Food and Environmental Virology

, Volume 3, Issue 1, pp 35–42 | Cite as

Comparison of the Activity of Alcohol-Based Handrubs Against Human Noroviruses Using the Fingerpad Method and Quantitative Real-Time PCR

  • Pengbo Liu
  • David R. Macinga
  • Marina L. Fernandez
  • Carrie Zapka
  • Hui-Mien Hsiao
  • Brynn Berger
  • James W. Arbogast
  • Christine L. MoeEmail author
Original Paper


Noroviruses (NoV) are the most common cause of acute nonbacterial gastroenteritis in the United States, and human hands play an important role in their transmission. Little is known about the efficacy of hand hygiene agents against these highly infectious pathogens. We investigated the activity of seven commercially available hand hygiene products against human noroviruses by in vivo fingerpad tests. The in vivo activity of alcohol-based handrubs ranged from 0.10 to 3.74 log reduction and was not solely dependent on alcohol concentration. A handrub (VF481) based on 70% ethanol and a blend of other skin care ingredients reduced Norwalk virus (NV) by 3.74 log in 15 s and provided significantly greater NV reduction than all the other products tested (P < 0.001). Furthermore, VF481 was the most effective product tested against the NoV genogroup II strains Snow Mountain virus (GII.2) and a GII.4 strain. These results demonstrate that alcohol by itself is not effective against NoV, but effective formulation of alcohol-based handrubs can achieve significant reduction of norovirus RNA on fingers.


Norovirus Quantitative RT-PCR Handrub Fingerpad ASTM 



This work was supported by GOJO Industries, Inc. P. Liu and C. Moe received research funds from GOJO Industries, and D. Macinga, C. Zapka, and J. Arbogast are employees of GOJO Industries. We are grateful to Dr. Kim Green at NIH for her kind gift of the Norwalk Virus full-length cDNA clone and Dr. Michele E. Hardy at Montana State University and Dr. Lee-Ann Jaykus at North Carolina State University for their kind gifts of the Snow Mountain Virus clone and the GII.4 virus. We also thank John Rice for proofreading, Yaping Wang for statistical analyses, and Dr. Lee-Ann Jaykus for critical review of the manuscript.


