Parasitology Research

, Volume 112, Issue 1, pp 163–168 | Cite as

Detection of toxoplasmosis in patients with end-stage renal disease by enzyme-linked immunosorbent assay and polymerase chain reaction methods

  • J. Saki
  • S. KhademvatanEmail author
  • S. Soltani
  • H. Shahbazian
Original Paper


Toxoplasmosis caused by Toxoplasma gondii is an opportunistic infection. In healthy individuals, the infection is largely asymptomatic, but in immunocompromised people the parasite can become widely disseminated, causing severe toxoplasmosis. In patients undergoing haemodialysis, the phagocytic process shows a highly significant impairment. Therefore, this study aimed to investigate toxoplasmosis in patients with end-stage renal disease (ESRD) undergoing haemodialysis in Ahvaz hospitals, southwest of Iran. A total of 280 patients and 100 healthy subjects participated in this study. The presence of serum IgM and IgG antibodies against T. gondii was detected by ELISA and the presence of Toxoplasma parasites in whole blood was evaluated by GRA6 PCR. Anti-T. gondii IgG antibodies were detected in 82 (29.3 %) haemodialysis patients and 26 (26 %) controls. In addition, anti-T. gondii IgM antibodies were detected in 7.9 % of patients and in 4 % of controls. For both the antibodies, the differences were statistically significant (P < 0.05). PCR was performed with DNA extracted from blood samples of all patients and controls. PCR gave positive results with four of the 280 blood samples from patients but none for the control blood samples. The results revealed a high percentage of positivity for Toxoplasma antibodies in patients with ESRD undergoing haemodialysis and also confirmed the parasite in whole blood, indicating disseminated infection in these patients. Patients undergoing dialysis have a higher rate of active infection with Toxoplasma likely due to reactivation of a chronic infection. Thus, parasitological examinations of ESRD patients should be periodically carried out for monitoring and evaluating the possible dissemination of toxoplasmosis during haemodialysis.


Haemodialysis Patient Toxoplasmosis ESRD Patient Toxoplasmic Encephalitis GRA6 Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study originates from the thesis of Mrs. Shahrzad Soltani, an MSc student of medical parasitology, granted by the Ahvaz Jundishapur University of Medical Science and approved in the ethical committee (code no. CMRC-41). The authors would like to thank Rahman Abdizadeh for kindly providing us with Toxoplasma tachyzoites and all managers and staff of the hospitals in Ahvaz for their valuable collaboration. The authors declare that they have no conflicts of interest.


