Hostname: page-component-6bf8c574d5-9f2xs Total loading time: 0 Render date: 2025-03-05T13:32:11.985Z Has data issue: false hasContentIssue false

The association between Parkinson disease and Toxocara infection/exposure: A case-control study

Published online by Cambridge University Press:  05 March 2025

A. Alizadeh Khatir
Affiliation:
Mobility Impairment Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
A. Abbasi
Affiliation:
Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
S. Sarandili
Affiliation:
Curtin Medical School, Faculty of Health Sciences, Curtin University, Perth, Australia
M. Sepidarkish
Affiliation:
Department of Biostatistics and Epidemiology, School of Public Health, Babol University of Medical Sciences, Babol, Iran
A. Fazlollahpour-Naghibi
Affiliation:
Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
D. Arjmandi
Affiliation:
Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
A. Rostami*
Affiliation:
Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
*
Corresponding author: A. Rostami; Email: [email protected]

Abstract

Parkinson’s disease (PD) is a prevalent neurological disorder and the second most common neurodegenerative disease. Research has explored the impact of infectious agents, such as the parasites, on neurological conditions, including PD. Given the limited studies worldwide and in Iran, this study aims to investigate the relationship between Toxocara infection and PD. This case-control study involved 91 PD patients and 90 healthy controls. After obtaining consent, serum samples and questionnaires were collected. All sera were examined using an ELISA test for IgG antibodies against Toxocara canis. Results were analyzed with SPSS, using chi-square tests, and odds ratios (OR), and confidence intervals (CI) were calculated via univariate and multivariate analyses. The prevalence of anti-Toxocara IgG was 33% (30/91) in PD patients and 33.3% (30/90) in the control group. Both univariate analysis (OR: 0.98; 95% CI: 0.52–1.82) and multivariate analysis (OR: 0.95; 95% CI: 0.49–1.83) indicated no statistically significant association. Additionally, univariate analysis (OR: 0.49; 95% CI: 0.16–1.5) and multivariate analysis (OR: 0.37; 95% CI: 0.09–1.43) suggested non-significant association between Toxocara infection and the severity of PD. Our findings do not support a statistically significant association between Toxocara infection and the PD. While the analysis suggested that Toxocara infection might reduce the severity of PD, these results were also not statistically significant. Further research with larger sample sizes and diverse populations is needed to fully understand the potential relationship between Toxocara infection and PD.

Type
Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel Ghafar, AE, Elkowrany, SE, Salem, SA, Menaisy, AA, Fadel, WA and Awara, WM (1996) Effect of some parasitic infection on neurotransmitters in the brain of experimentally infected mice before and after treatment. Journal of the Egyptian Society of Parasitology 26, 497508.Google ScholarPubMed
Acioglu, C, Heary, RF and Elkabes, S (2022) Roles of neuronal toll-like receptors in neuropathic pain and central nervous system injuries and diseases. Brain, Behavior, and Immunity 102, 163178. doi: 10.1016/j.bbi.2022.02.016.CrossRefGoogle ScholarPubMed
