The Neglected Role of Trichomonas tenax in Oral Diseases: A Systematic Review and Meta-analysis

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Abstract

Purpose

Trichomonas tenax (T. tenax) is a commensal flagellated protozoan found in periodontal microenvironment of the oral cavity, with a possible role in periodontal diseases. The purpose of the present systematic review and meta-analysis was to determine the worldwide prevalence of T. tenax infection and to show the neglected association of this parasitic infection with oral diseases.

Methods

To find literatures published until August 2020, five English databases (PubMed, Scopus, Science Direct, Web of Science and Google Scholar) were explored. Finally, 65 papers were qualified to be included in the current study.

Results

Our results revealed a global pooled prevalence of 17% (95% CI 14–22%) for T. tenax infection. The highest prevalence was estimated at 56% (42–69%) in Chile, while the lowest prevalence was related to Kenya with 3% (1–6%). The age-based analysis found that the infection was most common in 46–55 mean age group with 15% (0–100%). The overall prevalence regarding culture method, molecular method and direct method was 21% (12–32%), 19% (8–35%) and 17% (12–23%), respectively. Moreover, the subgroup analysis showed the pooled prevalence in patient with candidiasis [22% (3–52%)], gingivitis [21% (9–36%)] and periodontitis [27% (10–48%)].

Conclusion

Our study specified a connection between T. tenax protozoa and periodontitis disease. However, more epidemiological studies as well as clinical trials are needed to precisely identify this relation.

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Change history

  • 01 March 2021

    One of the affiliations was incorrect. This has now been corrected.

References

  1. 1.

    Benabdelkader S, Andreani J, Gillet A, Terrer E, Pignoly M, Chaudet H et al (2019) Specific clones of Trichomonas tenax are associated with periodontitis. PLoS One 14(3):0213338. https://doi.org/10.1371/journal.pone.0213338

    CAS  Article  Google Scholar 

  2. 2.

    Hassan HAH, Ibrahim AHH, Karim FA, Amina I, Osama IM, Ghada HE (2014) Relation between Trichomonas tenax and pulmonary diseases. Egypt J Med Sci 35:633–652

    Google Scholar 

  3. 3.

    Marty M, Lemaitre M, Kémoun P, Morrier JJ, Monsarrat P (2017) Trichomonas tenax and periodontal diseases: A concise review. Parasitology 144:1–9. https://doi.org/10.1017/S0031182017000701

    Article  Google Scholar 

  4. 4.

    Szczepaniak K, Lojszczyk-Szczepaniak A, Tomczuk K, Skrzypek T, Lisiak B, Abbass ZAAH (2015) Canine Trichomonas tenax mandibular gland infestation. Acta Vet Scand 58(1):1–4. https://doi.org/10.1186/s13028-016-0197-4

    Article  Google Scholar 

  5. 5.

    Dybicz M, Perkowski K, Baltaza W, Padzik M, Sędzikowska A, Chomicz L (2018) Molecular identification of Trichomonas tenax in the oral environment of domesticated animals in Poland–potential effects of host diversity for human health. Ann Agric Environ Med 25(3): 464–468. https://doi.org/10.26444/aaem/92309

  6. 6.

    Kikuta N, Yamamoto A, Fukura K, Goto N (1997) Specific and sensitive detection of Trichomonas tenax by the polymerase chain reaction. Lett Appl Microbiol 24(3):193–197

    CAS  Article  Google Scholar 

  7. 7.

    Bisson C, Lec PH, Blique M, Thilly N, Machouart M (2018) Presence of trichomonads in subgingival biofilm of 195 patients with periodontitis. Parasitol Res 117:3767–3774. https://doi.org/10.1007/s00436-018-6077-2

    Article  PubMed  Google Scholar 

  8. 8.

    Ghabanchi J, Zibaei M, Afkar MD, Sarbazie AH (2010) Prevalence of oral Entamoeba gingivalis and Trichomonas tenax in patients with periodontal disease and healthy population in Shiraz, southern Iran. Indian J Dent Res 21:89. https://doi.org/10.4103/0970-9290.62821

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Dybicz M, Perkowski K, Sedzikowska A, Baltaza W, Chomicz L (2018) 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, https://doi.org/10.17420/ap6403.151

  10. 10.

    Duboucher C, Farto-Bensasson F, Chéron M, Peltier JY, Beaufils F, Périé G (2000) Lymph node infection by Trichomonas tenax: Report of a case with co-infection by Mycobacterium tuberculosis. Hum Pathol 31: 13–17–1321. https://doi.org/10.1053/hupa.2000.18502

  11. 11.

