Yıl 2018, Cilt 43, Sayı 4, Sayfalar 605 - 616 2018-06-15


Meltem Yesilcimen Akbas [1] , Taner Şar [2]

88 160

In this work, the prevention and removal of biofilm formations of B. cereus vegetative cells and spore formations by citric acid (2%) and chlorine (200 ppm) treatments on microtitration plates were investigated. The biofilms were produced in the presence of glucose and milk (TSBG and TSBM) for 24-72 hours. B. cereus biofilms, formed by vegetative cells in TSBG and TSBM were inhibited by citric acid treatments by up to 59% and removed about 38-63%, respectively. However, biofilms of B. cereus spores were prevented about 56% and removed by 40-56%. It was shown that citric acid treatment (2%) could be as effective as chlorine treatment for biofilms of B. cereus vegetative cells and spores. 

Bu çalışmada, önemli bir gıda patojeni olan B. cereus vejetatif hücrelerinin ve sporlarının mikrotitrasyon plaklarında, glukoz ve süt içeren besiyerleri kullanılarak (TSBG ve TSBS) oluşturduğu 24-72 saatlik biyofilmlerinin, %2 sitrik asit ve 200 ppm klor uygulamaları ile önlenmesi ve ortadan kaldırılması araştırılmıştır. B. cereus vejetatif hücrelerinin TSBG ve TSBS besiyerleri kullanıldığında oluşan biyofilmlerinin, sitrik asit uygulamaları ile %59 oranında önlendiği ve %38-63 oranlarında giderildiği belirlenmiştir. B. cereus spor biyofilmlerinin ise, %56 oranında önlenebildiği ve %40-56 oranlarında giderilebildiği görülmüştür. Sitrik asit uygulamasının (%2) oluşan B. cereus vejetatif hücrelerinin ve sporlarının biyofilmleri üzerinde klor kadar etkili olabildiği tespit edilmiştir.