  1. Abbas MM, Zaki M, Afify NA (1996) Prevalence of Toxoplasma gondii and cytomegalovirus antibodies in patients with chronic renal failure. J Egypt Soc Parasitol 26:671–676PubMedGoogle Scholar
  2. Alfonso Y, Fraga J, Fonseca C, Jiménez N, Pinillos T, Dorta-Contreras AJ, Cox R, Capó V, Pomier O, Bandera F, Ginorio D (2009) Molecular diagnosis of Toxoplasma gondii infection in cerebrospinal fluid from AIDS patients. Cerebrospinal Fluid Res 6(1):2PubMedCrossRefGoogle Scholar
  3. Alonso R, Martínez E, Laynez P, Miguélez M, Piñero JE, Valladares B (2002) Detection by nested-PCR of Toxoplasma gondii in patients infected with human immunodeficiency virus. Med Clin (Barc) 118(8):294–296Google Scholar
  4. Assmar M, Amirkhani A, Piazak N, Hovanesian A, Kooloobandi A, Etessami R (1997) Toxoplasmosis in Iran. Results of a seroepidemiological study. Bull Soc Pathol Exot 90(1):19–21PubMedGoogle Scholar
  5. Athlin L, Domellöf L (1986) The phagocytic process of human peritoneal macrophages in cancer or uremia. Acta Pathol Microbiol Immunol Scand C 94(2):63–68PubMedGoogle Scholar
  6. Aufy SM, Mahgoub AM, Saadi MG, Adel Elmallawany M (2009) Serological detection of Toxoplasma gondii in chronic renal failure patients and renal transplant recipients. J Egypt Soc Parasitol 39(3):943–950PubMedGoogle Scholar
  7. Cingolani A, De Luca A, Ammassari A, Murri R, Linzalone A, Grillo R, Antinori A (1996) PCR detection of Toxoplasma gondii DNA in CSF for the differential diagnosis of AIDS-related focal brain lesions. J Med Microbiol 45:472–476PubMedCrossRefGoogle Scholar
  8. Coelho RA, Kobayashi M, Carvalho LB Jr (2003) Prevalence of IgG antibodies specific to Toxoplasma gondii among blood donors in Recife, Northeast Brazil. Rev Inst Med Trop Sao Paulo 45(4):229–231PubMedCrossRefGoogle Scholar
  9. Colombo FA, Vidal JE, Penalva de Oliveira AC, Hernandez AV, Bonasser-Filho F, Nogueira RS, Focaccia R, Pereira-Chioccola VL (2005) Diagnosis of cerebral toxoplasmosis in AIDS patients in Brazil: importance of molecular and immunological methods using peripheral blood samples. J Clin Microbiol 43(10):5044–5047PubMedCrossRefGoogle Scholar
  10. Fan CK, Hung CC, Su KE, Chiou HY, Gil V, Ferreira Mda C, Tseng LF (2007) Seroprevalence of Toxoplasma gondii infection among inhabitants in the Democratic Republic of Sao Tome and Principe. Trans R Soc Trop Med Hyg 101(11):1157–1158PubMedCrossRefGoogle Scholar
  11. Fazaeli A, Carter PE, Darde ML, Pennington TH (2000) Molecular typing of Toxoplasma gondii strains by GRA6 gene sequence analysis. Int J Parasitol 30:637–642PubMedCrossRefGoogle Scholar
  12. Ferreira MS, Borges AS (2002) Some aspects of protozoan infections in immunocompromised patients: a review. Mem Inst Oswaldo Cruz 97:443–457PubMedCrossRefGoogle Scholar
  13. Fuccillo DA, Madden DL, Tzan N, Sever JL (1987) Difficulties associated with serological diagnosis of Toxoplasma gondii infection. Diagn Clin Immunol 5:8–13PubMedGoogle Scholar
  14. Gallino A, Maggiorini M, Kiowski W, Martin X, Wunderli W, Schneider J, Turina M, Follath F (1996) Toxoplasmosis in heart transplant recipients. Eur J Cli Microbiol Infect Dis 15(5):389–393CrossRefGoogle Scholar
  15. Garcia SL, Bruckner AD (1997) Parasitic infections in the compromised host (Toxoplasma gondii). In: Garcia SL, Bruckner AD (eds) Diagnostic medical parasitology. American Society for Microbiology, Washington DC, pp 423–424Google Scholar
  16. Gharavi MJ, Jalali S, Khademvatan S, Heydari S (2011) Detection of IgM and IgG anti-Toxoplasma antibodies in renal transplant recipients using ELFA, ELISA and ISAGA methods: comparison of pre- and posttransplantation status. Ann Trop Med Parasitol 105(5):1–7CrossRefGoogle Scholar
