin Exp Invest 3:71-74.
Antoci E, Pinzone MR, Nunnari G, Stefani S, Cacopardo B (2013) Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among subjects working on bovine dairy farms. Infez. Med. 21:125-129.
Arefi F, Mohsenzadeh M, Razmyar J (2014) Isolation, antimicrobial susceptibility and mecA gene analysis of methicillin-resistant Staphylococcus aureus in Iranian white cheeses. Iran J Vet Res 15:127-131.
Can HY, Çelik TH (2012) Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control 24:100-103.
CLSI (Clinical and Laboratory Standards Instıtute) (2012)M100-S22, 32(3). ISBN 1-56238-785-5. ISSN 1558-6502.
CLSI (Clinical and Laboratory Standards Instıtute) (2014) M100–S24, 34(1). ISBN 1-56238-897-5. ISSN 1558-6502.
Cortimiglia C, Luini M, Bianchini V, Marzagalli L, Vezzoli F, Avisani D, Bertoletti M, Ianzano A, Franco A, Battisti A (2016) Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus clonal complexes in bulk tank milk from dairy cattle herds in Lombardy Region (Northern Italy). Epidemiol Infect 144(14):3046-3051.
Cuny C, Köck R, Witte W (2013) Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany, Int J Med Microbiol., 303(6-7): 331-337.
Çakır Ö (2011) Erzincan Tulum Peynirinin Bazı Fiziksel, Kimyasal ve Mikrobiyolojik Özelliklerinin Tespiti ile Bu Örneklerde Koagülaz (+) S. aureus ve E. coli O157:H7’nin Aranması. Yüksek Lisans tezi, Atatürk Üniversitesi, Erzurum.
Daka D, G/silassie S, Yihdego D (2012) Antibiotic-resistance Staphylococcus aureus isolated from cow’s milk in the Hawassa area, South Ethiopia. Ann Clin Microbiol Antimicrob 11:26.
Dutfield G (2009) Intellectual Property Rights and the Life Science Industries: Past, Present, and Future. 2nd edition, World Scientific Publishing Co, London, England.
Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci 99:7687-7692.
Erdem Z, Türkyılmaz S (2013) Molecular typing of methicillin resistant Staphylococcus aureus strains isolated from cows and farm workers. Kafkas Univ Vet Fak Derg 19:963-968.
European Food Safety Authority (EFSA) (2008) European Food Safety Authority Panel on Biological Hazards. Foodborne antimicrobial resistance as a biological hazard. Scientific Opinion. EFSA J 765:1-87.
EFSA (European Food Safety Authority) (2009) Assessment of the Public Health significance of methicillin-resistant Staphylococcus aureus (MRSA) in animals and foods. Scientific Opinion of the Panel on Biological Hazards (Question No EFSA-Q-2008-300). EFSA J 993:1-73.
Feßler AT, Kadlec K, Hassel M, Hauschild T, Eidam C, Ehricht R, Monecke S, Schwarz S (2011) Characterization of methicillinresistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ Microbiol 77:7151-7157.
Garcia-Alvarez L, Holden MTG, Lindsay H, RWebb C, Brown DFC, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RLR, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA (2011) Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11:595-603.
Grave K, Torren-Edo J, Mackay D (2010) Comparison of the sales of veterinary antibacterial agents between 10 European countries. J Antimicrob Chemother 65:2037-2040.
Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E (2006) Emergence and resurgence of methicillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368:874–885.
Hardy KJ, Hawkey PM, Gao F, Oppenheim BA (2004) Methicillin resistant Staphylococcus aureus in the critically ill. Br J Anaesthesia 92:121-130.
Hoegh SV, Skov MN, Boye K, Worning P, Jensen TG, Kemp M (2014) Variations in the Staphylococcus aureus-specific nuc gene can potentially lead to misidentification of meticillin-susceptible and -resistant S. aureus. J Med Microbiol 63:1020-1022.
Huber H, Koller S, Giezendanner N, Stephan R, Zweifel C (2010) Prevalence and characteristics of meticillin-resistant Staphylococcus aureus in humans in contact with farm animals, in livestock and in food of animal origin, Switzerland, 2009. Euro Surveill 15:19542.
Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Opda 6:41-52.
Jevons MP (1961) Celbenin-resistant staphylococci. Brit Med J 1:124-125.
Jones TF, Kellum ME, Porter SS, Bell M, Schaffner W (2002) An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 8:82-84.
Kalsoom F, Syed NHS, Farzana J (2004) Antibiotic resistance pattern against various isolates of Staphylococcus aureus from raw milk samples. J Res Sci 15:145-151.
Kanaan MHG and Al-Shammary AHA (2013) Detection of methicillin or multidrug resistant Staphylococcus aureus (MRSA) in locally produced raw milk and soft cheese in Baghdad markets. Iraqi J Vet Sci 37:226-231.
Karpiškova R, Šťastkova Z, Karpiškova S (2009) Nalezy methicilin rezistentnich Staphylococcus aureus u zviřat. Veterinařstvi 59:34-36.
Kaynarca S, Türkyılmaz S (2010) Sığır mastitislerinden izole edilen stafilokoklarda metisilin direnci ve slaym pozitifliği. Kafkas Univ Vet Fak Derg 16:567-572.
Kluytmans JA (2010) Methicillin-resistant Staphylococcus aureus in food products: Cause for concern or case for complacency? Clin Microbiol Infect 16:11-15.
Knox R (1961) Correspondence. Brit Med Jour 1:126.
