Investigation of Dientamoeba fragilis Prevalence and Evaluation of Sociodemographic and Clinical Features in Patients with Gastrointestinal Symptoms

Abstract

Background

Dientamoeba fragilis is a protozoan parasite of the human gastrointestinal tract and still controversial in association with gastrointestinal symptoms.

Purpose

We present cross-sectional study of the prevalence of D. fragilis, and sociodemographic and clinical features in the patients with gastrointestinal symptoms.

Methods

A total of 490 fecal specimens were collected from outpatients with gastrointestinal symptoms in the Department of Parasitology, Faculty of Medicine, Ege University and Celal Bayar University, Turkey. Fecal specimens were examined with microscopy and inoculated in Robinson medium. D. fragilis-positive samples were examined for the presence of other intestinal parasites using enzyme immunoassay. Real-time PCR analysis was performed on all samples.

Results

Of the 490 stool specimens examined by real-time PCR, 59 patients were positive for D. fragilis infection with prevalence rate of 12.04%. Forty-four of positive patients (74.5%) were found to be infected with only D. fragilis, while 23.7% were co-infected with Blastocystis and 1.7% were co-infected with Rotavirus. No statistically significant difference was found in all the examined patients in terms of D. fragilis positivity for all sociodemographic parameters. Loose stool consistency was associated with the presence of D. fragilis, with 18.3% (P = 0.001). When the clinical symptoms of all the patients participating in this study were examined, diarrhea was statistically more significant in patients with the presence of D. fragilis (16.3%; P = 0.001). The rate of diarrhea in D. fragilis-positive patients (84.09%; P = 0.0005) was higher than that of D. fragilis-negative patients and it was statistically significant.

Conclusion

This study is important for assessing the prevalence of D. fragilis and its association with other factors in symptomatic patients in a large sample group in Turkey, as well as investigating the relationship of identified symptoms with the D. fragilis pathogenicity. It is suggested that D. fragilis in this case is not a commensal parasite but a pathogenic parasite and that the most common clinical symptom is diarrhea.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Anuar T.S., Hasim L., Moktar N., Salleh F.M., Al-Mekhlafi H.M. 2015. Prevalence of Dientamoeba fragilis among an Orang Asli population in rural Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 46, 844.

  2. 2.

    Barratt J.L., Harkness J., Marriott D., Ellis J.T., Stark D. 2011. A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microbes 2, 3-12. https://doi.org/10.4161/gmic.2.1.14755.

  3. 3.

    Borody T., Warren E., Wettstein A., Robertson G., Recabarren P., Fontella A., Herdnman K., Surace R. 2002. Eradication of Dientamoeba fragilis can resolve IBS-like symptoms. J Gastroenterol Hepatol 17, A103.

  4. 4.

    Caccio S.M. 2017. Molecular epidemiology of Dientamoeba fragilis. Acta tropica. https://doi.org/10.1016/j.actatropica.2017.06.029.

  5. 5.

    Calik S., Karaman U., Colak C. 2011. Prevalence of microsporidium and other intestinal parasites in children from Malatya, Turkey. Indian journal of microbiology 51, 345-349.

  6. 6.

    de Jong M.J., Korterink J.J., Benninga M.A., Hilbink M., Widdershoven J., Deckers-Kocken J.M. 2014. Dientamoeba fragilis and chronic abdominal pain in children: a case-control study. Arch Dis Child 99, 1109-1113. https://doi.org/10.1136/archdischild-2014-305942.

  7. 7.

    Dean AG S.K., Soe MM 2018. Open Source Epidemiologic Statistics for Public Health, OpenEpi.

  8. 8.

    Dogan N., Öz Y., Koçman N.Ü., Nursal A.F. 2012. Comparison of individual differences in the direct microscopic examination in the diagnosis of intestinal parasites. Türkiye Parazitolojii Dergisi 36, 211.

  9. 9.

    Enserink R., Scholts R., Bruijning-Verhagen P., Duizer E., Vennema H., de Boer R., Kortbeek T., Roelfsema J., Smit H., Kooistra-Smid M., van Pelt W. 2014. High detection rates of enteropathogens in asymptomatic children attending day care. PloS one 9, e89496. https://doi.org/10.1371/journal.pone.0089496.

  10. 10.

    Garcia L.S. 2016. Dientamoeba fragilis, One of the Neglected Intestinal Protozoa. J Clin Microbiol 54, 2243-2250. https://doi.org/10.1128/jcm.00400-16.

