Human coronavirus 229E remains infectious on common touch surface materials

mBio

Volumn 6, Issue 6, 2015, Pages

  Warnes, Sarah L ^a   Little, Zoë R ^a   Keevil, C William ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; GLASS; POLITEF; POLYVINYLCHLORIDE; REACTIVE OXYGEN METABOLITE; SILASTIC; STAINLESS STEEL; ZINC; ALLOY; DISINFECTANT AGENT;

ARTICLE; BUILDING MATERIAL; CERAMIC TILE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENETIC DAMAGE; HUMAN; HUMAN CELL; HUMAN CORONAVIRUS 229E; LUNG ALVEOLUS CELL; NONHUMAN; NOROVIRUS; OXIDATIVE STRESS; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PUBLIC HEALTH; SURFACE PROPERTY; VIRAL CONTAMINATION; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS GENOME; VIRUS INACTIVATION; VIRUS MORPHOLOGY; VIRUS TRANSMISSION; VIRUS VIRULENCE; CELL LINE; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; TIME FACTOR; VIRUS CULTURE;

ALLOYS; CELL LINE; COPPER; CORONAVIRUS 229E, HUMAN; DISINFECTANTS; ENVIRONMENTAL MICROBIOLOGY; HUMANS; MICROBIAL VIABILITY; TIME FACTORS; VIRUS CULTIVATION; ZINC;

EID: 84952802042     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01697-15     Document Type: Article

References (52)

