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Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması

Year 2019, Volume: 17 Issue: 1, 131 - 139, 26.03.2019
https://doi.org/10.24323/akademik-gida.544978

Abstract

Biyofilm, mikroorganizmaların canlı veya cansız bir
yüzeye yapışarak kendi ürettikleri ekzopolimerik yapıda jelsi bir tabaka içine
gömülü halde birbirlerine, bir katı yüzeye ya da bir ara yüzeye tutunarak
oluşturdukları topluluk olarak tanımlanır. Gıda endüstrisinde biyofilm oluşumu
gıdalarda bozulmalara, gıda işleme ekipmanlarında hasarlara ve patojen
kontaminasyonları ile hastalıklara neden olduğu için istenmeyen bir durumdur. Biyofilmler
antimikrobiyel maddelere karşı planktonik hücrelerden daha dirençlidirler. Biyofilmlerdeki
bakterilerin antimikrobiyellere karşı gösterdikleri dirençten birçok olası
mekanizma sorumludur. Biyofilmlerdeki direnç mekanizmasını etkileyen başlıca
faktörler ekzopolisakkarit matriksi, enzimler, heterojenlik, hücresel
persistans, metabolik aktivite, genetik adaptasyon, kitle algılama, stres cevapları,
dış membran yapısı ve sızdırma pompaları’dır. Direnç mekanizmalarının tam
olarak anlaşılması biyofilm oluşumunun önlenmesi ve kontrol edilmesinde fayda
sağlayacaktır. Sonuç olarak etkili bir biyofilm kontrolü için araştırmacılar öncelikle
direnç mekanizmaları üzerinde yoğunlaşmalı ve daha sonra koruyucu önlemlerin
alınması gerekmektedir. Bu derlemede, gıda endüstrisindeki bakteriyel biyofilmlerin
antimikrobiyel maddelere karşı gösterdikleri direnç mekanizması üzerinde
durulmuştur.