Aghamolaie, S, Seyyedtabaei, SJ, Behniafar, H, Foroutan, M, Saber, V, Hanifehpur, H, Mehravar, S and Rostami, A (2019) Seroepidemiology, modifiable risk factors and clinical symptoms of Toxocara spp. infection in northern Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 113, 116122.CrossRefGoogle ScholarPubMed
Alexoudi, A, Alexoudi, I and Gatzonis, S (2018) Parkinson’s disease pathogenesis, evolution and alternative pathways: A review. Revue Neurologique (Paris) 174, 699704. doi: 10.1016/j.neurol.2017.12.003.CrossRefGoogle ScholarPubMed
Allen, JE and Maizels, RM (2011) Diversity and dialogue in immunity to helminths. Natural Reviews Immunology 11, 375388. doi: 10.1038/nri2992.CrossRefGoogle ScholarPubMed
Bayani, M, Riahi, SM, Bazrafshan, N, Ray Gamble, H and Rostami, A (2019) Toxoplasma gondii infection and risk of Parkinson and Alzheimer diseases: A systematic review and meta-analysis on observational studies. Acta Tropica 196, 165171. doi: 10.1016/j.actatropica.2019.05.015.CrossRefGoogle ScholarPubMed
Bisetegn, H, Debash, H, Ebrahim, H, Mahmood, N, Gedefie, A, Tilahun, M, Alemayehu, E, Mohammed, O and Feleke, DG (2023) Global seroprevalence of Toxoplasma gondii infection among patients with mental and neurological disorders: A systematic review and meta-analysis. Health Science Reports 6, e1319. doi: 10.1002/hsr2.1319.CrossRefGoogle ScholarPubMed
Bopeththa, B and Ralapanawa, U (2017) Post encephalitic parkinsonism following dengue viral infection. BMC Research Notes 10, 655. doi: 10.1186/s13104-017-2954-5.CrossRefGoogle ScholarPubMed
Bu, XL, Wang, X, Xiang, Y, Shen, LL, Wang, QH, Liu, YH, Jiao, SS, Wang, YR, Cao, HY, Yi, X, Liu, CH, Deng, B, Yao, XQ, Xu, ZQ, Zhou, HD and Wang, YJ (2015) The association between infectious burden and Parkinson’s disease: A case-control study. Parkinsonism & Related Disorders 21, 877881. doi: 10.1016/j.parkreldis.2015.05.015.CrossRefGoogle ScholarPubMed
Çelik, T, Kaplan, Y, Ataş, E, Öztuna, D and Berilgen, S (2013) Toxocara seroprevalence in patients with idiopathic Parkinson’s disease: Chance association or coincidence? Biomed Research International 2013, 685196. doi: 10.1155/2013/685196.CrossRefGoogle ScholarPubMed
Chatzikonstantinou, S, Polymeropoulos, K, Stavrati, A, Konstantinidis, G and Kazis, D (2022) Toxocara canis infection manifesting as cerebral vasculitis: A case report. Neurological Sciences 43, 45834586. doi: 10.1007/s10072-022-06052-5.CrossRefGoogle ScholarPubMed
Chen, J, Liu, Q, Liu, GH, Zheng, WB, Hong, SJ, Sugiyama, H, Zhu, XQ and Elsheikha, HM (2018) Toxocariasis: A silent threat with a progressive public health impact. Infectious Diseases of Poverty 7, 59. doi: 10.1186/s40249-018-0437-0.CrossRefGoogle ScholarPubMed
Choi, D, Lim, JH, Choi, DC, Lee, KS, Paik, SW, Kim, SH, Choi, YH and Huh, S (2012) Transmission of Toxocara canis via ingestion of raw cow liver: a cross-sectional study in healthy adults. Korean Journal of Parasitology 50, 2327. doi: 10.3347/kjp.2012.50.1.23.CrossRefGoogle ScholarPubMed