1. ZambonM. 2014. Influenza and other emerging respiratory viruses. Medicine 42:45-51 http://dx.doi.org/10.1016/j.mpmed.2013.10.017.
2. Ruuskanen O, Lahti E, Jennings LC, Murdoch DR. 2011. Viral pneumonia. Lancet 377:1264-1275. http://dx.doi.org/10.1016/S0140-6736(10)61459-6.
3. Van den Brand JM, Smits SL, Haagmans BL. 2015. Pathogenesis of Middle East respiratory syndrome coronavirus. J Pathol 235:175-184. http://dx.doi.org/10.1002/path.4458.
4. Gralinski LE, Baric RS. 2015. Molecular pathology of emerging coronavirus infections. J Pathol 235:185-195. http://dx.doi.org/10.1002/ path.4454.
5. Coleman CM, Frieman MB. 2014. Coronaviruses: important emerging human pathogens. J Virol 88:5209-5212. http://dx.doi.org/10.1128/ JVI.03488-13.
6. Chan JFW, Lau SKP, To KKW, Cheng VCC, Woo PCY, Yuen K. 2015. Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease. Clin Microbiol Rev 28:465-522. http://dx.doi.org/10.1128/CMR.00102-14.
7. Cong Y, Ren X. 2014. Coronavirus entry and release in polarized epithelial cells: a review. Rev Med Virol 24:308-315. http://dx.doi.org/10.1002/ rmv.1792.
8. Hemida MG, Al-Naeem A, Perera RAPM, Chin AWH, Poon LLM, Peiris M. 2015. Lack of Middle East respiratory syndrome coronavirus transmission from infected camels. Emerg Infect Dis 21:699-701. http:// dx.doi.org/10.3201/eid2104.141949.
9. Oboho IK, Tomczyk SM, Al-Asmari AM, Banjar AA, Al-Mugti H, Aloraini MS, Alkhaldi KZ, Almohammadi EL, Alraddadi BM, Gerber SI, Swerdlow DL, Watson JT, Madani TA. 2015. 2014 MERS-CoV outbreak in Jeddah-a link to health care facilities. N Engl J Med 372: 846-854. http://dx.doi.org/10.1056/NEJMoa1408636.
10. Butler D. 2015. South Korean MERS outbreak spotlights lack of research. Nature 522:139-140. http://dx.doi.org/10.1038/522139a.
11. KiM. 2015. 2015 MERS outbreak in Korea: hospital-to-hospital transmission. Epidemiol Health 37:e2015033. http://dx.doi.org/10.4178/epih/ e2015033.
12. Otter JA, Yezli S, Salkeld JAG, French GL. 2013. Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings. Am J Infect Control 41:S6-S11. http://dx.doi.org/10.1016/ j.ajic.2012.12.004.
13. Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH, Jr. 1982. Survival of influenza viruses on environmental surfaces. J Infect Dis 146:47-51. http://dx.doi.org/10.1093/infdis/146.1.47.
14. Wilks SA, Michels H, Keevil CW. 2005. The survival of Escherichia coli O157 on a range of metal surfaces. Int J Food Microbiol 105:445-454. http://dx.doi.org/10.1016/j.ijfoodmicro.2005.04.021.
15. Noyce JO, Michels H, Keevil CW. 2006. Potential use of copper surfaces to reduce survival of epidemic meticillin-resistant Staphylococcus aureus in the healthcare environment. J Hosp Infect 63:289-297. http://dx.doi.org/ 10.1016/j.jhin.2005.12.008.
16. Noyce JO, Michels H, Keevil CW. 2006. Use of copper cast alloys to control Escherichia coli O157 cross-contamination during food processing. Appl Environ Microbiol 72:4239-4244. http://dx.doi.org/10.1128/ AEM.02532-05.
17. Weaver L, Michels HT, Keevil CW. 2008. Survival of Clostridium difficile on copper and steel: futuristic options for hospital hygiene. J Hosp Infect 68:145-151. http://dx.doi.org/10.1016/j.jhin.2007.11.011.
18. Weaver L, Michels HT, Keevil CW. 2010. Potential for preventing spread of fungi in air-conditioning systems constructed using copper instead of aluminium. Lett Appl Microbiol 50:18-23. http://dx.doi.org/10.1111/ j.1472-765X.2009.02753.x.
19. Warnes SL, Green SM, Michels HT, Keevil CW. 2010. Biocidal efficacy of copper alloys against pathogenic enterococci involves degradation of genomic and plasmid DNAs. Appl Environ Microbiol 76:5390-5401. http://dx.doi.org/10.1128/AEM.03050-09.
20. Warnes SL, Keevil CW. 2011. Mechanism of copper surface toxicity in vancomycin-resistant enterococci following wet or dry surface contact. Appl Environ Microbiol 77:6049-6059. http://dx.doi.org/10.1128/ AEM.00597-11.
