Research Article
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Investigation of Biofilm Forming Abilities of Slaughterhouse and Dairy Originated Pathogenic Bacteria by Congo Red Agar and Microplate Methods

Year 2023, , 18 - 26, 30.06.2023
https://doi.org/10.58833/bozokvetsci.1287983

Abstract

In this study, a comparison of the efficacy and sensitivity of Congo Red Agar (CCA) and Microplate (MP) methods in determining the biofilm-forming abilities of Staphylococcus aureus, Listeria spp, Escherichia coli, and Salmonella spp isolates isolated from slaughterhouses and dairy farms and posing a risk to public health was intended. It was found that 51.1% of 135 isolates were identified as biofilm producers in CCA and 53% in MP. Among the isolates analysed, the CCA method's sensitivity was highest in S. aureus (97%), followed by Listeria spp. (59%), Salmonella spp (17%). and E. coli (13%). The specificity rates were 89%, 59% and 39% for E. coli, Salmonella spp. and Listeria spp., respectively. However, since all S. aureus isolates gave positive biofilm results in the MP test, the specificity of CCA could not be determined for this isolate. As a result, the sensitivity of the CCA method was higher only for S. aureus among the analysed isolates, while the selectivity of this method was good for other isolates. It is important to accurately determine the biofilm abilities of pathogen strains that may pose a risk to public health in food and food processing environments. Therefore, it was concluded that the complementary application of CCA with the MP method is important for the reliability of the results and the detection of biofilms.

