Inactivation efficacy of nonthermal plasmaactivated solutions against Newcastle disease virus

Applied and Environmental Microbiology

Volumn 84, Issue 9, 2018, Pages

  Su, Xia ^a   Tian, Ying ^b   Zhou, Hongzhuan ^a   Li, Yinglong ^b   Zhang, Zhenhua ^a   Jiang, Beiyu ^a   Yang, Bing ^a   Zhang, Jue ^b   Fang, Jing ^b  

^a INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

Biological damage; Inactivation efficacy; Newcastle disease virus; Physicochemical property; Plasma activated solution

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; BIOMEDICAL EQUIPMENT; ELECTRON SPIN RESONANCE SPECTROSCOPY; MAGNETIC MOMENTS; NUCLEIC ACIDS; PROTEINS; REDOX REACTIONS; SCANNING ELECTRON MICROSCOPY; SODIUM CHLORIDE;

BIOLOGICAL DAMAGE; ELECTRON SPIN RESONANCE SPECTRA; INACTIVATION EFFICACY; NEWCASTLE DISEASE VIRUS; OXIDATION REDUCTION POTENTIAL; PHYSICOCHEMICAL PROPERTY; REACTIVE OXYGEN AND NITROGEN SPECIES; TOTAL PROTEIN CONCENTRATION;

VIRUSES;

BIOASSAY; DISEASE; DISINFECTION; EFFICIENCY MEASUREMENT; ELECTRICAL CONDUCTIVITY; ELECTRON SPIN RESONANCE; INJURY; MORPHOLOGY; PHYSICOCHEMICAL PROPERTY; PLASMA; PROTEIN; REDOX POTENTIAL; VIRUS;

NEWCASTLE DISEASE VIRUS;

ANIMAL; CHICK EMBRYO; HEMAGGLUTINATION TEST; NEWCASTLE DISEASE; NEWCASTLE DISEASE VIRUS; PHYSIOLOGY; PLASMA GAS; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRUS INACTIVATION;

ANIMALS; CHICK EMBRYO; HEMAGGLUTINATION TESTS; MICROSCOPY, ELECTRON, SCANNING; NEWCASTLE DISEASE; NEWCASTLE DISEASE VIRUS; PLASMA GASES; VIRUS INACTIVATION;

EID: 85045531812     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02836-17     Document Type: Article

References (66)

