1887

Journal of Medical Microbiology logo

Volume 47, Issue 1

Isolation, Identification and Increasing Importance of ‘Free-Living’ Amoebae Causing Human Disease Free

Abstract

Amphizoic small amoebic protozoa are capable of existing both in ‘free-living’ and in ‘parasitic’ form depending on the actual conditions. Two genera ( and ) have become recognised as opportunist human parasites. Since the first description in 1965 of a lethal case of primary amoebic meningoencephalitis (PAM) caused by , many more (mostly lethal) cases have been reported, while granulomatous amoebic encephalitis (GAE), as well as eye (keratinitis, conjunctivitis, etc.), ear, nose, skin and internal organ infections caused by have also occurred in rapidly increasing numbers. Both pathogenic and non-pathogenic species of and are found worldwide in water, soil and dust, where they provide a potential source of infection. Successful differential diagnosis and appropriate (specific) therapy depends on precise laboratory identification of the ‘free-living’ amoebae. In most cases, isolation from the environment can be achieved, but identification and differentiation of the pathogenic and non-pathogenic strains is not easy. The methods presently available do not fulfil completely the requirements for specificity, sensitivity and reliability. Morphological criteria are inadequate, while thermophilic character, pH dependency and even virulence in infected mice, are not unambiguous features of pathogenicity of the different strains. More promising are molecular methods, such as restriction endonuclease digestion of whole-cell DNA or mitochondrial DNA, as well as iso-enzyme profile analysis after iso-electric focusing and staining for acid phosphatase and propionyl esterase activity. Use of appropriate monoclonal antibodies has also yielded promising results in the differentiation of human pathogenic and non-pathogenic strains. However, quicker, simpler, more specific and reliable methods are still highly desirable. The significance of endosymbiosis (especially with strains) is not well understood. The results of a systematic survey in Hungary for the isolation and identification of ‘free-living’ amoebae, including an investigation of the Hungarian amoebic fauna, the isolation of possibly pathogenic strains and of some strains from eye diseases, as well as the finding of a case of endosymbiosis, are also reported here.

  • Received:
  • Accepted:
  • Published Online:
© 1998 The Pathological Society of Great Britain and Ireland
Loading

Article metrics loading...

/content/journal/jmm/10.1099/00222615-47-1-5
1998-01-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/47/1/medmicro-47-1-5.html?itemId=/content/journal/jmm/10.1099/00222615-47-1-5&mimeType=html&fmt=ahah

References

  1. Page F. C. Rosculus ithacus Hawes, 1963 (Amoebida, Flabel-luidae) and the amphizoic tendency in amoebae. Acta Protozool 1974; 13:143–154
     [Google Scholar]
  2. Daggett P. M., Sawyer T. K., Nerad T. A. Distribution and possible interrelationships of pathogenic and nonpathogenic Acanthamoeba from aquatic environments. Microb Ecol 1982; 8:371–386
     [Google Scholar]
  3. Stevens A. R., Tyndall R. L., Coutant C. C., Willaert E. Isolation of the etiological agent of primary amoebic meningoencephalitis from artificially heated waters. Appl Environ Microbiol 1977; 34:701–705
     [Google Scholar]
  4. Sison J. P., Kemper C. A., Loveless M., McShane D., Visvesvara G. S., Deresinksi S. C. Disseminated Acanthamoeba infection in patients with AIDS: case reports and review. Clin Infect Dis 1995; 20:1207–1216
     [Google Scholar]
  5. Kilvington S., Larkin D. F. P., White D. G., Beeching J. R. Laboratory investigation of Acanthamoeba keratitis. J Clin Microbiol 1990; 28:2722–2725
     [Google Scholar]
