The molecular mechanisms of copper and silver ion disinfection of bacteria and viruses

Critical Reviews in Environmental Control

Volumn 18, Issue 4, 1989, Pages 295-315

  Thurman, Robert B ^a   Gerba, Charles P ^b  

^a Enivronmental Research Laboratory ^*  (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; DRINKING WATER; SILVER;

DISINFECTION; NONHUMAN; REVIEW; WATER TREATMENT;

EID: 0024243101     PISSN: 1040838X     EISSN: None     Source Type: Journal    
DOI: 10.1080/10643388909388351     Document Type: Article

References (119)

1. Babich, H. and Stotzky, G., Environmental factors that influence the toxicity of heavy metal and gaseous pollutants to microorganisms, CRC Crit. Rev, Microbiol., 8(2), 99, 1980.
2. Sundberg, R. J. and Martin, R. B., Interactions of histidine and other imidazole derivatives with transition metal ions in chemical and biological systems, Chem. Rev., 74, 471, 1974.
3. Phillips, C. R. and Warshowsky, B., Chemical disinfectants, Am. Rev. Microbiol., 12, 525, 1958.
4. Just, J. and Szniolis, A. Germicidal properties of silver in water, J. Am. Water Works Assoc., 28, 492, 1936.
5. Kojarmek, A. M. and Halevy, A. H., Sucrose pulsing of gladiolus stems before storage to increase spike quality, Hortic. Sci. 11, 572, 1976.
6. Modak, S. and Fox, C. L., Jr., Synergistic action of silver sulfadiazine and sodium piperacillin on resistant Pseudomonas aeruginosa in vitro and in experimental burn wound infections, J. Trauma, 25, 27, 1985.
7. Muller, G., Kempf, T., Goethe, H., and Herrmann, R., Drinking water preservation for life boats, Forum Staedte Hyg., 28, 33, 1977.
8. Speck, W. T., Driscoll, J. R. Polin R. A., and Rosenkranz, H. S., Bacterial colonization in the new-born, effect of cord care, Pediatrics, 10, 335, 1976.
9. Wang, P. Y., Silver ion-dextran hydrogel on Pseudomonas aeruginosa infected rodent skin wound, Org. Coat. Appl. Polym. Sci., 48, 393, 1983.
10. Block, S. S., Definition in terms, in Disinfection, Sterilization and Preservation, Block, S. S. Ed., Lea ‖ Febiger Philadelphia, 1983, 877.
11. Koski, T. A. and Chen, J. H. S., Methods of testing viracides, in Disinfection, Sterilization and Preservation, Block, S. S., Ed., Lea ‖ Febiger, Philadelphia, 1977, 116.
12. Thurman, R. B. and Gerba, C. P., Molecular mechanisms of viral inactivation by water disinfectants, in Advances in Applied Microbiology, Vol. 33, Academic Press, San Diego, CA, 1988, 75.
13. Chang, S. L. Modern concept of disinfection, in Proc. Natl. Special Conf. Disinfection, American Society of Civil Engineers, New York, 1970, 635.
14. Shimizu, F., Shimizu, Y., and Kumagai, K., Specific inactivation of Herpes Simplex, Antimicrob. Agents Chemother., 10, 57, 1976.
15. Cooksey, D. A. Characterization of a copper resistance plasmid conserved in copper-resistant strains of Pseudomonas syringae pv. tomato, Appl. Environ. Microbiol., 53, 454, 1987.
16. Bender, C. L. and Cooksey, D. A., Indigenous plasmids in Pseudomonas syringae pv. tomato and Xanthomonas campestris pv. vesicatoria in tomato and pepper seeds, Phytopathology, 72, 1143, 1986.
17. Stall, R. E., Loschke, D. C., and Jones, J. B., Linkage of copper resistance and avirulence loci on a self-transmissible plasmid in Xanthomonas campestris pv. vesicatoria, Phytopathology, 76, 240, 1986.
