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Parasitology Research

, Volume 117, Issue 12, pp 3715–3723 | Cite as

Intestinal helminths and protozoan infections in patients with colorectal cancer: prevalence and possible association with cancer pathogenesis

  • Abdurakhim Toychiev
  • Sulayman Abdujapparov
  • Alim Imamov
  • Behzod Navruzov
  • Nikolay Davis
  • Najiya Badalova
  • Svetlana Osipova
Original Paper

Abstract

The purpose of the present study was to determine the prevalence of intestinal helminths and protozoa in colorectal cancer (CRC) patients and to evaluate the possible association between the prevalence and CRC pathogenesis. A total of 200 CRC patients and 200 residents of Tashkent, who had no complaints related to the gastrointestinal tract, were examined by triple coproscopy using a concentration method and estimations of protozoan infection intensity. Of the CRC patients tested, 144 were classified as T1-4N0M0 (without metastases) and 56 were classified as T1–4N1–2M0–1 (with metastases). Parasitological examination was performed during CRC diagnosis before and after surgery and chemotherapy. A significantly higher prevalence of Blastocystis sp., Chilomastix mesnili, Jodamoeba butschlii, and Endolimax nana was found in CRC patients than in the control population (p < 0.0001), amounting to 80, 20, 22.5, and 11.5%, respectively. The high prevalence of Blastocystis sp., as well as the patterns of infection intensity, was stable at all stages of examination. The ratio of the number of CRC patients with and without Blastocystis sp. in the T1–4N0M0 and T1–4N1–2M0–1 groups amounted to 3.3 and 7.0, respectively. The ratios for C. mesnili, E. coli, J. butschlii, and E. nana in both groups were 0.2 and 0.2, 0.07 and 0.07, 0.3 and 0.16, and 0.18 and 0.01, respectively. The prevalence of helminths and Giardia lamblia in CRC patients and the control population was not significantly different. Taken together, these data indicate a possible role for Blastocystis sp. in CRC pathogenesis. Diagnosis, treatment, and further observation of patients with Blastocystis sp. are necessary at all stages of CRC, including during diagnosis and before and after surgery and chemotherapy.

Keywords

Colorectal cancer Blastocystis sp. Intestinal helminths Protozoan infections CRC 

Notes

Funding

Funding was provided by the Ministry of Public Health of the Republic of Uzbekistan (ADCC 15.21.2). The Ministry of Public Health of the Republic of Uzbekistan had no role in the design of the study or in any aspect of conducting the study (the collection, management, analysis, and interpretation of the data or the preparation, review, or approval of the manuscript).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics statement

The study was approved by the Medical Ethics Committee of the Ministry of Health of the Republic of Uzbekistan in accordance with the Declaration of Helsinki (World Medical Association 2013). The trial is registered at the US National Institutes of Health (ClinicalTrials.gov) #NCT03173001. Both informed and written consents were obtained from the patients and controls.

