A microscopic description and ultrastructural characterisation of Dientamoeba fragilis: An emerging cause of human enteric disease

International Journal for Parasitology

Volumn 42, Issue 2, 2012, Pages 139-153

  Banik, Gouri R ^a,b   Birch, Debra ^c   Stark, Damien ^a,b   Ellis, John T ^b  

^a ST VINCENT S HOSPITAL   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

Dientamoeba fragilis; Dientamoebiasis; Electron microscopy; Trichomonad; Ultrastructure; Virus like particle

Indexed keywords

DIARRHEAL DISEASE; DNA; ENDOPARASITE; GASTROENTERITIS; MORPHOLOGY; PROTOZOAN; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRUS PARTICLE;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL NUCLEUS; CELL SHAPE; CELL SIZE; CELL SURFACE; CELL ULTRASTRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENTAL STAGE; DIENTAMOEBA; DNA DETERMINATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; LYSOSOME; MICROSCOPY; MONONUCLEAR CELL; NONHUMAN; PARASITE DEVELOPMENT; PARASITE ISOLATION; PHAGOCYTOSIS; POPULATION ABUNDANCE; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; VIRUS PARTICLE;

CYTOPLASM; DIARRHEA; DIENTAMOEBA; DIENTAMOEBIASIS; GASTROENTERITIS; HUMANS; MICROSCOPY; ORGANELLES; VIROSOMES;

DIENTAMOEBA FRAGILIS; HISTOMONAS; PROTOZOA; TRICHOMONADIDA; TRICHOMONAS;

EID: 84856462159     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2011.10.010     Document Type: Article

References (91)

