Resistance of Acanthamoeba cysts to disinfection treatments used in health care settings

Journal of Clinical Microbiology

Volumn 48, Issue 8, 2010, Pages 2689-2697

  Coulon, Céline ^a,b   Collignon, Anne ^b   McDonnell, Gerald ^c   Thomas, Vincent ^a  

^a STERIS SA R and D   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c STERIS Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCIDE; DISINFECTANT AGENT;

ACANTHAMOEBA; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CYST (RESTING STAGE); DISINFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PESTICIDE RESISTANCE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; DNA SEQUENCE; DRUG EFFECTS; DRUG RESISTANCE; HEALTH CARE FACILITY; HEAT; HUMAN; INFECTION CONTROL; MICROBIAL VIABILITY; MOLECULAR GENETICS; PROCEDURES; PROTOZOAN SPORE; RADIATION RESPONSE; TIME;

ACANTHAMOEBA; DISINFECTANTS; DRUG RESISTANCE; HEALTH FACILITIES; HOT TEMPERATURE; HUMANS; INFECTION CONTROL; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SPORES, PROTOZOAN; TIME FACTORS;

ACANTHAMOEBA; PROTOZOA;

EID: 77955446656     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00309-10     Document Type: Article

References (63)

1. Adekambi, T., S. Ben Salah, M. Khlif, D. Raoult, and M. Drancourt. 2006. Survival of environmental mycobacteria in Acanthamoeba polyphaga. Appl. Environ. Microbiol. 72:5974-5981.
2. Anger, C., and J. M. Lally. 2008. Acanthamoeba: a review of its potential to cause keratitis, current lens care solution disinfection standards and methodologies, and strategies to reduce patient risk. Eye Contact Lens 34:247-253.
3. Barbaree, J. M., B. S. Fields, J. C. Feeley, G. W. Gorman, and W. T. Martin. 1986. Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila. Appl. Environ. Microbiol. 51:422-424.
4. Barbee, S. L., D. J. Weber, M. D. Sobsey, and W. A. Rutala. 1999. Inactivation of Cryptosporidium parvum oocyst infectivity by disinfection and sterilization processes. Gastrointest. Endosc. 49:605-611.
5. Barete, S., A. Combes, J. F. de Jonckheere, A. Datry, S. Varnous, V. Martinez, S. G. Ptacek, E. Caumes, F. Capron, C. Frances, C. Gibert, and O. Chosidow. 2007. Fatal disseminated Acanthamoeba lenticulata infection in a heart transplant patient. Emerg. Infect. Dis. 13:736-738.
6. Barker, J., and M. R. Brown. 1994. Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140(Pt 6):1253-1259. (Pubitemid 2111945)
7. Beattie, T. K., D. V. Seal, A. Tomlinson, A. K. McFadyen, and A. M. Grimason. 2003. Determination of amoebicidal activities of multipurpose contact lens solutions by using a most probable number enumeration technique. J. Clin. Microbiol. 41:2992-3000.
8. Best, M., S. A. Sattar, V. S. Springthorpe, and M. E. Kennedy. 1990. Efficacies of selected disinfectants against Mycobacterium tuberculosis. J. Clin. Microbiol. 28:2234-2239.
9. Booton, G. C., D. J. Kelly, Y. W. Chu, D. V. Seal, E. Houang, D. S. Lam, T. J. Byers, and P. A. Fuerst. 2002. 18S ribosomal DNA typing and tracking of Acanthamoeba species isolates from corneal scrape specimens, contact lenses, lens cases, and home water supplies of Acanthamoeba keratitis patients in Hong Kong. J. Clin. Microbiol. 40:1621-1625.
10. Booton, G. C., G. S. Visvesvara, T. J. Byers, D. J. Kelly, and P. A. Fuerst. 2005. Identification and distribution of Acanthamoeba species genotypes associated with nonkeratitis infections. J. Clin. Microbiol. 43:1689-1693.