  6. Szénási Z., Endo T., Yagita K., Urbán E., Végh M., Nagy E. Isolation and restriction enzyme analysis of mitochondrial DNA (mtDNA) of Hungarian Acanthamoeba isolates from human eye infection and from the environment. Parasitol Hung 1995; 28:5–12
     [Google Scholar]
  7. Végh M., Nagy E., Matyi A. Homhautulkus bei weichen Kontaktlinsen. Contactologia 1988; 4:194–195
     [Google Scholar]
  8. Illingworth C. D., Cook S. D., Karabatsas C. H., Easty D. L. Acanthamoeba keratitis: risk factors and outcome. Br J Ophthalmol 1995; 79:1078–1082
     [Google Scholar]
  9. D’Aversa G., Stem G. A., Driebe W. T. Diagnosis and successful medical treatment of Acanthamoeba keratitis. Arch Ophthalmol 1995; 113:1120–1123
     [Google Scholar]
  10. Radford C. F., Bacon A. S., Dart J. K. G., Minassian D. C. Risk factors for acanthamoeba keratitis in contact lens users: a case-control study. B M J 1995; 310:1567–1570
     [Google Scholar]
  11. Chatteijee A., Kwartz J., Ridgway A. E. A., Storey J. K. Disposable soft contact lens ulcers: a study of 43 cases seen at Manchester Royal Eye Hospital. Cornea 1995; 14:138–141
     [Google Scholar]
  12. Bacon A. S., Frazer D. G., Dart J. K. G., Matheson M., Ficker L. A., Wright P. A review of 72 consecutive cases of Acanthamoeba keratitis, 1984-1992. Eye 1993; 7:719–725
     [Google Scholar]
  13. Gray T. B., Cursons R. T. M., Sherwan J. F., Rose P. R. Acanthamoeba, bacterial, and fungal contamination of contact lens storage cases. Br J Ophthalmol 1995; 79:601–605
     [Google Scholar]
  14. Matyi A., Somogyi I., Deák J., Nagy E., Földes J. Acanthamoeba castellanii által okozott meningoencephalitis magyar-orszagi elöfordulása (Meningoencephalitis caused by Acanthamoeba castellanii in Hungary). Orv Hetil 1985; 126:2541–2544
     [Google Scholar]
  15. Larkin D. F. P., Easty D. L. External eye flora as a nutrient source for Acanthamoeba. Graefes Arch Clin Exp Ophthalmol 1990; 228:458–460
     [Google Scholar]
  16. Sykora J. L., Keleti G., Martinez A. J. Occurrence and pathogenicity of Naegleria fowleri in artifically heated waters. Appl Environ Microbiol 1983; 45:974–979
     [Google Scholar]
  17. De Jonckheere J. F., Yagita K., Endo T. Restriction-fragment-length polymorphism and variation in electrophoretic karyotype in Naegleria fowleri from Japan. Parasitol Res 1992; 78:475–478
     [Google Scholar]
  18. De Jonckheere J. F. Geographic origin and spread of pathogenic Naegleria fowleri deduced from restriction enzyme patterns of repeated DNA. Biosystems 1988; 21:269–275
     [Google Scholar]
  19. De Jonckheere J. F., Yagita K., Kuroki T., Endo T. First isolation of pathogenic Naegleria fowleri in Japan. Jpn J Parasitol 1991; 40:352–357
     [Google Scholar]
  20. Sparagano O., Drouet E., Brebant R., Manet E., Denoyel G. A., Pemin P. Use of monoclonal antibodies to distinguish pathogenic Naegleria fowleri (cysts, trophozoites, or flagellate forms) from other Naegleria species. J Clin Microbiol 1993; 31:2758–2763
     [Google Scholar]
  21. Yagita K., Endo T. Restriction enzyme analysis of mitochondrial DNA of Acanthamoeba strains in Japan. J Protozool 1990; 37:570–575
     [Google Scholar]
  22. Gautom R. K., Lory S., Seyedirashti S., Bergeron D., Fritsche T. Mitochondrial DNA fingerprinting of Acanthamoeba spp. isolated from clinical and environmental sources. J Clin Microbiol 1994; 32:1070–1073
     [Google Scholar]
  23. Badenoch P. R., Adams M., Coster D. J. Comeal vimlence, cytopathic effect on human keratocytes and genetic characterization of Acanthamoeba. Int J Parasitol 1995; 25:229–239
     [Google Scholar]
  24. Bogler S. A., Zarley C. D., Burianek L. L., Fuerst P. A., Byers T. J. Interstrain mitochondrial DNA polymorphism detected in Acanthamoeba by restriction endonuclease analysis. Mol Biochem Parasitol 1983; 8:145–163
     [Google Scholar]
