{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T02:24:14Z","timestamp":1793327054923,"version":"4.5.0"},"reference-count":55,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2020,4,2]],"date-time":"2020-04-02T00:00:00Z","timestamp":1585785600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005274","name":"North-West University","doi-asserted-by":"publisher","award":["0000"],"award-info":[{"award-number":["0000"]}],"id":[{"id":"10.13039\/501100005274","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Background: Biofilm formation in S. aureus may reduce the rate of penetration of antibiotics, thereby complicating treatment of infections caused by these bacteria. The aim of this study was to correlate biofilm-forming potentials, antimicrobial resistance, and genes in S. aureus isolates. Methods: A total of 64 milk samples were analysed, and 77 S. aureus were isolated. Results: Seventy (90.9%) isolates were biofilm producers. The ica biofilm-forming genes were detected among 75.3% of the isolates, with icaA being the most prevalent (49, 63.6%). The icaB gene was significantly (P = 0.027) higher in isolates with strong biofilm formation potentials. High resistance (60%\u201390%) of the isolates was observed against ceftriaxone, vancomycin, and penicillin, and 25 (32.5%) of S. aureus showed multidrug resistance (MDR) to at least three antibiotics. Five resistance genes, namely blaZ (29, 37.7%), vanC (29, 37.7%), tetK (24, 31.2%), tetL (21, 27.3%), and msrA\/B (16, 20.8%) were detected. Most MDR phenotypes possessed at least one resistance gene alongside the biofilm genes. However, no distinct pattern was identified among the resistance and biofilm phenotypes. Conclusions: The high frequency of potentially pathogenic MDR S. aureus in milk samples intended for human consumption, demonstrates the public health relevance of this pathogen in the region.<\/jats:p>","DOI":"10.3390\/antibiotics9040156","type":"journal-article","created":{"date-parts":[[2020,4,2]],"date-time":"2020-04-02T10:33:58Z","timestamp":1585823638000},"page":"156","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":51,"title":["Genotypic and Phenotypic Evaluation of Biofilm Production and Antimicrobial Resistance in Staphylococcus aureus Isolated from Milk, North West Province, South Africa"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2132-7363","authenticated-orcid":false,"given":"Marie Ebob Agbortabot","family":"Bissong","sequence":"first","affiliation":[{"name":"Antibiotic Resistance and Phage Biocontrol Research Group (AREPHABREG), Department of Microbiology, School of Biological Sciences, North-West University\u2014Mafikeng Campus, Private Bag X2046, Mmabatho 2735, South Africa"},{"name":"Department of Biomedical Science, University of Bamenda, Bambili P. O. Box 39, Cameroon"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0227-1432","authenticated-orcid":false,"given":"Collins Njie","family":"Ateba","sequence":"additional","affiliation":[{"name":"Antibiotic Resistance and Phage Biocontrol Research Group (AREPHABREG), Department of Microbiology, School of Biological Sciences, North-West University\u2014Mafikeng Campus, Private Bag X2046, Mmabatho 2735, South Africa"},{"name":"Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho, Mafikeng 2735, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1146\/annurev.mi.34.100180.003015","article-title":"Natural populations of the genus Staphylococcus","volume":"34","author":"Kloos","year":"1980","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_2","unstructured":"Sussmann, M., and Newcastle, U.T. (2002). Staphylococcus aureus. Molecular Medical Microbiology, Academic Press. [2nd ed.]."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Gyles, C.L., Songer, J.G., and Thoen, C.O. (2004). Staphylococcus. Pathogenesis of Bacterial Infections in Animals, Blackwell Publishing. [3rd ed.].","DOI":"10.1002\/9780470344903"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1128\/CMR.00002-11","article-title":"Food animals and antimicrobials: Impacts on human health","volume":"24","author":"Marshall","year":"2011","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_5","first-page":"63","article-title":"Staphylococcus aureus and food poisoning","volume":"2","author":"Baron","year":"2003","journal-title":"Gen. Mol. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1007\/s11908-005-0043-8","article-title":"Virulence determinants in Staphylococcus aureus and their involvement in clinical syndromes","volume":"7","author":"Ferry","year":"2005","journal-title":"Curr. Infect. Dis. Rep."