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February 02, 2021; 96 (5) Article

Association of APOE4 and Clinical Variability in Alzheimer Disease With the Pattern of Tau- and Amyloid-PET

View ORCID ProfileRenaud La Joie, Adrienne V. Visani, Orit H. Lesman-Segev, Suzanne L. Baker, Lauren Edwards, Leonardo Iaccarino, David N. Soleimani-Meigooni, Taylor Mellinger, Mustafa Janabi, Zachary A. Miller, David C. Perry, Julie Pham, Amelia Strom, Maria Luisa Gorno-Tempini, Howard J. Rosen, Bruce L. Miller, William J. Jagust, Gil D. Rabinovici
First published December 1, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011270
Renaud La Joie
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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  • ORCID record for Renaud La Joie
Adrienne V. Visani
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Orit H. Lesman-Segev
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Suzanne L. Baker
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Lauren Edwards
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Leonardo Iaccarino
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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David N. Soleimani-Meigooni
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Taylor Mellinger
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Mustafa Janabi
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Zachary A. Miller
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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David C. Perry
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Julie Pham
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Amelia Strom
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Maria Luisa Gorno-Tempini
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Howard J. Rosen
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Bruce L. Miller
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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William J. Jagust
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Gil D. Rabinovici
From the Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences (R.L.J., A.V.V., O.H.L.-V., L.E., L.I., D.N.S.-M., T.M., Z.A.M., D.C.P., J.P., A.S., M.L.G.-T., H.J.R., B.L.M., G.D.R.), and Department of Radiology and Biomedical Imaging (G.D.R.), University of California, San Francisco; Department of Diagnostic Imaging (O.H.L.-V.), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel; Molecular Biophysics and Integrated Bioimaging Division (S.L.B., M.J., W.J.J., G.D.R.), Lawrence Berkeley National Laboratory; and Helen Wills Neuroscience Institute (W.J.J., G.D.R.), University of California Berkeley.
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Citation
Association of APOE4 and Clinical Variability in Alzheimer Disease With the Pattern of Tau- and Amyloid-PET
Renaud La Joie, Adrienne V. Visani, Orit H. Lesman-Segev, Suzanne L. Baker, Lauren Edwards, Leonardo Iaccarino, David N. Soleimani-Meigooni, Taylor Mellinger, Mustafa Janabi, Zachary A. Miller, David C. Perry, Julie Pham, Amelia Strom, Maria Luisa Gorno-Tempini, Howard J. Rosen, Bruce L. Miller, William J. Jagust, Gil D. Rabinovici
Neurology Feb 2021, 96 (5) e650-e661; DOI: 10.1212/WNL.0000000000011270

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Abstract

Objective To assess whether Alzheimer disease (AD) clinical presentation and APOE4 relate to the burden and topography of β-amyloid (Aβ) and tau pathologies using in vivo PET imaging.

Methods We studied 119 Aβ-positive symptomatic patients aged 48–95 years, including 29 patients with logopenic variant primary progressive aphasia (lvPPA) and 21 with posterior cortical atrophy (PCA). Pittsburgh compound B (PiB)–Aβ and flortaucipir (tau)–PET standardized uptake value ratio (SUVR) images were created. General linear models assessed relationships between demographic/clinical variables (phenotype, age), APOE4, and PET (including global cortical and voxelwise SUVR values) while controlling for disease severity using the Clinical Dementia Rating Sum of Boxes.

Results PiB-PET binding showed a widespread cortical distribution with subtle differences across phenotypes and was unrelated to demographic/clinical variables or APOE4. Flortaucipir-PET was commonly elevated in temporoparietal regions, but showed marked phenotype-associated differences, with higher binding observed in occipito-parietal areas for PCA, in left temporal and inferior frontal for lvPPA, and in medial temporal areas for other AD. Cortical flortaucipir-PET binding was higher in younger patients across phenotypes (r = −0.63, 95% confidence interval [CI] −0.72, −0.50), especially in parietal and dorsal prefrontal cortices. The presence of APOE4 was associated with a focal medial temporal flortaucipir-SUVR increase, controlling for all other variables (entorhinal: + 0.310 SUVR, 95% CI 0.091, 0.530).

Conclusions Clinical phenotypes are associated with differential patterns of tau but not amyloid pathology. Older age and APOE4 are not only risk factors for AD but also seem to affect disease expression by promoting a more medial temporal lobe–predominant pattern of tau pathology.

Glossary

Aβ=
β-amyloid;
AD=
Alzheimer disease;
CDR=
Clinical Dementia Rating;
CDR-SB=
Clinical Dementia Rating scale, Sum of Boxes;
CI=
confidence interval;
FTP=
flortaucipir;
FWE=
familywise error;
GLM=
General Linear Model;
GM=
gray matter;
LBNL=
Lawrence Berkeley National Laboratory;
lvPPA=
logopenic variant primary progressive aphasia;
MTL=
medial temporal lobe;
PCA=
posterior cortical atrophy;
PiB=
Pittsburgh compound B;
PVC=
partial volume correction;
SUVR=
standard uptake value ratio;
UCSF=
University of California San Francisco;
VBM=
voxel-based morphometry

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.

  • Editorial, page 191

  • Received March 23, 2020.
  • Accepted in final form September 11, 2020.
  • © 2020 American Academy of Neurology
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