{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T02:46:22Z","timestamp":1792291582318,"version":"4.4.0"},"reference-count":89,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2017,9,1]],"date-time":"2017-09-01T00:00:00Z","timestamp":1504224000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Background: Resistance of Staphylococcus aureus to commonly used antibiotics is linked to their ability to acquire and disseminate antimicrobial-resistant determinants in nature, and the marine environment may serve as a reservoir for antibiotic-resistant bacteria. This study determined the antibiotic sensitivity profile of S. aureus isolated from selected beach water and intertidal beach sand in the Eastern Cape Province of South Africa. Methods: Two hundred and forty-nine beach sand and water samples were obtained from 10 beaches from April 2015 to April 2016. Staphylococcus aureus was isolated from the samples using standard microbiological methods and subjected to susceptibility testing to 15 antibiotics. Methicillin-resistant Staphylococcus aureus (MRSA) was detected by susceptibility to oxacillin and growth on Brilliance MRSA II agar. Antibiotic resistance genes including mecA, femA rpoB, blaZ, ermB, ermA, ermC, vanA, vanB, tetK and tetM were screened. Results: Thirty isolates (12.3%) were positive for S. aureus by PCR with over 50% showing phenotypic resistance to methicillin. Resistance of S. aureus to antibiotics varied considerably with the highest resistance recorded to ampicillin and penicillin (96.7%), rifampicin and clindamycin (80%), oxacillin (73.3%) and erythromycin (70%). S. aureus revealed varying susceptibility to imipenem (96.7%), levofloxacin (86.7%), chloramphenicol (83.3%), cefoxitin (76.7%), ciprofloxacin (66.7%), gentamycin (63.3%), tetracycline and sulfamethoxazole-trimethoprim (56.7%), and vancomycin and doxycycline (50%). All 30 (100%) S. aureus isolates showed multiple antibiotic-resistant patterns (resistant to three or more antibiotics). The mecA, femA, rpoB, blaZ, ermB and tetM genes were detected in 5 (22.7%), 16 (53.3%), 11 (45.8%), 16 (55.2%), 15 (71.4%), and 8 (72.7%) isolates respectively; Conclusions: Results from this study indicate that beach water and sand from the Eastern Cape Province of South Africa may be potential reservoirs of antibiotic-resistant S. aureus which could be transmitted to exposed humans and animals.<\/jats:p>","DOI":"10.3390\/ijerph14091001","type":"journal-article","created":{"date-parts":[[2017,9,1]],"date-time":"2017-09-01T11:05:24Z","timestamp":1504263924000},"page":"1001","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":106,"title":["Antimicrobial Susceptibility of Staphylococcus aureus Isolated from Recreational Waters and Beach Sand in Eastern Cape Province of South Africa"],"prefix":"10.3390","volume":"14","author":[{"given":"Olufemi Emmanuel","family":"Akanbi","sequence":"first","affiliation":[{"name":"Microbial Pathogenicity and Molecular Epidemiology Research Group (MPMERG), Department of Biochemistry and Microbiology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henry Akum","family":"Njom","sequence":"additional","affiliation":[{"name":"Microbial Pathogenicity and Molecular Epidemiology Research Group (MPMERG), Department of Biochemistry and Microbiology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justine","family":"Fri","sequence":"additional","affiliation":[{"name":"Microbial Pathogenicity and Molecular Epidemiology Research Group (MPMERG), Department of Biochemistry and Microbiology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony C.","family":"Otigbu","sequence":"additional","affiliation":[{"name":"Microbial Pathogenicity and Molecular Epidemiology Research Group (MPMERG), Department of Biochemistry and Microbiology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna M.","family":"Clarke","sequence":"additional","affiliation":[{"name":"Microbial Pathogenicity and Molecular Epidemiology Research Group (MPMERG), Department of Biochemistry and Microbiology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2017,9,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/j.ijheh.2013.07.009","article-title":"Occupational exposure to raw meat: A newly-recognized risk factor for Staphylococcus aureus nasal colonization amongst food handlers","volume":"217","author":"Ho","year":"2014","journal-title":"Int. J. Hyg. Environ. Health"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1128\/CMR.17.1.218-234.2004","article-title":"Staphylococcus aureus capsular polysaccharides","volume":"17","author":"Lee","year":"2004","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","first-page":"352","article-title":"Antibiotic-resistant