Cocoros, NM, Svensson, E, Szépligeti, SK, Vestergaard, SV, Szentkúti, P, Thomsen, RW, Borghammer, P, Sørensen, HT and Henderson, VW (2021) Long-term risk of Parkinson disease following influenza and other infections. JAMA Neurology 78, 14611470. doi: 10.1001/jamaneurol.2021.3895.CrossRefGoogle ScholarPubMed
de Almeida Carvalho, EA and Rocha, RL (2014) Visceral larva migrans syndromes associated with toxocariasis: Epidemiology, clinical and laboratory aspects of human toxocariasis. Current Tropical Medicine Reports 1, 7479.CrossRefGoogle Scholar
Di Lazzaro, G, Picca, A, Boldrini, S, Bove, F, Marzetti, E, Petracca, M, Piano, C, Bentivoglio, AR and Calabresi, P (2024) Differential profiles of serum cytokines in Parkinson’s disease according to disease duration. Neurobiology of Disease 190, 106371. doi: 10.1016/j.nbd.2023.106371.CrossRefGoogle ScholarPubMed
Discacciati, A, Orsini, N and Greenland, S (2015) Approximate Bayesian logistic regression via penalized likelihood by data augmentation. The Stata Journal 15, 712736.CrossRefGoogle Scholar
Dourmashkin, RR, Dunn, G, Castano, V and McCall, SA (2012) Evidence for an enterovirus as the cause of encephalitis lethargica. BMC Infectious Diseases 12, 136. doi: 10.1186/1471-2334-12-136.CrossRefGoogle Scholar
Eslahi, AV, Badri, M, Khorshidi, A, Majidiani, H, Hooshmand, E, Hosseini, H, Taghipour, A, Foroutan, M, Pestehchian, N and Firoozeh, F (2020) Prevalence of Toxocara and Toxascaris infection among human and animals in Iran with meta-analysis approach. BMC Infectious Diseases 20, 117.CrossRefGoogle ScholarPubMed
Espay, AJ and Henderson, KK (2011) Postencephalitic parkinsonism and basal ganglia necrosis due to Epstein-Barr virus infection. Neurology 76, 15291530. doi: 10.1212/WNL.0b013e318217e7dd.CrossRefGoogle ScholarPubMed
Fallah, M, Davoodi, L, Najafi-Vosough, R, Sardari, M, Kordi, S, Faizi, F, Azarghoon, L, Afrabandpey, AA, Zare, H and Shojaei, AA (2021) Seroprevalence of toxocara in patients attending qaemshahr rural health centers, iran 2019. Journal of Mazandaran University of Medical Sciences 31, 194200.Google Scholar
Fan, C-K (2020) Pathogenesis of cerebral toxocariasis and neurodegenerative diseases. Advances in Parasitology 109, 233259.CrossRefGoogle ScholarPubMed
Fan, CK, Holland, CV, Loxton, K and Barghouth, U (2015b) Cerebral Toxocariasis: Silent progression to neurodegenerative disorders? Clinical Microbiology Reviews 28, 663686. doi: 10.1128/cmr.00106-14.CrossRefGoogle ScholarPubMed
Fata, A, Hosseini, SM, Woo, SJ, Zibaei, M, Berenji, F, Farash, BRH and Moghaddas, E (2021) Frequency of Toxocara Antibodies in Patients Clinically Suspected to Ocular Toxocariasis, Northeast of Iran. Iranian Journal of Parasitologyl 16, 305311. doi: 10.18502/ijpa.v16i2.6312.Google ScholarPubMed
Faure, G, Goulenok, T, Lariven, S, Dossier, A, Henry-Feugeas, MC, Argy, N and Papo, T (2021) Eosinophilic meningomyelitis caused by Toxocara spp. in a migrant coming from La Reunion. Journal of Travel Medicine 28. doi: 10.1093/jtm/taab075.CrossRefGoogle Scholar
Firouzeh, N, Ziaali, N, Sheibani, V, Doustimotlagh, AH, Afgar, A, Zamanpour, M, Keshavarz, H, Shojaee, S, Shafiei, R, Esmaeilpour, K and Babaei, Z (2021) Chronic toxoplasma gondii Infection potentiates Parkinson’s disease course in mice model. Iranian Journal of Parasitology 16, 527537. doi: 10.18502/ijpa.v16i4.7863.Google ScholarPubMed
