Abstract
Objective:
This study examined the moderating effect of traumatic brain injury (TBI) history on subjective and objective cognition across multiple cognitive domains.
Setting, participants, and design:
Participants included 242 Vietnam-Era Veterans with a history of no TBI (n=86), mild TBI (n=74), or moderate-to-severe TBI (n=82) from the observational Department of Defense-Alzheimer’s Disease Neuroimaging Initiative (DoD-ADNI) study.
Main Measures:
Objective cognition was the outcome and was measured using neuropsychological measures in the domains of memory, attention/executive functioning, and language. Subjective cognition was measured using the memory, divided attention, and language subscales from the Everyday Cognition (ECog) measure. TBI severity status was the moderating variable.
Results:
Veterans with a history of moderate-to-severe TBI had a stronger negative association between subjective and objective attention relative to participants without a TBI (p=.002). Although this association did not differ between mild TBI and no TBI history groups (p=.100), the association between subjective and objective attention for the mild TBI group was intermediate to the no TBI and moderate-to-severe TBI history groups. TBI status did not moderate associations between subjective and objective memory or language.
Conclusion:
Results highlight the importance of assessing subjective and objective cognition in older Veterans and the relevance of attention in the context of TBI history. More work is needed to better understand the intersection of TBI and aging and how these factors may be used to guide individualized assessment and treatment approaches for older Veterans.
Keywords: subjective cognition, traumatic brain injury, cognitive aging, Veterans, neuropsychology, subjective cognitive decline, attention, executive functioning, brain injuries, traumatic
INTRODUCTION
Subjective cognitive concerns are often what brings older Veterans into a clinic, but it can be unclear how to interpret these concerns, particularly in the context of a history of traumatic brain injury (TBI). The degree of objective cognitive decline following a TBI may vary both across and within TBI severity groups. Prior studies involving TBI have shown mixed findings regarding the extent to which subjective and objective cognition are associated. While some studies demonstrate notable associations,1,2 some studies also show that factors such as depression or posttraumatic stress disorder (PTSD) may be particularly related to subjective concerns.2-4 Veterans with a history of TBI can report experiencing cognitive difficulties, even years after the TBI event, and despite performing within normal limits on objective measures.5 Studies that have examined the relationship of TBI history with subjective and objective cognition, however, have largely focused on younger Veterans.
Although TBI is a risk factor for dementia,6 very few studies have examined how TBI history may impact the associations of subjective and objective cognition within the context of aging, which has unique considerations given the many factors that can influence cognition in older Veterans (e.g., psychiatric symptoms, AD genetic susceptibility, and vascular health). The construct of subjective cognitive decline has garnered significant attention in the Alzheimer’s disease (AD) literature as a way to identify subtle cognitive declines prior to meeting criteria for mild cognitive impairment (MCI)7 and is often included in MCI diagnostic criteria.8 However, similar to TBI literature, evidence of a meaningful relationship between subjective and objective cognition may be impacted by demographic, physical health, and psychiatric factors, which is why it is critical to examine these associations in the context of older Veterans with and without TBI history.9,10
Using data from the Brain Aging in Vietnam War Veterans/Department of Defense-Alzheimer’s Disease Neuroimaging Initiative (DoD-ADNI), we examined associations of subjective and objective cognition among cognitive domains that could be impacted my TBI and/or aging and AD, including memory, attention/executive functioning, and language, and the extent to which TBI severity moderates these relationships. We hypothesized that participants with a TBI history (both mild and moderate-to-severe TBI) would have stronger associations between subjective and objective memory and attention/executive function than the no TBI group.
METHODS
Participants
Data used in this current study were obtained from the publicly available DoD-ADNI database (adni.loni.usc.edu). The main aims/methods of DoD-ADNI and up-to-date information can be found at www.adni-info.org. This research was approved by the institutional review boards of all participating sites within ADNI and written informed consent was obtained for all study participants. The current study included 242 Vietnam-Era Veterans with available demographic, neuropsychological, psychiatric, TBI history, and health data.