Supplementary material

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References

  1. Aranzamendi C, Fransen F, Langelaar M, Franssen F, van der Ley P, van Putten JP et al (2012) Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro. Parasite Immunol 34:210–223CrossRefGoogle Scholar
  2. Brindley PJ, da Costa JM, Sripa B (2015) Why does infection with some helminthes cause cancer? Trends Cancer 1(3):174–182CrossRefGoogle Scholar
  3. Buquéa A, Bloy N, Aranda F, Castoldi F, Eggermont A, Cremer I et al (2015) Trial watch: immunomodulatory monoclonal antibodies for oncological indications. Oncoimmunology 4(4):e1008814CrossRefGoogle Scholar
  4. Chan KH, Chandramathi S, Suresh K, Chua KH, Kuppusamy UR (2012) Effects of symptomatic and asymptomatic isolates of Blastocystis hominis on colorectal cancer cell line, HCT116. Parasitol Res 110(6):2475–2480CrossRefGoogle Scholar
  5. Chandramathi S, Suresh K (2010) Solubilized antigen of Blastocystis hominis facilitates the growth of human colorectal cancer cells, HCT116. Parasitol Res 106(4):941–945CrossRefGoogle Scholar
  6. Chandramathi S, Suresh K, Anita ZB, Kuppusamy UR (2012) Infections of Blastocystis hominis and microsporidia in cancer patients: are they opportunistic? Trans R Soc Trop Med Hyg 106(4):267–269CrossRefGoogle Scholar
  7. Coleman O, Nunes T (2016) Role of the microbiota in colorectal Cancer: updates on microbial associations and therapeutic implications. Biores Open Access 5(1):279–288CrossRefGoogle Scholar
  8. Devera R, Azacon B, Jiménez M (1998) Blastocystis hominis in patients at the Ruiz y Paez University hospital from Bolivar City, Venezuela. Bol Chil Parasitol 53(3–4):65–70PubMedGoogle Scholar
  9. Edge SB, Compton CC (2010) The American joint committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17(6):1471–1474CrossRefGoogle Scholar
  10. Favoriti P, Carbone G, Greco M, Pirozzi F, Pirozzi RE, Corcione F (2016) Worldwide burden of colorectal cancer: a review. Updat Surg 68(1):7–11CrossRefGoogle Scholar
  11. Fukugaiti MH, Ignacio A, Fernandes MR, Ribeiro U Jr, Nakano V, Avila-Campos MJ (2015) High occurrence of fusobacterium nucleatum and Clostridium difficile in the intestinal microbiota of colorectal carcinoma patients. Braz J Microbiol 46(4):1135–1140CrossRefGoogle Scholar
  12. Hamilton SR, Aaltonen LA (2000) World Health Organization classification of Tumours. Pathology and genetics of Tumours of the digestive system. In: Hamilton SR, Rubio CA et al (eds) Chapter 6. Tumours of the Colon and Rectum. IARC Press, Lyon, pp 101–117Google Scholar
  13. Hogan BV, Peter MB, Shenoy HG, Horgan K, Hughes TA (2011) Surgery induced immunosuppression. Surgeon 9(1):38–43CrossRefGoogle Scholar
  14. Horiki N, Kaneda Y, Maruyama M, Fujita Y, Tachibana H (1999) Intestinal blockage by carcinoma and Blastocystis hominis infection. Am J Trop Med Hyg 60(3):400–402CrossRefGoogle Scholar
  15. Hou N, Zhang X, Zhao L, Zhao X, Li Z, Song T (2013) A novel chronic stress-induced shift in the Th1 to Th2-response promotes colon cancer growth. Biochem Biophys Res Commun 439(4):471–476CrossRefGoogle Scholar
  16. Kumarasamy V, Roslani AC, Rani KU, Kumar Govind S (2014) Advantage of using colonic washouts for Blastocystis detection in colorectal cancer patients. Parasit Vectors 7:162CrossRefGoogle Scholar
  17. Kumarasamy V, Kuppusamy UR, Jayalakshmi P, Samudi C, Ragavan ND, Kumar S (2017) Exacerbation of colon carcinogenesis by Blastocystis sp. PLoS One 12(8):e0183097CrossRefGoogle Scholar
  18. Landman C, Quevrain E (2016) Gut microbiota: description, role and pathophysiological implication. Rev Med Interne 37(6):418–423CrossRefGoogle Scholar
  19. Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA (2014) Chronic inflammation and cytokines in tumor microenvironment. J Immunol Res 2014:149185CrossRefGoogle Scholar
  20. Ling A, Lundberg IV, Eklof V, Wikberg ML, Oberg A, Edin S et al (2015) The infiltration, and prognostic importance, of Th1 lymphocytes vary in molecular subgroups of colorectal cancer. J Pathol Clin Res 2(1):21–31CrossRefGoogle Scholar
  21. Lopez-Romero G, Quintero J, Astiazaran-Garcia H, Velazquez C (2015) Host defense against Giardia lamblia. Parasite Immunol 37(8):394–406CrossRefGoogle Scholar
  22. Maizels RM, Hewitson JP, Smith KA (2012) Susceptibility and immunity to helminth parasites. Curr Opin Immunol 24:459–466CrossRefGoogle Scholar