References

  • [1] Dufour, D., Leung V., Lévesque C.M. (2012). Bacterial biofilm: structure, function, and antimicrobial resistance. Endodontic Topics, 22, 2–16.
  • [2] Sereno, M.J., Ziech, R.E., Druziani, J.T., Pereira, J.G., Bersot, L.S. (2017). Antimicrobial susceptibility and biofilm production by salmonella sp. strains isolated from frozen poultry carcasses. Brazilian Journal of Poultry Science, 19(1), 103-108.
  • [3] Xu, D., Jia, R., Li, Y., Gu, T. (2017). Advances in the treatment of problematic industrial biofilms. World Journal of Microbiological Biotechnology, 33, 97
  • [4] Trachoo, N. (2003). Biofilms and the food industry. Jornal of Science and Technology, 25(6), 807-815.
  • [5] Meyer, B. (2003). Approaches to prevention, removal and killing of biofilms. International Biodeterioration & Biodegradation, 51, 249-253.
  • [6] Houdt R.V., Michiels, C.W. (2010). Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109: 1117–1131.
  • [7] Tan, S.Y.E., Chew, S.C., Tan, S.Y.Y., Givskov, M., Yang, L. (2014). Emerging frontiers in detection and control of bacterial biofilms. Current Opinion in Biotechnology, 26, 1–6.
  • [8] Shi, X., Zhu, X. (2009). Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20, 407-413.
  • [9] Simoes, V., Simoes L.C., Vieira V.J. (2010). A review of current and emergent biofilm control strategies. LWT - Food Science and Technology, 43, 573–583.
  • [10] Bridier, A., Vizuete, P.S., Guilbaud, M., Piard, J.C., Naitali, M., Briandet, R. (2015). Biofilm-associated persistence of food-borne pathogens. Food Microbiology, 45, 167-178.
  • [11] Cahill, S.M., Desmarchelier, P., Fattori, V., Bruno, A., Cannavan, A. (2017). Global perspectives on antimicrobial resistance in the food chain. Food Protection Trends, 37(5), 353–360.
  • [12] Paraje, M.G. (2011). Antimicrobial resistance in biofilms. Science against microbial pathogens: communicating current research and technological advances, Edited by A. Mendez Vilas, Formatex.
  • [13] Gilbert, P., McBain, A.J., Rickard, A.H. (2003). Formation of microbial biofilm in hygienic situations: a problem of control. International Biodeterioration & Biodegradation, 51, 245-248.
  • [14] Jahid, I.K., Hu, S.D. (2012). A review of microbial biofilms of produce: future challenge to food safety. Food Science and Biotechnology, 21(2), 299-316.
  • [15] Myszka, K., Czaczyk, K. (2011). Bacterial biofilms on food contact surfaces – a review. Polish Journal of Food and Nutritional Science, 61(3), 173-180.
  • [16] Kumar, C.G., Anand, S.K. (1998). Significance of microbial biofilms in food industry: a review. International Journal of Food Microbiology, 42, 9–27.
  • [17] Turhan, E.U., Metselaar, K.I., Abee, T. (2016). Listeria monocytogenes’in asit dirençli türlerinin benzalkonyum klorür direnci ve biyofilm oluşumu. Türkiye 12.Gıda Kongresi, Trakya Üniversitesi, 05-07 Ekim, 2016, Edirne, S136, 13s.
  • [18] Turhan, E.U., Erginkaya, Z., 2016. Gıda endüstrisindeki biyofilmlerin önlenmesinde biyolojik yaklaşımlar. 1st International Mediterranean Science and Engineering Congress (IMSEC 2016), 26-28 October 2016, Adana/Turkey.
  • [19] Turhan, E.U., Erginkaya, Z., Uney, M.H., Ozer, E.A. (2017). Inactivation effect of probiotic biofilms on growth of Listeria monocytogenes. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 23(4), 541-546.
  • [20] Cappitelli, F., Polo, A., Villa, F. (2014). Biofilm formation in food processing environments is still poorly understood and controlled. Food Engineering Reviews, 6, 29–42.
  • [21] Verraes, C., Boxstael S.V., Meervenne, E.V., Coillie, E.V., Butaye, P., Catry, B., Schaetzen, M.A., Huffel, X.V., Imberechts, H., Dierick, K., Daube, G., Saegerman, C., Block, J.D., Dewulf, J., Herman, L. (2013). Antimicrobial resistance in the food chain: a review. International Journal of Environmental Research and Public Health, 10, 2643-2669.
  • [22] Akan, E., Kınık, Ö. (2014). Biyofilm oluşum mekanizması ve biyofilmlerin gıda güvenliğine etkisi. Gıda ve Yem Bilimi - Teknolojisi Dergisi, 14, 42-51.
  • [23] Gün, İ., Ekinci, F.Y. (2009). Biyofilmler: yüzeylerdeki mikrobiyel yaşam. Gıda, 34(3), 165-173.
  • [24] Bridier, A., Briandet, R., Thomas, V., Brissonnet, F.D. (2011). Resistance of bacterial biofilms to disinfectants: a review. Biofouling, 27(9), 1017-1032.
  • [25] Akbas, M.Y., Cag, S. (2016). Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. Food Science and Technology International, 22(7), 587–597.
  • [26] Langsrud, S., Sidhua, M.S., Heir, E., Holck, A.L. (2003). Bacterial disinfectant resistance a challenge for the food industry. International Biodeterioration & Biodegradation, 51, 283-290.
  • [27] Araujo, P., Lemos, M., Mergulhão, F., Melo, L., Simões, M. (2011). Antimicrobial resistance to disinfectants in biofilms. Science against microbial pathogens: communicating current research and technological advances, Edited by A. Mendez Vilas, Formatex Research Center, Badajoz.
  • [28] Srey, S., Jahid, I.K., Ha, S.D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31, 572-585.
  • [29] Turhan, E.U, Kalkan, S., Erginkaya, Z. (2017). The use of phages for the removal of biofilms in the food industry. in: Antimicrobial research: Novel bioknowledge and educational programs, Edited by A. Méndez-Vilas , Formatex Research Center, Badajoz, pp.351-357.
  • [30] Ünal E., Kalkan S., Erginkaya Z. (2010). “Use of Lactic Acid Bacteria Biofilms as Biocontrol Agents”. Science and Technology Aganist Microbial Pathogens. Research, Development and Evalution. Edited by A. Méndez-Vilas, Formatex Research Center, Badajoz.
  • [31] Kubota, H., Senda, S., Tokuda, H., Uchiyama, H., Nomura, N. (2009). Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiology, 26, 592-597.
  • [32] Singh, S., Singh, S.K., Chowdhury, I., Singh, R. (2017). Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. The Open Microbiology Journal, 11, 53-62.
  • [33] Brooks, J.D., Flint, S.H. (2008). Biofilms in the food industry: problems and potential solutions. International Journal of Food Science and Technology, 43, 2163-2176.
  • [34] Kubota, H., Senda, S., Tokuda, H., Uchiyama, H., Nomura, N. (2008). Biofilm formation by lactic acid bacteria and resistance to environmental stress. Journal of Bioscience and Bioengineering, 106(4), 381-386.
  • [35] Ibusquize, P.S., Herrera, J.J.R., Cabo, M.L. (2011). Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiology, 28, 418-425.
  • [36] Davidson, P.M., Harrison, M.A. (2002). Resistance and adaptation to food antimicrobials, sanitizers, and other process controls. Food Technology, 56(11), 69-78.
  • [37] Mah, T.F.C., Otoole, G.A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9(1), 34-39.
  • [38] Stewart, P.S., Costerton, J.W. (2001). Antibiotic resistance of bacteria in biofilms. The Lancet, 358, 135-138.
  • [39] Hoiby, N., Bjarnsholt T., Givskov, M., Molin, S., Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35, 322-332.
  • [40] Simoes, M., Simoes, L.C., Vieira, M.J. (2010). A review of current and emergent biofilm control strategies. LWT - Food Science and Technology 43: 573-583.
  • [41] Pan, Y., Breidt, F., Kathariou, J., Kathariou, S. (2006). Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Applied and Environmental Microbiology, 72(12), 7711-7717.
  • [42] Çağlar, K. (2005). Dezenfektanlara Direnç Gelişim Mekanizmaları? Dezenfeksiyon İşlemini Ne Kadar Tehdit Etmektedir? 4. Ulusal Sterilizasyon Dezenfeksiyon Kongresi, 20-24 Nisan 2005, Samsun/Türkiye.
  • [43] Meral, H., Korukluoğlu, M., 2014. Laktik asit bakterilerinin antibiyotik direnç mekanizmaları. U. Ü. Ziraat Fakültesi Dergisi, 28(2), 71-82.
  • [44] Shemesh, M., Tam, A., Aharoni, R., Steinberg, D. (2010). Genetic adaptation of Streptococcus mutans during biofilm formation on different types of surfaces. BMC Microbiology, 10, 51.
  • [45] Özel B., Şimşek, Ö. (2017). Nisinin sinerjistik antimikrobiyel etkisi. Akademik Gıda, 15(3), 288-299.
  • [46] Afnor Official Distributor of Standards, (2006). EN 1040, NF T 150. https://www.boutique.afnor.org.