Measures
Neuropsychological outcomes.
Three composite scores were calculated using available neuropsychological measures in DoD-ADNI.11 The memory composite included the immediate and delayed recall scores from the Rey Auditory Verbal Learning Test and the Wechsler Memory Scale–Revised Logical Memory. The attention (and executive functioning) composite included Trail Making Test, Parts A and B total time. The language composite included the total correct scores from the 30-item Boston Naming Test and Animal Fluency (adapted from The Consortium to Establish a Registry for Alzheimer's Disease [CERAD]). Composite scores were calculated by converting raw scores to z-scores for each measure and taking the mean of the measures in each domain; the attention composite was multiplied by −1, so higher scores indicated better performance. Domain composites were each Blom-transformed to reduce skewness.
Subjective cognitive decline.
The Everyday Cognition (ECog) measure was used to assess subjective cognition.12 Participants rate their ability to perform everyday tasks relative to 10 years ago. The everyday tasks are divided into six cognitive domains: memory, language, visuospatial, planning, organization, and divided attention. We focused on the memory (eight items), divided attention (four items), and language (nine items) domains to mirror the available neuropsychological composite scores. Higher scores are associated with more subjective cognitive decline.
TBI history.
TBI severity was based on Veteran Affairs (VA)/DoD criteria 2021 Clinical Practice Guidelines.13 Each TBI was coded and severity was based on the most severe TBI sustained in their lifetime. Participants with a history of penetrating head injury were excluded from DoD-ADNI during screening. An injury was classified as mild if the participant endorsed a loss of consciousness (LOC) of <30 minutes, or alteration of consciousness (AOC) or post-traumatic amnesia (PTA) up to 24 hours. The moderate and severe TBI criteria were combined since the information for PTA >1 day was not available. Thus, the moderate-to-severe TBI criteria included: LOC >30 minutes, AOC >24 hours, or PTA >1 day. Three participants who reported a hospitalization for a head/neck injury but did not meet criteria for TBI based on their report of LOC, AOC, or PTA were excluded. Based on these VA/DoD criteria, 86 participants had no history of TBI, 74 participants had a history of mild TBI, and 82 participants had a history of moderate-to-severe TBI. For the mild TBI group, on average, most participants had LOC<5 mins (56.4%), AOC<5 minutes (42.4%, with 30.5% having AOC of 30 minutes to 24 hours), and only 8 participants in this group reported any PTA (all PTA was <24 hours). For the moderate-to-severe TBI group, LOC ranged from <5 mins to >24 hours (36.5% with LOC of 30 minutes to 24 hours), and, on average, most had AOC >24 hours (80.9%), and PTA >24 hours (62.5%). Total number of TBIs was also used as a covariate in follow-up analyses.
Additional variables.
Current PTSD symptom severity measured using the Clinician-Administered PTSD Scale (CAPS)14 was included as a covariate in all models. Additional measures to describe the sample and used as covariates in follow-up analyses included: Geriatric Depression Scale (GDS) to measure depressive symptom severity, pulse pressure (systolic minus diastolic blood pressure; a proxy for arterial stiffening) to measure of vascular health, and apolipoprotein (APOE) ε4 genotype (non-carrier vs. carrier) as a measure of genetic susceptibility to AD. The Mini-Mental State Exam (MMSE) was using as a global cognition measure to characterize the sample.
Statistical Analyses
Analyses of variance and chi-square tests were used to characterize the TBI groups. General linear models, adjusting for age, education, PTSD symptom severity, and TBI severity (no TBI was reference group) first examined the associations between domain-specific subjective and objective cognition across the sample (Model 1). Specifically, subjective memory was included in the objective memory model, subjective attention in the objective attention model, and subjective language in the objective language model. Next, the models tested whether TBI severity moderated the associations of domain-specific subjective and objective cognition (Model 2). Follow-up analyses examined the pattern of results when the following covariates were included both separately and in the same model to adjust for additional factors/comorbidities that could impact these associations: total number of TBIs, race, ethnicity, APOE ε4, pulse pressure, and depressive symptom severity.
