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August 11, 2020; 95 (6) Article

Time course and diagnostic utility of NfL, tau, GFAP, and UCH-L1 in subacute and chronic TBI

Pashtun Shahim, Adam Politis, Andre van der Merwe, Brian Moore, Vindhya Ekanayake, Sara M. Lippa, Yi-Yu Chou, Dzung L. Pham, View ORCID ProfileJohn A. Butman, Ramon Diaz-Arrastia, Henrik Zetterberg, Kaj Blennow, Jessica M. Gill, David L. Brody, View ORCID ProfileLeighton Chan
First published July 8, 2020, DOI: https://doi.org/10.1212/WNL.0000000000009985
Pashtun Shahim
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Adam Politis
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Andre van der Merwe
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Brian Moore
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Vindhya Ekanayake
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Sara M. Lippa
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Yi-Yu Chou
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Dzung L. Pham
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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John A. Butman
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Ramon Diaz-Arrastia
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Henrik Zetterberg
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Kaj Blennow
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Jessica M. Gill
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David L. Brody
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Leighton Chan
From the NIH (P.S., A.P., S.M.L., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); Center for Neuroscience and Regenerative Medicine (P.S., A.v.d.M., B.M., V.E., Y.-Y.C., D.L.P., J.A.B., J.M.G., D.L.B., L.C.); The Henry M. Jackson Foundation for the Advancement of Military Medicine (P.S., A.v.d.M., B.M., V.E., D.L.B.), Bethesda, MD; Department of Psychiatry and Neurochemistry (P.S., H.Z., K.B.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Clinical Neurochemistry Laboratory (P.S., H.Z., K.B.), Sahlgrenska University Hospital, Mölndal, Sweden; National Intrepid Center of Excellence (S.M.L.) and Defense and Veterans Brain Injury Center (S.M.L.), Walter Reed National Military Medical Center, Bethesda, MD; Department of Neurology (R.D.-A.), University of Pennsylvania, Philadelphia; UK Dementia Research Institute at UCL (H.Z.); Department of Neurodegenerative Disease (H.Z.), UCL Institute of Neurology, London, UK; and Uniformed Services University of the Health Sciences (D.L.B.), Bethesda, MD.
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Time course and diagnostic utility of NfL, tau, GFAP, and UCH-L1 in subacute and chronic TBI
Pashtun Shahim, Adam Politis, Andre van der Merwe, Brian Moore, Vindhya Ekanayake, Sara M. Lippa, Yi-Yu Chou, Dzung L. Pham, John A. Butman, Ramon Diaz-Arrastia, Henrik Zetterberg, Kaj Blennow, Jessica M. Gill, David L. Brody, Leighton Chan
Neurology Aug 2020, 95 (6) e623-e636; DOI: 10.1212/WNL.0000000000009985

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This article has a correction. Please see:

  • Time Course and Diagnostic Utility of Nfl, Tau, GFAP, and UCH-L1 in Subacute and Chronic TBI - March 23, 2021
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Abstract

Objective To determine whether neurofilament light (NfL), glial fibrillary acidic protein (GFAP), tau, and ubiquitin C-terminal hydrolase-L1 (UCH-L1) measured in serum relate to traumatic brain injury (TBI) diagnosis, injury severity, brain volume, and diffusion tensor imaging (DTI) measures of traumatic axonal injury (TAI) in patients with TBI.

Methods Patients with TBI (n = 162) and controls (n = 68) were prospectively enrolled between 2011 and 2019. Patients with TBI also underwent serum, functional outcome, and imaging assessments at 30 (n = 30), 90 (n = 48), and 180 (n = 59) days, and 1 (n = 84), 2 (n = 57), 3 (n = 46), 4 (n = 38), and 5 (n = 29) years after injury.

Results At enrollment, patients with TBI had increased serum NfL compared to controls (p < 0.0001). Serum NfL decreased over the course of 5 years but remained significantly elevated compared to controls. Serum NfL at 30 days distinguished patients with mild, moderate, and severe TBI from controls with an area under the receiver-operating characteristic curve (AUROC) of 0.84, 0.92, and 0.92, respectively. At enrollment, serum GFAP was elevated in patients with TBI compared to controls (p < 0.001). GFAP showed a biphasic release in serum, with levels decreasing during the first 6 months of injury but increasing over the subsequent study visits. The highest AUROC for GFAP was measured at 30 days, distinguishing patients with moderate and severe TBI from controls (both 0.89). Serum tau and UCH-L1 showed weak associations with TBI severity and neuroimaging measures. Longitudinally, serum NfL was the only biomarker that was associated with the likely rate of MRI brain atrophy and DTI measures of progression of TAI.

Conclusions Serum NfL shows greater diagnostic and prognostic utility than GFAP, tau, and UCH-L1 for subacute and chronic TBI.

Classification of evidence This study provides Class III evidence that serum NfL distinguishes patients with mild TBI from healthy controls.

Glossary

AD=
axial diffusivity;
AUROC=
area under the receiver operating characteristic curve;
CC=
corpus callosum;
DoD=
Department of Defense;
DTI=
diffusion tensor imaging;
FA=
fractional anisotropy;
GFAP=
glial fibrillary acidic protein;
GM=
gray matter;
GOS-E=
Glasgow Outcome Scale–Extended;
MD=
mean diffusivity;
mTBI=
mild TBI;
NfL=
neurofilament light;
RD=
radial diffusivity;
TAI=
traumatic axonal injury;
TBI=
traumatic brain injury;
UCH-L1=
ubiquitin C-terminal hydrolase-L1;
VA=
Veterans Affairs;
WM=
white matter

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.

  • See the Highlighted Changes supplement, showing the changes made in this updated version: http://links.lww.com/WNL/B340.

  • Editorial, page 235

  • See page 241

  • Class of Evidence: NPub.org/coe

  • Received August 28, 2019.
  • Accepted in final form January 28, 2020.
  • © 2020 American Academy of Neurology
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  • Reader response: Time course and diagnostic utility of NfL, tau, GFAp, and UCH-L1 in subacute and chronic TBI
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    • Davin K. Quinn, MD, Associate Professor, UNM Department of Psychiatry and Behavioral Sciences (Albuquerque)
    Submitted August 05, 2020
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