Mild cognitive impairment associated with limbic and neocortical lewy body disease

A clinicopathological study

Jennifer Molano, Bradley F Boeve, Tanis Jill Ferman, Glenn Smith, Joseph E Parisi, Dennis W Dickson, David S Knopman, Neill R Graff Radford, Yonas Endale Geda, John A Lucas, Kejal M Kantarci, Maria Shiung, Clifford R Jr. Jack, Michael Silber, V. Shane Pankratz, Ronald Carl Petersen

Research output: Contribution to journalArticle

147 Citations (Scopus)

Abstract

There are little data on the relationship between Lewy body disease and mild cognitive impairment syndromes. The Mayo Clinic aging and dementia databases in Rochester, Minnesota, and Jacksonville, Florida were queried for cases who were diagnosed with mild cognitive impairment between 1 January 1996 and 30 April 2008, were prospectively followed and were subsequently found to have autopsy-proven Lewy body disease. The presence of rapid eye movement sleep behaviour disorder was specifically assessed. Mild cognitive impairment subtypes were determined by clinical impression and neuropsychological profiles, based on prospective operational criteria. The diagnosis of clinically probable dementia with Lewy bodies was based on the 2005 McKeith criteria. Hippocampal volumes, rate of hippocampal atrophy, and proton magnetic resonance spectroscopy were assessed on available magnetic resonance imaging and spectroscopy scans. Eight subjects were identified; six were male. Seven developed dementia with Lewy bodies prior to death; one died characterized as mild cognitive impairment. The number of cases and median age of onset (range) for specific features were: seven with rapid eye movement sleep behaviour disorder-60 years (27-91 years), eight with cognitive symptoms-69 years (62-89 years), eight with mild cognitive impairment-70.5 years (66-91 years), eight with parkinsonism symptoms-71 years (66-92 years), six with visual hallucinations-72 years (64-90 years), seven with dementia-75 years (67-92 years), six with fluctuations in cognition and/or arousal-76 years (68-92 years) and eight dead-76 years (71-94 years). Rapid eye movement sleep behaviour disorder preceded cognitive symptom onset in six cases by a median of 10 years (2-47 years) and mild cognitive impairment diagnosis by a median of 12 years (3-48 years). The mild cognitive impairment subtypes represented include: two with single domain non-amnestic mild cognitive impairment, three with multi-domain non-amnestic mild cognitive impairment, and three with multi-domain amnestic mild cognitive impairment. The cognitive domains most frequently affected were attention and executive functioning, and visuospatial functioning. Hippocampal volumes and the rate of hippocampal atrophy were, on average, within the normal range in the three cases who underwent magnetic resonance imaging, and the choline/creatine ratio was elevated in the two cases who underwent proton magnetic resonance spectroscopy when they were diagnosed as mild cognitive impairment. On autopsy, six had neocortical-predominant Lewy body disease and two had limbic-predominant Lewy body disease; only one had coexisting high-likelihood Alzheimer's disease. These findings indicate that among Lewy body disease cases that pass through a mild cognitive impairment stage, any cognitive pattern or mild cognitive subtype is possible, with the attention/executive and visuospatial domains most frequently impaired. Hippocampal volume and proton magnetic resonance spectroscopy data were consistent with recent data in dementia with Lewy bodies. All cases with rapid eye movement sleep behaviour disorder and mild cognitive impairment were eventually shown to have autopsy-proven Lewy body disease, indicating that rapid eye movement sleep behaviour disorder plus mild cognitive impairment probably reflects brainstem and cerebral Lewy body disease.

Original languageEnglish (US)
Pages (from-to)540-556
Number of pages17
JournalBrain
Volume133
Issue number2
DOIs
StatePublished - Feb 2010

Fingerprint

Lewy Body Disease
REM Sleep Behavior Disorder
Autopsy
Neurobehavioral Manifestations
Cognitive Dysfunction
Atrophy
Dementia
Magnetic Resonance Imaging
Creatine
Hallucinations
Parkinsonian Disorders
Choline
Arousal
Age of Onset
Cognition
Brain Stem

Keywords

  • Dementia
  • Dementia with Lewy bodies
  • Lewy body disease
  • Mild cognitive impairment
  • Neuropathology

