{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T05:25:29Z","timestamp":1768281929160,"version":"3.49.0"},"reference-count":47,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2018,2,19]],"date-time":"2018-02-19T00:00:00Z","timestamp":1518998400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Antibiotic resistance poses an important threat to global public health and has become a challenge to modern medicine. The occurrence of antibiotic-resistant bacteria in a broad range of foods has led to a growing concern about the impact that food may have as a reservoir of antibiotic resistance genes. Considering Minas Frescal Cheese (MFC)\u2014a typical Brazilian white soft cheese\u2014and its economic and cultural values, in this study, medically relevant antimicrobial-resistance genetic markers (AR genes) were screened, and the occurrence of integrons were evaluated in manufactured MFC using culture-independent approaches. Through a fingerprinting analysis, the tested MFCs were brand-clustered, indicating reproducibility along the production chain. A common core of resistance markers in all brands evaluated and related antimicrobials such as \u03b2-lactams, tetracyclines, quinolones, and sulfonamide was detected. Several other markers, including efflux pumps and aminoglycosides-resistance were distributed among brands. Class 1 and 2 integrons were observed, respectively, in 77% and 97% of the samples. The presence of AR genes is of special interest due to their clinical relevance. Taken together, the data may suggest that the production chain of MFC might contribute to the spread of putative drug-resistant bacteria, which could greatly impact human health. Furthermore, detection of class 1 and class 2 integrons in MFC has led to discussions about resistance gene spread in this traditional cheese, providing evidence of potential horizontal transfer of AR genes to human gut microbiota.<\/jats:p>","DOI":"10.3390\/genes9020106","type":"journal-article","created":{"date-parts":[[2018,2,20]],"date-time":"2018-02-20T03:54:22Z","timestamp":1519098862000},"page":"106","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Antibiotic Resistance Genetic Markers and Integrons in White Soft Cheese: Aspects of Clinical Resistome and Potentiality of Horizontal Gene Transfer"],"prefix":"10.3390","volume":"9","author":[{"given":"Ana Caroline","family":"De Paula","sequence":"first","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julliane","family":"Medeiros","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Analice","family":"De Azevedo","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J\u00e9ssica","family":"De Assis Chagas","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"V\u00e2nia","family":"Da Silva","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6882-8312","authenticated-orcid":false,"given":"Cl\u00e1udio","family":"Diniz","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Institute of Biological Sciences, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2018,2,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.nmni.2015.02.007","article-title":"The global threat of antimicrobial resistance: Science for intervention","volume":"6","author":"Roca","year":"2015","journal-title":"New Microbes New Infect."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1177\/003335491212700103","article-title":"A Review of antibiotic use in food animals: Perspective, policy, and potential","volume":"127","author":"Landers","year":"2012","journal-title":"Public Health Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2016.01881","article-title":"Antibiotic resistance in the food chain: A developing country-perspective","volume":"7","author":"Founou","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.cofs.2017.01.010","article-title":"Antibiotic resistance in the food supply chain: Where can sequencing and metagenomics aid risk assessment?","volume":"14","year":"2017","journal-title":"Curr. Opin. Food Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2643","DOI":"10.3390\/ijerph10072643","article-title":"Antimicrobial resistance in the food chain: A review","volume":"10","author":"Verraes","year":"2013","journal-title":"Int. J.  Environ. Res. Public Health"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1089\/fpd.2014.1865","article-title":"Multidrug-resistant pathogens in the food supply","volume":"12","author":"Doyle","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"167","DOI":"10.2147\/IDR.S48820","article-title":"Horizontal gene transfer in the human gastrointestinal tract: Potential spread of antibiotic resistance genes","volume":"7","author":"Huddleston","year":"2014","journal-title":"Infect. Drug Resist."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1007\/s12263-011-0226-x","article-title":"Antibiotic resistance determinants in the interplay between food and gut microbiota","volume":"6","author":"Devirgiliis","year":"2011","journal-title":"Genes Nutr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2013.00173","article-title":"Food and human gut as reservoirs of transferable antibiotic resistance encoding genes","volume":"4","author":"Rolain","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_10","first-page":"1","article-title":"Acquired antibiotic resistance genes: An overview","volume":"2","author":"Mevius","year":"2011","journal-title":"Front. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1128\/MMBR.00056-13","article-title":"Integrons: Past, present, and future","volume":"78","author":"Gillings","year":"2014","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/s12941-015-0100-6","article-title":"Resistance integrons: Class 1, 2 and 3 integrons","volume":"14","author":"Deng","year":"2015","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.ijfoodmicro.2005.03.008","article-title":"Antibiotic resistance in food lactic acid bacteria\u2014A review","volume":"105","author":"Mathur","year":"2005","journal-title":"Int. J. Food Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1089\/fpd.2012.1222","article-title":"Microbiological food safety issues in Brazil: Bacterial pathogens","volume":"10","author":"Gomes","year":"2013","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.foodcont.2005.10.005","article-title":"The quality of Minas Frescal cheese produced by different technological processes","volume":"18","author":"Carvalho","year":"2007","journal-title":"Food Control"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4954","DOI":"10.1128\/AEM.01828-07","article-title":"Retail survey of Brazilian milk and Minas Frescal cheese and a contaminated dairy plant to establish prevalence, relatedness, and sources of Listeria monocytogenes isolates","volume":"74","author":"Brito","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"8","DOI":"10.53393\/rial.2011.v70.32584","article-title":"Queijo Minas Frescal: Perfil higi\u00eanico-sanit\u00e1rio e avalia\u00e7\u00e3o da rotulagem","volume":"70","author":"Visotto","year":"2011","journal-title":"Rev. Inst. Adolfo Lutz"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1111\/1750-3841.12088","article-title":"Prevalence, antimicrobial resistance, and virulence characteristics of mecA-encoding coagulase-negative Staphylococci isolated from soft cheese in Brazil","volume":"78","author":"Fontes","year":"2013","journal-title":"J. Food Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2641","DOI":"10.3168\/jds.2015-9693","article-title":"Identification and molecular phylogeny of coagulase-negative staphylococci isolates from Minas Frescal cheese in southeastern Brazil: Superantigenic toxin production and antibiotic resistance","volume":"99","author":"Nunes","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Bel\u00e9n Fl\u00f3rez, A., Alegr\u00eda, \u00c1., Rossi, F., Delgado, S., Felis, G.E., Torriani, S., and Mayo, B. (2014). Molecular identification and quantification of tetracycline and erythromycin resistance genes in Spanish and Italian retail cheeses. BioMed Res. Int.","DOI":"10.1155\/2014\/746859"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.3390\/ijms10041538","article-title":"Resistance to \u03b2-lactams in bacteria isolated from different types of Portuguese cheese","volume":"10","author":"Amador","year":"2009","journal-title":"Int. J. Mol. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"175","DOI":"10.4236\/aim.2014.43023","article-title":"Antimicrobial resistance in Enterococcus sp isolated from soft cheese in Southern Brazil","volume":"4","author":"Rocha","year":"2014","journal-title":"Adv. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2675","DOI":"10.3168\/jds.2015-10725","article-title":"Short communication: Prevalence, antimicrobial resistance, and resistant traits of coagulase-negative staphylococci isolated from cheese samples in Turkey","volume":"99","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"138","DOI":"10.3389\/fmicb.2013.00138","article-title":"The antibiotic resistance \u201cmobilome\u201d: Searching for the link between environment and clinic","volume":"4","author":"Perry","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_25","first-page":"12","article-title":"In vitro antimicrobial comparison of Taif and Egyptian Pomegranate Peels and seeds extracts","volume":"3","author":"Gaber","year":"2015","journal-title":"J. Appl. Biol. Biotechnol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.fm.2017.02.005","article-title":"Bacterial ecology of artisanal Minas cheeses assessed by culture-dependent and -independent methods","volume":"65","author":"Perin","year":"2017","journal-title":"Food Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.ijfoodmicro.2015.08.006","article-title":"Microbiota of Minas cheese as influenced by the nisin producer Lactococcus lactis subsp. lactis GLc05","volume":"214","author":"Perin","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.ijfoodmicro.2008.09.021","article-title":"Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana","volume":"128","author":"Devirgiliis","year":"2008","journal-title":"Int. J. Food Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Grossman, T.H. (2016). Tetracycline