Memory Impairments Associated With Mild Traumatic Brain Injury: A Critically Appraised Topic

in International Journal of Athletic Therapy and Training

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Karlee BurnsDepartment of Kinesiology, Temple University, Philadelphia, PA, USA

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Leah SanfordDepartment of Neuroscience, Temple University, Philadelphia, PA, USA

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Ryan TierneyDepartment of Health and Rehabilitation Sciences, Temple University, Philadelphia, PA, USA

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Jane McDevittDepartment of Health and Rehabilitation Sciences, Temple University, Philadelphia, PA, USA

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Clinical Question: Do sports-related mild traumatic brain injury in adolescents and young adults produce changes that can be identified with functional magnetic resonance imaging that are associated with memory impairment? Clinical Bottom Line: After sport-related mild traumatic brain injury, functional magnetic resonance imaging identified inconsistent structural changes (e.g., cortical thickness changes, brain activation patterns), and negative performance changes in memory function (e.g., lower neuropsychological scores) in adolescents and young adults 9 days to more than a year following injury.

Key Points

  1. Adolescents and young adults with sport-related mild traumatic brain injury (i.e., 9 days to 12 months postinjury) performed worse on memory tests than healthy controls.
  2. There is low-level evidence suggesting structural changes (e.g., cortical thinning) are occurring following sport-related mild traumatic brain injury in areas of the brain associated with memory function (e.g., hippocampus, prefrontal cortex) within approximately 1 year following the individuals last injury.
  3. Clinicians (e.g., athletic trainers, physicians) should be familiar with sport-related mild traumatic brain injury screening, be able to identify lingering symptoms, and manage individuals after mild traumatic brain injury following best practices to reduce repeated injury, increase time between potential injury, and improve overall patient outcomes.

Clinical Scenario

Mild traumatic brain injury (mTBI) is an acute brain injury resulting from an impact event to the head or body.1,2 Memory impairment (e.g., difficulty remembering, confusion) is a common symptom following mTBI.3 Neuroimaging (e.g., functional magnetic resonance imaging [fMRI]) has established that memory functions occur in the hippocampal, cerebellum, and prefrontal cortex regions of the brain.4,5 If memory functions are impaired, neuropathological changes are likely to have occurred in these regions.6 These neuropathological changes are referred to as a secondary injury and in mTBI are commonly associated with white and gray matter volumetric and cerebral cortex thickness changes (e.g., cortical thinning).7,8

Memory, cognitive function, sensory processing, and control of movement are routinely identified with the use of fMRI.9 Blood-oxygen-level-dependent (BOLD) contrast is currently the standard for neuroimaging studies in identifying functional deficits. BOLD fMRI measures oxygen concentration changes in the tissue, blood volume changes, and tissue perfusion.9 There is evidence of a relationship between BOLD images and structural changes in white matter microstructural changes in cortical regions following mTBI.10 Performing BOLD fMRI simultaneously with neuropsychological testing (e.g., cognitive tasks) and determining differences in BOLD activation levels identifies areas of decreased brain activity.11

There are no direct treatments for memory impairments following brain injury, only exercises to help prevent progression.12 As a result, mTBI patients may experience prolonged memory impairments depending on severity of the injury.6 Prolonged memory impairments may be due to impact-induced volume loss in the hippocampus region, resulting in a disruption of its two main neurotransmitters, glutamate, and gamma aminobutyric acid. An imbalance in synaptic currents of these two key neurotransmitters are a potential cause of the secondary injuries in the hippocampus (e.g., loss/injury of dendritic spines).13 Memory impairment is commonly assessed clinically after sport-related mTBI with validated assessments evaluating executive function, working and spatial memory, and verbal fluency.14,15 Individuals with mTBI have performed worse on these memory assessments than peers without injury.16,17 However, the relationship between fMRI findings and clinical tests has not been well established though this is essential in interpreting the relationships between imaging measures and clinical outcomes. Therefore, the purpose of this CAT was to determine if sport-related mTBI was associated with structural (e.g., cortical thinning) or functional (e.g., decreased tissue perfusion) changes visible with fMRI that were associated with memory impairments (i.e., worse performance during memory assessment).

Focused Clinical Question

Do sports-related mTBIs in adolescents and young adults produce changes that can be identified with fMRI that are associated with memory impairment?