ASJC Scopus subject areas

  • Clinical Neurology

Cite this

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title = "Mild cognitive impairment associated with limbic and neocortical lewy body disease: A clinicopathological study",
abstract = "There are little data on the relationship between Lewy body disease and mild cognitive impairment syndromes. The Mayo Clinic aging and dementia databases in Rochester, Minnesota, and Jacksonville, Florida were queried for cases who were diagnosed with mild cognitive impairment between 1 January 1996 and 30 April 2008, were prospectively followed and were subsequently found to have autopsy-proven Lewy body disease. The presence of rapid eye movement sleep behaviour disorder was specifically assessed. Mild cognitive impairment subtypes were determined by clinical impression and neuropsychological profiles, based on prospective operational criteria. The diagnosis of clinically probable dementia with Lewy bodies was based on the 2005 McKeith criteria. Hippocampal volumes, rate of hippocampal atrophy, and proton magnetic resonance spectroscopy were assessed on available magnetic resonance imaging and spectroscopy scans. Eight subjects were identified; six were male. Seven developed dementia with Lewy bodies prior to death; one died characterized as mild cognitive impairment. The number of cases and median age of onset (range) for specific features were: seven with rapid eye movement sleep behaviour disorder-60 years (27-91 years), eight with cognitive symptoms-69 years (62-89 years), eight with mild cognitive impairment-70.5 years (66-91 years), eight with parkinsonism symptoms-71 years (66-92 years), six with visual hallucinations-72 years (64-90 years), seven with dementia-75 years (67-92 years), six with fluctuations in cognition and/or arousal-76 years (68-92 years) and eight dead-76 years (71-94 years). Rapid eye movement sleep behaviour disorder preceded cognitive symptom onset in six cases by a median of 10 years (2-47 years) and mild cognitive impairment diagnosis by a median of 12 years (3-48 years). The mild cognitive impairment subtypes represented include: two with single domain non-amnestic mild cognitive impairment, three with multi-domain non-amnestic mild cognitive impairment, and three with multi-domain amnestic mild cognitive impairment. The cognitive domains most frequently affected were attention and executive functioning, and visuospatial functioning. Hippocampal volumes and the rate of hippocampal atrophy were, on average, within the normal range in the three cases who underwent magnetic resonance imaging, and the choline/creatine ratio was elevated in the two cases who underwent proton magnetic resonance spectroscopy when they were diagnosed as mild cognitive impairment. On autopsy, six had neocortical-predominant Lewy body disease and two had limbic-predominant Lewy body disease; only one had coexisting high-likelihood Alzheimer's disease. These findings indicate that among Lewy body disease cases that pass through a mild cognitive impairment stage, any cognitive pattern or mild cognitive subtype is possible, with the attention/executive and visuospatial domains most frequently impaired. Hippocampal volume and proton magnetic resonance spectroscopy data were consistent with recent data in dementia with Lewy bodies. All cases with rapid eye movement sleep behaviour disorder and mild cognitive impairment were eventually shown to have autopsy-proven Lewy body disease, indicating that rapid eye movement sleep behaviour disorder plus mild cognitive impairment probably reflects brainstem and cerebral Lewy body disease.",
keywords = "Dementia, Dementia with Lewy bodies, Lewy body disease, Mild cognitive impairment, Neuropathology",
author = "Jennifer Molano and Boeve, {Bradley F} and Ferman, {Tanis Jill} and Glenn Smith and Parisi, {Joseph E} and Dickson, {Dennis W} and Knopman, {David S} and {Graff Radford}, {Neill R} and Geda, {Yonas Endale} and Lucas, {John A} and Kantarci, {Kejal M} and Maria Shiung and Jack, {Clifford R Jr.} and Michael Silber and Pankratz, {V. Shane} and Petersen, {Ronald Carl}",
year = "2010",
month = "2",
doi = "10.1093/brain/awp280",
language = "English (US)",
volume = "133",
pages = "540--556",
journal = "Brain",
issn = "0006-8950",
publisher = "Oxford University Press",
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T1 - Mild cognitive impairment associated with limbic and neocortical lewy body disease

T2 - A clinicopathological study

AU - Molano, Jennifer

AU - Boeve, Bradley F

AU - Ferman, Tanis Jill

AU - Smith, Glenn

AU - Parisi, Joseph E

AU - Dickson, Dennis W

AU - Knopman, David S

AU - Graff Radford, Neill R

AU - Geda, Yonas Endale

AU - Lucas, John A

AU - Kantarci, Kejal M

AU - Shiung, Maria

AU - Jack, Clifford R Jr.

