Research Article
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Year 2019, Volume: 20 Issue: 1, 57 - 62, 15.04.2019
https://doi.org/10.23902/trkjnat.471236

Abstract

Salmonella enterica serotiplerinin neden olduğu salmonelloz vakaları dünya
çapında en önemli gıda kökenli hastalıkların başında gelmektedir. Bu
patojenlerin oluşturduğu biyofilm yapısı hem gıda kontaminasyonlarına neden
olmakta hem de enfeksiyonlar için kaynak oluşturmaktadır. Bu çalışmada gıda
kökenli Salmonella enterica
izolatlarının polistirende ve hava-sıvı ara fazında biyofilm oluşturma
yetenekleri ve ayrıca Kongo kırmızısı agar plakalarında koloni morfolojilerinin
belirlenmesi amaçlanmıştır. Çalışmada Edirne ilinde satışa sunulan tavuk
karkaslarından izole edilmiş 32 adet Salmonella
izolatı kullanılmıştır. İzolatların plastik yüzeylerdeki biyofilm oluşturma
yeteneklerinin belirlenmesinde boyanmış bakteriyel biyofilmlerin optik
yoğunluklarının ölçülmesi esasına dayanan mikroplaka tekniği kullanılmıştır.
Polistren plakalardaki biyofilm oluşturma sonuçlarına göre, izolatların en
güçlü biyofilm oluşturma kapasitesi 22°C'de 3 günde gözlemlenmiştir. Bütün
izolatlar 22°C'de sıvı-hava ara fazında pelikül oluştururken izolatların sadece
% 13'ü (Infantis, Kentucky ve Enteritidis serovarlarını içeren) 37°C'de
sıvı-hava ara fazında pelikül oluşturmaktadır. Kongo kırmızısı agarda üç farklı
koloni morfolojisi (saw; pürüzsüz ve beyaz, bdar; kahverengi, kuru ve pürüzlü,
rdar; kırmızı, kuru ve pürüzlü) belirlenmiştir. Salmonella izolatlarının yüksek biyofilm oluşturma kapasiteleri,
virülens ve özellikle tıbbi olarak önemli antibiyotikleri içeren direnç
faktörlerinin gıda zinciri yolu ile geniş çaplı yayılımına neden olabilir. Bu
durum halk sağlığı açısından büyük bir endişe kaynağı oluşturmaktadır.

