Abstract
Biofilm formation of Salmonella Virchow was monitored with respect to time at three different temperature (20, 25 and 27.5 °C) and pH (5.2, 5.9 and 6.6) values. As the temperature increased at a constant pH level, biofilm formation decreased while as the pH level increased at a constant temperature, biofilm formation increased. Modified Gompertz equation with high adjusted determination coefficient (R2 adj) and low mean square error (MSE) values produced reasonable fits for the biofilm formation under all conditions. Parameters of the modified Gompertz equation could be described in terms of temperature and pH by use of a second order polynomial function. In general, as temperature increased maximum biofilm quantity, maximum biofilm formation rate and time of acceleration of biofilm formation decreased; whereas, as pH increased; maximum biofilm quantity, maximum biofilm formation rate and time of acceleration of biofilm formation increased. Two temperature (23 and 26 °C) and pH (5.3 and 6.3) values were used up to 24 h to predict the biofilm formation of S. Virchow. Although the predictions did not perfectly match with the data, reasonable estimates were obtained. In principle, modeling and predicting the biofilm formation of different microorganisms on different surfaces under various conditions could be possible.
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Austin, J. W., Sanders, G., Kay, W. W., Collinson, S. K. (1933) Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162, 295–301.
Castelijn, G. A. A., Van Der Veen, S., Zwietering, M. H., Moezelaar, R., Abee, T. (1933) Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling 28, 51–63.
Chavant, P., Martinie, B., Meylheuc, T., Bellon-Fontaine, M. N., Hebraud, M. (1933) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl. Environ. Microbiol. 68, 728–737.
Cunliffe, D., Smart, C. A., Alexander, C., Vulfson, E. N. (1933) Bacterial adhesion at synthetic surfaces. Appl. Environ. Microbiol. 65, 4995–5002.
Dewanti, R., Wong, A. C. L. (1933) Influence of culture conditions on biofilm formation by Escherichia coli O157:H7. Int. J. Food Microbiol. 26, 147–164.
Di Bonaventura, G., Piccolomini, R., Paludi D. Diorio, V., Vergara, A., Conter, M. (1933) Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 104, 1552–1561.
Duguid, J. P., Anderson, E. S., Campbell, I. (1933) Fimbriae and adhesive properties in Salmonellae. J. Pathol. Bacteriol. 92, 107–138.
Frank, J. F., Koffi, R. A. (1933) Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. J. Food Prot. 53, 550–554.
Gerstel, U., Römling, U. (1933) Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella Typhimurium. Environ. Microbiol. 3, 638–648.
Gibson, H., Taylor, J. H., Hall, K. E., Holah, J. T. (1933) Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J. Appl. Microbiol. 87, 41–48.
Gorski, L., Palumbo, J., Mandrell, R. (1933) Attachment of Listeria monocytogenes to radish tissue is dependent upon temperature and flagellar motility. Appl. Environ. Microbiol. 69, 258–266.
Herald, P., Zottola, E. (1933) Scanning electron microscopic examination of Yersinia enterocolitica attached to stainless steel at elevated temperature and pH values. J. Food Prot. 51, 445–448.
Hohmann, E. L. (1933) Nontyphoidal salmonellosis. Clin. Infect. Dis. 32, 263–269.
Hood, S. K., Zottola, E. A. (1933) Isolation and identification of adherent Gram-negative microorganisms from four meat-processing facilities. J. Food. Prot. 60, 1135–1138.
Joseph, B., Otta, S., Karunasagar, I., Karunasagar, I. (1933) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64, 367–372.
Karaca, B., Buzrul, S., Tato, V., Akçelik, N., Akçelik, M. (1933) Modeling and predicting the biofilm formation of different Salmonella strains. J. Food Safety 33, 503–508.
Kuusela, P., Moran, A. P., Vartio, T., Kosunen, T. U. (1933) Interaction of Campylobacter jejuni with extracellular matrix components. Biochim. Biophys. 993, 297–300.
Mafu, A. A., Roy, D., Goulet, J., Magny, P. (1933) Attachment of Listeria monocytogenes to stainless steel, glass, polypropylene, and rubber surfaces after short contact times. J. Food Prot. 53, 742–746.
Mai, Conner, T. D. (1933) Effect of temperature and growth media on the attachment of Listeria monocytogenes to stainless steel. Int. J. Food. Microbiol. 120, 282–286.
Møretrø, T., Vestby, L. K., Nesse, L. L., Hannevik, S., Kotlarz, K., Langsrud, S. (1933) Evaluation of efficiency of disinfectants against Salmonella from the feed industry. J. Appl. Microbiol. 106, 1005–1012.
