Skip to main content
SpringerLink
Log in

Enteric Viral Surrogate Reduction by Chitosan

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

Enteric viruses are a major problem in the food industry, especially as human noroviruses are the leading cause of nonbacterial gastroenteritis. Chitosan is known to be effective against some enteric viral surrogates, but more detailed studies are needed to determine the precise application variables. The main objective of this work was to determine the effect of increasing chitosan concentration (0.7–1.5 % w/v) on the cultivable enteric viral surrogates, feline calicivirus (FCV-F9), murine norovirus (MNV-1), and bacteriophages (MS2 and phiX174) at 37 °C. Two chitosans (53 and 222 kDa) were dissolved in water (53 kDa) or 1 % acetic acid (222 KDa) at 0.7–1.5 %, and were then mixed with each virus to obtain a titer of ~5 log plaque-forming units (PFU)/mL. These mixtures were incubated for 3 h at 37 °C. Controls included untreated viruses in phosphate-buffered saline and viruses were enumerated by plaque assays. The 53 kDa chitosan at the concentrations tested reduced FCV-F9, MNV-1, MS2, and phi X174 by 2.6–2.9, 0.1–0.4, 2.6–2.8, and 0.7–0.9 log PFU/mL, respectively, while reduction by 222 kDa chitosan was 2.2–2.4, 0.8–1.0, 2.6–5.2, and 0.5–0.8 log PFU/mL, respectively. The 222 kDa chitosan at 1 and 0.7 % w/v in acetic acid (pH 4.5) caused the greatest reductions of MS2 by 5.2 logs and 2.6 logs, respectively. Overall, chitosan treatments showed the greatest reduction of MS2, followed by FCV-F9, phi X174, and MNV-1. These two chitosans may contribute to the reduction of enteric viruses at the concentrations tested but would require use of other hurdles to eliminate food borne viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Badawy, M., & Rabea, E. I. (2009). Potential of the biopolymer chitosan with different molecular weights to control postharvest gray mold of tomato fruit. Postharvest Biology and Technology, 51, 110–117.

    Article  CAS  Google Scholar 

  • Bae, J., & Schwab, K. J. (2008). Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Applied and Environmental Microbiology, 74, 477–484.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bidawid, S., Farber, J. M., & Sattar, S. A. (2000). Contamination of foods by food handlers: Experiments on hepatitis A virus transfer to food and its interruption. Applied and Environmental Microbiology, 66, 2759–2763.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bozkurt, H., D’Souza, D. H., & Davidson, P. M. (2014). Thermal inactivation of human norovirus surrogates in spinach and measurement of its uncertainty. Journal of Food Protection, 77(2), 276–283.

    Article  PubMed  Google Scholar 

  • Brentlinger, K. L., Hafenstein, S., Novak, C. R., Fane, B. A., Borgon, R., McKenna, R., & Agbandje-McKenna, M. (2002). Microviridae, a family divided: Isolation, characterization, and genome sequence of phi MH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibriobacteriovirus. Journal of Bacteriology, 184, 1089–1094.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cannon, J. L., Papafragkou, E., Park, G. W., Osborne, J., Jaykus, L. A., & Vinje, J. (2006). Surrogates for the study of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection, 69, 2761–2765.

    PubMed  Google Scholar 

  • Chirkov, S. N. (2002). The antiviral activity of chitosan (review). Applied Biochemistry and Microbiology, 38, 1–8.

    Article  CAS  Google Scholar 

  • Cromeans, T., Park, G. W., Costantini, V., Lee, D., Wang, Q., Farkas, T., et al. (2014). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environmental Microbiology, 80(18), 5743–5751.

    Article  PubMed Central  PubMed  Google Scholar 

  • Davis, R., Zivanovic, S., D’Souza, D. H., & Davidson, P. M. (2012). Effectiveness of chitosan on the inactivation of enteric viral surrogates. Food Microbiology, 32, 57–62.

    Article  CAS  PubMed  Google Scholar 

  • Devlieghere, F., Vermeulen, A., & Debevere, J. (2004). Chitosan: antimicrobial activity, interactions with food components and applicability as a coating on fruit and vegetables. Food Microbiology, 21, 703–714.

    Article  CAS  Google Scholar 

  • D’Souza, D. H., Sair, A., Williams, K., Papafragkou, E., Jean, J., Moore, C., & Jaykus, L. (2006). Persistence of caliciviruses on environmental surfaces and their transfer to food. International Journal of Food Microbiology, 108, 84–91.

    Article  PubMed  Google Scholar 

  • El Ghaouth, A., Arul, J., Asselin, A., & Benhamou, N. (1992). Antifungal activity of chitosan on post-harvest pathogens: Induction of morphological and cytological alterations in Rhizopus stolonifer. Mycological Research, 96, 769–779.

    Article  Google Scholar 

  • Hall, A. J., Lopman, B. A., Payne, D. C., Patel, M. M., Gastanaduy, P. A., Vinje, J., & Parashar, U. D. (2013). Norovirus disease in the United States. Emerging Infectious Disease, 19, 1198–1205.

    Article  Google Scholar 

  • Hall, A. J., Wikswo, M. E., Pringle, K., Gould, L. H., & Parashar, U. D. (2014). Vital signs: Foodborne norovirus outbreaks—United States, 2009-2012. Morbidity and Mortality Weekly Report, 63, 491–495.