18. Adaskaveg, J. E. and Hine, R. B., Copper tolerance and zinc sensitivity of Mexican strains of Xanthomonas campestris pv. vesicatoria, casual agent of bacterial spot of pepper, Plant Dis., 69, 993, 1985.
19. Wood, J. M., Microbiological strategies in resistance to metal ion toxicity, in Metal Ions in Biological Systems, Vol. 18, Sigel, H., Ed., Marcel Dekker, New York, 1984, 334.
20. Hendry, A. T. and Stewart, I. O., Silver-resistant Enterobacteriaceae from hospital patients, Can. J. Microbiol, 25, 915, 1979.
21. Pumpel, T. and Schinner, F., Silver tolerance and silver accumulation of microorganisms from soil materials of a silver mine, Appl. Microbiol Biotechnol., 24, 244, 1986.
22. Park, G. A., Adsorption in the marine environment, in Chemical Ocean, Vol. 1, Riley, J. P. and Skirrow, G., Eds., Academic Press, New York, 1976, 241.
23. Murray, J. P., Thermodynamics of Poliovirus Adsorption, Ph.D. thesis, Stanford University, Palo Alto, CA, 1978, 71.
24. Lippy, E. C., Chlorination to prevent and control waterborne diseases, J. Am. Water Works Assoc., January, 49, 1986.
25. Sletten, O., Halogens and their role in disinfection, J. Am. Water Works Assoc., December, 690, 1974.
26. Wood, J. M., Evolutionary aspects of metal ion transport through cell membranes, in Metal Ions in Biological Systems, Vol. 18, Sigel, H., Ed., Marcel Dekker, New York, 1984, 233.
27. Alvarez, M. E. and O'Brien, R. T., Effects of chlorine concentration on the structure of poliovirus, Appl. Environ. Microbiol., 43, 237, 1982.
28. Sharp, D. G., Virion aggregation and disinfection of water by chlorine and bromine, EPA-600/S2-82-022, National Technical Information Service, VA, 1982.
29. Young, D. C. and Sharp, D. G., Partial reactivation of chlorine-treated echovirus, Appl. Environ. Microbiol., 37, 766, 1979.
30. Young, D. C. and Sharp, D. G., Virion conformational forms and the complex inactivation kinetics of echovirus by chlorine in water, Appl. Environ. Microbiol., 49, 359, 1985.
31. Sharp, D. G., Floyd, R., and Johnson, J. D., Nature of the surviving plaque-forming unit of reovirus in water containing bromine, Appl. Environ. Microbiol., 29, 94, 1975.
32. Luria, S. E., Reactivation of irradiated bacteriophage by transfer of self-reproducing units, Proc. Natl. Acad. Sci. U.S.A., 33, 253, 1947.
33. Luria, S. E. and Dulbecco, R., Genetic recombinations leading to production of active bacteriophage from ultraviolet inactivated bacteriophage particles, Genetics, 34, 93, 1949.
34. Chambers, C. W. and Proctor, C. M., The bacteriological and chemical behavior of silver in low concentration, Division of Water Supply and Pollution Control, U.S. Department of Health, Education and Welfare, Cincinnati, OH, 1960.
35. Cllver, D. O., Foell, W. K., and Goepfert, J. M., Biocidal effects of silver, Final Technical Report, Contract NAS 9–9300, University of Wisconsin, Madison, February, 1971.
36. Netzer, A. and Hughes, D. E., Adsorption of copper, lead and cobalt by activated carbon, Water Res., 18, 927, 1984.
37. James, G. V., Water Treatment, 4th ed., CRC Press, Cleveland, OH, 1971, 38.
38. Wuhrmann, K. and Zobrist, F., Investigations into the bactericidal action of silver in water, Schweiz. Hydrol. 20, 218, 1958.
39. Jensen, A. and Jorgensen, S. E., Analytical chemistry applied to metal ions in the environment, in Metal Ions in Biological Systems, Vol. 18, Sigel, H., Ed., Marcel Dekker, New York, 1984, 5.