References

  • 1. Aksoy, D. & Şen, E. 2015. Investigation of pathogenic phenotypes and virulence determinants of food-borne Salmonella enterica strains in Caenorhabditis elegans animal model. Bulletin of Microbiology, 49(4): 513-524.
  • 2. Albayrak, F., Cokca, F., Erdem, B. & Aysev, A.D. 2004. Predictive value of nalidixic acid resistance for detecting salmonellae with decreased ciprofloxacin susceptibility. International Journal of Antimicrobial Agents, 23(4): 332-336.
  • 3. Antunes, P., Mourão, J., Campos, J. & Peixe, L. 2016. Salmonellosis: the role of poultry meat. Clinical Microbiology and Infection, 22(2): 110-121.
  • 4. Borges, K.A., Furian, T.Q., Souza, S.N., Menezes, R., Tondo, E.C., Salle, C.T., Moraes H.L.S. & Nascimento, V.P. 2018. Biofilm formation capacity of Salmonella serotypes at different temperature conditions. Pesquisa Veterinária Brasileira, 38(1): 71-76.
  • 5. Cookson, A.L., Cooley, W.A. & Woodward, M.J. 2002. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence in abiotic surfaces. International Journal of Medical Microbiology, 292(3/4): 195.
  • 6. Costerton, J.W., Stewart, P.S. & Greenberg, E. P. 1999. Bacterial biofilms: a common cause of persistent infections. Science, 284(5418): 1318-1322.
  • 7. Cunliffe, D., Smart, C.A., Alexander, C. & Vulfson, E.N. 1999. Bacterial adhesion at synthetic surfaces. Applied and environmental microbiology, 65(11): 4995-5002.
  • 8. Díez-García, M., Capita, R. & Alonso-Calleja, C. 2012. Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry. Food Microbiology, 31(2): 173-180.
  • 9. Donlan, R.M. 2002. Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8(9): 881.
  • 10. Durul, B., Acar, S., Bulut, E., Kyere, E. O. & Soyer, Y. 2015. Subtyping of Salmonella food isolates suggests the geographic clustering of serotype Telaviv. Foodborne Pathogens and Disease, 12(12): 958-965.
  • 11. Ercis, S., Erdem, B., Hasçelik, G. & Gur, D. 2006. Nalidixic acid resistance in Salmonella strains with decreased susceptibility to ciprofloxacin isolated from humans in Turkey. Japanese Journal of Infectious Diseases, 59(2): 117.
  • 12. Erol, İ. 1999. Ankara’da tüketime sunulan kıymalarda Salmonella’ların varlığı ve serotip dağılımı. Turkish Journal of Veterinary and Animal Science, 23(4): 321-5.
  • 13. Gerstel, U. & Römling, U. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environmental Microbiology, 3(10): 638-648.
  • 14. Genualdi, S., Nyman, P. & Begley, T. 2014. Updated evaluation of the migration of styrene monomer and oligomers from polystyrene food contact materials to foods and food simulants. Food Additives & Contaminants: Part A, 31(4): 723-733.
  • 15. Hoelzer, K., Switt, A. I. M. & Wiedmann, M. 2011. Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research, 42(1): 34.
  • 16. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S. & Ciofu, O. 2010. Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35(4): 322-332.
  • 17. Karaca, B., Akcelik, N. & Akcelik, M. 2013. Biofilm-producing abilities of Salmonella strains isolated from Turkey. Biologia, 68(1): 1-10.
  • 18. Lin, D., Chen, K., Chan, E.W.C. & Chen, S. 2015. Increasing prevalence of ciprofloxacin-resistant food-borne Salmonella strains harboring multiple PMQR elements but not target gene mutations. Scientific Reports, 5: 14754.
  • 19. Milanov, D., Prunić, B., & Ljubojević, D. 2017. Biofilm forming ability of Salmonella enterica serovar Tennessee isolates originating from feed. Veterinarski Arhiv, 87(6): 691-702.
  • 20. Ozdemir, K. & Acar, S. 2014. Plasmid profile and pulsed–field gel electrophoresis analysis of Salmonella enterica isolates from humans in Turkey. PloS One, 9(5): e95976.
  • 21. Panisello, P.J., Rooney, R., Quantick, P.C. & Stanwell-Smith, R. 2000. Application of foodborne disease outbreak data in the development and maintenance of HACCP systems. International Journal of Food Microbiology, 59(3): 221-234.
  • 22. Piras, F., Fois, F., Consolati, S.G., Mazza, R. & Mazzette, R. 2015. Influence of temperature, source, and serotype on biofilm formation of Salmonella enterica isolates from pig slaughterhouses. Journal of Food Protection, 78(10): 1875-1878.
  • 23. Römling, U., Sierralta, W.D., Eriksson, K. & Normark, S. (1998). Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Molecular Microbiology, 28(2): 249-264.
  • 24. Römling, U., Rohde, M., Olsén, A., Normark, S. & Reinköster, J. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Molecular Microbiology, 36(1): 10-23.
  • 25. Shia, X. &, Zhu, X. 2009. Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20(9): 407-413.
  • 26. Sinde, E. & Carballo, J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiology, 17(4): 439-447.
  • 27. Solano, C., García, B., Valle, J., Berasain, C., Ghigo, J. M., Gamazo, C. & Lasa, I. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Molecular Microbiology, 43(3): 793-808.
  • 28. Srey, S., Jahid, I.K. & Ha, S.D. 2013. Biofilm formation in food industries: a food safety concern. Food Control, 31(2): 572-585.
  • 29. Steenackers, H., Hermans, K., Vanderleyden, J. & De Keersmaecker, S.C. 2012. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Research International, 45(2): 502-531.
  • 30. Stepanović, S., Vuković, D., Dakić, I., Savić, B. & Švabić-Vlahović, M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40(2): 175-179.
  • 31. Stepanović, S., Ćirković, I., Mijač, V. & Švabić-Vlahović, M. 2003. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiology, 20(3): 339-343.
  • 32. Stepanović, S., Ćirković, I., Ranin, L. & Svabić‐Vlahović, M. 2004. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in Applied Microbiology, 38(5): 428-432.
  • 33. Turki, Y., Ouzari, H., Mehri, I., Aissa, R.B. & Hassen, A. 2012. Biofilm formation, virulence gene and multi-drug resistance in Salmonella Kentucky isolated in Tunisia. Food Research International, 45(2): 940-946.
  • 34. Van Houdt, R. & Michiels, C. W. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109(4): 1117-1131.
  • 35. Velhner, M., Kozoderović, G., Grego, E., Galić, N., Stojanov, I., Jelesić, Z., & Kehrenberg, C. 2014. Clonal spread of Salmonella enterica serovar Infantis in Serbia: Acquisition of mutations in the topoisomerase genes gyrA and parC leads to increased resistance to fsluoroquinolones. Zoonoses and Public Health, 61(5): 364-370.
  • 36. Vestby, L.K., Møretrø, T., Ballance, S., Langsrud, S., & Nesse, L.L. 2009a. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Veterinary Research, 5(1): 43.
  • 37. Vestby, L.K., Møretrø, T., Langsrud, S., Heir, E., & Nesse, L.L. 2009b. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal-and feed factories. BMC Veterinary Research, 5(1): 20.

DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES

Year 2019, Volume: 20 Issue: 1, 57 - 62, 15.04.2019
https://doi.org/10.23902/trkjnat.471236

Abstract

Salmonellosis caused by non-typhodial Salmonella enterica serotypes is one of
the most important food-borne diseases worldwide and biofilm structure formed
by these pathogens provide a reservoir for food contamination and a source for
infections. This study was performed in order to determine biofilm formation abilities
of food borne Salmonella isolates on
polystyrene and on air liquid interphase and their colony morphologies when
grown on Congo Red Agar plates. 32 food-borne Salmonella strains isolated from retail chicken carcasses in Edirne
province of Turkey and belonging to the Infantis, Enteritidis, Kentucky and
Telaviv serotypes were used. The microtiter plate technique was used to
determine biofilm formation abilities of the isolates on polystyrene surfaces
by measuring the optical density (OD) values of the stained bacterial biofilms.
The results showed that the strongest biofilm formation capacities of the
isolates were observed at 22°C for 3 days of incubation. Although all isolates
formed pellicle on the liquid-air interface at 22°C, only 13% of the isolates
belonging to the Infantis, Kentucky and Enteritidis serovars formed pellicle at
liquid-air interface at 37°C. Three different colony morphotypes (saw; smooth
and white, bdar; brown, dry and rough, rdar; red, dry and rough) were
determined on Congo Red Agar among the isolates. High biofilm formation
abilities of the tested Salmonella
isolates can lead to widespread of virulence and resistance properties,
especially to medically important antibiotics such as ciprofloxacin, via food
chain. This situation constitutes an important concern for public health.

