Assessment of the role of Trichomonas tenax in the etiopathogenesis of human periodontitis: A systematic review

Autoři: C. Bisson aff001;  S. M. Dridi aff003;  M. Machouart aff001
Působiště autorů: Stress, Immunity, Pathogens Laboratory, EA7300 Lorraine University, Faculty of Medicine, Vandoeuvre- lès- Nancy, France aff001;  CHU Odontologie de Nancy - Department of Periodontology– Rue du Docteur Heydenreich, Nancy, University Lorraine, France aff002;  CHU Odontologie de Nice -Department of periodontology- CHU Saint Roch – Department of Periodontology, Nice, France aff003;  CHU Brabois, Parasitology - Mycology Laboratory, CHU Nancy-Brabois, Vandoeuvre-les -Nancy, France aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article



This systematic review was to assess the presence of Trichomonas tenax in patients with periodontitis and to elucidate its potential role in the onset and development of this disease.


Systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and by consulting the five databases: Medline, Science Direct, Web of Science, Dentistry and Oral Science Sources and Cochrane Central Register of Controlled Trials. Following Koch’s postulates revisited by Socransky as PICO framework, this collection data was only including full text of clinical trials concerning patients with periodontitis, case-reports and in vitro research published between 1960 and March 2019.


On the 376 studies identified, only 25 fulfilled our eligible criteria. Most of these studies were in vitro research articles designed to evaluate potential virulence factors, and others were clinical trials (case-control studies, randomized controlled trial) and case-reports. The analysis of these papers has shown that i) Trichomonas tenax is more frequently detected in dental biofilm from sites with periodontitis than in healthy sites; ii) this live flagellate seems capable of producing diverse enzymes that could participate in periodontal breakdown and has the capacity to adhere to epithelial cells, its lysed form could induce the synthesis of IL-8 from macrophage cell lines; iii) the impact of non-surgical treatment of periodontitis have not been thoroughly evaluated on the presence of T. tenax


This systematic review has reported the presence of T. tenax more frequently in diseased than healthy sites and the capacity of this flagellate to synthesis enzymes which could participate to the degradation of periodontal tissues. Nevertheless, these data do not meet all the postulates and are not enough to provide firm conclusions about the role of T. tenax in the etiopathogenesis of periodontitis.

Klíčová slova:

Cytotoxicity – Pathogenesis – Periodontal diseases – Periodontitis – Proteases – Protozoans – Trichomonas vaginalis – Virulence factors


1. Marcenes W, Kassebaum NJ, Bernabé E, Flaxman A, Naghavi M, Lopez A, et al. Global burden of oral conditions in 1990–2010: a systematic analysis. J Dent Res. 2013; 92: 592–597. doi: 10.1177/0022034513490168 23720570

2. Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJ, Marcenes W. Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression. J Dent Res. 2014; 93: 1045–1053. doi: 10.1177/0022034514552491 25261053

3. Hajishengallis G, Moutsopoulos NM, Hajishengallis E, Chavakis T. Immune and regulatory functions of neutrophils in inflammatory bone loss. Seminars in Immunology. 2016; 28: 146–58. doi: 10.1016/j.smim.2016.02.002 26936034

4. Avila M, Ojcius DM, Yilmaz O. The oral microbiota: living with a permanent guest. DNA Cell Biol. 2009; 28: 405–411. doi: 10.1089/dna.2009.0874 19485767

5. Li F, Zhu C, Deng FY, Wong MCM, Lu HX, Feng XP. Herpesviruses in etiopathogenesis of aggressive periodontitis: A meta-analysis based on case-control studies. PLoS One. 2017; 12: e0186373. doi: 10.1371/journal.pone.0186373 29036216

6. Canabarro A, Valle C, Farias MR, Santos FB, Lazera M, Wanke B. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013; 48: 428–432. doi: 10.1111/jre.12022 23137301