1. Seal BS, King DJ, Sellers HS. 2000. The avian response to Newcastle disease virus. Dev Comp Immunol 24:257-268. https://doi.org/10.1016/ S0145-305X(99)00077-4
2. Alexander D. 2000. Newcastle disease, other avian paramyxoviruses, and pneumovirus infections, p 63-99. In Saif YM, Glisson JR, Fadly AM, McDougald LR, Swayne D (ed), Diseases of poultry. Iowa State University Press, Ames, IA
3. Ganar K, Das M, Sinha S, Kumar S. 2014. Newcastle disease virus: current status and our understanding. Virus Res 184:71-81. https://doi.org/10 .1016/j.virusres.2014.02.016
4. World Bank. 2011. World livestock disease atlas: a quantitative analysis of global animal health data (2006-2009). The World Bank, Washington, DC. http://documents.worldbank.org/curated/en/323671468179364909/ pdf/668590WP00PUBL00Livestock0Atlas0web.pdf
5. Kaleta EF, Baldauf C. 1988. Newcastle disease in free-living and pet birds, p 197-246. In Alexander DJ (ed), Newcastle disease. Springer, Boston, MA
6. Kim LM, King DJ, Guzman H, Tesh RB, Travassos da Rosa APA, Bueno R, Dennett JA, Afonso CL. 2008. Biological and phylogenetic characterization of pigeon paramyxovirus serotype 1 circulating in wild North American pigeons and doves. J Clin Microbiol 46:3303-3310. https://doi.org/ 10.1128/JCM.00644-08
7. Pchelkina IP, Manin TB, Kolosov SN, Starov SK, Andriyasov AV, Chvala IA, Drygin VV, Yu Q, Miller PJ, Suarez DL. 2013. Characteristics of pigeon paramyxovirus serotype-1 isolates (PPMV-1) from the Russian Federation from 2001 to 2009. Avian Dis 57:2-7. https://doi.org/10.1637/10246-051112-Reg.1
8. Alexander DJ. 2000. Newcastle disease and other avian paramyxoviruses. Rev Sci Tech 19:443-462. https://doi.org/10.20506/rst.19.2.1231
9. Kapczynski DR, Afonso CL, Miller PJ. 2013. Immune responses of poultry to Newcastle disease virus. Dev Comp Immunol 41:447-453. https://doi .org/10.1016/j.dci.2013.04.012
10. Swayne DE, King DJ. 2003. Avian influenza and Newcastle disease. J Am Vet Med Assoc 222:1534-1540. https://doi.org/10.2460/javma.2003.222 .1534
11. 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
12. Niemira BA. 2012. Cold plasma decontamination of foods. Annu Rev Food Sci Technol 3:125-142. https://doi.org/10.1146/annurev-food-022811-101132
13. Pankaj SK, Bueno-Ferrer C, Misra NN, Milosavljević V, O'Donnell CP, Bourke P, Keener KM, Cullen PJ. 2014. Applications of cold plasma technology in food packaging. Trends Food Sci Technol 35:5-17. https:// doi.org/10.1016/j.tifs.2013.10.009
14. Pan J, Yang X, Sun K, Wang J, Sun P, Wu H, Becker KH, Zhu W, Zhang J, Fang J. 2013. Tooth bleaching using low concentrations of hydrogen peroxide in the presence of a nonthermal plasma jet. IEEE Trans Plasma Sci 41:325-329. https://doi.org/10.1109/TPS.2012.2233753
15. Ma R, Wang G, Tian Y, Wang K, Zhang J, Fang J. 2015. Non-thermal plasma-activated water inactivation of food-borne pathogen on fresh produce. J Hazard Mater 300:643-651. https://doi.org/10.1016/j.jhazmat .2015.07.061
16. Xu Y, Tian Y, Ma R, Liu Q, Zhang J. 2016. Effect of plasma activated water on the postharvest quality of button mushrooms, Agaricus bisporus. Food Chem 197:436-444. https://doi.org/10.1016/j.foodchem.2015.10 .144
17. Oehmigen K, Hähnel M, Brandenburg R, Wilke C, Weltmann KD, von Woedtke T. 2010. The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7:250-257. https://doi.org/10.1002/ppap.200900077
18. Kamgang-Youbi G, Herry JM, Meylheuc T, Brisset JL, Bellon-Fontaine MN, Doubla A, Naïtali M. 2009. Microbial inactivation using plasma-activated water obtained by gliding electric discharges. Lett Appl Microbiol 48: 13-18. https://doi.org/10.1111/j.1472-765X.2008.02476.x
19. Burlica R, Grim RG, Shih KY, Balkwill D, Locke BR. 2010. Bacteria inactivation using low power pulsed gliding arc discharges with water spray. Plasma Process Polym 7:640-649. https://doi.org/10.1002/ppap.200900183
20. Traylor MJ, Pavlovich MJ, Karim S, Hait P, Sakiyama Y, Clark DS, Graves DB. 2011. Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44:472001. https://doi.org/10.1088/0022-3727/44/ 47/472001
21. 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. https://doi.org/10.1088/0022-3727/46/17/175203
22. Dobrynin D, Fridman G, Friedman G, Fridman A. 2009. Physical and biological mechanisms of direct plasma interaction with living tissue. New J Phys 11:115020. https://doi.org/10.1088/1367-2630/11/11/115020
