Virucidal effect of cold atmospheric gaseous plasma on feline calicivirus, a surrogate for human norovirus

Applied and Environmental Microbiology

Volumn 81, Issue 11, 2015, Pages 3612-3622

  Aboubakr, Hamada A ^a,c   Williams, Paul ^b   Gangal, Urvashi ^b   Youssef, Mohammed M ^c   El Sohaimy, Sobhy A A ^d   Bruggeman, Peter J ^b   Goyal, Sagar M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c Alexandria University   (Egypt)

^d City of Scientific Research and Technological Applications   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

ARGON; ATMOSPHERIC PRESSURE; FOOD PROCESSING; GAS MIXTURES; GASES; PLASMA APPLICATIONS; PLASMA JETS; VIRUSES; WATER TREATMENT;

FELINE CALICIVIRUS; MINIMALLY PROCESSED; NON-THERMAL TECHNOLOGY; PROCESSING METHOD; RADIO FREQUENCY ATMOSPHERIC PRESSURE PLASMA JET; REACTIVE OXYGEN AND NITROGEN SPECIES; READY-TO-EAT FOODS; VIRUCIDAL ACTIVITY;

NITROGEN PLASMA;

DISTILLATION; FILTER; FOOD PROCESSING; OXIDATION; PLASMA; POWER GENERATION; PROTEIN; VIRUS;

FELINE CALICIVIRUS; MIRIDAE; NOROVIRUS;

AIR; ANTIVIRUS AGENT; ARGON; OXYGEN; PLASMA GAS;

CHEMISTRY; DRUG EFFECTS; FELINE CALICIVIRUS; HUMAN; MICROBIAL VIABILITY; PHARMACOLOGY; PHYSIOLOGY; PLASMA GAS; TIME FACTOR; VIRUS LOAD;

AIR; ANTIVIRAL AGENTS; ARGON; CALICIVIRUS, FELINE; HUMANS; MICROBIAL VIABILITY; OXYGEN; PLASMA GASES; TIME FACTORS; VIRAL LOAD;

EID: 84930022656     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00054-15     Document Type: Article

References (55)