  25. Byers T. J., Bogler S. A., Burianek L. L. Analysis of mitchondrial DNA variation as an approach to systematic relationships in the genus Acanthamoeba. J Protozool 1983; 30:198–203
     [Google Scholar]
  26. Byers T. J., Hugo E. R., Stewart V. J. Genes of Acanthamoeba: DNA, RNA and protein sequences (a review). J Protozool 1990; 37:17s–25s
     [Google Scholar]
  27. Urbán E., Szénási Z., Vegh M., Endo T., Yagita K., Nagy E. Isolation of Acanthamoeba spp from human sample and from the environment. Clin Exp Lab Med 1995; 22:248–252
     [Google Scholar]
  28. Martinez A. J. (ed) Free-living amebas: natural history, prevention, diagnosis, pathology, and treatment of disease. Boca Raton: CRC Press; 1985
     [Google Scholar]
  29. Huizinga H. W., McLaughlin G. L. Thermal ecology of Naegleria fowleri from a power plant cooling reservoir. Appl Environ Microbiol 1990; 56:2200–2205
     [Google Scholar]
  30. Martinez A. J., Guerra A. E., Garcia-Tamayo J., Cespedes G., Gonzalez Alfonzo J. E., Visvesvara G. S. Granulomatous amebic encephalitis: a review and report of a spontaneous case from Venezuela. Acta Neuropathol 1994; 87:430–434
     [Google Scholar]
  31. Flores B. M., Garcia C. A., Stamm W. E., Torian B. E. Differentiation of Naegleria fowled from Acanthamoeba species by using monoclonal antibodies and flow cytometry. J Clin Microbiol 1990; 28:1999–2005
     [Google Scholar]
  32. Fowler M., Carter R. E Acute pyogenic meningitis probably due to Acanthamoeba sp.: a preliminary report. B M J 1965; 2:740–742
     [Google Scholar]
  33. Tyndall R. L., Ironside K. S., Metier P. L., Tan E. L., Flazen T. C., Eliermans C. B. Effect of thermal additions on the density and distribution of thermophilic amoebae and pathogenic Naegleria fowled in a newly created cooling lake. Appl Environ Microbiol 1989; 55:722–732
     [Google Scholar]
  34. Griffin J. L. Temperature tolerance of pathogenic and nonpathogenic free-living amoebas. Science 1972; 178:869–870
     [Google Scholar]
  35. De Jonckheere J., Voorde H. The distribution of Naegleria fowled in man-made thermal waters. Am J Trop Med Hyg 1977; 26:10–15
     [Google Scholar]
  36. Duma R. J. (ed) Study of pathogenic free-living amebas in fresh-water lakes in Virginia. US Environmental Protection Agency Publication No. EPA-600/S1-80-0-037. Washington, DC: Environmental Protection Agency; 1980
     [Google Scholar]
  37. Fliermans C. B., Tyndall R. L., Domingue E. L., Willaert E. J. P. Isolation of Naegleria fowled from artificially heated waters. J Therm Biol 1979; 4:303–305
     [Google Scholar]
  38. Wellings F. M., Amuso P. T., Chang S. L., Lewis A. L. Isolation and identification of pathogenic Naegleria from Florida lakes. Appl Environ Microbiol 1977; 34:661–667
     [Google Scholar]
  39. De Jonckheere J., Van Dijck P., van de Voorde H. The effect of the thermal pollution on the distribution of Naegleria fowled. J Hyg 1975; 75:7–13
     [Google Scholar]
  40. Shapiro M. A., Karol M. H., Keleti G., Sykora J. L., Martinez A. J. The role of free living amoebae occurring in heated effluents as causative agents of human disease. In Proceedings of International Conference on Coal Fired Power Plants and Aquatic Environment Copenhagen: Water Quality Institute; 198299–111
     [Google Scholar]
  41. Wellings F. M., Amuso P. T., Lewis A. L. Pathogenic Naegleria, distribution in nature. Report No. EPA-600/1-79-018 Cincinnati: US Environmental Protection Agency; 1979
     [Google Scholar]
  42. Rondanelli E. G. (ed) Infectious diseases 1. Amphizoic amoebae human pathology. Padua: Piccin Nuova Libraria; 1987
     [Google Scholar]
  43. De Jonckheere J. F. Characterization of Naegleria species by restriction endonuclease digestion of whole-cell DNA. Mol Biochem Parasitol 1987; 24:55–66
     [Google Scholar]
  44. McLaughlin G. L., Brandt F. H., Visvesvara G. S. Restriction fragment length polymorphisms of the DNA of selected Naegleria and Acanthamoeba amoebae. J Clin Microbiol 1988; 26:1655–1658