nosocomial pathogens. Part I: Diagnostic and typing methods","volume":"47","author":"Witte","year":"2004","journal-title":"Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"53","DOI":"10.2166\/wh.2003.0007","article-title":"Estimating the global burden of thalassogenic diseases: Human infectious diseases caused by wastewater pollution of the marine environment","volume":"1","author":"Shuval","year":"2003","journal-title":"J. Water Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/s12403-009-0012-9","article-title":"Skin-related symptoms following exposure to recreational water: A systematic review and meta-analysis","volume":"1","author":"Yau","year":"2009","journal-title":"Water Qual. Expos. Health"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2760","DOI":"10.1128\/JCM.39.8.2760-2767.2001","article-title":"Genetic variation among hospital isolates of methicillin-sensitive Staphylococcus aureus: Evidence for horizontal transfer of virulence genes","volume":"39","author":"Moore","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/S0966-842X(02)02459-9","article-title":"Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved","volume":"10","author":"Boyd","year":"2002","journal-title":"Trends Microbiol."},{"key":"ref_8","first-page":"489","article-title":"A quantitative and qualitative appraisal of microbial pollution of water by swimmers: A preliminary report","volume":"64","author":"Robinton","year":"1966","journal-title":"J. Hyg."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"11","DOI":"10.2166\/wst.1995.0547","article-title":"Association of staphylococcal skin infections and swimming","volume":"31","author":"Charoenca","year":"1995","journal-title":"Water Sci. Technol"},{"key":"ref_10","unstructured":"WHO (2003). Coastal and Fresh Waters. Guidelines for Safe Recreational Water Environments, World Health Organization."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/S0043-1354(96)00377-6","article-title":"Bather-related microbial and yeast populations in sand and seawater","volume":"31","author":"Papadakis","year":"1997","journal-title":"Water Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1289\/ehp.01109645","article-title":"Marine swimming-related illness: Implications for monitoring and environmental policy","volume":"109","author":"Henrickson","year":"2001","journal-title":"Environ. Health Perspect."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/S0025-326X(00)00007-2","article-title":"Comparative survival of faecal and human contaminants and use of Staphylococcus aureus as an effective indicator of human pollution","volume":"40","author":"Gabutti","year":"2000","journal-title":"Mar. Pollut. Bull."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1080\/09603129109356701","article-title":"Health effects of swimmers and nonpoint sources of contaminated waters","volume":"1","author":"Calderon","year":"1991","journal-title":"Int. J. Environ. Health Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.2105\/AJPH.75.9.1071","article-title":"A prospective study of swimming-related illness. II. Morbidity and the microbiological quality of water","volume":"75","author":"Seyfried","year":"1985","journal-title":"Am. J. Public Health"},{"key":"ref_16","first-page":"1","article-title":"Virulence and antibiotic resistance gene combinations among Staphylococcus aureus isolated from coastal waters of Oahu, Hawaii","volume":"12","author":"Stotts","year":"2005","journal-title":"J. Young Investig."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"5113","DOI":"10.1128\/JCM.41.11.5113-5120.2003","article-title":"Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: Establishing a national database","volume":"41","author":"McDougal","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Plano, L.R.W., Garza, A.C., Shibata, T., Elmir, S.M., Kish, J., Sinigalliano, C.D., Gidley, M.L., Miller, G., Withum, K., and Fleming, L.E. (2011). Shedding of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from adult and pediatric bathers in marine waters. BMC Microbiol., 1.","DOI":"10.1186\/1471-2180-11-5"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.watres.2006.10.005","article-title":"Quantitative evaluation of bacteria released by bathers in marine water","volume":"41","author":"Elmir","year":"2007","journal-title":"Water Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4802","DOI":"10.1016\/j.watres.2009.06.025","article-title":"Performance of CHROMagar Staph aureus and CHROMagar MRSA for detection of Staphylococcus aureus in beach water and sand-comparison of culture, agglutination, and molecular