Skip to main content
Springer Nature Link
Log in

The correlation between Toxoplasma gondii infection and Parkinson’s disease: a case-control study

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

Toxoplasma gondii is an obligate intracellular parasite that infects all nucleate cells of vertebrates. Human infected by vertical transmission and also using raw or undercooked meat or food and water that contaminated with mature oocysts. Parkinson‘s disease as neurodegenerative disease affects people above 60 years. Due to high prevalence of toxoplasmosis in Iran and evidence about effects of T. gondii on neurodegenerative diseases, this study has been conducted to investigate possible correlation between Toxoplasma and Parkinson’s disease in Iran. Seventy five Parkinson’s patients and equal healthy volunteers were enrolled. After obtaining informed consent and sociodemographic features, 5 ml blood sample were collected and then anti-Toxoplasma IgG and IgM levels were examined by ELISA method. Data was analyzed with Chi-squre and Fisher’s test by usig stata 11 software. Binary logistic regression was used for multivariate analysis in assessing the correlation between toxoplasmosis and Parkinson. Eighty five percent of Parkinson’s group and 90.3 % of control group were positive for anti-Toxoplasma IgG antibody. In this investigation no statically differences were observed between groups and age, gender, residency and using raw or undercooked meat. There is no significant association between IgG positive titer and Parkinson’s disease. However, statistically significant association was found between Parkinson and keeping cat (P = 0.03) as well as the using of undercooked egg (P = 0.004). Although there is high level of anti-Toxoplasma IgG antibody in Parkinson’s patients which reflects chronic Toxoplasma infection; we couldn’t detect any statistical association between T. gondii infection and Parkinson’s disease.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Alipour A, Shohaee S, Mohebali M, Tehranidoost M, Masoleh FA, Keshavarz H (2011) Toxoplasma infection in schizophrenia patients: a comparative study with control group. Iran J Parasitol 6:31–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarado-Esquivel C, Alanis-Quinones OP, Arreola-Valenzuela MÁ, Rodriguez-Briones A, Piedra-Nevarez LJ, Duran-Morales E, Estrada-Martinez S, Martinez-Garcia SA, Liesenfeld O (2006) Seroepidemiology of Toxoplasma gondii infection in psychiatric inpatients in a northern Mexican city. BMC Infect Dis 6:1–7

    Article  Google Scholar 

  • Alvardo-Esquivel C, Urbina-Álvarez JD, Estrada-Martinez S, Torres-Castorena A, Molotla-De-Leon G, Liesenfeld O, Dubey JP (2011) Toxoplasma gondii infection and schizophrenia: a case control study in a low Toxoplasma seroprevalence Mexican population. Parasitol Int 60:151–155. doi:10.1016/j.parint.2010.12.003

    Article  Google Scholar 

  • Arling TA, Yolken RH, Lapidus M, Langenberg P, Dickerson FB, Zimmerma SA, Balis T, Cabassa JA, Scrandis DA, Tonelli LH (2009) Toxoplasma gondii antibody titers and history of suicide attempts in patients with recurrent mood disorders. J Nerv Ment Dis 3:905–908. doi:10.1097/NMD.0b013e3181c29a23

    Article  Google Scholar 

  • Barragan A, Sibley LD (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J Exp Med 195:1625–1633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Çelik T, Kamisli Ö, Babur C, Çevlik MÖ, Öztuna D, Altinayar S (2010) Is there a relationship between Toxoplasma gondii infection and idiopathic Parkinson’s disease? Scand J Infect Dis 42:604–608. doi:10.3109/00365541003716500

    Article  PubMed  Google Scholar 

  • Cetinkaya Z, Yazar S, Gecici O, Namli MN (2007) Anti-Toxoplasma gondii antibodies in patients with schizophrenia—preliminary findings in a Turkish sample. Schizophr Bull 33:789–791. doi:10.1093/schbul/sbm021

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen H, Zhang S, Schwarzschild MA, Hernan M, Logroscino G, Willett W, Ascherio A (2004) Folate intake and risk of Parkinson’s disease. Am J Epidemiol 160:368–375

    Article  PubMed  Google Scholar 

  • Daryani A, Sharif M, Hosseni SH, Karimi S, Gholami S (2010) Serological survey of Toxoplasma gondii in schizophrenia patients referred to Psychiatric Hospital, Sari City Iran. Trop Biomed 27:476–482

    Google Scholar 

  • De lau LM, Breteler M (2006) Epidemiology of Parkinson’s disease. Lancet Neurol 5:525–535

