Antibiotic resistance traits and molecular subtyping of staphylococcus aureus isolated from raw sheep milk cheese

Journal of Food Science

Volumn 79, Issue 10, 2014, Pages M2066-M2071

  Spanu, Vincenzo ^a   Scarano, Christian ^a   Cossu, Francesca ^a   Pala, Carlo ^a   Spanu, Carlo ^a   De Santis, Enrico P L ^a  

^a UNIVERSITY OF SASSARI   (Italy)

Author keywords

Antibiotic resistance; Antibiotic resistance genes; Minimum inhibitory concentrations; Raw milk cheese; Staphylococcus aureus

Indexed keywords

ANTIINFECTIVE AGENT; VIRULENCE FACTOR;

ANIMAL; ANTIBIOTIC RESISTANCE; CHEESE; CLASSIFICATION; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MILK; PHENOTYPE; PULSED FIELD GEL ELECTROPHORESIS; SHEEP; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; CHEESE; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; MILK; PHENOTYPE; SHEEP; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84926236742     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/1750-3841.12590     Document Type: Article

References (37)

1. Alós JI, Aracil B, Oteo J, Torres C, Gómez Garcés JL. 2000. High prevalence of erythromycin-resistant, clindamycin/miocamycin-susceptible (M phenotype) Streptococcus pyogenes: result of Spanish multicentre study in 1998. J Antimic Ch 45:605-9.
2. Aminov RI, Garrigues-Jeanjean N, Mackie RI. 2001. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67(1):22-32. doi: 10.1128/AEM.67.1.22-32.2001.
3. Anderson KL, Lyman RL, Bodeis-Jones SM, White DG. 2006. Genetic diversity and antimicrobial susceptibility profiles among mastitis-causing Staphylococcus aureus isolated from bovine milk samples. Am J Vet Res 67(7):1185-91. doi: 10.2460/ajvr.67.7.1185.
4. Ashraf R, Shah NP. 2011. Antibiotic resistance of probiotic organisms and safety of probiotic dairy products. Intl Food Res J 18(3):837-53.
5. Can HY, Çelik TH, 2012. Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control 24(1):100-3. doi: 10.1016/j.foodcont.2011.09.009.
6. CLSI, 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-Ninth edition M07-A9, Vol. 32, No. 2. Wayne, PA: Clinical and Laboratory Standards Institute.
7. CLSI, 2013. Performance standards for antimicrobial susceptibility testing. CLSI approved standard Twenty-Third Informational Supplement M100-S23. Wayne, PA: Clinical and Laboratory Standards Institute.
8. Daka D, Solomon GS, Yihdego D. 2012. Antibiotic-resistance Staphylococcus aureus isolated from cow's milk in the Hawassa area, South Ethiopia. Ann Clin Microbiol Antimicrob 11:26. doi: 10.1186/1476-0711-11-26.
9. Depardieu F, Podglajen I, Leclercq R, Collatz E, Courvalin P. 2007. Modes and modulations of antibiotic resistance gene expression. Clin Microbiol Rev 20(1):79-114. doi: 10.1128/CMR.00015-06.
10. EFSA, 2013. European Food Safety Authority. 2013. The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2011. EFSA J 11(5):3196. doi: 10.2903/j.efsa.2013.3196.
11. Ertas N, Gonulalan Z, Yildirim Y, Kum E. 2010. Detection of Staphylococcus aureus enterotoxins in sheep cheese and dairy desserts by multiplex PCR technique. Intl J Food Microbiol 142:74-7. doi: 10.1016/j.ijfoodmicro.2010.06.002.
12. FSANZ, 2009. Food Standard Australia New Zealand. 2009. Microbiological Risk Assessment of Raw Milk Cheeses. Available from http://www.foodstandards.gov.au/code/proposals/documents/P1007%20PPPS%20for%20raw%20milk%201AR%20SD3%20Cheese%20Risk%20Assessment.pdf. Accessed 2014 July 10.
13. García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole KB, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Kirsty Girvan E, 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(8):595-603. doi:10.1016/S1473-3099(11)70126-8.
14. Goswitz JJ, Willard KE, Fasching CE, Peterson LR. 1992. Detection of gyrA gene mutations associated with ciprofloxacin resistance in methicillin-resistant Staphylococcus aureus: analysis by polymerase chain reaction and automated direct DNA sequencing. Antimicrob Agents Chemother 36(5):1166-69.
15. Gücükoğlu A, Çadirci Ö, Terzi G, Onur Kevenk T, Alişarli M. 2013. Determination of enterotoxigenic and Methicillin Resistant Staphylococcus aureus in ice cream. J Food Sci 78(5):M738-41. doi: 10.1111/1750-3841.12093.
16. Hu SK, Liu SY, Hu WF, Zheng TL, Xu JG, 2013. Molecular biological characteristics of Staphylococcus aureus isolated from food. Eur Food Res Technol 236(2):285-91. doi: 10.1007/s00217-012-1887-4.
17. 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(16):pii = 19542. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19542. Accessed 2014 Apr 15.
