Skip to main content
SpringerLink
Log in

Inactivation of bacterial and viral biothreat agents on metallic copper surfaces

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

In recent years several studies in laboratory settings and in hospital environments have demonstrated that surfaces of massive metallic copper have intrinsic antibacterial and antiviral properties. Microbes are rapidly inactivated by a quick, sharp shock known as contact killing. The underlying mechanism is not yet fully understood; however, in this process the cytoplasmic membrane is severely damaged. Pathogenic bacterial and viral high-consequence species able to evade the host immune system are among the most serious lethal microbial challenges to human health. Here, we investigated contact-killing mediated by copper surfaces of Gram-negative bacteria (Brucella melitensis, Burkholderia mallei, Burkholderia pseudomallei, Francisella tularensis tularensis and Yersinia pestis) and of Gram-positive endospore-forming Bacillus anthracis. Additionally, we also tested inactivation of monkeypox virus and vaccinia virus on copper. This group of pathogens comprises biothreat species (or their close relatives) classified by the Center for Disease and Control and Prevention (CDC) as microbial select agents posing severe threats to public health and having the potential to be deliberately released. All agents were rapidly inactivated on copper between 30 s and 5 min with the exception of B. anthracis endospores. For vegetative bacterial cells prolonged contact to metallic copper resulted in the destruction of cell structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Blattner FR, Plunkett G 3rd, Bloch CA et al (1997) The complete genome sequence of Escherichia coli K-12. Science 277(5331):1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Casey AL, Adams D, Karpanen TJ et al (2010) Role of copper in reducing hospital environment contamination. J Hosp Infect 74(1):72–77

    Article  CAS  PubMed  Google Scholar 

  • Cox MM, Keck JL, Battista JR (2010) Rising from the ashes: DNA repair in Deinococcus radiodurans. PLoS Genet 6(1):e1000815

    Article  PubMed Central  PubMed  Google Scholar 

  • DelVecchio VG, Kapatral V, Redkar RJ et al (2002) The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc Natl Acad Sci USA 99(1):443–448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Elguindi J, Wagner J, Rensing C (2009) Genes involved in copper resistance influence survival of Pseudomonas aeruginosa on copper surfaces. J Appl Microbiol 106(5):1448–1455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Espírito Santo C, Taudte N, Nies DH, Grass G (2008) Contribution of copper ion resistance to survival of Escherichia coli on metallic copper surfaces. Appl Environ Microbiol 74(4):977–986

    Article  PubMed  Google Scholar 

  • Espírito Santo C, Morais PV, Grass G (2010) Isolation and characterization of bacteria resistant to metallic copper surfaces. Appl Environ Microbiol 76(5):1341–1348

    Article  PubMed Central  Google Scholar 

  • Espírito Santo C, Lam EW, Elowsky CG et al (2011) Bacterial killing by dry metallic copper surfaces. Appl Environ Microbiol 77(3):794–802

    Article  PubMed  Google Scholar 

  • Espírito Santo C, Quaranta D, Grass G (2012) Antimicrobial metallic copper surfaces kill Staphylococcus haemolyticus via membrane damage. MicrobiologyOpen 1(1):46–52

    Article  Google Scholar 

  • Faundez G, Troncoso M, Navarrete P, Figueroa G (2004) Antimicrobial activity of copper surfaces against suspensions of Salmonella enterica and Campylobacter jejuni. BMC Microbiol 4:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Grass G, Rensing C, Solioz M (2011) Metallic copper as an antimicrobial surface. Appl Environ Microbiol 77(5):1541–1547

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(6):1776–1784

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kugelman JR, Johnston SC, Mulembakani PM et al (2014) Genomic variability of monkeypox virus among humans, Democratic Republic of the Congo. Emerg Infect Dis 20(2):232–239

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuroda M, Ohta T, Uchiyama I et al (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357(9264):1225–1240

    Article  CAS  PubMed  Google Scholar 

  • Larsson P, Oyston PC, Chain P et al (2005) The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37(2):153–159

    Article  CAS  PubMed  Google Scholar 

  • Li J, Dennehy JJ (2011) Differential bacteriophage mortality on exposure to copper. Appl Environ Microbiol 77(19):6878–6883

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Macomber L, Rensing C, Imlay JA (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 189(5):1616–1626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marennikova SS, Seluhina EM, Mal’ceva NN, Ladnyj ID (1972) Poxviruses isolated from clinically ill and asymptomatically infected monkeys and a chimpanzee. Bull World Health Organ 46(5):613–620

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mathews S, Hans M, Mucklich F, Solioz M (2013) Contact killing of bacteria on copper is suppressed if bacterial-metal contact is prevented and is induced on iron by copper ions. Appl Environ Microbiol 79(8):2605–2611

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mehtar S, Wiid I, Todorov SD (2008) The antimicrobial activity of copper and copper alloys against nosocomial pathogens and Mycobacterium tuberculosis isolated from healthcare facilities in the Western Cape: an in vitro study. J Hosp Infect 68(1):45–51