    Article  PubMed  Google Scholar 

  • Dubey J (2004) Toxoplasmosis—a waterborne zoonosis. Vet Parasitol 126:57–72

    Article  CAS  PubMed  Google Scholar 

  • Ferreira MS, Borges AS (2002) Some aspects of protozoan infections in immunocompromised patients: a review. Mem Inst Oswaldo Cruz 97:443–457

    Article  PubMed  Google Scholar 

  • Fleger J (2007) Effects of Toxoplasma on human behavior. Schizophr Bull 33:757–776. doi:10.1093/schbul/sb1074

    Article  Google Scholar 

  • Gaskell EA, Smith JE, Pinney JW, Westhead DR, Mcconkey GA (2009) A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS One 4:e4801. doi:10.1371/journal.pone.0004801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gazewood JD, Richards DR, Clebak K (2013) Parkinson disease: an update. Am Fam Physician 87:267–273

    PubMed  Google Scholar 

  • Guttmacher AE, Collins FS, Nussbaum RL, Ellis CE (2003) Alzheimer’s disease and Parkinson’s disease. N Eng J Med 348:1356–1364. doi:10.1056/NEJM2003RA020003

    Article  Google Scholar 

  • Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184. doi:10.1136/jnnp.55.3181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung BK, Pyo KH, Shin KY, Hwang Y, Lim H, Lee SJ, Moon JH, Lee SH, Suh YH, Chai JY (2012) Toxoplasma gondii infection in the brain inhibits neuronal degeneration and learning and memory impairments in a murine model of Alzheimer’s disease. PLoS One 7:e33312. doi:10.1371/journal.pone.0033312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koseoglu E, Yazar S, Koc I (2009) Is Toxoplasma gondii a causal agent in migraine? Am J Med Sci 338:120–122. doi:10.1097/MAJ.0b013e31819fBcac

    Article  PubMed  Google Scholar 

  • Kusbce OY, Miman O, Yaman M, Aktepe OC, Yazar S (2011) Could Toxoplasma gondii have any role in Alzheimer disease? Alzheimer Dis Assoc Disord 25:1–3. doi:10.1097/WAD.0b013e3181f73bc2

    Article  Google Scholar 

  • Ling VJ, Lester D, Mortensen PB, Langenberg PW, Postolache TT (2011) Toxoplasma gondii seropositivity and suicide rates in women. J Nerv Ment Dis 199:440–444. doi:10.1097/NMD.0b013e318221416e

    Article  PubMed  PubMed Central  Google Scholar 

  • Logroscino G (2005) The role of early life environmental risk factors in Parkinson disease: what is the evidence? Environ Health Perspect 113:1234–1238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miman O, Kusbeci OY, Aktepe OC, Cetinkaya Z (2010a) The probable relation between Toxoplasma gondii and Parkinson’s disease. Neurosci Lett 475:129–131

    Article  CAS  PubMed  Google Scholar 

  • Miman O, Mutlu EA, Ozcan O, Atambay M, Karlidag R, Unal S (2010b) Is there any role of Toxoplasma gondii in the etiology of obsessive–compulsive disorder? Psychiatry Res 177:263–265. doi:10.1016/i.psychres.2009.12.013

    Article  PubMed  Google Scholar 

  • Mostavafi S, JalaliMonfarad L (2012) Toxoplasmosis epidemiology in Iran: a systematic review. J Isfahan Med Sch 30:1–15

    Google Scholar 

  • Newman EJ, Breen K, Patterson J, Hadley DM, Grosset KA, Grosset DG (2009) Accuracy of Parkinson’s disease diagnosis in 610 general practice patients in the West of Scotland. Mov Disord 24:2379–2385. doi:10.1002/mds.22829

    Article  PubMed  Google Scholar 

  • Nuti A, Ceravolo R, Dell’agnello G, Gambaccini G, Bellini G, Kiferle L, Rossi C, Logi C, Bonuccelli U (2004) Environmental factors and Parkinson’s disease: a case–control study in the Tuscany region of Italy. Parkinsonism Relat Disord 10:481–485

    Article  CAS  PubMed  Google Scholar 

  • Obeso JA, Marin C, Rodriguez-Oroz C, Blesa J, Benitez-Temino B, Mena-Segovia J, Rodriguez M, Olanow CW (2008) The basal ganglia in Parkinson’s disease: current concepts and unexplained observations. Ann Neurol 64:S30–S46. doi:10.1002/ana.21481

    Article  PubMed  Google Scholar 

  • Okusaga O, Langenberg P, Sleemi A, Vaswani D, Giegling I, Hartmaan AM, Konte B, Friedl M, Groer MW, Yolken RH (2011) Toxoplasma gondii antibody titers and history of suicide attempts in patients with schizophrenia. Schizophr Res 133:150–155. doi:10.1016/i.schres.2011.08.006

