Efficacy of ethanol against viruses in hand disinfection

Journal of Hospital Infection

Volumn 98, Issue 4, 2018, Pages 331-338

  Kampf, G ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

Ethanol; Hand hygiene; Hand rub; Virucidal

Indexed keywords

ALCOHOL; TOPICAL ANTIINFECTIVE AGENT;

CALICIVIRIDAE; CONCENTRATION (PARAMETERS); ENTEROVIRUS; ENTEROVIRUS B; FOOT AND MOUTH DISEASE VIRUS; HAND DISINFECTION; HEPATITIS A VIRUS; HUMAN ADENOVIRUS 5; HUMAN POLIOVIRUS 1; INFECTION PREVENTION; INFECTION SENSITIVITY; NONHUMAN; NOROVIRUS; POLYOMAVIRUS; REVIEW; RHINOVIRUS; VIRAL CONTAMINATION; VIRUS ENVELOPE; VIRUS INACTIVATION; VIRUS INFECTION; DRUG EFFECT; HUMAN; MICROBIAL VIABILITY; PROCEDURES; TIME FACTOR; VIRUS;

ANTI-INFECTIVE AGENTS, LOCAL; ETHANOL; HAND DISINFECTION; HUMANS; MICROBIAL VIABILITY; TIME FACTORS; VIRUS INACTIVATION; VIRUSES;

EID: 85044046196     PISSN: 01956701     EISSN: 15322939     Source Type: Journal    
DOI: 10.1016/j.jhin.2017.08.025     Document Type: Review

References (78)

