Top

20-11-2023 | Parkinson's Disease | Review article

The risk of Parkinson’s disease in diabetic people: an updated systematic review and meta-analysis

Authors: Mobin Azami, Asra Moradkhani, Maryam Afraie, Sorour Khateri, Erfan Sharifian, Kamran Zamani, Yousef Moradi

Abstract

Background

Diabetes mellitus (DM) and the risk of Parkinson’s disease (PD) have been linked in previous studies. But the outcomes are still up for debate. This meta-analysis examined how DM affected the likelihood of developing PD.

Methods

A comprehensive search of international databases, including Medline (PubMed), Web of Sciences, Scopus, and EMBASE until January 2023, was conducted to assess the relationship between DM and PD. Cohort and case–control studies were included. Subgroup analysis was carried out based on the duration of PD, continent, age, PD criteria, DM criteria, and effect size.

Results

In the meta-analysis, 25 studies encompassing a total of 39,209,316 participants were incorporated. The collective estimation of the relative risk concerning the association between Diabetes Mellitus (DM) and Parkinson's Disease (PD) yielded a value of 1.22 (95% CI 1.08–1.37). Subsequent subgroup analyses unveiled a heightened risk of DM among patients in the Asian demographic, particularly those of a younger age and a longer duration of PD. The findings from our comprehensive meta-analysis underscore a potentially emerging connection between DM and PD.

Conclusion

These results showed that people with DM are more susceptible to developing other neurological diseases, such as PD, indicating that efforts are required to prevent the progression of such diseases among individuals with DM.

Available only for authorised users

Lang AE, Lozano AM (1998) Parkinson’s disease. N Engl J Med 339:1130–1143. https://doi.org/10.1056/NEJM199810153391607 CrossRefPubMed

Dickson DW, Braak H, Duda JE, Duyckaerts C, Gasser T, Halliday GM, Hardy J, Leverenz JB, Del Tredici K, Wszolek ZK (2009) Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria. The Lancet Neurology 8:1150–1157. https://doi.org/10.1016/S1474-4422(09)70238-8 CrossRefPubMed

Abeliovich A, Gitler AD (2016) Defects in trafficking bridge Parkinson’s disease pathology and genetics. Nature 539:207–216. https://doi.org/10.1038/nature20414 CrossRefPubMed

Feigin VL, Nichols E, Alam T, Bannick MS, Beghi E, Blake N, Culpepper WJ, Dorsey ER, Elbaz A, Ellenbogen RG (2019) Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the global burden of disease study 2016. The Lancet Neurology 18:459–480. https://doi.org/10.1016/S1474-4422(18)30499-X CrossRef

De Lau LML, Breteler MMB (2006) Epidemiology of Parkinson’s disease. The Lancet Neurology 5:525–535. https://doi.org/10.1016/S1474-4422(06)70471-9 CrossRefPubMed

Nussbaum RL, Ellis CE (2003) Alzheimer’s disease and Parkinson’s disease. N Engl J Med 348:1356–1364. https://doi.org/10.1056/NEJM2003ra020003 CrossRefPubMed

Forouhi NG, Wareham NJ (2010) Epidemiology of diabetes. Medicine 38:602–606. https://doi.org/10.1016/j.mpmed.2014.09.007 CrossRef

Roglic G (2016) WHO Global report on diabetes: a summary. Int J Noncommun Dis 1:3 CrossRef

Unger JW, Livingston JN, Moss AM (1991) Insulin receptors in the central nervous system: localization, signalling mechanisms and functional aspects. Prog Neurobiol 36:343–362. https://doi.org/10.1016/0301-0082(91)90015-s CrossRefPubMed

10.

Glabe CG (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol Aging 27:570–575. https://doi.org/10.1016/j.neurobiolaging.2005.04.017 CrossRefPubMed

11.

Santiago JA, Potashkin JA (2013) Shared dysregulated pathways lead to Parkinson’s disease and diabetes. Trends Mol Med 19:176–186. https://doi.org/10.1016/j.molmed.2013.01.002 CrossRefPubMed

12.

Schapira AHV (2008) Mitochondria in the aetiology and pathogenesis of Parkinson’s disease. The Lancet Neurology 7:97–109. https://doi.org/10.1016/S1474-4422(07)70327-7 CrossRefPubMed

13.

Lima M MS, Targa A DS, Noseda A CD, Rodriguesl S, Marcia Delattre A, dos Santos V et al (2014) Does Parkinson’s disease and type-2 diabetes mellitus present common pathophysiological mechanisms and treatments? CNS & Neurol Disord-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders) 13(3):418–428. https://doi.org/10.2174/18715273113126660155 CrossRef

14.