  1. Belliot, G., Lavaux, A., Souihel, D., Agnello, D., & Pothier, P. (2008). Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Applied and Environmental Microbiology, 74(10), 3315–3318.PubMedCrossRefGoogle Scholar
  2. Bidawid, S., Malik, N., Adegbunrin, O., Sattar, S. A., & Farber, J. M. (2004). Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: Experiments with feline calicivirus as a surrogate. Journal of Food Protection, 67(1), 103–109.PubMedGoogle Scholar
  3. Blanton, L. H., Adams, S. M., Beard, R. S., Wei, G., Bulens, S. N., Widdowson, M. A., et al. (2006). Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000–2004. The Journal of Infectious Diseases, 193(3), 413–421.PubMedCrossRefGoogle Scholar
  4. Butot, S., Putallaz, T., Amoroso, R., & Sanchez, G. (2009). Inactivation of enteric viruses in minimally processed berries and herbs. Applied and Environmental Microbiology, 75(12), 4155–4161.PubMedCrossRefGoogle Scholar
  5. Butot, S., Putallaz, T., & Sanchez, G. (2008). Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. International Journal of Food Microbiology, 126(1–2), 30–35.PubMedCrossRefGoogle Scholar
  6. Cannon, J. L., Papafragkou, E., Park, G. W., Osborne, J., Jaykus, L. A., & Vinje, J. (2006). Surrogates for the study of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection, 69(11), 2761–2765.PubMedGoogle Scholar
  7. Cheng, V. C., Tai, J. W., Ho, Y. Y., & Chan, J. F. (2009). Successful control of norovirus outbreak in an infirmary with the use of alcohol-based hand rub. The Journal of Hospital Infection, 72(4), 370–371.PubMedCrossRefGoogle Scholar
  8. Davis, M. A., Sheng, H., Newman, J., Hancock, D. D., & Hovde, C. J. (2006). Comparison of a waterless hand-hygiene preparation and soap-and-water hand washing to reduce coliforms on hands in animal exhibit settings. Epidemiology and Infection, 134(5), 1024–1028.PubMedCrossRefGoogle Scholar
  9. Duizer, E., Bijkerk, P., Rockx, B., De Groot, A., Twisk, F., & Koopmans, M. (2004). Inactivation of caliciviruses. Applied and Environmental Microbiology, 70(8), 4538–4543.PubMedCrossRefGoogle Scholar
  10. E-1838-02 Standard Test Method for Determining the Virus-Eliminating Effectiveness of Liquid Hygienic Handwash and Handrub Agents Using the Fingerpads of Adult Volunteers (ASTM International, 2002). ASTM International, West Conshohocken, PA.Google Scholar
  11. Gehrke, C., Steinmann, J., & Goroncy-Bermes, P. (2004). Inactivation of feline calicivirus, a surrogate of norovirus (formerly Norwalk-like viruses), by different types of alcohol in vitro and in vivo. The Journal of Hospital Infection, 56(1), 49–55.PubMedCrossRefGoogle Scholar
  12. Hansen, S., Stamm-Balderjahn, S., Zuschneid, I., Behnke, M., Ruden, H., Vonberg, R. P., et al. (2007). Closure of medical departments during nosocomial outbreaks: Data from a systematic analysis of the literature. The Journal of Hospital Infection, 65(4), 348–353.PubMedCrossRefGoogle Scholar
  13. Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557.PubMedCrossRefGoogle Scholar
  14. Kampf, G., Grotheer, D., & Steinmann, J. (2005). Efficacy of three ethanol-based hand rubs against feline calicivirus, a surrogate virus for norovirus. The Journal of Hospital Infection, 60(2), 144–149.PubMedCrossRefGoogle Scholar
  15. Kampf, G., Meyer, B., & Goroncy-Bermes, P. (2003). Comparison of two test methods for the determination of sufficient antimicrobial activity of three commonly used alcohol-based hand rubs for hygienic hand disinfection. The Journal of Hospital Infection, 55(3), 220–225.PubMedCrossRefGoogle Scholar
  16. Kramer, A., Galabov, A. S., Sattar, S. A., Dohner, L., Pivert, A., Payan, C., et al. (2006). Virucidal activity of a new hand disinfectant with reduced ethanol content: Comparison with other alcohol-based formulations. The Journal of Hospital Infection, 62(1), 98–106.PubMedCrossRefGoogle Scholar
  17. Lages, S. L., Ramakrishnan, M. A., & Goyal, S. M. (2008). In vivo efficacy of hand sanitisers against feline calicivirus: A surrogate for norovirus. The Journal of Hospital Infection, 68(2), 159–163.PubMedCrossRefGoogle Scholar
  18. Lindesmith, L., Moe, C., Lependu, J., Frelinger, J. A., Treanor, J., & Baric, R. S. (2005). Cellular and humoral immunity following Snow Mountain virus challenge. Journal of Virology, 79(5), 2900–2909.PubMedCrossRefGoogle Scholar
  19. Lindesmith, L., Moe, C., Marionneau, S., Ruvoen, N., Jiang, X., Lindblad, L., et al. (2003). Human susceptibility and resistance to Norwalk virus infection. Nature Medicine, 9(5), 548–553.PubMedCrossRefGoogle Scholar
  20. Liu, P., Yuen, Y., Hsiao, H. M., Jaykus, L. A., & Moe, C. (2010). Effectiveness of liquid soap and hand sanitizer against Norwalk virus on contaminated hands. Applied and Environmental Microbiology, 76(2), 394–399.PubMedCrossRefGoogle Scholar
  21. Lopman, B. A., Brown, D. W., & Koopmans, M. (2002). Human caliciviruses in Europe. Journal of Clinical Virology, 24(3), 137–160.PubMedCrossRefGoogle Scholar
  22. Macinga, D. R., Sattar, S. A., Jaykus, L. A., & Arbogast, J. W. (2008). Improved inactivation of non-enveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Applied and Environmental Microbiology, 74(16), 5047–5052.PubMedCrossRefGoogle Scholar