     [Google Scholar]
  45. De Jonckheere J. F. Isoenzyme patterns of pathogenic and nonpathogenic Naegleria spp. using agarose isoelectric focusing. Ann Microbiol 1982; 133:319–342
     [Google Scholar]
  46. Visvesvara G. S., Peralta M. J., Brandt F. H., Wilson M., Aloisio C., Franko E. Production of monoclonal antibodies to Naegleria fowled, agent of primary amebic meningoencephalitis. J Clin Microbiol 1987; 25:1629–1634
     [Google Scholar]
  47. Sawyer T. K., Visvesvara G. S., Harke B. A. Pathogenic amoebas from brackish and ocean sediments, with a description of Acanthamoeba hatchetti, n. sp. Science 1977; 196:1324–1325
     [Google Scholar]
  48. Brown T. J., Cursons R. T. M., Keys F. A. Amoebae from antarctic soil and water. Appl Environ Microbiol 1982; 44:491–493
     [Google Scholar]
  49. Franke E. D., Mackiewicz J. S. Isolation of Acanthamoeba and Naegleria from the intestinal contents of freshwater fishes and their potential pathogenicity. J Parasitol 1982; 68:164–166
     [Google Scholar]
  50. Kyle D. E., Noblet G. P. Seasonal distribution of thermotolerant free-living amoebae. I. Willard’s Pond. J Protozool 1986; 33:422–434
     [Google Scholar]
  51. Wiens J. J., Jackson W. B. Acanthamoeba keratitis: an update. Can J Ophthalmol 1988; 23:107–110
     [Google Scholar]
  52. Hseih W. C., Domic D. I. Acanthamoeba dendriform keratitis. J Am Optom Assoc 1989; 60:32–34
     [Google Scholar]
  53. Rivasi F., Longanesi L., Casolari C. Cytologic diagnosis of Acanthamoeba keratitis. Report of a case with correlative study with indirect immunofluorescence and scanning electron microscopy. Acta Cytol 1995; 39:821–826
     [Google Scholar]
  54. Stehr-Green J. K., Bailey T. M., Visvesvara G. S. The epidemiology of Acanthamoeba keratitis in the United States. Am J Ophthalmol 1989; 107:331–336
     [Google Scholar]
  55. Berger S. T., Mondino B. J., Hoft R. H. Successful medical management of Acanthamoeba keratitis. Am J Ophthalmol 1990; 110:395–403
     [Google Scholar]
  56. Driebe W. T., Stem G. A., Epstein R. J., Visvesvara G. S., Adi M., Komadina T. Acanthamoebic keratitis. Potential role for topical clotrimazole in combination chemotherapy. Arch Ophthalmol 1988; 106:1196–1201
     [Google Scholar]
  57. Fritsche T. R., Gautom R. K., Seyedirashti S., Bergeron D. L., Lindquist T. D. Occurrence of bacterial endosymbionts in Acanthamoeba spp. isolated from comeal and environmental specimens and contact lenses. J Clin Microbiol 1993; 31:1122–1126
     [Google Scholar]
  58. Matias R., Schottelius J., Raddatz C. F., Michel R. Species identification and characterization of an Acanthamoeba strain from human cornea. Parasitol Res 1991; 77:469–474
     [Google Scholar]
  59. Kilvington S., Beeching J. R., White D. G. Differentiation of Acanthamoeba strains from infected corneas and the environment by using restriction endonuclease digestion of wholecell DNA. J Clin Microbiol 1991; 29:310–314
     [Google Scholar]
  60. Van Klink F., Taylor W. M., Alizadeh H., Jager M. J., van Rooijen N., Niederkom J. Y. The role of macrophages in Acanthamoeba keratitis. Invest Ophthalmol Vis Sci 1996; 37:1271–1281
     [Google Scholar]
  61. Clinch T. E., Palmon F. E., Robinson M. J., Cohen E. J., Barron B. A., Laibson P. R. Microbial keratitis in children. Am J Ophthalmol 1994; 117:65–71
     [Google Scholar]
  62. Ficker L. A., Kirkness C., Wright P. Prognosis for keratoplasty in Acanthamoeba keratitis. Ophthalmology 1993; 100:105–110
     [Google Scholar]
  63. Cerva L. Amebic meningoencephalitis. In Braude A. (ed) Medical microbiology and infectious diseases Philadelphia: Saunders; 19811281
     [Google Scholar]
  64. Rivera F., Medina F., Ramerez P., Alcocer J., Vilaclara G., Robles E. Pathogenic and free-living protozoa cultured from the nasopharyngeal and oral regions of dental patients. Environ Res 1984; 33:428–440