References

  • 1. Flemming HC, Wingender J. The biofilm matrix. Nature Reviews Microbiology 2010; 8:623–33. doi: 10.1038/nrmicro2415.
  • 2. Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. Microbial Biofilms in the Food Industry—A Comprehensive Review. International Journal of Environmental Research and Public Health 2021; 18: 1–31. doi:10.3390/IJERPH18042014.
  • 3. Srinivasan R, Santhakumari S, Poonguzhali P, Geetha M, Dyavaiah M, Xiangmin L. Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections. Frontiers in Microbiology 2021; 12, 1106. doi: 10.3389/FMICB.2021.676458/BIBTEX.
  • 4. Kartal MO, Ekinci MB, Poyraz B. Biyofilm Yapısı ve Önlenmesi. Akademik Gıda 2021; 19, 353-63. doi: 10.24323/akademik-gida.1011231.
  • 5. Gupta P, Gupta H, Poluri KM. Geraniol eradicates Candida glabrata biofilm by targeting multiple cellular pathways. Applied Microbial and Cell Physiology 2021; 105, 5589-605. doi: 10.1007/s00253-021-11397-6.
  • 6. Gebreyohannes G, Nyerere A, Bii C, Sbhatu DB. Challenges of intervention, treatment, and antibiotic resistance of biofilm-forming microorganisms. Heliyon 2019;5: e02192. doi: 10.1016/J.HELIYON. 2019.E02192. 7. Abebe GM. The Role of Bacterial Biofilm in Antibiotic Resistance and Food Contamination. Int J Microbiol 2020;2020. doi: 10.1155/2020/1705814.
  • 8. Cepas V, López Y, Muñoz E, Rolo D, Ardanuy C, Martí S, et al. Relationship between Biofilm Formation and Antimicrobial Resistance in Gram-Negative Bacteria. Microbial Drug Resistance 2019; 25:72–9. doi: 10.1089/MDR.2018.0027.
  • 9. Myszka K, Czaczyk K. Bacterial biofilms on food contact surfaces - a review. Pol J Food Nutr Sci 2011; 61. doi: 10.2478/v10222-011-0018-4.
  • 10. Costerton JW, Montanaro L, Arciola CR. Biofilm in Implant Infections: Its Production and Regulation 2018;28:1062–8. doi: 10.1177/039139880502801103.
  • 11. Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15:167–93. doi: 10.1128/CMR.15.2.167-193.2002.
  • 12. Algburi A, Comito N, Kashtanov D, Dicks LMT, Chikindas ML. Control of biofilm formation: Antibiotics and beyond. Appl Environ Microbiol 2017;83. doi: 10.1128/AEM.02508-16.
  • 13. Dufour D, Leung V, Lévesque CM. Bacterial biofilm: structure, function, and antimicrobial resistance. Endod Topics 2010; 22:2–16. doi: 10.1111/J.1601-1546.2012.00277.X.
  • 14. Olanbiwoninu AA, Popoola BM. Biofilms and their impact on the food industry. Saudi J Biol Sci 2023;30. doi: 10.1016/J.SJBS.2022.103523.
  • 15. Achek R, Hotzel H, Nabi I, Kechida S, Mami D, Didouh N, et al. Phenotypic and Molecular Detection of Biofilm Formation in Staphylococcus aureus Isolated from Different Sources in Algeria. Pathogens 2020; 9:153. doi: 10.3390/PATHOGENS9020153.
  • 16. Agostinho Davanzo EF, Dos Santos RL, Castro VH de L, Palma JM, Pribul BR, Dallago BSL, et al. Molecular characterization of Salmonella spp. and Listeria monocytogenes strains from biofilms in cattle and poultry slaughterhouses located in the federal District and State of Goiás, Brazil. PLoS One 2021;16:e0259687. doi: 10.1371/JOURNAL.PONE.0259687.
  • 17. Bhardwaj DK, Taneja NK, DP S, Chakotiya A, Patel P, Taneja P, et al. Phenotypic and genotypic characterization of biofilm forming, antimicrobial resistant, pathogenic Escherichia coli isolated from Indian dairy and meat products. Int J Food Microbiol 2021; 336:108899. doi: 10.1016/J.IJFOODMICRO.2020.108899.
  • 18. Ćwiek K, Korzekwa K, Tabiś A, Bania J, Bugla-Płoskońska G, Wieliczko A. Antimicrobial Resistance and Biofilm Formation Capacity of Salmonella enterica Serovar Enteritidis Strains Isolated from Poultry and Humans in Poland. Pathogens 2020; 9:643. doi: 10.3390/PATHOGENS9080643.
  • 19. Kaptchouang Tchatchouang CD, Fri J, Montso PK, Amagliani G, Schiavano GF, Manganyi MC, et al. Evidence of Virulent Multi-Drug Resistant and Biofilm-Forming Listeria Species Isolated from Various Sources in South Africa. Pathogens 2022; 11:843. doi: 10.3390/PATHOGENS11080843/S1.
  • 20. Ma Y, Xu X, Gao Y, Zhan Z, Xu C, Qu X, et al. Antimicrobial resistance and molecular characterization of Salmonella enterica serovar Corvallis isolated from human patients and animal source foods in China. Int J Food Microbiol 2020; 335:108859. doi: 10.1016/J.IJFOODMICRO.2020.108859.
  • 21. Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. Evaluation of different detection methods of biofilm formation in the clinical isolates. Brazilian Journal of Infectious Diseases 2011; 15:305–11. doi: 10.1590/S1413-86702011000400002.
