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Inactivation of Adenovirus in Water by Natural and Synthetic Compounds

  • Lucas Ariel Totaro GarciaEmail author
  • Laurita Boff
  • Célia Regina Monte Barardi
  • Markus Nagl
Original Paper
  • 16 Downloads

Abstract

Millions of people use contaminated water sources for direct consumption. Chlorine is the most widely disinfection product but can produce toxic by-products. In this context, natural and synthetic compounds can be an alternative to water disinfection. Therefore, the aim of this study was to assess the inactivation of human adenovirus by N-chlorotaurine (NCT), bromamine-T (BAT) and Grape seed extract (GSE) in water. Distilled water artificially contaminated with recombinant human adenovirus type 5 (rAdV-GFP) was treated with different concentrations of each compound for up to 120 min, and viral infectivity was assessed by fluorescence microscopy. The decrease in activity of the compounds in the presence of organic matter was evaluated in water supplemented with peptone. As results, NCT and GSE inactivated approximately 2.5 log10 of adenovirus after 120 min. With BAT, more than 4.0 log10 decrease was observed within 10 min. The oxidative activity of 1% BAT decreased by 50% in 0.5% peptone within a few minutes, while the reduction was only 30% for 1% NCT in 5% peptone after 60 min. Organic matter had no effect on the activity of GSE. Moreover, the minimal concentration of BAT and GSE to kill viruses was lower than that known to kill human cells. It was concluded that the three compounds have potential to be used for water disinfection for drinking or reuse purposes.

Keywords

N-chlorotaurine Bromamine-T Grape seed extract Water disinfection Adenovirus 

Notes

Acknowledgements

This work was supported by The Brazilian National Council for Scientific and Technological Development (CNPq) [Grant Numbers 420398/2016-3], the Austrian Science Fund (FWF), grant no. KLI459-B30, and the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES). We would like to thank Dr. Martin Hermann (Medical University of Innsbruck) for assistance with fluorescence microscopy, Dr. Flávio Reginatto and Dra. Caroline Ortmann (Federal University of Santa Catarina) for their support on the GSE activity assays and Dr. Leandro Garcia (Cambridge University) for statistical assistance. The authors declare that they have no conflicts of interest.

