Abstract
Background/Objectives:
Prior studies of mortality following traumatic brain injury (TBI) have not focused specifically on older adults, compared to a non-TBI trauma cohort, or included specific causes of death. The objectives of this study were, among adults aged 65 years and older, to 1) generate standardized mortality ratios (SMRs) by cause of death for TBI and a non-TBI trauma cohort compared to a general population and 2) Assess risk of mortality associated with TBI compared to a non-TBI trauma cohort.
Design:
Retrospective cohort study of adults aged 65 years and older who were treated at an urban trauma center from 1997-2008.
Measurements:
Data from the trauma registry were linked to the National Death Index through 2008 to obtain date and cause of death. We identified individuals with TBI and non-TBI trauma and calculated age and sex adjusted SMRs by comparing to the state general population. We next compared time to mortality between individuals with TBI (n=852) and non-TBI trauma (n=1,050), adjusting for potential confounders.
Results:
Compared to the age-and sex-adjusted state general population, older adults with TBI (SMR 8.1; 95% confidence interval (CI) 7.4, 9.0) and non-TBI trauma (SMR 6.7; 95% CI 6.1, 7.4) were at greatly increased risk of mortality. Highest SMRs in both cohorts were observed for accidents. In adjusted Cox regression models, TBI was not associated with increased risk of all-cause mortality (hazard ratio 1.03; 95% CI 0.87, 1.23) compared to non-TBI trauma.
Conclusions:
This study provides evidence that, over a four-year follow-up of older adults, any moderate-severe injury is associated with increased mortality risk. Specifically, older injured adults are at high risk of death from accidental and therefore preventable causes, suggesting that intervention could reduce mortality.
Keywords: traumatic brain injury, older adults, traumatic injury, mortality
Introduction
Traumatic brain injury (TBI) caused over 600,000 emergency department visits and hospitalizations and resulted in almost 21,000 deaths among older adults in the United States in 2013 alone.1 Among survivors of TBI, an even larger number develop sequelae leading to death at a later time.2–4
There is a body of evidence linking TBI to subsequent neurodegenerative decline, including increased risk of Alzheimer’s disease.5, 6 Other studies have provided evidence for increased risk of psychiatric disorders, epilepsy, and stroke following TBI. 7–10 These chronic sequelae likely contribute to increased risk of mortality.3, 4, 11 What is unknown is whether TBI alone is responsible for increased mortality risk or whether any trauma would have the same effect. Individuals with TBI have a higher burden of comorbidities compared to the general population which would likely increase their risk of mortality, but this higher burden of comorbidities may be also present among other trauma patients.12
Prior studies of mortality following TBI have not focused specifically on older adults, compared to a non-TBI trauma cohort, or included specific causes of death. Nonetheless, increased risk of death has been reported.3, 13–15 Among individuals with moderate-severe TBI, standardized mortality ratios (SMR) for all-cause mortality among those aged 65 and older ranged from 1.11-1.99 with the highest SMR observed for pneumonia, mental disorders and injuries.15 Another study reported that the SMR among a mixed-age population hospitalized with TBI was 2.47 (95% confidence interval (CI) 2.31, 2.65) and the highest SMR were observed for mental/behavioral disorders, dementia, and pneumonia.3
To better understand the association between TBI and subsequent post-discharge mortality among older adults, our objectives were to: 1) generate age and sex adjusted SMRs by cause of death for TBI and a non-TBI trauma cohort compared to a general population and 2) assess risk of mortality associated with TBI compared to a non-TBI trauma cohort. We hypothesized that risk of mortality among individuals with TBI would be elevated compared to the standard population and the trauma cohort.
Methods
We conducted a retrospective cohort study of adults aged 65 and older who were treated for traumatic injury at the R Adams Cowley Shock Trauma Center (STC) from 1997-2008. The STC treats more than 6,000 patients annually and is the busiest civilian trauma program in the United States.16 We excluded admissions with in-hospital deaths, deaths within sixty days of discharge from the STC, and individuals with less than sixty days follow-up due to study termination.