  • 22. Kırmusaoğlu S. The comparison of methods used for the detection of biofilm formation that cause antibiotic resistance of Staphylococcus epidermidis and Staphylococcus aureus. Ortadoğu Tıp Dergisi 2017; 9:28–33. doi: 10.21601/ORTADOGUTIPDERGISI.299940.
  • 23. Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence 2018; 9:522–54. doi: 10.1080/21505594.2017.1313372.
  • 24. Ertaş N, Gönülalan Z. Kayseri İlinde Satılan Çiğ Sütlerde Staphylococcus aureus ve Enterotoksinlerinin Varlığı Üzerine Araştırmalar. F.Ü.Sağ.Bil.Vet.Derg 2010; 24: 11–15.
  • 25. Clermont O, Lescat M, O’Brien CL, Gordon DM, Tenaillon O, Denamur E. Evidence for a human-specific Escherichia coli clone. Environmental Microbiology 2008; 10: 1000–1006. doi: 10.1111/J.1462-2920.2007.01520.X.
  • 26. Rahn K, De Grandis SA, Clarke RC, McEwen SA, Galán JE, Ginocchio C, Curtiss R, Gyles CL. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and Cellular Probes 1992; 6(4): 271–279. doi: 10.1016/0890-8508(92)90002-F.
  • 27. Al S, Disli HB, Hizlisoy H, Ertas Onmaz N, Yildirim Y, Gonulalan Z. Prevalence, and molecular characterization of Listeria monocytogenes isolated from wastewater of cattle slaughterhouses in Turkey. Journal of Applied Microbiology 2022; 132(2): 1518–1525. doi: 10.1111/JAM.15261.
  • 28. Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 1989; 42:872. doi: 10.1136/JCP.42.8.872.
  • 29. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40:175–9. doi: 10.1016/S0167-7012(00)00122-6.
  • 30. Öcal D, Tekeli A, Dolapçı İ. Koagülaz Negatif Stafilokoklarda Biyofilm Oluşumunun Çeşitli Kongo Kırmızısı Besiyerlerinde Değerlendirimi. Temel Tıp Bilimleri 2022; 75(1): 8-15. doi: 10.4274/atfm.galenos.2021.54366.
  • 31. Agresti A. An Introduction to Categorical Data Analysis. Second Edition. Wiley-Interscience, 2007.
  • 32. Kraemer HC. Evaluating medical tests: Objective and quantitative guidelines. Newbury Park, California: Sage publications Inc, 1992.
  • 33. Alvarez-Ordóñez A, Coughlan LM, Briandet R, Cotter PD. Biofilms in Food Processing Environments: Challenges and Opportunities 2019;10:173–95. doi: 10.1146/ANNUREV-FOOD-032818-121805.
  • 34. Uyanık T, Bölükbaş A, Gücükoğlu A, Çadırcı Ö. Çeşitli gıda örnekleri ve kesimhanelerden izole edilen bazı patojen bakterilerin biyofilm oluşturma yeteneğinin araştırılması. Journal of Advances in VetBio Science and Techniques 2022; 7:338–45. doi: 10.31797/VETBIO.1194207.
  • 35. Shi X, Zhu X. Biofilm formation and food safety in food industries. Trends Food Sci Technol 2009; 20:407–13. doi: 10.1016/J.TIFS.2009.01.054.
  • 36. Shakya P, Nayak A, Jogi J, Rai A, Bordoloi S, Scholar HK, et al. Phenotypic detection and comparison of biofilm production in methicillin resistant Staphylococcus aureus. The Pharma Innovation Journal 2022:1352–7.
  • 37. Jain A, Agarwal A. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J Microbiol Methods 2009; 76:88–92. doi: 10.1016/J.MIMET.2008.09.017.
  • 38. Melo P de C, Menezes Ferreira L, Nader Filho A, Francisco Zafalon L, Godoy Vicente HI, de Souza V. Comparison of methods for the detection of biofilm formation by Staphylococcus aureus isolated from bovine subclinical mastitis. Brazilian Journal of Microbiology 2013; 44:119. doi: 10.1590/S1517-83822013005000031.
  • 39. Kowalska J, Maćkiw E, Stasiak M, Kucharek K, Postupolski J. Biofilm-Forming Ability of Pathogenic Bacteria Isolated from Retail Food in Poland. J Food Prot 2020; 83:2032–40. doi: 10.4315/JFP-20-135.
  • 40. Chen GQ, Wu YH, Wang YH, Chen Z, Tong X, Bai Y, et al. Effects of microbial inactivation approaches on quantity and properties of extracellular polymeric substances in the process of wastewater treatment and reclamation: A review. J Hazard Mater 2021; 413:125283. doi: 10.1016/J.JHAZMAT.2021.125283.
  • 41. Gungor C, Barel M, Dishan A, Burak Disli H, Koskeroglu K, Onmaz NE. From cattle to pastirma: Contamination source of methicillin susceptible and resistant Staphylococcus aureus (MRSA) along the pastirma production chain. LWT 2021; 151:112130. doi: 10.1016/J.LWT.2021.112130.
  • 42. Knobloch JKM, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol 2002; 191:101–6. doi: 10.1007/S00430-002-0124-3/METRICS.
  • 43. Sharlee R. Detection of biofilm production among Staphylococcus aureus by Congo red method and tube method. Indian Journal of Microbiology Research 2020; 7:222–5. doi: 10.18231/J.IJMR.2020.040.
  • 44. Tahaei SAS, Stájer A, Barrak I, Ostorházi E, Szabó D, Gajdács M. Correlation between biofilm-formation and the antibiotic resistant phenotype in Staphylococcus aureus isolates: A laboratory-based study in Hungary and a review of the literature. Infect Drug Resist 2021; 14:1155–68. doi: 10.2147/IDR.S303992.