Gale, SD and Hedges, DW (2020) Neurocognitive and neuropsychiatric effects of toxocariasis. Advances in Parasitology 109, 261272.CrossRefGoogle ScholarPubMed
Goetz, CG, Tilley, BC, Shaftman, SR, Stebbins, GT, Fahn, S, Martinez-Martin, P, Poewe, W, Sampaio, C, Stern, MB, Dodel, R, Dubois, B, Holloway, R, Jankovic, J, Kulisevsky, J, Lang, AE, Lees, A, Leurgans, S, LeWitt, PA, Nyenhuis, D, Olanow, CW, Rascol, O, Schrag, A, Teresi, JA, van Hilten, JJ and LaPelle, N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Movement Disorders 23, 21292170. doi: 10.1002/mds.22340.CrossRefGoogle ScholarPubMed
Harris, MA, Tsui, JK, Marion, SA, Shen, H and Teschke, K (2012) Association of Parkinson’s disease with infections and occupational exposure to possible vectors. Movement Disorders 27, 11111117. doi: 10.1002/mds.25077.CrossRefGoogle ScholarPubMed
He, S, Yuan, LP, Zhang, JW and Han, X (2015) Postencephalitic parkinsonism and selective involvement of substantia nigra. Neurological Sciences 36, 653655. doi: 10.1007/s10072-015-2064-x.CrossRefGoogle ScholarPubMed
Hemling, N, Röyttä, M, Rinne, J, Pöllänen, P, Broberg, E, Tapio, V, Vahlberg, T and Hukkanen, V (2003) Herpesviruses in brains in Alzheimer’s and Parkinson’s diseases. Annals of Neurology 54, 267271. doi: 10.1002/ana.10662.CrossRefGoogle ScholarPubMed
Johnson, ME, Stecher, B, Labrie, V, Brundin, L and Brundin, P (2019) Triggers, facilitators, and aggravators: Redefining Parkinson’s disease pathogenesis. Trends in Neurosciences 42, 413. doi: 10.1016/j.tins.2018.09.007.CrossRefGoogle ScholarPubMed
Kannarkat, GT, Boss, JM and Tansey, MG (2013) The role of innate and adaptive immunity in Parkinson’s disease. Journal of Parkinson’s Disease 3, 493514. doi: 10.3233/jpd-130250.CrossRefGoogle ScholarPubMed
Knüppel, S (2010) A graphical tool for analyzing causal diagrams. Epidemiology 21, 159.CrossRefGoogle Scholar
Koprich, JB, Johnston, TH, Huot, P, Reyes, MG, Espinosa, M and Brotchie, JM (2011) Progressive neurodegeneration or endogenous compensation in an animal model of Parkinson’s disease produced by decreasing doses of alpha-synuclein. PLoS One 6, e17698. doi: 10.1371/journal.pone.0017698.CrossRefGoogle ScholarPubMed
Laurence, M, Benito-León, J and Calon, F (2019) Malassezia and Parkinson’s disease. Frontiers in Neurology 10, 758. doi: 10.3389/fneur.2019.00758.CrossRefGoogle ScholarPubMed
Li, KL, Huang, HY, Ren, H and Yang, XL (2022) Role of exosomes in the pathogenesis of inflammation in Parkinson’s disease. Neural Regeneration Research 17, 18981906. doi: 10.4103/1673-5374.335143.Google Scholar
Luna, J, Cicero, CE, Rateau, G, Quattrocchi, G, Marin, B, Bruno, E, Dalmay, F, Druet-Cabanac, M, Nicoletti, A and Preux, P-M (2018) Updated evidence of the association between toxocariasis and epilepsy: systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12, e0006665.CrossRefGoogle ScholarPubMed
Ma G, Holland, CV, Wang, T, Hofmann, A, Fan, C-K, Maizels, RM, Hotez, PJ and Gasser, RB (2018) Human toxocariasis. The Lancet Infectious Diseases 18, e14e24.Google Scholar
Ma G, Rostami, A, Wang, T, Hofmann, A, Hotez, PJ and Gasser, RB (2020) Global and regional seroprevalence estimates for human toxocariasis: A call for action. Advances in Parasitology 109, 275290. doi: 10.1016/bs.apar.2020.01.011.Google Scholar
