Toxoplasma gondii in cancer patients receiving chemotherapy: seroprevalence and interferon gamma level

  • Mona Ibrahim Ali
  • Wegdan Mohamed Abd El WahabEmail author
  • Doaa Ahmed Hamdy
  • Ahmed Hassan
Original Article


Toxoplasma gondii is an opportunistic parasite causing life-threatening diseases in immune-compromised patients. The purpose of the study is to determine the seroprevalence of Toxoplasma gondii in chemotherapy receiving cancer patients in relation to different types of malignancies, and to estimate the level of interferon gamma in Toxoplasma seropositive and seronegative cancer patients and healthy controls. Anti-Toxoplasma IgG and IgM antibodies, and interferon gamma were analyzed in 120 cancer patients receiving chemotherapy (60 having hematological malignancies and 60 with solid organ tumors) and 60 healthy controls using ELISA method. Toxoplasma (IgG and IgM) were determined in (66.7% and 9.2%) of the cancer group compared to (33.3% and 6.7%) of the control group with statistical significance only in IgG seropositivity (p < 0.001, OR = 4). Patients with hematological malignancies had higher IgG seropositivity than solid organ tumors (40% vs 26.7%). The difference between the groups was statistically significant (p = 0.002, OR = 3.5). Median level of interferon gamma was in the same range between cancer patients and control group. However, it was highly elevated in Toxoplasma seropositive (76 pg/ml) than seronegative (44.5 pg/ml) cases with statistical significance (p < 0.001). T. gondii infection remains a major threat to cancer patients and still needs proper screening, diagnosis and treatment.