References

  • 1. Aksoy, D. & Şen, E. 2015. Investigation of pathogenic phenotypes and virulence determinants of food-borne Salmonella enterica strains in Caenorhabditis elegans animal model. Bulletin of Microbiology, 49(4): 513-524.
  • 2. Albayrak, F., Cokca, F., Erdem, B. & Aysev, A.D. 2004. Predictive value of nalidixic acid resistance for detecting salmonellae with decreased ciprofloxacin susceptibility. International Journal of Antimicrobial Agents, 23(4): 332-336.
  • 3. Antunes, P., Mourão, J., Campos, J. & Peixe, L. 2016. Salmonellosis: the role of poultry meat. Clinical Microbiology and Infection, 22(2): 110-121.
  • 4. Borges, K.A., Furian, T.Q., Souza, S.N., Menezes, R., Tondo, E.C., Salle, C.T., Moraes H.L.S. & Nascimento, V.P. 2018. Biofilm formation capacity of Salmonella serotypes at different temperature conditions. Pesquisa Veterinária Brasileira, 38(1): 71-76.
  • 5. Cookson, A.L., Cooley, W.A. & Woodward, M.J. 2002. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence in abiotic surfaces. International Journal of Medical Microbiology, 292(3/4): 195.
  • 6. Costerton, J.W., Stewart, P.S. & Greenberg, E. P. 1999. Bacterial biofilms: a common cause of persistent infections. Science, 284(5418): 1318-1322.
  • 7. Cunliffe, D., Smart, C.A., Alexander, C. & Vulfson, E.N. 1999. Bacterial adhesion at synthetic surfaces. Applied and environmental microbiology, 65(11): 4995-5002.
  • 8. Díez-García, M., Capita, R. & Alonso-Calleja, C. 2012. Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry. Food Microbiology, 31(2): 173-180.
  • 9. Donlan, R.M. 2002. Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8(9): 881.
  • 10. Durul, B., Acar, S., Bulut, E., Kyere, E. O. & Soyer, Y. 2015. Subtyping of Salmonella food isolates suggests the geographic clustering of serotype Telaviv. Foodborne Pathogens and Disease, 12(12): 958-965.
  • 11. Ercis, S., Erdem, B., Hasçelik, G. & Gur, D. 2006. Nalidixic acid resistance in Salmonella strains with decreased susceptibility to ciprofloxacin isolated from humans in Turkey. Japanese Journal of Infectious Diseases, 59(2): 117.
  • 12. Erol, İ. 1999. Ankara’da tüketime sunulan kıymalarda Salmonella’ların varlığı ve serotip dağılımı. Turkish Journal of Veterinary and Animal Science, 23(4): 321-5.
  • 13. Gerstel, U. & Römling, U. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environmental Microbiology, 3(10): 638-648.
  • 14. Genualdi, S., Nyman, P. & Begley, T. 2014. Updated evaluation of the migration of styrene monomer and oligomers from polystyrene food contact materials to foods and food simulants. Food Additives & Contaminants: Part A, 31(4): 723-733.
  • 15. Hoelzer, K., Switt, A. I. M. & Wiedmann, M. 2011. Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research, 42(1): 34.
  • 16. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S. & Ciofu, O. 2010. Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35(4): 322-332.
  • 17. Karaca, B., Akcelik, N. & Akcelik, M. 2013. Biofilm-producing abilities of Salmonella strains isolated from Turkey. Biologia, 68(1): 1-10.
  • 18. Lin, D., Chen, K., Chan, E.W.C. & Chen, S. 2015. Increasing prevalence of ciprofloxacin-resistant food-borne Salmonella strains harboring multiple PMQR elements but not target gene mutations. Scientific Reports, 5: 14754.
  • 19. Milanov, D., Prunić, B., & Ljubojević, D. 2017. Biofilm forming ability of Salmonella enterica serovar Tennessee isolates originating from feed. Veterinarski Arhiv, 87(6): 691-702.
  • 20. Ozdemir, K. & Acar, S. 2014. Plasmid profile and pulsed–field gel electrophoresis analysis of Salmonella enterica isolates from humans in Turkey. PloS One, 9(5): e95976.
  • 21. Panisello, P.J., Rooney, R., Quantick, P.C. & Stanwell-Smith, R. 2000. Application of foodborne disease outbreak data in the development and maintenance of HACCP systems. International Journal of Food Microbiology, 59(3): 221-234.
  • 22. Piras, F., Fois, F., Consolati, S.G., Mazza, R. & Mazzette, R. 2015. Influence of temperature, source, and serotype on biofilm formation of Salmonella enterica isolates from pig slaughterhouses. Journal of Food Protection, 78(10): 1875-1878.
  • 23. Römling, U., Sierralta, W.D., Eriksson, K. & Normark, S. (1998). Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Molecular Microbiology, 28(2): 249-264.
  • 24. Römling, U., Rohde, M., Olsén, A., Normark, S. & Reinköster, J. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Molecular Microbiology, 36(1): 10-23.
  • 25. Shia, X. &, Zhu, X. 2009. Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20(9): 407-413.
  • 26. Sinde, E. & Carballo, J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiology, 17(4): 439-447.
  • 27. Solano, C., García, B., Valle, J., Berasain, C., Ghigo, J. M., Gamazo, C. & Lasa, I. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Molecular Microbiology, 43(3): 793-808.
  • 28. Srey, S., Jahid, I.K. & Ha, S.D. 2013. Biofilm formation in food industries: a food safety concern. Food Control, 31(2): 572-585.
  • 29. Steenackers, H., Hermans, K., Vanderleyden, J. & De Keersmaecker, S.C. 2012. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Research International, 45(2): 502-531.
  • 30. Stepanović, S., Vuković, D., Dakić, I., Savić, B. & Švabić-Vlahović, M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40(2): 175-179.
  • 31. Stepanović, S., Ćirković, I., Mijač, V. & Švabić-Vlahović, M. 2003. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiology, 20(3): 339-343.
  • 32. Stepanović, S., Ćirković, I., Ranin, L. & Svabić‐Vlahović, M. 2004. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in Applied Microbiology, 38(5): 428-432.
  • 33. Turki, Y., Ouzari, H., Mehri, I., Aissa, R.B. & Hassen, A. 2012. Biofilm formation, virulence gene and multi-drug resistance in Salmonella Kentucky isolated in Tunisia. Food Research International, 45(2): 940-946.
  • 34. Van Houdt, R. & Michiels, C. W. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109(4): 1117-1131.
  • 35. Velhner, M., Kozoderović, G., Grego, E., Galić, N., Stojanov, I., Jelesić, Z., & Kehrenberg, C. 2014. Clonal spread of Salmonella enterica serovar Infantis in Serbia: Acquisition of mutations in the topoisomerase genes gyrA and parC leads to increased resistance to fsluoroquinolones. Zoonoses and Public Health, 61(5): 364-370.
  • 36. Vestby, L.K., Møretrø, T., Ballance, S., Langsrud, S., & Nesse, L.L. 2009a. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Veterinary Research, 5(1): 43.
  • 37. Vestby, L.K., Møretrø, T., Langsrud, S., Heir, E., & Nesse, L.L. 2009b. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal-and feed factories. BMC Veterinary Research, 5(1): 20.
There are 37 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Article/Araştırma Makalesi
Authors