    Article  PubMed  Google Scholar 

  • Olanow CW, Stern MB, Sethi K (2009) The scientific and clinical basis for the treatment of Parkinson disease (2009). Neurology 72:S1–S136

    Article  PubMed  Google Scholar 

  • Pandey S (2012) Parkinson’s disease: recent advances. J Assoc Physicians India 60:30–32

    PubMed  Google Scholar 

  • Pearce BD, Kruszon-Moran D, Jones JL (2012) The relationship between Toxoplasma gondii infection and mood disorders in the third national health and nutrition survey. Biol Psychiatry 72:290–295. doi:10.1016/i.biopsych.2012.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  • Priyadarshi A, Khuder SA, Schaub EA, Preyadarshi SS (2001) Environmental risk factors and Parkinson’s disease: a meta-analysis. Environ Res 86:122–127

    Article  CAS  PubMed  Google Scholar 

  • Robert-Gangneux F, Darde ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25:264–296. doi:10.1128/CMR.0501.311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skallova A, Kodym P, Frynta D, Flege J (2006) The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitol 133:525–535. doi:10.1017/S0031182006000886

    Article  CAS  Google Scholar 

  • Torrey EF, Bartko JJ, Lun ZR, Yolken RH (2007) Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr Bull 33:729–736. doi:10.1093/schbul/sbl050

    Article  PubMed  Google Scholar 

  • Vlajinac H, Dzoljic E, Maksimovlic J, Marinkovic J, Sipetic S, Kostic V (2013) Infections as a risk factor for Parkinson’s disease: a case-control study. Int J Neurosci 123:329–332

    Article  PubMed  Google Scholar 

  • Yagmur F, Yazar S, Temel HO, Cavusoglu M (2010) May Toxoplasma gondii increase suicide attempt-preliminary results in Turkish subjects? Forensic Sci Int 199:15–17

    Article  PubMed  Google Scholar 

  • Yazar S, Yaman O, Eser B, Altuntas F, Kurnaz F, Şahin I (2004) Investigation of anti-Toxoplasma gondii antibodies in patients with neoplasia. J Med Microbiol 53:1183–1186. doi:10.1099/jmm.045587-0

    Article  CAS  PubMed  Google Scholar 

  • Yolken R, Dickerson F, Fuller Torrey E (2009) Toxoplasma and schizophrenia. Parasite Immunol 31:706–715. doi:10.1111/j.1365-3024.2009.01131.x

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Du Y, Li Q, Dong Z (2007) High risk of psychosis may be associated with toxoplasmosis. Life Sci J 4:38–41

    Google Scholar 

Download references

Acknowledgments

This work was supported fully by Neurosciences Research Center (Grant no: 1303), Tabriz University of Medical Sciences, Tabriz, Iran. This is a report of a database from thesis of Faezeh Hamidi registered in Tabriz University of Medical Sciences.

Conflict of interest

The authors have no conflicts of interest.

Author information

Authors and Affiliations

  1. Neurosciences Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Mahmoud Mahami Oskouei, Faezeh Hamidi & Mahnaz Talebi

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

    Mahmoud Mahami Oskouei, Faezeh Hamidi & Esmaeil Fallah

  3. Department of Neurology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Mehdi Farhoudi & Ali Akbar Taheraghdam

  4. Department of Immunology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Tohid Kazemi

  5. Department of Biostatistics and Epidemiology, Faculty of Health Sciences, Tabriz University of Medical Sciences, Tabriz, Iran

    Homayoun Sadeghi-Bazargani

Authors
  1. Mahmoud Mahami Oskouei
    View author publications

    Search author on:PubMed Google Scholar

  2. Faezeh Hamidi
    View author publications

    Search author on:PubMed Google Scholar

  3. Mahnaz Talebi
    View author publications

    Search author on:PubMed Google Scholar

  4. Mehdi Farhoudi
    View author publications

    Search author on:PubMed Google Scholar

  5. Ali Akbar Taheraghdam
    View author publications

    Search author on:PubMed Google Scholar

  6. Tohid Kazemi
    View author publications

    Search author on:PubMed Google Scholar

  7. Homayoun Sadeghi-Bazargani
    View author publications

    Search author on:PubMed Google Scholar

  8. Esmaeil Fallah
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to Mahmoud Mahami Oskouei or Mahnaz Talebi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahami Oskouei, M., Hamidi, F., Talebi, M. et al. The correlation between Toxoplasma gondii infection and Parkinson’s disease: a case-control study. J Parasit Dis 40, 872–876 (2016). https://doi.org/10.1007/s12639-014-0595-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-014-0595-3

Keywords

Profiles

  1. Mehdi Farhoudi View author profile