1. Scharff RL. 3 March 2010. Health-related costs from foodborne illness in the United States. http://www.publichealth.lacounty.gov/eh/docs/Report Publication/HlthRelatedCostsFromFoodborneIllinessUS.pdf.
2. Anonymous. 2012. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2010. EFSA J 10:2597. http://dx.doi.org/10.2903/j.efsa .2012.2597.
3. European Center for Disease Prevention and Control. 2013. Factsheet for health professionals. http://www.ecdc.europa.eu/en /healthtopics/norovirus_infection/factsheet-health-professionals /Pages/factsheet_health_professionals.aspx.
4. CDC. 30 December 2014. U.S. trends and outbreaks. http://www.cdc.gov /norovirus/trends-outbreaks.html.
5. European Food Safety Authority. 30 April 2009. Community summary report. Food-borne outbreaks in the European Union in 2007. European Food Safety Authority, Parma, Italy. http://www.efsa.europa .eu/de/efsajournal/doc/271r.pdf.
6. Misra NN, Tiwari BK, Raghavarao KSMS, Cullen PJ. 2011. Nonthermal plasma inactivation of food-borne pathogens. Food Eng Rev 3:159-170. http://dx.doi.org/10.1007/s12393-011-9041-9.
7. Hirneisen KA, Black EP, Cascarino JL, Fino VR, Hoover DG, Kniel KE. 2010. Viral inactivation in foods: a review of traditional and novel foodprocessing technologies. Compr Rev Food Sci Food Saf 9:3-20. http://dx .doi.org/10.1111/j.1541-4337.2009.00092.x.
8. Mormann S, Dabisch-Ruthe M, Becker B. 2010. Inactivation of norovirus in foods: inoculation study using human norovirus. Fleischwirtschaft 90:116-121.
9. Hirneisen KA, Markland SM, Kniel KE. 2011. Ozone inactivation of norovirus surrogates on fresh produce. J Food Prot 74:836-839. http://dx .doi.org/10.4315/0362-028X.JFP-10-438.
10. Feng K, Divers E, Ma Y, Li J. 2011. Inactivation of a human norovirus surrogate, human norovirus virus-like particles, and vesicular stomatitis virus by gamma irradiation. Appl Environ Microbiol 77:3507-3517. http: //dx.doi.org/10.1128/AEM.00081-11.
11. Aboubakr HA, El-Banna AA, Youssef MM, Al-Sohaimy SAA, Goyal SM. 2014. Antiviral effects of Lactococcus lactis on feline calicivirus, a human norovirus surrogate. Food EnvironVirol 6:282-289. http://dx.doi .org/10.1007/s12560-014-9164-2.
12. Graves DB. 2012. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J PhysDAppl Phys 45:263001. http://dx.doi.org/10.1088/0022-3727/45/26/263001.
13. Fridman A. 2008. Plasma chemistry. Cambridge University Press, New York, NY.
14. Bruggeman P, Locke BR. 2013. Assessment of potential applications of plasma with liquid water, p 13-40. In Chu PK, Lu XP (ed), Low temperature plasma technology: methods and applications. CRC Press, Boca Raton, FL.
15. Cecchi JL. 1990. Introduction to plasma concept and discharge, p 14-69. In Rossnagel SM, Cuomo JJ, Westwood WD (ed), Handbook of plasma processing technology, fundamentals, etching, deposition and surface interactions. Noyes Publications, Saddle River, NJ.
16. Azharonok V, Krat'ko L, Nekrashevich YI, Filatova I, Mel'nikova L, Dudchik N, Yanetskaya S, Bologa M. 2009. Bactericidal action of the plasma of high-frequency capacitive and barrier discharges on microorganisms. J Eng Phys Thermophys 82:419-426. http://dx.doi.org/10.1007/s10891-009-0210-0.
17. Fernández A, Noriega E, Thompson A. 2013. Inactivation of Salmonella enterica serovar Typhimurium on fresh produce by cold atmospheric gas plasma technology. Food Microbiol 33:24-29. http://dx.doi.org/10.1016/j.fm.2012.08.007.
18. Liu F, Sun P, Bai N, Tian Y, Zhou H, Wei S, Zhou Y, Zhang J, Zhu W, Becker K. 2010. Inactivation of bacteria in an aqueous environment by a direct current, cold atmospheric pressure air plasma micro jet. Plasma Process Polym 7:231-236. http://dx.doi.org/10.1002/ppap.200900070.
19. Noriega E, Sharma G, Laca A, Diaz M, Kong MG. 2011. Cold atmospheric gas plasma disinfection of chicken muscle and chicken skin contaminated with Listeria monocytogenes. Food Microbiol 28:1293-1300. http://dx.doi.org/10.1016/j.fm.2011.05.007.