  • 45. Ebineshan K, Pallapati MS, Srikantam A. Occurrence of bacterial biofilm in leprosy plantar ulcers. Lepr Rev 2020; 91:130–8. doi: 10.47276/LR.91.2.130.
  • 46. Dhanawade NB, Kalorey DR, Srinivasan R, Barbuddhe SB, Kurkure N V. Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis. Vet Res Commun 2010; 34:81–9. doi: 10.1007/S11259-009-9326-0.
  • 47. Moretro T, Langsrud S, Heir E. Bacteria on Meat Abattoir Process Surfaces after Sanitation: Characterisation of Survival Properties of Listeria monocytogenes and the Commensal Bacterial Flora. Adv Microbiol 2013; 2013:255–64. doi: 10.4236/AIM.2013.33037.
  • 48. Doijad SP, Barbuddhe SB, Garg S, Poharkar K V., Kalorey DR, Kurkure N V., et al. Biofilm-Forming Abilities of Listeria monocytogenes Serotypes Isolated from Different Sources. PLoS One 2015;10: e0137046. doi: 10.1371/JOURNAL.PONE.0137046.
  • 49. Davarpanah M, Bialvaei AZ. Prevalence, antimicrobial resistance, and biofilm-formation of Listeria monocytogenes in bulk raw milk in East Azerbaijan province, Iran. Reviews and Research in Medical Microbiology 2023; 2023:73–8. doi: 10.1097/MRM.0000000000000313.
  • 50. Flament-Simon SC, Duprilot M, Mayer N, García V, Alonso MP, Blanco J, et al. Association between kinetics of early biofilm formation and clonal lineage in Escherichia coli. Front Microbiol 2019; 10:1183. doi: 10.3389/FMICB.2019.01183/BIBTEX.
  • 51. Tajbakhsh E, Ahmadi P, Abedpour-Dehkordi E, Arbab-Soleimani N, Khamesipour F. Biofilm formation, antimicrobial susceptibility, serogroups and virulence genes of uropathogenic E. coli isolated from clinical samples in Iran. Antimicrob Resist Infect Control 2016; 5:1–8. doi: 10.1186/S13756-016-0109-4/TABLES/5.
  • 52. Onmaz NE, Yildirim Y, Karadal F, Hizlisoy H, Al S, Gungor C, et al. Escherichia coli O157 in fish: Prevalence, antimicrobial resistance, biofilm formation capacity, and molecular characterization. LWT 2020; 133:109940. doi: 10.1016/J.LWT.2020.109940.
  • 53. Dishan A, Hizlisoy H, Barel M, Disli HB, Gungor C, Ertas Onmaz N, et al. Biofilm formation, antibiotic resistance and genotyping of Shiga toxin-producing Escherichia coli isolated from retail chicken meats. British Poultry Science 2022. doi: 10.1080/00071668.2022.2116697.
  • 54. Fazel A, Bavari S, Borji S. Detecting of biofilm formation in the clinical isolates of Pseudomonas aeruginosa and Escherichia coli: an evaluation of different screening methods. Journal of Current Biomedical Reports 2021;2. doi: 10.52547/JCBioR.2.2.56.
  • 55. Sanchez CJ, Mende K, Beckius ML, Akers KS, Romano DR, Wenke JC, et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 2013; 13:47. doi: 10.1186/1471-2334-13-47.
  • 56. Amrutha B, Sundar K, Shetty PH. Study on E. coli and Salmonella biofilms from fresh fruits and vegetables. J Food Sci Technol 2017; 54:1091–7. doi: 10.1007/S13197-017-2555-2/FIGURES/4.
  • 57. Aksoy D. Determination of in vitro Biofilm Formation Abilities of Food Borne Salmonella Enterica Isolates. Trak Univ J Nat Sci 2019; 20:57–62. doi: 10.23902/TRKJNAT.471236.
  • 58. Çufaoğlu G, Onaran Acar B, Cengiz G, Ayaz ND, Göncüoğlu M. Mono-and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Mol Psychiatry 2021; 47:149–53. doi: 10.5152/actavet.2021.21006.
  • 59. Açıkalın D. Salmonella Infantis Suşlarının Oluşturduğu Biyofilm Üzerine Çevresel ve Genetik Faktörlerin Etkisinin Araştırılması, Yüksek Lisans Tezi, Türkiye Cumhuriyeti Ankara Üniversitesi Sağlık Bilimleri Enstitüsü, 2017.
  • 60. Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, et al. Living on a surface: swarming and biofilm formation. Trends Microbiol 2008; 16:496–506. doi: 10.1016/J.TIM.2008.07.004.
  • 61. Vázquez-Sánchez D, Antunes Galvão J, Oetterer M. Contamination sources, biofilm-forming ability and biocide resistance of Shiga toxin-producing Escherichia coli O157:H7 and non-O157 isolated from tilapia-processing facilities. J Food Saf 2018;38: e12446. doi: 10.1111/JFS.12446.
  • 62. Chauhan A, Bernardin A, Mussard W, Kriegel I, Estève M, Ghigo JM, et al. Preventing Biofilm Formation and Associated Occlusion by Biomimetic Glycocalyxlike Polymer in Central Venous Catheters. J Infect Dis 2014; 210:1347–56. doi: 10.1093/INFDIS/JIU249.
  • 63. Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv 2017; 7:36670–83. doi: 10.1039/C7RA02497E.
  • 64. Öcal DN, Dolapçi I, Karahan ZC, Tekeli A. Investigation of biofilm formation properties of Staphylococcus isolates. Mikrobiyol Bul 2017; 51:10–9. doi: 10.5578/MB.46552.

