Abstract
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.
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References
Abbas MM, Zaki M, Afify NA (1996) Prevalence of Toxoplasma gondii and cytomegalovirus antibodies in patients with chronic renal failure. J Egypt Soc Parasitol 26:671–676
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):2
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):294–296
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):19–21
Athlin L, Domellöf L (1986) The phagocytic process of human peritoneal macrophages in cancer or uremia. Acta Pathol Microbiol Immunol Scand C 94(2):63–68
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):943–950
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 45:472–476
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):229–231
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):5044–5047
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):1157–1158
Fazaeli A, Carter PE, Darde ML, Pennington TH (2000) Molecular typing of Toxoplasma gondii strains by GRA6 gene sequence analysis. Int J Parasitol 30:637–642
Ferreira MS, Borges AS (2002) Some aspects of protozoan infections in immunocompromised patients: a review. Mem Inst Oswaldo Cruz 97:443–457
Fuccillo DA, Madden DL, Tzan N, Sever JL (1987) Difficulties associated with serological diagnosis of Toxoplasma gondii infection. Diagn Clin Immunol 5:8–13
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):389–393
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 423–424
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):1–7
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):519–521
Gross U (2004) Prevalence and public-health-aspects of toxoplasmosis. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 47(7):692–697
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 25:1257–1262
House A (1986) Psychosocial problems of patients on the renal unit and their relation to treatment outcome. J Psychosom Res 31(4):441–452
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 106:680–686
Jonathan H (2005) Hemodialysis complications. Am J Kidney Dis 45(6):1122–1131
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):357–365
Kaitelidou D, Ziroyanis PN, Maniadakis N, Liaropoulos L, Theodorou M (2004) The socioeconomic impact of haemodialysis. Hippokratia 8(2):81–87
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 101:619–625
Kortbeek LM, De Melker HE, Veldhuijzen IK, Conyn-Van Spaendonck MAE (2004) Population-based Toxoplasma seroprevalence study in the Netherlands. Epidemiol Infect 132:839–845
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 49:89–92
Langhoff E, Ladefoyed J (1988) In vitro immune function in patients with minor, moderate and severe kidney impairment. AMPIS 96:655–659
Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15(2):211–222
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 2858–2888
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 2:183–192
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):224–238
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):1378–1382
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 43:1570–1574
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):875–877
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):61–63
Sensini A (2006) Toxoplasma gondii infection in pregnancy: opportunities and pitfalls of serological diagnosis. Clin Microbiol Infect 12:504–512
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):134–137
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 11:11–15
Solhjoo K, Jahromi AS, Parnian-Rad A (2010) Anti-Toxoplasma gondii antibodies in haemodialysis patients. Am J Infect Dis 6(1):13–17
Subauste CS, Remington JS (1993) Immunity to Toxoplasma gondii. Curr Opin Immunol 5(4):532–537
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):265–269
Szepietowski JC, Reich A, Pacan P (2004) Psychodermatoses in haemodialysis patients. Dermatology 209(4):344
Velimirovic B (1984) Toxoplasmosis in immunosuppression and AIDS. Infection 12(5):315–317
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 19:626–634
Vonesh EF, Snyder JJ, Foley RN, Collins AJ (2004) The differential impact of risk factors on mortality in haemodialysis and peritoneal dialysis. Kidney Int 66:2389–2401
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):509–516
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):288–292
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):1550–1552
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):59–66
Acknowledgments
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.
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Saki, J., Khademvatan, S., Soltani, S. et al. Detection of toxoplasmosis in patients with end-stage renal disease by enzyme-linked immunosorbent assay and polymerase chain reaction methods. Parasitol Res 112, 163–168 (2013). https://doi.org/10.1007/s00436-012-3120-6
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DOI: https://doi.org/10.1007/s00436-012-3120-6