  17. Grant IH, Gold JW, Rosenblum M, Niedzwiecki D, Armstrong D (1990) Toxoplasma gondii serology in HIV-infected patients: the development of central nervous system toxoplasmosis in AIDS. AIDS 4(6):519–521PubMedCrossRefGoogle Scholar
  18. Gross U (2004) Prevalence and public-health-aspects of toxoplasmosis. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 47(7):692–697PubMedGoogle Scholar
  19. Held TK, Krüger D, Switala AR, Beyer J, Kingreen D, Busemann C, Janitschke K, Siegert W (2000) Diagnosis of toxoplasmosis in bone marrow transplant recipients: comparison of PCR-based results and immunohistochemistry. Bone Marrow Transplant 25:1257–1262PubMedCrossRefGoogle Scholar
  20. House A (1986) Psychosocial problems of patients on the renal unit and their relation to treatment outcome. J Psychosom Res 31(4):441–452CrossRefGoogle Scholar
  21. Jenum PA, Holberg-Petersen M, Melby KK, Stray-Pedersen B (1998) Diagnosis of congenital Toxoplasma gondii infection by polymerase chain reaction (PCR) on amniotic fluid samples. The Norwegian experience. APMIS 106:680–686PubMedCrossRefGoogle Scholar
  22. Jonathan H (2005) Hemodialysis complications. Am J Kidney Dis 45(6):1122–1131CrossRefGoogle Scholar
  23. Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB (2002) Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol 154(4):357–365CrossRefGoogle Scholar
  24. Kaitelidou D, Ziroyanis PN, Maniadakis N, Liaropoulos L, Theodorou M (2004) The socioeconomic impact of haemodialysis. Hippokratia 8(2):81–87Google Scholar
  25. Kompalic-Cristo A, Frotta C, Suárez-Mutis M, Fernandes O, Britto C (2007) Evaluation of a real-time PCR assay based on the repetitive B1 gene for the detection of Toxoplasma gondii in human peripheral blood. Parasitol Res 101:619–625PubMedCrossRefGoogle Scholar
  26. Kortbeek LM, De Melker HE, Veldhuijzen IK, Conyn-Van Spaendonck MAE (2004) Population-based Toxoplasma seroprevalence study in the Netherlands. Epidemiol Infect 132:839–845PubMedCrossRefGoogle Scholar
  27. Lamoril J, Molina JM, de Gouvello A, Garin YJ, Deybach JC, Modaï J, Derouin F (1996) Detection by PCR of Toxoplasma gondii in blood in the diagnosis of cerebral toxoplasmosis in patients with AIDS I. Clin Pathol 49:89–92CrossRefGoogle Scholar
  28. Langhoff E, Ladefoyed J (1988) In vitro immune function in patients with minor, moderate and severe kidney impairment. AMPIS 96:655–659Google Scholar
  29. Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15(2):211–222PubMedCrossRefGoogle Scholar
  30. Montoya JG, Remington JS (2000) Toxoplasma gondii. In: Mandell GL, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases. Churchill Livingstone pp, Philadelphia, pp 2858–2888Google Scholar
  31. Nafar M, Mousavi SM, Mahdavi-Mazdeh M, Pour-Reza-Gholi F, Firoozan A, Einollahi B, Lessan-Pezeshki ML, Asbaghi-Namini S, Farrokhi F (2008) Burden of chronic kidney disease in Iran: a screening program is of essential need. Iran J Kidney Dis 2:183–192PubMedGoogle Scholar
  32. Navia BA, Petito CK, Gold JWM, Cho ES, Jordon BD, Price JW (1986) Cerebral toxoplasmosis complicating the acquired immune deficiency syndrome: clinical and neuropathological findings in 27 patients. Ann Neurol 19(3):224–238PubMedCrossRefGoogle Scholar
  33. Ocak S, Duran N, Eskiocak AF, Aytac H (2005) Anti-Toxoplasma gondii antibodies in hemodialysis patients receiving long-term hemodialysis therapy in Turkey. Saudi Med J 26(9):1378–1382PubMedGoogle Scholar
  34. Petersen E, Borobio MV, Guy E, Liesenfeld O, Meroni V, Naessens A, Spranzi E, Thulliez P (2005) European multicenter study of the LIAISON automated diagnostic system for determination of Toxoplasma gondii-specific immunoglobulin G (IgG) and IgM and the IgG avidity index. J Clin Microbiol 43:1570–1574PubMedCrossRefGoogle Scholar