},{"key":"ref_7","first-page":"207","article-title":"Staphylococcal biofilms","volume":"322","author":"Otto","year":"2008","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1073\/pnas.1115006109","article-title":"How Staphylococcus aureus biofilms develop their characteristic structure","volume":"109","author":"Periasamy","year":"2012","journal-title":"PNAS"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4711","DOI":"10.1128\/IAI.66.10.4711-4720.1998","article-title":"The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide\/adhesion","volume":"66","author":"McKenney","year":"1998","journal-title":"Infect. Immun."},{"key":"ref_10","first-page":"1","article-title":"Prevalence of adhesion and regulation of biofilm-related genes in different clones of Staphylococcus aureus","volume":"2012","author":"Atshan","year":"2012","journal-title":"J. Biomed. Biotech."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.1128\/IAI.72.4.2177-2185.2004","article-title":"Role of biofilm\u2014Associated protein bap in the pathogenesis of bovine Staphylococcus aureus","volume":"72","author":"Cucarella","year":"2004","journal-title":"Infect. Immun."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.resmic.2005.11.003","article-title":"A family of surface proteins involved in biofilm formation","volume":"157","author":"Lassa","year":"2006","journal-title":"Res. Microbiol."},{"key":"ref_13","unstructured":"Garc\u00e9s, L. (2020, January 12). The Detrimental Impacts of Industrial Animal Agriculture: A Case for Humane and Sustainable Agriculture, Compassion in World Farming Trust. Available online: http:\/\/www.ciwf.org.uk\/includes\/documents\/cm_docs\/2008\/d\/detrimental_impact_industrial_animal_agriculture_2002.pdf."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1590\/s0100-736x2016001000006","article-title":"Antimicrobial resistance profiles of Staphylococcus aureus clusters on small dairy farms in southern Brazil","volume":"36","author":"Girardini","year":"2016","journal-title":"Pesq. Vet. Bras."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"25","DOI":"10.2147\/IJGM.S153268","article-title":"In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance","volume":"11","author":"Neopane","year":"2018","journal-title":"Int. J. Gen. Med."},{"key":"ref_16","first-page":"583","article-title":"Antibiotic management and resistance in livestock production","volume":"101","author":"Henton","year":"2011","journal-title":"S. Afr. Med. J."},{"key":"ref_17","first-page":"870","article-title":"Structural basis for the \u00df-lactam resistance of PBP2a from methicillin\u2014Resistant Staphylococcus aureus","volume":"9","author":"Lim","year":"2002","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"630","DOI":"10.3201\/eid1304.060833","article-title":"MRSA transmission between cows and humans","volume":"13","author":"Somogyi","year":"2007","journal-title":"Emerg. Infect. Dis."},{"key":"ref_19","first-page":"S82","article-title":"The relationship between antimicrobial resistance and patient outcomes: Mortality, length of hospital stay, and health care costs","volume":"42","author":"Cosgrove","year":"2006","journal-title":"Genet. Mol. Res."},{"key":"ref_20","unstructured":"Fauci, A., Braunwald, E., Casper, D., Hauser, S., Longo, D., and Jameson, J. (2013). Staphylococcal infections. Harrison\u2019s Principles of Internal Medicine, The McGraw-Hill Companies Inc."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"10254","DOI":"10.3390\/ijerph120910254","article-title":"Detection of antibiotic resistant Staphylococcus aureus from milk: A public health implication","volume":"12","author":"Akindolire","year":"2015","journal-title":"Int. J. Environ. Res. Public Health."