Human Coronaviruses: Insights into Environmental Resistance and Its Influence on the Development of New Antiseptic Strategies

Viruses - Tập 4 Số 11 - Trang 3044-3068
Chloé Geller1, Mihayl Varbanov1, Raphaël E. Duval1
1UMR 7565, SRSMC, Université de Lorraine – CNRS, Faculty of Pharmacy, 5 rue Albert Lebrun, BP 80403, 54001 Nancy Cedex, France

Tóm tắt

The Coronaviridae family, an enveloped RNA virus family, and, more particularly, human coronaviruses (HCoV), were historically known to be responsible for a large portion of common colds and other upper respiratory tract infections. HCoV are now known to be involved in more serious respiratory diseases, i.e. bronchitis, bronchiolitis or pneumonia, especially in young children and neonates, elderly people and immunosuppressed patients. They have also been involved in nosocomial viral infections. In 2002–2003, the outbreak of severe acute respiratory syndrome (SARS), due to a newly discovered coronavirus, the SARS-associated coronavirus (SARS-CoV); led to a new awareness of the medical importance of the Coronaviridae family. This pathogen, responsible for an emerging disease in humans, with high risk of fatal outcome; underline the pressing need for new approaches to the management of the infection, and primarily to its prevention. Another interesting feature of coronaviruses is their potential environmental resistance, despite the accepted fragility of enveloped viruses. Indeed, several studies have described the ability of HCoVs (i.e. HCoV 229E, HCoV OC43 (also known as betacoronavirus 1), NL63, HKU1 or SARS-CoV) to survive in different environmental conditions (e.g. temperature and humidity), on different supports found in hospital settings such as aluminum, sterile sponges or latex surgical gloves or in biological fluids. Finally, taking into account the persisting lack of specific antiviral treatments (there is, in fact, no specific treatment available to fight coronaviruses infections), the Coronaviridae specificities (i.e. pathogenicity, potential environmental resistance) make them a challenging model for the development of efficient means of prevention, as an adapted antisepsis-disinfection, to prevent the environmental spread of such infective agents. This review will summarize current knowledge on the capacity of human coronaviruses to survive in the environment and the efficacy of well-known antiseptic-disinfectants against them, with particular focus on the development of new methodologies to evaluate the activity of new antiseptic-disinfectants on viruses.

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Tài liệu tham khảo

Virus Taxonomy: 2011 Release (current). Available online:http://ictvonline.org/virusTaxonomy.asp?version=2011.

Almeida, 1967, The morphology of three previously uncharacterized human respiratory viruses that grow in organ culture, J. Gen. Virol., 1, 175, 10.1099/0022-1317-1-2-175

Bradburne, 1967, Effects of a "new" human respiratory virus in volunteers, Br. Med. J., 3, 767, 10.1136/bmj.3.5568.767

Hamre, 1966, A new virus isolated from the human respiratory tract, Proc. Soc. Exp. Biol. Med., 121, 190, 10.3181/00379727-121-30734

McIntosh, 1967, Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease, Proc. Natl. Acad. Sci. USA, 57, 933, 10.1073/pnas.57.4.933

Larson, 1980, Isolation of rhinoviruses and coronaviruses from 38 colds in adults, J. Med. Virol., 5, 221, 10.1002/jmv.1890050306

Esper, 2005, Evidence of a novel human coronavirus that is associated with respiratory tract disease in infants and young children, J. Infect. Dis., 191, 492, 10.1086/428138

Fouchier, 2004, A previously undescribed coronavirus associated with respiratory disease in humans, Proc. Natl. Acad. Sci. USA, 101, 6212, 10.1073/pnas.0400762101

Pyrc, 2004, Identification of a new human coronavirus, Nat. Med., 10, 368, 10.1038/nm1024

Woo, 2005, Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia, J. Virol., 79, 884, 10.1128/JVI.79.2.884-895.2005

Drosten, 2003, Identification of a novel coronavirus in patients with severe acute respiratory syndrome, N. Engl. J. Med., 348, 1967, 10.1056/NEJMoa030747

Ksiazek, 2003, A novel coronavirus associated with severe acute respiratory syndrome, N. Engl. J. Med., 348, 1953, 10.1056/NEJMoa030781

Peiris, 2003, Coronavirus as a possible cause of severe acute respiratory syndrome, Lancet, 361, 1319, 10.1016/S0140-6736(03)13077-2

(2003). A multicentre collaboration to investigate the cause of severe acute respiratory syndrome. Lancet, 361, 1730–1733.