  35. Punda-Polić V, Tonkić M, Capkun V (2000) Prevalence of antibodies to Toxoplasma gondii in the female population of the County of Split Dalmatia, Croatia. Eur J Epidemiol 16(9):875–877PubMedCrossRefGoogle Scholar
  36. Salahi-Moghaddam A, Hafizi A (2009) A serological study on Toxoplasma gondii infection among people in south of Tehran, Iran. Korean J Parasitol 47(1):61–63PubMedCrossRefGoogle Scholar
  37. Sensini A (2006) Toxoplasma gondii infection in pregnancy: opportunities and pitfalls of serological diagnosis. Clin Microbiol Infect 12:504–512PubMedCrossRefGoogle Scholar
  38. Sharif M, Ajami A, Daryani A, Ziaei H, Khalilian A (2006) Serological survey of toxoplasmosis in women referred to medical health laboratory before marriage, Northern Iran, 2003–2004. Int J Mol Med Adv Sci 2(2):134–137Google Scholar
  39. Silva MT, Araújo A (2005) Highly active antiretroviral therapy access and neurological complications of human immunodeficiency virus infection: impact versus resources in Brazil. J Neurovirol 11:11–15PubMedCrossRefGoogle Scholar
  40. Solhjoo K, Jahromi AS, Parnian-Rad A (2010) Anti-Toxoplasma gondii antibodies in haemodialysis patients. Am J Infect Dis 6(1):13–17CrossRefGoogle Scholar
  41. Subauste CS, Remington JS (1993) Immunity to Toxoplasma gondii. Curr Opin Immunol 5(4):532–537PubMedCrossRefGoogle Scholar
  42. Sulowicz W, Hanicki Z, Chichocki T, Zembala M, Ruggiero I, Uracz W (1991) Functional characteristics of peritoneal macrophages of renal failure patients on peritoneal dialysis. Perit Dial Int 11(3):265–269PubMedGoogle Scholar
  43. Szepietowski JC, Reich A, Pacan P (2004) Psychodermatoses in haemodialysis patients. Dermatology 209(4):344PubMedCrossRefGoogle Scholar
  44. Velimirovic B (1984) Toxoplasmosis in immunosuppression and AIDS. Infection 12(5):315–317PubMedCrossRefGoogle Scholar
  45. Vidal JE, Hernandez AV, de Oliveira AC, Dauar RF, Barbosa SP Jr, Focaccia R (2005) Cerebral toxoplasmosis in HIV-positive patients in Brazil: clinical features and predictors of treatment response in the HAART era. AIDS Patient Care STDS 19:626–634PubMedCrossRefGoogle Scholar
  46. Vonesh EF, Snyder JJ, Foley RN, Collins AJ (2004) The differential impact of risk factors on mortality in haemodialysis and peritoneal dialysis. Kidney Int 66:2389–2401PubMedCrossRefGoogle Scholar
  47. Wanke C, Tuazon CU, Kovacs A (1987) Toxoplasma encephalitis in patients with acquired immune deficiency syndrome: diagnosis and response to therapy. AmJTrop Med Hyg 36(3):509–516Google Scholar
  48. Yazar S, Demirtaş F, Yalçin S, Yaman O, Tokgöz B, Utaş C, Sahin I (2003) Anti-Toxoplama gondii antibodies in haemodialysis patients with chronic renal failure. Yonsei Med J 44(2):288–292PubMedGoogle Scholar
  49. Youssefi MR, Sefidgar AA, Mostafazadeh A, Omran SM (2007) Serologic evaluation of toxoplasmosis in matrimonial women in Babol Iran. Pak J Biol Sci 10(9):1550–1552PubMedCrossRefGoogle Scholar
  50. Zangerle R, Allerberger F, Pohl P, Fritsch P, Dierich MP (1991) High risk of developing toxoplasmic encephalitis in AIDS patients seropositive to Toxoplasma gondii. Med Microbiol Immunol (Berl) 180(2):59–66CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • J. Saki
    • 1
  • S. Khademvatan
    • 1
    • 2
    Email author
  • S. Soltani
    • 1
  • H. Shahbazian
    • 3
  1. 1.Department of Medical ParasitologyAhvaz Jundishapur University of Medical SciencesAhvazIran
  2. 2.Cellular and Molecular Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran
  3. 3.Department of Nephrology, Golestan Hospital and Diabetes Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran

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