1887

Abstract

is responsible for severe skin and respiratory infections and food poisoning, resulting in hospitalizations and high morbidity worldwide. have extensive virulence mechanisms and antimicrobial resistance that pose a global challenge to contain the spread of infectious outbreaks. Antimicrobials are used as growth promoters, and for prevention and treatment of infections in animals that provide us with food. The improvement of animal health is undeniable, but the selection of multidrug-resistant strains that can spread resistance genes among microorganisms is undesirable. The administration of sublethal doses of antimicrobials in farm animals causes stress to inducing the formation of a complex extracellular polymeric structure called biofilm. Such a structure may favor the persistence of infection by disseminating antimicrobial-resistant strains that can be consumed in contaminated food of animal origin. In ruminant mastitis and hospitals, the potential of the biofilm structure in the persistence of infections, especially those caused by , has already been demonstrated, as well as its role as a source of resistant genes. In the meat production chain, the potential for persistent contamination by biofilm structure is evidently a worrying health risk . This review brings together studies demonstrating that biofilm production facilitates the exchange of mobile genetic elements and random mutations in strains within the structure. This contributes to the emergence of more resistant clonal complexes and, with biofilm support, persists in the meat production chain.

Funding
This study was supported by the:
  • Faperj
    • Principle Award Recipient: PedroPanzenhagen
  • CNPq
    • Principle Award Recipient: AnaCarolina Silva de Jesus
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001245
2022-10-06
2024-12-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/10/mic001245.html?itemId=/content/journal/micro/10.1099/mic.0.001245&mimeType=html&fmt=ahah

References

  1. Otto M, Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA. Staphylococcal Biofilms. Microbiol Spectr 2018; 6:207–228 [View Article]
    [Google Scholar]
  2. Gordon RJ, Lowy FD. Pathogenesis of methicillin‐resistant Staphylococcus aureus infection. CLIN INFECT DIS 2008; 46 Suppl 5:S350–S359 [View Article]
    [Google Scholar]
  3. Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and Staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014; 2014:1–9 [View Article]
    [Google Scholar]
  4. Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. Microbial biofilms in the food industry—a comprehensive review. Int J Environ Res Public Health 2021; 18:2014 [View Article]
    [Google Scholar]
  5. Lindsay JA. Genomic variation and evolution of Staphylococcus aureus . Int J Med Microbiol 2010; 300:98–103 [View Article]
    [Google Scholar]
  6. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009; 7:629–641 [View Article]
    [Google Scholar]
  7. Kong C, Neoh H, Nathan S. Targeting Staphylococcus aureus toxins: a potential form of anti-virulence therapy. Toxins 2016; 8:E72 [View Article]
    [Google Scholar]
  8. Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 2018; 31:e00020-18 [View Article]
    [Google Scholar]
  9. Vázquez-Sánchez D, Galvão JA, Oetterer M. Contamination sources, biofilm-forming ability and biocide resistance of Staphylococcus aureus in tilapia-processing facilities. Food Sci Technol Int 2018; 24:209–222 [View Article]
    [Google Scholar]
  10. Kranjec C, Morales Angeles D, Torrissen Mårli M, Fernández L, García P et al. Staphylococcal biofilms: challenges and novel therapeutic perspectives. Antibiotics 2021; 10:131 [View Article]
    [Google Scholar]
  11. Miao J, Lin S, Soteyome T, Peters BM, Li Y et al. Biofilm formation of Staphylococcus aureus under food heat processing conditions: first report on CML production within biofilm. Sci Rep 2019; 9:1312 [View Article]
    [Google Scholar]