40. Charney, J., Fischer, W. P. M., Sagin, J. F., and Tytell, A. A., Inactivation of concentrated purified poliovirus suspensions, Ann. N. Y. Acad. Sci., 83, 649, 1960.
41. Chick, H., Factors conditioning the velocity of disinfection, Chem. Ads., 7, 2273, 1913.
42. Floyd, R., Johnson, J. D., and Sharp, D. G. Inactivation by bromine of single poliovirus particles in water, Appl. Environ. Microbiol., 31, 298, 1976.
43. Poduska, R. A. and Hershey, D., Model for virus inactivation by chlorination, J. Water Pollut. Control Fed., 44, 738, 1972.
44. Boardman, G. D. and Sproul, O. J., Protection of viruses during disinfection by adsorption to particulate matter, J. Water Pollut. Control Fed., 49, 1857, 1977.
45. Butler, M., Medlen, A. R., and Taylor, G. R., Electrofocusing of viruses and sensitivity to disinfection, Water Sci. Technol., 17, 201, 1985.
46. Young, D. C., Johnson, J. D., and Sharp, D. G., The complex reaction kinetics of echo-1 virus with chlorine in water (39965), Proc. Soc. Exp. Biol. Med., 156, 496, 1977.
47. Mandel, B., Characterization of type 1 poliovirus by electrophoretic analysis, Virology, 44, 544, 1971.
48. Grimmel, M., Zibirre, R., and Koch, G., Fluorescence spectrophotometric study of structural alterations in the capsid of poliovirus, Arch. Virol., 78, 191, 1983.
49. Sterritt, R. M. and Lester, J. N., Interactions of heavy metals with bacteria, Sci. Total Environ., 14, 5, 1980.
50. Ehret, W. F., College Chemistry, 6th ed., Appleton-Century, New York, 1935, 551.
51. Martin, R. B., Bioinorganic chemistry of metal ion toxicity, in Metal Ions in Biological Systems, Vol. 20, Sigel, H., Ed., Marcel Dekker, New York, 1986, 21.
52. Osterberg, R., Metal ion-protein interactions in solutions, in Metal Ions in Biological Systems, Vol. 3, Sigel, H., Ed., Marcel Dekker, New York, 1974, 46.
53. Leonard, A., Chromosome damage in individuals exposed to heavy metals, in Metal Ions in Biological Systems, Vol. 20, Sigel, H., Ed., Marcel Dekker, New York, 1986, 229.
54. Fair, G. M., Geyer, J. C., and Okun, D. A., Elements of Water Supply and Wastewater Disposal, 2nd ed., John Wiley ‖ Sons, New York, 1971.
55. Murray, J. P. and Laband, S. J., Degradation of poliovirus by adsorption on inorganic surfaces, Appl. Environ. Microbiol., 37, 480, 1979.
56. Bitton, G. and Friehofer, V. Influence of extracellular polysaccharides on the toxicity of copper and cadmium toward Klebsiella aerogenes, Microbiol. Ecol., 4, 119, 1978.
57. Totsuka, A. and Ohtaki, K., The effects of amino acids and metals on the infectivity of poliovirus ribonucleic acid, Jpn. J. Microbiol., 18, 107, 1974.
58. Yamamoto, N., Hiatt, C. W., and Haller, W., Mechanism of inactivation of bacteriophages by metals, Biochim. Biophys. Acta, 91, 257, 1964.
59. Jordan, F. T. and Nassar, T. J., The influence of copper on the survival of infectious bronchitis vaccine virus in water. Vet. Rec, 89, 609, 1971.
60. Singh, A., LeChevallier, M. W. and McFeters, G. A., Reduced virulence of Yersinia enterocolitica by copper-induced injury, Appl. Environ. Microbiol. 50, 406, 1985.
61. Tilton, R. C. and Rosenberg, B., Reversal of the silver inhibition of microorganisms by agar, Appl. Environ. Microbiol., 35, 1116, 1978.