  23. Magulski, T., Paulmann, D., Bischoff, B., Becker, B., Steinmann, E., Steinmann, J., et al. (2009). Inactivation of murine norovirus by chemical biocides on stainless steel. BMC Infectious Diseases, 9, 107–113.PubMedCrossRefGoogle Scholar
  24. Mbithi, J. N., Springthorpe, V. S., & Sattar, S. A. (1993). Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin). Applied and Environmental Microbiology, 59(10), 3463–3469.PubMedGoogle Scholar
  25. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., et al. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5(5), 607–625.PubMedCrossRefGoogle Scholar
  26. Moe, C. L., Christmas, W. A., Echols, L. J., & Miller, S. E. (2001). Outbreaks of acute gastroenteritis associated with Norwalk-like viruses in campus settings. Journal of American College Health, 50(2), 57–66.PubMedCrossRefGoogle Scholar
  27. Okunishi, J., Okamoto, K., Nishihara, Y., Tsujitani, K., Miura, T., Matsuse, H., et al. (2010). Investigation of in vitro and in vivo efficacy of a novel alcohol based hand rub, MR06B7. Yakugaku Zasshi-Journal of the Pharmaceutical Society of Japan, 130(5), 747–754.PubMedCrossRefGoogle Scholar
  28. Park, G. W., Barclay, L., Macinga, D., Charbonneau, D., Pettigrew, C. A., & Vinje, J. (2010). Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus and GII.4 norovirus. Journal of Food Protection, 73(12), 2232–2238.PubMedGoogle Scholar
  29. Rodriguez-Lazaro, D., Lombard, B., Smith, H., Rzezutka, A., D’Agostino, M., Helmuth, R., et al. (2007). Trends in analytical methodology in food safety and quality: Monitoring microorganisms and genetically modified organisms. Trends in Food Science and Technology, 18(6), 306–319.CrossRefGoogle Scholar
  30. Sattar, S. A., Abebe, M., Bueti, A. J., Jampani, H., Newman, J., & Hua, S. (2000). Activity of an alcohol-based hand gel against human adeno-, rhino-, and rotaviruses using the fingerpad method. Infection Control and Hospital Epidemiology, 21(8), 516–519.PubMedCrossRefGoogle Scholar
  31. Sattar, S. A., & Ansari, S. A. (2002). The fingerpad protocol to assess hygienic hand antiseptics against viruses. Journal of Virological Methods, 103(2), 171–181.PubMedCrossRefGoogle Scholar
  32. Schwab, K. J., Estes, M. K., Neill, F. H., & Atmar, R. L. (1997). Use of heat release and an internal RNA standard control in reverse transcription-PCR detection of Norwalk virus from stool samples. Journal of Clinical Microbiology, 35(2), 511–514.PubMedGoogle Scholar
  33. Siebenga, J. J., Vennema, H., Zheng, D. P., Vinje, J., Lee, B. E., Pang, X. L., et al. (2009). Norovirus illness is a global problem: Emergence and spread of norovirus GII.4 variants, 2001–2007. Journal of Infectious Diseases, 200(5), 802–812.PubMedCrossRefGoogle Scholar
  34. Straub, T. M., Honer zu Bentrup, K., Orosz-Coghlan, P., Dohnalkova, A., Mayer, B. K., Bartholomew, R. A., et al. (2007). In vitro cell culture infectivity assay for human noroviruses. Emerging Infectious Diseases, 13(3), 396–403.PubMedCrossRefGoogle Scholar
  35. Teunis, P. F., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., et al. (2008). Norwalk virus: How infectious is it? Journal of Medical Virology, 80(8), 1468–1476.PubMedCrossRefGoogle Scholar
  36. Todd, E. C., Greig, J. D., Bartleson, C. A., & Michaels, B. S. (2008). Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 4. Infective doses and pathogen carriage. Journal of Food Protection, 71(11), 2339–2373.PubMedGoogle Scholar
  37. Topping, J. R., Schnerr, H., Haines, J., Scott, M., Carter, M. J., Willcocks, M. M., et al. (2008). Temperature inactivation of Feline calicivirus vaccine strain FCV F-9 in comparison with human noroviruses using an RNA exposure assay and reverse transcribed quantitative real-time polymerase chain reaction—A novel method for predicting virus infectivity. Journal of Virological Methods, 156, 89–95.PubMedCrossRefGoogle Scholar
  38. Weber, D. J., Sickbert-Bennett, E., Gergen, M. F., & Rutala, W. A. (2003). Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands. The Journal of the American Medical Association, 289(10), 1274–1277.CrossRefGoogle Scholar
  39. Widdowson, M. A., Sulka, A., Bulens, S. N., Beard, R. S., Chaves, S. S., Hammond, R., et al. (2005). Norovirus and foodborne disease, United States, 1991–2000. Emerging Infectious Diseases, 11(1), 95–102.PubMedGoogle Scholar
  40. Wu, H. M., Fornek, M., Schwab, K. J., Chapin, A. R., Gibson, K., Schwab, E., et al. (2005). A norovirus outbreak at a long-term-care facility: The role of environmental surface contamination. Infection Control and Hospital Epidemiology, 26(10), 802–810.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2011

Authors and Affiliations

  • Pengbo Liu
    • 1
  • David R. Macinga
    • 2
  • Marina L. Fernandez
    • 3
  • Carrie Zapka
    • 2
  • Hui-Mien Hsiao
    • 4
  • Brynn Berger
    • 5
  • James W. Arbogast
    • 2
  • Christine L. Moe
    • 4
    Email author
  1. 1.Hubert Department of Global HealthRollins School of Public Health, Emory UniversityAtlantaUSA
  2. 2.GOJO Industries, Inc.AkronUSA
  3. 3.Hubert Department of Global HealthRollins School of Public Health, Emory UniversityAtlantaUSA
  4. 4.Hubert Department of Global HealthRollins School of Public Health, Emory UniversityAtlantaUSA
  5. 5.Hubert Department of Global HealthRollins School of Public Health, Emory UniversityAtlantaUSA

Personalised recommendations