Comment

. 2023 Jan;50(2):435-452.

doi: 10.1007/s00259-022-05963-x. Epub 2022 Sep 24.

Associations between near end-of-life flortaucipir PET and postmortem CTE-related tau neuropathology in six former American football players

Michael L Alosco^#¹, Yi Su^#², Thor D Stein^#^{1

3

4

5}, Hillary Protas⁶, Jonathan D Cherry^{1

3}, Charles H Adler⁷, Laura J Balcer⁸, Charles Bernick^{9

10}, Surya Vamsi Pulukuri¹, Bobak Abdolmohammadi¹, Michael J Coleman¹¹, Joseph N Palmisano¹², Yorghos Tripodis^{1

13}, Jesse Mez^{1

4}, Gil D Rabinovici¹⁴, Kenneth L Marek¹⁵, Thomas G Beach¹⁶, Keith A Johnson^{17

18

19

20}, Bertrand Russell Huber^{1

3

5

21}, Inga Koerte^{11

17

22

23

24}, Alexander P Lin^{11

25}, Sylvain Bouix¹¹, Jeffrey L Cummings²⁶, Martha E Shenton^{3

11

20

27}, Eric M Reiman^#²⁸, Ann C McKee^#^{1

3

4

5}, Robert A Stern^#^{29

30}; DIAGNOSE C. T. E. Research Project

Collaborators, Affiliations

Collaborators

DIAGNOSE C. T. E. Research Project:
Eric Reiman, Yi Su, Kewei Chen, Hillary Protas, Connie Boker, Michael L Alosco, Rhoda Au, Robert C Cantu, Lindsay Farrer, Robert Helm, Douglas I Katz, Neil Kowall, Jesse Mez, Gustavo Mercier, James Otis, Robert A Stern, Jason Weller, Irene Simkin, Alondra Andino, Shannon Conneely, Courtney Diamond, Tessa Fagle, Olivia Haller, Tennyson Hunt, Nicole Gullotti, Megan Mariani, Brian Mayville, Kathleen McLaughlin, Mary Nanna, Taylor Platt, Surya Pulukuri, Fiona Rice, Madison Sestak, Michael McClean, Yorghos Tripodis, Douglas Annis, Christine Chaisson, Diane B Dixon, Carolyn Finney, Kerrin Gallagher, Kaitlin Hartlage, Jun Lu, Brett Martin, Emmanuel Ojo, Joseph N Palmisano, Brittany Pine, Janani Ramachandran, Sylvain Bouix, Jennifer Fitzsimmons, Alexander P Lin, Inga K Koerte, Ofer Pasternak, Martha E Shenton, Hector Arcinieago, Tashrif Billah, Elena Bonke, Katherine Breedlove, Eduardo Coello, Michael J Coleman, Leonhard Jung, Huijun Liao, Maria Loy, Elizabeth Rizzoni, Vivian Schultz, Annelise Silva, Brynn Vessey, Tim L T Wiegand, Sarah Banks, Charles Bernick, Jason Miller, Aaron Ritter, Marwan Sabbagh, Raelynn de la Cruz, Jan Durant, Morgan Golceker, Nicolette Harmon, Kaeson Kaylegian, Rachelle Long, Christin Nance, Priscilla Sandoval, Robert W Turner, Kenneth L Marek, Andrew Serrano, Charles H Adler, David W Dodick, Yonas Geda, Jennifer V Wethe, Bryce Falk, Amy Duffy, Marci Howard, Michelle Montague, Thomas Osgood, Debra Babcock, Patrick Bellgowan, Laura Balcer, William Barr, Judith Goldberg, Thomas Wisniewski, Ivan Kirov, Yvonne Lui, Charles Marmar, Lisena Hasanaj, Liliana Serrano, Alhassan Al-Kharafi, Allan George, Sammie Martin, Edward Riley, William Runge, Jeffrey L Cummings, Elaine R Peskind, Elizabeth Colasurdo, Daniel S Marcus, Jenny Gurney, Richard Greenwald, Keith A Johnson

