Skip to main content

Advertisement

SpringerLink
Log in

Seroepidemiology and Associated Risk Factors of Toxoplasma gondii in Hemodialysis Patients

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Immunocompromised patients may be at risk for reactivation of the toxoplasmosis infection, because of defection in cell-mediated immunity. Therefore, early diagnosis would be highly desirable in these individuals. This case–control study was designed to increase information about toxoplasmosis in hemodialysis (HD) patients in Guilan province, Iran.

Methods

The study was performed among 150 patients and 150 controls referred to hospitals of Guilan University of Medical Sciences during 2018–2019. Questionnaire forms, including demographic and epidemiological information, were completed. Peripheral blood samples were taken for serum separation and were collected into tubes and then kept at − 20 °C until use. IgG and IgM antibodies to Toxoplasma gondii were detected by a commercial ELISA kit. Accordingly, IgG absorbance levels < 9 were considered negative, 9–11 was considered borderline, and > 11 was positive; IgM absorbance levels < 0.9 were considered negative, 0.9–1.1 was assumed to be borderline, and > 1.1 was positive.

Results

Throughout the study, 72.0% of HD patients and 64.7% of the control group were positive for anti-Toxoplasma IgG antibody subsequently. 2% of HD patients and 0.7% of the control group were positive for anti-Toxoplasma IgM antibody and these difference weren’t significant between control and ones with HD (P > 0.05). There was no significant difference between dialysis duration factor and the seropositivity rate. Seroprevalence of T. gondii infection did not vary significantly with age, educational level, residence and presence of a cat at home. On the contrary, seroprevalence varied significantly with gender and consumption of raw vegetables.

Conclusion

Because of the high percentage of positivity for Toxoplasma IgG antibodies in hemodialysis patients, we suggest a periodically screening program to carry out for monitoring and evaluating the possible dissemination of toxoplasmosis during hemodialysis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Nahnoush RK, Youssif EM, Hassanin OM (2016) Detection of toxoplasmosis in hemodialysis Egyptian patients using serological and molecular techniques. Aust J Basic Appl Sci 10:197–201

    Google Scholar 

  2. Velimirovic B (1984) Toxoplasmosis in immunosuppression and AIDS. Infection 12:315–317. https://doi.org/10.1007/BF01651143

    Article  CAS  PubMed  Google Scholar 

  3. Wanke C, Tuazon CU, Kovacs A, Dina T, Davis DO, Barton N et al (1987) Toxoplasma encephalitis in patients with acquired immune deficiency syndrome: diagnosis and response to therapy. Am J Trop Med Hyg 36:509–516. https://doi.org/10.4269/ajtmh.1987.36.509

    Article  CAS  PubMed  Google Scholar 

  4. Gallino A, Maggiorini M, Kiowski W, Martin X, Wunderli W, Schneider J et al (1996) Toxoplasmosis in heart transplant recipients. Eur J Clin Microbiol Infect Dis 15:389–393. https://doi.org/10.1007/BF01690095

    Article  CAS  PubMed  Google Scholar 

  5. 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 2:134–137. https://medwelljournals.com/abstract/?doi=ijmmas.2006.134.137

    Google Scholar 

  6. Saki J, Mohammadpour N, Moramezi F, Khademvatan S (2015) Seroprevalence of Toxoplasma gondii in women who have aborted in comparison with the women with normal delivery in Ahvaz, southwest of Iran. Sci World J 2015:764369. https://doi.org/10.1155/2015/764369

    Article  CAS  Google Scholar 

  7. Khademvatan S, Saki J, Khajeddin N, Izadi-Mazidi M, Beladi R, Shafiee B et al (2014) Toxoplasma gondii exposure and the risk of schizophrenia. Jundishapur J Microbiol 7(11):e12776. https://doi.org/10.5812/jjm.18789