Dalle S, Burcelin R, Gourdy P (2013) Specific actions of GLP-1 receptor agonists and DPP4 inhibitors for the treatment of pancreatic β-cell impairments in type 2 diabetes. Cell Signal 25(2):570–579. https://doi.org/10.1016/j.cellsig.2012.11.009 CrossRefPubMed

15.

Campbell RK (2011) Clarifying the role of incretin-based therapies in the treatment of type 2 diabetes mellitus. Clin Ther 33(5):511–527. https://doi.org/10.1016/j.clinthera.2011.04.015 CrossRefPubMed

16.

Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, Holloway HW et al (2009) GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism. Proc Natl Acad Sci 106(4):1285–1290. https://doi.org/10.1073/pnas.0806720106 CrossRefPubMedPubMedCentral

17.

Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev 10:1–11. https://doi.org/10.1186/s13643-021-01626-4 CrossRef

18.

Moola S, Munn Z, Sears K, Sfetcu R, Currie M, Lisy K, Tufanaru C, Qureshi R, Mattis P, Mu P (2015) Conducting systematic reviews of association (etiology): the Joanna Briggs institute’s approach. Int J Evid Based Healthc 13:163–169. https://doi.org/10.1097/xeb.0000000000000064 CrossRefPubMed

19.

Peters MDJ, Godfrey C, McInerney P, Baldini SC, Khalil H, Parker D, Aromataris E, Munn Z (2017) Scoping reviews. Joanna Briggs Inst Rev Manual 2015:1–24

20.

Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9(1):1–30 CrossRefPubMed

21.

Suzuki M, Yoshioka M, Hashimoto M, Murakami M, Kawasaki K, Noya M, Takahashi D, Urashima M (2012) 25-hydroxyvitamin D, vitamin D receptor gene polymorphisms, and severity of Parkinson’s disease. Mov Disord 27:264–271. https://doi.org/10.1002/mds.24016 CrossRefPubMed

22.

Xu Q, Park Y, Huang X, Hollenbeck A, Blair A, Schatzkin A, Chen H (2011) Diabetes and risk of Parkinson’s disease. Diabetes Care 34:910–915. https://doi.org/10.2337/dc10-1922 CrossRefPubMedPubMedCentral

23.

Coureuil M, Bourdoulous S, Marullo S, Nassif X (2014) Invasive meningococcal disease: a disease of the endothelial cells. Trends Mol Med 20:571–578. https://doi.org/10.1016/j.molmed.2014.08.002 CrossRefPubMed

24.

Luchsinger JA, Tang M-X, Stern Y, Shea S, Mayeux R (2001) Diabetes mellitus and risk of Alzheimer’s disease and dementia with stroke in a multiethnic cohort. Am J Epidemiol 154:635–641. https://doi.org/10.1093/aje/154.7.635 CrossRefPubMed

25.

Ott A, Stolk R, Hofman A, van Harskamp F, Grobbee D, Breteler M (1996) Association of diabetes mellitus and dementia: the Rotterdam Study. Diabetologia 39:1392–1397. https://doi.org/10.1007/s001250050588 CrossRefPubMed

26.

Chohan H, Senkevich K, Patel RK, Bestwick JP, Jacobs BM, Bandres Ciga S, Gan-Or Z, Noyce AJ (2021) Type 2 diabetes as a determinant of Parkinson’s disease risk and progression. Mov Disord 36:1420–1429. https://doi.org/10.1002/mds.28551 CrossRefPubMedPubMedCentral

27.

Jeong SM, Han K, Kim D, Rhee SY, Jang W, Shin DW (2020) Body mass index, diabetes, and the risk of Parkinson’s disease. Mov Disord 35:236–244. https://doi.org/10.1002/mds.27922 CrossRefPubMed

28.

Palacios N, Gao X, McCullough ML, Jacobs EJ, Patel AV, Mayo T, Schwarzschild MA, Ascherio A (2011) Obesity, diabetes, and risk of Parkinson’s disease. Mov Disord 26:2253–2259. https://doi.org/10.1002/mds.23855 CrossRefPubMedPubMedCentral

29.

Politis M, Wu K, Molloy S, G. Bain P, Chaudhuri KR, Piccini P, (2010) Parkinson’s disease symptoms: the patient’s perspective. Mov Disord 25:1646–1651. https://doi.org/10.1002/mds.23135 CrossRefPubMed

30.

