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Evaluation of Antimicrobial and Antibiofilm Activities of Lactic Acid Bacteria (LAB) Against Citrobacter spp. Isolates

Year 2023, , 27 - 36, 01.03.2023

Safiye Elif Korcan , Sevim Feyza Erdoğmuş , Mine Erik , Arzu Ünal , Beytullah Kenar

https://doi.org/10.35414/akufemubid.1149039

Abstract

The aim of this research was to evaluate the antimicrobial and antibiofilm effects of LABs against Citrobacter isolates. In this study, Citrobacter isolates (C1, C2, C3) which were identified as Citrobacter braakii with the BD PhoenixTM automation system. Biofilm formation investigated by Congo red agar method and microtiter plate method. Acording to antibiogram test results, all isolates was resistance to ampicillin, amoxicillin-clavulanate. Antimicrobial activity test results revealed that extracts of LABs (Lactococcus lactis (L1), Lactobacillus fermentum (L2), Enterococcus faecalis (L3), Lactobacillus casei (L4), Lactobacillus plantarum (L5), Enterococcus faecium (L6), Lactobacillus curvatus (L7), Enterococcus durans (L8) Lactococcus garviae (L9), Enterococcus faecalis (L10)) extracts have an antimicrobial effect on Citrobacter braakii. The highest antimicrobial effect determined on C2 isolate and the lowest effect determined on C3. According to antibiofilm test results, it was observed that high doses of L1, L2, L4, L6, L7, L8 extracts inhibited biofilm formation in all Citrobacter isolates.