Mechanism of Antimicrobial Resistance in Bacterial Biofilms

Year 2019, Volume: 17 Issue: 1, 131 - 139, 26.03.2019
https://doi.org/10.24323/akademik-gida.544978

Abstract

Biofilm is defined as a community in which
microorganisms adhere to a living or inanimate surface, embedded in a
gelatinous layer in a self-produced matrix of extrapolymeric substances,
adhered to each other, to a solid surface or to an interface. In food industry,
biofilm formation is undesirable as they cause food spoilage, damages in food
processing equipment and diseases due to pathogenic contamination. Biofilms are
more resistant to antimicrobial agents than planktonic cells. There are various
possible mechanisms responsible for antimicrobial resistance of the bacteria in
biofilms. The main factors that affect resistance mechanism in biofilms are
characterized as exopolysaccharide matrix, enzymes, heterogeneity, cellular persistence,
metabolic activity, genetic adaptation, quorum sensing, stress responses, outer
membrane structure and efflux pumps. A whole understanding of resistance
mechanisms can provide benefits to prevent and control biofilm formation. As a
result, researchers should initially focus on the mechanisms of resistance for
effective biofilm control and then protective measures must be taken. In the
present review, the resistance mechanisms of bacterial biofilms in food industry
against antimicrobial agents are focused.