    Duboucher C, Mogenet M, Perie G (1995) Salivary trichomoniasis: A case report of infestation of a submaxillary gland by Trichomonas tenax. Arch Pathol Lab Med 119:277–279

    CAS  PubMed  Google Scholar 

  12. 12.

    Lewis KL, Doherty DE, Ribes J, Seabolt JP, Bensadoun ES (2003) Empyema caused by Trichomonas. Chest 123:291–292. https://doi.org/10.1378/chest.123.1.291

    Article  PubMed  Google Scholar 

  13. 13.

    Martínez-Girón R, Esteban JG, Ribas A, Doganci L (2008) Protozoa in respiratory pathology: A review. Eur Respir. J 32: 1354–1370. https://doi.org/10.1183/09031936.00022008

  14. 14.

    El-Sherbini GT (2012) In vitro effect of pomegranate extract on Trichomonas Tenax. J Bacteriol Parasitol 3(143):2. https://doi.org/10.4172/2155-9597.1000143

    Article  Google Scholar 

  15. 15.

    Brosh-Nissimov T, Hindiyeh M, Azar R, Smollan G, Belausov N, Mandelboim M, Keller N, Gefen Halevi S (2019) 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 25:123–124. https://doi.org/10.1016/j.cmi.2018.09.011

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Bisson C, Dridi SM, Machouart M (2019) Assessment of the role of Trichomonas tenax in the etiopathogenesis of human periodontitis: A systematic review. PLoS One 14:e0226266. https://doi.org/10.1371/journal.pone.0226266

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Moher D, Liberati A, Tetzlaff J, Altman DG, Altman D, Antes G (2009) Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLOS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Zibaei M, Nosrati MRC, Shadnoosh F, Houshmand E, Karami MF, Rafsanjani MK, Badri M (2020) Insights into hookworm prevalence in Asia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 114(3):141–154. https://doi.org/10.1093/trstmh/trz115

    Article  PubMed  Google Scholar 

  19. 19.

    Eslahi AV, Badri M, Khorshidi A, Majidiani H, Hooshmand E, Hosseini H, Zibaei M (2020) Prevalence of Toxocara and Toxascaris infection among human and animals in Iran with meta-analysis approach. BMC Infect Dis 20(1):1–17. https://doi.org/10.1186/s12879-020-4759-8

    Article  Google Scholar 

  20. 20.

    Eslahi AV, Badri M, Nahavandi KH, Houshmand E, Dalvand S, Riahi SM, Ghanbari Johkool M, Asadi N, Khademvatan S (2021) Prevalence of strongyloidiasis in the general population of the world: a systematic review and meta-analysis. Pathog Glob Health. https://doi.org/10.1080/20477724.2020.1851922

    Article  PubMed  Google Scholar 

  21. 21.

    Wells G, Shea B, O’Connell, D, Peterson J, Welch, V, Losos M, Tugwell P (2012) The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. http. www. ohric a/progr ams/clini cal_epide miolo gy/oxfor dasp.

  22. 22.

    Badri M, Eslahi AV, Olfatifar M (2021) dalvand S, Houshmand E, Abdoli A, Majidiani H, Sima H (2021) Keys to unlock the enigma of ocular toxocariasis: a systematic review and meta-analysis. Ocul Immunol Inflamm. 6:245–264

    Google Scholar 

  23. 23.

    Marsh PD (1994) Microbial ecology of dental plaque and its significance in health and disease. ADRm 8:263–271. https://doi.org/10.1177/08959374940080022001

    CAS  Article  Google Scholar 

  24. 24.

    Marsh PD (1999) Microbiologic aspects of dental plaque and dental caries. Dent Clin N Am 43:599–614

    CAS  PubMed  Google Scholar 

  25. 25.

    Long J, Cai Q, Steinwandel M, Hargreaves MK, Bordenstein SR, Blot WJ (2017) Association of oral microbiome with type 2 diabetes risk. J Periodontal Res 52:636–643. https://doi.org/10.1111/jre.12432

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Xiao E, Mattos M, Vieira GHA, Chen S, Corrêa JD, Wu Y (2017) Diabetes Enhances IL-17 Expression and Alters the Oral Microbiome to Increase Its Pathogenicity. Cell Host Microbe 22:120–128. https://doi.org/10.1016/j.chom.2017.06.014

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Huang C, Shi G (2019) Smoking and microbiome in oral, airway, gut and some systemic diseases. J Transl Med. https://doi.org/10.1186/s12967-019-1971-7

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Wu J, Li M, Huang R (2019) The effect of smoking on caries-related microorganisms. Tob Induc Dis https://doi.org/10.18332/tid/105913

  29. 29.