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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 post-transplantation status. Ann Trop Med Parasitol 105(5):367–371. https://doi.org/10.1179/1364859411Y.0000000022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rezavand B, Poornaki AM, Mokhtari KR, Mohammad A, Andalibian A, Abdi J (2016) Identification and determination of the prevalence of Toxoplasma gondii in patients with chronic renal failure by ELISA and PCR. Asian Pac J Trop Dis 6(5):347–349. https://doi.org/10.1016/S2222-1808(15)61044-1

    Article  CAS  Google Scholar 

  10. Nissapatorn V, Leong TH, Lee R, Init-Ithoi IJ, Yen TS (2011) Seroepidemiology of toxoplasmosis in renal patients. Southeast Asian J Trop Med Public Health 42:237–247

    PubMed  Google Scholar 

  11. Alvarado-Esquivel C, Liesenfeld O, Torres-Castorena A, Estrada-Martínez S, Urbina-Alvarez JD, Ramos-de la Rocha M et al (2010) Seroepidemiology of Toxoplasma gondii infection in patients with vision and hearing impairments, cancer, HIV, or undergoing hemodialysis in Durango, Mexico. J Parasitol 96:505–508. https://doi.org/10.1645/GE-2378.1

    Article  CAS  PubMed  Google Scholar 

  12. Foroutan M, Rostami A, Majidiani H, Riahi SM, Khazaei S, Badri M et al (2018) A systematic review and meta-analysis of the prevalence of toxoplasmosis in hemodialysis patients in Iran. Epidemiol Health 40:e2018016. https://doi.org/10.4178/epih.e2018016

    Article  PubMed  PubMed Central  Google Scholar 

  13. Arefkhah N, Hosseini SA, Karimzade R, Moshfe A, Hadinia F, Larki RA et al (2019) Seroprevalence and risk factors of Toxoplasma gondii infection among cancer and hemodialysis patients in southwest Iran. Clin Epidemiol Glob Health 7:596–599. https://doi.org/10.1016/j.cegh.2019.01.007

    Article  Google Scholar 

  14. Saki J, Khademvatan S, Soltani S, Shahbazian H (2013) 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. https://doi.org/10.1007/s00436-012-3120-6

    Article  CAS  PubMed  Google Scholar 

  15. Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios CIS (2007) Basic science and dialysis: disturbances of acquired immunity in hemodialysis patients. Semin Dial 20:440–451. https://doi.org/10.1111/j.1525-139X.2007.00283.x

    Article  PubMed  Google Scholar 

  16. Sasai M, Pradipta A, Yamamoto M (2018) Host immune responses to Toxoplasma gondii. Int Immunol 10(30):113–119. https://doi.org/10.1093/intimm/dxy004

    Article  CAS  Google Scholar 

  17. Ferreira MS, Borges AS (2002) Some aspects of protozoan infections in mmunocompromised patients: a review. Memórias do Instituto Oswaldo Cruz 97:443–457. https://doi.org/10.1590/s0074-02762002000400001

    Article  PubMed  Google Scholar 

  18. Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15:211–222. https://doi.org/10.1093/clinids/15.2.211

    Article  CAS  PubMed  Google Scholar 

  19. 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 11:265–269

    Article  CAS  PubMed  Google Scholar 

  20. Julvez J, Magnaval JF, Meynard D, Perie C, Baixench MT (1996) Seroepidemiology of toxoplasmosis in Niamey. Niger Med Tropicale (Mars) 56:48–50

    CAS  Google Scholar 

  21. Liesenfeld O, Press C, Montoya JG, Gill R, Isaac-Renton JL, Hedman K et al (1997) Falsepositive results in immunoglobulin M (IgM) Toxoplasma antibody tests and importance of confirmatory testing: the Platelia Toxo IgM test. J Clin Microbiol 35:174–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chandrasena N, Herath R, Rupasinghe N, Samarasinghe B, Samaranayake H, Kastuririratne A et al (2016) Toxoplasmosis awareness, seroprevalence and risk behavior among pregnant women in the Gampaha district, Sri Lanka. Pathog Glob Health 110:62–67. https://doi.org/10.1080/20477724.2016.1173325