analyses","volume":"43","author":"Goodwin","year":"2009","journal-title":"Water Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1093\/jac\/dkp368","article-title":"Characterization of methicillin-resistant and methicillin-resistant coagulase-negative Staphylococcus spp. isolated from US West Coast public marine beaches","volume":"64","author":"Soge","year":"2009","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S171","DOI":"10.1086\/653517","article-title":"Meeting the challenges of methicillin-resistant Staphylococcus aureus with outpatient parenteral antimicrobial therapy","volume":"51","author":"Tice","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1571","DOI":"10.1111\/j.1365-2672.2011.05013.x","article-title":"Indicator microbes correlate with pathogenic bacteria, yeasts and helminthes in sand at a subtropical recreational beach site","volume":"110","author":"Shah","year":"2011","journal-title":"J. Appl. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4195","DOI":"10.1016\/j.watres.2012.04.001","article-title":"A multi-beach study of Staphylococcus aureus, MRSA, and enterococci in seawater and beach sand","volume":"46","author":"Goodwin","year":"2012","journal-title":"Water Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.meegid.2008.07.007","article-title":"The evolution of Staphylococcus aureus","volume":"8","author":"Deurenberg","year":"2008","journal-title":"Infect. Genet. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1128\/jb.158.2.513-516.1984","article-title":"Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus","volume":"158","author":"Hartman","year":"1984","journal-title":"J. Bacteriol."},{"key":"ref_27","unstructured":"Tavares, A.L. (2014). Community-Associated Methicillin-Resistant Staphylococcus aureus (CA-MRSA) in Portugal: Origin, Epidemiology and Virulence. [Ph.D. Thesis, Universidade Nova de Lisboa]."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1051\/vetres:2001129","article-title":"Antimicrobial resistance in staphylococci from animals with particular reference to bovine Staphylococcus aureus, porcine Staphylococcus hyicus and canine Staphylococcus intermedius","volume":"32","author":"Werckenthin","year":"2001","journal-title":"Vet. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1016\/j.cell.2007.03.004","article-title":"Molecular mechanisms of antibacterial multidrug resistance","volume":"128","author":"Alekshun","year":"2007","journal-title":"Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1128\/JCM.44.1.108-118.2006","article-title":"Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States","volume":"44","author":"Tenover","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/j.addr.2005.04.002","article-title":"Bacterial resistance to antibiotics: Enzymatic degradation and modification","volume":"57","author":"Wright","year":"2005","journal-title":"Adv. Drug Deliv. Rev."},{"key":"ref_32","unstructured":"GOOGLE MAPS (2016, June 18). Map of Eastern Cape Beaches. [Online]. Available online: https:\/\/www.google.co.za\/maps\/search\/eastern+cape+beaches+map+from+east+london+to+port+elizabeth\/@33.9988012,22.5881698,2619m\/data = !3m2!1e3!4b1?hl = en&authuser = 0."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.marpolbul.2006.12.018","article-title":"Luminex detection of faecal indicators in river samples, marine recreational water, and beach sand","volume":"54","author":"Baums","year":"2007","journal-title":"Mar. Pollut. Bull."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1111\/j.1472-765X.1994.tb00458.x","article-title":"Evaluation of different DNA extraction procedures for the detection of Salmonella from chicken products by polymerase chain reaction","volume":"19","author":"Soumet","year":"1994","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1514","DOI":"10.1128\/JCM.40.4.1514-1517.2002","article-title":"Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from coagulase-negative staphylococci and determine methicillin resistance from blood cultures","volume":"40","author":"Maes","year":"2002","journal-title":"J. Clin. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1093\/ajcp\/45.4_ts.493","article-title":"Antibiotic susceptibility testing by a standardized single disk method","volume":"45","author":"Bauer","year":"1966","journal-title":"Am. J. Clin. Pathol."},{"key":"ref_37","unstructured":"Clinical Laboratory Standards Institute (2014). Performance Standards for Antimicrobial Susceptibility Testing: Eighteenth Informational Supplement, Clinical Laboratory Standards Institute. CLSI Document M100-S18."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.1128\/JCM.02995-12","article-title":"Evaluation of brilliance MRSA 2 agar for detection of methicillin-resistant Staphylococcus aureus in clinical samples","volume":"51","author":"Veenemans","year":"2013","journal-title":"J. Clin. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3332","DOI":"10.1128\/JCM.39.9.3332-3338.2001","article-title":"Multiplex PCR protocol for the diagnosis of Staphylococcal infection","volume":"39","author":"Mason","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1128\/JCM.38.3.1032-1035.2000","article-title":"Multiplex PCR for Detection of Genes for Staphylococcus aureus Enterotoxins, Exfoliative Toxins, Toxic Shock Syndrome Toxin 1, and Methicillin Resistance","volume":"38","author":"Mehrotra","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0924-8579(97)00027-7","article-title":"Antibiotics for treatment of infections caused by MRSA and elimination of MRSA carriage. What are the choices?","volume":"9","author":"Schmitz","year":"1997","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1128\/AAC.44.2.231-238.2000","article-title":"Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis","volume":"44","author":"Martineau","year":"2000","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/0167-4781(95)00054-K","article-title":"Nucleotide sequence of the Staphylococcus aureus RNA polymerase rpoB gene and comparison of its predicted amino acid sequence with those of other bacteria","volume":"1262","author":"Aboshkiwa","year":"1995","journal-title":"Biochim. Biophys. Acta BBA Gene Struct. Express."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"4089","DOI":"10.1128\/JCM.41.9.4089-4094.2003","article-title":"Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus","volume":"41","author":"Strommenger","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.ijheh.2012.12.004","article-title":"Detection and genotyping of vancomycin-resistant Enterococcus spp. by multiplex polymerase chain reaction in Korean aquatic environmental samples","volume":"216","author":"Nam","year":"2012","journal-title":"Int. J. Hyg. Environ. Health"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"468","DOI":"10.3201\/eid1106.040831","article-title":"Methicillin-resistant-Staphylococcus aureus hospitalizations, United States","volume":"11","author":"Kuehnert","year":"2005","journal-title":"Emerg. Infect. Dis."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.copbio.2008.05.006","article-title":"Antibiotics and antibiotic resistance in water environments","volume":"19","author":"Baquero","year":"2008","journal-title":"Curr. Opin. Biotechnol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1007\/s10661-009-1180-6","article-title":"Antimicrobial resistance of heterotrophic marine bacteria isolated from seawater and sands of recreational beaches with different organic pollution levels in southeastern Brazil: evidences of resistance dissemination","volume":"169","author":"Oliveira","year":"2010","journal-title":"Environ. Monit. Assess."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"139","DOI":"10.3923\/jest.2011.139.149","article-title":"Occurrence and seasonal distribution of antibiotic resistance heterotrophic bacteria and physico-chemical characteristics of Muthupettai mangrove environment, southeast coast of India","volume":"4","author":"Manivasagan","year":"2011","journal-title":"J. Environ. Sci. Technol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.marpolbul.2009.09.025","article-title":"Detection of antibiotic resistant bacteria inhabiting the sand of non-recreational marine beach","volume":"60","author":"Mudryk","year":"2010","journal-title":"Mar. Pollut. Bull."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.marpolbul.2004.10.001","article-title":"Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach","volume":"50","author":"Mudryk","year":"2005","journal-title":"Mar. Pollut. Bull."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1111\/j.1574-6941.2003.tb01073.x","article-title":"Detection of antibiotic resistant bacteria and their resistance genes in wastewater, surface water and drinking water biofilms","volume":"43","author":"Schwartz","year":"2003","journal-title":"FEMS Microbiol Ecol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1128\/CMR.00081-09","article-title":"Community-Associated Methicillin-Resistant Staphylococcus aureus: Epidemiology and Clinical Consequences of an Emerging Epidemic","volume":"23","author":"David","year":"2010","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/S1473-3099(05)70112-2","article-title":"Community-acquired meticillin-resistant Staphylococcus aureus: An emerging threat","volume":"5","author":"Zetola","year":"2005","journal-title":"Lancet Infect. Dis."