Affiliations

¹ Boston University Alzheimer's Disease Research Center, Boston University CTE Center, Department of Neurology, Boston University School of Medicine, Boston, MA, USA.
² Banner Alzheimer's Institute, Arizona State University, and Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
³ VA Boston Healthcare System, Boston, MA, USA.
⁴ Framingham Heart Study, Framingham, MA, USA.
⁵ VA Bedford Healthcare System, Bedford, MA, USA.
⁶ Banner Alzheimer's Institute, Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
⁷ Department of Neurology, Mayo Clinic College of Medicine, Mayo Clinic Arizona, Scottsdale, AZ, USA.
⁸ Departments of Neurology, Population Health and Ophthalmology, NYU Grossman School of Medicine, New York, NY, USA.
⁹ Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA.
¹⁰ Department of Neurology, University of Washington, Seattle, WA, USA.
¹¹ Psychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital, Boston, MA, USA.
¹² Biostatistics and Epidemiology Data Analytics Center (BEDAC), Boston University School of Public Health, Boston, MA, USA.
¹³ Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA.
¹⁴ Memory & Aging Center, Departments of Neurology, Radiology & Biomedical Imaging, University of California San Francisco, San Francisco, CA, USA.
¹⁵ Institute for Neurodegenerative Disorders, Invicro, LLC, New Haven, CT, USA.
¹⁶ Banner Sun Health Research Institute, Sun City, Arizona, USA.
¹⁷ Massachusetts General Hospital, Boston, MA, USA.
¹⁸ Harvard Medical School, Boston, MA, USA.
¹⁹ Gordon Center for Medical Imaging, Boston, MA, USA.
²⁰ Brigham and Women's Hospital, Boston, MA, USA.
²¹ National Center for PTSD, VA Boston Healthcare, Jamaica Plain, MA, USA.
²² cBRAIN, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Ludwig Maximilians University, Munich, Germany.
²³ Graduate School of Systemic Neurosciences, Ludwig Maximilians University, Munich, Germany.
²⁴ NICUM (NeuroImaging Core Unit Munich), Ludwig Maximilians University, Munich, Germany.
²⁵ Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
²⁶ Chambers-Grundy Center for Transformative Neuroscience, Department of Brain Health, School of Integrated Health Sciences, University of Nevada Las Vegas, Las Vegas, NV, USA.
²⁷ Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
²⁸ Banner Alzheimer's Institute, University of Arizona, Arizona State University, Translational Genomics Research Institute, and Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
²⁹ Boston University Alzheimer's Disease Research Center, Boston University CTE Center, Department of Neurology, Boston University School of Medicine, Boston, MA, USA. bobstern@bu.edu.
³⁰ Departments of Neurosurgery, and Anatomy & Neurobiology, Boston University School of Medicine, Boston, MA, USA. bobstern@bu.edu.

^# Contributed equally.

PMID: 36152064
PMCID: PMC9816291
DOI: 10.1007/s00259-022-05963-x

Comment

Associations between near end-of-life flortaucipir PET and postmortem CTE-related tau neuropathology in six former American football players

Michael L Alosco et al. Eur J Nucl Med Mol Imaging. 2023 Jan.

. 2023 Jan;50(2):435-452.

doi: 10.1007/s00259-022-05963-x. Epub 2022 Sep 24.