    Article  CAS  PubMed  Google Scholar 

  • Mikolay A, Huggett S, Tikana L et al (2010) Survival of bacteria on metallic copper surfaces in a hospital trial. Appl Microbiol Biotechnol 87(5):1875–1879

    Article  CAS  PubMed  Google Scholar 

  • Nierman WC, DeShazer D, Kim HS et al (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci USA 101(39):14246–14251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(3):289–297

    Article  CAS  PubMed  Google Scholar 

  • Noyce JO, Michels H, Keevil CW (2007) Inactivation of influenza A virus on copper versus stainless steel surfaces. Appl Environ Microbiol 73(8):2748–2750

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nyerges G, Szathmary J, Benko A (1968) Comparative laboratory study of vaccines prepared from the international reference strain and from the “Budapest” strain of vaccinia virus. Acta Microbiol Acad Sci Hung 15(3):199–205

    CAS  PubMed  Google Scholar 

  • Parkhill J, Wren BW, Thomson NR et al (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413(6855):523–527

    Article  CAS  PubMed  Google Scholar 

  • Quaranta D, Krans T, Espírito Santo C et al (2011) Mechanisms of contact-mediated killing of yeast cells on dry metallic copper surfaces. Appl Environ Microbiol 77(2):416–426

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sahl JW, Stone JK, Gelhaus HC et al (2013) Genome sequence of Burkholderia pseudomallei NCTC 13392. Genome Announc 1(3) pii: e00183-13

  • Salgado CD, Sepkowitz KA, John JF et al (2013) Copper surfaces reduce the rate of healthcare-acquired infections in the intensive care unit. Infect Control Hosp Epidemiol 34(5):479–486

    Article  PubMed  Google Scholar 

  • Warnes SL, Keevil CW (2013) Inactivation of norovirus on dry copper alloy surfaces. PLoS ONE 8(9):e75017

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(16):5390–5401

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warnes SL, Highmore CJ, Keevil CW (2012) Horizontal transfer of antibiotic resistance genes on abiotic touch surfaces: implications for public health. mBio 3(6)

  • Weaver L, Michels HT, Keevil CW (2008) Survival of Clostridium difficile on copper and steel: futuristic options for hospital hygiene. J Hosp Infect 68(2):145–151

    Article  CAS  PubMed  Google Scholar 

  • Weaver L, Noyce JO, Michels HT, Keevil CW (2010) Potential action of copper surfaces on meticillin-resistant Staphylococcus aureus. J Appl Microbiol 109(6):2200–2205

    Article  CAS  PubMed  Google Scholar 

  • Wheeldon LJ, Worthington T, Lambert PA et al (2008) Antimicrobial efficacy of copper surfaces against spores and vegetative cells of Clostridium difficile: the germination theory. J Antimicrob Chemother 62(3):522–525

    Article  CAS  PubMed  Google Scholar 

  • Wilks SA, Michels HT, Keevil CW (2006) Survival of Listeria monocytogenes Scott A on metal surfaces: implications for cross-contamination. Int J Food Microbiol 111(2):93–98

    Article  PubMed  Google Scholar 

  • Wolff DA, Bubel HC (1964) The disposition of lysosomal enzymes as related to specific viral cytopathic effects. Virology 24:502–505

    Article  CAS  PubMed  Google Scholar 

  • Zeiger M, Solioz M, Edongue H, Arzt E, Schneider AS (2014) Surface structure influences contact killing of bacteria by copper. MicrobiologyOpen 3(3):327–332

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Holger Scholz (InstMikroBioBw, München), Wolf Splettstößer (InstMikroBioBw, München) and Birgit Strommenger (RKI, Werningerode) for sharing bacterial strains. Thanks are due to Daniela Horenkamp and Jutta Brohl for assistance in BSL-3-work. This work was supported by a research grant from the International Copper Association (ICA)/Copper Development Association (CDA) and CES by a graduate fellowship of the Fundação para a Ciência e Tecnologia, Portugal.

Author information

Authors and Affiliations

  1. Bundeswehr Institute of Microbiology, Munich, Germany

    Pauline Bleichert, Christophe Espírito Santo, Matthias Hanczaruk, Hermann Meyer & Gregor Grass

  2. Institute for Liver & Digestive Health, University College London Medical School, London, UK

    Christophe Espírito Santo

Authors
  1. Pauline Bleichert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christophe Espírito Santo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthias Hanczaruk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hermann Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gregor Grass
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregor Grass.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bleichert, P., Espírito Santo, C., Hanczaruk, M. et al. Inactivation of bacterial and viral biothreat agents on metallic copper surfaces. Biometals 27, 1179–1189 (2014). https://doi.org/10.1007/s10534-014-9781-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-014-9781-0

Keywords

Search

Navigation