RESULTS
Table 1 shows characteristics across the whole sample and by TBI history group. On average, participants were roughly 70 years old with 15 years of education; 44.6% of participants met criteria for PTSD based on the CAPS. The mild TBI group was slightly older than the no TBI and moderate-to-severe TBI groups and had the largest proportion who met criteria for PTSD. The no TBI group performed slightly better on the memory composite than the mild TBI group; they also reported less subjective cognitive difficulties in language and attention than the mild TBI group and less subjective difficulties in attention than the moderate-to-severe TBI group. Many characteristics did not differ across groups.
Table 1.
Sociodemographic and clinical characteristics by TBI group.
| Total Sample | No TBI | Mild TBI | Moderate-to-Severe TBI | p | |
|---|---|---|---|---|---|
| N | 242 | 86 | 74 | 82 | |
| Age, mean (SD) | 69.75 (4.37) | 69.23 (4.65)a | 70.79 (4.86)b,c | 69.36 (3.37)a | .047 |
| Education, mean (SD) | 15.21 (2.42) | 15.28 (2.28) | 15.05 (2.47) | 15.27 (2.53) | .809 |
| Men, N (%) | 240 (99.2%) | 86 (100%) | 73 (98.6%) | 81 (98.8%) | .571 |
| Race, N (%) | .305 | ||||
| American Indian/Alaska Native | 4 (1.7%) | 1 (1.2%) | 1 (1.4%) | 2 (2.4%) | |
| Asian | 3 (1.3%) | 3 (3.5%) | 0 (0.0%) | 0 (0.0%) | |
| Black/African American | 18 (7.4%) | 8 (9.3%) | 2 (2.7%) | 8 (9.8%) | |
| White | 204 (84.3%) | 69 (80.2%) | 67 (90.5%) | 68 (82.9%) | |
| More than one | 10 (4.1%) | 3 (3.5%) | 3 (4.1%) | 4 (4.9%) | |
| Unknown | 3 (1.2%) | 2 (2.3%) | 1 (1.4%) | 0 (0.0%) | |
| Ethnicity, N (%) | .283 | ||||
| Hispanic/Latino | 20 (8.3%) | 10 (11.6%) | 6 (8.1%) | 4 (4.9%) | |
| Non-Hispanic/Non-Latino | 222 (91.7%) | 76 (88.4%) | 68 (91.9%) | 78 (95.1%) | |
| Pulse pressure, mean (SD) | 59.53 (14.33) | 60.02 (15.14) | 59.19 (14.45) | 59.32 (13.49) | .923 |
| APOE ε4 carrier, N (%) | 65 (26.9%) | 21 (24.4%) | 20 (27.0%) | 24 (29.3%) | .777 |
| GDS, mean (SD) | 2.78 (2.86) | 2.65 (2.18) | 2.73 (2.60) | 2.95 (2.74) | .783 |
| Current PTSD, N (%) | 108 (44.6%) | 39 (45.3%) | 40 (54.1%)b | 29 (35.4%)a | .063 |
| Current CAPS score, mean (SD) | 30.28 (26.88) | 26.83 (29.07) | 34.51 (26.68) | 30.09 (24.32) | .196 |
| Lifetime CAPS score, mean (SD) | 43.32 (33.06) | 38.02 (38.44) | 46.99 (32.26) | 45.56 (26.75) | .175 |
| Years since most recent TBI, mean (SD)* | 38.36 (17.84) | - | 39.53 (18.08) | 37.30 (17.67) | .439 |
| Years since most severe TBI, mean (SD)* | 40.81 (16.82) | - | 39.53 (18.08) | 41.81 (15.63) | .368 |
| Number of TBIs, N (%)* | .146 | ||||
| 0 | 86 (35.5%) | 86 (100%) | - | - | |
| 1 | 93 (38.4%) | - | 51 (68.9%) | 42 (51.2%) | |
| 2 | 43 (17.8%) | - | 15 (20.3%) | 28 (34.1%) | |
| 3 | 15 (6.2%) | - | 7 (9.5%) | 8 (9.8%) | |
| 4-5 | 5 (2.0%) | - | 1 (1.4%) | 4 (4.8%) | |
| MMSE, mean (SD) | 28.30 (1.58) | 28.41 (1.39) | 28.27 (1.90) | 28.22 (1.45) | .729 |
| Memory, mean (SD) | 0.06 (0.95) | 0.23 (0.92)a | −0.08 (0.86)c | 0.02 (1.04) | .109 |
| Attention, mean (SD) | −0.02 (0.97) | 0.06 (0.95) | −0.07 (0.90) | −0.06 (1.04) | .636 |
| Language, mean (SD) | 0.06 (1.00) | 0.16 (1.02) | 0.02 (1.07) | −0.00 (0.94) | .519 |
| ECog Total, mean (SD) | 1.66 (0.55) | 1.54 (0.50)a,b | 1.72 (0.58)c | 1.73 (0.54)c | .043 |
| ECog Memory, mean (SD) | 1.98 (0.70) | 1.86 (0.68) | 2.05 (0.71) | 2.05 (0.69) | .152 |
| ECog Attention, mean (SD) | 1.82 (0.76) | 1.65 (0.69)a,b | 1.91 (0.78)c | 1.93 (0.77)c | .026 |
| ECog Language, mean (SD) | 1.72 (0.67) | 1.58 (0.59)a | 1.81 (0.75)c | 1.78 (0.65) | .060 |
significantly different than mTBI
significantly different than Moderate-to-Severe TBI