7. Feki A, Molet B, Haag R, Kremer M. [Protozoa of the human oral cavity (epidemiological correlations and pathogenic possibilities]. J Biol Buccale. 1981; 9: 155–161. 6943141

8. Benabdelkader S, Andreani J, Gillet A, Terrer E, Pignoly M, Chaudet H, et al. Specific clones of Trichomonas tenax are associated with periodontitis. PLoS One. 2019; 14: e0213338. doi: 10.1371/journal.pone.0213338 30856220

9. Marty M, Lemaitre M, Kémoun P, Morrier JJ, Monsarrat P. Trichomonas tenax and periodontal diseases: a concise review. Parasitology. 2017; 144: 1417–1425. doi: 10.1017/S0031182017000701 28583214

10. Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. Open Med. 2009; 3:e123–30. 21603045

11. Hardi AC, Fowler SA. Evidence-Based Medicine and Systematic Review Services at Becker Medical Library. Mo Med. 2014; 111: 416–418. 25438363

12. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol. 1992; 63: 322–331.

13. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999; 4: 1–6. doi: 10.1902/annals.1999.4.1.1 10863370

14. Wells G, Tugwell P, Shea B, Guyatt G, Peterson J, Zytaruk N, et al. Osteoporosis Methodology Group and The Osteoporosis Research Advisory Group. Meta-analyses of therapies for postmenopausal osteoporosis. V. Meta-analysis of the efficacy of hormone replacement therapy in treating and preventing osteoporosis in postmenopausal women. Endocr Rev. 2002; 23: 529–539. 12202468

15. Ferrara A, Conca R, Grassi L Jr, de Carneri I. Possible pathogenic role of Trichomonas tenax in chronic periodontitis. Ann Ist Super Sanita. 1986; 22: 253–255. 3752801

16. Rashidi Maybodi F, Haerian Ardakani A, Fattahi Bafghi A, Haerian Ardakani A, Zafarbakhsh A. The Effect of Nonsurgical Periodontal Therapy on Trichomonas Tenax and Entamoeba Gingivalis in Patients with Chronic Periodontitis. J Dent (Shiraz). 2016; 17: 171–176.

17. Ribeiro LC, Santos C, Benchimol M. Is Trichomonas tenax a Parasite or a Commensal? Protist. 2015; 166: 196–210. doi: 10.1016/j.protis.2015.02.002 25835639

18. Alderete JF, Garza GE. Specific nature of Trichomonas vaginalis parasitism of host cell surfaces. Infect Immun. 1985; 50: 701–708. 3877690

19. Alderete JF, Pearlman E. Pathogenic Trichomonas vaginalis cytoxicity to cell culture monolayers. Br J Vener Dis. 1984; 60: 99–105. doi: 10.1136/sti.60.2.99 6608395

20. El Sibaei MM, Abdel-Fattah NS, Ahmed SA, Abou-Seri HM. Growth kinetics, antigen profiling, and proteinase activity of Egyptian Trichomonas tenax isolates derived from patients having oral infections. Exp Parasitol. 2012; 130: 416–422. doi: 10.1016/j.exppara.2012.01.018 22348932

21. Yamamoto A, Asaga E, Nagao E, Igarashi T, Goto N. Characterization of the Cathepsin B-like Proteinases of Trichomonas Tenax ATCC 30207. Oral Microbiol Immunol. 2000; 15: 360–364. doi: 10.1034/j.1399-302x.2000.150604.x 11154432

22. Nagao E, Yamamoto A, Igarashi T, Goto N, Sasa R. Two Distinct Hemolysins in Trichomonas Tenax ATCC 30207. Oral Microbiol Immunol. 2000; 15: 355–359. doi: 10.1034/j.1399-302x.2000.150603.x 11154431

23. Segović S, Buntak-Kobler D, Galić N, Katunarić M. Trichomonas Tenax Proteolytic Activity. Coll Antropol. 1998; 22: 45–49. 9951139