Nguyen, H. D. N., Yang, Y. S., Yuk, H. G. (1933) Biofilm formation of Salmonella Typhimurium on stainless steel and acrylic surfaces as affected by temperature and pH level. LWT Food Sci. Technol. 55, 383–388.
Norwood, D., Gilmour, A. (1933) The differential adherence capabilities of two Listeria monocytogenes strains in monoculture and multispecies biofilms as a function of temperature. Lett. Appl. Microbiol. 33, 320–324.
Peel, M., Donachie, W., Shaw, A. (1933) Temperature-dependent expression of flagella Listeria monocytogenes studied by electron microscopy, SDS-PAGE and Western blotting. J. Gen. Microbiol. 134, 2171–2178.
Poulsen, L. V. (1933) Microbial biofilm in food processing. Food. Sci. Technol.-Leb. 32, 321–326.
Rode, T., Langsrud, S., Holck, A., Moretro, T. (1933) Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int. J. Food. Microbiol. 116, 372–383.
Römling, U., Bian, Z., Hammar, M., Sierralta, W. D., Normark, S. (1933) Curli fibers are highly conserved between Salmonella Typhimurium and E. coli with respect to operon structure and regulation. J. Bacteriol. 180, 722–731.
Römling, U., Rohde, M. (1933) Flagella modulate the multicellular behavior of Salmonella Typhimurium on the community level. FEMS Microbiol. Lett. 180, 91–102.
Römling, U., Rohde, M., Olsen, A., Normark, S., Reinköster, J. (1933) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella Typhimurium regulatesat least two independent pathways. Mol. Microbiol. 36, 10–23.
Sinde, E., Carballo, J. (1933) Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluoroethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiol. 17, 439–447.
Shi, X., Zhu, X. (1933) Biofilm formation and food safety in food industries. Trends. Food. Sci. Technol. 20, 407–413.
Smoot, L., Pierson, M. (1933) Effect of environmental stress on the ability of Listeria monocytogenes Scott A to food contact surfaces. J. Food Prot. 61, 1293–1298.
Speranza, B., Corbo, M. R., Sinigaglia, M. (1933) Effects of nutritional and environmental conditions on Salmonella sp. biofilm formation. J. Food Sci. 76, 12–16.
Stanley, P. (1933) Factors affecting the irreversible attachment of Pseudomonas aeruginosa to stainless steel. Can. J. Microbiol. 29, 1493–1499.
Steenackers, H., Hermans, K., Vanderleyden, J., De Keersmaecker, S. C. J. (1933) Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Research International. 45, 502–531.
Stepanovic, S., Vukovic, D., Dakic, I., Savic, B., Svabic-Vlahovic, M. (1933) A modified microtiterplate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods. 40, 175–179.
Stepanovic, S., Cirkovic, I., Mijac, V., Svabic-Vlahovic, M. (1933) Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol. 20, 339–343.
Stepanovic, S., Cirkovic, I., Ranin, L., Svabic-Vlahovic, M. (1933) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett. Appl. Microbiol. 38, 428–432.
Tondo, E. C., Machado, T. R. M., Malheiros, P. da S., Padrão, D. K., Carvalho, A. L. de, Brandelli, A. (1933) Adhesion and biocides inactivation of Salmonella on stainless steel and polyethylene. Braz. J. Microbiol. 41, 1027–1037.
Vestby, L. K., Møretrø, T., Langsrud, S., Heir, E., Nesse, L. L. (1933) Biofilm forming abilities of Salmonella are correlated with persistence in fish meal and feed factories. BMC Vet. Res. 5, 1–6.
Xu, H., Lee, H. Y., Ahn, J. (1933) Characteristics of biofilm formation by selected foodborne pathogens. J. Food Safety 31, 91–97.
Zwietering, M. H., Jongenburger, I., Rombouts, F. M., Vant Riet, K. (1933) Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56, 1875–1881.
Zwietering, M. H., De Koos, J. T., Hasenack, B. E., De Wit, J. C., Vant Riet, K. (1933) Modeling bacterial growth as a function of temperature. Appl. Environ. Microbiol. 57, 1094–1101.
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Nima Ariafar, M., Buzrul, S. & Akçelik, N. Modeling and Predicting the Biofilm Formation of Salmonella Virchow with Respect to Temperature and Ph. BIOLOGIA FUTURA 67, 99–111 (2016). https://doi.org/10.1556/018.67.2016.1.8
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DOI: https://doi.org/10.1556/018.67.2016.1.8