Vijiaratnam N, Lawton M, Real R, Heslegrave AJ, Guo T, Athauda D, Gandhi S, Girges C, Ben-Shlomo Y, Zetterberg H (2022) Diabetes and neuroaxonal damage in Parkinson’s disease. Mov Disord 37:1568–1569. https://doi.org/10.1002/mds.29067 CrossRefPubMedPubMedCentral

31.

Yue X, Li H, Yan H, Zhang P, Chang L, Li T (2016) Risk of Parkinson disease in diabetes mellitus: an updated meta-analysis of population-based cohort studies. Medicine. https://doi.org/10.1097/MD.0000000000003549 CrossRefPubMedPubMedCentral

32.

Cereda E, Barichella M, Pedrolli C, Klersy C, Cassani E, Caccialanza R, Pezzoli G (2011) Diabetes and risk of Parkinson’s disease: a systematic review and meta-analysis. Diabetes Care 34:2614–2623. https://doi.org/10.2337/dc11-1584 CrossRefPubMedPubMedCentral

33.

Lu L, Fu D-l, Li H-q, Liu A-j, Li J-h, Zheng G-q (2014) Diabetes and risk of Parkinson’s disease: an updated meta-analysis of case-control studies. PLoS ONE 9:e85781. https://doi.org/10.1371/journal.pone.0085781 CrossRefPubMedPubMedCentral

34.

Driver JA, Smith A, Buring JE, Gaziano JM, Kurth T, Logroscino G (2008) Prospective cohort study of type 2 diabetes and the risk of Parkinson’s disease. Diabetes Care 31:2003–2005. https://doi.org/10.2337/dc08-0688 CrossRefPubMedPubMedCentral

35.

Becker C, Brobert GP, Johansson S, Jick SS, Meier CR (2008) Diabetes in patients with idiopathic Parkinson’s disease. Diabetes Care 31:1808–1812. https://doi.org/10.2337/dc08-0479 CrossRefPubMedPubMedCentral

36.

Rhee SY, Han K-D, Kwon H, Park S-E, Park Y-G, Kim Y-H, Yoo S-J, Rhee E-J, Lee W-Y (2020) Association between glycemic status and the risk of Parkinson disease: a nationwide population-based study. Diabetes Care 43:2169–2175. https://doi.org/10.2337/dc19-0760 CrossRefPubMedPubMedCentral

37.

Simon KC, Chen H, Schwarzschild M, Ascherio A (2007) Hypertension, hypercholesterolemia, diabetes, and risk of Parkinson disease. Neurology 69:1688–1695. https://doi.org/10.1212/01.wnl.0000271883.45010.8a CrossRefPubMed

38.

Wang I-k, Lin C-L, Wu Y-Y, Chou C-Y, Lin S-Y, Liu J-H, Yen T-H, Huang C-C, Sung F-C (2014) Increased risk of Parkinson’s disease in patients with end-stage renal disease: a retrospective cohort study. Neuroepidemiology 42:204–210. https://doi.org/10.1159/000358921 CrossRefPubMed

39.

Qiu C, Hu G, Kivipelto M, Laatikainen T, Antikainen R, Fratiglioni L, Jousilahti P, Tuomilehto J (2011) Association of blood pressure and hypertension with the risk of Parkinson disease: the National FINRISK Study (Dallas, Tex : 1979). Hypertension 57:1094–1100. https://doi.org/10.1161/HYPERTENSIONAHA.111.171249 CrossRefPubMed

40.

Talim M (2007) Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients: Response to Targher et al. and Hu et al. Diabetes Care 30:e55–e55. https://doi.org/10.1002/mds.24016 CrossRefPubMed

41.

Hu G, Jousilahti P, Bidel S, Antikainen R, Tuomilehto J (2007) Type 2 diabetes and the risk of Parkinson’s disease. Diabetes Care 30:842–847. https://doi.org/10.2337/dc06-2011 CrossRefPubMed

42.

Sánchez-Gómez A, Díaz Y, Duarte-Salles T, Compta Y, Martí MJ (2021) Prediabetes, type 2 diabetes mellitus and risk of Parkinson’s disease: A population-based cohort study. Parkinsonism Relat Disord 89:22–27

43.

Miyake Y, Tanaka K, Fukushima W, Sasaki S, Kiyohara C, Tsuboi Y et al (2010) Case–control study of risk of Parkinson's disease in relation to hypertension, hypercholesterolemia, and diabetes in Japan. J Neurol Sci 293(1–2):82–86

44.