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ateba, C.N., Mbewe, M., Moneoang, M.S., and Bezuidenhout, C.C. (2010). Antibiotic-resistant Staphylococcus aureus isolated from milk in the Mafikeng Area, North West province, South Africa. S. Afr. J. Sci., 106.","DOI":"10.4102\/sajs.v106i11\/12.243"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2017.00511","article-title":"Molecular characterization of Staphylococcus aureus isolated from bovine mastitis and close human contacts in south african dairy herds: Genetic diversity and inter-species host transmission","volume":"8","author":"Schmidt","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_24","first-page":"1","article-title":"Prevalence of MRSA among large commercial pig herds in South Africa","volume":"85","author":"Lochem","year":"2018","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Akanbi, O.E., Njom, H.A., Fri, J., Otigbu, A.C., and Clarke, A.M. (2017). Antimicrobial susceptibility of Staphylococcus aureus isolated from recreational waters and beach sand in eastern cape province of South Africa. Int. J. Environ. Res. Public Health., 14.","DOI":"10.3390\/ijerph14091001"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.ijid.2014.10.011","article-title":"Staphylococcus aureus bacteraemia in Gauteng academic hospitals, South Africa","volume":"30","author":"Badat","year":"2015","journal-title":"Int. J. Infect. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.micpath.2015.10.023","article-title":"Biofilm formation in invasive Staphylococcus aureus isolates is associated with the clonal lineage","volume":"90","author":"Naicker","year":"2016","journal-title":"Microb. Pathog."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"8796","DOI":"10.3168\/jds.2017-13370","article-title":"Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China","volume":"100","author":"Liu","year":"2017","journal-title":"J. Dairy Sci."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Avila-Novoa, M.G., I\u00f1\u0131guez-Moreno, M., Sol\u0131s-Velazquez, O.A., Gonzalez-Gomez, J.P., Guerrero-Medina, P.J., and Gutierrez-Lomel, M. (2018). Biofilm Formation by Staphylococcus aureus isolated from Food Contact Surfaces in the Dairy Industry of Jalisco, Mexico. J. Food Qual., 1746139.","DOI":"10.1155\/2018\/1746139"},{"key":"ref_30","unstructured":"Nourbakhsh, F., and Namvar, A.E. (2016). Detection of genes involved in biofilm formation in Staphylococcus aureus isolates. GMS Hyg. Infect. Control, 11."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"65","DOI":"10.33073\/pjm-2012-009","article-title":"Biofilm production and presence of ica and bap genes in Staphylococcus aureus strains isolated from cows with Mastitis in the Eastern Poland","volume":"61","author":"Szweda","year":"2012","journal-title":"Pol. J. Microbiol."},{"key":"ref_32","first-page":"97","article-title":"Detection of biofilm producing coagulase positive Staphylococcus aureus from bovine mastitis, their pigment production, hemolytic activity and antibiotic sensitivity pattern","volume":"4","author":"Begum","year":"2007","journal-title":"J. Bangladesh Soc. Agric. Sci. Technol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.bjm.2016.10.001","article-title":"Biofilm production and beta-lactamic resistance in Brazilian Staphylococcus aureus isolates from bovine mastitis","volume":"48","author":"Marques","year":"2017","journal-title":"Braz. J. Microbiol."},{"key":"ref_34","first-page":"11","article-title":"Prevalence and Characterization of Staphylococcus aureus Cultured From Raw Milk Taken From Dairy Cows With Mastitis in Beijing, China","volume":"9","author":"Wang","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1289157","DOI":"10.1155\/2016\/1289157","article-title":"In Vitro and In Vivo Biofilm Characterization of Methicillin-Resistant Staphylococcus aureus from Patients Associated with Pharyngitis Infection","volume":"2016","author":"Gowrishankar","year":"2016","journal-title":"BioMed Res. Int."},{"key":"ref_36","first-page":"62","article-title":"Analysis of biofilm formation and associated genes detected in Staphylococcus isolates from bovine mastitis","volume":"10","author":"Li","year":"2012","journal-title":"Intern. J. Appl. Res. Vet. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"8","DOI":"10.4102\/jsava.v83i1.16","article-title":"A survey of antimicrobial usage in animals in South Africa with specific reference to food animals","volume":"83","author":"Eagar","year":"2012","journal-title":"J. S. Afr. Vet Assoc."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1172\/JCI68834","article-title":"Mechanisms of vancomycin resistance in Staphylococcus aureus","volume":"124","author":"Gardete","year":"2014","journal-title":"J. Clin. Investig."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"92","DOI":"10.11648\/j.ejcbs.20160206.16","article-title":"Prevalence and antibiotic susceptibility patterns of methicillin resistant Staphylococcus aureus in patients attending the Laquintinie Hospital Douala, Cameroon","volume":"2","author":"Bissong","year":"2016","journal-title":"Eur. J. Clin. Biomed. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"598","DOI":"10.14202\/vetworld.2017.598-604","article-title":"Molecular characterization of antibiotic-resistant Staphylococcus aureus from livestock (bovine and swine)","volume":"10","author":"Zehra","year":"2017","journal-title":"Vet. World"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.jiph.2016.05.010","article-title":"Molecular characterization of antimicrobial resistance genes against Staphylococcus aureus isolates from Trinidad and Tobago","volume":"10","author":"Akpaka","year":"2017","journal-title":"J. Infect. Public Health."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.bjm.2016.10.011","article-title":"Correlation of phenotypic tests with the presence of the blaZ gene for detection of beta-lactamase","volume":"48","author":"Ferreira","year":"2017","journal-title":"Braz. J. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1111\/j.1469-0691.2008.01997.x","article-title":"Comparison of phenotypic methods for penicillinase detection in Staphylococcus aureus","volume":"4","author":"Kaase","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.diagmicrobio.2012.07.013","article-title":"Presence of the blaZ beta-lactamase gene in isolates of Staphylococcus aureus that appear penicillin susceptible by conventional phenotypic methods","volume":"74","author":"Stamm","year":"2012","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1654","DOI":"10.1128\/jcm.30.7.1654-1660.1992","article-title":"Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene","volume":"30","author":"Brakstad","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"ref_46","first-page":"e10741","article-title":"Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA) strains","volume":"7","author":"Alfatemi","year":"2014","journal-title":"Jundishapur J. Microbiol."},{"key":"ref_47","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_48","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1128\/AEM.71.1.574-579.2005","article-title":"Molecular diversity and characterization of tetracycline-resistant Staphylococcus aureus isolates from a poultry processing plant","volume":"71","author":"Huys","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_49","first-page":"170","article-title":"Methylase genes-mediated erythromycin resistance in Staphylococcus aureus from bovine mastitis in China","volume":"67","author":"Ding","year":"2012","journal-title":"Israel J. Vet. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1099\/jmm.0.47144-0","article-title":"Identification and characterization of a vancomycin-resistant Staphylococcus aureus isolated from Kolkata (South Asia)","volume":"57","author":"Saha","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"335","DOI":"10.5001\/omj.2014.90","article-title":"VanA and vanB positive vancomycin-resistant Staphylococcus aureus among clinical isolates in Shiraz, South of Iran","volume":"29","author":"Saadat","year":"2014","journal-title":"Oman Med. J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1128\/jcm.22.6.996-1006.1985","article-title":"Adherence of coagulase-negative staphylococci to plastic tissue culture plates: A quantitative model for the adherence of staphylococci to medical devices","volume":"22","author":"Christensen","year":"1985","journal-title":"J. Clin. Microbiol."},{"key":"ref_53","unstructured":"Wayne, P.A. (2016). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [26th ed.]. CLSI supplement M100S."},{"key":"ref_54","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2008). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, Clinical and Laboratory Standards Institute. [3rd ed.]. CLSI document M31-A3."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"62","DOI":"10.4103\/2277-9175.179184","article-title":"Distribution of erm genes among Staphylococcus aureus isolates with inducible resistance to clindamycin in Isfahan, Iran","volume":"5","author":"Ghanbari","year":"2016","journal-title":"Adv. Biomed. Res."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/4\/156\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:14:35Z","timestamp":1760174075000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/4\/156"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,2]]},"references-count":55,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["antibiotics9040156"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics9040156","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,2]]}}}