Journal of Korean Medical Science

Korean Acad Medical Sciences (대한의학회)
권호 표지
DOI QR코드

DOI QR Code

The Prevalence of Cerebral Microbleeds in Non-Demented Parkinson's Disease Patients

  • Kim, Kyeong Joon (Department of Neurology, Dongguk University Ilsan Hospital) ;
  • Bae, Yun Jung (Department of Radiology, Seoul National University Bundang Hospital, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Kim, Jong-Min (Department of Neurology, Seoul National University Bundang Hospital, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Kim, Beom Joon (Department of Neurology, Seoul National University Bundang Hospital, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Oh, Eung Seok (Department of Neurology, Chungnam National University Hospital, Chungnam National University College of Medicine) ;
  • Yun, Ji Young (Department of Neurology, Ewha Womans University Mokdong Hospital, Ewha Womans University College of Medicine) ;
  • Kim, Ji Seon (Department of Neurology, Chungbuk National University Hospital, Chungbuk National University College of Medicine) ;
  • Kim, Han-Joon (Department of Neurology, Seoul National University Bundang Hospital, Seoul National University Hospital, Seoul National University College of Medicine)
  • Received : 2018.05.27
  • Accepted : 2018.08.12
  • Published : 2018.11.12
⟨ Previous Next ⟩

Abstract

Background: Cerebral microbleeds (CMBs) are associated with cerebrovascular risk factors and cognitive dysfunction among patients with Parkinson's disease (PD). However, whether CMBs themselves are associated with PD is to be elucidated. Methods: We analyzed the presence of CMBs using 3-Tesla brain magnetic resonance imaging in non-demented patients with PD and in age-, sex-, and hypertension-matched control subjects. PD patients were classified according to their motor subtypes: tremor-dominant, intermediate, and postural instability-gait disturbance (PIGD). Other cerebrovascular risk factors and small vessel disease (SVD) burdens were also evaluated. Results: Two-hundred and five patients with PD and 205 control subjects were included. The prevalence of CMBs was higher in PD patients than in controls (16.1% vs. 8.8%; odds ratio [OR], 2.126; P = 0.019); CMBs in the lobar area showed a significant difference between PD patients and controls (11.7% vs. 5.9%; OR, 2.234; P = 0.032). According to the motor subtype, CMBs in those with PIGD type showed significant difference from controls with respect to the overall brain area (21.1% vs. 8.9%; OR, 2.759; P = 0.010) and lobar area (14.6% vs. 4.9%; OR, 3.336; P = 0.016). Among PD patients, those with CMBs had higher age and more evidence of SVDs than those without CMBs. Conclusion: We found that CMBs are more frequent in PD patients than in controls, especially in those with the PIGD subtype and CMBs on the lobar area. Further study investigating the pathogenetic significance of CMBs is required.