  11. 11.

    Grendon J., DiGiacomo R., Frost F. 1995. Descriptive features of Dientamoeba fragilis infections. The Journal of tropical medicine and hygiene 98, 309-315.

  12. 12.

    Gülmez D., Saribas Z., Akyön Y., Ergüven S. 2013. The results of Hacettepe University Faculty of Medicine Parasitology Laboratory in 2003-2012: evaluation of 10 years. Türkiye Parazitolojii Dergisi 37, 97.

  13. 13.

    Hakansson E. 1936. Dientamoeba fragilis, a cause of Illness. The American journal of tropical medicine and hygiene 1, 175-185.

  14. 14.

    Holtman G.A., Kranenberg J.J., Blanker M.H., Ott A., Lisman-van Leeuwen Y., Berger M.Y. 2017. Dientamoeba fragilis colonization is not associated with gastrointestinal symptoms in children at primary care level. Fam Pract 34, 25-29. https://doi.org/10.1093/fampra/cmw111.

  15. 15.

    Hussein E.M., Al-Mohammed H.I., Hussein A.M. 2009. Genetic diversity of Dientamoeba fragilis isolates of irritable bowel syndrome patients by high-resolution melting-curve (HRM) analysis. Parasitology research 105, 1053-1060.

  16. 16.

    Incani R.N., Ferrer E., Hoek D., Ramak R., Roelfsema J., Mughini-Gras L., Kortbeek T., Pinelli E. 2017. Diagnosis of intestinal parasites in a rural community of Venezuela: Advantages and disadvantages of using microscopy or RT-PCR. Acta tropica 167, 64-70. https://doi.org/10.1016/j.actatropica.2016.12.014.

  17. 17.

    Jepps M.W., Dobell C. 1918. Dientamoeba fragilis n. g., n. sp., a new Intestinal Amoeba from Man. Parasitology 10, 352-367. https://doi.org/10.1017/s0031182000003929.

  18. 18.

    Johnson E.H., Windsor J.J., Clark C.G. 2004. Emerging from obscurity: biological, clinical, and diagnostic aspects of Dientamoeba fragilis. Clin Microbiol Rev 17, 553-570, table of contents. https://doi.org/10.1128/cmr.17.3.553-570.2004.

  19. 19.

    Jokelainen P., Hebbelstrup Jensen B., Andreassen B.U., Petersen A.M., Roser D., Krogfelt K.A., Nielsen H.V., Stensvold C.R. 2017. Dientamoeba fragilis, a Commensal in Children in Danish Day Care Centers. J Clin Microbiol 55, 1707-1713. https://doi.org/10.1128/jcm.00037-17.

  20. 20.

    Karaman U., Atambay M., Aycan O., Yoloğlu S., Daldal N. 2006. Incidence of intestinal parasites in municipal sanitary workers in Malatya. Turkiye parazitolojii dergisi 30, 181-183.

  21. 21.

    Karaman Ü. S.S., Calık S., Sasmaz S. 2011. Akut ve Kronik Ürtikerli Hastalarda Microsporidia Pozitiflik Oranı. Mikrobiyoloji Bülteni.

  22. 22.

    Knoll E.W., Howell K.M. 1945. Studies on Dientamoeba fragilis: its Incidence and possible Pathogenicity. American journal of clinical pathology 15, 178-183.

  23. 23.

    Krogsgaard L.R., Engsbro A.L., Stensvold C.R., Nielsen H.V., Bytzer P. 2015. The prevalence of intestinal parasites is not greater among individuals with irritable bowel syndrome: a population-based case-control study. Clinical Gastroenterology and Hepatology 13, 507-513. e502.

  24. 24.

    Lagacé-Wiens P.R., VanCaeseele P.G., Koschik C. 2006. Dientamoeba fragilis: an emerging role in intestinal disease. Canadian Medical Association Journal 175, 468-468.

  25. 25.

    Maier A., Krolik J., Majury A. 2014. Triage and protocol recommendations for the parasitology laboratory based on an epidemiological investigation of parasite diagnostics in Ontario laboratories. Canadian Journal of Infectious Diseases and Medical Microbiology 25, 305-310.

  26. 26.

    Mumcuoglu I., Coskun F.A., Aksu N., Pürnak T., Güngör Ç. 2013. Role of Dientamoeba fragilis and Blastocystis spp. in irritable bowel syndrome. Türkiye Parazitolojii Dergisi 37, 73.