Arden, 2005, New human coronavirus, HCoV-NL63, associated with severe lower respiratory tract disease in Australia, J. Med. Virol., 75, 455, 10.1002/jmv.20288

Bastien, 2005, Human coronavirus NL63 infection in Canada, J. Infect. Dis., 191, 503, 10.1086/426869

Vabret, 2005, Human coronavirus NL63, France, Emerg. Infect. Dis., 11, 1225, 10.3201/eid1108.050110

Sure, 2005, Croup is associated with the novel coronavirus NL63, PLoS Med., 2, e240, 10.1371/journal.pmed.0020240

Gerna, 2007, Human respiratory coronavirus HKU1 versus other coronavirus infections in Italian hospitalised patients, J. Clin. Virol., 38, 244, 10.1016/j.jcv.2006.12.008

Sloots, 2006, Evidence of human coronavirus HKU1 and human bocavirus in Australian children, J. Clin. Virol., 35, 99, 10.1016/j.jcv.2005.09.008

Chiu, 2005, Human coronavirus NL63 infection and other coronavirus infections in children hospitalized with acute respiratory disease in Hong Kong, China, Clin. Infect. Dis., 40, 1721, 10.1086/430301

Kon, 2012, Detection of human coronavirus NL63 and OC43 in children with acute respiratory infections in Niigata, Japan, between 2010 and 2011, Jpn. J. Infect. Dis., 65, 270, 10.7883/yoken.65.270

Gerna, 2006, Genetic variability of human coronavirus OC43-, 229E-, and NL63-like strains and their association with lower respiratory tract infections of hospitalized infants and immunocompromised patients, J. Med. Virol., 78, 938, 10.1002/jmv.20645

Esposito, 2006, Impact of human coronavirus infections in otherwise healthy children who attended an emergency department, J. Med. Virol., 78, 1609, 10.1002/jmv.20745

Vabret, 2008, Human (non-severe acute respiratory syndrome) coronavirus infections in hospitalised children in France, J. Paediatr. Child. Health., 44, 176, 10.1111/j.1440-1754.2007.01246.x

Talbot, 2009, The pediatric burden of human coronaviruses evaluated for twenty years, Pediatr. Infect. Dis. J., 28, 682, 10.1097/INF.0b013e31819d0d27

Vabret, 2003, An outbreak of coronavirus OC43 respiratory infection in Normandy, France, Clin. Infect. Dis., 36, 985, 10.1086/374222

Hendriksen, 2004, Frequent detection of human coronaviruses in clinical specimens from patients with respiratory tract infection by use of a novel real-time reverse-transcriptase polymerase chain reaction, J. Infect. Dis., 189, 652, 10.1086/381207

Riski, 1980, Coronavirus infections of man associated with diseases other than the common cold, J. Med. Virol., 6, 259, 10.1002/jmv.1890060309

Talbot, 2009, Coronavirus infection and hospitalizations for acute respiratory illness in young children, J. Med. Virol., 81, 853, 10.1002/jmv.21443

Woo, 2005, Clinical and molecular epidemiological features of coronavirus HKU1-associated community-acquired pneumonia, J. Infect. Dis., 192, 1898, 10.1086/497151

Gagneur, 2002, Coronavirus-related nosocomial viral respiratory infections in a neonatal and paediatric intensive care unit: a prospective study, J. Hosp. Infect., 51, 59, 10.1053/jhin.2002.1179

Sizun, 1995, Neonatal nosocomial respiratory infection with coronavirus: a prospective study in a neonatal intensive care unit, Acta Paediatr., 84, 617, 10.1111/j.1651-2227.1995.tb13710.x

Falsey, 2002, Rhinovirus and coronavirus infection-associated hospitalizations among older adults, J. Infect. Dis., 185, 1338, 10.1086/339881

Nicholson, 1997, Acute viral infections of upper respiratory tract in elderly people living in the community: comparative, prospective, population based study of disease burden, BMJ, 315, 1060, 10.1136/bmj.315.7115.1060

Pene, 2003, Coronavirus 229E-related pneumonia in immunocompromised patients, Clin. Infect. Dis., 37, 929, 10.1086/377612

