DOI QR코드

DOI QR Code

Inactivation of Campylobacter jejuni using Radio-frequency Atmospheric Pressure Plasma on Agar Plates and Chicken Hams

  • Received : 2012.11.26
  • Accepted : 2013.04.28
  • Published : 2013.06.30

Abstract

Radio-frequency driven atmospheric pressure plasma using argon gas was studied in the inactivation of Campylobacter jejuni in order to investigate its applicability. First, the inactivation study was conducted on an agar surface. C. jejuni NCTC11168 was reduced by more than 7 Log CFU after an 88 s treatment. Another strain, ATCC49943, was studied; however, the inactivation was less efficient, with a 5 Log CFU reduction after a 2 min treatment. Then, chicken breast ham was studied at the $10^6$ CFU inoculation level. The inactivation efficiency was much lower for both strains compared to that on the agar plates. C. jejuni NCTC11168 and ATCC49943 were reduced by 3 Log CFU after a 6 min treatment and by 1.5 Log CFU after a 10 min treatment, respectively. The scanning electron microscopy analysis indicated that C. jejuni cells were deformed or transformed into coccoid form under the plasma treatment. During the plasma treatment, the temperature of the samples did not rise above $43^{\circ}C$, suggesting that heat did not contribute to the inactivation. Meanwhile, water activity significantly decreased after a 10 min treatment (p<0.05). This study conveyed that radio-frequency atmospheric pressure plasma can effectively inactivate C. jejuni with strain-specific variation.

