Virucidal effect of acidic electrolyzed water and neutral electrolyzed water on avian influenza viruses

Abstract

The virucidal effects of two types of electrolyzed water, acidic electrolyzed water (AEW) and neutral electrolyzed water (NEW), on avian influenza viruses were studied. Virus titers of the highly pathogenic H5N1 virus and the low-pathogenic H9N2 virus irreversibly decreased by >5-log at 1 min after the viruses were mixed with NEW containing ≥43 ppm free available chlorine (FAC), but not with NEW containing <17 ppm FAC. The minimum concentration of FAC for a virucidal effect of NEW was estimated at around 40 ppm. In contrast, the virus titers decreased by >5 log at 1 min after the viruses were mixed with AEW, in which the concentration of the FAC ranged from 72 to 0 ppm. Thus, the virucidal effect of AEW did not depend on the presence of FAC. Reverse transcription polymerase chain reaction amplified fragments of the M and NP genes, but not the complete M gene, from RNA extracted from the AEW-inactivated virus. Moderate morphological changes were found under the electron microscope, although no changes were observed in the electrophoresed proteins of the AEW-inactivated virus. No viral genes were amplified from the RNA extracted from the NEW-inactivated virus, regardless of the length of the targeted genes. No viral particles were detected under the electron microscope and no viral proteins were detected by electrophoresis for the NEW-inactivated virus. Thus, this study demonstrated potent virucidal effects of AEW and NEW and differences in the virucidal mechanism of the two types of electrolyzed water.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 1.

    Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534–1541

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420–428

    CAS  PubMed Central  PubMed  Google Scholar 

  3. 3.

    World Health Organization (2013) Human infection with influenza A(H7N9) virus in China-update. http://www.who.int/csr/don/2013_04_23/en/index.html

  4. 4.

    Huang Y-R, Hung Y-C, Hsu S-Y, Huang Y-W, Hwang D-F (2008) Application of electrolyzed water in the food industry. Food Control 19:329–345

    Article  Google Scholar 

  5. 5.

    Thorn RM, Lee SW, Robinson GM, Greenman J, Reynolds DM (2012) Electrochemically activated solutions: evidence for antimicrobial efficacy and applications in healthcare environments. Eur J Clin Microbiol Infect Dis 31:641–653

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Morita C, Sano K, Morimatsu S, Kiura H, Goto T, Kohno T, Hong W, Miyoshi H, Iwasawa A, Nakamura Y, Tagawa M, Yokosuka O, Saisho H, Maeda T, Katsuoka Y (2000) Disinfection potential of electrolyzed solutions containing sodium chloride at low concentrations. J Virol Methods 85:163–174

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Park GW, Boston DM, Kase JA, Sampson MN, Sobsey MD (2007) Evaluation of liquid- and fog-based application of Sterilox hypochlorous acid solution for surface inactivation of human norovirus. Appl Environ Microbiol 73:4463–4468

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  8. 8.

    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

    CAS  PubMed  Article  Google Scholar 

  9. 9.

    Tanaka N, Fujisawa T, Daimon T, Fujiwara K, Tanaka N, Yamamoto M, Abe T (1999) The effect of electrolyzed strong acid aqueous solution on hemodialysis equipment. Artif Organ 23:1055–1062

    CAS  Article  Google Scholar 

  10. 10.

    Abadias M, Usall J, Oliveira M, Alegre I, Viñas I (2008) Efficacy of neutral electrolyzed water (NEW) for reducing microbial contamination on minimally-processed vegetables. Int J Food Microbiol 123:151–158

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Izumi H (1999) Electrolyzed water as a disinfectant for fresh-cut vegetables. J Food Sci 64:536–539

    CAS  Article  Google Scholar 

  12. 12.

    Imai K, Ogawa H, Bui VN, Inoue H, Fukuda J, Ohba M, Yamamoto Y, Nakamura K (2012) Inactivation of high and low pathogenic avian influenza virus H5 subtypes by copper ions incorporated in zeolite-textile materials. Antivir Res 93:225–233

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Bui VN, Ogawa H, Xininigen, Karibe K, Matsuo K, Awad SSA, Minoungou GL, Yoden S, Haneda H, Ngo LH, Tamaki S, Yamamoto Y, Nakamura K, Saito K, Watanabe Y, Runstadler J, Huettmann F, Happ GM, Imai K (2012) H4N8 subtype avian influenza virus isolated from shorebirds contains a unique PB1 gene and causes severe respiratory disease in mice. Virology 423:77–88

  14. 14.

