Advertisement

Impact of infection on risk of Parkinson’s disease: a quantitative assessment of case-control and cohort studies

  • Lei Meng
  • Liang Shen
  • Hong-Fang Ji
Article
  • 5 Downloads

Abstract

Identifying modifiable risk factors for Parkinson’s disease (PD) to help prevent this disease has attracted increasing interest in recent years for the limited effective drugs at present. Despite many studies indicated that infection acts as a risk factor for PD, there is no quantitative assessment of the impact of viral and bacterial infections on the risk of developing PD. The present study performed a meta-analysis on the basis of 38 datasets from 13 studies covering 287,773 PD cases and 7,102,901 controls to ascertain the association between PD and infection and the differences in the strength of the viral and bacterial infections. The overall meta-analytic results indicated that individuals with infection had a 20% increased risk of PD compared with controls (OR 1.20, 95%CI 1.07–1.32). The subgroup analysis according to the type of infection found that bacterial infection had a significant impact on increased risk of PD (OR 1.40, 95%CI 1.32–1.48). The present analysis indicated that infection could increase the risk of developing PD, and physician should be aware of the risk of developing PD in subjects with infection.

Keywords

Parkinson’s disease Bacteria Virus Infection Meta-analysis 

Notes

Authors’ contributions

L.S. and H.F.J. conceived and designed the study, L.M. and L.S.collected data and performed analysis, L.M., L.S., and H.F.J. analyzed the data and wrote the main manuscript text. All authors read and approved the final manuscript.

Funding information

This work was supported by the Shandong Provincial Natural Science Foundation (Grant Nos. JQ201508 and ZR2018MH010), Shandong Provincial Key Research and Development Program (Grant No. 2018GSF121001), and Talent program of Zibo.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