1. Abraham R., Honigberg B.M. Structure of Trichomonas gallinae (Rivolta). J. Parasitol. 1964, 50:608-619.
2. Adam R.D. Biology of Giardia lamblia. Clin. Microbiol. Rev. 2001, 14:447-475.
3. Alderete J.F., Garza G.E. Identification and properties of Trichomonas vaginalis proteins involved in cytadherence. Infect. Immun. 1988, 56:28-33.
4. Arroyo R., Engbring J., Alderete J.F. Molecular basis of host epithelial cell recognition by Trichomonas vaginalis. Mol. Microbiol. 1992, 6:853-862.
5. Barratt J.L., Banik G.R., Harkness J., Marriott D., Ellis J.T., Stark D. Newly defined conditions for the in vitro cultivation and cryopreservation of Dientamoeba fragilis: new techniques set to fast track molecular studies on this organism. Parasitology 2010, 137:1867-1878.
6. Barratt J.L.N., Harkness J., Marriott D., Ellis J.T., Stark D. A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microb. 2011, 2:3-12.
7. Barratt J.L., Harkness J., Marriott D., Ellis J.T., Stark D. The ambiguous life of Dientamoeba fragilis: the need to investigate current hypotheses on transmission. Parasitology 2011, 138:557-572.
8. Benchimol M., D Souza W. Fine structure and cytochemistry of the hydrogenosome of Tritrichomonas foetus. J. Protozool. 1983, 30:422-425.
9. Benchimol M., Kachar B., de Souza W. The structural organization of the pathogenic protozoan Tritrichomonas foetus as seen in replicas of quick frozen, freeze-fractured and deep etched cells. Biol. Cell. 1993, 77:289-295.
10. Benchimol M., Almeida J.C., de Souza W. Further studies on the organization of the hydrogenosome in Tritrichomonas foetus. Tissue Cell. 1996, 28:287-299.
11. Benchimol M., Leal D., Mattos A., Diniz J.A.P. Fine structure of Trichomonas gallinae. Biocell. 1997, 21:47-58.
12. Benchimol M. Ultrastructural characterization of the isolated hydrogenosome in Tritrichomonas foetus. Tissue Cell. 2000, 32:518-526.
13. Benchimol M., Monteiro S., Chang T.H., Alderete J.F. Virus in Trichomonas - an ultrastructural study. Parasitol. Int. 2002, 51:293-298.
14. Benchimol M., Engelke F. Hydrogenosome behavior during the cell cycle in Tritrichomonas foetus. Biol Cell. 2003, 95:283-293.
15. Benchimol M. Trichomonads under microscopy. Microsc. Microanal. 2004, 10:528-550.
16. Benchimol M. Mitosis in Giardia lamblia: multiple modes of cytokinesis. Protist. 2004, 155:33-44.
17. Benchimol M. Hydrogenosomes under microscopy. Tissue Cell. 2009, 41:151-168.
18. Borges F.P., Gottardi B., Stuepp C., Larré A.B., de Brum Vieira P., Tasca T., De Carli G.A. Morphological aspects of Monocercomonas sp. and investigation on probable pseudocysts occurrence. Parasitol. Res. 2007, 101:1503-1509.
19. Borges F.P., Wiltuschnig R.C., Tasca T., De Carli G.A. Scanning electron microscopy study of Tritrichomonas augusta. Parasitol. Res. 2004, 94:158-161.
20. Camp R.R., Mattern C.F., Honigberg B.M. Study of Dientamoeba fragilis Jepps & Dobell. I. Electronmicroscopic observations of the binucleate stages. II. Taxonomic position and revision of the genus. J. Protozool. 1974, 21:69-82.
21. Carlton J.M., Hirt R.P., Silva J.C., Delcher A.L., Schatz M., Zhao Q., Wortman J.R., Bidwell S.L., Alsmark U.C.M., Besteiro S.b., Sicheritz-Ponten T., Noel C.J., Dacks J.B., Foster P.G., Simillion C., Van de Peer Y., Miranda-Saavedra D., Barton G.J., Westrop G.D., Müller S., Dessi D., Fiori P.L., Ren Q., Paulsen I., Zhang H., Bastida-Corcuera F.D., Simoes-Barbosa A., Brown M.T., Hayes R.D., Mukherjee M., Okumura C.Y., Schneider R., Smith A.J., Vanacova S., Villalvazo M., Haas B.J., Pertea M., Feldblyum T.V., Utterback T.R., Shu C.-L., Osoegawa K., de Jong P.J., Hrdy I., Horvathova L., Zubacova Z., Dolezal P., Malik S.-B., Logsdon J.M., Henze K., Gupta A., Wang C.C., Dunne R.L., Upcroft J.A., Upcroft P., White O., Salzberg S.L., Tang P., Chiu C.-H., Lee Y.-S., Embley T.M., Coombs G.H., Mottram J.C., Tachezy J., Fraser-Liggett C.M., Johnson P.J. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212.