Köck R, Schaumburg F, Mellmann A, Köksal M, Jurke A, et al. (2013) Livestock-Associated Methicillin-Resistant Staphylococcus aureus (MRSA) as Causes of Human Infection and Colonization in Germany. PLoS ONE 8(2): e55040. doi:10.1371/journal.pone.0055040
Lee JH (2003) Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol 69:6489-6494.
Maes N, Magdalena J, Rottiers S, De Gheldre Y, Struelens MJ (2002) Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from coagulase-negative staphylococci and determine methicillin-resistance from blood cultures. J Clin Microbiol 40:1514-1517.
Mattner F, Biertz F, Ziesing S, Gastmeier P, Chaberny IF (2010) Long-term persistence of MRSA in re-admitted patients. Infection 38:363-371.
Mirzaei H, Tofighi A, Sarabi HK, Farajli M (2011) Prevalence of methicillin-resistant Stapylococcus aureus in raw milk and dairy products in Sarab by culture and PCR techniques. J Anim Vet Adv 10:3107-3111.
Özpınar N (2011) Erzincan Tulum Peynirinden İzole Edilen Staphylococcus aureus İzolatlarında Antibiyotik Direncinin ve Biyofilm Oluşturma Özelliğinin Fenotipik ve Genotipik Olarak Belirlenmesi. Yüksek Lisans tezi, Erciyes Üniversitesi, Kayseri.
Paterson GK, Larsen J, Harrison EM, Larsen AR, Morgan FJ, Peacock SJ, Parkhill J, Zadoks RN, Holmes MA (2012) First detection of livestock-associated meticillin-resistant Staphylococcus aureus CC398 in bulk tank milk in the United Kingdom. Euro Surveill 17:20337.
Pehlivanoğlu F and Yardımcı H (2012) Detection of Methicillin and Vancomycin resistance in Staphylococcus strains isolated from bovine milk samples with mastitis. Kafkas Univ Vet Fak Derg 18:849-855.
Petersen A, Stegger M, Heltberg O, Christensen J, Zeuthen A, Knudsen LK, Urth T, Sorum M, Schouls L, Larsen J, Skov R, Larsen AR (2013) Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin Microbiol Infect 19:16-22.
Riva A, Borghi E, Cirasola D, Colmegna S, Borgo F, Amato E, Pontello MM, Morace G (2015) Methicillin-Resistant Staphylococcus aureus in Raw Milk: Prevalence, SCCmec
Typing, Enterotoxin Characterization, and Antimicrobial Resistance Patterns. J Food Prot 78(6):1142-6.
Rolinson GN, Batchelor FR, Stevens S, Wood JC, Chain EB (1960) Bacteriological studies on a new penicillin-BRL 1241. Lancet 276:561-567.
Spellberg B, Guidos R, Gilbert D, Bradley J, Boucher HW, Scheld WM, Bartlett JG, Edwards JrJ, Infectious Disease Society of America (2008) The epidemic of antibiotic-resistant infections: A call to action for the medical community from the Infectious Diseases Society of America. Clin Infect Dis 46:155-64.
Spohr M, Rau J, Friedrich A, Klittich G, Fetsch A, Guerra B, Hammerl JA, Tenhagen BA (2011) Methicillin-resistant Staphylococcus aureus (MRSA) in three dairy herds in Southwest Germany. Zoonoses Public Hlth 58:252-261.
Sudağıdan M, Çavuşoğlu C, Bacakoğlu F (2008) Biyomalzeme yüzeylerinden izole edilen metisiline dirençli Staphylococcus aureus suşlarında virulans genlerinin araştırılması. Mikrobiyol Bült 42:29-39.
Tekinşen OC (2000) Süt Ürünleri Teknolojisi. Üçüncü baskı, Selçuk Üniversitesi, Konya, Turkey. Turkish Food Codex Cheese Communique. Communique No 2015/6.
Resmi Gazete, Sayı: 29261. Accessed 10 July 2015.
Türkyılmaz S, Tekbıyık S, Oryasin E, Bozdoğan B (2010) Molecular epidemiology and antimicrobial resistance mechanisms of methicillin resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Pub Hlth 57:197-203.
Ünal N (2013) Subklinik mastitisli inek sütlerinden izole edilen Staphylococcus aureus izolatlarında bazı toksin genleri ve metisilin direnç geninin araştırılması. Ankara Üniv Vet Fak Derg 60:21-26.
Vanderhaeghen W, Hermans K, Haesebrouck F, Butaye P (2010) Methicillin-resistant Staphylococcus aureus (MRSA) in food production animals. Epidemiol Infect 138:606-625.
Vyletelova M, Hanus O, Karpiskova R, Stastkova Z (2011) Occurance and antimicrobial sensitivity in staphylococci isolated from goat, sheep and cow’s milk. Acta Univ Agric Silvic Mendelianae Brun 59:209-214.
Witte W, Cuny C, Klare I, Nübel U, Strommenger B, Werner G (2008) Emergence and spread of antibiotic-resistant grampositive bacterial pathogens. Int J Med Microbiol 298:365-377.
Yasuda R, Kawano J, Onda H, Takagi M, Shimizu A, Anzai T (2000) Methicillin-resistant coagulase-negative staphylococci isolated from healthy horses in Japan. Am J Vet Res 61:1451-1455.
Yücel N and Anıl Y (2011) Çiğ süt ve peynir örneklerinden Staphylococcus aureus ve koagülaz negatif stafilokokların identifikasyonu ve antibiyotik duyarlılığı. Türk Hij Den Biyol