Keywords

References

  1. Fazekas F, Kleinert R, Roob G, Kleinert G, Kapeller P, Schmidt R, et al. Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol 1999;20(4):637-42.
  2. Jeerakathil T, Wolf PA, Beiser A, Hald JK, Au R, Kase CS, et al. Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham Study. Stroke 2004;35(8):1831-5. https://doi.org/10.1161/01.STR.0000131809.35202.1b
  3. Roob G, Schmidt R, Kapeller P, Lechner A, Hartung HP, Fazekas F. MRI evidence of past cerebral microbleeds in a healthy elderly population. Neurology 1999;52(5):991-4. https://doi.org/10.1212/WNL.52.5.991
  4. Tanaka A, Ueno Y, Nakayama Y, Takano K, Takebayashi S. Small chronic hemorrhages and ischemic lesions in association with spontaneous intracerebral hematomas. Stroke 1999;30(8):1637-42. https://doi.org/10.1161/01.STR.30.8.1637
  5. Yates PA, Villemagne VL, Ellis KA, Desmond PM, Masters CL, Rowe CC. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Front Neurol 2014;4:205.
  6. Kim JH, Park J, Kim YH, Ma HI, Kim YJ. Characterization of cerebral microbleeds in idiopathic Parkinson's disease. Eur J Neurol 2015;22(2):377-83. https://doi.org/10.1111/ene.12584
  7. Ham JH, Yi H, Sunwoo MK, Hong JY, Sohn YH, Lee PH. Cerebral microbleeds in patients with Parkinson's disease. J Neurol 2014;261(8):1628-35. https://doi.org/10.1007/s00415-014-7403-y
  8. Kim SW, Chung SJ, Oh YS, Yoon JH, Sunwoo MK, Hong JY, et al. Cerebral microbleeds in patients with dementia with Lewy bodies and Parkinson disease dementia. AJNR Am J Neuroradiol 2015;36(9):1642-7. https://doi.org/10.3174/ajnr.A4337
  9. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55(3):181-4. https://doi.org/10.1136/jnnp.55.3.181
  10. Han C, Jo SA, Jo I, Kim E, Park MH, Kang Y. An adaptation of the Korean mini-mental state examination (K-MMSE) in elderly Koreans: demographic influence and population-based norms (the AGE study). Arch Gerontol Geriatr 2008;47(3):302-10. https://doi.org/10.1016/j.archger.2007.08.012
  11. Kim JI, Sunwoo MK, Sohn YH, Lee PH, Hong JY. The MMSE and MoCA for screening cognitive impairment in less educated patients with Parkinson's disease. J Mov Disord 2016;9(3):152-9. https://doi.org/10.14802/jmd.16020
  12. Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, et al. Variable expression of Parkinson's disease: a base-line analysis of the DATATOP cohort. Neurology 1990;40(10):1529-34. https://doi.org/10.1212/WNL.40.10.1529
  13. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, et al. The seventh report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure: the JNC 7 report. JAMA 2003;289(19):2560-72. https://doi.org/10.1001/jama.289.19.2560
  14. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2014;37 Suppl 1:S81-90. https://doi.org/10.2337/dc14-S081
  15. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation 2002;106(25):3143-421. https://doi.org/10.1161/circ.106.25.3143
  16. Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009;8(2):165-74. https://doi.org/10.1016/S1474-4422(09)70013-4
  17. Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol 2013;12(5):483-97. https://doi.org/10.1016/S1474-4422(13)70060-7
  18. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol 1987;149(2):351-6. https://doi.org/10.2214/ajr.149.2.351
  19. Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology 2014;83(14):1228-34. https://doi.org/10.1212/WNL.0000000000000837
  20. Shoamanesh A, Kwok CS, Benavente O. Cerebral microbleeds: histopathological correlation of neuroimaging. Cerebrovasc Dis 2011;32(6):528-34. https://doi.org/10.1159/000331466
  21. Petrou M, Dwamena BA, Foerster BR, MacEachern MP, Bohnen NI, Muller ML, et al. Amyloid deposition in Parkinson's disease and cognitive impairment: a systematic review. Mov Disord 2015;30(7):928-35. https://doi.org/10.1002/mds.26191
  22. Masliah E, Rockenstein E, Veinbergs I, Sagara Y, Mallory M, Hashimoto M, et al. Beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci U S A 2001;98(21):12245-50. https://doi.org/10.1073/pnas.211412398
  23. Mrak RE, Griffin WS. Glia and their cytokines in progression of neurodegeneration. Neurobiol Aging 2005;26(3):349-54. https://doi.org/10.1016/j.neurobiolaging.2004.05.010
  24. Townsend KP, Obregon D, Quadros A, Patel N, Volmar C, Paris D, et al. Proinflammatory and vasoactive effects of Abeta in the cerebrovasculature. Ann N Y Acad Sci 2002;977(1):65-76. https://doi.org/10.1111/j.1749-6632.2002.tb04799.x
  25. Shoamanesh A, Preis SR, Beiser AS, Vasan RS, Benjamin EJ, Kase CS, et al. Inflammatory biomarkers, cerebral microbleeds, and small vessel disease: Framingham Heart Study. Neurology 2015;84(8):825-32. https://doi.org/10.1212/WNL.0000000000001279
  26. Rosidi NL, Zhou J, Pattanaik S, Wang P, Jin W, Brophy M, et al. Cortical microhemorrhages cause local inflammation but do not trigger widespread dendrite degeneration. PLoS One 2011;6(10):e26612. https://doi.org/10.1371/journal.pone.0026612
  27. Hirsch EC, Jenner P, Przedborski S. Pathogenesis of Parkinson's disease. Mov Disord 2013;28(1):24-30. https://doi.org/10.1002/mds.25032
  28. Przedborski S. Neuroinflammation and Parkinson's disease. Handb Clin Neurol 2007;83:535-51.
  29. Hirsch EC, Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 2009;8(4):382-97. https://doi.org/10.1016/S1474-4422(09)70062-6
  30. Nagatsu T, Mogi M, Ichinose H, Togari A. Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm Suppl 2000;(60):277-90.
  31. Yamashiro K, Tanaka R, Hoshino Y, Hatano T, Nishioka K, Hattori N. The prevalence and risk factors of cerebral microbleeds in patients with Parkinson's disease. Parkinsonism Relat Disord 2015;21(9):1076-81. https://doi.org/10.1016/j.parkreldis.2015.06.019

Cited by

  1. Ethnic Variation in the Manifestation of Parkinson’s Disease: A Narrative Review vol.10, pp.1, 2018, https://doi.org/10.3233/jpd-191763
  2. Total Cerebral Small Vessel Score Association With Hoehn and Yahr Stage in Parkinson’s Disease vol.13, pp.None, 2018, https://doi.org/10.3389/fnagi.2021.682776
  3. Amyloid related cerebral microbleed and plasma Aβ40 are associated with cognitive decline in Parkinson’s disease vol.11, pp.1, 2018, https://doi.org/10.1038/s41598-021-86617-0