23. Oehmigen K, Winter J, Hähnel M, Wilke C, Brandenburg R, Weltmann K-D, von Woedtke T. 2011. Estimation of possible mechanisms of Escherichia coli inactivation by plasma treated sodium chloride solution. Plasma Process Polym 8:904-913. https://doi.org/10.1002/ppap.201000099
24. Zhang Q, Liang Y, Feng H, Ma R, Tian Y, Zhang J, Fang J. 2013. A study of oxidative stress induced by non-thermal plasma-activated water for bacterial damage. Appl Phys Lett 102:203701. https://doi.org/10.1063/1 .4807133
25. Pavlovich MJ, Chang HW, Sakiyama Y, Clark DS, Graves DB. 2013. Ozone correlates with antibacterial effects from indirect air dielectric barrier discharge treatment of water. J Phys D Appl Phys 46:145202. https://doi .org/10.1088/0022-3727/46/14/145202
26. Mohades S, Laroussi M, Sears J, Barekzi N, Razavi H. 2015. Evaluation of the effects of a plasma activated medium on cancer cells. Phys Plasmas 22:122001. https://doi.org/10.1063/1.4933367
27. Park DP, Davis K, Gilani S, Alonzo CA, Dobrynin D, Friedman G, Fridman A, Rabinovich A, Fridman G. 2013. Reactive nitrogen species produced in water by non-equilibrium plasma increase plant growth rate and nutritional yield. Curr Appl Phys 13:S19-S29. https://doi.org/10.1016/j.cap .2012.12.019
28. Alshraiedeh NH, Alkawareek MY, Gorman SP, Graham WG, Gilmore BF. 2013 Atmospheric pressure, nonthermal plasma inactivation of MS2 bacteriophage: effect of oxygen concentration on virucidal activity. J Appl Microbiol 115:1420-1426. https://doi.org/10.1111/jam.12331
29. 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. Transl Vis Sci Technol 3:2. https://doi.org/10.1167/tvst.3.2.2
30. Zimmermann JL, Dumler K, Shimizu T, Morfill GE, Wolf A, Boxhammer V, Schlegel J, Gansbacher B, Anton M. 2011. Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D Appl Phys 44:505201. https://doi.org/10.1088/0022-3727/44/50/505201
31. Aboubakr HA, Williams P, Gangal U, Youssef MM, El-Sohaimy SAA, Bruggeman PJ, Goyal SM. 2015. Virucidal effect of cold atmospheric gaseous plasma on feline calicivirus, a surrogate for human norovirus. Appl Environ Microbiol 81:3612-3622. https://doi.org/10.1128/AEM.00054-15
32. Shen J, Tian Y, Li Y, Ma R, Zhang Q, Zhang J, Fang J. 2016. Bactericidal dffects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep 6:28505. https://doi.org/10.1038/srep28505
33. Crocitto LE, Korns D, Kretzner L, Shevchuk T, Blair SL, Wilson TG, Ramin SA, Kawachi MH, Smith SS. 2004. Prostate cancer molecular markers GSTP1 and hTERT in expressed prostatic secretions as predictors of biopsy results. Urology 64:821-825. https://doi.org/10.1016/j.urology .2004.05.007
34. Tagawa M, Yamaguchi T, Yokosuka O, Matsutani S, Maeda T, Saisho H. 2000 Inactivation of a hepadnavirus by electrolysed acid water. J Antimicrob Chemother 46:363-368. https://doi.org/10.1093/jac/46.3.363
35. Naïtali M, Kamgang-Youbi G, Herry J-M, Bellon-Fontaine M-N, Brisset J-L. 2010 Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma-treated water. Appl Environ Microbiol 76:7662-7664. https://doi.org/10.1128/AEM.01615-10
36. Golkowski M, Golkowski C, Leszczynski J, Plimpton SR, Maslowski P, Foltynowicz A, Ye J, McCollister B. 2012. Hydrogen-peroxide-enhanced nonthermal plasma effluent for biomedical applications. IEEE Trans Plasma Sci 40:1984-1991. https://doi.org/10.1109/TPS.2012.2200910
37. Maeda Y, Igura N, Shimoda M, Hayakawa I. 2003. Bactericidal effect of atmospheric gas plasma on Escherichia coli K-12. Int J Food Sci Technol 38:889-892. https://doi.org/10.1046/j.1365-2621.2003.00746.x
38. Lukes P, Clupek M, Babicky V, Sunka P. 2008. Ultraviolet radiation from the pulsed corona discharge in water. Plasma Sources Sci Technol 17:024012. https://doi.org/10.1088/0963-0252/17/2/024012
39. Sakiyama Y, Tomai T, Miyano M, Graves DB. 2009. Disinfection of E. coli by nonthermal microplasma electrolysis in normal saline solution. Appl Phys Lett 94:161501. https://doi.org/10.1063/1.3122148
40. Lukes P, Appleton AT, Locke BR. 2004. Hydrogen peroxide and ozone formation in hybrid gas-liquid electrical discharge reactors. IEEE Trans Ind Appl 40:60-67. https://doi.org/10.1109/TIA.2003.821799
41. Aubry JM. 1985. Search for singlet oxygen in the decomposition of hydrogen peroxide by mineral compounds in aqueous solutions. J Am Chem Soc 107:5844-5849. https://doi.org/10.1021/ja00307a002
42. Ikawa S, Kitano K, Hamaguchi S. 2010. Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Process Polym 7:33-42. https://doi.org/ 10.1002/ppap.200900090
43. Kim SJ, Chung TH, Bae SH, Leem SH. 2009. Bacterial inactivation using atmospheric pressure single pin electrode microplasma jet with a ground ring. Appl Phys Lett 94:141502. https://doi.org/10.1063/1.3114407