1. Goroncy-Bermes, P., Hand disinfection according to the European Standard EN 1500 (hygienic handrub): a study with gram-negative and gram-positive test organisms. Int J Hyg Environ Health 204 (2001), 123–126.
2. Goroncy-Bermes, P., Koburger, T., Meyer, B., Impact of the amount of hand rub applied in hygienic hand disinfection on the reduction of microbial counts on hands. J Hosp Infect 74 (2010), 212–218.
3. Kampf, G., Ostermeyer, C., Werner, H.-P., Suchomel, M., Efficacy of hand rubs with a low alcohol concentration listed as effective by a national hospital hygiene society in Europe. Antimicrob Resist Infect Control, 2, 2013, 19.
4. Kramer, A., Rudolph, P., Kampf, G., Pittet, D., Limited efficacy of alcohol-based hand gels. Lancet 359 (2002), 1489–1490.
5. Kampf, G., Rudolf, M., Labadie, J.-C., Barrett, S.P., Spectrum of antimicrobial activity and user acceptability of the hand disinfectant agent Sterillium Gel. J Hosp Infect 52 (2002), 141–147.
6. Macinga, D.R., Shumaker, D.J., Werner, H.P., Edmonds, S.L., Leslie, R.A., Parker, A.E., et al. The relative influences of product volume, delivery format and alcohol concentration on dry-time and efficacy of alcohol-based hand rubs. BMC Infect Dis, 14, 2014, 511.
7. Kampf, G., Marschall, S., Eggerstedt, S., Ostermeyer, C., Efficacy of ethanol-based hand foams using clinically relevant amounts: a cross-over controlled study among healthy volunteers. BMC Infect Dis, 10, 2010, 78.
8. World Health Organization, WHO model list of essential medicines. 2015, WHO, Geneva.
9. Department of Health and Human Services; Food and Drug Administration, Tentative final monograph for health care antiseptic products; proposed rule. Fed Reg 59 (1994), 31401–31452.
10. Department of Health and Human Services; Food and Drug Administration, Safety and effectiveness of healthcare antiseptics. Topical antimicrobial drug products for over-the-counter human use; proposed amendment of the tentative final monograph; reopening of administrative record; proposed rule. Fed Reg 80 (2015), 25166–25205.
11. EN 14885:2015, Chemical disinfectants and antiseptics. Application of European standards for chemical disinfectants and antiseptics. 2015, CEN (Comité Européen de Normalisation), Brussels.
12. Aitken, C., Jeffries, D.J., Nosocomial spread of viral disease. Clin Microbiol Rev 14 (2001), 528–546.
13. EN 14476:2013, Chemical disinfectants and antiseptics. Virucidal quantitative suspension test for chemical disinfectants and antiseptics used in human medicine. Test method and requirements (phase 2, step 1), 2013.
14. Klein, M., Deforest, A., Antiviral action of germicides. Soap Chem Spec 39 (1963), 70–72.
15. Rabenau, H.F., Kampf, G., Cinatl, J., Doerr, H.W., Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect 61 (2005), 107–111.
16. Siddharta, A., Pfaender, S., Vielle, N.J., Dijkman, R., Friesland, M., Becker, B., et al. Virucidal activity of World Health Organization-recommended formulations against enveloped viruses, including Zika, Ebola, and emerging coronaviruses. J Infect Dis 215 (2017), 902–906.
17. Eggers, M., Eickmann, M., Kowalski, K., Zorn, J., Reimer, K., Povidone-iodine hand wash and hand rub products demonstrated excellent in vitro virucidal efficacy against Ebola virus and modified vaccinia virus Ankara, the new European test virus for enveloped viruses. BMC Infect Dis, 15, 2015, 375.
18. Groupe, V., Engle, C.C., Gaffney, P.E., Virucidal activity of representative antiinfective agents against influenza A and vaccinia virus. Appl Microbiol 3 (1955), 333–336.
19. Jeong, E.K., Bae, J.E., Kim, I.S., Inactivation of influenza A virus H1N1 by disinfection process. Am J Infect Control 38 (2010), 354–360.