References

  • [1] Dufour, D., Leung V., Lévesque C.M. (2012). Bacterial biofilm: structure, function, and antimicrobial resistance. Endodontic Topics, 22, 2–16.
  • [2] Sereno, M.J., Ziech, R.E., Druziani, J.T., Pereira, J.G., Bersot, L.S. (2017). Antimicrobial susceptibility and biofilm production by salmonella sp. strains isolated from frozen poultry carcasses. Brazilian Journal of Poultry Science, 19(1), 103-108.
  • [3] Xu, D., Jia, R., Li, Y., Gu, T. (2017). Advances in the treatment of problematic industrial biofilms. World Journal of Microbiological Biotechnology, 33, 97
  • [4] Trachoo, N. (2003). Biofilms and the food industry. Jornal of Science and Technology, 25(6), 807-815.
  • [5] Meyer, B. (2003). Approaches to prevention, removal and killing of biofilms. International Biodeterioration & Biodegradation, 51, 249-253.
  • [6] Houdt R.V., Michiels, C.W. (2010). Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109: 1117–1131.
  • [7] Tan, S.Y.E., Chew, S.C., Tan, S.Y.Y., Givskov, M., Yang, L. (2014). Emerging frontiers in detection and control of bacterial biofilms. Current Opinion in Biotechnology, 26, 1–6.
  • [8] Shi, X., Zhu, X. (2009). Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20, 407-413.
  • [9] Simoes, V., Simoes L.C., Vieira V.J. (2010). A review of current and emergent biofilm control strategies. LWT - Food Science and Technology, 43, 573–583.
  • [10] Bridier, A., Vizuete, P.S., Guilbaud, M., Piard, J.C., Naitali, M., Briandet, R. (2015). Biofilm-associated persistence of food-borne pathogens. Food Microbiology, 45, 167-178.
  • [11] Cahill, S.M., Desmarchelier, P., Fattori, V., Bruno, A., Cannavan, A. (2017). Global perspectives on antimicrobial resistance in the food chain. Food Protection Trends, 37(5), 353–360.
  • [12] Paraje, M.G. (2011). Antimicrobial resistance in biofilms. Science against microbial pathogens: communicating current research and technological advances, Edited by A. Mendez Vilas, Formatex.
  • [13] Gilbert, P., McBain, A.J., Rickard, A.H. (2003). Formation of microbial biofilm in hygienic situations: a problem of control. International Biodeterioration & Biodegradation, 51, 245-248.
  • [14] Jahid, I.K., Hu, S.D. (2012). A review of microbial biofilms of produce: future challenge to food safety. Food Science and Biotechnology, 21(2), 299-316.
  • [15] Myszka, K., Czaczyk, K. (2011). Bacterial biofilms on food contact surfaces – a review. Polish Journal of Food and Nutritional Science, 61(3), 173-180.
  • [16] Kumar, C.G., Anand, S.K. (1998). Significance of microbial biofilms in food industry: a review. International Journal of Food Microbiology, 42, 9–27.
  • [17] Turhan, E.U., Metselaar, K.I., Abee, T. (2016). Listeria monocytogenes’in asit dirençli türlerinin benzalkonyum klorür direnci ve biyofilm oluşumu. Türkiye 12.Gıda Kongresi, Trakya Üniversitesi, 05-07 Ekim, 2016, Edirne, S136, 13s.
  • [18] Turhan, E.U., Erginkaya, Z., 2016. Gıda endüstrisindeki biyofilmlerin önlenmesinde biyolojik yaklaşımlar. 1st International Mediterranean Science and Engineering Congress (IMSEC 2016), 26-28 October 2016, Adana/Turkey.
  • [19] Turhan, E.U., Erginkaya, Z., Uney, M.H., Ozer, E.A. (2017). Inactivation effect of probiotic biofilms on growth of Listeria monocytogenes. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 23(4), 541-546.
  • [20] Cappitelli, F., Polo, A., Villa, F. (2014). Biofilm formation in food processing environments is still poorly understood and controlled. Food Engineering Reviews, 6, 29–42.
  • [21] Verraes, C., Boxstael S.V., Meervenne, E.V., Coillie, E.V., Butaye, P., Catry, B., Schaetzen, M.A., Huffel, X.V., Imberechts, H., Dierick, K., Daube, G., Saegerman, C., Block, J.D., Dewulf, J., Herman, L. (2013). Antimicrobial resistance in the food chain: a review. International Journal of Environmental Research and Public Health, 10, 2643-2669.
  • [22] Akan, E., Kınık, Ö. (2014). Biyofilm oluşum mekanizması ve biyofilmlerin gıda güvenliğine etkisi. Gıda ve Yem Bilimi - Teknolojisi Dergisi, 14, 42-51.