21. Warnes SL, Caves V, Keevil CW. 2012. Mechanism of copper surface toxicity in Escherichia coli O157:H7 and Salmonella involves immediate membrane depolarization followed by slower rate of DNA destruction which differs from that observed for Gram-positive bacteria. Environ Microbiol 14:1730-1743. http://dx.doi.org/10.1111/j.1462-2920.2011.02677.x.
22. Casey AL, Adams D, Karpanen TJ, Lambert PA, Cookson BD, Nightingale P, Miruszenko L, Shillam R, Christian P, Elliott TSJ. 2010. Role of copper in reducing hospital environment contamination. J Hosp Infect 74:72-77. http://dx.doi.org/10.1016/j.jhin.2009.08.018.
23. Karpanen TJ, Casey AL, Lambert PA, Cookson BD, Nightingale P, Miruszenko L, Elliott TSJ. 2012. The antimicrobial efficacy of copper alloy furnishing in the clinical environment: a crossover study. Infect Control Hosp Epidemiol 33:3-9. http://dx.doi.org/10.1086/663644.
24. Schmidt MG, Attaway HH, Sharpe PA, John J, Jr, Sepkowitz KA, Morgan A, Fairey SE, Singh S, Steed LL, Cantey JR, Freeman KD, Michels HT, Salgado CD. 2012. Sustained reduction of microbial burden on common hospital surfaces through introduction of copper. J Clin Microbiol 50:2217-2223. http://dx.doi.org/10.1128/JCM.01032-12.
25. Salgado CD, Sepkowitz KA, John JF, Cantey JR, Attaway HH, Freeman KD, Sharpe PA, Michels HT, Schmidt MG. 2013. Copper surfaces reduce the rate of healthcare-acquired infections in the intensive care unit. Infect Control Hosp Epidemiol 34:479-486. http://dx.doi.org/10.1086/670207.
26. Warnes SL, Keevil CW. 2013. Inactivation of norovirus on dry copper alloy surfaces. PLoS One 8:e75017. http://dx.doi.org/10.1371/ journal.pone.0075017.
27. Warnes SL, Summersgill EN, Keevil CW. 2015. Inactivation of murine norovirus on a range of copper alloy surfaces is accompanied by loss of capsid integrity. Appl Environ Microbiol 81:1085-1091. http:// dx.doi.org/10.1128/AEM.03280-14.
28. Manuel CS, Moore MD, Jaykus LA. 2015. Destruction of the capsid and genome of GII.4 human norovirus occurs during exposure to metal alloys containing copper. Appl Environ Microbiol 81:4940-4946. http:// dx.doi.org/10.1128/AEM.00388-15.
29. Pene F, Merlat A, Vabret A, Rozenberg F, Buzyn A, Dreyfus F, Cariou A, Freymuth F, Lebon P. 2003. Coronavirus 229E-related pneumonia in immunocompromised patients. Clin Infect Dis 37:929-932. http:// dx.doi.org/10.1086/377612.
30. Boucher A, Desforges M, Duquette P, Talbot PJ. 2007. Long-term human coronavirus-myelin cross-reactive T-cell clones derived from multiple sclerosis patients. Clin Immunol 123:258-267. http://dx.doi.org/ 10.1016/j.clim.2007.02.002.
31. Corman VM, Baldwin HJ, Fumie TA, Melim ZR, Annan A, Owusu M, Nkrumah EE, Maganga GD, Oppong S, Adu-Sarkodie Y, Vallo P, da Silva Filho LV, Leroy EM, Thiel V, van der Hoek L, Poon LL, Tschapka M, Drosten C, Drexler JF. 16 September 2015. Evidence for an ancestral association of human coronavirus 229E with bats. J Virol http:// dx.doi.org/10.1128/JVI.01755-15.
32. Shi Y, Wu Y, Zhang W, Qi J, Gao GF. 2014. Enabling the "host jump": structural determinants of receptor-binding specificity in influenza A viruses. Nat Rev Microbiol 12:822-831. http://dx.doi.org/10.1038/ nrmicro3362.
33. Xie X, Li Y, Chwang ATY, Ho PL, Seto WH. 2007. How far droplets can move in indoor environments-revisiting the wells evaporationfalling curve. Indoor Air 17:211-225. http://dx.doi.org/10.1111/j.1600-0668.2007.00469.x.
34. Yezli S, Otter JA. 2011. Minimum infective dose of the major respiratory and enteric viruses transmitted through food and the environment. Food Environ Virol 3:1-30. http://dx.doi.org/10.1007/s12560-011-9056-7.
35. Boone S, Gerba C. 2005. The occurrence of influenza A virus on household and day care center fomites. J Infect 51:103-109. http://dx.doi.org/ 10.1016/j.jinf.2004.09.011.