Search Strategy

A search of PubMed and Google Scholar was conducted using the following patient group, intervention, comparison, outcome set up to generate a Boolean phrase. Boolean phrase: “mTBI” OR “traumatic brain injury,” AND “fMRI” OR “functional magnetic resonance imaging,” AND “memory” OR “memory function,” AND “sport.”

  • - Patient group: diagnosed sports-related mTBI patients

  • - Intervention: fMRI

  • - Comparison: none

  • - Outcome: objective measure of memory impairment

Inclusion Criteria

Patients mTBI occurred as a result of a sports-related incident.

  • - Included memory function as an outcome measure

  • - Utilized fMRI

  • - Performed within the past 10 years

Exclusion Criteria

  • - Patients mTBI occurred outside of sport setting

  • - Patient population age was under 10 years or over 30 years

  • - Did not include imaging

Evidence Quality Assessment

Validity of the included studies were assessed using the STROBE checklist for cohort studies and the Center of Evidence-Based Management critical appraisal of case study forms.18 For each selected study, two researchers independently scored the articles, and the averages were used for strength of recommendation.

Results of Search

In total, the search yielded 133 records (5 from PubMed, 128 from Google Scholar). A summary of search results can be seen in Figure 1. The articles in Table 1 met all inclusion criteria for this CAT. All included articles used a case-control study design. There were differences in fMRI findings between studies; however, all studies found changes related to brain activity and memory function in those that had sustained a mTBI. Individuals with previous mTBI performed worse on the memory assessments or had to use additional compensatory mechanisms, identified with fMRI, to maintain memory performance.

Figure 1
Figure 1

—Included studies.

Citation: International Journal of Athletic Therapy and Training 27, 5; 10.1123/ijatt.2021-0020

Results of Evidence Assessment

Each study was assessed using the STROBE checklist. The List et al.,19 Keightley et al.,20 and Westfall et al.21 studies received a score of 20/22. The Slobounov et al.22 study received a score of 18/22.

Clinical Bottom Line

Although results suggest that there is low-level evidence of abnormal fMRI results in sport-related mTBI groups (e.g., cortical thinning), these adolescents and young adults also performed worse than the control groups on the memory-specific neuropsychological tests (Rey Auditory Verbal Learning Test [AVLT] Delayed Memory Recall and Verbal Fluency, Regensburger Verbal Fluency Test [RWT]) as soon as 9 days after injury and up to more than 1-year postinjury.19,20 As memory problems (e.g., difficulty concentrating) are a commonly reported mTBI symptom,23 there is reason to believe that loss and/or injury of dendritic spines in the hippocampal or prefrontal cortex regions are present.19 Currently, there are no direct treatments for memory impairment or for the physiological effects in the brain due to secondary injury; however, there are ways to prevent progression.19 These neuropathological changes may occur immediately upon injury or have a sustained effect. Clinicians can promote healthy recovery exercises such as limited screen time, less strenuous mental activities, and appropriate recovery time following injury to improve memory post-mTBI.6,24,25

Strength of Recommendation

Results from the involved studies consistently indicated poor memory following injury (Table 1). However, the relatively low-level quality of the studies (i.e., case-control), inconsistent imaging reports, and use of variable memory tests across studies make it difficult to directly compare changes and limit the strength of the recommendation. Therefore, we assign a Strength of Recommendation Taxonomy rating of C.

Table 1

Included Studies

Keightley et al.20List et al.19Slobounov et al.22Westfall et al.21
Study titleA functional magnetic resonance imaging study of working memory in youth after sports-related concussion: Is it still working?Cognitive function and brain structure after recurrent mild traumatic brain injuries in young to middle-aged adultsFunctional abnormalities in normally appearing athletes following mTBI: A functional MRI studyIncreased brain activation during working memory processing after pediatric mTBI
Participants15 youth with mTBI (mean age = 14.5 years)

15 age-matched controls (mean age = 14 years)
20 young and middle-aged participants with mTBI (mean age = 25.5 years)

21 age-, sex-, education-matched controls (mean age = 25.7 years)
15 collegiate athletes with mTBI (mean age = 20.8 years)

15 control athletes (mean age = 21.3 years)
19 adolescents (mean age = 14.7 years; mean 7.5 months post-mTBI)