Maiti, P, Manna, J and Dunbar, GL (2017) Current understanding of the molecular mechanisms in Parkinson’s disease: Targets for potential treatments. Translational Neurodegeneration 6, 28. doi: 10.1186/s40035-017-0099-z.CrossRefGoogle ScholarPubMed
Maizels, RM (2013) Toxocara canis: Molecular basis of immune recognition and evasion. Veterinary Parasitology 193, 365374. doi: 10.1016/j.vetpar.2012.12.032.CrossRefGoogle ScholarPubMed
Morimatsu, Y, Akao, N, Akiyoshi, H, Kawazu, T, Okabe, Y and Aizawa, H (2006) A familial case of visceral larva migrans after ingestion of raw chicken livers: Appearance of specific antibody in bronchoalveolar lavage fluid of the patients. American Journal of Tropical Medicine and Hygiene 75, 303306.CrossRefGoogle ScholarPubMed
Navarro-López, EM, Çelikok, U and Şengör, NS (2021) A dynamical model for the basal ganglia-thalamo-cortical oscillatory activity and its implications in Parkinson’s disease. Cognitive Neurodynamics 15, 693720. doi: 10.1007/s11571-020-09653-y.CrossRefGoogle ScholarPubMed
Nicoletti, A (2020) Neurotoxocariasis. Advances in Parasitology 109, 219231.CrossRefGoogle ScholarPubMed
Nohtani, M, Asgari, Q, Mikaeili, F, Ostovan, VR, Mirzaeipour, M, Bahreini, MS and Rashidi, S (2022) Toxoplasma reduces complications of Parkinson’s disease: An experimental study in BALB/c mice. Journal of Parasitology Research 2022, 5716765. doi: 10.1155/2022/5716765.CrossRefGoogle ScholarPubMed
Othman, AA, Abdel-Aleem, GA, Saied, EM, Mayah, WW and Elatrash, AM (2010) Biochemical and immunopathological changes in experimental neurotoxocariasis. Molecular and Biochemical Parasitology 172, 18. doi: 10.1016/j.molbiopara.2010.03.006.CrossRefGoogle ScholarPubMed
Ou, Z, Pan, J, Tang, S, Duan, D, Yu, D, Nong, H and Wang, Z (2021) Global trends in the incidence, prevalence, and years lived with disability of Parkinson’s disease in 204 countries/territories from 1990 to 2019. Frontiers in Public Health 9, 776847. doi: 10.3389/fpubh.2021.776847.CrossRefGoogle ScholarPubMed
Poewe, W, Seppi, K, Tanner, CM, Halliday, GM, Brundin, P, Volkmann, J, Schrag, AE and Lang, AE (2017) Parkinson disease. Nature Reviews Disease Primers 3, 17013. doi: 10.1038/nrdp.2017.13.CrossRefGoogle ScholarPubMed
Quintero-Cusguen, P, Gutiérrez-Álvarez, AM and Patiño, DR (2021) Toxocariosis. Acta Neurológica Colombiana 37, 169173.CrossRefGoogle Scholar
Raissi, V, Sohrabi, N, Bayat, F, Etemadi, S, Raiesi, O, Jalali, P, Karami, M, Abdollahi, A, Hoseiny, Z, Shayanfard, M, Alizadeh, G, Gadalla, ME and Ibrahim, A (2021) Human Toxocariasis in individuals with blood disorders and cancer patients: the first seroepidemiological study in Iran. Journal of Parasitic Diseases 45, 643650. doi: 10.1007/s12639-021-01347-4.CrossRefGoogle Scholar
Rostami, A, Riahi, SM, Holland, CV, Taghipour, A, Khalili-Fomeshi, M, Fakhri, Y, Omrani, VF, Hotez, PJ and Gasser, RB (2019) Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis. PLoS Neglected Tropical Diseases 13, e0007809. doi: 10.1371/journal.pntd.0007809.CrossRefGoogle ScholarPubMed