     [Google Scholar]
  65. Lindquist T. D., Sher N. A., Doughman D. J. Clinical signs and medical therapy of early Acanthamoeba keratitis. Arch Ophthalmol 1988; 106:73–77
     [Google Scholar]
  66. Brandt F. H., Ware D. A., Visvesvara G. S. Viability of Acanthamoeba cysts in ophthalmic solution. Appl Environ Microbiol 1989; 55:1144–1146
     [Google Scholar]
  67. De Jonckheere J. F. Use of an axenic medium for differentiation between pathogenic and nonpathogenic Naegleria fowled isolates. Appl Environ Microbiol 1977; 33:751–757
     [Google Scholar]
  68. Anzil A. P., Rao C., Wrzolek M. A., Visvesvara G. S., Sher J. H., Kozlowski P. B. Amebic meningoencephalitis in a patient with AIDS caused by a newly recognized opportunistic pathogen, Leptomyxid ameba. Arch Pathol Lab Med 1991; 115:21–25
     [Google Scholar]
  69. Griffin J. L. The pathogenic amoeboflagellate Naegleria fowled: environmental isolations, competitors, ecological interactions, and the flagellate-empty habitat hypothesis. J Protozool 1983; 30:403–409
     [Google Scholar]
  70. Sykora J. L., Keleti G., Martinez A. J. Occurrence and pathogenicity of Naegleria fowled in artificially heated waters. Appl Environ Microbiol 1983; 45:974–979
     [Google Scholar]
  71. Costas M., Edwards S. W., Lloyd D., Griffiths A. J., Turner G. Restriction enzyme analysis of mitochondrial DNA of members of the genus Acanthamoeba as an aid in taxonomy. FEMS Microbiol Lett 1983; 17:231–234
     [Google Scholar]
  72. Brown G. G., Simpson M. V Intra-and interspecific variation of the mitochondrial genome in Rattus norvegicus and Rattus rattus: restriction enzyme analysis of variant mitochondrial DNA molecules and their evolutionary relationships. Genetics 1981; 97:125–143
     [Google Scholar]
  73. Yonekawa H., Moriwaki K., Gotoh O. Evolutionary relationships among five subspecies of Mus musculus based on restriction enzyme cleavage patterns of mitochondrial DNA. Genetics 1981; 98:801–816
     [Google Scholar]
  74. Uberlaker J. E. Acanthamoeba spp: “opportunistic pathogens.”. Trans Am Microsc Soc 1991; 110:289–299
     [Google Scholar]
  75. Visvesvara G. S. Classification of Acanthamoeba. Rev Infect Dis 1991; 13: Suppl 5S369–S372
     [Google Scholar]
  76. Page F. C. (ed) A new key to freshwater and soil gymnamoebae: with instructions for culture. Ambleside: Freshwater Biological Association; 1988
     [Google Scholar]
  77. Bogler S. A., Zarley C. D., Burianek L. L., Fuerst P. A., Byers T. J. Interstrain mitochondrial DNA polymorphism detected in Acanthamoeba by restriction endonuclease analysis. Mol Biochem Parasitol 1983; 8:145–163
     [Google Scholar]
  78. Pussard M., Pons R. Morphologie de la paroi kystique et taxonomie du genre Acanthamoeba (Protozoa, Amoebida). Protistologica 1977; 13:557–598
     [Google Scholar]
  79. Stevens A. R., O’Dell W. D. In vitro growth and virulence of Acanthamoeba. J Parasitol 1974; 60:884–885
     [Google Scholar]
  80. De Jonckheere J. F. Growth characteristics, cytopathic effect in cell culture, and virulence in mice of 36 type strains belonging to 19 different Acanthamoeba spp. Appl Environ Microbiol 1980; 39:681–685
     [Google Scholar]
  81. Byers T. J., Bogler S. A., Burianek L. L. Analysis of mitochondrial DNA variation as an approach to systematic relationships in the genus Acanthamoeba. J Protozool 1983; 30:198–203
     [Google Scholar]
  82. Wilson A. C., Cann R. L., Carr S. M. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 1985; 26:375–400
     [Google Scholar]
  83. Fort P., Darlu P., Piechaczyk M., Jeanteur P., Thaler L. Clonal divergence of mitochondrial DNA versus populational evolution of nuclear genome. Evol Theory 1984; 7:81–90
     [Google Scholar]