significantly different than no TBI
no TBI group not included in between-group analysis since variable is specific to TBI. TBI=traumatic brain injury; APOE=apolipoprotein E; GDS=Geriatric Depression Scale; CAPS=Clinician-Administered PTSD Scale; MMSE=Mini-Mental State Exam; ECog=Everyday Cognition
First, the associations between domain-specific subjective and objective cognition were examined across the sample (Model 1; Table 2). Subjective memory was associated with objective memory (β=−.156, p=.013) and subjective language was associated with objective language (β=−.233, p<.001), but subjective attention was not associated with objective attention (β=−.068, p=.299). Additionally, TBI severity was not associated with any of the objective cognitive domain scores (all ps>.05) after adjusting for the other variables in the model.
Table 2.
Regression weights for associations between domain-specific subjective and objective cognition
| Memory | Attention | Language | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Model 1 | Model 2 | Model 1 | Model 2 | Model 1 | Model 2 | |||||||
| β | se | β | se | β | se | β | se | β | se | β | se | |
| Age | −.163** | .062 | −.168** | .062 | −.148* | .066 | −.130* | .065 | −.170* | .066 | −.163* | .067 |
| Education | .267*** | .059 | .269*** | .060 | .053 | .063 | .062 | .062 | .178** | .064 | .180** | .064 |
| CAPS | −.057 | .066 | −.062 | .066 | −.180** | .068 | −.196** | .068 | −.087 | .070 | −.086 | .070 |
| TBI Severity | ||||||||||||
| No TBI | - | - | - | - | - | - | - | - | - | - | - | - |
| Mild TBI | −.168 | .145 | −.180 | .146 | .006 | .149 | −.054 | .154 | .033 | .156 | .028 | .158 |
| Moderate-to-Severe TBI | −.151 | .138 | −.169 | .139 | −.070 | .149 | −.096 | .147 | −.079 | .149 | −.073 | .151 |
| ECog Score | −.156* | .062 | −.041 | .102 | −.068 | .065 | .195⊤ | .116 | −.233*** | .069 | −.250* | .123 |
| TBI Severity x ECog Score | ||||||||||||
| No TBI x ECog | - | - | - | - | - | - | - | - | - | - | - | - |
| Mild TBI x ECog | - | - | −.198 | .142 | - | - | −.258⊤ | .156 | - | - | .088 | .158 |
| Moderate-to-Severe TBI x ECog | - | - | −.148 | .141 | - | - | −.475** | .153 | - | - | −.052 | .165 |
CAPS= CAPS=Clinician-Administered PTSD Scale; TBI=traumatic brain injury; ECog=Everyday Cognition
p<.10
p<.05
p<.01
p<.001
Next, the subjective cognition x TBI severity interaction was added to each model (Model 2) to determine if TBI severity moderated the relationship between domain-specific subjective and objective cognition. This interaction was significant for attention (F(2,233)=4.79, p=.009, ηp2=.039). Specifically, relative to Veterans without a history of TBI, moderate-to-severe TBI (β=−.475, p=.002) showed a stronger negative association between subjective and objective attention such that greater subjective difficulties in attention were more strongly associated with poorer objective attention performance among those with moderate-to-severe TBI (see Figure 1). This result retained significance after Bonferroni correction for the 3-group comparison. While not statistically significant, the those with history of mild TBI had a pattern of a more negative association between subjective and objective attention than the no TBI group (β=−.258, p=.100). TBI severity did not moderate the associations between subjective and objective cognition for memory or language domains. We also examined the above models when total number of TBIs, race and ethnicity, depressive symptoms, APOE ε4 genotype, and pulse pressure were included as covariates, both independently and together, and the pattern of results did not change.