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1001\/jama.298.15.1763","article-title":"Invasive methicillin-resistant Staphylococcus aureus infections in the United States","volume":"298","author":"Klevens","year":"2007","journal-title":"JAMA"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/labinvest.3700501","article-title":"Community-acquired methicillin-resistant Staphylococcus aureus: The role of Panton-Valentine leukocidin","volume":"87","author":"Robert","year":"2007","journal-title":"Lab. Investig."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1128\/AEM.02127-09","article-title":"Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach","volume":"76","author":"Abdelzaher","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5681","DOI":"10.1016\/j.watres.2011.08.037","article-title":"Survival of environmental and clinical strains of methicillin-resistant Staphylococcus aureus (MRSA) in marine and fresh waters","volume":"45","author":"Bonilla","year":"2011","journal-title":"Water Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1128\/AEM.06185-11","article-title":"Occurrence and persistence of human pathogens and indicator organisms in beach sands along the California coast","volume":"78","author":"Yamahara","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/j.meatsci.2004.10.011","article-title":"A note on the incidence and the antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples","volume":"69","author":"Gundogan","year":"2005","journal-title":"Meat Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrmicro2200","article-title":"Waves of resistance: Staphylococcus aureus in the antibiotic era","volume":"7","author":"Chambers","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_62","unstructured":"Akindolire, M.A. (2013). Detection and Molecular Characterization of Virulence Genes in Antibiotic Resistant Staphylococcus aureus from Milk in the North West Province. [Ph.D. Thesis, North West University]."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1017\/S0195941700082333","article-title":"First case of VRSA identified in Michigan","volume":"23","author":"Bartley","year":"2002","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/S0378-1135(00)00347-3","article-title":"Molecular epidemiology and genetic linkage of macrolide and aminoglycoside resistance in Staphylococcus intermedius of canine origin","volume":"79","author":"Boerlin","year":"2001","journal-title":"Vet. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Tanwar, J., Das, S., Fatima, Z., and Hameed, S. (2014). Multidrug resistance: An emerging crisis. Interdiscip. Perspect. Infect. Dis.","DOI":"10.1155\/2014\/541340"},{"key":"ref_66","first-page":"41","article-title":"Antibiotic resistance of Staphylococcus-like organisms isolated from a recreational sea beach on the southern coast of the Baltic Sea as one of the consequences of anthropogenic pressure","volume":"43","author":"Miranowicz","year":"2014","journal-title":"Int. J. Oceanogr. Hydrobiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4102\/sajs.v106i11\/12.243","article-title":"Antibiotic-resistant Staphylococcus aureus isolated from milk in the Mafikeng Area, North West province, South Africa","volume":"106","author":"Ateba","year":"2010","journal-title":"S. Afr. J. Sci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.foodcont.2005.09.013","article-title":"Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA)","volume":"18","author":"Pesavento","year":"2007","journal-title":"Food Control"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.ijfoodmicro.2006.10.049","article-title":"Occurrence, characterization and antimicrobial resistance of entero-toxigenic Staphylococcus aureus isolated from meat and dairy products","volume":"115","author":"Normanno","year":"2007","journal-title":"Int. J. Food Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/S1368-7646(03)00003-7","article-title":"Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: Genomic island SCC","volume":"6","author":"Ito","year":"2003","journal-title":"Drug Resist. Updates"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"3499","DOI":"10.1128\/AEM.64.9.3499-3502.1998","article-title":"Antibiotic resistance in Acinetobacter sp. isolated from sewers receiving waste effluent from a hospital and a pharmaceutical plant","volume":"64","author":"Guardabassi","year":"1998","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1016\/S0045-6535(01)00144-8","article-title":"Drugs in the environment: Emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources\u2014A review","volume":"45","year":"2001","journal-title":"Chemosphere"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1966","DOI":"10.1128\/AAC.37.9.1966","article-title":"Genes involved in the regulation of \u03b2-lactamase production in enterococci and staphylococci, Antimicrob","volume":"37","author":"Zscheck","year":"1993","journal-title":"Agents Chemoth."