References

  1. Adámez, J. D., Samino, E. G., Sánchez, E. V., & González-Gómez, D. (2012). In vitro estimation of the antibacterial activity and antioxidant capacity of aqueous extracts from grape-seeds (Vitis vinifera L.). Food Control 24(1–2), 136–141.  https://doi.org/10.1016/j.foodcont.2011.09.016.CrossRefGoogle Scholar
  2. Ashbolt, N. J. (2015). Microbial contamination of drinking water and human health from community water systems. Current Environmental Health Reports, 2(1), 95–106.  https://doi.org/10.1007/s40572-014-0037-5.CrossRefGoogle Scholar
  3. Bofill-Mas, S., Rusiñol, M., Fernandez-Cassi, X., Carratalà, A., Hundesa, A., & Girones, R. (2013). Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. BioMed Research International, 2013, 192089.  https://doi.org/10.1155/2013/192089.
  4. Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT Food Science and Technology, 28(1), 25–30.  https://doi.org/10.1016/S0023-6438(95)80008-5.CrossRefGoogle Scholar
  5. Bright, K. R., & Gilling, D. H. (2016). Natural virucidal compounds in foods. In Viruses in foods (pp. 449–469). Cham: Springer International Publishing.  https://doi.org/10.1007/978-3-319-30723-7_16.CrossRefGoogle Scholar
  6. Brown, V. A., Patel, K. R., Viskaduraki, M., Crowell, J. A., Perloff, M., Booth, T. D., et al. (2010). Repeat dose study of the cancer chemopreventive agent resveratrol in healthy volunteers: Safety, pharmacokinetics, and effect on the insulin-like growth factor axis. Cancer Research, 70(22), 9003–9011.  https://doi.org/10.1158/0008-5472.CAN-10-2364.CrossRefGoogle Scholar
  7. Clescerl, L., Greenberg, A., & Eaton, A. (1999). Standard methods for the examination of water and wastewater. (20th ed.). American Public Health Association.Google Scholar
  8. Corrales, M., Han, J. H., & Tauscher, B. (2009). Antimicrobial properties of grape seed extracts and their effectiveness after incorporation into pea starch films. International Journal of Food Science & Technology, 44(2), 425–433.  https://doi.org/10.1111/j.1365-2621.2008.01790.x.CrossRefGoogle Scholar
  9. D’Souza, D. H. (2014). Phytocompounds for the control of human enteric viruses. Current Opinion in Virology, 4, 44–49.  https://doi.org/10.1016/j.coviro.2013.12.006.CrossRefGoogle Scholar
  10. Dudani, A. K., Martyres, A., & Fliss, H. (2008). Short Communication: Rapid preparation of preventive and therapeutic whole-killed retroviral vaccines using the microbicide taurine chloramine. AIDS Research and Human Retroviruses, 24(4), 635–642.  https://doi.org/10.1089/aid.2007.0149.CrossRefGoogle Scholar
  11. Garcia, L. A. T., Nascimento, M. A., & Barardi, C. R. M. (2015). Effect of UV light on the inactivation of recombinant human adenovirus and murine norovirus seeded in seawater in shellfish depuration tanks. Food and Environmental Virology, 7(1), 67–75.  https://doi.org/10.1007/s12560-014-9177-x.CrossRefGoogle Scholar
  12. Geiger, R., Treml, B., Pinna, A., Barnickel, L., Prossliner, H., Reinstadler, H., et al. (2009). Tolerability of inhaled N-chlorotaurine in the pig model. BMC pulmonary medicine, 9, 33.  https://doi.org/10.1186/1471-2466-9-33.CrossRefGoogle Scholar
  13. Gottardi, W., Debabov, D., & Nagl, M. (2013). N-chloramines, a promising class of well-tolerated topical anti-infectives. Antimicrobial agents and chemotherapy, 57(3), 1107–1114.  https://doi.org/10.1128/AAC.02132-12.CrossRefGoogle Scholar
  14. Gottardi, W., Klotz, S., & Nagl, M. (2014). Superior bactericidal activity of N-bromine compounds compared to their N-chlorine analogues can be reversed under protein load. Journal of Applied Microbiology, 116(6), 1427–1437.  https://doi.org/10.1111/jam.12474.CrossRefGoogle Scholar
  15. Gottardi, W., & Nagl, M. (2002). Chemical properties of N-chlorotaurine sodium, a key compound in the human defence system. Archiv der Pharmazie, 335(9), 411–421.  https://doi.org/10.1002/1521-4184(200212)335:9%3C411::AID-ARDP411>3.0.CO;2-DCrossRefGoogle Scholar
  16. Gottardi, W., & Nagl, M. (2010). N-chlorotaurine, a natural antiseptic with outstanding tolerability. Journal of Antimicrobial Chemotherapy, 65(3), 399–409.  https://doi.org/10.1093/jac/dkp466.CrossRefGoogle Scholar