20. Alkawareek MY, Algwari QT, Gorman SP, Graham WG, O'Connell D, Gilmore BF. 2012. Application of atmospheric pressure nonthermal plasma for the in vitro eradication of bacterial biofilms. FEMS Immunol Med Microbiol 65:381-384. http://dx.doi.org/10.1111/j.1574-695X.2012.00942.x.
21. Terrier O, Essere B, Yver M, Barthélémy M, Bouscambert-Duchamp M, Kurtz P, van Mechelen D, Morfin F, Billaud G, Ferraris O, Lina B, Rosa-Calatrava M, Moules V. 2009. Cold oxygen plasma technology efficiency against different airborne respiratory viruses. J Clin Virol 45: 119-124. http://dx.doi.org/10.1016/j.jcv.2009.03.017.
22. Zimmermann JL, Dumler K, Shimizu T, Morfill GE, Wolf A, Boxhammer Schlegel VJ, Gansbacher B, Anton M. 2011. Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D Appl Phys 44: 505201. http://dx.doi.org/10.1088/0022-3727/44/50/505201.
23. Alekseev O, Donovan K, Limonnik V, Azizkhan-Clifford J. 2014. Nonthermal dielectric barrier discharge (DBD) plasma suppresses herpes simplex virus type 1 (HSV-1) replication in corneal epithelium. Trans Vis Sci Technol 3:2. http://dx.doi.org/10.1167/tvst.3.2.2.
24. van Gils CAJ, Hofmann S, Boekema BKHL, Brandenburg R, Bruggeman PJ. 2013. Mechanisms of bacterial inactivation in the liquid phase induced by a remote RF cold atmospheric pressure plasma jet. J Phys D Appl Phys 46: 175203. http://dx.doi.org/10.1088/0022-3727/46/17/175203.
25. Hofmann S, Gessel A, Bruggeman P. 2011. Power dissipation, gas temperatures and electron densities of cold atmospheric pressure helium and argon RF plasma jets. Plasma Sources Sci Technol 20:065010. http://dx .doi.org/10.1088/0963-0252/20/6/065010.
26. van Gessel AFH, Alards KMJ, Bruggeman PJ. 2013. NO production in an RF plasma jet at atmospheric pressure. J Phys D Appl Phys 46:265202. http://dx.doi.org/10.1088/0022-3727/46/26/265202.
27. Malik YS, Maherchandani S, Allwood PB, Goyal SM. 2005. Evaluation of animal origin cell cultures for in vitro cultivation of noroviruses. J Appl Res Clin Exp Ther 5:312-317.
28. van Gaens W, Bogaerts A. 2014. Reaction pathways of biomedically active species in an Ar plasma jet. Plasma Sources Sci Technol 23:035015. http://dx.doi.org/10.1088/0963-0252/23/3/035015.
29. van Ham BTJ, Hofmann S, Brandenburg R, Bruggeman PJ. 2014. In situ absolute air, O3 and NO densities in the effluent of a cold RF argon atmospheric pressure plasma jet obtained by molecular beam mass spectrometry. J Phys D Appl Phys 47:224013. http://dx.doi.org/10.1088/0022-3727/47/22/224013.
30. Bruggeman P, Leys C. 2009. Non-thermal plasmas in and in contact with liquids. J Phys D Appl Phys 42:053001. http://dx.doi.org/10.1088/0022-3727/42/5/053001.
31. Kärber G. 1931. 50% end point calculation. Arch Exp Pathol Pharmacol 162:480-483. http://dx.doi.org/10.1007/BF01863914.
32. Satterfield CH, Bonnell AH. 1995. Interferences in the titanium sulfate method for hydrogen peroxide. Anal Chem 27:1174-1175. http://dx.doi .org/10.1021/ac60103a042.
33. Eisenberg GM. 1943. Colorimetric determination of hydrogen peroxide. Ind Eng Chem Anal 15:327-328. http://dx.doi.org/10.1021/i560117a011.
34. Straub TM, Honerzu BK, Orosz-Coghlan P, Dohnalkova A, Mayer BK, Bartholomew RA, Valdez CO, Bruckner-Lea CJ, Gerba CP, Abbaszadegan MA, Nickerson CA. 2007. In vitro cell culture infectivity assay for human noroviruses. Emerg Infect Dis 13:396-403. http://dx.doi.org/10.3201/eid1303.060549.
35. D'Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, Jaykus L. 2006. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol 108:84-91. http://dx.doi.org /10.1016/j.ijfoodmicro.2005.10.024.
36. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus L, Vinjé J. 2006. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J Food Prot 69:2761-2765.
37. Sattar SA, Ali M, Tetro JA. 2011. In vivo comparison of two norovirus surrogates for testing ethanol-based handrubs: the mouse chasing the cat! PLoS One 6:e17340. http://dx.doi.org/10.1371/journal.pone.0017340.