Çeşitli Gıda Kaynaklı Patojenik Bakterilerin Biyofilm Oluşturma Yeteneklerinin Tespitinde Kongo Kırmızısı Agar’ın Etkinliğinin Değerlendirilmesi

Year 2023, , 18 - 26, 30.06.2023
https://doi.org/10.58833/bozokvetsci.1287983

Abstract

Bu çalışmada, daha önceki çalışmalarla mezbaha ve mandıralardan izole edilen ve halk sağlığı açısından risk oluşturan önemli patojenlerden Staphylococcus aureus, Listeria spp., Escherichia coli ve Salmonella spp. izolatlarının biyofilm oluşturma yeteneklerinin belirlenmesinde Kongo Kırmızısı Agar (KKA) ve Mikroplak (MP) yöntemlerinin etkinliğinin ve duyarlılıklarının karşılaştırılması amaçlandı. Çalışma sonucunda 135 izolatın %51.1’i KKA’da, %53’ü ise MP’de biyofilm üreticisi olarak belirlendi. Analiz edilen izolatlar arasında KKA yönteminin duyarlılığının en yüksek olduğu izolat S. aureus idi (%97) bunu Listeria spp. (%59), Salmonella spp (%17). ve E. coli (%13) izledi. Listeria spp., Salmonella spp .ve E. coli seçicilik oranları ise sırasıyla %39, %59 ve %89 idi. Ancak S. aureus izolatlarının tamamı MP testinde biyofilm pozitif sonuç verdiği için KKA’nın seçiciliği bu izolat için belirlenemedi. Sonuç olarak, KKA yönteminin duyarlılığı analiz edilen izolatlardan sadece S. aureus için yüksekti, diğer izolatlarda ise bu yöntemin seçiciliğinin iyi olduğu görüldü. Gıda ve gıda işleme ortamlarında halk sağlığı için risk oluşturabilen patojen suşlarına ait biyofilm yeteneklerinin doğru tespit edilmesi önem arz etmektedir. Bu nedenle, KKA’nın MP yöntemi ile tamamlayıcı bir şekilde uygulanması sonuçların güvenirliği ve biyofilmlerin tespiti için önemli olduğu sonucuna varıldı.

