A critical reappraisal of current staging of Lewy-related pathology in human brain

Acta Neuropathol. 2008 Jul;116(1):1-16. doi: 10.1007/s00401-008-0406-y. Epub 2008 Jul 1.

Abstract

Sporadic Parkinson disease (sPD) or brainstem-predominant type of Lewy body (LB) disease, and dementia with Lewy bodies (DLB), the two most frequent alpha-synucleinopathies, are progressive multisystem neurodegenerative disorders with widespread occurrence of alpha-synuclein (AS) deposits in the central, peripheral, and autonomic nervous system. For both LB-related disorders, staging/classification systems based on semiquantitative assessment of the distribution and progression pattern of Lewy-related/AS pathology are used that are considered to be linked to clinical dysfunctions. In PD, a six-stage system (Braak) has been suggested to indicate a predictable sequence of lesions with ascending progression from medullary and olfactory nuclei to the cortex, the first two presymptomatic stages being related to incidental LB disease, stages 3 and 4 with motor symptoms, and the last two (cortical) stages may be frequently associated with cognitive impairment. DLB, according to consensus pathologic guidelines, by semiquantitative scoring of AS pathology (LB density and distribution) in specific brain regions, is distinguished into three phenotypes (brainstem, transitional/limbic, and diffuse neocortical), also considering concomitant Alzheimer-related pathology. Retrospective clinico-pathologic studies, although largely confirming the staging system, particularly for younger onset PD with long duration, have shown that between 6.3 and 43% of the cases did not follow the proposed caudo-rostral progression pattern of AS pathology. There was sparing of medullary nuclei in 7-8.3% of clinically manifested PD cases with AS inclusions in midbrain and cortex corresponding to Braak stages 4 and 5, whereas mild parkinsonian symptoms were already observed in stages 2 and 3. There is considerable clinical and pathologic overlap between PD (with or without dementia) and DLB, corresponding to Braak LB stages 5 and 6, both frequently associated with variable Alzheimer-type pathology. Dementia often does not correlate with progressed stages of LB pathology, but may also be related to concomitant Alzheimer lesions or mixed pathologies. There is no relationship between Braak LB stage and the clinical severity of PD, and the predictive validity of this concept is doubtful, since large unselected, retrospective autopsy series in 30-55% of elderly subjects with widespread AS/Lewy-related pathology (Braak stages 5 and 6) reported no definite neuropsychiatric symptoms, suggesting considerable cerebral compensatory mechanisms. Applying the original criteria to large dementia samples, 49% of positive cases were not classifiable. Therefore, modified criteria for the categorization of Lewy-related pathology were proposed for patients with a history of dementia. The causes and molecular basis of the not infrequent deviations from the current staging schemes of AS pathology in PD and DLB, its relation to the onset of classical parkinsonian symptoms and for the lack of definite clinical deficits despite widespread AS pathology in the nervous system remain to be elucidated.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Brain / pathology*
  • Guidelines as Topic
  • Humans
  • Lewy Bodies / pathology*
  • Lewy Body Disease / classification*
  • Lewy Body Disease / pathology*