    Article  PubMed  PubMed Central  Google Scholar 

  23. Doudou Y, Renaud P, Coralie L, Jacqueline F, Hypolite S, Hypolite M et al (2014) Toxoplasmosis among pregnant women: high seroprevalence and risk factors in Kinshasa, Democratic Republic of Congo. Asian Pac J Trop Biomed 4:69–74. https://doi.org/10.1016/S2221-1691(14)60211-2

    Article  PubMed  Google Scholar 

  24. Hung CS, Su HW, Lee YL, Weng HW, Wang YC, Naito T et al (2015) Seroprevalence, seroconversion, and risk factors for toxoplasmosis among pregnant women in Taipei. Taiwan Jpn J Infec Dis 68:312–317. https://doi.org/10.7883/yoken.JJID.2014.263

    Article  CAS  Google Scholar 

  25. Mahmoudi MR, Kazemi B, Haghighi A, Karanis P (2015) Detection of Acanthamoeba and Toxoplasma in river water samples by molecular methods in Iran. Iranian J Parasitol 10:250–257

    Google Scholar 

  26. Karanis P, Aldeyarbi HM, Mirhashemi ME, Khalil KM (2013) The impact of the waterborne transmission of Toxoplasma gondii and analysis efforts for water detection: an overview and update. Environ Sci Pollut Res Int 20:86–99. https://doi.org/10.1007/s11356-012-1177-5

    Article  PubMed  Google Scholar 

  27. Roudi F, Azadi P, Mesgaran M (2017) Iran’s Population Dynamics and Demographic Window of Opportunity. Stanford Iran 2040 Project, Stanford University. Working Paper No. 4 . Stanford, CA 94305–6055, www.iranian-studies.stanford.edu/iran2040. Accessed Aug 2017

  28. 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 26:1378–1382

    PubMed  Google Scholar 

  29. Seyyedpour SH, Afshar P, Barzegarnejad A, Kalhori S, Agah R (2016) Evaluation of anti-toxoplasma gondii antibodies in hemodialysis patients with chronic kidney disease in Sari Iran. Nephro-Urol Mon 8:e40182. https://doi.org/10.5812/numonthly.40182

    Article  Google Scholar 

  30. Singh S, Munawwar A, Rao S, Mehta S, Hazarika NK (2014) Serologic prevalence of Toxoplasma gondii in Indian women of child bearing age and effects of social and environmental factors. PLoS Negl Trop Dis 8:e2737. https://doi.org/10.1371/journal.pntd.0002737

    Article  PubMed  PubMed Central  Google Scholar 

  31. Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB (2001) Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol 154:357–365. https://doi.org/10.1093/aje/154.4.357

    Article  CAS  PubMed  Google Scholar 

  32. Daryani A, Sharif M, Meigouni M (2011) Seroprevalence of IgG and IgM anti-Toxoplasma antibodies in HIV/AIDS patients, northern Iran. Asian Pac J Trop Med 4:271–274

    Article  PubMed  Google Scholar 

  33. Yazar S, Demirtaş F, Yalçin S, Yaman O, Tokgöz B, Utaş C et al (2003) Anti-Toxoplasma gondii antibodies in haemodialysis patients with chronic renal failure. Yonsei Med J 44:288–292. https://doi.org/10.3349/ymj.2003.44.2.288

    Article  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1099/jmm.0.45587-0

    Article  CAS  PubMed  Google Scholar 

  35. Lappalainen M, Hedman K (2004) Serodiagnosis of toxoplasmosis, the impact of measurement of IgG avidity. Annali dell'Istituto Superiore di Sanità 40:81–88

    PubMed  Google Scholar 

  36. Bayani M, Mostafazadeh A, Oliaee F, Kalantari N (2013) The prevalence of Toxoplasma gondii in hemodialysis patients. Iran Red Crescent Med J 15:e5225. https://doi.org/10.5812/ircmj.5225