    Arzmi MH, Dashper S, McCullough M (2019) Polymicrobial interactions of Candida albicans and its role in oral carcinogenesis. J Oral Pathol Med 48:546–551. https://doi.org/10.1111/jop.12905

    Article  PubMed  Google Scholar 

  30. 30.

    Slocum C, Kramer C, Genco CA (2016) Immune dysregulation mediated by the oral microbiome: potential link to chronic inflammation and atherosclerosis. J Intern Med 280:114–128. https://doi.org/10.1111/joim.12476

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Kleinstein SE, Nelson KE, Freire M (2020) Inflammatory networks linking oral microbiome with systemic health and disease. J Dent Res. https://doi.org/10.1177/0022034520926126

    Article  PubMed  Google Scholar 

  32. 32.

    Mahmoud MSE, Rahman GA (2004) Pulmonary trichomoniasis: improved diagnosis by using polymerase chain reaction targeting Trichomonas tenax 18S rRNA gene in sputum specimens. J Egypt Soc Parasitol 34:197–211

    PubMed  Google Scholar 

  33. 33.

    Ribeiro LC, Santos C, Benchimol M (2015) Is Trichomonas tenax a Parasite or a commensal? Protist 166:196–210. https://doi.org/10.1016/j.protis.2015.02.002

    Article  PubMed  Google Scholar 

  34. 34.

    Bózner P, Demeš P (1991) Cell-associated and extracellular proteolytic activity of an oral flagellate, Trichomonas tenax. Arch Oral Biol 36:77–83. https://doi.org/10.1016/0003-9969(91)90056-Z

    Article  PubMed  Google Scholar 

  35. 35.

    Bózner P, Demeš P (1991) Degradation of collagen types I, III, IV and V by extracellular proteinases of an oral flagellate Trichomonas tenax. Arch Oral Biol 36:765–770. https://doi.org/10.1016/0003-9969(91)90043-T

    Article  PubMed  Google Scholar 

  36. 36.

    Yamamoto A, Asaga E, Nagao E, Igarashi T, Goto N (2000) Characterization of the cathepsin B-like proteinases of Trichomonas tenax ATCC 30207. Oral Microbiol Immunol 15:360–364. https://doi.org/10.1034/j.1399-302x.2000.150604.x

    CAS  Article  PubMed  Google Scholar 

  37. 37.

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

    CAS  PubMed  Google Scholar 

  38. 38.

    Zvetkova A, Isev V, Stoilova R (1988) Humoral immune response against Trichomonas tenax in patients with chronic catarrhal gingivitis before and after specific Fasigyn treatment. Stomatologiia (Sofiia) 70:4–8

    CAS  Google Scholar 

  39. 39.

    Alou L, Giménez MJ, Manso F, Sevillano D, Torrico M, González N (2009) Tinidazole inhibitory and cidal activity against anaerobic periodontal pathogens. Int J Antimicrob Agents 33:449–452. https://doi.org/10.1016/j.ijantimicag.2008.10.012

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Metabolic Diseases Research Center, Research Institute for Prevention of Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran under the contract no. IR.QUMS.Rec.1399.273.

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Correspondence to Milad Badri.

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Supplementary Information

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Supplementary Figure 1 Forest plot of odds ratios of Trichomonas tenax in case–control studies (PDF 327 KB)

Supplementary Figure 2 Forest plots for random-effects meta-analysis of Trichomonas tenax based on Mean Age (PDF 288 KB)

Supplementary Figure 3 Forest plot of odds ratios of T. tenax in male and female (PDF 290 KB)

Supplementary Figure 4 Forest plot of odds ratios of T. tenax in male and female (PDF 525 KB)

Supplementary Figure 5 Forest plots for random-effects meta-analysis of T. tenax among oral candidiasis patients (PDF 241 KB)

Supplementary Figure 6 Forest plots for random-effects meta-analysis of T. tenax in patients with Gingivitis (PDF 249 KB)

Supplementary Figure 7 Forest plots for random-effects meta-analysis of T. tenax in patients with Periodontitis (PDF 273 KB)

Supplementary Figure 8 Forest plots for random-effects meta-analysis of T. tenax based on smoking habit (PDF 266 KB)

Supplementary Figure 9 Forest plots for random-effects meta-analysis of T. tenax in patients with Immunodeficiency disorders (PDF 256 KB)

Supplementary Figure 10 Forest plots for random-effects meta-analysis of T. tenax among diabetic patients (PDF 213 KB)

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Eslahi, A.V., Olfatifar, M., Abdoli, A. et al. The Neglected Role of Trichomonas tenax in Oral Diseases: A Systematic Review and Meta-analysis. Acta Parasit. (2021). https://doi.org/10.1007/s11686-021-00340-4

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Keywords

  • Prevalence
  • Trichomonas tenax
  • Worldwide
  • Oral health