Folz, 1999, Coronavirus pneumonia following autologous bone marrow transplantation for breast cancer, Chest, 115, 901, 10.1378/chest.115.3.901

Chany, 1982, Association of coronavirus infection with neonatal necrotizing enterocolitis, Pediatrics, 69, 209, 10.1542/peds.69.2.209

Vabret, 2006, Detection of the new human coronavirus HKU1: a report of 6 cases, Clin. Infect. Dis., 42, 634, 10.1086/500136

Zhang, 1994, Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child, J. Med. Virol., 44, 152, 10.1002/jmv.1890440207

Arbour, 1999, Acute and persistent infection of human neural cell lines by human coronavirus OC43, J. Virol., 73, 3338, 10.1128/JVI.73.4.3338-3350.1999

Arbour, 1999, Persistent infection of human oligodendrocytic and neuroglial cell lines by human coronavirus 229E, J. Virol., 73, 3326, 10.1128/JVI.73.4.3326-3337.1999

Bonavia, 1997, Infection of primary cultures of human neural cells by human coronaviruses 229E and OC43, J. Virol., 71, 800, 10.1128/jvi.71.1.800-806.1997

Arbour, 2000, Neuroinvasion by human respiratory coronaviruses, J. Virol., 74, 8913, 10.1128/JVI.74.19.8913-8921.2000

Murray, 1992, Detection of coronavirus RNA and antigen in multiple sclerosis brain, Ann. Neurol., 31, 525, 10.1002/ana.410310511

Stewart, 1992, Human coronavirus gene expression in the brains of multiple sclerosis patients, Virology, 191, 502, 10.1016/0042-6822(92)90220-J

Jacomy, 2004, Human respiratory coronavirus OC43: genetic stability and neuroinvasion, J. Virol., 78, 8824, 10.1128/JVI.78.16.8824-8834.2004

Riski, 1980, Carditis associated with coronavirus infection, Lancet, 2, 100, 10.1016/S0140-6736(80)92989-X

Hsu, 2003, Severe acute respiratory syndrome (SARS) in Singapore: clinical features of index patient and initial contacts, Emerg. Infect. Dis., 9, 713, 10.3201/eid0906.030264

Poutanen, 2003, Identification of severe acute respiratory syndrome in Canada, N. Engl. J. Med., 348, 1995, 10.1056/NEJMoa030634

Available online:http://www.who.int/csr/sars/country/table2004_04_21/en/index.html.

Lee, 2003, A major outbreak of severe acute respiratory syndrome in Hong Kong, N. Engl. J. Med., 348, 1986, 10.1056/NEJMoa030685

Varia, 2003, Investigation of a nosocomial outbreak of severe acute respiratory syndrome (SARS) in Toronto, Canada, CMAJ, 169, 285

Zhao, 2003, Description and clinical treatment of an early outbreak of severe acute respiratory syndrome (SARS) in Guangzhou, PR China, J. Med. Microbiol., 52, 715, 10.1099/jmm.0.05320-0

Booth, 2003, Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area, JAMA, 289, 2801, 10.1001/jama.289.21.JOC30885

Donnelly, 2003, Epidemiological determinants of spread of causal agent of severe acute respiratory syndrome in Hong Kong, Lancet, 361, 1761, 10.1016/S0140-6736(03)13410-1

Peiris, 2003, Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study, Lancet, 361, 1767, 10.1016/S0140-6736(03)13412-5

Peiris, 2003, The severe acute respiratory syndrome, N. Engl. J. Med., 349, 2431, 10.1056/NEJMra032498

Consensus document on the epidemiology of severe acute respiratory syndrome (SARS). Available online:http://www.who.int/csr/sars/en/WHOconsensus.pdf.

