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Corresponding author: James F. Sumowski, PhD, Neuropsychology and Neuroscience, Kessler Foundation Research Center, 300 Executive Dr, Ste 70, West Orange, NJ 07052.
Neuropsychology and Neuroscience, Kessler Foundation, West Orange, NJDepartment of Physical Medicine and Rehabilitation, Rutgers–New Jersey Medical School, Newark, NJ
Neuropsychology and Neuroscience, Kessler Foundation, West Orange, NJDepartment of Physical Medicine and Rehabilitation, Rutgers–New Jersey Medical School, Newark, NJTraumatic Brain Injury Laboratory, Kessler Foundation, West Orange, NJ
Department of Physical Medicine and Rehabilitation, Rutgers–New Jersey Medical School, Newark, NJTraumatic Brain Injury Laboratory, Kessler Foundation, West Orange, NJ
Neuropsychology and Neuroscience, Kessler Foundation, West Orange, NJDepartment of Physical Medicine and Rehabilitation, Rutgers–New Jersey Medical School, Newark, NJ
Neuropsychology and Neuroscience, Kessler Foundation, West Orange, NJDepartment of Physical Medicine and Rehabilitation, Rutgers–New Jersey Medical School, Newark, NJDepartment of Neurology and Neurosciences, Rutgers–New Jersey Medical School, Newark, NJ
To investigate whether the cognitive reserve hypothesis helps to explain differential cognitive impairment among survivors of traumatic brain injury (TBI), whereby survivors with greater intellectual enrichment (estimated with education) are less vulnerable to cognitive impairment.
Design
Cross-sectional study.
Setting
Medical rehabilitation research center.
Participants
Survivors of moderate or severe TBI (n=44) and healthy controls (n=36).
Interventions
Not applicable.
Main Outcome Measures
Intellectual enrichment was estimated with educational attainment. Group was defined as TBI or healthy control. Current cognitive status (processing speed, working memory, episodic memory) was evaluated with neuropsychological tasks.
Results
TBI survivors exhibited worse cognitive status than healthy persons (P<.001), and education was positively correlated with cognitive status in TBI survivors (r=.54, P<.001). Most importantly, regression analysis revealed an interaction between group and education (R2 change=.036, P=.004), whereas higher education attenuated the negative impact of TBI on cognitive status. TBI survivors with lower education performed much worse than matched healthy persons, but this TBI-related performance discrepancy was attenuated at higher levels of education.
Conclusions
Higher intellectual enrichment (estimated with education) reduces the negative effect of TBI on cognitive outcomes, thereby supporting the cognitive reserve hypothesis in persons with TBI. Future work is necessary to investigate whether intellectual enrichment can build cognitive reserve as a rehabilitative intervention in survivors of TBI.
Traumatic brain injury (TBI) 10-20 years later: a comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning.
such that 2 persons with similar injuries often have discrepant cognitive outcomes. This inconsistent relation between neurologic insult and cognitive outcome is observed across neurologic populations, including Alzheimer disease (AD). For instance, many older adults without dementia meet the neuropathologic criteria for probable or definite AD at autopsy.
This cognitive-pathologic discrepancy is explained in part by the cognitive reserve hypothesis, which posits that higher lifetime intellectual enrichment (often estimated with education) protects against disease-related cognitive decline.
Previous work with adult survivors of TBI has primarily shown positive correlations between intellectual enrichment and cognitive outcomes (ie, a main effect),
but herein we evaluate the cognitive reserve hypothesis in TBI by investigating whether educational attainment differentially impacts cognitive impairment after TBI (ie, an interaction effect).
Methods
Participants
The sample included 44 survivors of moderate (n=3) or severe (n=41) TBI (mean age ± SD, 39.3±10.6y; 12 women) and 36 healthy controls (mean age ± SD, 43.7±11.3y; 24 women). Survivors were at least 1 year postinjury (median, 5.9y; mean ± SD, 9.0±7.1y). Glasgow Coma Scale data were only available for a subset of TBI survivors (n=20; median, 4; mean ± SD, 5.2±2.9). The TBI sample was marginally younger (t78=1.79, P=.078), with a higher proportion of men (72.7% vs 33.3%; χ2=12.42, P<.001). Age and sex were controlled in subsequent analyses. The Kessler Foundation Institutional Review Board approved data collection, and written informed consent was obtained from all subjects.
Cognitive reserve
Lifetime intellectual enrichment was estimated with educational attainment (healthy controls: 14.77±1.93y; TBI: 13.84±1.94y).
Educational attainment was unrelated to time since injury (r=.074) or Glasgow Coma Scale scores (r=.093) for TBI survivors. As such, any protective effects of intellectual enrichment are not explained/confounded by any chance relation between educational attainment and injury severity.
Cognitive status
The most common cognitive deficits among TBI survivors include slowed processing speed, poor working memory, and episodic memory impairment.