62. Foye, W. O., Antimicrobial activities of mineral elements, in Microorganisms and Minerals, Weinberg, E. D., Ed., Marcel Dekker, New York, 1977.
63. Friberg, L., Nordberg, G. F., and Vouk, V. B., Eds., Silver, in Handbook on the Toxicity of Metals, Elsevier/North-Holland, Amsterdam, 1979, 579.
64. Youmans, T. and Davidson, N., On the complexing of desoxyribonucleic acid by silver, Biochim. Biophys. Acta, 55, 609, 1962.
65. Chambers, C. W., Proctor, C. M., and Kabler, P. W., Bactericidal effect of low concentrations of silver, J. Am. Water Works Assoc., 54, 208, 1962.
66. Woodward, R. L., Review of the bactericidal effectiveness of silver, J. Am. Water Works Assoc., July, 881, 1963.
67. Newton, W. L. and Jones, M. F., Effectiveness of silver ions against cysts of Entamoeba histolytica, J. Am. Water Works Assoc., 41, 1027, 1949.
68. Moroz, O. G., Kurskii, L. A., Prokuryakova, N. B., Rudenko, A. V., and Florensova, K. M., Susceptibility of organisms which cause intestinal infections to removal by silver, Khim. Technol. (Kiev), 2, 275, 1980.
69. McCoy, E. C. and Rosenkranz, H. S., Silver sulfadiazine: lack of mutagenic activity, Chemotherapy, 24, 87, 1978.
70. Zachary, L., Heggers, J. P., Robson, M. C., Leach, A., Ko, F., and Berta, M., The use of topical antimicrobials combined with biobrane in burn wound infections, J. Trauma, 22, 833, 1982.
71. Chang, T-W. and Weinstein, L., In vitro activity of silver sulfadiazine against Herpesvirus hominis, J. Infect. Ois., 132, 79, 1975.
72. Richards, R. M. E., Antimicrobial action of silver nitrate, Microbios, 31, 83, 1981.
73. Mahnel, H. and Schmidt, M., Effect of silver compounds on viruses in water, Zentralbl. Baktenol. Parasitenk. Infektionskr. Hyg. Abt. Orig. Reihe B., 182, 381, 1986.
74. Coleman, V. R., Wilkie, J., Levinson, W. E., Stevens, T., and Jawetz, E., Inactivation of Herpesvirus hominis types 1 and 2 by silver nitrate in vitro and in vivo, Antimicrob, Agents ‖ Chemother., 4, 259, 1973.
75. Prevot, J., Ouvrard, S, Coiron, C., and Festy, B., Persistance de virus dans des eaux de bassins de natation artificiellement contaminees, Rev. Int. Sci. L'eaux 2, 59, 1986.
76. Lawrence, C. A. and Block, S. S., Disinfection, sterilization and preservation, in Disinfection, Sterilization and Preservation, Block, S. S., Ed., Lea ‖ Febiger, Philadelphia, 1968.
77. Lund, E., The significance of oxidation in chemical inactivation of poliovirus, Arch. Ges. Virusforsch., 12, 648, 1963.
78. Samuni, A., Chevion, M., and Czapski, G., Roles of copper and superoxide anion radicals in the radiation-induced inactivation of T7 bacteriophage, Radiat. Res., 99, 562, 1984.
79. Samuni, A., Aronovitch, J., Godinger, D., Chevion, M., and Czapski, G., On the cytotoxicity of vitamin C and metal ions, Eur. J. Biochem., 137, 119, 1983.
80. Hatano, M. and Nozawa, T., Catalytic activity of poly-L, alpha-amino acid-metal ion complexes: new approaches to enzyme models, in Metal Ions in Biological Systems, Vol. 5, Sigel, H., Ed., Marcel Dekker, New York, 1976, 246.
81. Peterwig, H. G., Pharmacology and toxicology of heavy metals: silver, Pharmacol. Ther., 1 127, 1976.
82. Rahn, R. O. and Landry, L. C., Ultraviolet irradiation of nucleic acids complexed with heavy atoms. II. Phosphorescence and photodimerization of DNA complexed with Ag, Photochem. Photobiol., 18, 29, 1973.