  12. Lin Q, Sun H, Yao K, Cai J, Ren Y et al. The pPrevalence, aAntibiotic rResistance and bBiofilm formation of Staphylococcus aureus in bBulk rReady-tTo-eEat fFoods. Biomolecules 2019; 9:E524 [View Article]
    [Google Scholar]
  13. Hoveida L, Halaji M, Rostami S, Mobasherizadeh S. Biofilm-producing ability of Staphylococcus spp isolated from different foodstuff products. Ann Ig 2019; 31:140–147 [View Article]
    [Google Scholar]
  14. Aires-de-Sousa M. Methicillin-resistant Staphylococcus aureus among animals: current overview. Clin Microbiol Infect 2017; 23:373–380 [View Article]
    [Google Scholar]
  15. Di Ciccio P, Vergara A, Festino AR, Paludi D, Zanardi E et al. Biofilm formation by Staphylococcus aureus on food contact surfaces: relationship with temperature and cell surface hydrophobicity. Food Control 2015; 50:930–936 [View Article]
    [Google Scholar]
  16. Osman K, Alvarez-Ordóñez A, Ruiz L, Badr J, ElHofy F et al. Antimicrobial resistance and virulence characterization of Staphylococcus aureus and coagulase-negative staphylococci from imported beef meat. Ann Clin Microbiol Antimicrob 2017; 16:35 [View Article]
    [Google Scholar]
  17. Mirani ZA, Aziz M, Khan MN, Lal I, Hassan NU et al. Biofilm formation and dispersal of Staphylococcus aureus under the influence of oxacillin. Microb Pathog 2013; 61–62:66–72 [View Article]
    [Google Scholar]
  18. Giaouris E, Heir E, Desvaux M, Hébraud M, Møretrø T et al. Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front Microbiol 2015; 6:6 [View Article]
    [Google Scholar]
  19. Lindsay JA. Staphylococcus aureus genomics and the impact of horizontal gene transfer. Int J Med Microbiol 2014; 304:103–109 [View Article]
    [Google Scholar]
  20. Capita R, Alonso-Calleja C. Antibiotic-resistant bacteria: a challenge for the food industry. Crit Rev Food Sci Nutr 2013; 53:11–48 [View Article]
    [Google Scholar]
  21. Kelly BG, Vespermann A, Bolton DJ. Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens. Food Chem Toxicol 2009; 47:969–977 [View Article]
    [Google Scholar]
  22. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 2005; 187:2426–2438 [View Article]
    [Google Scholar]
  23. Boolchandani M, D’Souza AW, Dantas G. Sequencing-based methods and resources to study antimicrobial resistance. Nat Rev Genet 2019; 20:356–370 [View Article]
    [Google Scholar]
  24. Papadopoulos P, Papadopoulos T, Angelidis AS, Kotzamanidis C, Zdragas A et al. Prevalence, antimicrobial susceptibility and characterization of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus isolated from dairy industries in north-central and north-eastern Greece. Int J Food Microbiol 2019; 291:35–41 [View Article]
    [Google Scholar]
  25. Savage VJ, Chopra I, O’Neill AJ. Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrob Agents Chemother 2013; 57:1968–1970 [View Article]
    [Google Scholar]
  26. Gross M, Cramton SE, Götz F, Peschel A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 2001; 69:3423–3426 [View Article]
    [Google Scholar]
  27. Von CE, Heilmann C, Peters G. New aspects in the molecular basis of polymer-associated infections due to staphylococci. Eur J Clin Microbiol Infect Dis 1999; 18:843–846 [View Article]
    [Google Scholar]
  28. Otto M. Bacterial evasion of antimicrobial peptides by biofilm formation antimicrobial peptides and human disease. In Current Topics in Microbiology and Immunology vol 306 2006 pp 251–258 [View Article]
    [Google Scholar]
  29. Speziale P, Pietrocola G, Foster TJ, Geoghegan JA. Protein-based biofilm matrices in Staphylococci . Front Cell Infect Microbiol 2014; 4:4 [View Article]
    [Google Scholar]
  30. Mazmanian SK, Liu G, Ton-That H, Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 1999; 285:760–763 [View Article]
    [Google Scholar]
  31. Marques SC, Rezende J das GOS, Alves LA de F, Silva BC, Alves E et al. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Braz J Microbiol 2000; 38:538–543 [View Article]
    [Google Scholar]
  32. Ton-That H, Mazmanian SK, Faull KF, Schneewind O. Anchoring of surface proteins to the cell wall of Staphylococcus aureus . J Biol Chem 2000; 275:9876–9881 [View Article]