20. Kampf, G., Steinmann, J., Rabenau, H., Suitability of vaccinia virus and bovine viral diarrhea virus (BVDV) for determining activities of three commonly-used alcohol-based hand rubs against enveloped viruses. BMC Infect Dis, 7, 2007, 5.
21. Kramer, A., Galabov, A.S., Sattar, S.A., Döhner, L., Pivert, A., Payan, C., et al. Virucidal activity of a new hand disinfectant with reduced ethanol content: comparison with other alcohol-based formulations. J Hosp Infect 62 (2006), 98–106.
22. Martin, L.S., Meoougal, J.S., Loskoski, S.L., Disinfection and inactivation of the human T lymphotropic virus type III/lymphadenopathy associated virus. J Infect Dis 152 (1985), 400–403.
23. Spire, B., Barre-Sinoussi, F., Montagnier, L., Inactivation of lymphadenopathy associated virus by chemical disinfectants. Lancet 2 (1984), 899–901.
24. van Engelenburg, F.A., Terpstra, F.G., Schuitemaker, H., Moorer, W.R., The virucidal spectrum of a high concentration alcohol mixture. J Hosp Infect 51 (2002), 121–125.
25. van Bueren, J., Larkin, D.P., Simpson, R.A., Inactivation of human immunodeficiency virus type 1 by alcohols. J Hosp Infect 28 (1994), 137–148.
26. Bond, W.X.V., Favero, M.S., Petersen, N.J., Ebert, J.W., Inactivation of hepatitis B virus by intermediate to high-level disinfectant chemicals. J Clin Microbiol 18 (1983), 535–538.
27. Kobayashi, H., Tsuzuki, M., Koshimizu, K., Susceptibility of hepatitis B virus to disinfectants or heat. J Clin Microbiol 20 (1984), 214–216.
28. Bingel, K.F., Hermann, C., Die experimentelle Desinfektion des Vakzinevirus als Grundlage für die klinische Pockenimpfung. Med Welt 2 (1966), 76–82.
29. Grossgebauer, K., Zur Desinfektion der mit Pocken kontaminierten Hand. Gesundheitswes Desinfekt 59 (1967), 1–12.
30. Steinmann, J., Paulmann, D., Becker, B., Bischoff, B., Steinmann, E., Steinmann, J., Comparison of virucidal activity of alcohol-based hand sanitizers versus antimicrobial hand soaps in vitro and in vivo. J Hosp Infect 82 (2012), 277–280.
31. Rabenau, H.F., Rapp, I., Steinmann, J., Can vaccinia virus be replaced by MVA virus for testing virucidal activity of chemical disinfectants?. BMC Infect Dis, 10, 2010, 185.
32. Sauerbrei, A., Schacke, M., Gluck, B., Bust, U., Rabenau, H.F., Wutzler, P., Does limited virucidal activity of biocides include duck hepatitis B virucidal action?. BMC Infect Dis, 12, 2012, 276.
33. Bucca, M.A., The effect of various chemical agents on eastern equine encephalomyelitis virus. J Bacteriol 71 (1956), 491–492.
34. Cunningham, C.H., The effect of certain chemical agents on the virus of Newcastle disease of chicken. Am J Vet Res 9 (1948), 195–197.
35. Steinmann, J., Becker, B., Bischoff, B., Paulmann, D., Friesland, M., Pietschmann, T., et al. Virucidal activity of 2 alcohol-based formulations proposed as hand rubs by the World Health Organization. Am J Infect Control 38 (2010), 66–68.
36. Ciesek, S., Friesland, M., Steinmann, J., Wedemeyer, H., Manns, M.P., Steinmann, J., et al. How stable is the hepatitis C virus (HCV)? Environmental stability of HCV and its susceptibility to chemical biocides. J Infect Dis 201 (2010), 1859–1866.
37. Robert, Koch-Institut, Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2016. 2017 Berlin.
38. Steinmann, J., Becker, B., Bischoff, B., Magulski, T., Steinmann, J., Steinmann, E., Virucidal activity of Formulation I of the World Health Organization's alcohol-based handrubs: impact of changes in key ingredient levels and test parameters. Antimicrob Resist Infect Control, 2, 2013, 34.
39. Okunishi, J., Okamoto, K., Nishihara, Y., Tsujitani, K., Miura, T., Matsuse, H., et al. Investigation of in vitro and in vivo efficacy of a novel alcohol based hand rub, MR06B7. Yakugaku Zasshi 130 (2010), 747–754.
40. Macinga, D.R., Sattar, S.A., Jaykus, L.A., Arbogast, J.W., Improved inactivation of nonenveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Appl Environ Microbiol 74 (2008), 5047–5052.