  27. 27.

    Munasinghe V.S., Vella N.G., Ellis J.T., Windsor P.A., Stark D. 2013. Cyst formation and faecal-oral transmission of Dientamoeba fragilis–the missing link in the life cycle of an emerging pathogen. International journal for parasitology 43, 879-883. https://doi.org/10.1016/j.ijpara.2013.06.003.

  28. 28.

    Norberg A., Nord C.E., Evengård B. 2003. Dientamoeba fragilis—a protozoal infection which may cause severe bowel distress. Clinical Microbiology and Infection 9, 65-68. DOI:https://doi.org/10.1046/j.1469-0691.2003.00459.x.

  29. 29.

    Ogren J., Van Nguyen S., Nguyen M.K., Dimberg J., Matussek A. 2016. Prevalence of Dientamoeba fragilis, Giardia duodenalis, Entamoeba histolytica/dispar, and Cryptosporidium spp in Da Nang, Vietnam, detected by a multiplex real-time PCR. APMIS 124, 529-533. https://doi.org/10.1111/apm.12535.

  30. 30.

    Ozcakir O., Gureser S., Erguven S., Yilmaz Y.A., Topaloglu R., Hascelik G. 2007. Characteristics of Blastocystis hominis infection in a Turkish university hospital. Turkiye parazitolojii dergisi/Turkiye Parazitoloji Dernegi = Acta parasitologica Turcica/Turkish Society for Parasitology 31, 277-282.

  31. 31.

    Picado A., Osman M., El Safadi D., Cian A., Benamrouz S., Nourrisson C., Poirier P., Pereira B., Razakandrainibe R., Pinon A., Lambert C., Wawrzyniak I., Dabboussi F., Delbac F., Favennec L., Hamze M., Viscogliosi E., Certad G. 2016. Prevalence and Risk Factors for Intestinal Protozoan Infections with Cryptosporidium, Giardia, Blastocystis and Dientamoeba among Schoolchildren in Tripoli, Lebanon. PLoS neglected tropical diseases 10. https://doi.org/10.1371/journal.pntd.0004496.

  32. 32.

    Punsawad C., Phasuk N., Bunratsami S., Thongtup K., Siripakonuaong N., Nongnaul S. 2017. Prevalence of intestinal parasitic infection and associated risk factors among village health volunteers in rural communities of southern Thailand. BMC public health 17, 564.

  33. 33.

    Robinson G. 1968. The laboratory diagnosis of human parasitic amoebae. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 285-294.

  34. 34.

    Roser D., Simonsen J., Nielsen H.V., Stensvold C.R., Molbak K. 2013. Dientamoeba fragilis in Denmark: epidemiological experience derived from four years of routine real-time PCR. European journal of clinical microbiology & infectious diseases: official publication of the European Society of Clinical Microbiology 32, 1303-1310. https://doi.org/10.1007/s10096-013-1880-2.

  35. 35.

    Rostami A., Riahi S.M., Haghighi A., Saber V., Armon B., Seyyedtabaei S.J. 2017. The role of Blastocystis sp. and Dientamoeba fragilis in irritable bowel syndrome: a systematic review and meta-analysis. Parasitology research. https://doi.org/10.1007/s00436-017-5535-6.

  36. 36.

    Scholten T. 1972. An improved technique for the recovery of intestinal protozoa. The Journal of parasitology 58, 633-634.

  37. 37.

    Sivcan E., Charyyeva A., Ceylan Ş.S., Yürük M., Erdoğan E., Şahin İ. 2018. Gastrointestinal Şikayeti Olan Hastalarda Dientamoeba fragilis Enfeksiyonu. Mikrobiyol Bul 52, 166-179.

  38. 38.

    Spencer M.J., Chapin M.R., Garcia L.S. 1982. Dientamoeba fragilis: a gastrointestinal protozoan infection in adults. American Journal of Gastroenterology 77.

  39. 39.

    Staat M.A., Rice M., Donauer S., Mukkada S., Holloway M., Cassedy A., Kelley J., Salisbury S. 2011. Intestinal Parasite Screening in Internationally Adopted Children: Importance of Multiple Stool Specimens. Pediatrics 128, e613-e622.

  40. 40.

    Stark D., Al-Qassab S.E., Barratt J.L., Stanley K., Roberts T., Marriott D., Harkness J., Ellis J.T. 2011. Evaluation of multiplex tandem real-time PCR for detection of Cryptosporidium spp., Dientamoeba fragilis, Entamoeba histolytica, and Giardia intestinalis in clinical stool samples. J Clin Microbiol 49, 257-262. https://doi.org/10.1128/jcm.01796-10.