Sasco, AJ and Paffenbarger, RS Jr. (1985) Measles infection and Parkinson’s disease. American Journal of Epidemiology 122, 10171031. doi: 10.1093/oxfordjournals.aje.a114183.CrossRefGoogle ScholarPubMed
Shen, X, Yang, H, Wu, Y, Zhang, D and Jiang, H (2017) Meta-analysis: Association of Helicobacter pylori infection with Parkinson’s diseases. Helicobacter 22. doi: 10.1111/hel.12398.CrossRefGoogle ScholarPubMed
Shulman, JM, De Jager, PL and Feany, MB (2011) Parkinson’s disease: Genetics and pathogenesis. Annual Review of Pathology 6, 193222. doi: 10.1146/annurev-pathol-011110-130242.CrossRefGoogle ScholarPubMed
Taghipour, A, Habibpour, H, Mirzapour, A and Rostami, A (2021a) Toxocara infection/exposure and the risk of schizophrenia: A systematic review and meta-analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 115, 11141121. doi: 10.1093/trstmh/trab056.CrossRefGoogle ScholarPubMed
Taghipour, A, Habibpour, H, Mirzapour, A and Rostami, A (2021b) Toxocara infection/exposure and the risk of schizophrenia: A systematic review and meta-analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 115, 11141121.CrossRefGoogle ScholarPubMed
Taghipour, A, Rostami, A, Esfandyari, S, Aghapour, S, Nicoletti, A and Gasser, RB (2020) “Begging the question”—does toxocara infection/exposure associate with multiple sclerosis-risk? Pathogens 9, 938.CrossRefGoogle ScholarPubMed
Virus, MA, Ehrhorn, EG, Lui, LM and Davis, PH (2021) Neurological and neurobehavioral disorders associated with Toxoplasma gondii infection in humans. Journal of Parasitology Research 2021, 6634807. doi: 10.1155/2021/6634807.CrossRefGoogle ScholarPubMed
Vlajinac, H, Dzoljic, E, Maksimovic, J, Marinkovic, J, Sipetic, S and Kostic, V (2013) Infections as a risk factor for Parkinson’s disease: A case-control study. International Journal of Neuroscience 123, 329332. doi: 10.3109/00207454.2012.760560.CrossRefGoogle ScholarPubMed
Wijarnpreecha, K, Chesdachai, S, Jaruvongvanich, V and Ungprasert, P (2018) Hepatitis C virus infection and risk of Parkinson’s disease: A systematic review and meta-analysis. European Journal of Gastroenterology & Hepatology 30, 913. doi: 10.1097/meg.0000000000000991.CrossRefGoogle ScholarPubMed
Zheng, Z, Zhang, S, Zhang, H, Gao, Z, Wang, X, Liu, X, Xue, C, Yao, L and Lu, G (2022) Mechanisms of autoimmune cell in DA neuron apoptosis of Parkinson’s disease: Recent advancement. Oxidative Medicine and Cellular Longevity 2022, 7965433. doi: 10.1155/2022/7965433.CrossRefGoogle ScholarPubMed
Zhu, J, Cui, Y, Zhang, J, Yan, R, Su, D, Zhao, D, Wang, A and Feng, T Temporal trends in the prevalence of Parkinson’s disease from 1980 to 2023: a systematic review and meta-analysis. The Lancet Healthy Longevity 2024, e464-e479. doi: 10.1016/S2666-7568(24)00094-1CrossRefGoogle Scholar
Zibaei, M, Mahdavi, FS, Firoozeh, F, Hasani, H and Bahadory, S (2022) Ocular Toxocariasis associated with blurred vision and visual impairment: Report of four cases. Iranian Journal of Parasitology 17, 118123. doi: 10.18502/ijpa.v17i1.9034.Google ScholarPubMed
Zorina, SA, Jurja, S, Mehedinti, M, Stoica, AM, Chita, DS, Floris, SA and Axelerad, A (2023) Infectious microorganisms seen as etiologic agents in Parkinson’s disease. Life (Basel) 13. doi: 10.3390/life13030805.Google ScholarPubMed