38. Park GW, Barclay L, Macinga D, Charbonneau D, Pettigrew CA, Vinjé J. 2010. Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. J Food Prot 73:2232-2238.
39. Butot S, Putallaz T, Sanchez G. 2008. Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. Int J Food Microbiol 126:30-35. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.04.033.
40. Hury S, Vidal DR, Desor F, Pelletier J, Lagarde T. 1998. A parametric study of the destruction efficiency of Bacillus spores in low pressure oxygen- based plasmas. Lett Appl Microbiol 26:417-421. http://dx.doi.org/10.1046/j.1472-765X.1998.00365.x.
41. Allwood PB, Malik YS, Maherchandani S, Hedberg CW, Goyal SM. 2005. Effect of temperature on the survival of F-specific RNA coliphage, feline calicivirus, and Escherichia coli in chlorinated water. Int J Environ Res Public Health 2:442-446. http://dx.doi.org/10.3390/ijerph2005030008.
42. Niemira BA. 2012. Cold plasma reduction of Salmonella and Escherichia coli O157:H7 on almonds using ambient pressure gases. J Food Sci 77: M171. http://dx.doi.org/10.1111/j.1750-3841.2011.02594.x.
43. Lu XP, Ye T, Cao YG, Sun ZY, Xiong Q, Tang Z, Xiong Z, Hu J, Jiang Z, Pan Y. 2008. The roles of the various plasma agents in the inactivation of bacteria. J Appl Phys 104:053309. http://dx.doi.org/10.1063/1.2977674.
44. Sureshkumar S, Sankar R, Mandal M, Neogi S. 2010. Effective bacterial inactivation using low temperature radio frequency plasma. Int J Pharm 396:17-22. http://dx.doi.org/10.1016/j.ijpharm.2010.05.045.
45. Chen W, Huang J, Du N, Liu X, Wang X, Lv G-H, Zhang G, Guo L, Yang S. 2012. Treatment of Enterococcus faecalis bacteria by a helium atmospheric cold plasma brush with oxygen addition. J Appl Phys 112: 013304. http://dx.doi.org/10.1063/1.4732135.
46. Winter J, Wende K, Masur K, Iseni S, Dünnbier M, Hammer MU, Tresp H, Weltmann K-D, Reuter S. 2013. Feed gas humidity: a vital parameter affecting a cold atmospheric-pressure plasma jet and plasmatreated human skin cells. J Phys D Appl Phys 46:295401. http://dx.doi.org /10.1088/0022-3727/46/29/295401.
47. Liu DX, Iza F, Wang XH, Kong MG, Rong MZ. 2011. He+O2+H2O plasmas as a source of reactive oxygen species. Appl Phys Lett 98:221501. http://dx.doi.org/10.1063/1.3592775.
48. Boekema BKHL, Hofmann S, van Ham BJT, Bruggeman PJ, Middelkoop E. 2013. Antibacterial plasma at safe levels for skin cells. J PhysDAppl Phys 46:422001. http://dx.doi.org/10.1088/0022-3727/46/42/422001.
49. Yasuda H, Miura T, Kurita H, Takashima K, Mizuno A. 2010. Biological evaluation of DNA damage in bacteriophages inactivated by atmospheric pressure cold plasma. Plasma Process Polym 7:301-308. http://dx.doi.org /10.1002/ppap.200900088.
50. Gulati BR, Allwood PB, Hedberg CW, Goyal SM. 2001. Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce and a food-contact surface. J Food Prot 64:1430-1434.
51. Duizer E, Bijkerk P, Rockx B, de Groot A, Twisk F, Koopmans M. 2004. Inactivation of caliciviruses. Appl Environ Microbiol 70:4538-4543. http: //dx.doi.org/10.1128/AEM.70.8.4538-4543.2004.
52. Kingsley DH, Hoover DG, Papafragkou E, Richards GP. 2002. Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. J Food Prot 65:1605-1609.
53. Nuanualsuwan S, Mariam T, Himathongkham S, Cliver D. 2002. Ultraviolet Inactivation of feline calicivirus, human enteric viruses and coliphages. Photochem Photobiol 76:406-410. http://dx.doi.org/10.1562/0031-8655(2002)0760406UIOFCH2.0.CO2.
54. De Roda Husman AM, Bijkerk P, Lodder W, Van Den Berg H, Pribil W, Cabaj A, Gehringer P, Sommer R, Duizer E. 2004. Calicivirus inactivation by nonionizing (253.7-nanometer-wavelength [UV]) and ionizing (gamma) radiation. Appl Environ Microbiol 70:5089-5093. http: //dx.doi.org/10.1128/AEM.70.9.5089-5093.2004.
55. Khadre MA, Yousef AE. 2002. Susceptibility of human rotavirus to ozone, high pressure and pulsed electric field. J Food Prot 65:1441-1446.