{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T17:48:19Z","timestamp":1791654499135,"version":"4.3.4"},"reference-count":47,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T00:00:00Z","timestamp":1712707200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>This study aimed to assess (a) the biofilm producer ability and antimicrobial resistance profiles of Staphylococcus (Staph.) aureus and Streptococcus (Strep.) uberis isolated from cows with clinical mastitis (CM) and subclinical mastitis (SCM), and (b) the association between biofilm producer ability and antimicrobial resistance. We isolated a total of 197 Staph. aureus strains (SCM = 111, CM = 86) and 119 Strep. uberis strains (SCM = 15, CM = 104) from milk samples obtained from 316 cows distributed in 24 dairy herds. Biofilm-forming ability was assessed using the microplate method, while antimicrobial susceptibility was determined using the disk diffusion method against 13 antimicrobials. Among the isolates examined, 57.3% of Staph. aureus and 53.8% of Strep. uberis exhibited the ability to produce biofilm, which was categorized as strong, moderate, or weak. In terms of antimicrobial susceptibility, Staph. aureus isolates displayed resistance to penicillin (92.9%), ampicillin (50.8%), and tetracycline (52.7%). Conversely, Strep. uberis isolates exhibited resistance to penicillin (80.6%), oxacillin (80.6%), and tetracycline (37.8%). However, no significant correlation was found between antimicrobial resistance patterns and biofilm formation ability among the isolates.<\/jats:p>","DOI":"10.3390\/vetsci11040170","type":"journal-article","created":{"date-parts":[[2024,4,11]],"date-time":"2024-04-11T03:29:04Z","timestamp":1712806144000},"page":"170","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Biofilm Formation and Antimicrobial Resistance of Staphylococcus aureus and Streptococcus uberis Isolates from Bovine Mastitis"],"prefix":"10.3390","volume":"11","author":[{"given":"Carlos E.","family":"Fidelis","sequence":"first","affiliation":[{"name":"Department of Animal Nutrition and Production, School of Veterinary Medicine and Animal Science, University of S\u00e3o Paulo (USP), Pirassununga 13635-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8641-2086","authenticated-orcid":false,"given":"Alessandra M.","family":"Orsi","sequence":"additional","affiliation":[{"name":"Department of Animal Nutrition and Production, School of Veterinary Medicine and Animal Science, University of S\u00e3o Paulo (USP), Pirassununga 13635-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2708-5414","authenticated-orcid":false,"given":"Gustavo","family":"Freu","sequence":"additional","affiliation":[{"name":"Department of Animal Nutrition and Production, School of Veterinary Medicine and Animal Science, University of S\u00e3o Paulo (USP), Pirassununga 13635-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2138-4982","authenticated-orcid":false,"given":"Juliano L.","family":"Gon\u00e7alves","sequence":"additional","affiliation":[{"name":"Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48864, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4273-3494","authenticated-orcid":false,"given":"Marcos V. dos","family":"Santos","sequence":"additional","affiliation":[{"name":"Department of Animal Nutrition and Production, School of Veterinary Medicine and Animal Science, University of S\u00e3o Paulo (USP), Pirassununga 13635-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"9493","DOI":"10.3168\/jds.2018-14824","article-title":"Pathogen-Specific Production Losses in Bovine Mastitis","volume":"101","author":"Liski","year":"2018","journal-title":"J. Dairy Sci."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Freu, G., Garcia, B.L.N., Tomazi, T., Di Leo, G.S., Gheller, L.S., Bronzo, V., Moroni, P., and Dos Santos, M.V. (2023). Association between Mastitis Occurrence in Dairy Cows and Bedding Characteristics of Compost-Bedded Pack Barns. Pathogens, 12.","DOI":"10.3390\/pathogens12040583"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Monistero, V., Barberio, A., Cremonesi, P., Castiglioni, B., Morandi, S., Lassen, D.C.K., Astrup, L.B., Locatelli, C., Piccinini, R., and Filippa Addis, M. (2021). Genotyping and Antimicrobial Susceptibility Profiling of Streptococcus uberis Isolated from a Clinical Bovine Mastitis Outbreak in a Dairy Farm. Antibiotics, 10.","DOI":"10.3390\/antibiotics10060644"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1007\/s42770-023-00918-2","article-title":"Molecular Characterization of Persistent Subclinical Mastitis-Causing Staphylococcus aureus from Dairy Farms","volume":"54","author":"Lee","year":"2023","journal-title":"Braz. J. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.cvfa.2012.03.010","article-title":"Update on Control of Staphylococcus aureus and Streptococcus agalactiae for Management of Mastitis","volume":"28","author":"Keefe","year":"2012","journal-title":"Vet. Clin. N. Am. Food Anim. Pract."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.5713\/ajas.20.0156","article-title":"Bovine Mastitis: Risk Factors, Therapeutic Strategies, and Alternative Treatments\u2014A Review","volume":"33","author":"Cheng","year":"2020","journal-title":"Asian-Australas. J. Anim. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.vetmic.2012.07.043","article-title":"Antimicrobial Resistance and Molecular Epidemiology of Streptococci from Bovine Mastitis","volume":"161","author":"Rato","year":"2013","journal-title":"Vet. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1128\/JCM.01583-15","article-title":"Molecular Epidemiology of Streptococcus uberis Clinical Mastitis in Dairy Herds: Strain Heterogeneity and Transmission","volume":"54","author":"Davies","year":"2016","journal-title":"J. Clin. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Schmenger, A., and Kr\u00f6mker, V. (2020). Characterization, Cure Rates and Associated Risks of Clinical Mastitis in Northern Germany. Vet. Sci., 7.","DOI":"10.3390\/vetsci7040170"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Kaczorek, E., Ma\u0142aczewska, J., W\u00f3jcik, R., and Siwicki, A.K. (2017). Biofilm Production and Other Virulence Factors in Streptococcus spp. Isolated from Clinical Cases of Bovine Mastitis in Poland. BMC Vet. Res., 13.","DOI":"10.1186\/s12917-017-1322-y"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/s41579-022-00791-0","article-title":"The Biofilm Matrix: Multitasking in a Shared Space","volume":"21","author":"Flemming","year":"2023","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1016\/j.tim.2022.02.005","article-title":"Population Genetics, Biofilm Recalcitrance, and Antibiotic Resistance Evolution","volume":"30","author":"Roizman","year":"2022","journal-title":"Trends Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Sharma, S., Mohler, J., Mahajan, S.D., Schwartz, S.A., Bruggemann, L., and Aalinkeel, R. (2023). Microbial Biofilm: A Review on Formation, Infection, Antibiotic Resistance, Control Measures, and Innovative Treatment. Microorganisms, 11.","DOI":"10.3390\/microorganisms11061614"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.tvjl.2005.01.006","article-title":"Biofilms: A Role in Recurrent Mastitis Infections?","volume":"171","author":"Melchior","year":"2006","journal-title":"Vet. J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1186\/s40001-023-01121-7","article-title":"Biofilm and Wound Healing: From Bench to Bedside","volume":"28","author":"Goswami","year":"2023","journal-title":"Eur. J. Med. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"107106","DOI":"10.1016\/j.foodcont.2020.107106","article-title":"Prevalence of Multidrug-Resistant Staphylococcus aureus Isolates with Strong Biofilm Formation Ability among Animal-Based Food in Shanghai","volume":"112","author":"Ou","year":"2020","journal-title":"Food Control"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3168\/jds.2022-22267","article-title":"Invited Review: Antimicrobial Resistance in Bovine Mastitis Pathogens: A Review of Genetic Determinants and Prevalence of Resistance in European Countries","volume":"106","author":"Slowey","year":"2023","journal-title":"J. Dairy Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.prevetmed.2017.07.016","article-title":"Antibiotic Use by Farmers to Control Mastitis as Influenced by Health Advice and Dairy Farming Systems","volume":"146","author":"Poizat","year":"2017","journal-title":"Prev. Vet. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"125","DOI":"10.3109\/03009734.2014.905664","article-title":"Understanding and Changing Human Behaviour-Antibiotic Mainstreaming as an Approach to Facilitate Modification of Provider and Consumer Behaviour","volume":"119","author":"Lundborg","year":"2014","journal-title":"Ups. J. Med. Sci."},{"key":"ref_20","unstructured":"WHO (2014). Antimicrobial Resistance. Bull. World Health Organ., 61, 383\u2013394."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.rvsc.2023.05.016","article-title":"A Systematic Review and Meta-Analysis Revealed a High-Level Antibiotic Resistance of Bovine Mastitis Staphylococcus aureus in Iran","volume":"161","author":"Sharifi","year":"2023","journal-title":"Res. Vet. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"105032","DOI":"10.1016\/j.rvsc.2023.105032","article-title":"Antimicrobial Resistance of Streptococcus uberis Isolated from Bovine Mastitis: Systematic Review and Meta-Analysis","volume":"164","author":"Miotti","year":"2023","journal-title":"Res. Vet. Sci."},{"key":"ref_23","unstructured":"National Mastitis Council (2017). NMC Laboratory Handbook on Bovine Mastitis, National Mastitis Council."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2515","DOI":"10.3168\/jds.2018-15424","article-title":"Bovine Mastitis Bacteria Resolved by MALDI-TOF Mass Spectrometry","volume":"102","author":"Nonnemann","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0167-7012(00)00122-6","article-title":"A Modified Microtiter-Plate Test for Quantification of Staphylococcal Biofilm Formation","volume":"40","year":"2000","journal-title":"J. Microbiol. Methods"},{"key":"ref_26","unstructured":"CLSI (2021). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, Clinical and Laboratory Standards Institute. [3rd ed.]. CLSI Document M100-S25."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/j.vetmic.2009.12.013","article-title":"Assessing the Antimicrobial Susceptibility of Bacteria Obtained from Animals","volume":"141","author":"Schwarz","year":"2010","journal-title":"Vet. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"8607","DOI":"10.3168\/jds.2016-11310","article-title":"Investigation of the Antibiotic Resistance and Biofilm-Forming Ability of Staphylococcus aureus from Subclinical Bovine Mastitis Cases","volume":"99","author":"Demir","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.3168\/jds.2013-7387","article-title":"Biofilm-Producing Ability of Staphylococcus aureus Isolates from Brazilian Dairy Farms","volume":"97","author":"Lee","year":"2014","journal-title":"J. Dairy Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1080\/09168451.2015.1058701","article-title":"Environmental Factors That Shape Biofilm Formation","volume":"80","author":"Toyofuku","year":"2016","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"439","DOI":"10.5194\/aab-65-439-2022","article-title":"Antibiotic Resistance and Biofilm Formation in Staphylococcus aureus Isolated from Dairy Cows at the Stage of Subclinical Mastitis in Northern Kazakhstan","volume":"65","author":"Rychshanova","year":"2022","journal-title":"Arch. Anim. Breed."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"656810","DOI":"10.3389\/fvets.2021.656810","article-title":"Biofilm Research in Bovine Mastitis","volume":"8","author":"Pedersen","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"ref_33","first-page":"305","article-title":"Streptococcus uberis: In Vitro Biofilm Production in Response to Carbohydrates and Skim Milk","volume":"49","author":"Dieser","year":"2017","journal-title":"Rev. Argent. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1017\/S0022029923000158","article-title":"Biofilm Expression and Antimicrobial Resistance Patterns of Streptococcus uberis Isolated from Milk Samples of Dairy Cows in South Africa","volume":"90","author":"Magagula","year":"2023","journal-title":"J. Dairy Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1111\/jam.15362","article-title":"Capacity of Adherence, Invasion and Intracellular Survival of Streptococcus uberis Biofilm-forming Strains","volume":"132","author":"Moliva","year":"2022","journal-title":"J. Appl. Microbiol."