36. Casanova LM, Jeon S, Rutala WA, Weber DJ, Sobsey MD. 2010. Effects of air temperature and relative humidity on coronavirus survival on surfaces. Appl Environ Microbiol 76:2712-2717. http://dx.doi.org/10.1128/ AEM.02291-09.
37. Casanova L, Rutala W, Weber D, Sobsey M. 2010. Coronavirus survival on healthcare personal protective equipment. Infect Control Hosp Epidemiol 31:560-561. http://dx.doi.org/10.1086/652452.
38. Sizun J, Yu MWN, Talbot PJ. 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 46:55-60. http:// dx.doi.org/10.1053/jhin.2000.0795.
39. Nicas M, Best D. 2008. A study quantifying the hand-to-face contact rate and its potential application to predicting respiratory tract infection. J Occup Environ Hyg 5:347-352. http://dx.doi.org/10.1080/ 15459620802003896.
40. Karlstrom AR, Levine RL. 1991. Copper inhibits the protease from human immunodeficiency virus 1 by both cysteine-dependent and cysteineindependent mechanisms. Proc Natl Acad Sci U S A 88:5552-5556. http:// dx.doi.org/10.1073/pnas.88.13.5552.
41. Sagripanti JL, Routson LB, Bonifacino AC, Lytle CD. 1997. Mechanism of copper-mediated inactivation of herpes simplex virus. Antimicrob Agents Chemother 41:812-817.
42. Ding L, Zhao X, Huang Y, Du Q, Dong F, Zhang H, Song X, Zhang W, Tong D. 2013. Regulation of ROS in transmissible gastroenteritis virusactivated apoptotic signaling. Biochem Biophys Res Commun 442:33-37. http://dx.doi.org/10.1016/j.bbrc.2013.10.164.
43. Fujimori Y, Sato T, Hayata T, Nagao T, Nakayama M, Nakayama T, Sugamata R, Suzuki K. 2012. Novel antiviral characteristics of nanosized copper(I) iodide particles showing inactivation activity against 2009 pandemic H1N1 influenza virus. Appl Environ Microbiol 78:951-955. http:// dx.doi.org/10.1128/AEM.06284-11.
44. Hong R, Kang TY, Michels CA, Gadura N. 2012. Membrane lipid peroxidation in copper alloy-mediated contact killing of Escherichia coli. Appl Environ Microbiol 78:1776-1784. http://dx.doi.org/10.1128/ AEM.07068-11.
45. Sagripanti JL, Routson LB, Lytle CD. 1993. Virus inactivation by copper or iron ions alone and in the presence of peroxide. Appl Environ Microbiol 59:4374-4376.
46. Booth T, Kournikakis B, Bastien N, Ho J, Kobasa D, Stadnyk L, Li Y, Spence M, Paton S, Henry B, Mederski B, White D, Low D, McGeer A, Simor A, Vearncombe M, Downey J, Jamieson F, Tang P, Plummer F. 2005. Detection of airborne severe acute respiratory syndrome (SARS) coronavirus and environmental contamination in SARS outbreak units. J Infect Dis 191:1472-1477. http://dx.doi.org/10.1086/429634.
47. Breban R, Riou J, Fontanet A. 2013. Interhuman transmissibility of Middle East respiratory syndrome coronavirus: estimation of pandemic risk. Lancet 382:694-699. http://dx.doi.org/10.1016/S0140-6736(13)61492-0.
48. Soliman T, Cook AR, Coker RJ. 2015. Pilgims and MERS-CoV: what's the risk? Emerg Themes Epidemiol 12:3. http://dx.doi.org/10.1186/ s12982-015-0025-8.
49. Health Protection Agency (HPA) UK Novel Coronavirus Investigation team. 2013. Evidence of person-to-person transmission within a family cluster of novel coronavirus infections, United Kingdom, February 2013. Euro Surveill 18:20427.
50. Aberle JH, Popow-Kraupp T, Kreidl P, Laferl H, Heinz FX, Aberle SW. 2015. Influenza A and B viruses but not MERS-CoV in Hajj pilgrims, Austria, 2014. Emerg Infect Dis 21:726-727. http://dx.doi.org/10.3201/ eid2104.141745.
51. Webber MA, Whitehead RN, Mount M, Loman NJ, Pallen MJ, Piddock LJV. 2015. Parallel evolutionary pathways to antibiotic resistance selected by biocide exposure. J Antimicrob Chemother 70:2241-2248. http:// dx.doi.org/10.1093/jac/dkv109.
52. Michels HT, Keevil CW, Salgado CD, Schmidt MG. 2015. From laboratory research to a clinical trial: copper alloy surfaces kill bacteria and reduce hospital-acquired infections. HERD 9:64-79. http://dx.doi.org/ 10.1177/1937586715592650.