Keywords

Antibiotic resistance Biofilm Citrobacter spp. Lactic Acid Bacteria

References

  • Aydemir-Hançer, D., 2018. The biological significance of bacterial biofilms and effective control strategies. Turkish Journal of Life Sciences, 3(1), 218-230.
  • Bae, I.K., Park, I., Lee, J.J., Sun, H.I., Park, K.S., Lee, J.E., 2010. Novel variants of the qnrB gene, qnrB22 and qnrB23, in Citrobacter werkmanii and Citrobacter freundii. Antimicrobrobial Agents and Chemotheraphy, 54, 3068-3069.
  • Bayram, M. and Yıldırım, Z., 2016. Isolation of bacteriocin producing bacterium (Enterococcus faecium) from white cheese and characterization of its bacteriocin. Gaziosmanpasa Journal of Scientific Research, 13, 103-115.
  • Bendjeddou, K., Fons, M., Strocker, P., Sadoun, D., 2012. Characterization and purification of a bacteriocin from Lactobacillus paracasei subsp. paracasei BMK2005, an intestinal isolate active against multidrug-resistant pathogens. World Journal of Microbiology and Biotechnology, 28 (4), 1543-1552.
  • Carminati, D., Giraffa, G., Quiberoni, A., Binetti, A., Suárez, V., Reinheimer, J., 2010. Advances and trends in starter cultures for dairy fermentations. Biotechnology of lactic acid bacteria novel applications edited by Fernanda Mozzi, Raul R. Raya and Graciela M. Vignolo Blackwell Publishing, 177-192.
  • Cerning J., 1990. Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiology Reviews, 87, 113-130.
  • Ciccio, P., Vergara, Di A., Festino, A.R., Paludi, D., Zanardi, E., Ghidini S., Lanieri, A., 2015. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control, 50, 930-936.
  • Corcoran, M., Morris, D., De Lappe N., O'Connorb, J., Lalor, P., Dockery, P., Cormican, M., 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Applied and Environmental Microbiology, 80(4), 1507-1514. Costerton, J.W., 1999. Introduction to biofilm. International Journal of Antimicrobial Agents, 11, 217-221. Deziel, E., Comeau, Y., Villemur, R., 2001. Initiation of biofilm formation by P. aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. Journal of Bacteriology, 183, 1195-1204.
  • Dinçer, E., Kıvanç, M., Karaca, H., 2010. Lactic acid bacteria as biopreservative and bacteriocins. Journal of Food, 35 (1), 1-8.
  • Dixon, M., Flint, S., Palmer, J., Love, R., Biggs, P., Beuger, A., 2018. Analysis of culturable and non-culturable bacteria and their potential to form biofilms in a primary treated dairy wastewater system. Environmental Technology, 39, 17.
  • Donlan, R.M. and Costerton, J.W., 2002. Biofilms: survival mechanisms of clinically relevant microorganisms, Clinical Microbiology Reviews, 15, 167-193.
  • Doran, T.I., 1999. The role of Citrobacter in clinical disease of children: review. Clinical Infectious Disease, 28, 384-394.
  • Erdoğmuş, S.F. and Korcan, S.E., 2017. Researches on Science and Art in 21 st Century Turkey, Chapter: Investıgatıons of bacteriocins produced by lactic acid bacteria, 1, 1497-1503.
  • Galvez, A., Abriouel, H., Lopez, R.L., Omar, N.B., 2007. Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology, 120, 51-70.
  • Gomes, F., Martins, N., Ferreira, I.C.F.R., Henriques, M., 2019. Anti-biofilm activity of hydromethanolic plant extracts against Staphylococcus aureus isolates from bovine mastitis. Heliyon, 5(5), e01728. Gün, İ. and Ekinci, F.Y., 2009. Biofilms: microbial life of surfaces, Journal of Food, 34 (3), 165-173.
  • Ifeadike, C.O. Ironkwe, O.C. Adogu, P.O. Nnebue, C.C. Emelumadu, O.F. Nwabueze, S.A., 2012. Prevalence and pattern of bacteria and intestinal parasites among food handlers in the Federal Capital Territory of Nigeria. Nigerian Medical Journal, 53, 166-171.
  • Liu, L., Lan, R., Liu, L., Wang, Y., Zhang, Y., Wang, Y., Xu, J., 2017. Antimicrobial resistance and cytotoxicity of Citrobacter spp. in Maanshan Anhui province, China. Frontiers Microbiology, 8, 1357.
  • Looijesteijn PJ, Trapet L, de Vries E, Abee T and Hugenholtz J., 2001. Physiological function of exopolysaccharides produced by Lactococcus lactis. International Journal of Food Microbiology, 64 (1-2), 71-80.
  • Magnusson, J. and Schnürer, J., 2001. Lactobacillus coryniformis subsp.coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied and Environmental Microbiology, 67, 1-5.
  • Mah, T.F.C. and O’Toole, G.A., 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9, 34-39.
  • Marshall, V.M. and Rawson, H.L., 1999. Effects of exopolysaccharide producing strains of thermophilic lactic acid bacteria on texture of stirred yoghurt. International Journal of Food Science and Technology, 34, 137-143.
  • Nada, T., Baba, H., Kawamura, K., Ohkura, T., Torii, K., Ohta, M., 2004. A small outbreak of third generation cephem-resistant Citrobacter freundii infection on a surgical ward. Japanese Journal of Infection Disease, 57, 181-182.
  • Pasteris, S.E., Guidoli, M.G., Otero, M.C., Bühler, M.I., Nader-Macías, E.M., 2011. In vitro inhibition of Citrobacter freundii, a red-leg syndrome associated pathogen in raniculture, by indigenous Lactococcus lactis CRL 1584. Veterinary Microbiology, 151(3), 336-344.
  • Percival, S.L., Suleman Vuotto, L., C. Donelli, G., 2015. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. Journal of Medical Microbiology, 64, 323-334.
  • Pringsulaka, O., Thongngam, N., Suwannasai, N., Atthakor, W., Pothıvejkul, K., Rangsıruji, A., 2012. Partial characterization of bacteriocins produced by lactic acid bacteria isolated from Thai fermented meat and fish. Food Control, 23, 547-551.
  • Priyadarshini Rani, K.L. and Ramaswamy, R., 2016. Isolation and antibiotic sensitivity pattern of Citrobacter species with ESBL and AmpC detection at tertiary care hospital, Bangalore. Journal of Evolution Medical and Dental Science, 5(30), 1553-1556.
  • Rashid, M.H. and Kornberg, A., 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, 97, 4885-4890.
  • Rybalchenko, O.V., Bondarenko, V.M., Orlova, O.G., Markov, A.G., Amasheh, S., 2015. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation. Archieves of Microbiology, 197 (8), 1027-1032.
  • Schillinger, U. and Luke, F.K., 1989. Antibacterial activity of Lactobacillus sakei isolated from meat. Applied and Environmental Microbiology, 55(8), 1901-1906.
  • Settanni, L., Miceli A., Francesca, N., Cruciata, M., Moschetti, G., 2013. Microbiological investigation of Raphanus sativus L. grown hydroponically in nutrient solutions contaminated with spoilage and pathogenic bacteria. International Journal of Food Microbiology, 160, 344-352.
  • Srinivasan, R., Kumawat, D.K., Kumar, S., Kumar Saxena, A., 2013. Purification and characterization of a bacteriocin from Lactobacillus rhamnosus L34. Annals of Microbiology, 63(1), 387-392.
  • Subramanian, P., Umadevi, S., Kumar, S., Stephen, S., 2012. Determination of correlation between biofilm and extended spectrum β lactamases producers of Enterobacteriaceae. Scholars Research Journal, 2(1), 2-6.
  • Syne, S., Ramsubhag, A., Adesiyun, A., 2013. Microbiological hazard analysis of ready-to-eat meats processed at a food plant in Trinidad, West Indies. Infection Ecology and Epidemiology, 19, 3.
  • Szczuka, E. and Kaznowski, A., 2014. Antimicrobial activity of tigecycline alone or in combination with rifampin against Staphylococcus epidermidis in biofilm, Folia Microbiology, 59, 283-288.
  • Tamime, A.Y., Skriver, A., Nilsson, L.E., 2006. Starter cultures. Fermented Milks, 2, 11-52.
  • Tassew, H., Abdissa, A., Beyene, G., Gebre-Selassie, S., 2010. Microbial flora and food borne pathogens on minced meat and their susceptibility to antimicrobial agents. Ethiopian Journal of Health Sciences, 20, 137-143.
  • Tallon, R, Bressollier P. and Urdaci M.C., 2013. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Research in Microbiology, 154(10), 705-712.
  • Thenmozhi, R., Nithyanand, P., Rathna, J., Karutha Pandian, S., 2009. Antibiofilm activity of coral- associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunology Medical Microbiology, 57, 284-294.
  • Uludağ Altun, H. and Şener, B., 2008. Biofilm infections and antimicrobial resistance. Hacettepe Medical Journal, 39, 82-88.

Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi

Year 2023, , 27 - 36, 01.03.2023

Safiye Elif Korcan , Sevim Feyza Erdoğmuş , Mine Erik , Arzu Ünal , Beytullah Kenar

https://doi.org/10.35414/akufemubid.1149039

Abstract

Bu çalışmanın amacı; Citrobacter izolatlarına karşı laktik asit bakterilerinin antimikrobiyal ve antibiyofilm aktivitelerini belirlemektir. Bu çalışmada kullanılan Citrobacter izolatları (C1, C2, C3) BD PhoenixTM otomasyon sistemi ile Citrobacter braakii olarak tanımlanmıştır. Biyofilm oluşumu Kongo kırmızılı agar ve mikrotitrasyon plak metodu kullanılarak incelenmiştir. Antibiyogram test sonuçlarına göre, tüm izolatlar amfisilin ve amoksilin-klavulanata karşı dirençli bulunmuştur. Antimikrobiyal aktivite test sonuçları laktik asit bakterilerinden elde edilen ekstraktların (Lactococcus lactis (L1), Lactobacillus fermentum (L2), Enterococcus faecalis (L3), Lactobacillus casei (L4), Lactobacillus plantarum (L5), Enterococcus faecium (L6), Lactobacillus curvatus (L7), Enterococcus durans (L8) Lactococcus garviae (L9), Enterococcus faecalis (L10)) Citrobacter braakii üzerinde antimikrobiyal ve antibiyofilm etkinliğinin olduğu saptanmıştır. En yüksek antimikrobiyal etki C2 izolatı üzerinde ve en düşük etki C3 izolatı üzerinde belirlenmiştir. Antibiyofilm test sonuçlarına göre L1, L2, L4, L6, L7, L8 ekstraktlarının en yüksek dozlarının tüm Citrobacter izolatlarında biyofilm oluşumunu engellendiği görülmüştür.