  41. 41.

    Stark D., Barratt J., Chan D., Ellis J.T. 2016. Dientamoeba fragilis, the Neglected Trichomonad of the Human Bowel. Clin Microbiol Rev 29, 553-580. https://doi.org/10.1128/cmr.00076-15.

  42. 42.

    Stark D., Barratt J., Roberts T., Marriott D., Harkness J., Ellis J. 2010a. Comparison of microscopy, two xenic culture techniques, conventional and real-time PCR for the detection of Dientamoeba fragilis in clinical stool samples. European journal of clinical microbiology & infectious diseases 29, 411-416.

  43. 43.

    Stark D., Barratt J., Roberts T., Marriott D., Harkness J., Ellis J. 2010b. A review of the clinical presentation of dientamoebiasis. The American journal of tropical medicine and hygiene 82, 614-619. https://doi.org/10.4269/ajtmh.2010.09-0478.

  44. 44.

    Stark D., Beebe N., Marriott D., Ellis J., Harkness J. 2005. Prospective study of the prevalence, genotyping, and clinical relevance of Dientamoeba fragilis infections in an Australian population. J Clin Microbiol 43, 2718-2723. https://doi.org/10.1128/jcm.43.6.2718-2723.2005.

  45. 45.

    Stark D., Garcia L.S., Barratt J.L., Phillips O., Roberts T., Marriott D., Harkness J., Ellis J.T. 2014. Description of Dientamoeba fragilis cyst and precystic forms from human samples. J Clin Microbiol 52, 2680-2683. https://doi.org/10.1128/jcm.00813-14.

  46. 46.

    Stark D.J., Beebe N., Marriott D., Ellis J.T., Harkness J. 2006. Dientamoebiasis: clinical importance and recent advances. Trends in parasitology 22, 92-96.

  47. 47.

    Stensvold C., Arendrup M., Mølbak K., Nielsen H. 2007. The prevalence of Dientamoeba fragilis in patients with suspected enteroparasitic disease in a metropolitan area in Denmark. Clinical microbiology and infection 13, 839-842.

  48. 48.

    Stensvold C.R., Clark C.G. 2016. Current status of Blastocystis: A personal view. Parasitology international 65, 763-771. DOI:https://doi.org/10.1016/j.parint.2016.05.015.

  49. 49.

    Taş Z.C., Akbayram S., Ciçek M., Yilmaz H. 2009. Intestinal parasitoses detected in primary schoolchildren in the Van province. Turkiye parazitolojii dergisi 33, 289-293.

  50. 50.

    Verweij J.J., Mulder B., Poell B., van Middelkoop D., Brienen E.A., van Lieshout L. 2007. Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol Cell Probes 21, 400-404. https://doi.org/10.1016/j.mcp.2007.05.006.

  51. 51.

    Windsor J., Macfarlane L. 2005. Irritable bowel syndrome: the need to exclude Dientamoeba fragilis. The American journal of tropical medicine and hygiene 72, 501-501.

  52. 52.

    Windsor J., Macfarlane L., Hughes-Thapa G., Jones S., Whiteside T. 2003. Detection of Dientamoeba fragilis by culture. British journal of biomedical science 60, 79-83.

  53. 53.

    Winn W.C., Koneman E.W. 2006. Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6th ed. Lippincott Williams & Wilkins.

Download references

Acknowledgements

We thank all the patients who participated in the study, also we are grateful to Christen Rune Stensvold in Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark, for D. fragilis-positive control DNA. This study was supported by the grant given by the Scientific Research Projects Branch Directorate of Ege University, Turkey (Grant no.: 13-TIP-092).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mehmet Aykur.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by Dokuz Eylül University Clinical Research Ethics Committee (Protocol no.: 2013/16-02).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Aykur, M., Calıskan Kurt, C., Dirim Erdogan, D. et al. Investigation of Dientamoeba fragilis Prevalence and Evaluation of Sociodemographic and Clinical Features in Patients with Gastrointestinal Symptoms. Acta Parasit. 64, 162–170 (2019). https://doi.org/10.2478/s11686-018-00017-5

Download citation

Keywords

  • Dientamoeba fragilis
  • Prevalence
  • Clinical symptoms
  • Sociodemographic
  • RT-PCR