18. ISO, 2004a. Microbiology of food and animal feeding stuffs-horizontal method for the enumeration of Coagulase-Positive Staphylococci (Staphylococcus aureus and other species): Part 1: technique using Baird-Parker Agar Medium. ISO norm 6888-1:2004. International Organisation for Standardisation, Geneva, Switzerland.
19. ISO, 2004b. Microbiology of food and animal feeding stuffs-horizontal method for the enumeration of Coagulase-Positive Staphylococci (Staphylococcus aureus and other species): Part 2: technique using Rabbit-Plasma Fibrinogen Agar Medium. ISO norm 6888-2:2004. Geneva, Switzerland: International Organisation for Standardisation.
20. Jakobsen RA, Heggebø R, Sunde EB, Skjervheim M. 2011. Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiol 28:492-96. doi: 10.1016/j.fm.2010.10.017.
21. Jarraud S, Lyon GJ, Figueiredo AMS, Lina G, Vandenesch F, Etienne J, Muir TW, Novick RP. 2000. Exfoliatin-Producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 182(22):6517-22. doi: 10.1128/JB.182.22.6517-6522.2000.
22. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F. 2002. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70(2):631-41. doi: 10.1128/IAI.70.2.631-641.2002.
23. Lee JH. 2003. Methicillin (Oxacillin)-Resistant Staphylococcus aureus Strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol 69(11):6489-94. doi: 10.1128/AEM.69.11.6489-6494.2003.
24. Murchan S, Kaufmann ME, Deplano A, de Ryck R, Struelens M, Zinn CE, Fussing V, Salmenlinna S, Vuopio-Varkila J, El Solh N, Cuny C, Witte W, Tassios PT, Legakis N, van Leeuwen W, van Belkum A, Vindel A, Laconcha I, Garaizar J, Haeggman S, Olsson-Liljequist B, Ransjo U, Coombes G, Cookson B. 2003. Harmonization of Pulsed-Field Gel Electrophoresis protocols for epidemiological typing of strains of Methicillin-Resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol 41(4):1574-85. doi: 10.1128/JCM.41.4.1574-1585.2003.
25. Navratna V, Nadig S, Sood V, Prasad K, Arakere G, Gopal B. 2010. Molecular basis for the role of Staphylococcus aureus penicillin binding protein 4 in antimicrobial resistance. J Bacteriol 192(1):134-44. doi: 10.1128/JB.00822-09.
26. Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, Greco G, Bellacicco AL, Virgilio S, Celano GV. 2007. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Intl J Food Microbiol 117(2):219-22. doi: 10.1016/j.ijfoodmicro.2007.04.006.
27. Patel R, Uhl JR, Kohner P, Hopkins MK, Cockerill III FR. 1997. Multiplex PCR detection of vanA, vanB, vanC-1, and vanC-2/3 genes in Enterococci. J Clin Microbiol 35(3):703-7.
28. Rizek CF, Matté MH, Dropa M, Mamizuka EM, de Almeida LM, Lincopan N, Matté GR, Germano PM. 2011. Identification of Staphylococcus aureus carrying the mecA gene in ready-to-eat food products sold in Brazil. Foodborne Pathog Dis 8(4):561-63. doi: 10.1089/fpd.2010.0706.
29. Rosato E, Kreiswirth BN, Craig WA, Eisner W, Climo MW, Archer GL. 2003. mecA-blaZ corepressors in clinical Staphylococcus aureus isolates. Antimicrob Agents Ch 47(4): 1460-3. doi: 10.1128/AAC.47.4.1460-1463.2003.
30. Spanu V, Spanu C, Virdis S, Cossu F, Scarano C, De Santis EPL. 2012. Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese. Intl J Food Microbiol 153(1):53-7. doi: 10.1016/j.ijfoodmicro.2011.10.015.
31. Spanu V, Virdis S, Scarano C, Cossu F, De Santis EPL, Cosseddu AM, 2010. Antibiotic resistance assessment in S. aureus strains isolated from raw sheep's milk cheese. Vet Res Commun 34(1):S87-90. doi: 10.1007/s11259-010-9404-3.
32. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. 1995. Interpreting chromosomal DNA restriction patterns produced by Pulsed-Field Gel Electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33(9):2233-339.
33. Trzcinski K, Cooper BS, Hryniewicz W, Dowson CG. 2000. Expression of resistance to tetraciclines in strains of methicillin-resistance Staphylococcus aureus. J Antimic Ch 45:763-70.
34. Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P. 2010. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Vet Microbiol 144(1):166-71. doi: 10.1016/j.vetmic.2009.12.044.
35. Vautor E, Carsenti-Dellamonica H, Sabah M, Mancini G, Pépin M, Dellamonica P. 2007. Characterization of Staphylococcus aureus isolates recovered from dairy sheep farms (agr group, adherence, slime, resistance to antibiotics). Small Rumin Res 72:197-9. doi: 10.1016/j.smallrumres.2006.08.011.
36. Virdis S, Scarano C, Cossu F, Spanu V, Spanu C, De Santis EPL. 2010. Antibiotic resistance in Staphylococcus aureus and coagulase negative staphylococci isolated from goats with subclinical mastitis. Vet Med Intl 2010(2010):1-6. doi: 10.4061/2010/517060.
37. Xu J, Shi C, Song M, Xu X, Yang P, Paoli G, Shi X. 2014. Phenotypic and genotypic antimicrobial resistance traits of foodborne Staphylococcus aureus isolates from Shanghai. J Food Sci 79(4):M635-42. doi: 10.1111/1750-3841.12405.