Keywords

Antibiyobiyotik direnci Biyofilm Citrobacter spp. Laktik Asit Bakterileri

References

  • Aydemir-Hançer, D., 2018. The biological significance of bacterial biofilms and effective control strategies. Turkish Journal of Life Sciences, 3(1), 218-230.
  • Bae, I.K., Park, I., Lee, J.J., Sun, H.I., Park, K.S., Lee, J.E., 2010. Novel variants of the qnrB gene, qnrB22 and qnrB23, in Citrobacter werkmanii and Citrobacter freundii. Antimicrobrobial Agents and Chemotheraphy, 54, 3068-3069.
  • Bayram, M. and Yıldırım, Z., 2016. Isolation of bacteriocin producing bacterium (Enterococcus faecium) from white cheese and characterization of its bacteriocin. Gaziosmanpasa Journal of Scientific Research, 13, 103-115.
  • Bendjeddou, K., Fons, M., Strocker, P., Sadoun, D., 2012. Characterization and purification of a bacteriocin from Lactobacillus paracasei subsp. paracasei BMK2005, an intestinal isolate active against multidrug-resistant pathogens. World Journal of Microbiology and Biotechnology, 28 (4), 1543-1552.
  • Carminati, D., Giraffa, G., Quiberoni, A., Binetti, A., Suárez, V., Reinheimer, J., 2010. Advances and trends in starter cultures for dairy fermentations. Biotechnology of lactic acid bacteria novel applications edited by Fernanda Mozzi, Raul R. Raya and Graciela M. Vignolo Blackwell Publishing, 177-192.
  • Cerning J., 1990. Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiology Reviews, 87, 113-130.
  • Ciccio, P., Vergara, Di A., Festino, A.R., Paludi, D., Zanardi, E., Ghidini S., Lanieri, A., 2015. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control, 50, 930-936.
  • Corcoran, M., Morris, D., De Lappe N., O'Connorb, J., Lalor, P., Dockery, P., Cormican, M., 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Applied and Environmental Microbiology, 80(4), 1507-1514. Costerton, J.W., 1999. Introduction to biofilm. International Journal of Antimicrobial Agents, 11, 217-221. Deziel, E., Comeau, Y., Villemur, R., 2001. Initiation of biofilm formation by P. aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. Journal of Bacteriology, 183, 1195-1204.
  • Dinçer, E., Kıvanç, M., Karaca, H., 2010. Lactic acid bacteria as biopreservative and bacteriocins. Journal of Food, 35 (1), 1-8.
  • Dixon, M., Flint, S., Palmer, J., Love, R., Biggs, P., Beuger, A., 2018. Analysis of culturable and non-culturable bacteria and their potential to form biofilms in a primary treated dairy wastewater system. Environmental Technology, 39, 17.
  • Donlan, R.M. and Costerton, J.W., 2002. Biofilms: survival mechanisms of clinically relevant microorganisms, Clinical Microbiology Reviews, 15, 167-193.
  • Doran, T.I., 1999. The role of Citrobacter in clinical disease of children: review. Clinical Infectious Disease, 28, 384-394.
  • Erdoğmuş, S.F. and Korcan, S.E., 2017. Researches on Science and Art in 21 st Century Turkey, Chapter: Investıgatıons of bacteriocins produced by lactic acid bacteria, 1, 1497-1503.
  • Galvez, A., Abriouel, H., Lopez, R.L., Omar, N.B., 2007. Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology, 120, 51-70.
  • Gomes, F., Martins, N., Ferreira, I.C.F.R., Henriques, M., 2019. Anti-biofilm activity of hydromethanolic plant extracts against Staphylococcus aureus isolates from bovine mastitis. Heliyon, 5(5), e01728. Gün, İ. and Ekinci, F.Y., 2009. Biofilms: microbial life of surfaces, Journal of Food, 34 (3), 165-173.
  • Ifeadike, C.O. Ironkwe, O.C. Adogu, P.O. Nnebue, C.C. Emelumadu, O.F. Nwabueze, S.A., 2012. Prevalence and pattern of bacteria and intestinal parasites among food handlers in the Federal Capital Territory of Nigeria. Nigerian Medical Journal, 53, 166-171.
  • Liu, L., Lan, R., Liu, L., Wang, Y., Zhang, Y., Wang, Y., Xu, J., 2017. Antimicrobial resistance and cytotoxicity of Citrobacter spp. in Maanshan Anhui province, China. Frontiers Microbiology, 8, 1357.
  • Looijesteijn PJ, Trapet L, de Vries E, Abee T and Hugenholtz J., 2001. Physiological function of exopolysaccharides produced by Lactococcus lactis. International Journal of Food Microbiology, 64 (1-2), 71-80.