  • Abee, T., Kovács, Á.T., Kuipers, O.P., Van der Veen, S. (2011). Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol, 22(2): 172-179. Abraha, A., Bikila, T., Alemu, S., Muktar, Y. (2017). Bacillus cereus isolation and load from raw cow milk sold in Markets of Haramaya District, eastern Ethiopia. Int. J. Food Contam, 4(1): 15.
  • Akbas, M.Y., Cag, S. (2016). Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. RVCTA, 22(7): 587-597.
  • Akbas, M.Y., Kokumer, T. (2015). The prevention and removal of biofilm formation of Staphylococcus aureus strains isolated from raw milk samples by citric acid treatments. Int J Food Sci Technol, 50(7): 1666-1672.
  • Almasoud, A., Hettiarachchy, N., Rayaprolu, S., Babu, D., Kwon, Y.M., Mauromoustakos, A. (2016). Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157: H7 and Salmonella typhimurium. LWT-Food Sci Technol, 66: 560-564.
  • Almasoud, A., Hettiarachchy, N., Rayaprolu, S., Horax, R., Eswaranandam, S. (2015). Electrostatic spraying of organic acids on biofilms formed by E. coli O157: H7 and Salmonella Typhimurium on fresh produce. Food Res Int., 78: 27-33.
  • Austin, J.W., Berferin, G. (1995). Development of bacterial biofilms in dairy processing lines. J Dairy Res., 62: 509-519.Bennet, R.W., Belay, N. (2001). Bacillus cereus. In Compendium of methods for the microbiological examination of food, Downes, F.P., Ito, K. (Eds.), 4th edition, American Public Health Association, Washington, DC, Chapter 32, pp. 311–316.
  • Bremer, P.J., Fillery, S., McQuillan, A.J. (2006). Laboratory scale clean-in-place (CIP) studies on the effectiveness of different caustic and acid wash steps on the removal of dairy biofilms. Int J Food Microbiol, 106(3): 254-262.
  • Burgess, S.A., Lindsay, D., Flint, S.H. (2010). Thermophilic bacilli and their importance in dairy processing. Int J Food Microbiol, 144(2): 215-225.
  • Carlin, F., Brillard, J., Broussolle, V., Clavel, T., Duport, C., Jobin, M., Guinebretiere, M.H., Auger, S., Sorokine, A., Nguyen-The, C. (2010). Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment. Food Res. Int., 43(7): 1885-1894.
  • Corcoran, M., Morris, D., De Lappe, N., O'connor, J., Lalor, P., Dockery, P., Cormican, M. (2014). Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Appl Environ Microbiol, 80: 1507-1514.
  • Faille, C., Lequette, Y., Ronse, A., Slomianny, C., Garénaux, E., Guerardel, Y. (2010). Morphology and physico-chemical properties of Bacillus spores surrounded or not with an exosporium: consequences on their ability to adhere to stainless steel. Int J Food Microbiol, 143(3): 125-135.
  • Faot, F., Cavalcanti, Y.W., e Bertolini, M.D.M., de Rezende Pinto, L., da Silva, W.J., Cury, A.A.D.B. (2014). Efficacy of citric acid denture cleanser on the Candida albicans biofilm formed on poly (methyl methacrylate): effects on residual biofilm and recolonization process. BMC Oral Health, 14(1): 77.
  • Flemming, H.C., Wingender, J., Mayer, C., Korstgens, V., Borchard, W. (2000). Cohesiveness in biofilm matrix polymers. In Symposia-Society for General Microbiology, Cambridge; Cambridge University Press, pp. 87-106.
  • Flint, S.H., Bremer, P.J., Brooks, J.D. (1997). Biofilms in dairy manufacturing plant description, current concerns and methods of control. Biofouling, 11(1): 81-97.
  • Ghandbari, E.H. (1983). Reactions of Chlorine and Chlorine Dioxide with Free Fatty Acids, Fatty Acid Esters, and Triglycerides. In Water Chlorination: Environmental Impact and Health Effects, Vol. 4 ((Jolley, R.L., Brungs, W.A., Cotruvo, J.A., Cumming, R.B., Mattice, J.S., Jacobs, V.A., Eds.). Ann Arbor Sci. Publ., Ann Arbor. Mich, 167-180.
  • Gómez-López, V.M., Marín, A., Medina-Martínez, M.S., Gil, M.I., Allende, A. (2013). Generation of trihalomethanes with chlorine-based sanitizers and impact on microbial, nutritional and sensory quality of baby spinach. Postharvest Biol Technol., 85: 210-217.
  • Granum, P.E., Lund, T. (1997). Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett, 157(2), 223-228.
  • Grutsch, A.A., Nimmer, P.S., Pittsley, R.H., McKillip, J.L. (2018). Bacillus spp. as Pathogens in the Dairy Industry. Foodborne Diseases, 193-211.
  • Koutina, G., Skibsted, L.H. (2015). Calcium and phosphorus equilibria during acidification of skim milk at elevated temperature. Int Dairy J., 45: 1-7.
  • Kreske, A.C., Ryu, J.H., Pettigrew, C.A., Beuchat, L.R. (2006). Lethality of chlorine, chlorine dioxide, and a commercial produce sanitizer to Bacillus cereus and Pseudomonas in a liquid detergent, on stainless steel, and in biofilm. J Food Prot, 69(11): 2621-2634.
  • Lindsay, D., Brözel, V.S., Mostert, J.F., Von Holy, A. (2000). Physiology of dairy-associated Bacillus spp. over a wide pH range. Int J Food Microbiol., 54(1): 49-62.
  • Lücking, G., Stoeckel, M., Atamer, Z., Hinrichs, J., Ehling-Schulz, M. (2013). Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage. Int J Food Microbiol., 166(2): 270-279.
  • Marchand, S., De Block, J., De Jonghe, V., Coorevits, A., Heyndrickx, M., Herman, L. (2012). Biofilm formation in milk production and processing environments; influence on milk quality and safety. Comp Rev Food Sci Food Safety, 11(2): 133-147.
  • Mittelman, M. W. (1998). Structure and functional characteristics of bacterial biofilms in fluid processing operations. J Dairy Sci., 8(10), 2760-2764.
  • Neal-McKinney, J.M., Lu, X., Duong, T., Larson, C.L., Call, D.R., Shah, D.H., Konkel, M.E. (2012). Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One, 7(9): e43928.
  • Noss, C.I., Dennis, W.H., Olivieri, V.P., 1983. Reactivity of Chlorine Dioxide with Nucleic-acids and Proteins. In Water Chlorination: Environmental Impact and Health Effects, Vol. 4 ((Jolley, R.L., Brungs, W.A., Cotruvo, J.A., Cumming, R.B., Mattice, J.S., Jacobs, V.A., Eds.). Ann Arbor Sci. Publ., Ann Arbor. Mich, 1077–1086.
  • Ntrouka, V., Hoogenkamp, M., Zaura, E., van der Weijden, F. (2011). The effect of chemotherapeutic agents on titanium‐adherent biofilms. Clin Oral Implants, 22(11): 1227-1234.
  • Organji, R.S., Abulreesh, H.H., Elbanna, K., Osman, G.E.H., Khider, M. (2015). Occurrence and characterization of toxigenic Bacillus cereus in food and infant feces. Asian Pac J Trop Biomed., 5(7): 515-520.
  • Oulahal, N., Brice, W., Martial, A. Degraeve, P. (2008). Quantitative analysis of survival of Staphylococcus aureus or Listeria innocua on two types of surfaces: polypropylene and stainless steel in contact with different dairy products. Food Control, 19: 178-185.
  • Pagedar, A., Singh, J. (2012). Influence of physiological cell stages on biofilm formation by Bacillus cereus of dairy origin. Int Dairy J., 23(1): 30-35.
  • Parkar, S.G., Flint, S.H., Palmer, J.S., Brooks, J.D. (2001). Factors influencing attachment of thermophilic bacilli to stainless steel. J Appl Microbiol, 90(6): 901-908.
  • Ramos-Villarroel, A.Y., Martín-Belloso, O., Soliva-Fortuny, R. (2015). Combined effects of malic acid dip and pulsed light treatments on the inactivation of Listeria innocua and Escherichia coli on fresh-cut produce. Food Control, 52: 112-118.
  • Ricke S.C. (2003). Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Sciences, 82: 632-639.
  • Ryu, J.H., Beuchat, L.R. (2005). Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid–based sanitizer. J Food Prot, 68(12), 2614-2622.
  • Sadiq, R., Rodriguez, M.J. (2004). Disinfection by-products (DBPs) in drinking water and predictive models for their occurrence: A review. Sci Total Environ. 321: 21-46.
  • Sánchez, G., Elizaquível, P., Aznar, R., Selma, M.V. (2015). Virucidal effect of high power ultrasound combined with a chemical sanitizer containing peroxyacetic acid for water reconditioning in the fresh-cut industry. Food Control, 52: 126-131.
  • Schaeffer, A.B., Fulton, M.D. (1933). A simplified method of staining endospores. Science, 77(1990): 194-194.
  • Simões, M., Simoes, L.C., Vieira, M.J. (2010). A review of current and emergent biofilm control strategies. LWT-Food Sci Technol, 43(4): 573-583.
  • Stepanović, S., Vuković, D., Dakić, I., Savić, B., Švabić-Vlahović, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods, 40(2): 175-179.
  • Te Giffel, M.C., Beumer, R.R., Leijendekkers, S., Rombouts, F.M. (1996). Incidence of Bacillus cereus and Bacillus subtilis in foods in the Netherlands. Food Microbiology, 13(1), 53-58.
  • Van Haute, S., Sampers, I., Holvoet, K., Uyttendaele, M. (2013). Physicochemical quality and chemical safety of chlorine as a reconditioning agent and wash water disinfectant for fresh-cut lettuce washing. Appl Environ Microbiol, 79(9): 2850-2861.
  • Virto, R., Manas, P., Alvarez, I., Condon, S., Raso, J. (2005). Membrane damage and microbial inactivation by chlorine in the absence and presence of a chlorine-demanding substrate. Appl Environ Microbiol, 71(9): 5022-5028.
  • Waters, B.W., Hung, Y.C. (2014). The effect of organic loads on stability of various chlorine‐based sanitisers. Int J Food Sci Technol, 49(3): 867-875.
  • Zhang, Q.Q., Ye, K.P., Juneja, V.K., Xu, X. (2017). Response surface model for the reduction of Salmonella biofilm on stainless steel with lactic acid, ethanol, and chlorine as controlling factors. Journal of Food Safety, 37(3).1-7.
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Dergi Bölümü Makaleler