References

  • 1. Flemming HC, Wingender J. The biofilm matrix. Nature Reviews Microbiology 2010; 8:623–33. doi: 10.1038/nrmicro2415.
  • 2. Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. Microbial Biofilms in the Food Industry—A Comprehensive Review. International Journal of Environmental Research and Public Health 2021; 18: 1–31. doi:10.3390/IJERPH18042014.
  • 3. Srinivasan R, Santhakumari S, Poonguzhali P, Geetha M, Dyavaiah M, Xiangmin L. Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections. Frontiers in Microbiology 2021; 12, 1106. doi: 10.3389/FMICB.2021.676458/BIBTEX.
  • 4. Kartal MO, Ekinci MB, Poyraz B. Biyofilm Yapısı ve Önlenmesi. Akademik Gıda 2021; 19, 353-63. doi: 10.24323/akademik-gida.1011231.
  • 5. Gupta P, Gupta H, Poluri KM. Geraniol eradicates Candida glabrata biofilm by targeting multiple cellular pathways. Applied Microbial and Cell Physiology 2021; 105, 5589-605. doi: 10.1007/s00253-021-11397-6.
  • 6. Gebreyohannes G, Nyerere A, Bii C, Sbhatu DB. Challenges of intervention, treatment, and antibiotic resistance of biofilm-forming microorganisms. Heliyon 2019;5: e02192. doi: 10.1016/J.HELIYON. 2019.E02192. 7. Abebe GM. The Role of Bacterial Biofilm in Antibiotic Resistance and Food Contamination. Int J Microbiol 2020;2020. doi: 10.1155/2020/1705814.
  • 8. Cepas V, López Y, Muñoz E, Rolo D, Ardanuy C, Martí S, et al. Relationship between Biofilm Formation and Antimicrobial Resistance in Gram-Negative Bacteria. Microbial Drug Resistance 2019; 25:72–9. doi: 10.1089/MDR.2018.0027.
  • 9. Myszka K, Czaczyk K. Bacterial biofilms on food contact surfaces - a review. Pol J Food Nutr Sci 2011; 61. doi: 10.2478/v10222-011-0018-4.
  • 10. Costerton JW, Montanaro L, Arciola CR. Biofilm in Implant Infections: Its Production and Regulation 2018;28:1062–8. doi: 10.1177/039139880502801103.
  • 11. Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15:167–93. doi: 10.1128/CMR.15.2.167-193.2002.
  • 12. Algburi A, Comito N, Kashtanov D, Dicks LMT, Chikindas ML. Control of biofilm formation: Antibiotics and beyond. Appl Environ Microbiol 2017;83. doi: 10.1128/AEM.02508-16.
  • 13. Dufour D, Leung V, Lévesque CM. Bacterial biofilm: structure, function, and antimicrobial resistance. Endod Topics 2010; 22:2–16. doi: 10.1111/J.1601-1546.2012.00277.X.
  • 14. Olanbiwoninu AA, Popoola BM. Biofilms and their impact on the food industry. Saudi J Biol Sci 2023;30. doi: 10.1016/J.SJBS.2022.103523.
  • 15. Achek R, Hotzel H, Nabi I, Kechida S, Mami D, Didouh N, et al. Phenotypic and Molecular Detection of Biofilm Formation in Staphylococcus aureus Isolated from Different Sources in Algeria. Pathogens 2020; 9:153. doi: 10.3390/PATHOGENS9020153.
  • 16. Agostinho Davanzo EF, Dos Santos RL, Castro VH de L, Palma JM, Pribul BR, Dallago BSL, et al. Molecular characterization of Salmonella spp. and Listeria monocytogenes strains from biofilms in cattle and poultry slaughterhouses located in the federal District and State of Goiás, Brazil. PLoS One 2021;16:e0259687. doi: 10.1371/JOURNAL.PONE.0259687.
  • 17. Bhardwaj DK, Taneja NK, DP S, Chakotiya A, Patel P, Taneja P, et al. Phenotypic and genotypic characterization of biofilm forming, antimicrobial resistant, pathogenic Escherichia coli isolated from Indian dairy and meat products. Int J Food Microbiol 2021; 336:108899. doi: 10.1016/J.IJFOODMICRO.2020.108899.
  • 18. Ćwiek K, Korzekwa K, Tabiś A, Bania J, Bugla-Płoskońska G, Wieliczko A. Antimicrobial Resistance and Biofilm Formation Capacity of Salmonella enterica Serovar Enteritidis Strains Isolated from Poultry and Humans in Poland. Pathogens 2020; 9:643. doi: 10.3390/PATHOGENS9080643.
  • 19. Kaptchouang Tchatchouang CD, Fri J, Montso PK, Amagliani G, Schiavano GF, Manganyi MC, et al. Evidence of Virulent Multi-Drug Resistant and Biofilm-Forming Listeria Species Isolated from Various Sources in South Africa. Pathogens 2022; 11:843. doi: 10.3390/PATHOGENS11080843/S1.
  • 20. Ma Y, Xu X, Gao Y, Zhan Z, Xu C, Qu X, et al. Antimicrobial resistance and molecular characterization of Salmonella enterica serovar Corvallis isolated from human patients and animal source foods in China. Int J Food Microbiol 2020; 335:108859. doi: 10.1016/J.IJFOODMICRO.2020.108859.
  • 21. Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. Evaluation of different detection methods of biofilm formation in the clinical isolates. Brazilian Journal of Infectious Diseases 2011; 15:305–11. doi: 10.1590/S1413-86702011000400002.
  • 22. Kırmusaoğlu S. The comparison of methods used for the detection of biofilm formation that cause antibiotic resistance of Staphylococcus epidermidis and Staphylococcus aureus. Ortadoğu Tıp Dergisi 2017; 9:28–33. doi: 10.21601/ORTADOGUTIPDERGISI.299940.