  • Magnusson, J. and Schnürer, J., 2001. Lactobacillus coryniformis subsp.coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied and Environmental Microbiology, 67, 1-5.
  • Mah, T.F.C. and O’Toole, G.A., 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9, 34-39.
  • Marshall, V.M. and Rawson, H.L., 1999. Effects of exopolysaccharide producing strains of thermophilic lactic acid bacteria on texture of stirred yoghurt. International Journal of Food Science and Technology, 34, 137-143.
  • Nada, T., Baba, H., Kawamura, K., Ohkura, T., Torii, K., Ohta, M., 2004. A small outbreak of third generation cephem-resistant Citrobacter freundii infection on a surgical ward. Japanese Journal of Infection Disease, 57, 181-182.
  • Pasteris, S.E., Guidoli, M.G., Otero, M.C., Bühler, M.I., Nader-Macías, E.M., 2011. In vitro inhibition of Citrobacter freundii, a red-leg syndrome associated pathogen in raniculture, by indigenous Lactococcus lactis CRL 1584. Veterinary Microbiology, 151(3), 336-344.
  • Percival, S.L., Suleman Vuotto, L., C. Donelli, G., 2015. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. Journal of Medical Microbiology, 64, 323-334.
  • Pringsulaka, O., Thongngam, N., Suwannasai, N., Atthakor, W., Pothıvejkul, K., Rangsıruji, A., 2012. Partial characterization of bacteriocins produced by lactic acid bacteria isolated from Thai fermented meat and fish. Food Control, 23, 547-551.
  • Priyadarshini Rani, K.L. and Ramaswamy, R., 2016. Isolation and antibiotic sensitivity pattern of Citrobacter species with ESBL and AmpC detection at tertiary care hospital, Bangalore. Journal of Evolution Medical and Dental Science, 5(30), 1553-1556.
  • Rashid, M.H. and Kornberg, A., 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, 97, 4885-4890.
  • Rybalchenko, O.V., Bondarenko, V.M., Orlova, O.G., Markov, A.G., Amasheh, S., 2015. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation. Archieves of Microbiology, 197 (8), 1027-1032.
  • Schillinger, U. and Luke, F.K., 1989. Antibacterial activity of Lactobacillus sakei isolated from meat. Applied and Environmental Microbiology, 55(8), 1901-1906.
  • Settanni, L., Miceli A., Francesca, N., Cruciata, M., Moschetti, G., 2013. Microbiological investigation of Raphanus sativus L. grown hydroponically in nutrient solutions contaminated with spoilage and pathogenic bacteria. International Journal of Food Microbiology, 160, 344-352.
  • Srinivasan, R., Kumawat, D.K., Kumar, S., Kumar Saxena, A., 2013. Purification and characterization of a bacteriocin from Lactobacillus rhamnosus L34. Annals of Microbiology, 63(1), 387-392.
  • Subramanian, P., Umadevi, S., Kumar, S., Stephen, S., 2012. Determination of correlation between biofilm and extended spectrum β lactamases producers of Enterobacteriaceae. Scholars Research Journal, 2(1), 2-6.
  • Syne, S., Ramsubhag, A., Adesiyun, A., 2013. Microbiological hazard analysis of ready-to-eat meats processed at a food plant in Trinidad, West Indies. Infection Ecology and Epidemiology, 19, 3.
  • Szczuka, E. and Kaznowski, A., 2014. Antimicrobial activity of tigecycline alone or in combination with rifampin against Staphylococcus epidermidis in biofilm, Folia Microbiology, 59, 283-288.
  • Tamime, A.Y., Skriver, A., Nilsson, L.E., 2006. Starter cultures. Fermented Milks, 2, 11-52.
  • Tassew, H., Abdissa, A., Beyene, G., Gebre-Selassie, S., 2010. Microbial flora and food borne pathogens on minced meat and their susceptibility to antimicrobial agents. Ethiopian Journal of Health Sciences, 20, 137-143.
  • Tallon, R, Bressollier P. and Urdaci M.C., 2013. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Research in Microbiology, 154(10), 705-712.
  • Thenmozhi, R., Nithyanand, P., Rathna, J., Karutha Pandian, S., 2009. Antibiofilm activity of coral- associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunology Medical Microbiology, 57, 284-294.
  • Uludağ Altun, H. and Şener, B., 2008. Biofilm infections and antimicrobial resistance. Hacettepe Medical Journal, 39, 82-88.
There are 39 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Safiye Elif Korcan 0000-0001-7875-5516