24. Bózner P, Demes P. Degradation of Collagen Types I, III, IV and V by Extracellular Proteinases of an Oral Flagellate Trichomonas Tenax. Arch Oral Biol.1991; 36: 765–770. doi: 10.1016/0003-9969(91)90043-t 1747075

25. Bózner P, Demes P. Cell-associated and extracellular proteolytic activity of an oral flagellate, Trichomonas tenax. Arch Oral Biol. 1991; 36: 77–83. doi: 10.1016/0003-9969(91)90056-z 2012529

26. Govro EJ, Stuart MK. Cytokine response of human THP-1 macrophages to Trichomonas tenax. Exp Parasitol. 2016; 169: 77–80. doi: 10.1016/j.exppara.2016.07.011 27497807

27. Ioli A, Ferlazzo M, Fossari MT, Gembillo C, Skotarczak B, Vasi A, et al. Trichomonas tenax in haemodyalized patients-serologic research. Wiad Parazytol. 1987; 33: 165–167. 3687008

28. Kott H, Adler S. A Serological Study of Trichomonas Sp. Parasitic in Man. Trans R Soc Trop Med Hyg. 1961; 55: 333–344. doi: 10.1016/0035-9203(61)90102-x 13753502

29. Brosh-Nissimov T, Hindiyeh M, Azar R, Smollan G, Belausov N, Mandelboim M, et al. A false-positive Trichomonas vaginalis result due to Trichomonas tenax presence in clinical specimens may reveal a possible T. tenax urogenital infection. Clin Microbiol Infect. 2019; 25:123–124. doi: 10.1016/j.cmi.2018.09.011 30267929

30. Dimasuay KG, Rivera WL. First report of Trichomonas tenax infections in the Philippines. Parasitol Int. 2014; 63: 400–402. doi: 10.1016/j.parint.2013.12.015 24406842

31. Leterrier M, Morio F, Renard B, Poirier AS, Miegeville M, Chambreuil G. Trichomonads in Pleural Effusion: Case Report, Literature Review and Utility of PCR for Species Identification. New Microbiol. 2012; 35: 83–87. 22378558

32. Crucitti T, Jespers V, Mulenga C, Khondowe S, Vandepitte J, Buvé A. Trichomonas vaginalis is highly prevalent in adolescent girls, pregnant women, and commercial sex workers in Ndola, Zambia. Sex Transm Dis. 2010; 37: 223–227. 19940808

33. Chiche L, Donati S, Corno G, Benoit S, Granier I, Chouraki M, et al. Trichomonas tenax in pulmonary and pleural diseases. Presse Med. 2005; 34: 1371–1372. 16292189

34. Duboucher C, Farto-Bensasson F, Chéron M, Peltier JY, Beaufils F, Périé G. Lymph Node Infection by Trichomonas Tenax: Report of a Case with Co-Infection by Mycobacterium Tuberculosis. Hum Pathol.2000; 31: 1317–1321. doi: 10.1053/hupa.2000.18502 11070125

35. Jakobsen EB, Friis-Moller A, Friis J. Trichomonas Species in a Subhepatic Abscess. Eur J Clin Microbiol. 1987; 6: 296–297. doi: 10.1007/bf02017616 3622496

36. Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev. 1996; 9: 18–33. 8665474

37. Perez-Chaparro PJ, Gonçalves C, Figueiredo LC, Faveri M, Lobão E, Tamashiro N, et al. Newly identified pathogens associated with periodontitis: a systematic review. J Dent Res. 2014; 93: 846‑858. doi: 10.1177/0022034514542468 25074492

38. Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol. 2014; 35: 3–11. doi: 10.1016/ 24269668

39. Chen C, Hemme C, Beleno J, Shi Z, Ning D, Qin Y, et al. Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy. ISME J. 2018; 12: 1210–1224. doi: 10.1038/s41396-017-0037-1 29339824

40. Mehr A.K, Zarandi A, Anush K. Prevalence of Oral Trichomonas tenax in Periodontal Lesions of Down Syndrome in Tabriz, Iran. J Clin Diagn Res. 2015; 9:88–90.