Toxoplasma gondii Seroprevalence Cancer patients Interferon gamma 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Abd El Wahab WM, Shaapan RM, Hassanain MA, Elfadaly HA, Hamdy DA (2018) Toxoplasma gondii infection and associated sociodemographic and behavioral risk factors among blood donors. Asian J Epidemiol 11:52–58. CrossRefGoogle Scholar
  2. Abdel Malek RR, Wassef RM, Rizk EM, Sabry H, Tadros N, Boghdady AM (2018) Toxoplasmosis an overlooked disease: seroprevalence in cancer patients. Asian Pac J Cancer Prev 19:1987–1991. Google Scholar
  3. Abdul-Lateef HI, AL-Najar YSA, Abul Majeed NG (2012) The levels of IFN-, IL-12 and testosterone hormone in persons with toxoplasmosis. Fac Med Baghdad 54:79–82Google Scholar
  4. Abou-Bacar A, Pfaff AW, Georges S, Letscher-BruV Filisetti D, Villard O et al (2004) Role of NK cells and gamma interferon in transplacental passage of Toxoplasma gondii in a mouse model of primary infection. Infect Immune 17:1397–1401. CrossRefGoogle Scholar
  5. Alim M, Özçelik S, Özpınar N (2018) Seroprevalence of Toxoplasma gondii in patients receiving cancer treatment. Cumhur Med J 40:731–736. CrossRefGoogle Scholar
  6. Baird JR, Byrne KT, Lizotte PH, Toraya-Brown S, Scarlett UK, Alexander MP et al (2013) Immune-mediated regression of established B16F10 melanoma by intratumoral injection of attenuated Toxoplasma gondii protects against rechallenge. J Immunol 190:469–478CrossRefGoogle Scholar
  7. Baumgartner M (2011) Enforcing host cell polarity: an apicomplexan parasite strategy towards dissemination. Curr Opin Microbiol 14:436–444. CrossRefGoogle Scholar
  8. Bliss SK, Gavrilescu LC, Alcaraz A, Denkersi EY (2001) Neutrophil depletion during Toxoplasma gondii infection leads to impaired immunity and lethal systemic pathology. Infect Immune 69:4898–4905. CrossRefGoogle Scholar
  9. Carmen JC, Sinai AP (2007) Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Mol Microbiol 64:904–916. CrossRefGoogle Scholar
  10. Denkers EY, Gazzinelli RT (1998) Regulation and function of T-cell-mediated immunity during T. gondii infection. Clin Microbiol Rev 11:569–588CrossRefGoogle Scholar
  11. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3:991–998. CrossRefGoogle Scholar
  12. El Deeb HK, Salah Eldin H, Khodeer S, Allah AA (2012) Prevalence of Toxoplasma gondii infection in antenatal population in Menoufia, governorate Egypt. Acta Trop 124:185–191. CrossRefGoogle Scholar
  13. El Shazly AM, Afify EM, Morsy TA (1996) Antibodies against toxoplasma in children and adults with malignancy. J Egypt Soc Parasitol 26:781–787Google Scholar
  14. El-Geddawi OA, El-Sayad MH, Sadek NA, Hussien NA, Ahmed MA (2016) Detection of T. gondii infection in blood donors in Alexandria, Egypt, using serological and molecular strategies. J Egypt Soc Parasitol 9:24–30. Google Scholar
  15. Evering T, Weiss LM (2006) The immunology of parasite infections in immunocompromized hosts. Parasite Immunol 28:549–565. Google Scholar
  16. Ewald PW (2009) An evolutionary perspective on parasitism as a cause of cancer. Adv Parasitol 68:21–43. CrossRefGoogle Scholar
  17. Filisetti D, Candolfi E (2004) Immune response to Toxoplasma gondii. Annali dell’Istituto Superiore di Sanità 40:71–80Google Scholar
  18. Fox BA, Sanders KL, Chen S, Bzik DJ (2013) Targeting tumors with nonreplicating Toxoplasma gondii uracil auxotroph vaccines. Trends Parasitol 29:431–437. CrossRefGoogle Scholar
  19. Fox BA, Sanders KL, Rommereim LM, Guevara RB, Bzik DJ (2016) Secretion of rhoptry and dense granule effector proteins by non replicating Toxoplasma gondii uracil auxotrophs controls the development of antitumor immunity. PLoS Genet 12:e1006189. CrossRefGoogle Scholar
  20. Fox BA, Butler KL, Guevara RB, Bzik DJ (2017) Cancer therapy in a microbial bottle: uncorking the novel biology of the protozoan Toxoplasma gondii. PLoS Pathog 13:e1006523. CrossRefGoogle Scholar
  21. Gavrilescu LC, Denkers EY (2001) IFN-γ overproduction and high level apoptosis are associated with high but not low virulence Toxoplasma gondii. Infect J Immunol 167:902–909Google Scholar
  22. Halonen S (2004) Immune responses to Toxoplasma gondii in the central nervous system. In: Lindsay DS, Weiss LM (eds) opportunistic infections: Toxoplasma, Sarcocystis, and Microsporidia. Kluwer, Boston, pp 67–88. CrossRefGoogle Scholar
  23. Hassanain MA, Elfadaly HA, Abd El Wahab WM, Abo El-Maaty AM (2018) Comparative hormonal and immunoglobulin profiles of aborted women with or without toxoplasmosis. J Pregnancy Reprod 2:1–4. Google Scholar
  24. Hibbs JB, Lambert LH, Remington JS (1971) Resistance to murine tumors conferred by chronic infection with intracellular protozoa, Toxoplasma gondii and Besnoitia jellisoni. J Infect Dis 124:587–592CrossRefGoogle Scholar
  25. Huang H, Yan F, Li C, Zhao MY, Tang JW, Li XR (2000) Detection of Toxoplasma infection in women with gynaecologic neoplasms using ELISA. Chin J Parasitol Parasit Dis 18:165–166Google Scholar
  26. Hunter CA, Yu D, Gee M, Ngo CV, Sevignani C, Goldschmidt M, Golovkina TV, Evans S, Lee WF, Thomas-Tikhonenko A (2001) Cutting edge: systemic inhibition of angiogenesis underlies resistance to tumors during acute toxoplasmosis. J Immunol 166:5878–5881. CrossRefGoogle Scholar
  27. Jiang C, Li Z, Chen P, Chen L (2015) The seroprevalence of Toxoplasma gondii in Chinese population with cancer: a systematic review and meta-analysis. Medicine (Baltimore) 94:e2274. CrossRefGoogle Scholar
  28. Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP (2014) Toxoplasma gondii seroprevalence in the United States 2009–2010 and comparison with the past two decades. Am J Trop Med Hyg 90:1135–1139. CrossRefGoogle Scholar