Authors

Collaborators

DIAGNOSE C. T. E. Research Project:
Eric Reiman, Yi Su, Kewei Chen, Hillary Protas, Connie Boker, Michael L Alosco, Rhoda Au, Robert C Cantu, Lindsay Farrer, Robert Helm, Douglas I Katz, Neil Kowall, Jesse Mez, Gustavo Mercier, James Otis, Robert A Stern, Jason Weller, Irene Simkin, Alondra Andino, Shannon Conneely, Courtney Diamond, Tessa Fagle, Olivia Haller, Tennyson Hunt, Nicole Gullotti, Megan Mariani, Brian Mayville, Kathleen McLaughlin, Mary Nanna, Taylor Platt, Surya Pulukuri, Fiona Rice, Madison Sestak, Michael McClean, Yorghos Tripodis, Douglas Annis, Christine Chaisson, Diane B Dixon, Carolyn Finney, Kerrin Gallagher, Kaitlin Hartlage, Jun Lu, Brett Martin, Emmanuel Ojo, Joseph N Palmisano, Brittany Pine, Janani Ramachandran, Sylvain Bouix, Jennifer Fitzsimmons, Alexander P Lin, Inga K Koerte, Ofer Pasternak, Martha E Shenton, Hector Arcinieago, Tashrif Billah, Elena Bonke, Katherine Breedlove, Eduardo Coello, Michael J Coleman, Leonhard Jung, Huijun Liao, Maria Loy, Elizabeth Rizzoni, Vivian Schultz, Annelise Silva, Brynn Vessey, Tim L T Wiegand, Sarah Banks, Charles Bernick, Jason Miller, Aaron Ritter, Marwan Sabbagh, Raelynn de la Cruz, Jan Durant, Morgan Golceker, Nicolette Harmon, Kaeson Kaylegian, Rachelle Long, Christin Nance, Priscilla Sandoval, Robert W Turner, Kenneth L Marek, Andrew Serrano, Charles H Adler, David W Dodick, Yonas Geda, Jennifer V Wethe, Bryce Falk, Amy Duffy, Marci Howard, Michelle Montague, Thomas Osgood, Debra Babcock, Patrick Bellgowan, Laura Balcer, William Barr, Judith Goldberg, Thomas Wisniewski, Ivan Kirov, Yvonne Lui, Charles Marmar, Lisena Hasanaj, Liliana Serrano, Alhassan Al-Kharafi, Allan George, Sammie Martin, Edward Riley, William Runge, Jeffrey L Cummings, Elaine R Peskind, Elizabeth Colasurdo, Daniel S Marcus, Jenny Gurney, Richard Greenwald, Keith A Johnson

Affiliations

¹ Boston University Alzheimer's Disease Research Center, Boston University CTE Center, Department of Neurology, Boston University School of Medicine, Boston, MA, USA.
² Banner Alzheimer's Institute, Arizona State University, and Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
³ VA Boston Healthcare System, Boston, MA, USA.
⁴ Framingham Heart Study, Framingham, MA, USA.
⁵ VA Bedford Healthcare System, Bedford, MA, USA.
⁶ Banner Alzheimer's Institute, Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
⁷ Department of Neurology, Mayo Clinic College of Medicine, Mayo Clinic Arizona, Scottsdale, AZ, USA.
⁸ Departments of Neurology, Population Health and Ophthalmology, NYU Grossman School of Medicine, New York, NY, USA.
⁹ Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA.
¹⁰ Department of Neurology, University of Washington, Seattle, WA, USA.
¹¹ Psychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital, Boston, MA, USA.
¹² Biostatistics and Epidemiology Data Analytics Center (BEDAC), Boston University School of Public Health, Boston, MA, USA.
¹³ Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA.
¹⁴ Memory & Aging Center, Departments of Neurology, Radiology & Biomedical Imaging, University of California San Francisco, San Francisco, CA, USA.
¹⁵ Institute for Neurodegenerative Disorders, Invicro, LLC, New Haven, CT, USA.
¹⁶ Banner Sun Health Research Institute, Sun City, Arizona, USA.
¹⁷ Massachusetts General Hospital, Boston, MA, USA.
¹⁸ Harvard Medical School, Boston, MA, USA.
¹⁹ Gordon Center for Medical Imaging, Boston, MA, USA.
²⁰ Brigham and Women's Hospital, Boston, MA, USA.
²¹ National Center for PTSD, VA Boston Healthcare, Jamaica Plain, MA, USA.
²² cBRAIN, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Ludwig Maximilians University, Munich, Germany.
²³ Graduate School of Systemic Neurosciences, Ludwig Maximilians University, Munich, Germany.
²⁴ NICUM (NeuroImaging Core Unit Munich), Ludwig Maximilians University, Munich, Germany.
²⁵ Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
²⁶ Chambers-Grundy Center for Transformative Neuroscience, Department of Brain Health, School of Integrated Health Sciences, University of Nevada Las Vegas, Las Vegas, NV, USA.
²⁷ Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
²⁸ Banner Alzheimer's Institute, University of Arizona, Arizona State University, Translational Genomics Research Institute, and Arizona Alzheimer's Consortium, Phoenix, AZ, USA.
²⁹ Boston University Alzheimer's Disease Research Center, Boston University CTE Center, Department of Neurology, Boston University School of Medicine, Boston, MA, USA. bobstern@bu.edu.
³⁰ Departments of Neurosurgery, and Anatomy & Neurobiology, Boston University School of Medicine, Boston, MA, USA. bobstern@bu.edu.