41. Dybicz M, Perkowski K, Sędzikowska A, Baltaza W, Chomicz L. Studies on prevalence of infection with Trichomonas tenax identified by molecular techniques–in respect to oral health of patients with various systemic disease requiring immunosuppressive therapy. Ann Parasitol. 2018; 64: 193–197. 30316209

42. Wantland WW, Lauer D. Correlation of some oral hygiene variables with age, sex, and incidence of oral protozoa. J Dent Res. 1970; 49: 293–297. doi: 10.1177/00220345700490021601 5264592

43. Rosalem W, Rescala B, Teles RP, Fischer RG, Gustafsson A, Figueredo CM. Effect of non-surgical treatment on chronic and aggressive periodontitis: clinical, immunologic, and microbiologic findings. J Periodontol. 2011; 82: 979–989. doi: 10.1902/jop.2011.100579 21309718

44. Müller HP, Heinecke A, Borneff M, Kiencke C, Knopf A, Pohl S. Eradication of Actinobacillus actinomycetemcomitans from the oral cavity in adult periodontitis. J Periodontal Res. 1998; 33: 49–58. doi: 10.1111/j.1600-0765.1998.tb02291.x 9524321

45. Ribaux CL, Magloire H, Joffre A, Morrier JJ. Immunohistochemical localization of fibronectin-like protein on the cell surface of the oral flagelatte Trichomonas tenax. J Biol Buccale. 1983; 11: 41–51. 6343365

46. Bugueno IM, Khelif Y, Seelam N, Morand DN, Tenenbaum H, Davideau JL, et al. Porphyromonas gingivalis Differentially Modulates Cell Death Profile in Ox-LDL and TNF-α Pre-Treated Endothelial Cells. PLoS One. 2016; 11: e0154590. doi: 10.1371/journal.pone.0154590 27124409

47. De Diego I, Veillard F, Sztukowska MN, Guevara T, Potempa B, Pomowski A, et al. Structure and mechanism of cysteine peptidase gingipain K (Kgp), a major virulence factor of Porphyromonas gingivalis in periodontitis. J Biol Chem. 2014; 289: 32291–32302. doi: 10.1074/jbc.M114.602052 25266723

48. Sahingur SE, Xia XJ, Alamgir S, Honma K, Sharma A, Schenkein HA. DNA from Porphyromonas gingivalis and Tannerella forsythia induce cytokine production in human monocytic cell lines. Mol Oral Microbiol. 2010; 25: 123–135. doi: 10.1111/j.2041-1014.2009.00551.x 20331800

49. Tokuda M, Duncan M, Cho MI, Kuramitsu HK. Role of Porphyromonas gingivalis protease activity in colonization of oral surfaces. Infect Immun. 1996; 64: 4067–4073. 8926070

50. Hosogi Y, Hayakawa M, Abiko Y. Monoclonal antibody against Porphyromonas gingivalis hemagglutinin inhibits hemolytic activity. Eur J Oral Sci. 2001; 109: 109–113. doi: 10.1034/j.1600-0722.2001.00995.x 11347654

51. Balashova NV, Crosby JA, Al Ghofaily L, Kachlany SC. Leukotoxin confers beta-hemolytic activity to Actinobacillus actinomycetemcomitans. Infect Immun. 2006; 74: 2015–2021. doi: 10.1128/IAI.74.4.2015-2021.2006 16552030

52. Kachlany SC. Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy. J Dent Res. 2010; 89: 561–570. doi: 10.1177/0022034510363682 20200418

53. Chu L, Ebersole JL, Kurzban GP, Holt SC. Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect Immun. 1997; 65: 3231–3238. 9234780

54. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol. 2004; 4: 478–85. doi: 10.1038/nri1373 15173836

55. Ribaux CL. Study of an oral protozoan Trichomonas tenax using scanning and transmission electron microscopy. J Biol Buccale. 1979; 7: 157–168. 287668

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