  • 23. Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence 2018; 9:522–54. doi: 10.1080/21505594.2017.1313372.
  • 24. Ertaş N, Gönülalan Z. Kayseri İlinde Satılan Çiğ Sütlerde Staphylococcus aureus ve Enterotoksinlerinin Varlığı Üzerine Araştırmalar. F.Ü.Sağ.Bil.Vet.Derg 2010; 24: 11–15.
  • 25. Clermont O, Lescat M, O’Brien CL, Gordon DM, Tenaillon O, Denamur E. Evidence for a human-specific Escherichia coli clone. Environmental Microbiology 2008; 10: 1000–1006. doi: 10.1111/J.1462-2920.2007.01520.X.
  • 26. Rahn K, De Grandis SA, Clarke RC, McEwen SA, Galán JE, Ginocchio C, Curtiss R, Gyles CL. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and Cellular Probes 1992; 6(4): 271–279. doi: 10.1016/0890-8508(92)90002-F.
  • 27. Al S, Disli HB, Hizlisoy H, Ertas Onmaz N, Yildirim Y, Gonulalan Z. Prevalence, and molecular characterization of Listeria monocytogenes isolated from wastewater of cattle slaughterhouses in Turkey. Journal of Applied Microbiology 2022; 132(2): 1518–1525. doi: 10.1111/JAM.15261.
  • 28. Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 1989; 42:872. doi: 10.1136/JCP.42.8.872.
  • 29. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40:175–9. doi: 10.1016/S0167-7012(00)00122-6.
  • 30. Öcal D, Tekeli A, Dolapçı İ. Koagülaz Negatif Stafilokoklarda Biyofilm Oluşumunun Çeşitli Kongo Kırmızısı Besiyerlerinde Değerlendirimi. Temel Tıp Bilimleri 2022; 75(1): 8-15. doi: 10.4274/atfm.galenos.2021.54366.
  • 31. Agresti A. An Introduction to Categorical Data Analysis. Second Edition. Wiley-Interscience, 2007.
  • 32. Kraemer HC. Evaluating medical tests: Objective and quantitative guidelines. Newbury Park, California: Sage publications Inc, 1992.
  • 33. Alvarez-Ordóñez A, Coughlan LM, Briandet R, Cotter PD. Biofilms in Food Processing Environments: Challenges and Opportunities 2019;10:173–95. doi: 10.1146/ANNUREV-FOOD-032818-121805.
  • 34. Uyanık T, Bölükbaş A, Gücükoğlu A, Çadırcı Ö. Çeşitli gıda örnekleri ve kesimhanelerden izole edilen bazı patojen bakterilerin biyofilm oluşturma yeteneğinin araştırılması. Journal of Advances in VetBio Science and Techniques 2022; 7:338–45. doi: 10.31797/VETBIO.1194207.
  • 35. Shi X, Zhu X. Biofilm formation and food safety in food industries. Trends Food Sci Technol 2009; 20:407–13. doi: 10.1016/J.TIFS.2009.01.054.
  • 36. Shakya P, Nayak A, Jogi J, Rai A, Bordoloi S, Scholar HK, et al. Phenotypic detection and comparison of biofilm production in methicillin resistant Staphylococcus aureus. The Pharma Innovation Journal 2022:1352–7.
  • 37. Jain A, Agarwal A. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J Microbiol Methods 2009; 76:88–92. doi: 10.1016/J.MIMET.2008.09.017.
  • 38. Melo P de C, Menezes Ferreira L, Nader Filho A, Francisco Zafalon L, Godoy Vicente HI, de Souza V. Comparison of methods for the detection of biofilm formation by Staphylococcus aureus isolated from bovine subclinical mastitis. Brazilian Journal of Microbiology 2013; 44:119. doi: 10.1590/S1517-83822013005000031.
  • 39. Kowalska J, Maćkiw E, Stasiak M, Kucharek K, Postupolski J. Biofilm-Forming Ability of Pathogenic Bacteria Isolated from Retail Food in Poland. J Food Prot 2020; 83:2032–40. doi: 10.4315/JFP-20-135.
  • 40. Chen GQ, Wu YH, Wang YH, Chen Z, Tong X, Bai Y, et al. Effects of microbial inactivation approaches on quantity and properties of extracellular polymeric substances in the process of wastewater treatment and reclamation: A review. J Hazard Mater 2021; 413:125283. doi: 10.1016/J.JHAZMAT.2021.125283.
  • 41. Gungor C, Barel M, Dishan A, Burak Disli H, Koskeroglu K, Onmaz NE. From cattle to pastirma: Contamination source of methicillin susceptible and resistant Staphylococcus aureus (MRSA) along the pastirma production chain. LWT 2021; 151:112130. doi: 10.1016/J.LWT.2021.112130.
  • 42. Knobloch JKM, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol 2002; 191:101–6. doi: 10.1007/S00430-002-0124-3/METRICS.
  • 43. Sharlee R. Detection of biofilm production among Staphylococcus aureus by Congo red method and tube method. Indian Journal of Microbiology Research 2020; 7:222–5. doi: 10.18231/J.IJMR.2020.040.
  • 44. Tahaei SAS, Stájer A, Barrak I, Ostorházi E, Szabó D, Gajdács M. Correlation between biofilm-formation and the antibiotic resistant phenotype in Staphylococcus aureus isolates: A laboratory-based study in Hungary and a review of the literature. Infect Drug Resist 2021; 14:1155–68. doi: 10.2147/IDR.S303992.
  • 45. Ebineshan K, Pallapati MS, Srikantam A. Occurrence of bacterial biofilm in leprosy plantar ulcers. Lepr Rev 2020; 91:130–8. doi: 10.47276/LR.91.2.130.
  • 46. Dhanawade NB, Kalorey DR, Srinivasan R, Barbuddhe SB, Kurkure N V. Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis. Vet Res Commun 2010; 34:81–9. doi: 10.1007/S11259-009-9326-0.