  29. Jumaian NF (2005) Seroprevalence and risk factors for Toxoplasma infection in pregnant women in Jordan. East Mediterr Health J 11:45–51Google Scholar
  30. Kalantari N, Darabi ZA, Siadati S, Nikbakhsh N, Ghasemi M, Ghaffari T, Ghaffari S, Bayani M (2017) Detection of Toxoplasma gondii DNA in malignant breast tissues in breast cancer patients. Int J Mol Cell Med 6:190–196. Google Scholar
  31. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD (1998) Demonstration of an interferon gamma dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95:7556–7561. CrossRefGoogle Scholar
  32. Khalil HM, Makled MK, Azab ME, Abdalla HM, el Sherif EA, Nassef NS (1991) Opportunistic parasitic infections in immunocompromised hosts. J Egypt Soc Parasitol 21:657–658Google Scholar
  33. Khurana S, Dubey ML, Malla N (2005) Association of parasitic infections and cancers. Indian J Med Microbiol 23:74–79CrossRefGoogle Scholar
  34. Kojima M, Nakamura N, Murayama K, Igarashi T, Matsumoto M, Matsuda H et al (2010) Reactive lymphoid hyperplasia with giant follicles associated with a post therapeutic state of hematological malignancies. A report of eight cases. Tumori J 96:143–148CrossRefGoogle Scholar
  35. Maciel E, Siqueira I, Queiroz AC, Melo A (2000) Toxoplasma gondii myelitis in a patient with adult T-cell leukemia-lymphoma. Arq Neuropsiquiatr 58:1107–1109CrossRefGoogle Scholar
  36. Mellman I, Coukos G, Dranoff G (2011) Cancer immunotherapy comes of age. Nature 480(7378):480–489. CrossRefGoogle Scholar
  37. Mohammadi Manesh R, Hosseini Safa A, Sharafi SM, Jafari R, Bahadoran M, Yousefi M, Hamid Nasri H, Darani HY (2014) Parasites and chronic renal failure. J Renal Inj Prev 3:87–90. Google Scholar
  38. Mostafa NE, Abdel Hamed EF, Rahed HE, Mohamed SY, Abdelgawad M, Elasbali AM (2018) The relationship between toxoplasmosis and different types of human tumors. J Infect Dev Ctries 12:137–141. CrossRefGoogle Scholar
  39. Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 39:1385–1394. CrossRefGoogle Scholar
  40. Phuangphet W (2008) Toxoplasmosis: pathogenesis and immune response. Thammasat Med J 8:487Google Scholar
  41. Polat M, Kilic E, Yazar S (2012) Assessment of advanced positive oxidation product levels in Toxoplasma gondii positive individuals. J Health Sci 21:200–204Google Scholar
  42. Rai SK, Upadhyay MP, Shrestha HG (2003) Toxoplasma infection in selected patients in Kathmandu, Nepal. Nepal Med Coll J 5:89–91Google Scholar
  43. Sanad MM, Thagfan FA, Al Olayan EM, Almogren A, Al Hammaad A, Al-Mawash A et al (2014) Opportunistic coccidian parasites among Saudi cancer patients presenting with diarrhea: prevalence and immune status. Res J Parasitol 9:55–63. CrossRefGoogle Scholar
  44. Sanders KL, Fox BA, Bzik DJ (2015) Attenuated Toxoplasma gondii stimulates immunity to pancreatic cancer by manipulation of myeloid cell populations. Cancer Immunol Res 3:891–901. CrossRefGoogle Scholar
  45. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ et al (2001) IFN gamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:1107–1111. CrossRefGoogle Scholar
  46. Shen DF, Matteson DM, Tuaillon N, Suedekum BK, Buggage RR, Chan CC (2001) Involvement of apoptosis and interferon-g in murine toxoplasmosis. IOVS 42:2031–2036Google Scholar
  47. Shimelis T, Tebeje M, Tadesse E, Tegbaru B, Terefe A (2009) Sero-prevalence of latent Toxoplasma gondii infection among HIV-infected and HIV-uninfected people in Addis Ababa Ethiopia: a comparative cross-sectional study. BMC Res Notes 2:213. CrossRefGoogle Scholar
  48. Shin DW, Cha DY, Hua QJ, Cha G, Lee Y (2009) Seroprevalence of Toxoplasma gondii infection and characteristics of seropositive patients in general hospitals in Daejeon, Korea. Korean J Parasitol 47:125–130. CrossRefGoogle Scholar
  49. Street SE, Trapani JA, MacGregor D, Smyth MJ (2002) Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J Exp Med 196:129–134CrossRefGoogle Scholar
  50. Suzuki Y, Sa Q, Gehman M, Ochiai E (2012) Interferon-gamma- and perforin-mediated immune responses for resistance in the brain against Toxoplasma gondii. Expert Rev Mol Med 13:e31. CrossRefGoogle Scholar
  51. Walle F, Kebede N, Tsegaye A, Kassa T (2013) Seroprevalence and risk factors for toxoplasmosis in HIV infected and non-infected individuals in Bahir Dar, Northwest Ethiopia. Parasit Vectors 6:15. CrossRefGoogle Scholar
  52. Wang B, Pan X, Yin Y, Weng XH (2000) Investigation of anti-Toxoplasma gondii antibodies in immunodeficient patients. Chin J Parasitol Parasit Dis 18:224–226Google Scholar
  53. Wang L, He LY, Meng DD, Chen ZW, Wen H, Fang GS (2015) Seroprevalence and genetic characterization of Toxoplasma gondii in cancer patients in Anhui Province, Eastern China. Parasit Vectors 15:162. CrossRefGoogle Scholar
  54. Wang ZD, Liu HH, Ma ZX, Ma HY, Li ZY, Yang ZB et al (2017) Toxoplasma gondii infection in immunocompromised patients: a systematic review and meta-analysis. Front Microbiol 8:389. Google Scholar
  55. Yazar S, Yaman O, Eser B, Altuntas F, Kurnaz F, Sahin I (2004) Investigation of anti- toxoplasma gondii antibodies in patients with neoplasia. J Med Microbiol 53:1183–1186. CrossRefGoogle Scholar
  56. Young JD, McGwire BS (2005) Infliximab and reactivation of cerebral toxoplasmosis. N Engl J Med 353:1530–1531. CrossRefGoogle Scholar

Copyright information

© Indian Society for Parasitology 2019

Authors and Affiliations

  1. 1.Department of Medical Parasitology, College of MedicineBeni-Suef UniversityBeni-SuefEgypt
  2. 2.Department of Oncology, College of MedicineBeni-Suef UniversityBeni-SuefEgypt

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