Keywords

References

  1. AOAC. (2005) Official methods of analysis of the Association of Analytical Chemistry. Association of Official Analytical Chemists, Washington, DC, USA.
  2. Buck, G. E., Parshall, K. A., and Davis, C. P. (1983) Electron microscopy of the coccoid form of Campylobacter jejuni. J. Clin. Microbiol. 18, 420-421.
  3. Critzer, F. J., Kelly-Wintenberg, K., South, S. L., and Golden, D. A. (2007) Atmospheric plasma inactivation of foodborne pathogens on fresh produce surfaces. J. Food Prot. 70, 2290-2296.
  4. Deng, S., Cheng, C., Ni, G., Meng, Y., and Chen, H. (2010) Bacillus subtilis devitalization mechanism of atmosphere pressure plasma jet. Curr. Appl. Phys. 10, 1164-1168. https://doi.org/10.1016/j.cap.2010.02.004
  5. Dirks, B. P., Dobrynin, D., Fridman, G., Mukhin, Y., Fridman, A., and Quinlan, J. J. (2012) Treatment of raw poultry with nonthermal dielectric barrier discharge plasma to reduce Campylobacter jejuni and Salmonella enterica. J. Food Prot. 75, 22-28. https://doi.org/10.4315/0362-028X.JFP-11-153
  6. Dorrell, N., Mangan, J. A., Laing, K. G., Hinds, J., Linton, D., Al-Ghusein, H., Barrell, B. G., Parkhill, J., Stoker, N. G., Karlyshev, A. V., Butcher, P. D., and Wren, B. W. (2001) Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res. 11, 1706-1715. https://doi.org/10.1101/gr.185801
  7. Fernandez, A., Noriega, E., and Thompson, A. (2013) Inactivation of Salmonella enterica serovar Typhimurium on fresh produce by cold atmospheric gas plasma technology. Food Microbiol. 33, 24-29. https://doi.org/10.1016/j.fm.2012.08.007
  8. He, Y. and Chen, C. Y. (2010) Quantitative analysis of viable, stressed and dead cells of Campylobacter jejuni strain 81-176. Food Microbiol. 27, 439-446. https://doi.org/10.1016/j.fm.2009.11.017
  9. Hofreuter, D., Novik, V., and Galan, J. E. (2008) Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe. 4, 425-433. https://doi.org/10.1016/j.chom.2008.10.002
  10. Hofreuter, D., Tsai, J., Watson, R. O., Novik, V., Altman, B., Benitez, M., Clark, C., Perbost, C., Jarvie, T., Du, L., and Galan, J. E. (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74, 4694-4707. https://doi.org/10.1128/IAI.00210-06
  11. Humphrey, T., O'Brien, S., and Madsen, M. (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int. J. Food Microbiol. 117, 237-257. https://doi.org/10.1016/j.ijfoodmicro.2007.01.006
  12. Jang, K. I., Kim, M. G., Ha, S. D., Kim, K. S., Lee, K. H., Chung, D. H., Kim, C. H., and Kim, K. Y. (2007) Morphology and adhesion of Campylobacter jejuni to chicken skin under varying conditions. J. Microbiol. Biotechnol. 17, 202-206.
  13. Jin, S.-K., Shin, D., and Hur, I.-C. (2011) Effects of moisture content on quality characteristics of dry-cured ham during storage. Korean J. Food Sci. An. 31, 756-762. https://doi.org/10.5851/kosfa.2011.31.5.756
  14. Kim, B., Yun, H., Jung, S., Jung, Y., Jung, H., Choe, W., and Jo, C. (2011) Effect of atmospheric pressure plasma on inactivation of pathogens inoculated onto bacon using two different gas compositions. Food Microbiol. 28, 9-13. https://doi.org/10.1016/j.fm.2010.07.022
  15. Korachi, M., Gurol, C., and Aslan, N. (2010) Atmospheric plasma discharge sterilization effects on whole cell fatty acid profiles of Escherichia coli and Staphylococcus aureus. J. Electrostatics 68, 508-512. https://doi.org/10.1016/j.elstat.2010.06.014
  16. Laroussi, M. (2005) Low temperature plasma-based sterilization: overview and state-of-the-art. Plasma Process Polym. 2, 391-400. https://doi.org/10.1002/ppap.200400078
  17. Moran, A. P. and Upton, M. E. (1987a) Effect of medium supplements, illumination and superoxide dismutase on the production of coccoid forms of Campylobacter jejuni ATCC 29428. J. Appl. Bacteriol. 62, 43-51. https://doi.org/10.1111/j.1365-2672.1987.tb02379.x
  18. Moran, A. P. and Upton, M. E. (1987b) Factors affecting production of coccoid forms by Campylobacter jejuni on solid media during incubation. J. Appl. Bacteriol. 62, 527-537. https://doi.org/10.1111/j.1365-2672.1987.tb02685.x
  19. Moreau, M., Orange, N., and Feuilloley, M. G. (2008) Nonthermal plasma technologies: New tools for bio-decontamination. Biotechnol. Adv. 26, 610-617. https://doi.org/10.1016/j.biotechadv.2008.08.001
  20. Niemira, B. A. and Sites, J. (2008) Cold plasma inactivates Salmonella Stanley and Escherichia coli O157:H7 inoculated on golden delicious apples. J. Food Prot. 71, 1357-1365.