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tan DS, Zaman V (1973) Toxoplasma antibody survey in West Malaysia. Med J Malaysia 27:188–191

    CAS  PubMed  Google Scholar 

  38. Shamilah H, Lokman HS, Noor Azain MY, Malkith K, Yusri MY (2001) Seroprevalence of Toxoplasma gondii antibodies in HIV positive and negative patients using the immunofluorescence antibody test (IFAT) methods. Trop Biomed 18:137–1341

    Google Scholar 

  39. Zurainee MN, Khairul Anuar A, Fong MY, Hoh HB, Choon JNR (2000) Ocular presentations and Toxoplasma serology. J Univ Malaya Med Centre 2:98–102

    Google Scholar 

  40. Nissapatorn V, Abdullah KA (2004) Review on human toxoplasmosis in Malaysia: the past, present and prospective future. Southeast Asian J Trop Med Public Health 35(1):24–30

    PubMed  Google Scholar 

  41. Alvarado-Esquivel C, Estrada-Martínez S, Pizarro-Villalobos H, Arce-Quiñones M, Liesenfeld O, Dubey JP (2011) Seroepidemiology of Toxoplasma gondii infection in general population in a northern Mexican city. J Parasitol 97:40–43. https://doi.org/10.1645/GE-2612.1

    Article  CAS  PubMed  Google Scholar 

  42. Alvarado-Esquivel C, Pacheco-Vega SJ, Hernández-Tinoco J, Sánchez-Anguiano LF, Berumen-Segovia LO, Rodríguez-Acevedo FJ et al (2014) Seroprevalence of Toxoplasma gondii infection and associated risk factors in Huicholes in Mexico. Parasit Vect 7:301. https://doi.org/10.1186/1756-3305-7-301

    Article  CAS  Google Scholar 

  43. Guess T, McClelland E (2018) Differences in the male and female immune response to Cryptococcus neoformans infections. J Immunol Methods 200(1 Supplement):166–215

    Google Scholar 

  44. Klein SL, Marriott I, Fish EN (2015) Sex-based differences in immune function and responses to vaccination. Trans R Soc Trop Med Hyg 109:9–15. https://doi.org/10.1093/trstmh/tru167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Bamba S, Sourabié Y, Guiguemdé TR, Karou DS, Simporé J, Bambara M et al (2014) Seroprevalence of latent Toxoplasma gondii infection among HIV-infected pregnant women in Bobo-Dioulasso, Burkina Faso. Pak J Biol Sci 17:1074–1078. https://doi.org/10.3923/pjbs.2014.1074.1078

    Article  CAS  PubMed  Google Scholar 

  46. Kortbeek LM, De Melker HE, Veldhuijzen IK, Conyn-Van Spaendonck MA (2004) Population-based Toxoplasma seroprevalence study in The Netherlands. Epidemiol Infect 132:839–845. https://doi.org/10.1017/s0950268804002535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Bamba S, Cissé M, Sangaré I, Zida A, Ouattara S, Guiguemdé RT (2017) Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Bobo Dioulasso. Burkina Faso BMC Infect Dis 17:482. https://doi.org/10.1186/s12879-017-2583-6

    Article  PubMed  Google Scholar 

  48. Montoya JG, Remington JS (2008) Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis 47:554–566. https://doi.org/10.1086/590149

    Article  PubMed  Google Scholar 

  49. Nissapatorn V, Lee CK, Cho SM, Rohela M, Anuar AK, Quek KF et al (2003) Toxoplasmosis in HIV/AIDS patients in Malaysia. Southeast Asian J Trop Med Public Health 34(Suppl 2):80–85

    PubMed  Google Scholar 

  50. Sobral CA, Amendoeira MR, Teva A, Patel BN, Klein CH (2005) Seroprevalence of infection with Toxoplasma gondii in indigenous Brazilian populations. Am J Trop Med Hyg 72:37–41