antibiotics and resistance. Cold Spring Harb. Perspect. Med., 6.","DOI":"10.1101\/cshperspect.a025387"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1555","DOI":"10.1128\/AEM.70.3.1555-1562.2004","article-title":"Prevalence and molecular characterization of tetracycline resistance in Enterococcus isolates from food","volume":"70","author":"Huys","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Devirgiliis, C., Zinno, P., Stirpe, M., Barile, S., and Perozzi, G. (2014). Functional screening of antibiotic resistance genes from a representative metagenomic library of food fermenting microbiota. BioMed Res. Int., 1\u20139.","DOI":"10.1155\/2014\/290967"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.idairyj.2014.10.009","article-title":"Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy","volume":"42","author":"Carfora","year":"2015","journal-title":"Int. Dairy J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.foodcont.2015.02.013","article-title":"Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products","volume":"54","author":"Jamali","year":"2006","journal-title":"Food Control"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.ijfoodmicro.2011.10.015","article-title":"Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep\u2019s milk cheese","volume":"153","author":"Spanu","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1007\/s00253-015-7184-y","article-title":"Emerging resistance to aminoglycosides in lactic acid bacteria of food origin\u2014An impending menace","volume":"100","author":"Jaimee","year":"2016","journal-title":"App. Microbiol. Biotechnol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s10156-010-0120-2","article-title":"Plasmid-mediated quinolone resistance: An update","volume":"17","author":"Cano","year":"2011","journal-title":"J. Infect. Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.scitotenv.2008.06.023","article-title":"Detection of the sul1, sul2, and sul3 genes in sulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam","volume":"405","author":"Nonaka","year":"2008","journal-title":"Sci. Total Environ."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1054\/drup.2000.0146","article-title":"Sulfonamide resistance: Mechanisms and trends","volume":"3","year":"2000","journal-title":"Drug Resist. Updat."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrmicro1464","article-title":"Multidrug-resistance efflux pumps\u2014Not just for resistance","volume":"4","author":"Piddock","year":"2006","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Blanco, P., Hernando-Amado, S., Reales-Calderon, J.A., Corona, F., Lira, F., Alcalde-Rico, M., Bernardini, A., Sanchez, M.B., and Martinez, J.L. (2016). Bacterial multidrug efflux pumps: Much more than antibiotic resistance determinants. Microorganisms, 4.","DOI":"10.3390\/microorganisms4010014"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1761","DOI":"10.1128\/AAC.45.6.1761-1770.2001","article-title":"Multidrug efflux pumps: Expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms","volume":"45","author":"Kievit","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2807","DOI":"10.1128\/AAC.49.7.2807-2815.2005","article-title":"Sixteen homologs of the Mex-type multidrug resistance efflux pump in Bacteroides fragilis","volume":"49","author":"Ueda","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"147","DOI":"10.11606\/issn.1678-4456.bjvras.2017.118547","article-title":"Commonly screened antibiotics in raw milk from dairy plants under State Inspection in Rio Grande do Sul, Brazil","volume":"57","author":"Galvani","year":"2017","journal-title":"Braz. J. Vet. Res. Anim. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1146\/annurev-genet-102209-163504","article-title":"Integrons","volume":"44","author":"Cambray","year":"2010","journal-title":"Ann. Rev. Genet."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1038\/nrmicro1462","article-title":"Integrons: Agents of bacterial evolution","volume":"4","author":"Mazel","year":"2006","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1111\/j.1574-6976.2009.00175.x","article-title":"Gene cassettes and cassette arrays in mobile resistance integrons: Review article","volume":"33","author":"Partridge","year":"2009","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.ijfoodmicro.2014.07.031","article-title":"Characterization of integrons and resistance genes in multidrug-resistant Salmonella enterica isolated from meat and dairy products in Egypt","volume":"189","author":"Ahmed","year":"2014","journal-title":"Int. J. Food Microbiol."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/2\/106\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T14:55:38Z","timestamp":1760194538000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/2\/106"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,2,19]]},"references-count":47,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2018,2]]}},"alternative-id":["genes9020106"],"URL":"https:\/\/doi.org\/10.3390\/genes9020106","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,2,19]]}}}