19 healthy controls
Duration since last mTBI9–90 days (mean = 41 days)6–132 months (mean = 25.6 months)≤30 days3–12 months (mean = 7.5 months)
Inclusion criteria(a) mTBI diagnosed by physician per World Health Organization task force definition;

(b) no history of mTBI in the previous year besides current injury;

(c) functional knowledge of French or English
(a) mTBI > 6 months prior to study enrollment;

(b) reporting at least 2 mTBIs
Grade 1 mTBI with no LOC and posttraumatic amnesia under 30 min; seen in clinic within 30 days of injury; right-handedDiagnosed mTBI by sports medicine physician or other qualified personnel; right-handed; screened for metal and safety exclusions
Exclusion criteria(a) Premorbid diagnosis of learning disabilities, ADHD, and/or behavior problems;

(b) severe clinical criteria for ADHD (90th percentile all scales);

(c) severe pain and vestibular, neurological (other than mTBI), or musculoskeletal problems (other than upper-extremity injuries);

(d) violation of standard criteria regarding eligibility for MRI scan;

(e) left-handed
NoneNone(a) History of significant medical, neurological, or psychiatric diagnosis,

(b) previously diagnosed learning or attention deficit disorder
Outcome measuresROCF, verbal fluency, and AVLTAVLT, RWT, and ROCFVirtual corridor taskN-back task
ResultsThe control group had higher mean percentage BOLD signal change (i.e., brain activation) during verbal and nonverbal working memory than the mTBI group in the left and right dorsolateral prefrontal cortex, left premotor cortex, supplementary motor area, and left superior parietal lobule, left thalamus, and left caudate nucleus (p < .05)mTBI group scored lower on all memory assessments; however, they were not statistically significant when using the Bonferroni correction (p < .0042). There were no significant differences in cortical thicknesses between mTBI and control groups but a dose-dependent relationship was established in the mTBI group with lower cortical thickness in the left insula (p = .033) and right superior temporal cortex (p = .023) in those with a higher number of mTBIsmTBI group had significantly larger cluster size at parietal cortex, right hippocampus, and right dorsolateral prefrontal cortex; mTBI had higher BOLD signal % change during encoding at shared areas of activation, significantly different for mTBI at hippocampusmTBI group had significantly higher brain activation than controls during N-back task in bilateral sublobar insula, left middle and superior temporal gyri, left precentral gyrus, right frontal lobe subgyral region, and right medial frontal gyrus. No significant differences on n-back task performance or reaction time between groups
Evidence quality score20/2220/2218/2220/22
Support for answerYesYesYesYes

Note. mTBI = mild traumatic brain injury; ADHD = attention-deficit hyperactivity disorder; ROCF = Rey–Osterrieth Complex Figure Test; RWT = Regensburger Verbal Fluency Test; AVLT = Auditory Verbal Learning Test; LOC = loss of consciousness; MRI = magnetic resonance imaging.

Implications for Practice, Education, and Future Research

Memory impairment, identified by self-report or as a deficit on cognitive task,1921 is often reported following mTBI, and is the result of a neurophysiological change occurring in the hippocampal, cerebellum, and prefrontal cortex regions of the brain. Memory assessments can be performed over the course of a disease or illness to understand its progression and severity of impairment.26 The studies in this CAT were performed in the acute (9 days)20 and subchronic (>6 months)19 time frames following the last known injury; however, this does not account for the large lifespan changes that can occur following mTBI.

Overall, memory function was lower in participants that had sustained a previous mTBI than healthy controls.19,20 List et al. identified mTBI patients scored lower on all memory tests (e.g., AVLT, RWT, Rey-Osterrieth Complex Figure Test [ROCT]; described in Table 2) than matched healthy controls; however, within the mTBI group, the number of previous mTBIs was not correlated with cognitive scores (p > .2). There was also no association between cortical thickness between healthy and mTBI groups. A dose-dependent cortical thinning within the right temporal lobe and bilateral insula was identified when compared with individuals with no previous mTBI.