    Article  PubMed  Google Scholar 

  51. Sharif M, Daryani A, Ebrahimnejad Z, Gholami S, Ahmadpour E, Borhani SETAL (2016) Seroprevalence of anti-Toxoplasma IgG and IgM among individuals who were referred to medical laboratories in Mazandaran province, northern Iran. J Infect Public Health 9:75–80. https://doi.org/10.1016/j.jiph.2015.06.006

    Article  PubMed  Google Scholar 

  52. Vieira FP, Alves Mda G, Martins LM, Rangel AL, Dubey JP, Hill DETAL (2015) Waterborne toxoplasmosis investigated and analysed under hydrogeological assessment: new data and perspectives for further research. Memórias do Instituto Oswaldo Cruz 110:929–935. https://doi.org/10.1590/0074-02760150262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Pereira KS, Franco RM, Leal DA (2010) Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Adv Food Nutr Res 60:1–19. https://doi.org/10.1016/S1043-4526(10)60001-0

    Article  PubMed  Google Scholar 

  54. Lass A, Szostakowska B, Korzeniewski K, Karanis P (2017) The first detection of Toxoplasma gondii DNA in environmental air samples using gelatine filters, real-time PCR and loop-mediated isothermal (LAMP) assays: qualitative and quantitative analysis. Parasitology 144(13):1791–1801. https://doi.org/10.1017/S0031182017001172

    Article  CAS  PubMed  Google Scholar 

  55. Lass A, Pietkiewicz H, Modzelewska E, Dumètre A, Szostakowska B, Myjak P (2009) Detection of Toxoplasma gondii oocysts in environmental soil samples using molecular methods. Euro J Clin Microbiol Infect Dis 28(6):599–605. https://doi.org/10.1007/s10096-008-0681-5

    Article  CAS  Google Scholar 

  56. Gotteland C, Gilot-Fromont E, Aubert D, Poulle ML, Dupuis E, Dardé ML et al (2014) Spatial distribution of Toxoplasma gondii oocysts in soil in a rural area: Influence of cats and land use. Vet Parasitol 205(3–4):629–637. https://doi.org/10.1016/j.vetpar.2014.08.003

    Article  PubMed  Google Scholar 

  57. Buffolano W, Gilbert RE, Holland FJ, Fratta D, Palumbo F, Ades AE (1996) Risk factors for recent toxoplasma infection in pregnant women in Naples. Epidemiol Infect 116:347–351. https://doi.org/10.1017/s0950268800052675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kapperud G, Jenum PA, Stray-Pedersen B, Melby KK, Eskild A, Eng J (1996) Risk factors for Toxoplasma gondii infection in pregnancy. Results of a prospective case-control study in Norway. Am J Epidemiol 144:405–412. https://doi.org/10.1093/oxfordjournals.aje.a008942

    Article  CAS  PubMed  Google Scholar 

  59. Petersen E, Vesco G, Villari S, Buffolano W (2010) What do we know about risk factors for infection in humans with Toxoplasma gondii and how can we prevent infections? Zoonoses Public Health 57:8–17. https://doi.org/10.1111/j.1863-2378.2009.01278.x

    Article  CAS  PubMed  Google Scholar 

  60. Lass A, Pietkiewicz H, Szostakowska B, Myjak P (2012) The first detection of Toxoplasma gondii DNA in environmental fruits and vegetables samples. Eur J Clin Microbiol Infect Dis 31:1101–1108. https://doi.org/10.1007/s10096-011-1414-8

    Article  CAS  PubMed  Google Scholar 

  61. Saeedi M, Veghari GR, Marjani A (2007) Seroepidemiologic evaluation of anti-toxoplasma antibodies among women in north of Iran. Pak J Biol Sci 10:2359–2362. https://doi.org/10.3923/pjbs.2007.2359.2362