22. Cepicka I., Hampl V., Kulda J. Critical taxonomic revision of Parabasalids with description of one new genus and three new species. Protist. 2010, 161:400-433.
23. Cerva L., Nohýnková E. A light microscopic study of the course of cellular division of Giardia intestinalis trophozoites grown in vitro. Folia. Parasitol. 1992, 39:97-104.
24. Chen W., Chen J., Zhong X., Lin X., Chen L. Electron microscopic study on Trichomonas vaginalis adhering to and phagocytizing male genitourinary epithelial cells. Zhonghua Nan Ke Xue 2004, 10:86-89.
25. Craig C.F. The nuclear structure of Dientamoeba fragilis. J. Parasitol. 1926, 13:137-140.
26. Delgado-Viscogliosi P., Viscogliosi E., Gerbod D., Kulda J., Sogin M.L., Edgcomb V.P. Molecular phylogeny of parabasalids based on small subunit rRNA sequences, with emphasis on the Trichomonadinae subfamily. J. Eukaryot. Microbiol. 2000, 47:70-75.
27. Dobell C. Researches on the intestinal protozoa of monkeys and man. X. The life history of Dientamoeba fragilis: observations, experiments and speculations. Parasitology 1940, 32:417-461.
28. Ellis J., Revets H. Eimeria species which infect the chicken contain virus-like RNA molecules. Parasitology 1990, 101:163-169.
29. Fraga J., Rojas L., Sariego I., Fernández-Calienes A. Double-stranded RNA viral infection of Trichomonas vaginalis and correlation with genetic polymorphism of isolates. Exp. Parasitol. 2011, 127:593-599.
30. Gerbod D., Edgcomb V.P., Noël C., Zenner L., Wintjens R., Delgado-Viscogliosi P., Holder M.E., Sogin M.L., Viscogliosi E. Phylogenetic position of the trichomonad parasite of turkeys, Histomonas meleagridis (Smith) Tyzzer, inferred from small subunit rRNA sequence. J. Eukaryot. Microbiol. 2001, 48:498-504.
31. Gerbod D., Noël C., Dolan M.F., Edgcomb V.P., Kitade O., Noda S., Dufernez F., Ohkuma M., Kudo T., Capron M., Sogin M.L., Viscogliosi E. Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Devescovinidae and Calonymphidae (Trichomonadea). Mol. Phylogenet. Evol. 2002, 25:545-556.
32. Gerhold R.W., Allison A.B., Sellers H., Linnemann E., Chang T.H., Alderete J.F. Examination for double-stranded RNA viruses in Trichomonas gallinae and identification of a novel sequence of a Trichomonas vaginalis virus. Parasitol. Res. 2009, 105:775-779.
33. Granger B.L., Warwood S.J., Benchimol M., De Souza W. Transient invagination of flagella by Tritrichomonas foetus. Parasitol. Res. 2000, 86:699-709.
34. Honigberg B.M., Bennett C.J. Lightmicroscopic observations on structure and division of Histomonas meleagridis (Smith). J. Protozool. 1971, 18:687-697.
35. Honigberg B.M., Daniel W.A., Mattern C.F. Fine Structure of Trichomitus batrachorum (Perty). J. Protozool. 1972, 19:446-453.
36. Honigberg B.M. Trichomonads of veterinary importance. Parasitic Protozoa 1978, 163-273. Academic Press, New York. J.P. Kreier (Ed.).
37. Jahn C.L., Klobutcher L.A. Genome remodeling in ciliated protozoa. Annu. Rev. Microbiol. 2002, 56:489-520.
38. Jepps M.W., Dobell C. Dientamoeba fragilis n.g., n. sp., new intestinal amoeba from man. Parasitology 1918, 10:352-367.
39. Jhingan G.D., Panigrahi S.K., Bhattacharya A., Bhattacharya S. The nucleolus in Entamoeba histolytica and Entamoeba invadens is located at the nuclear periphery. Mol. Biochem. Parasitol. 2009, 167:72-80.
40. Johnson E.H., Windsor J.J., Clark C.G. Emerging from obscurity: biological, clinical, and diagnostic aspects of Dientamoeba fragilis. Clin. Microbiol. Rev. 2004, 17:553-570.
41. Kabnick K.S., Peattie D.A. In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. J. Cell. Sci. 1990, 95:353-360.
42. Kasprzak W., Majewska A.C. Viruses of parasitic protozoa. Wiad Parazytol. 1995, 41:131-137.