  84. Taylor J. W., Natvig D. O. Mitochondrial DNA and evolution of heterothallic and pseudohomothallic Neurospora species. Mycol Res 1989; 93:257–272
     [Google Scholar]
  85. Kong H. H., Park J. H., Chung D. I. Interstrain polymorphisms of isoenzyme profiles and mitochondrial DNA fingerprints among seven strains assigned to Acanthamoeba polyphaga. Korean J Parasitol 1995; 33:331–340
     [Google Scholar]
  86. Daggett P. M., Lipscomb D., Sawyer T. K., Nerad T. A. A molecular approach to the phylogeny of Acanthamoeba. Biosystems 1985; 18:399–405
     [Google Scholar]
  87. Hall J., Voelz H. Bacterial endosymbionts of Acanthamoeba sp. J Parasitol 1985; 71:89–95
     [Google Scholar]
  88. Drozanski W. J. Sarcobium lyticum gen. nov., sp. nov., an obligate intracellular bacterial parasite of small free-living amoebae. Int J Syst Bacteriol 1991; 41:82–87
     [Google Scholar]
  89. Gautom R. K., Fritsche T. R. Transmissibility of bacterial endosymbionts between isolates of Acanthamoeba spp. J Eukaryot Microbiol 1995; 42:452–456
     [Google Scholar]
  90. Michel R., Hauroder-Philippczyk B., Muller K. D., Weishaar I. Acanthamoeba from human mucosa infected with an obligate intracellular parasite. Eur J Protistol 1994; 30:104–110
     [Google Scholar]
  91. Yagita K., Matias R. R., Yasuda T., Natividad F. F., Enriquez G. L., Endo T. Acanthamoeba sp. from the Philippines: electron microscopy studies on naturally occurring bacterial symbionts. Parasitol Res 1995; 81:98–102
     [Google Scholar]
  92. Rowbotham T. J. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 1980; 33:1179–1183
     [Google Scholar]
  93. Bozue J. A., Johnson W. Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect Immun 1996; 64:668–673
     [Google Scholar]
  94. Fields B. S. Legionella and protozoa: interaction of a pathogen and its natural host. In Barbaree J. M., Breiman R. F., Dufour A. P. (eds) Legionella current status and emerging perspectives Washington DC: American Society for Microbiology; 1993129
     [Google Scholar]
  95. Fields B. S., Sanden G. N., Barbaree J. M. Intracellular multiplication of Legionella pneumophila in amoebae isolated from hospital hot water baths. Curr Microbiol 1989; 18:131–137
     [Google Scholar]
  96. Hay J., Seal D. V., Billcliffe B., Freer J. H. Non-culturable Legionella pneumophila associated with Acanthamoeba castellanii: detection of the bacterium using DNA amplification and hybridization. J Appl Bacteriol 1995; 78:61–65
     [Google Scholar]
  97. Dowling J. N., Saha A. K., Glew R. H. Virulence factors of the family Legionellaceae. Microbiol Rev 1992; 56:32–60
     [Google Scholar]
  98. Connor R., Hay J., Mead A. J. C., Seal D. V. Reversal of inhibitory effects of Acanthamoeba castellani lysate for Legionella pneumophila using catalase. J Microbiol Methods 1993; 18:311–316
     [Google Scholar]
  99. Hay J., Seal D. V. Surveying for legionnaires’ disease bacterium. Curr Opin Infect Dis 1994; 7:479–483
     [Google Scholar]
  100. Hay J., Seal D. V. Monitoring of hospital water supplies for Legionella. J Hosp Infect 1994; 26:75–78
     [Google Scholar]
  101. Culbertson C. G., Holmes D. H., Overton W. M. Hartmannella castellani (Acanthamoeba sp): preliminary report on experimental chemotherapy. Am J Clin Pathol 1965; 43:361–364
     [Google Scholar]
  102. Culbertson C. G., Ensminger P. W., Overton W. M. Hartmannella (Acanthamoeba). Experimental chronic, granulomatous brain infections produced by new isolates of low virulence. Am J Clin Pathol 1966; 46:305–314
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/00222615-47-1-5
Loading
Isolation, Identification and Increasing Importance of ‘Free-Living’ Amoebae Causing Human Disease
J. Med. Microbiol. 47, 5 (1998); https://doi.org/10.1099/00222615-47-1-5
/content/journal/jmm/10.1099/00222615-47-1-5
/content/journal/jmm/10.1099/00222615-47-1-5
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error