    [Google Scholar]
  33. Maira-Litrán T, Kropec A, Abeygunawardana C, Joyce J, Mark G et al. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 2002; 70:4433–4440 [View Article]
    [Google Scholar]
  34. O’Gara JP. Ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus . FEMS Microbiol Lett 2007; 270:179–188 [View Article]
    [Google Scholar]
  35. Oniciuc E-A, Cerca N, Nicolau AI. Compositional analysis of biofilms formed by Staphylococcus aureus isolated from food sources. Front Microbiol 2016; 7:7 [View Article]
    [Google Scholar]
  36. Gutiérrez D, Delgado S, Vázquez-Sánchez D, Martínez B, Cabo ML et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 2012; 78:8547–8554 [View Article] [PubMed]
    [Google Scholar]
  37. Cucarella C, Solano C, Valle J, Amorena B, Lasa I et al. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 2001; 183:2888–2896 [View Article]
    [Google Scholar]
  38. Dai J, Wu S, Huang J, Wu Q, Zhang F et al. Prevalence and characterization of Staphylococcus aureus isolated from pasteurized milk in China. Front Microbiol 2019; 10:641 [View Article]
    [Google Scholar]
  39. Achek R, Hotzel H, Nabi I, Kechida S, Mami D et al. Phenotypic and molecular detection of biofilm formation in Staphylococcus aureus isolated from different sources in Algeria. Pathogens 2020; 9:E153 [View Article]
    [Google Scholar]
  40. Zhang D-X, Li Y, Yang X-Q, Su H-Y, Wang Q et al. In vitro antibiotic susceptibility, virulence genes distribution and biofilm production of Staphylococcus aureus isolates from bovine mastitis in the liaoning province of China. Infect Drug Resist 2020; 13:1365–1375 [View Article]
    [Google Scholar]
  41. Schilcher K, Andreoni F, Dengler Haunreiter V, Seidl K, Hasse B et al. Modulation of Staphylococcus aureus biofilm matrix by subinhibitory concentrations of clindamycin. Antimicrob Agents Chemother 2016; 60:5957–5967 [View Article]
    [Google Scholar]
  42. Wesgate R, Grasha P, Maillard J-Y. Use of a predictive protocol to measure the antimicrobial resistance risks associated with biocidal product usage. Am J Infect Control 2016; 44:458–464 [View Article]
    [Google Scholar]
  43. Condell O, Iversen C, Cooney S, Power KA, Walsh C et al. Efficacy of biocides used in the modern food industry to control salmonella enterica, and links between biocide tolerance and resistance to clinically relevant antimicrobial compounds. Appl Environ Microbiol 2012; 78:3087–3097 [View Article]
    [Google Scholar]
  44. González-Rivas F, Ripolles-Avila C, Fontecha-Umaña F, Ríos-Castillo AG, Rodríguez-Jerez JJ. Biofilms in the spotlight: detection, quantification, and removal methods. Compr Rev Food Sci Food Saf 2018; 17:1261–1276 [View Article]
    [Google Scholar]
  45. Vergara A, Normanno G, Di Ciccio P, Pedonese F, Nuvoloni R et al. Biofilm formation and its relationship with the molecular characteristics of food-related methicillin-resistant Staphylococcus aureus (MRSA). J Food Sci 2017; 82:2364–2370 [View Article]
    [Google Scholar]
  46. Osman KM, Amer AM, Badr JM, Helmy NM, Elhelw RA et al. Antimicrobial resistance, biofilm formation and mecA characterization of methicillin-susceptible S Aureus and Non-S. Aureus of beef meat origin in Egypt. Front Microbiol 2016; 7:222 [View Article]
    [Google Scholar]
  47. Ou C, Shang D, Yang J, Chen B, Chang J et al. Prevalence of multidrug-resistant Staphylococcus aureus isolates with strong biofilm formation ability among animal-based food in Shanghai. Food Control 2020; 112:107106 [View Article]
    [Google Scholar]
  48. Hamadi F, Asserne F, Elabed S, Bensouda S, Mabrouki M et al. Adhesion of Staphylococcus aureus on stainless steel treated with three types of milk. Food Control 2014; 38:104–108 [View Article]
    [Google Scholar]
  49. Rubio C, Costa D, Bellon-Fontaine MN, Relkin P, Pradier CM et al. Characterization of bovine serum albumin adsorption on chromium and AISI 304 stainless steel, consequences for the Pseudomonas fragi K1 adhesion. Colloids Surf B Biointerfaces 2002; 24:193–205 [View Article]