  21. Park, S. F. (2002) The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int. J. Food Microbiol. 74, 177-188. https://doi.org/10.1016/S0168-1605(01)00678-X
  22. Parker, C. T., Quinones, B., Miller, W. G., Horn, S. T., and Mandrell, R. E. (2006) Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J. Clin. Microbiol. 44, 4125-4135. https://doi.org/10.1128/JCM.01231-06
  23. Perni, S., Liu, D. W., Shama, G., and Kong, M. G. (2008a) Cold atmospheric plasma decontamination of the pericarps of fruit. J. Food Prot. 71, 302-308.
  24. Perni, S., Shama, G., and Kong, M. G. (2008b) Cold atmospheric plasma disinfection of cut fruit surfaces contaminated with migrating microorganisms. J. Food Prot. 71, 1619-1625.
  25. Rod, S. K., Hansen, F., Leipold, F., and Knochel, S. (2012) Cold atmospheric pressure plasma treatment of ready-to-eat meat: Inactivation of Listeria innocua and changes in product quality. Food Microbiol. 30, 233-238. https://doi.org/10.1016/j.fm.2011.12.018
  26. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., Jones, J. L., and Griffin, P. M. (2011) Foodborne illness acquired in the United States--major pathogens. Emerg. Infect. Dis. 17, 7-15. https://doi.org/10.3201/eid1701.P11101
  27. Senorans, J., Ibanez, E., and Cifuentes, A. (2003) New trends in food processing. Crit. Rev. Food Sci. Nutr. 43, 507-526. https://doi.org/10.1080/10408690390246341
  28. Serra, X., Ruiz-Ramírez, J., Arnau, J., and Gou, P. (2005) Texture parameters of dry-cured ham m. biceps femoris samples dried at different levels as a function of water activity and water content. Meat Sci. 69, 249-254. https://doi.org/10.1016/j.meatsci.2004.07.004
  29. Srivastava, N., and Wang, C. (2011) Effects of water addition on OH radical generation and plasma properties in an atmospheric argon microwave plasma jet. J. Appl. Phys. 110, 053304. https://doi.org/10.1063/1.3632970
  30. Sureshkumar, A., Sankar, R., Mandal, M., and Neogi, S. (2010) Effective bacterial inactivation using low temperature radio frequency plasma. Int. J. Pharm. 396, 17-22. https://doi.org/10.1016/j.ijpharm.2010.05.045
  31. Tangwatcharin, P., Chanthachum, S., Khopaibool, P., and Griffiths, M. W. (2006) Morphological and physiological responses of Campylobacter jejuni to stress. J. Food Prot. 69, 2747-2753.
  32. Tendero, C., Tixier, C., Tristant, P., Desmaison, J., and Leprince, P. (2006) Atmospheric pressure plasmas: A review. Spectrochimica Acta Part B. 61, 2-30. https://doi.org/10.1016/j.sab.2005.10.003
  33. von Keudell, A., Awakowicz, P., Benedikt, J., Raballand, V., Yanguas-Gil, A., Opretzka, J., Flotgen, C., Reuter, R., Byelykh, L., Halfmann, H., Stapelmann, K., Denis, B., Wunderlich, J., Muranyi, P., Rossi, F., Kylian, O., Hasiwa, N., Ruiz, A., Rauscher, H., Sirghi, L., Comoy, E., Dehen, C., Challier, L., and Deslys, J. P. (2010) Inactivation of bacteria and biomolecules by low-pressure plasma discharges. Plasma Process. Polym. 7, 327-352. https://doi.org/10.1002/ppap.200900121
  34. Wareing, D. R., Bolton, F. J., Fox, A. J., Wright, P. A., and Greenway, D. L. (2002) Phenotypic diversity of Campylobacter isolates from sporadic cases of human enteritis in the UK. J. Appl. Microbiol. 92, 502-509. https://doi.org/10.1046/j.1365-2672.2002.01552.x
  35. Yang, B., Chen, J., Yu, Q., Li, H., Lin, M., Mustapha, A., Hong, L., and Wang, Y. (2011) Oral bacterial deactivation using a lowtemperature atmospheric argon plasma brush. J. Dent. 39, 48-56. https://doi.org/10.1016/j.jdent.2010.10.002
  36. Young, V. B. and Mansfield, L. S. (2005) Campylobacter infection- clinical context. In: Campylobacter molecular and cellular biology. Ketley, J. M. and Konkel, M. E. (ed) Horizon bioscience, UK, pp. 1-12.
  37. Yun, H., Kim, B., Jung, S., Kruk, Z. A., Kim, D. B., Choe, W., and Jo, C. (2010) Inactivation of Listeria monocytogenes inoculated on disposable plastic tray, aluminum foil, and paper cup by atmospheric pressure plasma. Food Control 21, 1182-1186. https://doi.org/10.1016/j.foodcont.2010.02.002

Cited by

  1. Strategies and novel technologies to control Campylobacter in the poultry chain: A review vol.19, pp.4, 2013, https://doi.org/10.1111/1541-4337.12544
  2. Non-thermal plasma: An advanced technology for food industry vol.26, pp.8, 2013, https://doi.org/10.1177/1082013220929474
  3. Application of cold plasma technology in the food industry and its combination with other emerging technologies vol.114, pp.None, 2021, https://doi.org/10.1016/j.tifs.2021.06.004