Figure 1.
Associations of subjective attention and model-predicted objective attention by TBI status. Shaded area represents 95% confidence interval.
DISCUSSION
Study findings show a stronger association between subjective and objective attention among Veterans with a history of TBI, particularly a moderate-to-severe TBI, compared to those without a history of TBI. These findings are partially consistent with the hypothesis that both mild and moderate-to-severe TBI would moderate the association between subjective attention, though only the moderate-to-severe group reached statistical significance. History of TBI did not moderate the association between subjective and objective memory or language.
This work is in older, Vietnam-Era Veterans, which addresses a significant gap in our understanding since most studies include primarily younger Veterans or service members. Compared to studies in younger samples, our results are somewhat consistent with a study of military personnel within 3 months of a mild-to-moderate TBI that showed self-reported executive functioning was associated with attention/processing speed performance, but not other domains of objective cognition.2 However, another study of patients seeking compensation, showed that self-reported attention predicted objective attention in the mild TBI group, while the moderate-to-severe TBI group showed an association between self-reported and objective learning and memory.1 There are several study differences that could account for our results not showing that moderate-to-severe TBI moderated the association between objective and subjective memory including: the age of the participants, time since injury, Veteran vs. compensation-seeking status, proportion with PTSD, differences in some measures of subjective and objective cognition, as well as the covariates included in analyses.
Subjective cognitive decline is associated with higher risk for progressing to dementia and is considered one of the earliest symptoms to emerge in preclinical AD.7,10 However, criteria for subjective cognitive decline often exclude individuals with medical or psychiatric conditions,7 which has resulted in a shortage of work examining subjective cognition in older Veterans with a history of TBI and PTSD. The results showing no moderating effect of TBI history on subjective and objective memory and language, two domains impacted early in AD, suggest that self-report of memory or language decline for an older Veteran with a TBI history has a similar association with memory and language performance on neuropsychological testing as an older Veteran who has not had a TBI. These findings may support the practice of being more inclusive of participants with a history of TBI history in AD studies on subjective cognitive decline, though additional work is needed to replicate these findings in older Veterans and extend the results in non-Veterans.
The reason for the moderating impact of TBI history on subjective and objective attention is unclear, though the measures of Trails A and B that were included in the attention composite may be particularly sensitive to changes due to both TBI (including mild TBI) and aging.15,16 The main effect of subjective attention on objective attention across the whole sample was non-significant, so it is possible that in general, one’s subjective rating of attention is influenced by real-world factors that may not contribute to how one performs in a controlled environment. However, in the context of a moderate-to-severe TBI history, there may be more consistency between their real-world experience of attention difficulties and objective performance because, on average, the moderate-to-severe TBI itself caused more severe cognitive difficulties, including in attention,17 that had a more prominent impact on their life, at least initially, and are therefore more aware. Alternatively, perhaps there are more noticeable changes in attention as someone with a history of moderate-to-severe TBI gets older due to chronic TBI-related structural18 and functional connectivity19 changes that could increase their vulnerability to age-related declines.