Hamming, 2004, Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis, J. Pathol., 203, 631, 10.1002/path.1570

Li, 2003, Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus, Nature, 426, 450, 10.1038/nature02145

Dwosh, 2003, Identification and containment of an outbreak of SARS in a community hospital, CMAJ, 168, 1415

Ng, 2003, Possible role of an animal vector in the SARS outbreak at Amoy Gardens, Lancet, 362, 570, 10.1016/S0140-6736(03)14121-9

Vijgen, 2005, Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event, J. Virol., 79, 1595, 10.1128/JVI.79.3.1595-1604.2005

Lau, 2005, Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats, Proc. Natl. Acad. Sci. USA, 102, 14040, 10.1073/pnas.0506735102

Li, 2005, Bats are natural reservoirs of SARS-like coronaviruses, Science, 310, 676, 10.1126/science.1118391

Poon, 2005, Identification of a novel coronavirus in bats, J. Virol., 79, 2001, 10.1128/JVI.79.4.2001-2009.2005

Woo, 2006, Molecular diversity of coronaviruses in bats, Virology, 351, 180, 10.1016/j.virol.2006.02.041

Kan, 2005, Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms, J. Virol., 79, 11892, 10.1128/JVI.79.18.11892-11900.2005

Cinatl, 2005, High-dose hydrocortisone reduces expression of the pro-inflammatory chemokines CXCL8 and CXCL10 in SARS coronavirus-infected intestinal cells, Int. J. Mol. Med., 15, 323

Cinatl, 2003, Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus, Lancet, 361, 2045, 10.1016/S0140-6736(03)13615-X

Morgenstern, 2005, Ribavirin and interferon-beta synergistically inhibit SARS-associated coronavirus replication in animal and human cell lines, Biochem. Biophys. Res. Commun., 326, 905, 10.1016/j.bbrc.2004.11.128

Mazzulli, 2004, Severe acute respiratory syndrome-associated coronavirus in lung tissue, Emerg. Infect. Dis., 10, 20, 10.3201/eid1001.030404

Yamamoto, 2004, HIV protease inhibitor nelfinavir inhibits replication of SARS-associated coronavirus, Biochem. Biophys. Res. Commun., 318, 719, 10.1016/j.bbrc.2004.04.083

Cinatl, 2005, Development of antiviral therapy for severe acute respiratory syndrome, Antiviral Res., 66, 81, 10.1016/j.antiviral.2005.03.002

Haagmans, 2006, Coronaviruses and their therapy, Antiviral Res., 71, 397, 10.1016/j.antiviral.2006.05.019

Bisht, 2004, Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice, Proc. Natl. Acad. Sci. USA., 101, 6641, 10.1073/pnas.0401939101

Kapadia, 2005, Long-term protection from SARS coronavirus infection conferred by a single immunization with an attenuated VSV-based vaccine, Virology, 340, 174, 10.1016/j.virol.2005.06.016

Chen, 2005, Recombinant modified vaccinia virus Ankara expressing the spike glycoprotein of severe acute respiratory syndrome coronavirus induces protective neutralizing antibodies primarily targeting the receptor binding region, J. Virol., 79, 2678, 10.1128/JVI.79.5.2678-2688.2005

Bukreyev, 2004, Mucosal immunisation of African green monkeys (Cercopithecus aethiops) with an attenuated parainfluenza virus expressing the SARS coronavirus spike protein for the prevention of SARS, Lancet, 363, 2122, 10.1016/S0140-6736(04)16501-X

Ishii, 2006, Induction of protective immunity against severe acute respiratory syndrome coronavirus (SARS-CoV) infection using highly attenuated recombinant vaccinia virus DIs, Virology, 351, 368, 10.1016/j.virol.2006.03.020

See, 2006, Comparative evaluation of two severe acute respiratory syndrome (SARS) vaccine candidates in mice challenged with SARS coronavirus, J. Gen. Virol., 87, 641, 10.1099/vir.0.81579-0

Czub, 2005, Evaluation of modified vaccinia virus Ankara based recombinant SARS vaccine in ferrets, Vaccine, 23, 2273, 10.1016/j.vaccine.2005.01.033

He, 2006, Antigenic and immunogenic characterization of recombinant baculovirus-expressed severe acute respiratory syndrome coronavirus spike protein: implication for vaccine design, J. Virol., 80, 5757, 10.1128/JVI.00083-06

Zhou, 2006, A recombinant baculovirus-expressed S glycoprotein vaccine elicits high titers of SARS-associated coronavirus (SARS-CoV) neutralizing antibodies in mice, Vaccine, 24, 3624, 10.1016/j.vaccine.2006.01.059

He, 2004, Inactivated SARS-CoV vaccine elicits high titers of spike protein-specific antibodies that block receptor binding and virus entry, Biochem. Biophys. Res. Commun., 325, 445, 10.1016/j.bbrc.2004.10.052