  17. Gottardi, W., & Nagl, M. (2013). Active halogen compounds and proteinaceous material: loss of activity of topical anti-infectives by halogen consumption. Journal of Pharmacy and Pharmacology, 65(2), 213–218.  https://doi.org/10.1111/j.2042-7158.2012.01589.x.CrossRefGoogle Scholar
  18. Gowda, N. M. M., Trieff, N. M., & Stanton, G. J. (1986). Kinetics of inactivation of adenovirus in water by chloramine-T. Water Research, 20(7), 817–823.  https://doi.org/10.1016/0043-1354(86)90167-3.CrossRefGoogle Scholar
  19. Hofer, E., Neher, A., Gunkel, A. R., & Nagl, M. (2003). In vitro study on the influence of N-chlorotaurine on the ciliary beat frequency of nasal mucosa. American Journal of Rhinology, 17(3), 149–152. http://www.ncbi.nlm.nih.gov/pubmed/12862403.
  20. Jakobek, L. (2015). Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chemistry, 175, 556–567.  https://doi.org/10.1016/J.FOODCHEM.2014.12.013.CrossRefGoogle Scholar
  21. Jayaprakasha, G. K., Selvi, T., & Sakariah, K. K. (2003). Antibacterial and antioxidant activities of grape (Vitis vinifera) seed extracts. Food Research International, 36(2), 117–122.  https://doi.org/10.1016/S0963-9969(02)00116-3.CrossRefGoogle Scholar
  22. Joshi, S. S., Su, X., & D’Souza, D. H. (2015). Antiviral effects of grape seed extract against feline calicivirus, murine norovirus, and hepatitis A virus in model food systems and under gastric conditions. Food Microbiology, 52, 1–10.  https://doi.org/10.1016/j.fm.2015.05.011.CrossRefGoogle Scholar
  23. Kontny, E., Chorazy-Massalska, M., Rudnicka, W., Marcinkiewicz, J., & Maśliński, W. (2006). Cytotoxicity of taurine metabolites depends on the cell type. Advances in Experimental Medicine and Biology, 583, 157–171. http://www.ncbi.nlm.nih.gov/pubmed/17153599.
  24. Kyriakopoulos, A., Logotheti, S., Marcinkiewicz, J., & Nagl, M. (2016). N-chlorotaurine and N-bromotaurine combination regimen for the cure of valacyclovir-unresponsive herpes zoster comorbidity in a multiple sclerosis patient.International Journal of Medical and Pharmaceutical Case Reports, 7(2), 1–6.  https://doi.org/10.9734/IJMPCR/2016/25476.CrossRefGoogle Scholar
  25. La Rosa, G., Fratini, M., della Libera, S., Iaconelli, M., & Muscillo, M. (2012). Emerging and potentially emerging viruses in water environments. Annali dell’Istituto superiore di sanita, 48(4), 397–406.  https://doi.org/10.4415/ANN_12_04_07.CrossRefGoogle Scholar
  26. LeChevallier, M., & Au, K.-K. (2004). Water treatment and pathogen control: Process efficiency in achieving safe drinking water. Geneva: WHO.Google Scholar
  27. Li, D., Baert, L., Zhang, D., Xia, M., Zhong, W., Van Coillie, E., et al. (2012). Effect of grape seed extract on human norovirus GII.4 and murine norovirus 1 in viral suspensions, on stainless steel discs, and in lettuce wash water. Applied and Environmental Microbiology, 78(21), 7572–7578.  https://doi.org/10.1128/AEM.01987-12.CrossRefGoogle Scholar
  28. Marcinkiewicz, J., Wojas-Pelc, A., Walczewska, M., Lipko-Godlewska, S., Jachowicz, R., Maciejewska, A., et al. (2008). Topical taurine bromamine, a new candidate in the treatment of moderate inflammatory acne vulgaris: a pilot study. European journal of dermatology: EJD, 18(4), 433–439.  https://doi.org/10.1684/ejd.2008.0460.Google Scholar
  29. Nagl, M., Larcher, C., & Gottardi, W. (1998a). Activity of N-chlorotaurine against herpes simplex- and adenoviruses. Antiviral research, 38(1), 25–30. http://www.ncbi.nlm.nih.gov/pubmed/9614001.
  30. Nagl, M., Nguyen, V. A., Gottardi, W., Ulmer, H., & Höpfl, R. (2003). Tolerability and efficacy of N-chlorotaurine in comparison with chloramine T for the treatment of chronic leg ulcers with a purulent coating: a randomized phase II study. The British journal of dermatology, 149(3), 590–597. http://www.ncbi.nlm.nih.gov/pubmed/14510994.
  31. Nagl, M., Pfausler, B., Schmutzhard, E., Fille, M., & Gottardi, W. (1998b). Tolerance and bactericidal action of N-chlorotaurine in a urinary tract infection by an omniresistant Pseudomonas aeruginosa. Zentralblatt fur Bakteriologie: international journal of medical microbiology, 288(2), 217–223. http://www.ncbi.nlm.nih.gov/pubmed/9809403.