    PubMed  Google Scholar 

  • Helander, I. M., Nurmiaho-Lassila, E. L., Ahvenainen, R., Rhoades, J., & Roller, S. (2001). Chitosan disrupts the barrier properties of the outer membrane of gram-negative bacteria. International Journal of Food Microbiology, 71, 235–244.

    Article  CAS  PubMed  Google Scholar 

  • Kochkina, Z. M., & Chirkov, S. N. (2000). Effect of chitosan derivatives on the reproduction of coliphages T2 and T7. Microbiology, 69, 208–211.

    Article  CAS  Google Scholar 

  • Kong, M., Chen, X. G., Liu, C. S., Liu, C. G., Meng, X. H., & Yu, L. J. (2008). Antibacterial mechanism of chitosan microspheres in a solid dispersing system against E. coli. Colloids Surfaces B: Biointerfaces, 65, 197–202.

    Article  CAS  PubMed  Google Scholar 

  • Langlet, J., Gaboriaud, F., & Gantzer, C. (2007). Effects of pH on plaque forming unit counts and aggregation of MS2 bacteriophage. Journal of Applied Microbiology, 103, 1632–1638.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Du, Y. M., Wang, X. H., & Sun, L. P. (2004). Chitosan kills bacteria through cell membrane damage. International Journal of Food Microbiology, 95, 147–155.

    Article  CAS  Google Scholar 

  • Liu, J., Tian, S., Meng, X., & Xu, Y. (2007). Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Postharvest Biology and Technology, 44, 300–306.

    Article  CAS  Google Scholar 

  • Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., et al. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5, 607–625.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pospieszny, H., Chirkov, S., & Atabekov, J. (1991). Induction of antiviral resistance in plants by chitosan. Plant Science, 79, 63–68.

    Article  CAS  Google Scholar 

  • Rabea, E. I., Badawy, M. E., Stevens, C. V., Smagghe, G., & Steurbaut, W. (2003). Chitosan as antimicrobial agent: Applications and mode of action. Biomacromolecules, 4, 1457–1465.

    Article  CAS  PubMed  Google Scholar 

  • Reddy, M. V. B., Belkacemi, K. R., Corcuff, R., Castaigne, F., & Arul, J. (2000). Effect of pre-harvest chitosan sprays on post-harvest infection by Botrytis cinerea and quality of strawberry fruit. Postharvest Biology and Technology, 20, 39–51.

    Article  Google Scholar 

  • Sair, A. I., D’Souza, D. H., & Jaykus, L. A. (2002a). Human enteric viruses as causes of foodborne disease. Comprehensive Reviews in Food Science and Food Safety, 1, 73–89.

    Article  CAS  Google Scholar 

  • Sair, A. I., D’Souza, D. H., Moe, C. L., & Jaykus, L. A. (2002b). Improved detection of human enteric viruses in foods by RT-PCR. Journal of Virological Methods, 100, 57–69.

    Article  CAS  PubMed  Google Scholar 

  • Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Disease, 17(1), 7–15.

    Article  Google Scholar 

  • Seyfarth, F., Schliemann, S., Elsner, P., & Hipler, U. C. (2008). Antifungal effect of high- and low-molecular-weight chitosan hydrochloride, carboxymethyl chitosan, chitosan oligosaccharide and N-acetyl-d-glucosamine against Candida albicans, Candida krusei and Candida glabrata. International Journal of Pharmaceutics, 353, 139–148.

    CAS  PubMed  Google Scholar 

  • Shahidi, F., Arachchi, J. K. V., & Jeon, Y.-J. (1999). Food applications of chitin and chitosans. Trends in Food Science and Technology, 10, 37–51.

    Article  CAS  Google Scholar 

  • Su, X., Zivanovic, S., & D’Souza, D. H. (2009). Effect of chitosan on the infectivity of murine norovirus, feline calicivirus, and bacteriophage MS2. Journal of Food Protection, 72, 2623–2628.

    CAS  PubMed  Google Scholar 

  • Sudarshan, N. R., Hoover, D. G., & Knorr, D. (1992). Antibacterial action of chitosan. Food Biotechnology, 6, 257–272.

    Article  CAS  Google Scholar 

  • Wang, G. H. (1992). Inhibition and inactivation of 5 species of foodborne pathogens by chitosan. Journal of Food Protection, 55, 916–919.

    Google Scholar 

  • Wobus, C. E., Thackray, L. B., & Virgin, H. W. (2006). Murine norovirus: a model system to study norovirus biology and pathogenesis. Journal of Virology, 80, 5104–5112.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng, L.-Y., & Zhu, J.-F. (2003). Study on antimicrobial activity of chitosan with different molecular weights. Carbohydrate Polymers, 54, 527–530.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the funding for this research that was provided by the Tennessee Agricultural Experiment Station Hatch Fund (TEN 398) and UT Innovation Grants program funding to D. D’Souza and S. Zivanovic. The authors gratefully acknowledge the assistance provided by Primex for the 222 kDa chitosan used in the research.

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, University of Tennessee, 2605 River Drive, Knoxville, TN, 37996, USA

    Robert Davis, Svetlana Zivanovic, P. Michael Davidson & Doris H. D’Souza

Authors
  1. Robert Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana Zivanovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Michael Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Doris H. D’Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Doris H. D’Souza.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

As this article does not contain any studies with human participants or animals performed by any of the authors, informed consent was not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davis, R., Zivanovic, S., Michael Davidson, P. et al. Enteric Viral Surrogate Reduction by Chitosan. Food Environ Virol 7, 359–365 (2015). https://doi.org/10.1007/s12560-015-9208-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-015-9208-2

Keywords

Search

Navigation