83. 2+on the sensitivity of phage and of transforming DNA to ultraviolet radiation, Photochem. Photobiol., 18, 39, 1973.
84. Grier, N., Silver and its compounds, in Disinfection, Sterilization and Preservation, Block, S. S., Ed., Lea ‖ Febiger, Philadelphia, 1983, 375.
85. Ricketts, C. R., Mechanism of prophylaxis by silver compounds against infection of burns, Br. Med. J, 2, 444, 1970.
86. Fox, C. L., Jr. and Modak, S. M., Mechanisms of silver sulphadiazine action on burn wound infections, Antimicrob. Agents ‖ Chemother., 5, 528, 1974.
87. Eichhorn, G. L., Berger, N. A., Butzow, J. J., Clark, P., Heim, J., Pitha, J., Richardson, C., Rifkind, J. M., Shin, Y., and Tarien, E., Some effects of metal ions on the structure and function of nucleic acids, in Metal Ions in Biological Systems, Vol. 40, Dhar, S. K., Ed., Plenum Press, New York, 1973 43.
88. Barton, J. K. and Lippard, S. J., Heavy metal interactions with nucleic acids, in Nucleic Acid-Metal Interactions, Spiro, T. G., Ed., John Wiley ‖ Sons, New York, 1980, 33.
89. Richard, H., Schreiber, J. P., and Duane, M., Interactions of metallic ions with DNA. V. DNA renaturation mechanism in the presence of Cu(II), Biopolymers, 12, 1, 1973.
90. Plastourgou, M. and Hoffman, M. R., Transformation and fate of organic esters in layered-flow systems: the role of trace metal catalysis, Environ. Sci. Technol, 18, 756, 1984.
91. Schindler, P. W., Surface complexation, in Metal Ions in Biological Systems, Vol. 18, Sigel, H., Ed., Marcel Dekker, New York, 1984, 105.
92. Stumm, W. and Morgan, J. J., The solid-solution interface, in Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Water, 2nd ed., John Wiley ‖ Sons, New York, 1981.
93. Domek, M. J., LeChevallier, M. W., Cameron, S. C., and McFeters, G. A., Evidence for the role of copper in the injury process of coliform bacteria in drinking water, Appl. Environ. Microbiol., 48, 289, 1984.
94. Hay, R. W., Metal ion-catalyzed decarboxylations of biological interest, in Metal Ions in Biological Systems, Vol. 5, Sigel, H., Ed., Marcel Dekker, New York, 1976, 127.
95. Martin, R. B., Acid-catalyzed ester hydrolysis, J. Am. Chem. Soc., 89, 2501, 1967.
96. Huff, J. W., Sastry, K. S., Gordon, M. P., and Wacker, W. E. C., The action of metal ions on tobacco mosaic virus ribonucleic acid, Biochemistry, 3, 501, 1964.
97. Daune, M., Interactions of metal ions with nucleic acids, in Metal Ions In Biological Systems, Vol. 3, Sigel, H., Ed., Marcel Dekker, New York, 1974, 2.
98. Davydova, S. L., Macromolecules of biological interest in complex formation, in Metal Ions in Biological Systems, Vol. 8, Sigel, H., Ed., Marcel Dekker, New York, 1979, 183.
99. Martin, R. B. and Mariam, Y. H., Interaction between metal ions and nucleic bases, nucleosides, and nucleotides in solution, in Metal Ions in Biological Systems, Vol. 8, Sigel, H., Ed., Marcel Dekker, New York, 1979, 57.
100. Singh, A. and McFeters, G. A., Recovery, growth and production of heat-stable enterotoxin by Escherichia coli after copper-induced injury, Appl. Environ. Microbiol., 51, 738, 1986.
101. Singh, A. and McFeters, G. A., Survival and virulence of copper- and chlorine-stressed Yersinia enterocolitica in experimentally infected mice, Appl. Environ. Microbiol., 53, 1768, 1987.