44. - radicals in aqueous solution. J Phys Chem Ref Data 14:1041-1100. https://doi.org/10.1063/1.555739
45. Bruggeman P, Schram DC. 2010. On OH production in water containing atmospheric pressure plasmas. Plasma Sources Sci Technol 19:045025. https://doi.org/10.1088/0963-0252/19/4/045025
46. Cheeseman KH, Slater TF. 1993. An introduction to free radical biochemistry. Br Med Bull 49:481-493. https://doi.org/10.1093/oxfordjournals .bmb.a072625
47. Moisan M, Barbeau J, Moreau S, Pelletier J, Tabrizian M, Yahia LH. 2001. Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. Int J Pharm 226:1-21. https://doi.org/10.1016/S0378-5173(01)00752-9
48. Wu Y, Liang Y, Wei K, Li W, Yao M, Zhang J, Grinshpun SA. 2015. MS2 virus inactivation by atmospheric-pressure cold plasma using different gas carriers and power levels. Appl Environ Microbiol 81:996-1002. https://doi.org/10.1128/AEM.03322-14
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. https:// doi.org/10.1002/ppap.200900088
50. Yu S, Chen Q, Liu J, Wang K, Jiang Z, Sun Z, Zhang J, Fang J. 2015. Dielectric barrier structure with hollow electrodes and its recoil effect. Appl Phys Lett 106:244101. https://doi.org/10.1063/1.4922395
51. Wise MG, Suarez DL, Seal BS, Pedersen JC, Senne DA, King DJ, Kapczynski DR, Spackman E. 2004. Development of a real-time reverse-transcription PCR for detection of Newcastle disease virus RNA in clinical samples. J Clin Microbiol 42:329-338. https://doi.org/10.1128/JCM.42.1.329-338.2004
52. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493-497. https://doi.org/10.1093/oxford journals.aje.a118408
53. Desingu PA, Singh SD, Dhama K, Kumar ORV, Singh R, Singh RK. 2015. A rapid method of accurate detection and differentiation of Newcastle disease virus pathotypes by demonstrating multiple bands in degenerate primer based nested RT-PCR. J Virol Methods 212:47-52. https://doi .org/10.1016/j.jviromet.2014.11.005
54. Goyal SM, Anantharaman S, Ramakrishnan MA, Sajja S, Kim SW, Stanley NJ, Farnsworth JE, Kuehn TH, Raynor PC. 2011. Detection of viruses in used ventilation filters from two large public buildings. Am J Infect Control 39:e30-e38. https://doi.org/10.1016/j.ajic.2010.10.036
55. Westbury HA. 1979. Newcastle disease virus-some properties of Australian strains. Avian Dis 23:564-570. https://doi.org/10.2307/1589731
56. Office International des Epizooties (OIE). 2008. Manual of diagnostic tests and vaccines for terrestrial animals (mammals, birds and bees), 6th ed, vol 1. Office International des Epizooties (OIE), Paris, France
57. McFerson LL. 1993. Understanding ORP's role in the disinfection process. Water Eng Manage 140:29-31
58. Halliwell B. 2006. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312-322. https:// doi.org/10.1104/pp.106.077073
59. Sun P, Wu H, Bai N, Zhou H, Wang R, Feng H, Zhu W, Zhang J, Fang J. 2012 Inactivation of Bacillus subtilis spores in water by a direct-current, cold atmospheric-pressure air plasma microjet. Plasma Process Polym 9:157-164. https://doi.org/10.1002/ppap.201100041
60. Palmer RMJ, Ferrige AG, Moncada S. 1987. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524-526. https://doi.org/10.1038/327524a0
61. Wang G, Zhu R, Yang L, Wang K, Zhang Q, Su X, Yang B, Zhang J, Fang J. 2016. Non-thermal plasma for inactivated-vaccine preparation. Vaccine 34:1126-1132. https://doi.org/10.1016/j.vaccine.2015.10.099
62. Kruger NJ. 1994. The Bradford method for protein quantitation, p 9-15. In Walker JM (ed), Basic protein and peptide protocols. Humana Press, Totowa, NJ
63. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. https://doi.org/10.1016/0003-2697 (76)90527-3
64. Nachamkin I, Panaro NJ, Li M, Ung H, Yuen PK, Kricka LJ, Wilding P. 2001. Agilent 2100 bioanalyzer for restriction fragment length polymorphism analysis of the Campylobacter jejuni flagellin gene. J Clin Microbiol 39:754-757. https://doi.org/10.1128/JCM.39.2.754-757.2001
65. Sun W, Zhao C, Li Y, Wang L, Nie G, Peng J, Wang A, Zhang P, Tian W, Li Q, Song J, Wang C, Xu X, Tian Y, Zhao D, Xu Z, Zhong G, Han B, Ling S, Chang Y-Z, Li Y. 2016. Osteoclast-derived microRNA-containing exosomes selectively inhibit osteoblast activity. Cell Discov 2:16015. https:// doi.org/10.1038/celldisc.2016.15
66. Lu C-Y, Tso D-J, Yang T, Jong Y-J, Wei Y-H. 2002. Detection of DNA mutations associated with mitochondrial diseases by Agilent 2100 bioanalyzer. Clin Chim Acta 318:97-105. https://doi.org/10.1016/S0009-8981(01)00809-9