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August 13, 2013; 81 (7) Article

Very low levels of education and cognitive reserve

A clinicopathologic study

Jose Marcelo Farfel, Ricardo Nitrini, Claudia Kimie Suemoto, Lea Tenenholz Grinberg, Renata Eloah Lucena Ferretti, Renata Elaine Paraizo Leite, Edilaine Tampellini, Luzia Lima, Daniela Souza Farias, Ricardo Caires Neves, Roberta Diehl Rodriguez, Paulo Rossi Menezes, Felipe Fregni, David A. Bennett, Carlos Augusto Pasqualucci, Wilson Jacob Filho, On behalf of the Brazilian Aging Brain Study Group
First published July 19, 2013, DOI: https://doi.org/10.1212/WNL.0b013e3182a08f1b
Jose Marcelo Farfel
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Ricardo Nitrini
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Claudia Kimie Suemoto
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Lea Tenenholz Grinberg
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Renata Eloah Lucena Ferretti
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Renata Elaine Paraizo Leite
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Edilaine Tampellini
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Luzia Lima
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Daniela Souza Farias
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Ricardo Caires Neves
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Roberta Diehl Rodriguez
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Paulo Rossi Menezes
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Felipe Fregni
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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David A. Bennett
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Carlos Augusto Pasqualucci
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Wilson Jacob Filho
From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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From the Departments of Geriatrics (J.M.F., C.K.S., W.J.F.), Neurology (R.N.), Pathology (L.T.G., R.D.R., C.A.P.), and Preventive Medicine (P.R.M.), Discipline of Physiopathology (L.T.G., R.E.P.L.), and Brazilian Aging Brain Study Group, LIM-22 (R.E.P.L., E.T., L.L., D.S.F., R.C.N.), University of São Paulo Medical School, São Paulo, Brazil; Memory and Aging Center (L.T.G.), Department of Neurology, University of California, San Francisco; Medical-Surgical Nursing Department (R.E.L.F.), University of São Paulo Nursing School, São Paulo; Instituto Israelita de Ensino e Pesquisa (E.T., L.L., D.S.F.), Hospital Israelita Brasileiro Albert Einstein, São Paulo, Brazil; Departments of Physical Medicine and Rehabilitation and Neurology (F.F.), Harvard Medical School, Boston, MA; and Rush Alzheimer's Disease Center (D.A.B.), Rush University Medical Center, Chicago, IL.
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Very low levels of education and cognitive reserve
A clinicopathologic study
Jose Marcelo Farfel, Ricardo Nitrini, Claudia Kimie Suemoto, Lea Tenenholz Grinberg, Renata Eloah Lucena Ferretti, Renata Elaine Paraizo Leite, Edilaine Tampellini, Luzia Lima, Daniela Souza Farias, Ricardo Caires Neves, Roberta Diehl Rodriguez, Paulo Rossi Menezes, Felipe Fregni, David A. Bennett, Carlos Augusto Pasqualucci, Wilson Jacob Filho, On behalf of the Brazilian Aging Brain Study Group
Neurology Aug 2013, 81 (7) 650-657; DOI: 10.1212/WNL.0b013e3182a08f1b

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Abstract

Objective: We conducted a clinicopathologic study in a large population with very low levels of education to determine whether very few years of education could contribute to cognitive reserve and modify the relation of neuropathologic indices to dementia.

Methods: In this cross-sectional study, we included 675 individuals 50 years of age or older from the Brazilian Aging Brain Study Group. Cognitive abilities were evaluated through a structured interview with an informant at the time of autopsy, including the Clinical Dementia Rating (CDR) scale. Neuropathologic examinations were performed using immunohistochemistry and following internationally accepted criteria. Multivariate linear regression models were conducted to determine whether the association between cognitive abilities (measured by CDR sum of boxes) and years of education was independent of sociodemographic variables and neuropathologic indices, including neuritic plaques, neurofibrillary tangles, lacunar infarctions, small-vessel disease, and Lewy bodies. In addition, interaction models were used to examine whether education modified the relation between neuropathologic indices and cognition.

Results: Mean education was 3.9 ± 3.5 years. Formal education was associated with a lower CDR sum of boxes (β = −0.197; 95% confidence interval −0.343, −0.052; p = 0.008), after adjustment for sociodemographic variables and neuropathologic indices. Furthermore, education modified the relationship of lacunar infarcts with cognitive abilities (p = 0.04).

Conclusions: Even a few years of formal education contributes to cognitive reserve.

GLOSSARY

AD=
Alzheimer disease;
BABSG=
Brazilian Aging Brain Study Group;
CDR=
Clinical Dementia Rating;
H&E=
hematoxylin & eosin

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received December 26, 2012.
  • Accepted in final form May 8, 2013.
  • © 2013 American Academy of Neurology
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Neurology: 101 (6)

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