    Article  PubMed  Google Scholar 

  62. Rafiei A, Hamadi A, Amani F (2006) Seroprevalence of Toxoplasma among girl students in Ahvaz city. Iran J Infect Trop Dis 10:35–41

    Google Scholar 

  63. Nijem KI, Al-Amleh S (2009) Seroprevalence and associated risk factors of toxoplasmosis in pregnant women in Hebron district, Palestine. East Mediterr Health J 15:1278–1284

    CAS  PubMed  Google Scholar 

  64. Ertug S, Okyay P, Turkmen M (2005) Yuksel H (2005) Seroprevalence and risk factors for Toxoplasma infection among pregnant women in Aydin province, Turkey. BMC Public Health 15(5):66. https://doi.org/10.1186/1471-2458-5-66

    Article  Google Scholar 

  65. Ishaku B, Umoh J, Lawal I, Randawa A (2009) Seroprevalence and risk factors for toxoplasmosis among antenatal women in Zaria. Nigerian Res J Med Sci 4:483–488

    Google Scholar 

  66. Dubey J, BC JP (1988) Toxoplasmosis in sheep, goats, pigs and cattle. In: Dubey J, Beattie C (eds) Toxoplasmosis in animals and man. CRC Press, Boca Raton, pp 61–114

    Google Scholar 

  67. Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 5:1–38. https://doi.org/10.2166/wh.2006.002

    Article  PubMed  Google Scholar 

  68. Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks-an update 2004–2010. Water Res 45:6603–6614. https://doi.org/10.1016/j.watres.2017.01.036

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Authors gratefully acknowledge hemodialysis patients, healthy controls, medical doctors and personal of medical Lab for their valuable cooperation in this project. This project was supported by Guilan University of Medical Sciences.

Funding

Funded by the Guilan University of medical sciences.

Author information

Author notes

  1. Farshid Saadat and Mohammad Reza Mahmoudi equally contributed.

Authors and Affiliations

  1. Cellular and Molecular Research Center, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Farshid Saadat, Mohammad Reza Mahmoudi, Ebrahim Rajabi & Bijan Majidi Shad

  2. Department of Parasitology, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Mohammad Reza Mahmoudi & Zahra Atrkar Roshan

  3. Medical Biotechnology Research Center, Guilan University of Medical Sciences, Rasht, Iran

    Mohammad Reza Mahmoudi

  4. Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Farshid Saadat

  5. Faculty of Medicine and University Hospital, University of Cologne, Cologne, Germany

    Panagiotis Karanis

  6. Department of Basic and Clinical Sciences, University of Nicosia Medical School, Nicosia, Cyprus

    Panagiotis Karanis

Authors
  1. Farshid Saadat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Reza Mahmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ebrahim Rajabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zahra Atrkar Roshan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bijan Majidi Shad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Panagiotis Karanis
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MRM: literature review, analysis of results and manuscript preparation; ER: collection of samples and preparation of samples; FS: analysis of results and manuscript preparation; ZAR: performance of analyses; BMS: collection of samples; PK: literature review, analysis of results, manuscript preparation and corrections.

Corresponding authors

Correspondence to Mohammad Reza Mahmoudi or Panagiotis Karanis.

Ethics declarations

Competing Interests

The authors declare that they have no conflict of interest.

Ethical Approval

The study was approved by the Ethics Committee of Guilan University of Medical Sciences with ethics number of IR.GUMS.REC.1396.164.

Informed Consent

Patients voluntarily agreed to participate in the study and gave their written informed consent.

Consent for Publication

All authors declare their consent for publication.

Availability of supporting data

Yes.

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saadat, F., Mahmoudi, M.R., Rajabi, E. et al. Seroepidemiology and Associated Risk Factors of Toxoplasma gondii in Hemodialysis Patients. Acta Parasit. 65, 906–912 (2020). https://doi.org/10.1007/s11686-020-00238-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-020-00238-7

Keywords

Search

Navigation