    [Google Scholar]
  50. Pagedar A, Singh J, Batish VK. Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. J Basic Microbiol 2010; 50 Suppl 1:S98–106 [View Article]
    [Google Scholar]
  51. Oulahal N, Brice W, Martial A, Degraeve P. Quantitative analysis of survival of Staphylococcus aureus or Listeria innocua on two types of surfaces: polypropylene and stainless steel in contact with three different dairy products. Food Control 2008; 19:178–185 [View Article]
    [Google Scholar]
  52. Rode TM, Langsrud S, Holck A, Møretrø T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 2007; 116:372–383 [View Article]
    [Google Scholar]
  53. Rabello RF, Bonelli RR, Penna BA, Albuquerque JP, Souza RM et al. Antimicrobial resistance in farm animals in Brazil: an update overview. Animals 2020; 10:552 [View Article]
    [Google Scholar]
  54. Verraes C, Van Boxstael S, Van Meervenne E, Van Coillie E, Butaye P et al. Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health 2013; 10:2643–2669 [View Article]
    [Google Scholar]
  55. Depoorter P, Persoons D, Uyttendaele M, Butaye P, De Zutter L et al. Assessment of human exposure to 3rd generation cephalosporin resistant E. coli (CREC) through consumption of broiler meat in Belgium. Int J Food Microbiol 2012; 159:30–38 [View Article]
    [Google Scholar]
  56. Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 2014; 12:465–478 [View Article]
    [Google Scholar]
  57. de Souza EL, Meira QGS, de Medeiros Barbosa I, Athayde AJAA, da Conceição ML et al. Biofilm formation by Staphylococcus aureus from food contact surfaces in a meat-based broth and sensitivity to sanitizers. Braz J Microbiol 2014; 45:67–75 [View Article]
    [Google Scholar]
  58. Vázquez-Sánchez D, Habimana O, Holck A. Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Curr Microbiol 2013; 66:110–121 [View Article]
    [Google Scholar]
  59. Cirz RT, Romesberg FE. Induction and inhibition of ciprofloxacin resistance-conferring mutations in hypermutator bacteria. Antimicrob Agents Chemother 2006; 50:220–225 [View Article]
    [Google Scholar]
  60. Cirz RT, Jones MB, Gingles NA, Minogue TD, Jarrahi B et al. Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J Bacteriol 2007; 189:531–539 [View Article]
    [Google Scholar]
  61. Gemmell CG, Ford CW. Virulence factor expression by gram-positive cocci exposed to subinhibitory concentrations of linezolid. J Antimicrob Chemother 2002; 50:665–672 [View Article]
    [Google Scholar]
  62. Queck SY, Khan BA, Wang R, Bach T-HL, Kretschmer D et al. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog 2009; 5:e1000533 [View Article]
    [Google Scholar]
  63. Clements MO, Watson SP, Foster SJ. Characterization of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. J Bacteriol 1999; 181:3898–3903 [View Article]
    [Google Scholar]
  64. Park S, You X, Imlay JA. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli . Proc Natl Acad Sci 2005; 102:9317–9322 [View Article]
    [Google Scholar]
  65. Boles BR, Singh PK. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci 2008; 105:12503–12508 [View Article]
    [Google Scholar]
  66. Ryder VJ, Chopra I, O’Neill AJ. Increased mutability of Staphylococci in biofilms as a consequence of oxidative stress. PLoS One 2012; 7:e47695 [View Article]
    [Google Scholar]
  67. Michel B. After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol 2005; 3:e255 [View Article]
    [Google Scholar]
  68. Mesak LR, Miao V, Davies J. Effects of subinhibitory concentrations of antibiotics on SOS and DNA repair gene expression in Staphylococcus aureus . Antimicrob Agents Chemother 2008; 52:3394–3397 [View Article]
    [Google Scholar]
  69. Maiques E, Ubeda C, Campoy S, Salvador N, Lasa I et al. Beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus . J Bacteriol 2006; 188:2726–2729 [View Article]
    [Google Scholar]