102. Singh, A., Yeager, R., and McFeters, G. A., Assessment of in vivo revival, growth, and pathogenicity of Escherichia coli strains after copper- and chlorine-induced injury, Appl. Environ. Microbiol., 52, 832, 1986.
103. Rifkind, J. M., Shin, Y. A., Heim, J. M., and Eichhorn, G. L. Cooperative disordering of single-stranded polynucleotides through copper crosslinking, Biopolymers, 15, 1879, 1976.
104. Ueda, K., Morita, J., Yamashita, K., and Komano, T., Inactivation of bacteriophage 0X174 by mitomycin C in the presence of sodium hydrosulfite and cupric ions, Chem. Biol. Interact., 29, 145, 1980.
105. Nishioka, H., Mutagenic activities of metal compounds in bacteria, Mutat. Res., 31, 185, 1975.
106. Kada, T., Sadaie, Y., and Tutikawa, K., In vitro and host-mediated “rec-assay” procedures for screening chemical mutagens, and phloxine, a mutagenic red dye detected, Mutat. Res., 16, 165, 1972.
107. Hutchinson, D. W., Metal chelators as potential antiviral agents, Antiviral Res., 5, 193, 1985.
108. Buffie, J., Natural organic matter and metal-organic interactions in aquatic systems, in Metal Ions in Biological Systems, Vol. 18, Sigel, H., Ed., Marcel Dekker, New York, 1984, 165.
109. Wong, K., Morgan, A. R., and Paranchych, W., Controlled cleavage of phage R17 RNA within the virion by treatment with ascorbate and copper (II), Can. J. Biochem., 52, 950, 1974.
110. Shinohara, K., So, M., Nonaka, M., Nishiyama, K., Murakami, H., and Omura, H., Lambda DNA-fragmenting actions of ascorbic acid and triose reductone in the presence of copper (II), J. Nutr. Sci. VitaminoL, 29, 671, 1983.
111. Edebo, L., Singh, M. P., and Hoglund, S., Inactivation of some coliphages with copper-thiol complexes, J. Gen. Virol., I, 567, 1967.
112. Dubes, G. R. and Al-Moslih, M. I., Effect of inactivator(s) formed from copper and phenol impurity(ies) on the sedimentation rate of transfective poliovirion RNA, Arch. Virol., 66, 45, 1980.
113. Hay, R. W. and Morris, P. J., Metal ion promoted hydrolysis, in Metal ions in Biological Systems, Vol. 5, Sigel, H., Ed., Marcel Dekker, New York, 1976, 173.
114. Zimmer, C., Luck, G., Fritzsche, H., and Triebel, H., DNA-copper (II) complex and the DNA con-formation, Biopolymers, 10, 441, 1971.
115. Eichhorn, G. L. and Clark, P., Interactions of metal ions with polynucleotides and related compounds. V. The unwinding and rewinding of DNA strands under the influence of copper (II) ion, Proc. Natl. Acad. Sci. U.S.A., 53, 586, 1965.
116. Sigman, D. S., Graham, D. R., D'Aurora, V., and Stern A. M., Oxygen-dependent cleavage of DNA by the 1, 10-phenathroline cuprous complex, J. Biol. Chem., 254, 12269, 1979.
117. Kuwahara, J., Suzuki, T., Funakoshi, K., and Sugiura, Y., Photosensitive DNA cleavage and phage inactivation by copper (II)-camptothecin, Biochemistry, 25, 1216, 1986.
118. Vasudevachari, M. B. and Antony, A., Inhibition of avian myeloblastosis virus reverse transcriptase and virus inactivation by metal complexes of isonicotinic acid hydrazide, Antiviral Res., 2, 291, 1982.
119. Taylor, G. R., The effect of disinfectants on picornavirus structure and infectivity, in Viruses and Disinfection of Water and Wastewater, Butler, M., Medlen, A. R., and Morris, R., Eds., University of Surrey, Guildford, Surrey, England, 1982, 289.