^# Contributed equally.

PMID: 36152064
PMCID: PMC9816291
DOI: 10.1007/s00259-022-05963-x

Abstract

Purpose: Flourine-18-flortaucipir tau positron emission tomography (PET) was developed for the detection for Alzheimer's disease. Human imaging studies have begun to investigate its use in chronic traumatic encephalopathy (CTE). Flortaucipir-PET to autopsy correlation studies in CTE are needed for diagnostic validation. We examined the association between end-of-life flortaucipir PET and postmortem neuropathological measurements of CTE-related tau in six former American football players.

Methods: Three former National Football League players and three former college football players who were part of the DIAGNOSE CTE Research Project died and agreed to have their brains donated. The six players had flortaucipir (tau) and florbetapir (amyloid) PET prior to death. All brains from the deceased participants were neuropathologically evaluated for the presence of CTE. On average, the participants were 59.0 (SD = 9.32) years of age at time of PET. PET scans were acquired 20.33 (SD = 13.08) months before their death. Using Spearman correlation analyses, we compared flortaucipir standard uptake value ratios (SUVRs) to digital slide-based AT8 phosphorylated tau (p-tau) density in a priori selected composite cortical, composite limbic, and thalamic regions-of-interest (ROIs).

Results: Four brain donors had autopsy-confirmed CTE, all with high stage disease (n = 3 stage III, n = 1 stage IV). Three of these four met criteria for the clinical syndrome of CTE, known as traumatic encephalopathy syndrome (TES). Two did not have CTE at autopsy and one of these met criteria for TES. Concomitant pathology was only present in one of the non-CTE cases (Lewy body) and one of the CTE cases (motor neuron disease). There was a strong association between flortaucipir SUVRs and p-tau density in the composite cortical (ρ = 0.71) and limbic (ρ = 0.77) ROIs. Although there was a strong association in the thalamic ROI (ρ = 0.83), this is a region with known off-target binding. SUVRs were modest and CTE and non-CTE cases had overlapping SUVRs and discordant p-tau density for some regions.

Conclusions: Flortaucipir-PET could be useful for detecting high stage CTE neuropathology, but specificity to CTE p-tau is uncertain. Off-target flortaucipir binding in the hippocampus and thalamus complicates interpretation of these associations. In vivo biomarkers that can detect the specific p-tau of CTE across the disease continuum are needed.

Keywords: Biomarkers; Chronic traumatic encephalopathy; Flortaucipir; Football; Neurodegenerative disease; Positron emission tomography imaging; Repetitive head impacts; Tau.

PubMed Disclaimer

Conflict of interest statement

CHA consulted for Avion, CND Life Sciences, Jazz, and Precon Health. LJB is Editor-in-Chief of the Journal of Neuro-Ophthalmology and is a paid consultant to Biogen (Cambridge, MA, USA). CB receives research support from the Ultimate Fighting Championship, Top Rank promotions, Haymon Boxing, Las Vegas Raiders, and Professional Bull Riders. He is a paid consultant for Aurora Concussion Therapy Systems, Inc. (St. Paul, MN). APL consulted for Agios, Biomarin, and Moncton MRI. He is a co-founder of BrainSpec, Inc. GDR receives research support from Avid Radiopharmaceuticals, GE Healthcare, Life Molecular Imaging, and Genentech. He has served as a paid consultant to Eisai, Eli Lilly, GE Healthcare, Johnson & Johnson, Genentech, and Roche. JLC has provided consultation to Acadia, Alkahest, AlphaCognition, AriBio, Avanir, Axsome, Behren Therapeutics, Biogen, Biohaven, Cassava, Cortexyme, Diadem, EIP Pharma, Eisai, GemVax, Genentech, Green Valley, Grifols, Janssen, LSP, Merck, NervGen, Novo Nordisk, Oligomerix, Ono, Otsuka, PRODEO, Prothena, ReMYND, Renew, Resverlogix, Roche, Signant Health, Suven, United Neuroscience, and Unlearn AI pharmaceutical, assessment, and investment companies. EMR is a compensated scientific advisor for Alkahest, Alzheon, Aural Analytics, Denali, Green Valley, Retromer Therapeutics, and Vaxxinity, and a co-founder of ALZPath. RAS is a paid consultant to Biogen (Cambridge, MA, USA) and Lundbeck (Copenhagen, Denmark). He is a member of the Board of Directors of King-Devick Technologies, Inc. (Chicago, IL, USA), and he receives royalties for published neuropsychological tests from Psychological Assessment Resources, Inc. (Lutz, FL, USA). He has been a member of the Medical Science Committee for the National Collegiate Athletic Association Student-Athlete Concussion Injury Litigation. KM is a consultant for the Michael J Fox Foundation, GE Healthcare, Roche, UCB, BIAL, Denali, Takeda, Cerapsir, UCB, Biohaven, Neuron23, Aprinoia, Astellas, Calico, Inhibikase, Genentech, and Invicro. TGB has been a paid consultant to Acadia Pharmaceuticals and has been a paid consultant, scientific advisory board member, and stock options holder with Vivid Genomics. The remaining authors have no conflicts of interest to disclose. IKK receives funding for a collaborative project and serves as a paid scientific advisor for Abbott. She receives royalties for book chapters. Her spouse is an employee at Siemens AG and stockholder of Siemens Healthineers.