Spruth, 2006, A double-inactivated whole virus candidate SARS coronavirus vaccine stimulates neutralising and protective antibody responses, Vaccine, 24, 652, 10.1016/j.vaccine.2005.08.055

Tang, 2004, Inactivated SARS-CoV vaccine prepared from whole virus induces a high level of neutralizing antibodies in BALB/c mice, DNA Cell Biol., 23, 391, 10.1089/104454904323145272

Xiong, 2004, Immunogenicity of SARS inactivated vaccine in BALB/c mice, Immunol. Lett., 95, 139, 10.1016/j.imlet.2004.06.014

Takasuka, 2004, A subcutaneously injected UV-inactivated SARS coronavirus vaccine elicits systemic humoral immunity in mice, Int. Immunology, 16, 1423, 10.1093/intimm/dxh143

Stadler, 2005, SARS vaccine protective in mice, Emerg. Infect. Dis., 11, 1312, 10.3201/eid1108.041003

Woo, 2005, SARS coronavirus spike polypeptide DNA vaccine priming with recombinant spike polypeptide from Escherichia coli as booster induces high titer of neutralizing antibody against SARS coronavirus, Vaccine, 23, 4959, 10.1016/j.vaccine.2005.05.023

Yang, 2004, A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice, Nature, 428, 561, 10.1038/nature02463

Zhao, 2004, DNA vaccine of SARS-Cov S gene induces antibody response in mice, Acta Biochim. Biophys. Sin., 36, 37, 10.1093/abbs/36.1.37

Wang, 2005, Immune responses with DNA vaccines encoded different gene fragments of severe acute respiratory syndrome coronavirus in BALB/c mice, Biochem. Biophys. Res. Commun., 327, 130, 10.1016/j.bbrc.2004.11.147

Perlman, 2005, Immunopathogenesis of coronavirus infections: implications for SARS, Nat. Rev. Immunol., 5, 917, 10.1038/nri1732

Bolles, 2011, A double-inactivated severe acute respiratory syndrome coronavirus vaccine provides incomplete protection in mice and induces increased eosinophilic proinflammatory pulmonary response upon challenge, J. Virol., 85, 12201, 10.1128/JVI.06048-11

Deming, 2006, Vaccine efficacy in senescent mice challenged with recombinant SARS-CoV bearing epidemic and zoonotic spike variants, PLoS Med., 3, e525, 10.1371/journal.pmed.0030525

Lokugamage, 2008, Chimeric coronavirus-like particles carrying severe acute respiratory syndrome coronavirus (SCoV) S protein protect mice against challenge with SCoV, Vaccine, 26, 797, 10.1016/j.vaccine.2007.11.092

Yasui, 2008, Prior immunization with severe acute respiratory syndrome (SARS)-associated coronavirus (SARS-CoV) nucleocapsid protein causes severe pneumonia in mice infected with SARS-CoV, J. Immunol., 181, 6337, 10.4049/jimmunol.181.9.6337

Tseng, 2012, Immunization with SARS coronavirus vaccines leads to pulmonary immunopathology on challenge with the SARS virus, PLoS ONE., 7, e35421, 10.1371/journal.pone.0035421

Olsen, 2003, Transmission of the severe acute respiratory syndrome on aircraft, N. Engl. J. Med., 349, 2416, 10.1056/NEJMoa031349

Lee, 2003, The SARS epidemic in Hong Kong, J. Epidemiol. Community Health., 57, 652, 10.1136/jech.57.9.652

Ijaz, M.K., Brunner, A.H., Sattar, S.A., Nair, R.C., and Johnson-Lussenburg, C.M. (1985). Survival characteristics of airborne human coronavirus 229E. J. Gen. Virol., 66 ( Pt 12).

Rabenau, 2005, Stability and inactivation of SARS coronavirus, Med. Microbiol. Immunol., 194, 1, 10.1007/s00430-004-0219-0

Duan, 2003, Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation, Biomed. Environ. Sci., 16, 246

Sizun, 2000, Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections, J. Hosp. Infect., 46, 55, 10.1053/jhin.2000.0795

Lai, 2005, Survival of severe acute respiratory syndrome coronavirus, Clin. Infect. Dis., 41, e67, 10.1086/433186

Chen, 2004, SARS in hospital emergency room, Emerg. Infect. Dis., 10, 782, 10.3201/eid1005.030579