  • [23] Gün, İ., Ekinci, F.Y. (2009). Biyofilmler: yüzeylerdeki mikrobiyel yaşam. Gıda, 34(3), 165-173.
  • [24] Bridier, A., Briandet, R., Thomas, V., Brissonnet, F.D. (2011). Resistance of bacterial biofilms to disinfectants: a review. Biofouling, 27(9), 1017-1032.
  • [25] Akbas, M.Y., Cag, S. (2016). Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. Food Science and Technology International, 22(7), 587–597.
  • [26] Langsrud, S., Sidhua, M.S., Heir, E., Holck, A.L. (2003). Bacterial disinfectant resistance a challenge for the food industry. International Biodeterioration & Biodegradation, 51, 283-290.
  • [27] Araujo, P., Lemos, M., Mergulhão, F., Melo, L., Simões, M. (2011). Antimicrobial resistance to disinfectants in biofilms. Science against microbial pathogens: communicating current research and technological advances, Edited by A. Mendez Vilas, Formatex Research Center, Badajoz.
  • [28] Srey, S., Jahid, I.K., Ha, S.D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31, 572-585.
  • [29] Turhan, E.U, Kalkan, S., Erginkaya, Z. (2017). The use of phages for the removal of biofilms in the food industry. in: Antimicrobial research: Novel bioknowledge and educational programs, Edited by A. Méndez-Vilas , Formatex Research Center, Badajoz, pp.351-357.
  • [30] Ünal E., Kalkan S., Erginkaya Z. (2010). “Use of Lactic Acid Bacteria Biofilms as Biocontrol Agents”. Science and Technology Aganist Microbial Pathogens. Research, Development and Evalution. Edited by A. Méndez-Vilas, Formatex Research Center, Badajoz.
  • [31] Kubota, H., Senda, S., Tokuda, H., Uchiyama, H., Nomura, N. (2009). Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiology, 26, 592-597.
  • [32] Singh, S., Singh, S.K., Chowdhury, I., Singh, R. (2017). Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. The Open Microbiology Journal, 11, 53-62.
  • [33] Brooks, J.D., Flint, S.H. (2008). Biofilms in the food industry: problems and potential solutions. International Journal of Food Science and Technology, 43, 2163-2176.
  • [34] Kubota, H., Senda, S., Tokuda, H., Uchiyama, H., Nomura, N. (2008). Biofilm formation by lactic acid bacteria and resistance to environmental stress. Journal of Bioscience and Bioengineering, 106(4), 381-386.
  • [35] Ibusquize, P.S., Herrera, J.J.R., Cabo, M.L. (2011). Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiology, 28, 418-425.
  • [36] Davidson, P.M., Harrison, M.A. (2002). Resistance and adaptation to food antimicrobials, sanitizers, and other process controls. Food Technology, 56(11), 69-78.
  • [37] Mah, T.F.C., Otoole, G.A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9(1), 34-39.
  • [38] Stewart, P.S., Costerton, J.W. (2001). Antibiotic resistance of bacteria in biofilms. The Lancet, 358, 135-138.
  • [39] Hoiby, N., Bjarnsholt T., Givskov, M., Molin, S., Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35, 322-332.
  • [40] Simoes, M., Simoes, L.C., Vieira, M.J. (2010). A review of current and emergent biofilm control strategies. LWT - Food Science and Technology 43: 573-583.
  • [41] Pan, Y., Breidt, F., Kathariou, J., Kathariou, S. (2006). Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Applied and Environmental Microbiology, 72(12), 7711-7717.
  • [42] Çağlar, K. (2005). Dezenfektanlara Direnç Gelişim Mekanizmaları? Dezenfeksiyon İşlemini Ne Kadar Tehdit Etmektedir? 4. Ulusal Sterilizasyon Dezenfeksiyon Kongresi, 20-24 Nisan 2005, Samsun/Türkiye.
  • [43] Meral, H., Korukluoğlu, M., 2014. Laktik asit bakterilerinin antibiyotik direnç mekanizmaları. U. Ü. Ziraat Fakültesi Dergisi, 28(2), 71-82.
  • [44] Shemesh, M., Tam, A., Aharoni, R., Steinberg, D. (2010). Genetic adaptation of Streptococcus mutans during biofilm formation on different types of surfaces. BMC Microbiology, 10, 51.
  • [45] Özel B., Şimşek, Ö. (2017). Nisinin sinerjistik antimikrobiyel etkisi. Akademik Gıda, 15(3), 288-299.
  • [46] Afnor Official Distributor of Standards, (2006). EN 1040, NF T 150. https://www.boutique.afnor.org.
There are 46 citations in total.