Figures

**Fig. 1**
Phosphorylated tau neuropathology in the dorsolateral frontal cortex and hippocampus of six deceased American football players. Representative images of hyperphosphorylated tau (AT8 antibody) staining from former American football players. Of the six cases, two individuals did not receive a diagnosis of CTE (cases 1 and 2), three had CTE stage III (cases 3–5), and one had CTE stage IV (case 6). Of note, case 4 had low cortical tau burden (i.e., cortical sparring) but had high burden in the medial temporal lobes. The first column depicts a low power overview of cortical regions (A,D,G,J,M,P) (scale bar = 3 mm). All cortical images came from the dorsolateral frontal cortex except case 4, which came from the entorhinal cortex given it was a low cortical burden case of CTE. The second column shows a high-power view of perivascular tau pathology (B,E,H,K,N,Q) (scale bar = 200 µm). No perivascular tau was observed in cases 1 and 2. The third column depicts the posterior hippocampus (C,F,I,L,O,R) (scale bar = 3 mm)

**Fig. 2**
Flortaucipir PET images of six deceased American football players. Five participants had dynamically acquired PET scans after 80 min post-injection for at least 20 min and one participant’s flortaucipir scan ended at 90 min after injection. Voxel-wise SUVR values are represented relative to a cerebellar reference region and scaled for a range of 0–2.0. The flortaucipir PET images are of two former American football players without autopsy-confirmed CTE (a, b), three who had CTE stage III at autopsy (c–e), and one who had CTE stage IV at autopsy (f)

**Fig. 3**
Associations between antemortem flortaucipir SUVRs and postmortem phosphorylated tau density. Cortical composite is the mean of the dorsolateral frontal cortex, orbital-frontal cortex, superior temporal cortex, and the inferior parietal cortex. Limbic composite is the mean of the entorhinal cortex, amygdala, and the hippocampus

**Fig. 4**
Association between antemortem flortaucipir SUVRs and postmortem phosphorylated tau density in cortical regions of interest

**Fig. 5**
Association between antemortem flortaucipir SUVRs and postmortem phosphorylated tau density in limbic regions of interest

See this image and copyright information in PMC

Comment on

Tau PET and multimodal brain imaging in patients at risk for chronic traumatic encephalopathy.
Lesman-Segev OH, La Joie R, Stephens ML, Sonni I, Tsai R, Bourakova V, Visani AV, Edwards L, O'Neil JP, Baker SL, Gardner RC, Janabi M, Chaudhary K, Perry DC, Kramer JH, Miller BL, Jagust WJ, Rabinovici GD. Lesman-Segev OH, et al. Neuroimage Clin. 2019;24:102025. doi: 10.1016/j.nicl.2019.102025. Epub 2019 Oct 17. Neuroimage Clin. 2019. PMID: 31670152 Free PMC article.

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Associations between near end-of-life flortaucipir PET and postmortem CTE-related tau neuropathology in six former American football players

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Associations between near end-of-life flortaucipir PET and postmortem CTE-related tau neuropathology in six former American football players

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