Dowell, 2004, Severe acute respiratory syndrome coronavirus on hospital surfaces, Clin. Infect. Dis., 39, 652, 10.1086/422652

Casanova, 2009, Survival of surrogate coronaviruses in water, Water Res., 43, 1893, 10.1016/j.watres.2009.02.002

Lamarre, 1989, Effect of pH and temperature on the infectivity of human coronavirus 229E, Can. J. Microbiol., 35, 972, 10.1139/m89-160

Sturman, 1990, Conformational change of the coronavirus peplomer glycoprotein at pH 8.0 and 37 degrees C correlates with virus aggregation and virus-induced cell fusion, J. Virol., 64, 3042, 10.1128/jvi.64.6.3042-3050.1990

Daniel, 1987, Physico-chemical properties of murine hepatitis virus, strain A 59. Brief report, Arch. Virol., 96, 241, 10.1007/BF01320963

Pocock, 1975, The influence of pH on the growth and stability of transmissible gastroenteritis virus in vitro, Arch. Virol., 49, 239, 10.1007/BF01317542

Pratelli, 2008, Canine coronavirus inactivation with physical and chemical agents, Vet. J., 177, 71, 10.1016/j.tvjl.2007.03.019

First data on stability and resistance of SARS coronavirus compiled by members of WHO laboratory network. Available online:http://www.who.int/csr/sars/survival_2003_05_04/en/index.html.

Lipsitch, 2003, Transmission dynamics and control of severe acute respiratory syndrome, Science, 300, 1966, 10.1126/science.1086616

Riley, 2003, Transmission dynamics of the etiological agent of SARS in Hong Kong: impact of public health interventions, Science, 300, 1961, 10.1126/science.1086478

Seto, 2003, Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS), Lancet, 361, 1519, 10.1016/S0140-6736(03)13168-6

(2003). Global surveillance for Severe Acute Respiratory Syndrome (SARS). Wkly. Epidemiol. Rec., 78, 100–109.

(2007). Chemical disinfectants and- Virucidal quantitative suspension test for chemical disinfectants and antiseptics used in human medicine - Test method and requirements (phase 2, step 1). NF EN 14476+A1.

(1997). Standard Test Method for Efficacy of Virucidal Agents Intended for Inanimate Environmental Surfaces. E1053-97 (last reapproval in 2002).

(Standard Test Method for Efficacy of Antimicrobial Agents Against Viruses in Suspension. E1052-96 (last reapproval in 2002), 1996). Standard Test Method for Efficacy of Antimicrobial Agents Against Viruses in Suspension. E1052-96 (last reapproval in 2002).

(2004). Standard Test Method for Neutralization of Virucidal Agents in Virucidal Efficacy Evaluations. E1482-04.

(2002). Standard Test Method for Determining the Virus-Eliminating Effectiveness of Liquid Hygienic Handwash and Handrub Agents Using the Fingerpads of Adult Volunteers. E1838-02.

(2009). Standard Test Method for Evaluation of Hygienic Handwash and Handrub Formulations for Virus-Eliminating Activity Using the Entire Hand. E2011-09.

Sattar, 1989, Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses, Epidemiol. Infect., 102, 493, 10.1017/S0950268800030211

Kariwa, 2006, Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents, Dermatology., 212 Suppl 1, 119, 10.1159/000089211

Geller, 2009, A new Sephadex-based method for removing microbicidal and cytotoxic residues when testing antiseptics against viruses: Experiments with a human coronavirus as a model, J. Virol. Methods., 159, 217, 10.1016/j.jviromet.2009.03.023

Geller, 2010, Antiseptic properties of two calix[4]arenes derivatives on the human coronavirus 229E, Antiviral Res., 88, 343, 10.1016/j.antiviral.2010.09.009

Rabenau, 2005, Efficacy of various disinfectants against SARS coronavirus, J. Hosp. Infect., 61, 107, 10.1016/j.jhin.2004.12.023

Hulkower, 2011, Inactivation of surrogate coronaviruses on hard surfaces by health care germicides, Am. J. Infect. Control., 39, 401, 10.1016/j.ajic.2010.08.011

Dellanno, 2009, The antiviral action of common household disinfectants and antiseptics against murine hepatitis virus, a potential surrogate for SARS coronavirus, Am. J. Infect. Control., 37, 649, 10.1016/j.ajic.2009.03.012