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August 25, 2020; 95 (8) Article

Association of cerebrovascular reactivity and Alzheimer pathologic markers with cognitive performance

Sandeepa Sur, Zixuan Lin, Yang Li, Sevil Yasar, Paul Rosenberg, View ORCID ProfileAbhay Moghekar, Xirui Hou, Rita Kalyani, Kaisha Hazel, George Pottanat, Cuimei Xu, Peter van Zijl, Jay Pillai, Peiying Liu, Marilyn Albert, Hanzhang Lu
First published July 13, 2020, DOI: https://doi.org/10.1212/WNL.0000000000010133
Sandeepa Sur
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Zixuan Lin
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Yang Li
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Sevil Yasar
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Paul Rosenberg
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Abhay Moghekar
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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  • ORCID record for Abhay Moghekar
Xirui Hou
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Rita Kalyani
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Kaisha Hazel
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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George Pottanat
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Cuimei Xu
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Peter van Zijl
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Jay Pillai
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Peiying Liu
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Marilyn Albert
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Hanzhang Lu
From the Departments of Radiology (S.S., Z.L., Y.L., X.H., K.H., G.P., C.X., P.v.Z., J.P., P.L., H.L.), Biomedical Engineering (Z.L., X.H., H.L.), Medicine (S.Y., R.K.), Psychiatry and Behavioral Sciences (P.R.), Neurology (A.M., M.A.), and Neurosurgery (J.P.), Johns Hopkins University, School of Medicine; and F.M. Kirby Research Center (P.v.Z., H.L.), Kennedy Krieger Institute, Baltimore, MD.
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Citation
Association of cerebrovascular reactivity and Alzheimer pathologic markers with cognitive performance
Sandeepa Sur, Zixuan Lin, Yang Li, Sevil Yasar, Paul Rosenberg, Abhay Moghekar, Xirui Hou, Rita Kalyani, Kaisha Hazel, George Pottanat, Cuimei Xu, Peter van Zijl, Jay Pillai, Peiying Liu, Marilyn Albert, Hanzhang Lu
Neurology Aug 2020, 95 (8) e962-e972; DOI: 10.1212/WNL.0000000000010133

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Abstract

Objective To determine whether MRI-based cerebrovascular reactivity (CVR) can predict cognitive performance independently of Alzheimer pathologic markers, we studied the relationship between cognition, CVR, and CSF-derived β-amyloid42 (Aβ42) and tau in a group of elderly individuals with mixed Alzheimer and vascular cognitive impairment and dementia.

Methods This was a cross-sectional study of 72 participants 69 ± 8 years of age consisting of individuals with normal cognition (n = 28) and cognitive impairment (n = 44) (including 36 with mild cognitive impairment [MCI] and 8 with mild dementia). CVR was measured with hypercapnia-MRI. Whole-brain CVR (percent blood oxygen level–dependent per 1 mm Hg Etco2) was used to estimate vasodilatory capacity. Montreal Cognitive Assessment (MoCA) scores, cognitive domains scores, and a global composite cognitive score were obtained. AD biomarkers included CSF assays of Aβ42 and tau.

Results Whole-brain CVR was lower in the impaired (mean ± SE, 0.132 ± 0.006%/mm Hg) compared to the normal (0.151 ± 0.007%/mm Hg) group (β = −0.02%/mm Hg; 95% confidence interval [CI] −0.038 to −0.001). After adjustment for CSF Aβ42 and tau, higher whole-brain CVR was associated with better performance on the MoCA (β = 29.64, 95% CI 9.94–49.34) and with a global composite cognitive score (β = 4.32, 95% CI 0.05–8.58). When the CVR marker was compared with the Fazekas score based on white matter hyperintensities and vascular risk-score in a single regression model predicting the MoCA score, only CVR revealed a significant effect (β = 28.09, 95% CI 6.14–50.04), while the other 2 measures were not significant.

Conclusions CVR was significantly associated with cognitive performance independently of AD pathology. Whole-brain CVR may be a useful biomarker for evaluating cognitive impairment related to vascular disease in older individuals.

Classification of evidence This study provides Class II evidence that CVR was significantly associated with cognitive performance independent of AD pathology.

Glossary

Aβ42=
β-amyloid42;
AD=
Alzheimer disease;
ARIC=
Atherosclerosis Risk in Communities;
BMI=
body mass index;
BOLD=
blood oxygen level–dependent;
CI=
confidence interval;
CVR=
cerebrovascular reactivity;
FLAIR=
fluid-attenuated inversion recovery;
MCI=
mild cognitive impairment;
MoCA=
Montreal Cognitive Assessment;
TE=
echo time;
TI=
inversion time;
TR=
repetition time;
VCID=
vascular cognitive impairment and dementia;
VRS=
vascular risk score;
WMH=
white matter hyperintensities

Footnotes

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

  • Class of Evidence: NPub.org/coe

  • Received September 20, 2019.
  • Accepted in final form March 17, 2020.
  • © 2020 American Academy of Neurology
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