Deniz Aksoy 0000-0001-8696-9725

Publication Date April 15, 2019
Submission Date October 16, 2018
Acceptance Date March 18, 2019
Published in Issue Year 2019 Volume: 20 Issue: 1

Cite

APA Aksoy, D. (2019). DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES. Trakya University Journal of Natural Sciences, 20(1), 57-62. https://doi.org/10.23902/trkjnat.471236
AMA Aksoy D. DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES. Trakya Univ J Nat Sci. April 2019;20(1):57-62. doi:10.23902/trkjnat.471236
Chicago Aksoy, Deniz. “DETERMINATION OF in Vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella Enterica ISOLATES”. Trakya University Journal of Natural Sciences 20, no. 1 (April 2019): 57-62. https://doi.org/10.23902/trkjnat.471236.
EndNote Aksoy D (April 1, 2019) DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES. Trakya University Journal of Natural Sciences 20 1 57–62.
IEEE D. Aksoy, “DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES”, Trakya Univ J Nat Sci, vol. 20, no. 1, pp. 57–62, 2019, doi: 10.23902/trkjnat.471236.
ISNAD Aksoy, Deniz. “DETERMINATION OF in Vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella Enterica ISOLATES”. Trakya University Journal of Natural Sciences 20/1 (April 2019), 57-62. https://doi.org/10.23902/trkjnat.471236.
JAMA Aksoy D. DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES. Trakya Univ J Nat Sci. 2019;20:57–62.
MLA Aksoy, Deniz. “DETERMINATION OF in Vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella Enterica ISOLATES”. Trakya University Journal of Natural Sciences, vol. 20, no. 1, 2019, pp. 57-62, doi:10.23902/trkjnat.471236.
Vancouver Aksoy D. DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES. Trakya Univ J Nat Sci. 2019;20(1):57-62.

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