AU - Silber, Michael

AU - Pankratz, V. Shane

AU - Petersen, Ronald Carl

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N2 - There are little data on the relationship between Lewy body disease and mild cognitive impairment syndromes. The Mayo Clinic aging and dementia databases in Rochester, Minnesota, and Jacksonville, Florida were queried for cases who were diagnosed with mild cognitive impairment between 1 January 1996 and 30 April 2008, were prospectively followed and were subsequently found to have autopsy-proven Lewy body disease. The presence of rapid eye movement sleep behaviour disorder was specifically assessed. Mild cognitive impairment subtypes were determined by clinical impression and neuropsychological profiles, based on prospective operational criteria. The diagnosis of clinically probable dementia with Lewy bodies was based on the 2005 McKeith criteria. Hippocampal volumes, rate of hippocampal atrophy, and proton magnetic resonance spectroscopy were assessed on available magnetic resonance imaging and spectroscopy scans. Eight subjects were identified; six were male. Seven developed dementia with Lewy bodies prior to death; one died characterized as mild cognitive impairment. The number of cases and median age of onset (range) for specific features were: seven with rapid eye movement sleep behaviour disorder-60 years (27-91 years), eight with cognitive symptoms-69 years (62-89 years), eight with mild cognitive impairment-70.5 years (66-91 years), eight with parkinsonism symptoms-71 years (66-92 years), six with visual hallucinations-72 years (64-90 years), seven with dementia-75 years (67-92 years), six with fluctuations in cognition and/or arousal-76 years (68-92 years) and eight dead-76 years (71-94 years). Rapid eye movement sleep behaviour disorder preceded cognitive symptom onset in six cases by a median of 10 years (2-47 years) and mild cognitive impairment diagnosis by a median of 12 years (3-48 years). The mild cognitive impairment subtypes represented include: two with single domain non-amnestic mild cognitive impairment, three with multi-domain non-amnestic mild cognitive impairment, and three with multi-domain amnestic mild cognitive impairment. The cognitive domains most frequently affected were attention and executive functioning, and visuospatial functioning. Hippocampal volumes and the rate of hippocampal atrophy were, on average, within the normal range in the three cases who underwent magnetic resonance imaging, and the choline/creatine ratio was elevated in the two cases who underwent proton magnetic resonance spectroscopy when they were diagnosed as mild cognitive impairment. On autopsy, six had neocortical-predominant Lewy body disease and two had limbic-predominant Lewy body disease; only one had coexisting high-likelihood Alzheimer's disease. These findings indicate that among Lewy body disease cases that pass through a mild cognitive impairment stage, any cognitive pattern or mild cognitive subtype is possible, with the attention/executive and visuospatial domains most frequently impaired. Hippocampal volume and proton magnetic resonance spectroscopy data were consistent with recent data in dementia with Lewy bodies. All cases with rapid eye movement sleep behaviour disorder and mild cognitive impairment were eventually shown to have autopsy-proven Lewy body disease, indicating that rapid eye movement sleep behaviour disorder plus mild cognitive impairment probably reflects brainstem and cerebral Lewy body disease.

AB - There are little data on the relationship between Lewy body disease and mild cognitive impairment syndromes. The Mayo Clinic aging and dementia databases in Rochester, Minnesota, and Jacksonville, Florida were queried for cases who were diagnosed with mild cognitive impairment between 1 January 1996 and 30 April 2008, were prospectively followed and were subsequently found to have autopsy-proven Lewy body disease. The presence of rapid eye movement sleep behaviour disorder was specifically assessed. Mild cognitive impairment subtypes were determined by clinical impression and neuropsychological profiles, based on prospective operational criteria. The diagnosis of clinically probable dementia with Lewy bodies was based on the 2005 McKeith criteria. Hippocampal volumes, rate of hippocampal atrophy, and proton magnetic resonance spectroscopy were assessed on available magnetic resonance imaging and spectroscopy scans. Eight subjects were identified; six were male. Seven developed dementia with Lewy bodies prior to death; one died characterized as mild cognitive impairment. The number of cases and median age of onset (range) for specific features were: seven with rapid eye movement sleep behaviour disorder-60 years (27-91 years), eight with cognitive symptoms-69 years (62-89 years), eight with mild cognitive impairment-70.5 years (66-91 years), eight with parkinsonism symptoms-71 years (66-92 years), six with visual hallucinations-72 years (64-90 years), seven with dementia-75 years (67-92 years), six with fluctuations in cognition and/or arousal-76 years (68-92 years) and eight dead-76 years (71-94 years). Rapid eye movement sleep behaviour disorder preceded cognitive symptom onset in six cases by a median of 10 years (2-47 years) and mild cognitive impairment diagnosis by a median of 12 years (3-48 years). The mild cognitive impairment subtypes represented include: two with single domain non-amnestic mild cognitive impairment, three with multi-domain non-amnestic mild cognitive impairment, and three with multi-domain amnestic mild cognitive impairment. The cognitive domains most frequently affected were attention and executive functioning, and visuospatial functioning. Hippocampal volumes and the rate of hippocampal atrophy were, on average, within the normal range in the three cases who underwent magnetic resonance imaging, and the choline/creatine ratio was elevated in the two cases who underwent proton magnetic resonance spectroscopy when they were diagnosed as mild cognitive impairment. On autopsy, six had neocortical-predominant Lewy body disease and two had limbic-predominant Lewy body disease; only one had coexisting high-likelihood Alzheimer's disease. These findings indicate that among Lewy body disease cases that pass through a mild cognitive impairment stage, any cognitive pattern or mild cognitive subtype is possible, with the attention/executive and visuospatial domains most frequently impaired. Hippocampal volume and proton magnetic resonance spectroscopy data were consistent with recent data in dementia with Lewy bodies. All cases with rapid eye movement sleep behaviour disorder and mild cognitive impairment were eventually shown to have autopsy-proven Lewy body disease, indicating that rapid eye movement sleep behaviour disorder plus mild cognitive impairment probably reflects brainstem and cerebral Lewy body disease.

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KW - Neuropathology

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