41. Wutzler, P., Sauerbrei, A., Virucidal efficacy of a combination of 0.2% peracetic acid and 80% (v/v) ethanol (PAA-ethanol) as a potential hand disinfectant. J Hosp Infect 46 (2000), 304–308.
42. Iwasawa, A., Niwano, Y., Kohno, M., Ayaki, M., Virucidal activity of alcohol-based hand rub disinfectants. Biocontrol Sci 17 (2012), 45–49.
43. Paulmann, D., Steinmann, J., Becker, B., Bischoff, B., Steinmann, E., Steinmann, J., Virucidal activity of different alcohols against murine norovirus, a surrogate of human norovirus. J Hosp Infect 79 (2011), 378–379.
44. Park, G.W., Barclay, L., Macinga, D., Charbonneau, D., Pettigrew, C.A., Vinje, J., Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. J Food Prot 73 (2010), 2232–2238.
45. Tung, G., Macinga, D., Arbogast, J., Jaykus, L.A., Efficacy of commonly used disinfectants for inactivation of human noroviruses and their surrogates. J Food Prot 76 (2013), 1210–1217.
46. Belliot, G., Lavaux, A., Souihel, D., Agnello, D., Pothier, P., Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Appl Environ Microbiol 74 (2008), 3315–3318.
47. Gehrke, C., Steinmann, J., Goroncy-Bermes, P., Inactivation of feline calicivirus, a surrogate of norovirus (formerly Norwalk-like viruses), by different types of alcohol in vitro and in vivo. J Hosp Infect 56 (2004), 49–55.
48. Shimizu-Onda, Y., Akasaka, T., Yagyu, F., Komine-Aizawa, S., Tohya, Y., Hayakawa, S., et al. The virucidal effect against murine norovirus and feline calicivirus as surrogates for human norovirus by ethanol-based sanitizers. J Infect Chemother 19 (2013), 779–781.
49. Akasaka, T., Shimizu-Onda, Y., Hayakawa, S., Ushijima, H., The virucidal effects against murine norovirus and feline calicivirus F4 as surrogates for human norovirus by the different additive concentrations of ethanol-based sanitizers. J Infect Chemother 22 (2016), 191–193.
50. Drulak, M., Wallbank, A.M., Lebtag, I., Werboski, L., Poffenroth, L., The relative effectiveness of commonly used disinfectants in inactivation of coxsackievirus B5. J Hygiene 81 (1978), 389–397.
51. Moldenhauer, D., Quantitative evaluation of the effects of disinfectants against viruses in suspension experiments. Zentralbl Bakteriol Mikrobiol Hyg B 179 (1984), 544–554.
52. Drulak, M., Wallbank, A.M., Lebtag, I., The relative effectiveness of commonly used disinfectants in inactivation of echovirus 11. J Hygiene 81 (1978), 77–87.
53. Kurtz, J.B., Virucidal effect of alcohols against echovirus 11. Lancet 1 (1979), 496–497.
54. Chang, S.C., Li, W.C., Huang, K.Y., Huang, Y.C., Chiu, C.H., Chen, C.J., et al. Efficacy of alcohols and alcohol-based hand disinfectants against human enterovirus 71. J Hosp Infect 83 (2013), 288–293.
55. Tyler, R., Ayliffe, G.A.J., Bradley, C., Virucidal activity of disinfectants: studies with the poliovirus. J Hosp Infect 15 (1990), 339–345.
56. Ionidis, G., Hubscher, J., Jack, T., Becker, B., Bischoff, B., Todt, D., et al. Development and virucidal activity of a novel alcohol-based hand disinfectant supplemented with urea and citric acid. BMC Infect Dis, 16, 2016, 77.
57. Schürmann, W., Eggers, H.J., Antiviral activity of an alcoholic hand disinfectant: comparison of the in vitro suspension test with the in vivo experiments on hands, and on individual fingertips. Antiviral Res 3 (1983), 25–41.
58. Wolff, M.H., Schmitt, J., Rahaus, M., König, A., Hepatitis A virus: a test method for virucidal activity. J Hosp Infect 48 (2001), S18–S22.
59. Harada, Y.U., Lekcharoensuk, P., Furuta, T., Taniguchi, T., Inactivation of foot-and-mouth disease virus by commercially available disinfectants and cleaners. Biocontrol Sci 20 (2015), 205–208.
60. Schwebke, I., Eggers, M., Gebel, J., Geisel, B., Glebe, D., Rapp, I., et al. Prüfung und Deklaration der Wirksamkeit von Desinfektionsmitteln gegen Viren zur Anwendung im humanmedizinischen Bereich: Stellungnahme des Arbeitskreises Viruzidie beim Robert Koch-Institut. Bundesgesundheitsblatt 60 (2017), 353–363.