  32. Nagl, M., Teuchner, B., Pöttinger, E., Ulmer, H., & Gottardi, W. (2000). Tolerance of N-chlorotaurine, a new antimicrobial agent, in infectious conjunctivitis – A phase II pilot study. Ophthalmologica, 214(2), 111–114.  https://doi.org/10.1159/000027477.CrossRefGoogle Scholar
  33. Nair, C. G., Lalithakumari, R., & Senan, P. I. (1978). Bromamine-T as a new oxidimetric titrant. Talanta, 25(9), 525–527. http://www.ncbi.nlm.nih.gov/pubmed/18962313.
  34. OECD. (2010). Test No. 209: Activated Sludge, Respiration Inhibition Test (Carbon and Ammonium Oxidation). OECD Guidelines for the Testing of Chemicals, Sect (2). Paris: OECD Publishing.  https://doi.org/10.1787/9789264070080-en.Google Scholar
  35. Reynolds, K. A., Mena, K. D., & Gerba, C. P. (2008). Risk of waterborne illness via drinking water in the United States. Reviews of environmental contamination and toxicology, 192, 117–158. http://www.ncbi.nlm.nih.gov/pubmed/18020305.
  36. Romanowski, E. G., Yates, K. A., Teuchner, B., Nagl, M., Irschick, E. U., & Gordon, Y. J. (2006). N-Chlorotaurine is an effective antiviral agent against adenovirus in vitro and in the Ad5/NZW rabbit ocular model. Investigative Opthalmology & Visual Science, 47(5), 2021.  https://doi.org/10.1167/iovs.05-1270.
  37. Sánchez-Moreno, C., Larrauri, J. A., & Saura-Calixto, F. (1998). A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture, 76(2), 270–276.CrossRefGoogle Scholar
  38. Sano, A. (2017). Safety assessment of 4-week oral intake of proanthocyanidin-rich grape seed extract in healthy subjects. Food and Chemical Toxicology 108(Pt B), 519–523.  https://doi.org/10.1016/j.fct.2016.11.021.CrossRefGoogle Scholar
  39. Sauerbrei, A., Sehr, K., Brandstädt, A., Heim, A., Reimer, K., & Wutzler, P. (2004). Sensitivity of human adenoviruses to different groups of chemical biocides. Journal of Hospital Infection, 57(1), 59–66.  https://doi.org/10.1016/j.jhin.2004.01.022.CrossRefGoogle Scholar
  40. Singleton, V. L., Orthofer, R., & Lamuela-Raventós, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology, 299, 152–178.  https://doi.org/10.1016/S0076-6879(99)99017-1.CrossRefGoogle Scholar
  41. Su, X., & D’Souza, D. H. (2011). Grape seed extract for control of human enteric viruses. Applied and Environmental Microbiology, 77(12), 3982–3987.  https://doi.org/10.1128/AEM.00193-11.CrossRefGoogle Scholar
  42. Uchio, E., Inoue, H., & Kadonosono, K. (2010). Antiadenoviral effects of N-chlorotaurine in vitro confirmed by quantitative polymerase chain reaction methods. Clinical Ophthalmology, 4, 1325–1329.  https://doi.org/10.2147/OPTH.S14282.CrossRefGoogle Scholar
  43. UN. (2015). A 10 year storyThe water for life decade 2005–2015 and beyond. http://www.un.org/waterforlifedecade/pdf/WaterforLifeENG.pdf. Accessed 9 July 2018.
  44. Walczewska, M., Peruń, A., Białecka, A., Śróttek, M., Jamróz, W., Dorożyński, P., et al. (2017). Comparative analysis of microbicidal and anti-inflammatory properties of novel taurine Bromamine derivatives and Bromamine T. In Advances in experimental medicine and biology (Vol. 975, pp. 515–534).  https://doi.org/10.1007/978-94-024-1079-2_41.
  45. WHO. (2018). Disease burden and mortality estimates. WHO. Geneva: World Health Organization. http://www.who.int/healthinfo/global_burden_disease/estimates/en/. Accessed 3 September 2018.
  46. Yoon, J., Jekle, A., Najafi, R., Ruado, F., Zuck, M., Khosrovi, B., et al. (2011). Virucidal mechanism of action of NVC-422, a novel antimicrobial drug for the treatment of adenoviral conjunctivitis. Antiviral Research, 92(3), 470–478.  https://doi.org/10.1016/j.antiviral.2011.10.009.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Virologia Aplicada/Departamento de Microbiologia, Imunologia e ParasitologiaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Division of Hygiene and Medical MicrobiologyMedical University of InnsbruckInnsbruckAustria

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