References

  1. Arai H, Furuya T, Mizuno Y, Mochizuki H (2006) Inflammation and infection in Parkinson’s disease. Histol Histopathol 21:673–678PubMedGoogle Scholar
  2. Barcia C, Ros CM, Annese V, Gómez A, Ros-Bernal F, Aguado-Llera D, Martínez-Pagán ME, de Pablos V, Fernandez-Villalba E, Herrero MT (2012) IFN-gamma signaling, with the synergistic contribution of TNF-alpha, mediates cell specific microglial and astroglial activation in experimental models of Parkinson’s disease. Cell Death Dis 3:e379CrossRefGoogle Scholar
  3. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov 3:205–214CrossRefGoogle Scholar
  4. Bras JM, Singleton A (2009) Genetic susceptibility in Parkinson’s disease. Biochim Biophys Acta 1792:597–603CrossRefGoogle Scholar
  5. Brown GC (2007) Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans 35:1119–1121CrossRefGoogle Scholar
  6. 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, Wang YJ (2015) The association between infectious burden and Parkinson’s disease: a case-control study. Parkinsonism Relat Disord 21:877–881CrossRefGoogle Scholar
  7. Carvey PM, Chang QA, Ling Z (2004) Prenatal lipopolysaccharide (LPS) induces permanent reductions in dopamine neurons: effect of epigenetic alterations in CNS inflammatory homeostasis as an animal model for Parkinson's disease. Mov Disord 19:S151CrossRefGoogle Scholar
  8. Collier TJ, Kanaan NM, Kordower JH (2011) Ageing as a primary risk factor for Parkinson’s disease: evidence from studies of non-human primates. Nat Rev Neurosci 12:359–366CrossRefGoogle Scholar
  9. Danzer M, Samberger C, Schicho R, Lippe IT, Holzer P (2004) Immunocytochemical characterization of rat brainstem neurons with vagal afferent input from the stomach challenged by acid or ammonia. Eur J Neurosci 19:85–92CrossRefGoogle Scholar
  10. De Chiara G, Marcocci ME, Sgarbanti R, Civitelli L, Ripoli C, Piacentini R, Garaci E, Grassi C, Palamara AT (2012) Infectious agents and neurodegeneration. Mol Neurobiol 46:614–638CrossRefGoogle Scholar
  11. Fang F, Wirdefeldt K, Jacks A, Kamel F, Ye W, Chen H (2012) CNS infections, sepsis and risk of Parkinson’s disease. Int J Epidemiol 41:1042–1049CrossRefGoogle Scholar
  12. Fletcher NF, Wilson GK, Murray J, Hu K, Lewis A, Reynolds GM, Stamataki Z, Meredith LW, Rowe IA, Luo G, Lopez-Ramirez MA, Baumert TF, Weksler B, Couraud PO, Kim KS, Romero IA, Jopling C, Morgello S, Balfe P, McKeating JA (2012) Hepatitis C virus infects the endothelial cells of the blood-brain barrier. Gastroenterology 142:634–643.e6CrossRefGoogle Scholar
  13. Gao HM, Kotzbauer PT, Uryu K, Leight S, Trojanowski JQ, Lee VM (2008) Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. J Neurosci 28:7687–7698CrossRefGoogle Scholar
  14. Hamza TH, Zabetian CP, Tenesa A, Laederach A, Montimurro J, Yearout D, Kay DM, Doheny KF, Paschall J, Pugh E, Kusel VI, Collura R, Roberts J, Griffith A, Samii A, Scott WK, Nutt J, Factor SA, Payami H (2010) Common genetic variation in the HLA region is associated with late-onset sporadic Parkinson’s disease. Nat Genet 42:781–785CrossRefGoogle Scholar
  15. Harris MA, Tsui JK, Marion SA, Shen H, Teschke K (2012) Association of Parkinson’s disease with infections and occupational exposure to possible vectors. Mov Disord 27:1111–1117CrossRefGoogle Scholar
  16. Huang HK, Wang JH, Lei WY, Chen CL, Chang CY, Liou LS (2018) Helicobacter pylori infection is associated with an increased risk of Parkinson’s disease: a population-based retrospective cohort study. Parkinsonism Relat Disord 47:26–31CrossRefGoogle Scholar
  17. Jang H, Boltz DA, Webster RG, Smeyne RJ (2009) Viral Parkinsonism. Biochim Biophys Acta 1792:714–721CrossRefGoogle Scholar
  18. Kim JM, Jang ES, Ok K, Oh ES, Kim KJ, Jeon B, Jo HJ, Ki M, Jeong SH (2016) Association between hepatitis C virus infection and Parkinson’s disease. Mov Disord 31:1584–1585CrossRefGoogle Scholar
  19. Lai SW, Lin CH, Lin HF, Lin CL, Lin CC, Liao KF (2017) Herpes zoster correlates with increased risk of Parkinson’s disease in older people: a population-based cohort study in Taiwan. Medicine (Baltimore) 96:e6075CrossRefGoogle Scholar
  20. Lang AE, Lozan AM (1998) Parkinson’s disease. N Engl J Med 339:1044–1053CrossRefGoogle Scholar
  21. Lees AJ, Hardy J, Revesz T (2009) Parkinson’s disease. Lancet 373:2055–2066CrossRefGoogle Scholar