11. Buck, S. L., and R. A. Rosenthal. 1996. A quantitative method to evaluate neutralizer toxicity against Acanthamoeba castellanii. Appl. Environ. Microbiol. 62:3521-3526.
12. Buck, S. L., R. A. Rosenthal, and B. A. Schlech. 2000. Methods used to evaluate the effectiveness of contact lens care solutions and other compounds against Acanthamoeba: a review of the literature. CLAO J. 26:72-84.
13. Byers, T. J., B. G. Kim, L. E. King, and E. R. Hugo. 1991. Molecular aspects of the cell cycle and encystment of Acanthamoeba. Rev. Infect. Dis. 13(Suppl. 5):S373-S384.
14. Carlesso, A. M., G. L. Artuso, K. Caumo, and M. B. Rott. 2010. Potentially pathogenic Acanthamoeba isolated from a hospital in Brazil. Curr. Microbiol. 60:185-190.
15. Chavez-Munguia, B., M. Omana-Molina, M. Gonzalez-Lazaro, A. Gonzalez-Robles, P. Bonilla, and A. Martinez-Palomo. 2005. Ultrastructural study of encystation and excystation in Acanthamoeba castellanii. J. Eukaryot. Microbiol. 52:153-158.
16. Critchley, M., and R. Bentham. 2009. The efficacy of biocides and other chemical additives in cooling water systems in the control of amoebae. J. Appl. Microbiol. 106:784-789.
17. Dart, J. K., V. P. Saw, and S. Kilvington. 2009. Acanthamoeba keratitis: diagnosis and treatment update 2009. Am. J. Ophthalmol. 148:487-499.
18. Duarte, R. S., M. C. Lourenco, S. Fonseca Lde, S. C. Leao, L. Amorim Ede, I. L. Rocha, F. S. Coelho, C. Viana-Niero, K. M. Gomes, M. G. da Silva, N. S. Lorena, M. B. Pitombo, R. M. Ferreira, M. H. Garcia, G. P. de Oliveira, O. Lupi, B. R. Vilaca, L. R. Serradas, A. Chebabo, E. A. Marques, L. M. Teixeira, M. Dalcolmo, S. G. Senna, and J. L. Sampaio. 2009. Epidemic of postsurgical infections caused by Mycobacterium massiliense. J. Clin. Microbiol. 47:2149-2155.
19. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
20. Eterpi, M., G. McDonnell, and V. Thomas. 2009. Disinfection efficacy against parvoviruses in comparison to reference viruses. J. Hosp. Infect. 73:64-70.
21. Greub, G., and D. Raoult. 2003. Biocides currently used for bronchoscope decontamination are poorly effective against free-living amoebae. Infect. Control Hosp. Epidemiol. 24:784-786.
22. Greub, G., and D. Raoult. 2004. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17:413-433.
23. Griffiths, P. A., J. R. Babb, C. R. Bradley, and A. P. Fraise. 1997. Glutaraldehyde-resistant Mycobacterium chelonae from endoscope washer disinfectors. J. Appl. Microbiol. 82:519-526.
24. Hoffmann, R., and R. Michel. 2001. Distribution of free-living amoebae (FLA) during preparation and supply of drinking water. Int. J. Hyg. Environ. Health 203:215-219.
25. Hughes, R., W. Heaselgrave, and S. Kilvington. 2003. Acanthamoeba polyphaga strain age and method of cyst production influence the observed efficacy of therapeutic agents and contact lens disinfectants. Antimicrob. Agents Chemother. 47:3080-3084.
26. Johnston, S. P., R. Sriram, Y. Qvarnstrom, S. Roy, J. Verani, J. Yoder, S. Lorick, J. Roberts, M. J. Beach, and G. Visvesvara. 2009. Resistance of Acanthamoeba cysts to disinfection in multiple contact lens solutions. J. Clin. Microbiol. 47:2040-2045.
27. Khunkitti, W., D. Lloyd, J. R. Furr, and A. D. Russell. 1998. Acanthamoeba castellanii: growth, encystment, excystment and biocide susceptibility. J. Infect. 36:43-48. (Pubitemid 128645624)
28. Kilvington, S. 1991. Moist-heat disinfection of Acanthamoeba cysts. Rev. Infect. Dis. 13(Suppl. 5):S418.