  • 47. Moretro T, Langsrud S, Heir E. Bacteria on Meat Abattoir Process Surfaces after Sanitation: Characterisation of Survival Properties of Listeria monocytogenes and the Commensal Bacterial Flora. Adv Microbiol 2013; 2013:255–64. doi: 10.4236/AIM.2013.33037.
  • 48. Doijad SP, Barbuddhe SB, Garg S, Poharkar K V., Kalorey DR, Kurkure N V., et al. Biofilm-Forming Abilities of Listeria monocytogenes Serotypes Isolated from Different Sources. PLoS One 2015;10: e0137046. doi: 10.1371/JOURNAL.PONE.0137046.
  • 49. Davarpanah M, Bialvaei AZ. Prevalence, antimicrobial resistance, and biofilm-formation of Listeria monocytogenes in bulk raw milk in East Azerbaijan province, Iran. Reviews and Research in Medical Microbiology 2023; 2023:73–8. doi: 10.1097/MRM.0000000000000313.
  • 50. Flament-Simon SC, Duprilot M, Mayer N, García V, Alonso MP, Blanco J, et al. Association between kinetics of early biofilm formation and clonal lineage in Escherichia coli. Front Microbiol 2019; 10:1183. doi: 10.3389/FMICB.2019.01183/BIBTEX.
  • 51. Tajbakhsh E, Ahmadi P, Abedpour-Dehkordi E, Arbab-Soleimani N, Khamesipour F. Biofilm formation, antimicrobial susceptibility, serogroups and virulence genes of uropathogenic E. coli isolated from clinical samples in Iran. Antimicrob Resist Infect Control 2016; 5:1–8. doi: 10.1186/S13756-016-0109-4/TABLES/5.
  • 52. Onmaz NE, Yildirim Y, Karadal F, Hizlisoy H, Al S, Gungor C, et al. Escherichia coli O157 in fish: Prevalence, antimicrobial resistance, biofilm formation capacity, and molecular characterization. LWT 2020; 133:109940. doi: 10.1016/J.LWT.2020.109940.
  • 53. Dishan A, Hizlisoy H, Barel M, Disli HB, Gungor C, Ertas Onmaz N, et al. Biofilm formation, antibiotic resistance and genotyping of Shiga toxin-producing Escherichia coli isolated from retail chicken meats. British Poultry Science 2022. doi: 10.1080/00071668.2022.2116697.
  • 54. Fazel A, Bavari S, Borji S. Detecting of biofilm formation in the clinical isolates of Pseudomonas aeruginosa and Escherichia coli: an evaluation of different screening methods. Journal of Current Biomedical Reports 2021;2. doi: 10.52547/JCBioR.2.2.56.
  • 55. Sanchez CJ, Mende K, Beckius ML, Akers KS, Romano DR, Wenke JC, et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 2013; 13:47. doi: 10.1186/1471-2334-13-47.
  • 56. Amrutha B, Sundar K, Shetty PH. Study on E. coli and Salmonella biofilms from fresh fruits and vegetables. J Food Sci Technol 2017; 54:1091–7. doi: 10.1007/S13197-017-2555-2/FIGURES/4.
  • 57. Aksoy D. Determination of in vitro Biofilm Formation Abilities of Food Borne Salmonella Enterica Isolates. Trak Univ J Nat Sci 2019; 20:57–62. doi: 10.23902/TRKJNAT.471236.
  • 58. Çufaoğlu G, Onaran Acar B, Cengiz G, Ayaz ND, Göncüoğlu M. Mono-and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Mol Psychiatry 2021; 47:149–53. doi: 10.5152/actavet.2021.21006.
  • 59. Açıkalın D. Salmonella Infantis Suşlarının Oluşturduğu Biyofilm Üzerine Çevresel ve Genetik Faktörlerin Etkisinin Araştırılması, Yüksek Lisans Tezi, Türkiye Cumhuriyeti Ankara Üniversitesi Sağlık Bilimleri Enstitüsü, 2017.
  • 60. Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, et al. Living on a surface: swarming and biofilm formation. Trends Microbiol 2008; 16:496–506. doi: 10.1016/J.TIM.2008.07.004.
  • 61. Vázquez-Sánchez D, Antunes Galvão J, Oetterer M. Contamination sources, biofilm-forming ability and biocide resistance of Shiga toxin-producing Escherichia coli O157:H7 and non-O157 isolated from tilapia-processing facilities. J Food Saf 2018;38: e12446. doi: 10.1111/JFS.12446.
  • 62. Chauhan A, Bernardin A, Mussard W, Kriegel I, Estève M, Ghigo JM, et al. Preventing Biofilm Formation and Associated Occlusion by Biomimetic Glycocalyxlike Polymer in Central Venous Catheters. J Infect Dis 2014; 210:1347–56. doi: 10.1093/INFDIS/JIU249.
  • 63. Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv 2017; 7:36670–83. doi: 10.1039/C7RA02497E.
  • 64. Öcal DN, Dolapçi I, Karahan ZC, Tekeli A. Investigation of biofilm formation properties of Staphylococcus isolates. Mikrobiyol Bul 2017; 51:10–9. doi: 10.5578/MB.46552.
There are 63 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Sciences
Journal Section Research Articles
Authors

Dursun Alp Gündoğ 0000-0002-1581-1813

Güven Güngör 0000-0003-3695-9443

Candan Güngör 0000-0002-4321-2770

Nurhan Ertaş Onmaz 0000-0002-4679-6548

Zafer Gönülalan 0000-0002-3935-6296

Publication Date June 30, 2023
Submission Date April 26, 2023
Published in Issue Year 2023

Cite

Vancouver Gündoğ DA, Güngör G, Güngör C, Ertaş Onmaz N, Gönülalan Z. Çeşitli Gıda Kaynaklı Patojenik Bakterilerin Biyofilm Oluşturma Yeteneklerinin Tespitinde Kongo Kırmızısı Agar’ın Etkinliğinin Değerlendirilmesi. Bozok Vet Sci. 2023;4(1):18-26.