Sevim Feyza Erdoğmuş 0000-0002-4319-7558

Mine Erik 0000-0003-4703-5131

Arzu Ünal 0000-0003-4427-3169

Beytullah Kenar 0000-0001-6573-680X

Publication Date March 1, 2023
Submission Date July 26, 2022
Published in Issue Year 2023

Cite

APA Korcan, S. E., Erdoğmuş, S. F., Erik, M., Ünal, A., et al. (2023). Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, 23(1), 27-36. https://doi.org/10.35414/akufemubid.1149039
AMA Korcan SE, Erdoğmuş SF, Erik M, Ünal A, Kenar B. Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. March 2023;23(1):27-36. doi:10.35414/akufemubid.1149039
Chicago Korcan, Safiye Elif, Sevim Feyza Erdoğmuş, Mine Erik, Arzu Ünal, and Beytullah Kenar. “Laktik Asit Bakterilerinin (LAB) Citrobacter Spp. İzolatlarına Karşı Antimikrobiyal Ve Antibiyofilm Aktivitelerinin Değerlendirilmesi”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 23, no. 1 (March 2023): 27-36. https://doi.org/10.35414/akufemubid.1149039.
EndNote Korcan SE, Erdoğmuş SF, Erik M, Ünal A, Kenar B (March 1, 2023) Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 23 1 27–36.
IEEE S. E. Korcan, S. F. Erdoğmuş, M. Erik, A. Ünal, and B. Kenar, “Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi”, Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 23, no. 1, pp. 27–36, 2023, doi: 10.35414/akufemubid.1149039.
ISNAD Korcan, Safiye Elif et al. “Laktik Asit Bakterilerinin (LAB) Citrobacter Spp. İzolatlarına Karşı Antimikrobiyal Ve Antibiyofilm Aktivitelerinin Değerlendirilmesi”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 23/1 (March 2023), 27-36. https://doi.org/10.35414/akufemubid.1149039.
JAMA Korcan SE, Erdoğmuş SF, Erik M, Ünal A, Kenar B. Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2023;23:27–36.
MLA Korcan, Safiye Elif et al. “Laktik Asit Bakterilerinin (LAB) Citrobacter Spp. İzolatlarına Karşı Antimikrobiyal Ve Antibiyofilm Aktivitelerinin Değerlendirilmesi”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 23, no. 1, 2023, pp. 27-36, doi:10.35414/akufemubid.1149039.
Vancouver Korcan SE, Erdoğmuş SF, Erik M, Ünal A, Kenar B. Laktik Asit Bakterilerinin (LAB) Citrobacter spp. İzolatlarına Karşı Antimikrobiyal ve Antibiyofilm Aktivitelerinin Değerlendirilmesi. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2023;23(1):27-36.


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