Yazar: Meltem Yesilcimen Akbas (Sorumlu Yazar)
Ülke: Turkey

Yazar: Taner Şar

Bibtex @araştırma makalesi { gida410777, journal = {GIDA}, issn = {1300-3070}, eissn = {1309-6273}, address = {Gıda Teknolojisi Derneği}, year = {2018}, volume = {43}, pages = {605 - 616}, doi = {10.15237/gida.GD18041}, title = {B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ}, key = {cite}, author = {Yesilcimen Akbas, Meltem and Şar, Taner} }
APA Yesilcimen Akbas, M , Şar, T . (2018). B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ. GIDA, 43 (4), 605-616. DOI: 10.15237/gida.GD18041
MLA Yesilcimen Akbas, M , Şar, T . "B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ". GIDA 43 (2018): 605-616 <http://dergipark.gov.tr/gida/issue/37107/410777>
RIS TY - JOUR T1 - B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ AU - Meltem Yesilcimen Akbas , Taner Şar Y1 - 2018 PY - 2018 N1 - doi: 10.15237/gida.GD18041 DO - 10.15237/gida.GD18041 T2 - GIDA JF - Journal JO - JOR SP - 605 EP - 616 VL - 43 IS - 4 SN - 1300-3070-1309-6273 M3 - doi: 10.15237/gida.GD18041 UR - http://dx.doi.org/10.15237/gida.GD18041 Y2 - 2018 ER -
EndNote %0 GIDA B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ %A Meltem Yesilcimen Akbas , Taner Şar %T B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ %D 2018 %J GIDA %P 1300-3070-1309-6273 %V 43 %N 4 %R doi: 10.15237/gida.GD18041 %U 10.15237/gida.GD18041
ISNAD Yesilcimen Akbas, Meltem , Şar, Taner . "B. CEREUS BİYOFİLMLERİNİN SİTRİK ASİT UYGULAMALARI İLE KONTROLÜ". GIDA 43 / 4 (Haziran 2018): 605-616. http://dx.doi.org/10.15237/gida.GD18041