    Yamada K, Ogawa H, Hara A, Yoshida Y, Yonezawa Y, Karibe K, Nghia VB, Yoshimura H, Yamamoto Y, Yamada M, Nakamura K, Imai K (2009) Mechanism of the antiviral effect of hydroxytyrosol on influenza virus appears to involve morphological change of the virus. Antivir Res 83:35–44

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Lénès D, Deboosere N, Ménard-Szczebara F, Jossent J, Alexandre V, Machinal C, Vialette M (2010) Assessment of the removal and inactivation of influenza viruses H5N1 and H1N1 by drinking water treatment. Water Res 44:2473–2486

    PubMed  Article  Google Scholar 

  16. 16.

    Rice EW, Adcock NJ, Sivaganesan M, Brown JD, Stallknecht DE, Swayne DE (2007) Chlorine inactivation of highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 13:1568–1570

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  17. 17.

    Al-Haq MI, Seo Y, Oshita S, Kawagoe Y (2002) Disinfection effects of electrolyzed oxidizing water on suppressing fruit rot of pear caused by Botryosphaeria berengeriana. Food Res Int 35:657–664

    Article  Google Scholar 

  18. 18.

    Park H, Hung Y-C, Chung D (2004) Effects of chlorine and pH on efficacy of electrolyzed water for inactivating Escherichia coli O157:H7 and Listeria monocytogenes. Int J Food Microbiol 91:13–18

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Scholtissek C (1985) Stability of infectious influenza A viruses to treatment at low pH and heating. Arch Virol 85:1–11

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Al-Haq MI, Sugiyama J, Isobe S (2005) Applications of electrolyzed water in agriculture & food industries. Food Sci Technol Res 11:135–150

    Article  Google Scholar 

  21. 21.

    Venkitanarayanan KS, Ezeike GO, Hung Y-C, Doyle MP (1999) Efficacy of electrolyzed oxidizing water for inactivating Escherichia coli O157:H7, Salmonella enteritidis, and Listeria monocytogenes. Appl Environ Microbiol 65:4276–4279

    CAS  PubMed Central  PubMed  Google Scholar 

  22. 22.

    Hsu S-Y, Kao H-Y (2004) Effects of storage conditions on chemical and physical properties of electrolyzed oxidizing water. J Food Eng 65:465–471

    Article  Google Scholar 

  23. 23.

    Len SV, Hung YC, Chung D, Anderson JL, Erickson MC, Morita K (2002) Effects of storage conditions and pH on chlorine loss on electrolyzed oxidizing (EO) water. J Agric Food Chem 50:209–212

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Beumer RR, Duizer E (2012) Residual viral and bacterial contamination of surfaces after cleaning and disinfection. Appl Environ Microbiol 78:7769–7775

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  25. 25.

    Oomori T, Oka T, Inuta T, Arata Y (2000) The efficiency of disinfection of acidic electrolyzed water in the presence of organic materials. Anal Sci 16:365–369

    CAS  Article  Google Scholar 

  26. 26.

    Park E-J, Alexander E, Taylor GA, Costa R, Kang D-H (2009) The decontaminative effects of acidic electrolyzed water for Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on green onions and tomatoes with differing organic demands. Food Microbiol 26:386–390

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Bonde MR, Nester SE, Khayat A, Smilanick JL, Frederick RD, Schaad NW (1999) Comparison of effects of acidic electrolyzed water and NaOCl on Tilletia indica teliospore germination. Plant Dis 83:627–632

    CAS  Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Sachiko Matsuda for technical assistance. This work was partially supported by a Grant-in-Aid for the Bilateral Joint Projects of The Japan Society for the Promotion of Science, Japan.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Haruko Ogawa.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tamaki, S., Bui, V.N., Ngo, L.H. et al. Virucidal effect of acidic electrolyzed water and neutral electrolyzed water on avian influenza viruses. Arch Virol 159, 405–412 (2014). https://doi.org/10.1007/s00705-013-1840-2

Download citation

Keywords

  • Virus Titer
  • H9N2 Virus
  • Avian Influenza Virus
  • Highly Pathogenic Avian Influenza
  • Free Chlorine