43. Kietzmann G.E. Relationships of Trichomonas gallinae to the palatal-esophageal junction of ring doves (Streptopelia risoria) as revealed by scanning electron microscopy. J. Parasitol. 1993, 79:408-415.
44. Kurnatowska A., Hajdukiewicz G. Trichomonas vaginalis variability in axenic cultures evaluated in scanning electron microscope. Wiad. Parazytol 1977, 23:481-487.
45. Ludvík J., Shipstone A.C. The ultrastructure of Entamoeba histolytica. Bull. World Health Organ. 1970, 43:301-308.
46. Malla N., Kaul P., Sehgal R., Gupta I. The presence of dsRNA virus in Trichomonas vaginalis isolates from symptomatic and asymptomatic Indian women and its correlation with in vitro metronidazole sensitivity. Indian J. Med. Microbiol. 2011, 29:152-157.
47. Mattern C.F., Honigberg B.M., Daniel W.A. The mastigont system of Trichomonas gallinae (Rivolta) as revealed by electron microscopy. J. Protozool. 1967, 14:320-339.
48. Mehlhorn H., Al-Quraishy S., Aziza A., Hess M. Fine structure of the bird parasites Trichomonas gallinae and Tetratrichomonas gallinarum from cultures. Parasitol. Res. 2009, 105:751-756.
49. Mielewczik M., Mehlhorn H., Al-Quraishy S., Grabensteiner E., Hess M. Transmission electron microscopic studies of stages of Histomonas meleagridis from clonal cultures. Parasitol. Res. 2008, 103:745-750.
50. Moody A.H., Fleck S.L. Versatile Field's stain. J. Clin. Pathol. 1985, 38:842-843.
51. Müller M. Biochemistry of protozoan microbodies: peroxisomes, alpha-glycerophosphate oxidase bodies, hydrogenosomes. Annu. Rev. Microbiol. 1975, 29:467-483.
52. Munsch M., Lotfi A., Hafez H.M., Al-Quraishy S., Mehlhorn H. Light and transmission electron microscopic studies on trophozoites and cyst-like stages of Histomonas meleagridis from cultures. Parasitol. Res. 2009, 104:683-689.
53. Ockert G., Schneider W. Electron microscopic findings in Dientamoeba fragilis. Z. Gesamte Hyg. 1974, 20:555-557.
54. Ohkuma M., Iida T., Ohtoko K., Yuzawa H., Noda S., Viscogliosi E., Kudo T. Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Mol. Phylogenet. Evol. 2005, 35:646-655.
55. Ovcinnikov N.M., Delektorskij V.V., Turanova E.N., Yashkova G.N. Further studies of Trichomonas vaginalis with transmission and scanning electron microscopy. Br. J. Vener Dis. 1975, 51:357-375.
56. Prescott D.M. The DNA of ciliated protozoa. Microbiol. Rev. 1994, 58:233-267.
57. Revets H., Dekegel D., Deleersnijder W., De Jonckheere J., Peeters J., Leysen E., Hamers R. Identification of virus-like particles in Eimeria stiedae. Mol. Biochem. Parasitol. 1989, 36:209-215.
58. Sawangjaroen N., Luke R., Prociv P. Diagnosis by faecal culture of Dientamoeba fragilis infections in Australian patients with diarrhoea. Trans. R Soc. Trop. Med. Hyg. 1993, 87:163-165.
59. Schuster F.L. Ultrastructure of Histomonas meleagridis (Smith) Tyzzer, a Parasitic Amebo-Flagellate. J. Parasitol. 1968, 54:725-737.
60. Shaia C.I., Voyich J., Gillis S.J., Singh B.N., Burgess D.E. Purification and expression of the Tf190 adhesin in Tritrichomonas foetus. Infect. Immun. 1998, 66:1100-1105.
61. Shiflett A.M., Johnson P.J. Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol. 2010, 64:409-429.
62. Silard R., Colea A., Panaitescu D., Florescu P., Roman N. Studies on Dientamoeba fragilis in Romania. I. Dientamoeba fragilis isolated from clinical cases. Problems of diagnosis, incidence, clinical aspects. Arch. Roum. Pathol. Exp. Microbiol. 1979, 38:359-372.
63. Silard R., Burghelea B., Panaitescu D., Burcos V. Ultrastructure of Dientamoeba fragilis: a study of the mononucleated stage. Arch. Roum. Pathol. Exp. Microbiol. 1984, 43:87-101.
64. Silard R., Burghelea B. Endosymbionts in Dientamoeba fragilis trophozoites resistant to antiprotozoal drugs. Arch. Roum. Pathol. Exp. Microbiol. 1986, 45:65-74.
65. Silberman J.D., Clark C.G., Sogin M.L. Dientamoeba fragilis shares a recent common evolutionary history with the trichomonads. Mol. Biochem. Parasitol. 1996, 76:311-314.
66. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 1975, 98:503-517.
67. Stabler R.M. The morphology of Trichomonas gallinae (=columbae). J. Morphol. 1941, 69:501-515.
68. Stabler R.M. Trichomonas gallinae: a review. Exp. Parasitol. 1954, 3:368-402.
69. Stairs C.W., Roger A.J., Hampl V. Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a firmicute. Mol. Biol. Evol. 2011, 28:2087-2099.
70. Stark D., Phillips O., Peckett D., Munro U., Marriott D., Harkness J., Ellis J. Gorillas are a host for Dientamoeba fragilis: an update on the life cycle and host distribution. Vet. Parasitol. 2008, 151:21-26.
71. Stark D., Barratt J., Roberts T., Marriot D., Harkness J., Ellis J. Comparison of microscopy, two xenic culture techniques, conventional and real-time PCR for the detection of Dientamoeba fragilis in clinical stool samples. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29:411-416.
72. Stark D., Barratt J., Roberts T., Marriott D., Harkness J., Ellis J. A review of the clinical presentation of dientamoebiasis. Am. J. Trop. Med. Hyg. 2010, 82:614-619.
73. Stark D.J., Beebe N., Marriott D., Ellis J.T., Harkness J. Dientamoebiasis: clinical importance and recent advances. Trends Parasitol. 2006, 22:92-96.
74. Svärd S.G., Hagblom P., Palm J.E. Giardia lamblia - a model organism for eukaryotic cell differentiation. FEMS Microbiol. Lett. 2003, 218:3-7.
75. Tarr P.I., Aline R.F., Smiley B.L., Scholler J., Keithly J., Stuart K. LR1: a candidate RNA virus of Leishmania. Proc. Natl. Acad. Sci. U S A 1988, 85:9572-9575.
76. Tasca T., De Carli G.A. Scanning electron microscopy study of Trichomonas gallinae. Vet. Parasitol. 2003, 118:37-42.
77. Tasca T., De Carli G.A. Morphological study of Tetratrichomonas didelphidis isolated from opossum Lutreolina crassicaudata by scanning electron microscopy. Parasitol. Res. 2007, 100:1385-1388.
78. Wang A.L., Wang C.C. The double-stranded RNA in Trichomonas vaginalis may originate from virus-like particles. Proc. Natl. Acad. Sci. U S A 1986, 83:7956-7960.
79. Wang A.L., Wang C.C. Discovery of a specific double-stranded RNA virus in Giardia lamblia. Mol. Biochem. Parasitol. 1986, 21:269-276.
80. Wang A.L., Wang C.C. Viruses of the protozoa. Annu. Rev. Microbiol. 1991, 45:251-263.
81. Wang A.L., Wang C.C. Viruses of parasitic protozoa. Parasitol. Today 1991, 7:76-80.
82. Wang A.L., Wang C.C. A linear double-stranded RNA in Trichomonas vaginalis. J. Biol. Chem. 1985, 260:3697-3702.
83. Warton A., Honigberg B.M. Structure of trichomonads as revealed by scanning electron microscopy. J. Protozool. 1979, 26:56-62.
84. Wenrich D.H. Studies on Dientamoeba fragilis (protozoa). III. Binary fission with special reference to nuclear division. J. Parasitol. 1939, 25:43-45.
85. Wenrich D.H. Nuclear structure and nuclear division in Dientamoeba fragilis (Protozoa). J. Morphol. 1944, 74:467-491.
86. Wenrich D.H. Studies on Dientamoeba fragilis (protozoa). IV. Further observations, with an outline of present-day knowledge of this species. J. Parasitol. 1944, 30:322-337.
87. Wiesehahn G.P., Jarroll E.L., Lindmark D.G., Meyer E.A., Hallick L.M. Giardia lamblia: autoradiographic analysis of nuclear replication. Exp. Parasitol. 1984, 58:94-100.
88. Windsor J.J., Johnson E.H. Dientamoeba fragilis: the unflagellated human flagellate. Br. J. Biomed. Sci. 1999, 56:293-306.
89. Windsor J.J., Macfarlane L., Hughes-Thapa G., Jones S.K., Whiteside T.M. Detection of Dientamoeba fragilis by culture. Br. J. Biomed. Sci. 2003, 60:79-83.
90. Zaragatzki E., Hess M., Grabensteiner E., Abdel-Ghaffar F., Al-Rasheid K.A., Mehlhorn H. Light and transmission electron microscopic studies on the encystation of Histomonas meleagridis. Parasitol. Res. 2010, 106:977-983.
91. Zubácová Z., Cimburek Z., Tachezy J. Comparative analysis of trichomonad genome sizes and karyotypes. Mol. Biochem. Parasitol. 2008, 161:49-54.