  70. Nagel M, Reuter T, Jansen A, Szekat C, Bierbaum G. Influence of ciprofloxacin and vancomycin on mutation rate and transposition of IS256 in Staphylococcus aureus . Int J Med Microbiol 2011; 301:229–236 [View Article]
    [Google Scholar]
  71. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP et al. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci . Mol Microbiol 2005; 56:836–844 [View Article]
    [Google Scholar]
  72. Abbasi K, Tajbakhsh E, Momtaz H. Antimicrobial resistance and biofilm encoding genes amongst the Staphylococcus aureus bacteria isolated from meat and meat products. NIDOC-ASRT 2021; 52:55–62 [View Article]
    [Google Scholar]
  73. Pekana A, Green E. Antimicrobial resistance profiles of Staphylococcus aureus isolated from meat carcasses and bovine milk in abattoirs and dairy farms of the eastern cape, South Africa. Int J Environ Res Public Health 2018; 15:10 [View Article]
    [Google Scholar]
  74. Overview of global meat market developments in 2019. FAO 202011
    [Google Scholar]
  75. Andrzejewska M, Szczepańska B, Śpica D, Klawe JJ. Prevalence, virulence, and antimicrobial resistance of campylobacter spp. in raw milk, beef, and pork eat in northern poland. Foods 2019; 8: E420 [View Article]
    [Google Scholar]
  76. Schelin J, Susilo YB, Johler S. Expression of Staphylococcal enterotoxins under stress encountered during food production and preservation. Toxins 2017; 9:401 [View Article]
    [Google Scholar]
  77. Lin Q, Sun H, Yao K, Cai J, Ren Y et al. The prevalence, antibiotic resistance and biofilm formation of Staphylococcus aureus in bulk ready-to-eat foods. Biomolecules 2019; 9:E524 [View Article]
    [Google Scholar]
  78. Zhang Y, Xu D, Shi L, Cai R, Li C et al. Association between agr type, virulence factors, biofilm formation and antibiotic resistance of Staphylococcus aureus isolates from pork production. Front Microbiol 2018; 9:1876 [View Article]
    [Google Scholar]
  79. Abdalrahman LS, Stanley A, Wells H, Fakhr MK. Isolation, virulence, and antimicrobial resistance of methicillin-resistant Staphylococcus aureus (MRSA) and methicillin sensitive Staphylococcus aureus (MSSA) strains from Oklahoma retail poultry meats. Int J Environ Res Public Health 2015; 12:6148–6161 [View Article]
    [Google Scholar]
  80. Castaño-Arriba A, González-Machado C, Igrejas G, Poeta P, Alonso-Calleja C et al. Antibiotic resistance and biofilm-forming ability in Enterococcal isolates from red meat and poultry preparations. Pathogens 2020; 9:12 [View Article]
    [Google Scholar]
  81. Elsayed MM, Elgohary FA, Zakaria AI, Elkenany RM, El-Khateeb AY. Novel eradication methods for Staphylococcus aureus biofilm in poultry farms and abattoirs using disinfectants loaded onto silver and copper nanoparticles. Environ Sci Pollut Res Int 2020; 27:30716–30728 [View Article]
    [Google Scholar]
  82. Bennett SD, Walsh KA, Gould LH. Foodborne disease outbreaks caused by bacillus cereus, clostridium perfringens, and Staphylococcus aureus--United States, 1998-2008. Clin Infect Dis 2013; 57:425–433 [View Article]
    [Google Scholar]
  83. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis 2011; 17:7–15 [View Article]
    [Google Scholar]
  84. Torki Baghbaderani Z, Shakerian A, Rahimi E. Phenotypic and genotypic assessment of antibiotic resistance of Staphylococcus aureus bacteria isolated from retail meat. Infect Drug Resist 2020; 13:1339–1349 [View Article]
    [Google Scholar]
  85. Rodríguez-Lázaro D, Alonso-Calleja C, Oniciuc EA, Capita R, Gallego D et al. Characterization of biofilms formed by foodborne methicillin-resistant Staphylococcus aureus . Front Microbiol 2018; 9:3004 [View Article]
    [Google Scholar]
  86. Parisi A, Caruso M, Normanno G, Latorre L, Sottili R et al. Prevalence, antimicrobial susceptibility and molecular typing of methicillinr resistant Staphylococcus aureus (MRSA) in bulk tank milk from southern Italy. Food Microbiol 2016; 58:36–42 [View Article]
    [Google Scholar]