},{"key":"ref_36","first-page":"273","article-title":"luxS Gene and Biofilm Formation in Streptococcus uberis Isolated from Bovine Mastitis Cases","volume":"40","author":"Greeshma","year":"2021","journal-title":"Asian J. Dairy Food Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1590\/1808-1657v74p0012007","article-title":"Sensibilidade Antimicrobiana Dos Staphylococcus aureus Isolados No Leite de Vacas Com Mastite","volume":"74","author":"Ferreira","year":"2007","journal-title":"Arq. Inst. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Kaczorek-\u0141ukowska, E., Ma\u0142aczewska, J., Sowi\u0144ska, P., Szyma\u0144ska, M., W\u00f3jcik, E.A., and Siwicki, A.K. (2022). Staphylococcus aureus from Subclinical Cases of Mastitis in Dairy Cattle in Poland, What Are They Hiding? Antibiotic Resistance and Virulence Profile. Pathogens, 11.","DOI":"10.3390\/pathogens11121404"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Freu, G., Tomazi, T., Filho, A.F.S., Heinemann, M.B., and Dos Santos, M.V. (2022). Antimicrobial Resistance and Molecular Characterization of Staphylococcus aureus Recovered from Cows with Clinical Mastitis in Dairy Herds from Southeastern Brazil. Antibiotics, 11.","DOI":"10.3390\/antibiotics11040424"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Jain, V.K., Singh, M., Joshi, V.G., Chhabra, R., Singh, K., and Rana, Y.S. (2022). Virulence and Antimicrobial Resistance Gene Profiles of Staphylococcus aureus Associated with Clinical Mastitis in Cattle. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0264762"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"McDougall, S., Clausen, L., Ha, H.J., Gibson, I., Bryan, M., Hadjirin, N., Lay, E., Raisen, C., Ba, X., and Restif, O. (2020). Mechanisms of \u03b2-Lactam Resistance of Streptococcus uberis Isolated from Bovine Mastitis Cases. Vet. Microbiol., 242.","DOI":"10.1016\/j.vetmic.2020.108592"},{"key":"ref_42","first-page":"1435","article-title":"Antimicrobial Resistance of Streptococcus uberis Isolated from Bovine Mastitis: A Review","volume":"56","author":"Zhang","year":"2022","journal-title":"Indian. J. Anim. Res."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Tomazi, T., Freu, G., Alves, B.G., de Souza Filho, A.F., Heinemann, M.B., and dos Santos, M.V. (2019). Genotyping and Antimicrobial Resistance of Streptococcus uberis Isolated from Bovine Clinical Mastitis. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0223719"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"4075","DOI":"10.3168\/jds.2008-1040","article-title":"Identification and Antimicrobial Resistance of Streptococcus uberis and Streptococcus parauberis Isolated from Bovine Milk Samples","volume":"91","author":"Koort","year":"2008","journal-title":"J. Dairy Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.vetmic.2014.02.045","article-title":"Antimicrobial Susceptibility and Distribution of Inhibition Zone Diameters of Bovine Mastitis Pathogens in Flanders, Belgium","volume":"171","author":"Lommelen","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"104937","DOI":"10.1016\/j.prevetmed.2020.104937","article-title":"Antimicrobial Use for Treatment of Clinical Mastitis in Dairy Herds from Brazil and Its Association with Herd-Level Descriptors","volume":"176","author":"Tomazi","year":"2020","journal-title":"Prev. Vet. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"12030","DOI":"10.3168\/jds.2021-20177","article-title":"Association between Antimicrobial Use and Antimicrobial Resistance of Streptococcus uberis Causing Clinical Mastitis","volume":"104","author":"Martins","year":"2021","journal-title":"J. Dairy Sci."}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/11\/4\/170\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:26:00Z","timestamp":1760106360000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/11\/4\/170"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,10]]},"references-count":47,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["vetsci11040170"],"URL":"https:\/\/doi.org\/10.3390\/vetsci11040170","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,10]]}}}