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Research ArticleNeuroimaging Physics/Functional Neuroimaging/CT and MRI Technology

Cognitive and Salience Network Connectivity Changes following a Single Season of Repetitive Head Impact Exposure in High School Football

Mohammad I. Kawas, Kyle M. Atcheson, William C. Flood, Christopher A. Sheridan, Richard A. Barcus, Laura A. Flashman, Thomas W. McAllister, Megan E. Lipford, Jeongchul Kim, Jillian E. Urban, Elizabeth M. Davenport, Christopher G. Vaughan, Kiran K. Solingapuram Sai, Joel D. Stitzel, Joseph A. Maldjian and Christopher T. Whitlow
American Journal of Neuroradiology August 2024, 45 (8) 1116-1123; DOI: https://doi.org/10.3174/ajnr.A8294
Mohammad I. Kawas
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
bDepartment of Physiology (M.I.K.), Faculty of Medicine, University of Jordan, Amman, Jordan
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  • ORCID record for Mohammad I. Kawas
Kyle M. Atcheson
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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William C. Flood
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Christopher A. Sheridan
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Richard A. Barcus
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Laura A. Flashman
cDepartment of Neuropsychology (L.A.F.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Thomas W. McAllister
dDepartment of Psychiatry (T.W.M.), Indiana University School of Medicine, Indianapolis, Indiana
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Megan E. Lipford
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Jeongchul Kim
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Jillian E. Urban
eDepartment of Biomedical Engineering (J.E.U., J.D.S.), Wake Forest School of Medicine, Winston-Salem, North Carolina
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Elizabeth M. Davenport
fDepartment of Radiology (E.M.D., J.A.M), University of Texas Southwestern Medical Center, Dallas, Texas
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Christopher G. Vaughan
gDivision of Pediatric Neuropsychology (C.G.V.), Children’s National Hospital, Washington, DC
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Kiran K. Solingapuram Sai
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Joel D. Stitzel
eDepartment of Biomedical Engineering (J.E.U., J.D.S.), Wake Forest School of Medicine, Winston-Salem, North Carolina
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Joseph A. Maldjian
fDepartment of Radiology (E.M.D., J.A.M), University of Texas Southwestern Medical Center, Dallas, Texas
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Christopher T. Whitlow
aFrom the Department of Radiology (M.I.K., K.M.A., W.C.F., C.A.S., R.A.B., M.E.L., J.K., K.K.S.S., C.T.W.), Wake Forest School of Medicine/Atrium Health Wake Forest Baptist, Winston-Salem, North Carolina
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Abstract

BACKGROUND AND PURPOSE: During a season of high school football, adolescents with actively developing brains experience a considerable number of head impacts. Our aim was to determine whether repetitive head impacts in the absence of a clinically diagnosed concussion during a season of high school football produce changes in cognitive performance or functional connectivity of the salience network and its central hub, the dorsal anterior cingulate cortex.

MATERIALS AND METHODS: Football players were instrumented with the Head Impact Telemetry System during all practices and games, and the helmet sensor data were used to compute a risk-weighted exposure metric (RWEcp), accounting for the cumulative risk during the season. Participants underwent MRI and a cognitive battery (ImPACT) before and shortly after the football season. A control group of noncontact/limited-contact-sport athletes was formed from 2 cohorts: one from the same school and protocol and another from a separate, nearly identical study.

RESULTS: Sixty-three football players and 34 control athletes were included in the cognitive performance analysis. Preseason, the control group scored significantly higher on the ImPACT Visual Motor (P = .04) and Reaction Time composites (P = .006). These differences increased postseason (P = .003, P < .001, respectively). Additionally, the control group had significantly higher postseason scores on the Visual Memory composite (P = .001). Compared with controls, football players showed significantly less improvement in the Verbal (P = .04) and Visual Memory composites (P = .01). A significantly greater percentage of contact athletes had lower-than-expected scores on the Verbal Memory (27% versus 6%), Visual Motor (21% versus 3%), and Reaction Time composites (24% versus 6%). Among football players, a higher RWEcp was significantly associated with greater increments in ImPACT Reaction Time (P = .03) and Total Symptom Scores postseason (P = .006). Fifty-seven football players and 13 control athletes were included in the imaging analyses. Postseason, football players showed significant decreases in interhemispheric connectivity of the dorsal anterior cingulate cortex (P = .026) and within-network connectivity of the salience network (P = .018). These decreases in dorsal anterior cingulate cortex interhemispheric connectivity and within-network connectivity of the salience network were significantly correlated with deteriorating ImPACT Total Symptom (P = .03) and Verbal Memory scores (P = .04).

CONCLUSIONS: Head impact exposure during a single season of high school football is negatively associated with cognitive performance and brain network connectivity. Future studies should further characterize these short-term effects and examine their relationship with long-term sequelae.

ABBREVIATIONS:

ACC
anterior cingulate cortex
BOLD
blood oxygenation level–dependent
dACC
dorsal anterior cingulate cortex
DMN
default mode network
HIE
head impact exposure
IHC
interhemispheric connectivity
RPFC
rostral prefrontal cortex
RWEcp
risk-weighted exposure combined probability
SN
salience network
  • © 2024 by American Journal of Neuroradiology
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American Journal of Neuroradiology: 45 (8)
American Journal of Neuroradiology
Vol. 45, Issue 8
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Cite this article
Mohammad I. Kawas, Kyle M. Atcheson, William C. Flood, Christopher A. Sheridan, Richard A. Barcus, Laura A. Flashman, Thomas W. McAllister, Megan E. Lipford, Jeongchul Kim, Jillian E. Urban, Elizabeth M. Davenport, Christopher G. Vaughan, Kiran K. Solingapuram Sai, Joel D. Stitzel, Joseph A. Maldjian, Christopher T. Whitlow
Cognitive and Salience Network Connectivity Changes following a Single Season of Repetitive Head Impact Exposure in High School Football
American Journal of Neuroradiology Aug 2024, 45 (8) 1116-1123; DOI: 10.3174/ajnr.A8294

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Cognitive Network in Repetitive Head Impacts
Mohammad I. Kawas, Kyle M. Atcheson, William C. Flood, Christopher A. Sheridan, Richard A. Barcus, Laura A. Flashman, Thomas W. McAllister, Megan E. Lipford, Jeongchul Kim, Jillian E. Urban, Elizabeth M. Davenport, Christopher G. Vaughan, Kiran K. Solingapuram Sai, Joel D. Stitzel, Joseph A. Maldjian, Christopher T. Whitlow
American Journal of Neuroradiology Aug 2024, 45 (8) 1116-1123; DOI: 10.3174/ajnr.A8294
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