29. Kilvington, S., and C. Anger. 2001. A comparison of cyst age and assay method of the efficacy of contact lens disinfectants against Acanthamoeba. Br. J. Ophthalmol. 85:336-340.
30. Kilvington, S., T. Gray, J. Dart, N. Morlet, J. R. Beeching, D. G. Frazer, and M. Matheson. 2004. Acanthamoeba keratitis: the role of domestic tap water contamination in the United Kingdom. Invest. Ophthalmol. Vis. Sci. 45:165-169.
31. Kohsler, M., D. Leitsch, U. Furnkranz, M. Duchene, H. Aspock, and J. Walochnik. 2008. Acanthamoeba strains lose their abilities to encyst synchronously upon prolonged axenic culture. Parasitol. Res. 102:1069-1072.
32. Lackner, P., R. Beer, G. Broessner, R. Helbok, B. Pfausler, C. Brenneis, H. Auer, J. Walochnik, and E. Schmutzhard. 2010. Acute granulomatous Acanthamoeba encephalitis in an immunocompetent patient. Neurocrit. Care 12:91-94.
33. Ledee, D. R., A. Iovieno, D. Miller, N. Mandal, M. Diaz, J. Fell, M. E. Fini, and E. C. Alfonso. 2009. Molecular identification of T4 and T5 genotypes in isolates from Acanthamoeba keratitis patients. J. Clin. Microbiol. 47:1458-1462.
34. Lloyd, D., N. A. Turner, W. Khunkitti, A. C. Hann, J. R. Furr, and A. D. Russell. 2001. Encystation in Acanthamoeba castellanii: development of biocide resistance. J. Eukaryot. Microbiol. 48:11-16.
35. Lorenzo-Morales, J., J. Kliescikova, E. Martinez-Carretero, L. M. De Pablos, B. Profotova, E. Nohynkova, A. Osuna, and B. Valladares. 2008. Glycogen phosphorylase in Acanthamoeba spp.: determining the role of the enzyme during the encystment process using RNA interference. Eukaryot. Cell 7:509-517.
36. Loret, J. F., M. Jousset, S. Robert, C. Anselme, G. Saucedo, F. Ribas, A. Martinez, and V. Catalan. 2008. Elimination of free-living amoebae by drinking water treatment processes. Eur. J. Water Quality 39:37-50.
37. Marciano-Cabral, F., and G. Cabral. 2003. Acanthamoeba spp. as agents of disease in humans. Clin. Microbiol. Rev. 16:273-307.
38. Mazur, T., E. Hadas, and I. Iwanicka. 1995. The duration of the cyst stage and the viability and virulence of Acanthamoeba isolates. Trop. Med. Parasitol. 46:106-108.
39. Nagington, J., P. G. Watson, T. J. Playfair, J. McGill, B. R. Jones, and A. D. M. Steele. 1974. Amoebic infection of the eye. Lancet 304:1537-1540.
40. Neff, R. J., S. A. Ray, W. F. Benton, and M. Wilborn. 1964. Induction of synchronous encystation (differentiation) in Acanthamoeba spp., p. 55-83. In D. M. Prescott (ed.), Methods in cell physiology, vol. 1. Academic Press, New York, NY.
41. Pumidonming, W., M. Koehsler, and J. Walochnik. 2010. Acanthamoeba strains show reduced temperature tolerance after long-term axenic culture. Parasitol. Res. 106:553-559.
42. Rivera, F., P. Bonilla, E. Ramirez, A. Calderon, E. Gallegos, S. Rodriguez, R. Ortiz, D. Hernandez, and V. Rivera. 1994. Seasonal distribution of air-borne pathogenic and free-living amoebae in Mexico City and its suburbs. Water Air Soil Pollution 74:65-87. (Pubitemid 24406077)
43. Rodriguez-Zaragoza, S. 1994. Ecology of free-living amoebae. Crit. Rev. Microbiol. 20:225-241.
44. Rohr, U., S. Weber, R. Michel, F. Selenka, and M. Wilhelm. 1998. Comparison of free-living amoebae in hot water systems of hospitals with isolates from moist sanitary areas by identifying genera and determining temperature tolerance. Appl. Environ. Microbiol. 64:1822-1824.