Notably, the varying associations between subjective and objective attention across TBI history groups suggests that assessment of both subjective and objective cognition is important. It is possible that, in addition to TBI history and aging, PTSD symptoms also contribute to these associations given that there was a main effect of CAPS score on objective attention performance and there was a high rate of PTSD in the sample (44.6%). More work is needed to disentangle these cognitive associations at the intersection of aging, TBI, and PTSD, particularly given that both TBI and PTSD are be associated with increased risk of dementia.6,20
The current study has several strengths including the multiple domains of cognition that were evaluated as well as the follow-up examination of multiple covariates relevant to both aging/AD, including psychiatric symptoms. Multiple limitations include: 1) the sample primarily included white men, which significantly limits the generalizability of the results; 2) relying on self-report of TBI history to define TBI groups and being unable to separate moderate and severe TBI histories given the potential heterogeneity of the combined group; and 3) the neuropsychological battery did not include sensitive measures of visuospatial functioning or other aspects of attention not requiring speeded visual scanning or motor functioning and executive functioning such as planning or inhibition and performance validity was not assessed. While there is overlap between the some of the domain-specific ECog items and the neuropsychological measures (i.e., “forgetting names of objects” on ECog Language may be assessed on the BNT), all of the items are not perfectly aligned with the measures used in the neuropsychological domain score. Notably, the items on the ECog are potentially more ecologically valid in that they are capturing the participants’ real-world experience and comparing their experience to how they functioned in the past, while the neuropsychological measures may be testing cognition in a standardized environment but that may not allow for compensatory strategies or capture the extent that it may be relevant to their daily life.21
While the association between subjective and objective attention was moderated by TBI history, associations between subjective and objective memory and language were not. Together, results highlight the potential importance of assessing domain-specific subjective and objective cognition, and attention in particular, in older Veterans. More work is needed to better understand the intersection of TBI and aging in the context of additional commonly co-occurring conditions such as PTSD and vascular disease in order to inform how these intersecting factors may be used to guide individualized and nuanced assessment and treatment approaches for older Veterans presenting to clinic with subjective cognitive decline.
FUNDING:
This work was supported by the U.S. Department of Veterans Affairs Clinical Sciences Research and Development Service (1IK2CX001865 to KRT, IK2CX001952 to VCM, 1I01CX001842 to KJB), National Institutes of Health/National Institute on Aging grants (R03 AG070435 to KRT, R01 AG063782 to KJB), and the Alzheimer’s Association (AARG-22-723000 to KRT). Data collection and sharing for this project was funded by the Alzheimer's Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: Alzheimer's Association; Alzheimer's Drug Discovery Foundation; BioClinica, Inc.; Biogen Idec Inc.; Bristol-Myers Squibb Company; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; F. Hoffmann-La Roche Ltd and its affiliated company Genentech, Inc.; GE Healthcare; Innogenetics, N.V.; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Medpace, Inc.; Merck & Co., Inc.; Meso Scale Diagnostics, LLC.; NeuroRx Research; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Synarc Inc.; and Takeda Pharmaceutical Company. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health (www.fnih.org). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimer's Disease Cooperative Study at the University of California, San Diego. ADNI data are disseminated by the Laboratory for Neuro Imaging at the University of Southern California. This research was also supported by NIH grants P30 AG010129 and K01 AG030514.
Footnotes
Data used in preparation of this article were obtained from the Alzheimer’s Disease Neuroimaging Initiative (ADNI) database (adni.loni.usc.edu). As such, the investigators within the ADNI contributed to the design and implementation of ADNI and/or provided data but did not participate in analysis or writing of this report. A complete listing of ADNI investigators can be found at: http://adni.loni.usc.edu/wp-content/uploads/how_to_apply/ADNI_Acknowledgement_List.pdf
DISCLOSURES: The authors report no disclosures.
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