Table 2

Memory Assessments

Memory testOutcomeDescription
AVLT33Verbal memoryPatients presented verbally with 15 unrelated words; patients are asked to recite as many words as they can recall. Repeated for a total of five trials. Score includes sum of words recalled within each trial and sum of words across five trials.
N-back test34Working memoryParticipants are shown stimuli in a sequence and they have to decide if it matches the one that appeared n items ago.
RWT35Verbal fluencyParticipants write as many words as possible beginning with the letter “s” or “g/r,” names of food or clothes/flowers within 1 min. No repetitions, no proper names, words should not begin with the same word stem, and words should only be words that could be used in English books or newspaper. Score total number of correct words.
ROCF36Visual memory and perceptual organizationPatient shown complex figure and asked to replicate it by copying it (recognition) and then is given 2–5 min to recreate the figure (recall). Scored on a 36-point system.
Visual corridor task22Spatial memoryPatients positioned in virtual reality paradigm. First shown navigation route, then they navigate randomly, then navigate purposefully with goal of reaching target room. Total time of runs is scored.

Note. ROCF = Rey–Osterrieth Complex Figure Test; RWT = Regensburger Verbal Fluency Test; AVLT = Auditory Verbal Learning Test.

Keightley et al.20 had similar findings with adolescent individuals with previous mTBI performing significantly worse on working memory tests (i.e., AVLT, verbal fluency) than those without mTBI history. Individuals with injury also had different cortical activation patterns in the dorsolateral prefrontal cortex, temporal, and parietal regions, which were identified with BOLD imaging. These findings suggest that adolescents may not be able to perform compensatory strategies (e.g., additional neural activation) to support memory function after mTBI.

Slobounov et al.22 had individuals with mTBI perform virtual reality memory tasks and found that individuals and controls performed similarly. However, those with previous brain injuries had increased brain signal, indicating they may be recruiting larger cerebral resources to maintain the same level of function they previously had. Westfall et al.21 also identified an increase in brain activation in previously concussed individuals during working memory tasks (e.g., N-back task) compared with healthy controls. These findings are differing to the Keightley et al.20 findings where the adolescents were not able to provide compensatory approaches to maintain performance.

Functional and structural findings after sport-related mTBI remain to be a critical area of research. Translating these findings to clinical practice can be difficult with the majority of individuals sustaining sport-related mTBIs returning to competition within a few weeks.27 Abnormal neurologic images, especially in chronic cases, are well documented in sport-related mTBI patients; however, the clinical relevance of these findings remains to be elucidated.28,29 Possibly, abnormal cortical activation patterns and decreased cortical thickness identified by imaging is related to worse performance on neuropsychological (e.g., memory) tests. Improving screening mechanisms, identifying lingering symptoms, and managing individuals following best practices may reduce the number of repeated mTBIs, increase time between injuries, and improve patient outcomes following sport-related mTBI.25,30

There were some limitations with each of the studies included in this review. The time frames of imaging after injury varied significantly between studies (9 days to >6 months) and in the selection of memory tests limiting the ability to compare results. There were also differences in imaging techniques (1 T vs. 3 T); however, all studies provided detailed descriptions of fMRI setup and image filtering techniques. In addition, imaging following sport-related mTBI is typically reserved for research settings and individuals with chronic mTBI with unresolved symptoms, restricting widespread clinical application.31 Finally, all study participants were adolescents or young adults, limiting generalizability to other populations.

Each of the mentioned studies demonstrated modest results, but future studies could be improved. As mTBI recovery can be an ongoing and lifelong process, future research should aim to conduct longitudinal studies with similar memory tests at standardized time points post injury similar to large-scale concussion research endeavors and grounded in theory.32 This topic should be revisited in 2 years or as additional research is published.

CAT Kill Date: September 2024

Critically appraised topics have limited life and should be revisited approximately 2 years after publication (see https://doi.org/10.1123/ijatt.2018-0093).

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  • Expand
  • 1.

    Katz DI, Cohen SI, Alexander MP. Mild traumatic brain injury. Handb Clin Neurol. 2015;127:131156. PubMed ID: 25702214 doi:10.1016/b978-0-444-52892-6.00009-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    McCrory P, Meeuwisse W, Dvorak J, et al. Consensus statement on concussion in sport—The 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51:838847. PubMed ID: 28446457 doi:10.1136/bjsports-2017-097699

    • Search Google Scholar
    • Export Citation
  • 3.

    Røe C, Sveen U, Alvsåker, B-HE. Post-concussion symptoms after mild traumatic brain injury: influence of demographic factors and injury severity in a 1-year cohort study. Disabil Rehabil. 2009; 31(15):12351243. PubMed ID: 19116810 doi:10.1080/09638280802532720

    • Crossref
    • Search Google Scholar
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