  87. Wu D, Wang H, Zhu F, Jiang S, Sun L et al. Characterization of an ST5-SCCmec II-T311 methicillin-resistant Staphylococcus aureus strain with a widespread cfr-positive plasmid. J Infect Chemother 2020; 26:699–705 [View Article]
    [Google Scholar]
  88. Shen J, Wang Y, Schwarz S. Presence and dissemination of the multiresistance gene cfr in gram-positive and gram-negative bacteria. J Antimicrob Chemother 2013; 68:1697–1706 [View Article]
    [Google Scholar]
  89. Osman K, Badr J, Al-Maary KS, Moussa IMI, Hessain AM et al. Prevalence of the antibiotic resistance genes in coagulase-positive-and negative-Staphylococcus in chicken meat retailed to consumers. Front Microbiol 2016; 7:1846 [View Article]
    [Google Scholar]
  90. Mulders MN, Haenen APJ, Geenen PL, Vesseur PC, Poldervaart ES et al. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in the Netherlands. Epidemiol Infect 2010; 138:743–755 [View Article]
    [Google Scholar]
  91. van Rijen MML, Van Keulen PH, Kluytmans JA. Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to animal farming. Clin Infect Dis 2008; 46:261–263 [View Article]
    [Google Scholar]
  92. Rao RT, Sharma S, Sivakumar N, Jayakumar K. Genomic islands and the evolution of livestock-associated Staphylococcus aureus genomes. Biosci Rep 2020; 40:13 [View Article]
    [Google Scholar]
  93. Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus . Proc Natl Acad Sci U S A 2009; 106:19545–19550 [View Article]
    [Google Scholar]
  94. Okorie-Kanu OJ, Anyanwu MU, Ezenduka EV, Mgbeahuruike AC, Thapaliya D et al. Molecular epidemiology, genetic diversity and antimicrobial resistance of Staphylococcus aureus isolated from chicken and pig carcasses, and carcass handlers. PLoS One 2020; 15:e0232913 [View Article]
    [Google Scholar]
  95. Shittu AO, Okon K, Adesida S, Oyedara O, Witte W et al. Antibiotic resistance and molecular epidemiology of Staphylococcus aureus in Nigeria. BMC Microbiol 2011; 11:92 [View Article]
    [Google Scholar]
  96. Nulens E, Stobberingh EE, van Dessel H, Sebastian S, van Tiel FH et al. Molecular characterization of Staphylococcus aureus bloodstream isolates collected in a Dutch university hospital between 1999 and 2006. J Clin Microbiol 2008; 46:2438–2441 [View Article]
    [Google Scholar]
  97. Fagerlund A, Langsrud S, Heir E, Mikkelsen MI, Møretrø T. Biofilm matrix composition affects the susceptibility of food associated Staphylococci to cleaning and disinfection agents. Front Microbiol 2016; 7:7 [View Article]
    [Google Scholar]
  98. Mesa Varona O, Chaintarli K, Muller-Pebody B, Anjum MF, Eckmanns T et al. Monitoring antimicrobial resistance and drug usage in the human and livestock sector and foodborne antimicrobial resistance in six European countries. Infect Drug Resist 2020; 13:957–993 [View Article]
    [Google Scholar]
  99. Pérez VKC, Custódio DAC, Silva EMM, de Oliveira J, Guimarães AS et al. Virulence factors and antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis in Brazil. Braz J Microbiol 2020; 51:2111–2122 [View Article]
    [Google Scholar]
  100. Novick RP, Schlievert P, Ruzin A. Pathogenicity and resistance islands of staphylococci . Microbes Infect 2001; 3:585–594 [View Article]
    [Google Scholar]
  101. Lee H-W, Yoon S-R, Kim S-J, Lee HM, Lee JY et al. Identification of microbial communities, with a focus on foodborne pathogens, during kimchi manufacturing process using culture-independent and -dependent analyses. LWT - Food Science and Technology 2017; 81:153–159 [View Article]
    [Google Scholar]
  102. Gavrilova E, Anisimova E, Gabdelkhadieva A, Nikitina E, Vafina A et al. Newly isolated lactic acid bacteria from silage targeting biofilms of foodborne pathogens during milk fermentation. BMC Microbiol 2019; 19:248 [View Article]
    [Google Scholar]
  103. Founou LL, Founou RC, Essack SY. Antibiotic resistance in the food chain: a developing country-erspective. Front Microbiol 2016; 7:7 [View Article]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.001245
Loading
/content/journal/micro/10.1099/mic.0.001245
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error