Details

Primary Language Turkish
Journal Section Review Papers
Authors

Emel Ünal Turhan 0000-0002-0284-574X

Zerrin Erginkaya 0000-0001-6208-2927

Publication Date March 26, 2019
Submission Date March 21, 2018
Published in Issue Year 2019 Volume: 17 Issue: 1

Cite

APA Ünal Turhan, E., & Erginkaya, Z. (2019). Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması. Akademik Gıda, 17(1), 131-139. https://doi.org/10.24323/akademik-gida.544978
AMA Ünal Turhan E, Erginkaya Z. Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması. Akademik Gıda. March 2019;17(1):131-139. doi:10.24323/akademik-gida.544978
Chicago Ünal Turhan, Emel, and Zerrin Erginkaya. “Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması”. Akademik Gıda 17, no. 1 (March 2019): 131-39. https://doi.org/10.24323/akademik-gida.544978.
EndNote Ünal Turhan E, Erginkaya Z (March 1, 2019) Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması. Akademik Gıda 17 1 131–139.
IEEE E. Ünal Turhan and Z. Erginkaya, “Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması”, Akademik Gıda, vol. 17, no. 1, pp. 131–139, 2019, doi: 10.24323/akademik-gida.544978.
ISNAD Ünal Turhan, Emel - Erginkaya, Zerrin. “Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması”. Akademik Gıda 17/1 (March 2019), 131-139. https://doi.org/10.24323/akademik-gida.544978.
JAMA Ünal Turhan E, Erginkaya Z. Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması. Akademik Gıda. 2019;17:131–139.
MLA Ünal Turhan, Emel and Zerrin Erginkaya. “Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması”. Akademik Gıda, vol. 17, no. 1, 2019, pp. 131-9, doi:10.24323/akademik-gida.544978.
Vancouver Ünal Turhan E, Erginkaya Z. Bakteriyel Biyofilmlerdeki Antimikrobiyel Direnç Mekanizması. Akademik Gıda. 2019;17(1):131-9.

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