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"6489","DOI":"10.1128\/AEM.69.11.6489-6494.2003","article-title":"Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans","volume":"69","author":"Lee","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.foodcont.2013.02.017","article-title":"MRSA detection in raw milk, some dairy products and hands of dairy workers in Egypt, a mini-survey","volume":"33","author":"Kamal","year":"2013","journal-title":"Food Control"},{"key":"ref_76","first-page":"3107","article-title":"Prevalence of Methicillin-Resistant Staphylococcus aureus in Raw Milk and Dairy Products in Sarab by Culture and PCR Techniques","volume":"10","author":"Mirzaei","year":"2011","journal-title":"J. Anim. Vet. Adv."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/j.watres.2008.11.036","article-title":"A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-resistant S. aureus in a municipal wastewater treatment plant","volume":"43","author":"Melin","year":"2009","journal-title":"Water Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.diagmicrobio.2006.10.022","article-title":"Detection of mecA-mediated resistance using reference and commercial testing methods in a collection of Staphylococcus aureus expressing borderline oxacillin MICs","volume":"58","author":"Swenson","year":"2007","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2155","DOI":"10.1128\/AAC.46.7.2155-2161.2002","article-title":"Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus","volume":"46","author":"Oliveira","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1128\/CMR.10.4.781","article-title":"Methicillin resistance in staphylococci: Molecular and biochemical basis and clinical implications","volume":"10","author":"Chambers","year":"1997","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1093\/clinids\/5.Supplement_3.S407","article-title":"Rifampin: Mechanisms of action and resistance","volume":"5","author":"Wehrli","year":"1983","journal-title":"Rev. Infect. Dis."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2590","DOI":"10.1128\/AAC.42.10.2590","article-title":"Characterization of mutants in the rpoB gene that confer rifampin resistance in Staphylococcus aureus","volume":"42","author":"Soussy","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"29428","DOI":"10.1074\/jbc.270.49.29428","article-title":"The b-subunit rif-cluster I is only angstroms away from the active center of Escherichia coli RNA polymerase","volume":"270","author":"Severinov","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/0022-2836(88)90517-7","article-title":"Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance","volume":"202","author":"Jin","year":"1988","journal-title":"J. Mol. Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1128\/AAC.39.3.577","article-title":"Erythromycin resistance by ribosomes modification","volume":"39","author":"Weisblum","year":"1995","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"3024","DOI":"10.1128\/AAC.42.11.3024","article-title":"Characterization of erythromycin- resistant isolates of Staphylococcus aureus recovered in the United States from 1958 through 1969","volume":"42","author":"Nicola","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.fm.2007.09.004","article-title":"Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities","volume":"25","author":"Simeoni","year":"2008","journal-title":"Food Microbiol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"3507","DOI":"10.1128\/jb.173.11.3507-3513.1991","article-title":"femA, Which Encodes a Factor Essential for Expression of Methicillin Resistance, Affects Glycine Content of Peptidoglycan in Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Strains","volume":"173","author":"Maidhof","year":"1991","journal-title":"J. Bacterial."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1017\/S0950268800051682","article-title":"Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction","volume":"113","author":"Kobayashi","year":"1994","journal-title":"Epidemiol. Infect."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/14\/9\/1001\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T18:43:53Z","timestamp":1760208233000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/14\/9\/1001"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,9,1]]},"references-count":89,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2017,9]]}},"alternative-id":["ijerph14091001"],"URL":"https:\/\/doi.org\/10.3390\/ijerph14091001","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,9,1]]}}}