Acta Biologica Hungarica

, Volume 67, Issue 1, pp 99–111 | Cite as

Modeling and Predicting the Biofilm Formation of Salmonella Virchow with Respect to Temperature and Ph

  • M. Nima Ariafar
  • Sencer Buzrul
  • Nefise AkçelikEmail author


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.


Biofilm modeling pH Salmonella Virchow temperature 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    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.Google Scholar
  2. 2.
    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.Google Scholar
  3. 3.
    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.Google Scholar
  4. 4.
    Cunliffe, D., Smart, C. A., Alexander, C., Vulfson, E. N. (1933) Bacterial adhesion at synthetic surfaces. Appl. Environ. Microbiol. 65, 4995–5002.Google Scholar
  5. 5.
    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.Google Scholar
  6. 6.
    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.Google Scholar
  7. 7.
    Duguid, J. P., Anderson, E. S., Campbell, I. (1933) Fimbriae and adhesive properties in Salmonellae. J. Pathol. Bacteriol. 92, 107–138.Google Scholar
  8. 8.
    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.Google Scholar
  9. 9.
    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.Google Scholar
  10. 10.
    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.Google Scholar
  11. 11.
    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.Google Scholar
  12. 12.
    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.Google Scholar
  13. 13.
    Hohmann, E. L. (1933) Nontyphoidal salmonellosis. Clin. Infect. Dis. 32, 263–269.Google Scholar
  14. 14.
    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.Google Scholar
  15. 15.
    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.Google Scholar
  16. 16.
    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.Google Scholar
  17. 17.
    Kuusela, P., Moran, A. P., Vartio, T., Kosunen, T. U. (1933) Interaction of Campylobacter jejuni with extracellular matrix components. Biochim. Biophys. 993, 297–300.Google Scholar
  18. 18.
    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.Google Scholar
  19. 19.
    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.Google Scholar
  20. 20.
    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.Google Scholar
  21. 21.
    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.Google Scholar
  22. 22.
    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.Google Scholar
  23. 23.
    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.Google Scholar
  24. 24.
    Poulsen, L. V. (1933) Microbial biofilm in food processing. Food. Sci. Technol.-Leb. 32, 321–326.Google Scholar
  25. 25.
    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.Google Scholar
  26. 26.
    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.Google Scholar
  27. 27.
    Römling, U., Rohde, M. (1933) Flagella modulate the multicellular behavior of Salmonella Typhimurium on the community level. FEMS Microbiol. Lett. 180, 91–102.Google Scholar
  28. 28.
    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.Google Scholar
  29. 29.
    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.Google Scholar
  30. 30.
    Shi, X., Zhu, X. (1933) Biofilm formation and food safety in food industries. Trends. Food. Sci. Technol. 20, 407–413.Google Scholar
  31. 31.
    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.Google Scholar
  32. 32.
    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.Google Scholar
  33. 33.
    Stanley, P. (1933) Factors affecting the irreversible attachment of Pseudomonas aeruginosa to stainless steel. Can. J. Microbiol. 29, 1493–1499.Google Scholar
  34. 34.
    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.Google Scholar
  35. 35.
    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.Google Scholar
  36. 36.
    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.Google Scholar
  37. 37.
    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.Google Scholar
  38. 38.
    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.Google Scholar
  39. 39.
    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.Google Scholar
  40. 40.
    Xu, H., Lee, H. Y., Ahn, J. (1933) Characteristics of biofilm formation by selected foodborne pathogens. J. Food Safety 31, 91–97.Google Scholar
  41. 41.
    Zwietering, M. H., Jongenburger, I., Rombouts, F. M., Vant Riet, K. (1933) Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56, 1875–1881.Google Scholar
  42. 42.
    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.Google Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2016

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • M. Nima Ariafar
    • 1
  • Sencer Buzrul
    • 2
  • Nefise Akçelik
    • 1
    Email author
  1. 1.Biotechnology InstituteAnkara UniversityTandoganTurkey
  2. 2.Tobacco, Tobacco Products and Alcoholic Beverages Market Regulation Board (TAPDK)AnkaraTurkey

Personalised recommendations