45. Santos, L. C., M. S. Oliveira, R. D. Lobo, H. R. Higashino, S. F. Costa, I. M. van der Heijden, M. C. Giudice, A. R. Silva, and A. S. Levin. 2009. Acanthamoeba spp. in urine of critically ill patients. Emerg. Infect. Dis. 15:1144-1146.
46. Schroeder, J. M., G. C. Booton, J. Hay, I. A. Niszl, D. V. Seal, M. B. Markus, P. A. Fuerst, and T. J. Byers. 2001. Use of subgenic 18S ribosomal DNA PCR and sequencing for genus and genotype identification of acanthamoebae from humans with keratitis and from sewage sludge. J. Clin. Microbiol. 39:1903-1911.
47. Schroeder-Diedrich, J. M., P. A. Fuerst, and T. J. Byers. 1998. Group-I introns with unusual sequences occur at three sites in nuclear 18S rRNA genes of Acanthamoeba lenticulata. Curr. Genet. 34:71-78.
48. Reference deleted.
49. Sharbati-Tehrani, S., J. Stephan, G. Holland, B. Appel, M. Niederweis, and A. Lewin. 2005. Porins limit the intracellular persistence of Mycobacterium smegmatis. Microbiology 151:2403-2410. (Pubitemid 40984313)
50. Spanakos, G., K. Tzanetou, D. Miltsakakis, E. Patsoula, E. Malamou-Lada, and N. C. Vakalis. 2006. Genotyping of pathogenic acanthamoebae isolated from clinical samples in Greece - report of a clinical isolate presenting T5 genotype. Parasitol. Int. 55:147-149.
51. Sriram, R., M. Shoff, G. Booton, P. Fuerst, and G. S. Visvesvara. 2008. Survival of Acanthamoeba cysts after desiccation for more than 20 years. J. Clin. Microbiol. 46:4045-4048.
52. Storey, M. V., J. Winiecka-Krusnell, N. J. Ashbolt, and T. A. Stenstrom. 2004. The efficacy of heat and chlorine treatment against thermotolerant acanthamoebae and legionellae. Scand. J. Infect. Dis. 36:656-662.
53. Svetlikova, Z., H. Skovierova, M. Niederweis, J. L. Gaillard, G. McDonnell, and M. Jackson. 2009. The role of porins in the susceptibility of Mycobacterium smegmatis and Mycobacterium chelonae to aldehyde-based disinfectants and drugs. Antimicrob. Agents Chemother. 53:4015-4018.
54. Reference deleted.
55. Thomas, V., T. Bouchez, V. Nicolas, S. Robert, J. F. Loret, and Y. Lévi. 2004. Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence. J. Appl. Microbiol. 97:950-963.
56. Thomas, V., K. Herrera-Rimann, D. S. Blanc, and G. Greub. 2006. Biodiversity of amoebae and amoebae-resisting bacteria in a hospital water network. Appl. Environ. Microbiol. 72:2428-2438.
57. Thomas, V., J. F. Loret, M. Jousset, and G. Greub. 2008. Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ. Microbiol. 10:2728-2745.
58. Thomas, V., and G. McDonnell. 2007. Relationship between mycobacteria and amoebae: ecological and epidemiological concerns. Lett. Appl. Microbiol. 45:349-357.
59. Thomas, V., G. McDonnell, S. P. Denyer, and J. Y. Maillard. 2010. Freeliving amoebae and their intracellular pathogenic microorganisms: risks for water quality. FEMS Microbiol. Rev. 34:231-259.
60. Turner, N. A., A. D. Russell, J. R. Furr, and D. Lloyd. 2000. Emergence of resistance to biocides during differentiation of Acanthamoeba castellanii. J. Antimicrob. Chemother. 46:27-34.
61. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
62. Wilson, J., and A. B. Margolin. 2003. Efficacy of glutaraldehyde disinfectant against Cryptosporidium parvum in the presence of various organic soils. J. AOAC Int. 86:96-100.
63. Wilson, J. A., and A. B. Margolin. 1999. The efficacy of three common hospital liquid germicides to inactivate Cryptosporidium parvum oocysts. J. Hosp. Infect. 42:231-237.