Traumatic brain injury (TBI) 10-20 years later: a comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning.
We assessed processing speed with the Symbol Digit Modalities Test (oral version), working memory with Letter-Number Sequencing, and episodic memory with the Selective Reminding Test (total learning). Performance on each measure was entered into a principal components analysis to create a single cognitive status score used in subsequent analyses (71.8% of variance).
Statistical analysis
We tested if intellectual enrichment (estimated with education) moderates the deleterious effect of TBI on cognitive status (interaction effect) by performing a hierarchical regression predicting cognitive status, with age, sex, group, and education in step 1, and the interaction between group and education in step 2. We expected a group by education interaction, where TBI survivors with lower education would show cognitive deficits relative to healthy persons, but such deficits would be attenuated in patients with higher education.
Results
Cognitive status was lower among TBI survivors (−.70±.72) than healthy persons (.85±.50, t78=10.92, P<.001). Significant (all Ps<.001) raw score differences also existed for each of the 3 cognitive scores contributing to the cognitive status composite: Symbol Digit Modalities Test (healthy: 64.39±9.76; TBI: 37.2±11.5), Letter-Number Sequencing (healthy: 12.44±2.57; TBI: 9.25±2.3), and Selective Reminding Test (healthy: 141.44±5.7; TBI: 113.27±23).
The full regression model was significant (F5,74=10.91, P<.001, R2=.691). After controlling for age, sex, group, and education, there was an interaction between group and education (R2 change=.036, P=.004). TBI survivors with lower education performed worse than healthy persons, but this TBI-related performance discrepancy was attenuated at higher levels of education (fig 1A).
Fig 1Plot of the interaction between group (TBI, healthy) and educational attainment on the cognitive status component score. Solid line indicates TBI group; dashed line, healthy control group (A). Scatterplot of the relation between years of educational attainment and cognitive status for TBI patients and healthy persons. Red indicates TBI group; blue, health control group (B).
The cognitive reserve hypothesis predicts that intellectual enrichment will be more related to cognitive status within neurologic samples than healthy persons. This is because among healthy persons, there are no deleterious effects of neurologic disease processes on cognitive status for intellectual enrichment to protect against. Indeed, there was a strong positive relation between education and cognitive status among TBI survivors (r=.538, P<.001), but there was no relation among healthy persons (r=.035, P=.841). We provide the raw data demonstrating this divergent relation (fig 1B).
Discussion
Higher education attenuated the deleterious effect of moderate to severe TBI on cognitive status, thereby supporting the cognitive reserve hypothesis in TBI. This finding helps to explain the variable cognitive outcomes across TBI survivors with similar injuries
because survivors with higher education can sustain a given injury with lesser cognitive decline than a person with less education. Our findings extend earlier work linking higher premorbid intelligence (another proxy of cognitive reserve) with better cognitive performance in adult survivors of TBI
; however, we add to the literature by directly testing the cognitive reserve hypothesis with an interaction between TBI and intellectual enrichment (education).
Study limitations
Although limited by a relatively small sample size, our study provides a proof of concept for cognitive reserve in TBI. The small sample size may limit the generalizability of our findings because our small samples may not adequately represent the populations of healthy persons and survivors of TBI. For instance, we confirmed our hypothesis that educational attainment would be more related to cognitive status in survivors of TBI than in healthy persons; however, one might expect at least a small positive correlation between education and cognitive status in healthy persons. This is one way in which our healthy sample may differ from the general population. Another limitation relates to our sole use of educational attainment as an estimate of intellectual enrichment because the construct validity of education as an independent contributor to reserve has been questioned,
future research should investigate whether intellectual enrichment moderates/attenuates the negative effect of disease-related neuropathologic changes (ie, cerebral atrophy) on cognitive outcomes in TBI survivors.
Conclusions
Ultimately, consideration of lifetime intellectual enrichment through proxies, such as education or vocabulary knowledge, may help identify TBI survivors at greatest risk of cognitive impairment (ie, survivors with lower cognitive reserve), who can then be targeted for early intervention cognitive rehabilitation. Also, encouraging survivors to engage in intellectually enriching activities may help protect against cognitive decline, although future experimental work is necessary to draw a causal link between enrichment and neurocognitive protection.
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How common are the “common” neurologic disorders?.
Traumatic brain injury (TBI) 10-20 years later: a comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning.
Supported by the New Jersey Commission on Brain Injury Research (grant no. CBIR11PJT020 ); the National Institute on Disability and Rehabilitation Research (grant no. H133A070037 ); and a fellowship training grant from the Department of Education, National Institute on Disability and Rehabilitation Research (grant no. H133P090009 ).
The content of this article does not necessarily represent the policy of the Department of Education, and one should not assume endorsement by the federal government.
No commercial party having a direct financial interest in the results of the research supporting this article has conferred or will confer a benefit on the authors or on any organization with which the authors are associated.
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