61. Grayson, M.L., Melvani, S., Druce, J., Barr, I.G., Ballard, S.A., Johnson, P.D., et al. Efficacy of soap and water and alcohol-based hand-rub preparations against live H1N1 influenza virus on the hands of human volunteers. Clin Infect Dis 48 (2009), 285–291.
62. Larson, E.L., Cohen, B., Baxter, K.A., Analysis of alcohol-based hand sanitizer delivery systems: efficacy of foam, gel, and wipes against influenza A (H1N1) virus on hands. Am J Infect Control 40 (2012), 806–809.
63. Hendley, J.O., Mika, L.A., Gwaltney, J.M. Jr., Evaluation of virucidal compounds for inactivation of rhinovirus on hands. Antimicrob Agents Chemother 14 (1978), 690–694.
64. Davies, J.G., Babb, J.R., Bradley, C.R., Ayliffe, G.A.J., Preliminary study of test methods to assess the virucidal activity of skin disinfectants using poliovirus and bacteriophages. J Hosp Infect 25 (1993), 125–131.
65. Steinmann, J., Nehrkorn, R., Meyer, A., Two in vivo protocols for testing virucidal efficacy of handwashing and hand disinfection. Zentralbl Hyg Umweltmed 196 (1995), 425–436.
66. Sattar, S., Ali, M., Tetro, J.A., In vivo comparison of two human norovirus surrogates for testing ethanol-based handrubs: the mouse chasing the cat!. PLoS One, 6, 2011, e17340.
67. Bellamy, K., Alcock, R., Babb, J.R., Davies, J.G., Ayliffe, G.A., A test for the assessment of “hygienic” hand disinfection using rotavirus. J Hosp Infect 24 (1993), 201–210.
68. Lages, S.L.S., Ramakrishnan, M.A., Goyal, S.M., In-vivo efficacy of hand sanitisers against feline calicivirus: a surrogate for norovirus. J Hosp Infect 68 (2008), 159–163.
69. Kampf, G., Grotheer, D., Steinmann, J., Efficacy of three ethanol-based hand rubs against feline calicivirus, a surrogate for norovirus. J Hosp Infect 60 (2005), 144–149.
70. Turner, R.B., Fuls, J.L., Rodgers, N.D., Effectiveness of hand sanitizers with and without organic acids for removal of rhinovirus from hands. Antimicrob Agents Chemother 54 (2010), 1363–1364.
71. Suchomel, M., Kundi, M., Pittet, D., Weinlich, M., Rotter, M.L., Testing of the World Health Organization recommended formulations in their application as hygienic hand rubs and proposals for increased efficacy. Am J Infect Control 40 (2011), 328–331.
72. Sauerbrei, A., Sehr, K., Brandstadt, A., Heim, A., Reimer, K., Wutzler, P., Sensitivity of human adenoviruses to different groups of chemical biocides. J Hosp Infect 57 (2004), 59–66.
73. Chaberny, I.E., Schnitzler, P., Geiss, H.K., Wendt, C., An outbreak of epidemic keratoconjunctivtis in a pediatric unit due to adenovirus type 8. Infect Control Hosp Epidemiol 24 (2003), 514–519.
74. Kampf, G., Reichel, M., Gehäufte Hautirritationen durch ein viruzides Händedesinfektionsmittel mit hohem Phosphorsäuregehalt. Arbeitsmed Sozialmed Präventivmed 45 (2010), 546–547.
75. Stauffer, F., Griess, M., Pleininger, G., Zhumadilova, A., Assadian, O., Acceptability and tolerability of liquid versus gel and standard versus virucidal alcohol-based hand rub formulations among dental students. Am J Infect Control 41 (2013), 1007–1011.
76. Conrad, A., Grotejohann, B., Schmoor, C., Cosic, D., Dettenkofer, M., Safety and tolerability of virucidal hand rubs: a randomized, double-blind, cross-over trial with healthy volunteers. Antimicrob Resist Infect Control, 4, 2015, 37.
77. Larson, E., Girard, R., Pessoa-Silva, C.L., Boyce, J., Donaldson, L., Pittet, D., Skin reactions related to hand hygiene and selection of hand hygiene products. Am J Infect Control 34 (2006), 627–635.
78. Eggers, H.-J., Experiments on antiviral activity of hand disinfectants. Some theoretical and practical considerations. Zentralbl Bakteriol 273 (1990), 36–51.