Sun Y, Chang Y-H, Chen H-F, Su Y-H, Su H-F, Li C-Y (2012) Risk of Parkinson disease onset in patients with diabetes: a 9-year population-based cohort study with age and sex stratifications. Diabetes Care 35(5):1047–1049

45.

Schernhammer E, Hansen J, Rugbjerg K, Wermuth L, Ritz B (2011) Diabetes and the risk of developing Parkinson’s disease in Denmark. Diabetes Care 34(5):1102–1108

46.

Ou R, Wei Q, Hou Y, Zhang L, Liu K, Lin J et al (2021) Effect of diabetes control status on the progression of Parkinson’s disease: A prospective study. Ann Clin Transl Neurol 8(4):887–897

47.

D'Amelio M, Ragonese P, Callari G, Di Benedetto N, Palmeri B, Terruso V et al (2009) Diabetes preceding Parkinson's disease onset. A case–control study. Parkinsonism Relat Disord 15(9):660–664

48.

Yang Y-W, Hsieh T-F, Li C-I, Liu C-S, Lin W-Y, Chiang J-H et al (2017) Increased risk of Parkinson disease with diabetes mellitus in a population-based study. Med 96(3)

49.

Kim WC (2018) Effect of diabetes mellitus on development of Parkinson's disease. Parkinsonism Relat Disord 46:e78

50.

Lee C-J, Yeh Y-C, Liang C-Y, Chen Y-Y (2017) Risk of Parkinson’s Disease in Patients with Type 2 Diabetes Mellitus and Other Comorbidities: A 5-Year Population-Based Cohort Study in Taiwan. Changhua J Med 15(3):128–137

51.

Powers KM, Smith-Weller T, Franklin GM, Longstreth Jr WT, Swanson PD, Checkoway H (2006) Diabetes, smoking, and other medical conditions in relation to Parkinson's disease risk. Parkinsonism Relat Disord 12(3):185–189

52.

Scigliano G, Musicco M, Soliveri P, Piccolo I, Ronchetti G, Girotti F (2006) Reduced risk factors for vascular disorders in Parkinson disease patients: a case-control study. Stroke 37(5):1184–1188

53.

Pupillo E, Cricelli C, Mazzoleni F, Cricelli I, Pasqua A, Pecchioli S et al (2016) Epidemiology of Parkinson's disease: a population-based study in primary care in Italy. Neuroepidemiology 47(1):38–45

54.

Lee SE, Han K, Baek JY, Ko KS, Lee K-U, Koh EH et al (2018) Association between diabetic retinopathy and parkinson disease: the Korean national health insurance service database. J Clin Endocrinol Metab 103(9):3231–3238

55.

Kummer BR, Diaz I, Wu X, Aaroe AE, Chen ML, Ladecola C et al (2019) Associations between cerebrovascular risk factors and parkinson disease. Ann Neurol 86(4):572–581

56.

Azizova TV, Bannikova MV, Grigoryeva ES, Rybkina VL, Hamada N (2020) Occupational exposure to chronic ionizing radiation increases risk of Parkinson's disease incidence in Russian Mayak workers. Int J Epidemiol 49(2):435–447

57.

Kizza J, Lewington S, Mappin‐Kasirer B, Turnbull I, Guo Y, Bian Z et al (2019) Cardiovascular risk factors and Parkinson's disease in 500,000 Chinese adults. Ann Clin Transl Neurol 6(4):624–632

58.

Jacobs BM, Belete D, Bestwick J, Blauwendraat C, Bandres-Ciga S, Heilbron K et al (2020) Parkinson’s disease determinants, prediction and gene–environment interactions in the UK Biobank. J Neurol Neurosurg Psychiatry 91(10):1046–1054

Title: The risk of Parkinson’s disease in diabetic people: an updated systematic review and meta-analysis
Authors: Mobin Azami
Asra Moradkhani
Maryam Afraie
Sorour Khateri
Erfan Sharifian
Kamran Zamani
Yousef Moradi
Publication date: 20-11-2023
Publisher: Springer International Publishing
Keywords: Parkinson's Disease
Diabetes
Published in: Acta Neurologica Belgica
Print ISSN: 0300-9009
Electronic ISSN: 2240-2993
DOI: https://doi.org/10.1007/s13760-023-02424-6

Keynote Webinar | Spotlight on Diet and Diabetes

Springer Medicine

The risk of Parkinson’s disease in diabetic people: an updated systematic review and meta-analysis

Abstract

Background

Methods

Results

Conclusion

Keynote Webinar | Spotlight on Diet and Diabetes

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content