  22. Lema Tomé CM, Tyson T, Rey NL, Grathwohl S, Britschgi M, Brundin P (2013) Inflammation and α-synuclein’s prion-like behavior in Parkinson’s disease – is there a link? Mol Neurobiol 47:561–574CrossRefGoogle Scholar
  23. Liu B, Gao HM, Hong JS (2003) Parkinson’s disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ Health Perspect 111:1065–1073CrossRefGoogle Scholar
  24. Martyn CN, Osmond C (1995) Parkinson’s disease and the environment in early life. J Neurol Sci 132(2):201–206CrossRefGoogle Scholar
  25. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–269CrossRefGoogle Scholar
  26. Nielsen HH, Qiu J, Friis S, Wermuth L, Ritz B (2012) Treatment for Helicobacter pylori infection and risk of Parkinson’s disease in Denmark. Eur J Neurol 19:864–869CrossRefGoogle Scholar
  27. Pakpoor J, Noyce A, Goldacre R, Selkihova M, Mullin S, Schrag A, Lees A, Goldacre M (2017) Viral hepatitis and Parkinson disease: a national record-linkage study. Neurology 88:1630–1633CrossRefGoogle Scholar
  28. Parkinson J (2002) An essay on the shaking palsy. 1817. J Neuropsychiatr Clin Neurosci 14:223–236CrossRefGoogle Scholar
  29. Pringsheim T, Jette N, Frolkis A, Steeves TD (2014) The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 29:1583–1590CrossRefGoogle Scholar
  30. Ritz B, Ascherio A, Checkoway H, Marder KS, Nelson LM, Rocca WA, Ross GW, Strickland D, Van Den Eeden SK, Gorell J (2007) Pooled analysis of tobacco use and risk of Parkinson disease. Arch Neurol 64:990–997CrossRefGoogle Scholar
  31. Ross GW, Abbott RD, Petrovitch H, Morens DM, Grandinetti A, Tung KH, Tanner CM, Masaki KH, Blanchette PL, Curb JD, Popper JS, White LR (2000) Association of coffee and caffeine intake with the risk of Parkinson disease. JAMA 283:2674–2679CrossRefGoogle Scholar
  32. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK (2009) A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137:47–59CrossRefGoogle Scholar
  33. Schapira AH (2006) Etiology of Parkinson’s disease. Neurology 66:S10–S23CrossRefGoogle Scholar
  34. Shen CH, Chou CH, Liu FC, Lin TY, Huang WY, Wang YC, Kao CH (2016) Association between tuberculosis and Parkinson disease: a nationwide, population-based cohort study. Medicine (Baltimore) 95:e2883CrossRefGoogle Scholar
  35. Takahashi M, Yamada T, Nakajima S, Nakajima K, Yamamoto T, Okada H (1995) The substantia nigra is a major target for neurovirulent influenza a virus. J Exp Med 181:2161–2169CrossRefGoogle Scholar
  36. Tsai HH, Liou HH, Muo CH, Lee CZ, Yen RF, Kao CH (2016) Hepatitis C virus infection as a risk factor for Parkinson disease: a nationwide cohort study. Neurology 86:840–846CrossRefGoogle Scholar
  37. Vila M, Przedborski S (2004) Genetic clues to the pathogenesis of Parkinson’s disease. Nat Med 10(suppl):S58–S62CrossRefGoogle Scholar
  38. Vlajinac H, Dzoljic E, Maksimovic J, Marinkovic J, Sipetic S, Kostic V (2013) Infections as a risk factor for Parkinson’s disease: a case-control study. Int J Neurosci 123:329–332CrossRefGoogle Scholar
  39. Weissenborn K, Ennen JC, Bokemeyer M, Ahl B, Wurster U, Tillmann H, Trebst C, Hecker H, Berding G (2006) Monoaminergic neurotransmission is altered in hepatitis C virus infected patients with chronic fatigue and cognitive impairment. Gut 55:1624–1630CrossRefGoogle Scholar
  40. Whitton PS (2007) Inflammation as a causative factor in the aetiology of Parkinson’s disease. Br J Pharmacol 150:963–976CrossRefGoogle Scholar
  41. Wu WY, Kang KH, Chen SL, Chiu SY, Yen AM, Fann JC, Su CW, Liu HC, Lee CZ, Fu WM, Chen HH, Liou HH (2015) Hepatitis C virus infection: a risk factor for Parkinson’s disease. J Viral Hepat 22:784–791CrossRefGoogle Scholar
  42. Zhou L, Miranda-Saksena M, Saksena NK (2013) Viruses and neurodegeneration. Virol J 10:172CrossRefGoogle Scholar

Copyright information

© Journal of NeuroVirology, Inc. 2019

Authors and Affiliations

  1. 1.Institute of Biomedical ResearchShandong University of TechnologyZiboPeople’s Republic of China
  2. 2.Zibo Key Laboratory for Neurodegenerative Diseases Drug Development, Shandong Provincial Research Center for Bioinformatic Engineering and Technique, School of Life SciencesShandong University of TechnologyZiboPeople’s Republic of China

Personalised recommendations