  23. Massacand JC, Stettler RC, Meier R, Humphreys NE, Grencis RK, Marsland BJ, Harris NL (2009) Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc Natl Acad Sci U S A 106:13968–13973CrossRefGoogle Scholar
  24. Mohamed AM, Ahmed MA, Ahmed SA, Al-Semany SA, Alghamdi SS, Zaglool DA (2017) Predominance and association risk of Blastocystis hominis subtype I in colorectal cancer: a case control study. Infect Agents Cancer 12:21CrossRefGoogle Scholar
  25. Müller J, Sidler D, Nachbur U, Wastling J, Brunner T, Hemphill A (2008) Thiazolides inhibit growth and induce glutathione-S-transferase pi (GSTP1)-dependent cell death in human colon cancer cells. Int J Cancer 123(8):1797–1806CrossRefGoogle Scholar
  26. O'Connell JB, Maggard MA, Liu JH, Etzioni DA, Ko CY (2004) Are survival rates different for young and older patients with rectal cancer? Dis Colon Rectum 47(12):2064–2069CrossRefGoogle Scholar
  27. Panczyk M (2014) Pharmacogenetics research on chemotherapy resistance in colorectal cancer over the last 20 years. World J Gastroenterol 20(29):9775–9827CrossRefGoogle Scholar
  28. Peterson MR, Weidner N (2011) Gastrointestinal neoplasia associated with bowel Parasitosis: real or imaginary? J Trop Med 2011:234254CrossRefGoogle Scholar
  29. Rasti S, Hassanzadeh M, Hooshyar H, Momen-Heravi M, Mousavi SGA, Abdoli A (2017) Intestinal parasitic infections in different groups of immunocompromised patients in Kashan and Qom cities, central Iran. Scand J Gastroenterol 52(6–7):738–741CrossRefGoogle Scholar
  30. Senkowski W, Zhang X, Olofsson MH, Isacson R, Höglund U, Gustafsson M, Nygren P, Linder S, Larsson R, Fryknäs M (2015) Three-dimensional cell culture-based screening identifies the anthelmintic drug Nitazoxanide as a candidate for treatment of colorectal Cancer. Mol Cancer Ther 14(6):1504–1516CrossRefGoogle Scholar
  31. Sharp SP, Avram D, Stain SC, Lee EC (2017) Local and systemic Th17 immune response associated with advanced stage colon cancer. J Surg Res 208:180–186CrossRefGoogle Scholar
  32. Siegel RS, Ward EM, Jemal A (2012) Trends in colorectal Cancer incidence rates in the United States by tumor location and stage, 1992–2008. Cancer Epidemiol Biomark Prev 21(3):411–416CrossRefGoogle Scholar
  33. Steer H (2007) Blastocystis hominis and colorectal cancer. Ann R Coll Surg Engl 89(5):539CrossRefGoogle Scholar
  34. Taşova Y, Sahin B, Koltaş S, Paydaş S (2000) Clinical significance and frequency of Blastocystis hominis in Turkish patients with hematological malignancy. Acta Med Okayama 54(3):133–136PubMedGoogle Scholar
  35. Triantafillidis JK, Nasioulas G, Kosmidis PA (2009) Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res 29:2727–2737PubMedGoogle Scholar
  36. Truant AL, Elliott SH, Kelly MT, Smith JH (1981) Comparison of formalin-ethyl ether sedimentation, formalin-ethyl acetate sedimentation, and zinc sulfate flotation techniques for detection of intestinal parasites. J Clin Microbiol 13(5):882–884PubMedPubMedCentralGoogle Scholar
  37. Walsh KP, Brady MT, Finlay CM, Boon L, Mills KH (2009) Infection with a helminth parasite attenuates autoimmunity through TGF-β-mediated suppression of Th17 and Th1 responses. J Immunol 183:1577–1586CrossRefGoogle Scholar
  38. Wang X, Huycke MM (2015) Colorectal cancer: role commensal bacteria and bystander effects. Gut Microbes 6:370–376CrossRefGoogle Scholar
  39. WorldMedicalAssociation (2013) World medical association declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310(20):2191–2194CrossRefGoogle Scholar
  40. Yersal O, Malatyali E, Ertabaklar H, Oktay E, Barutca S, Ertug S (2016) Blastocystis subtypes in cancer patients: analysis of possible risk factors and clinical characteristics. Parasitol Int 65(6 Pt B):792–796CrossRefGoogle Scholar
  41. Yu YN, Yu TC, Zhao HJ, Sun TT, Chen HM, Chen HY, An HF, Weng YR, Yu J, Li M, Qin WX, Ma X, Shen N, Hong J, Fang JY (2015) Berberine may rescue fusobacterium nucleatum-induced colorectal tumorogenesis by modulating the tum0or microenvironment. Oncotarget 6(31):32013–32026CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Immunology of Parasitic DiseasesThe Research Institute of Epidemiology, Microbiology and Infectious DiseasesTashkentUzbekistan
  2. 2.Department of ColoproctologyThe Research Center of OncologyTashkentUzbekistan
  3. 3.Department of ChemotherapyThe Research Center of OncologyTashkentUzbekistan
  4. 4.Department of SurgeryTashkent Medical AcademyTashkentUzbekistan

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