Data for this study came from STC trauma registry (STR) which contains data on all STC admissions since 1996 and includes demographic and clinical information, mechanism of injury, details on the nature and severity of the injury, and procedures performed. We linked the study sample to the National Death Index (NDI) Plus system using names and Social Security numbers to obtain date and cause of death.17 This was a secondary analysis of STR data linked to the NDI for a different study; thus, we were limited to data linked through 2008. This study was approved by the Institutional Review Board of the University of Maryland, Baltimore.
Traumatic brain injury
The Abbreviated Injury Scale (AIS) scoring system ranks anatomic injury severity relative to its threat to life on a 1-6 scale, with lower scores indicating milder injury.18 For this study we defined isolated TBI as an AIS head score >2 and no AIS scores for any other body regions >2.
Other trauma
We created a comparison cohort of injured patients aged 65 and older without TBI. Inclusion criteria were an AIS head score <2 and an AIS score for any other body region >2. We applied the same exclusion criteria as with the TBI cohort.
Maryland general population
We obtained age and sex adjusted mortality rates for Maryland residents aged 65 and older during 1999-2008 from the Centers for disease Control and Prevention (CDC) Wide-ranging OnLine Data for Epidemiologic Research (WONDER) database.19 The number of deaths, death rates, and standard errors for death rates can be obtained by place of residence (total U.S., region, state and county), age group (single-year-of age, 5-year age groups, 10-year age groups and infant age groups), and sex.19 Due to small numbers, we did not adjust for race.
Outcome
Date and cause of death were obtained through the NDI linkage. To determine cause of death, International Classification of Disease, Ninth Revision, (ICD-9) codes were used for deaths in 1997 and 1998 and International Classification of Disease, Tenth Revision (ICD-10) codes were used for later deaths. Individuals without a date of death in the NDI were considered to be alive and were censored as of 12/31/2008. We calculated follow-up time by subtracting the admission date of TBI from either the date of death or 12/31/2008. Cause of death groupings were made for the most common causes of death using National Vital Statistics Office groupings.20
Covariates
Information on comorbidities present at baseline was obtained through patient history recorded in the STR. Injury mechanism was categorized as falls, motor vehicle crash, assaults, and other. The GCS is a measure of neurological deficit in eye opening, verbal and motor response.21 The injury severity score (ISS) is used to assign an overall severity score for patients with multiple injuries.22 It is calculated by summing the squares of the three highest AIS scores in separate body regions. Because we required an AIS head >2 and excluded individuals with AIS > 2 for any body region except head, we created ISS categories as follows: 9-15, 16-24, >24.
Data Analysis
We compared distributions of all variables between the TBI and trauma cohorts using Chi square goodness of fit and Student’s t-tests. We calculated the standardized mortality ratio (SMR) and its 95% confidence interval (CI) overall and according to cause of death. First, we used the standard Maryland population to generate the expected number of deaths, adjusting for age and sex. We then divided the number of observed deaths in the study population by the number of expected deaths to obtain the SMR and calculated the 95% CI using standard methods. This was performed separately for the TBI and trauma cohorts.
To determine whether TBI was independently associated with increased mortality comparing to a non-TBI trauma cohort, we conducted a time to event analysis using cox proportional hazards models and controlling for potential confounders not in the causal pathway and identified in bivariate analysis using a p-value of <0.05 for inclusion. Individuals were censored at the date of death or the end of the study period (December 31, 2008). First, we modelled time to any death (all-cause mortality). Next, we modelled time to each of the primary causes of death. Hazard ratios (HR) and 95% CI are reported. Stata 14.0 (College Station, Texas, USA) was used for all data analysis.
Results
Between January 1997 and December 2008, 6,313 people aged ≥65 years were treated at the R Adams Cowley Shock Trauma center for trauma including TBI. Of this group, 1,121 (18%) had isolated TBI and 1,340 (21%) had non-TBI trauma. After excluding 207 people who died within first two months of injury and 388 people without adequate follow-up (i.e., admitted after October 31, 2008), the final sample included 852 people in the TBI cohort and 1,050 people in the non-TBI trauma cohort.
Table 1 shows comparison of study participant characteristics at injury according to TBI status. Patients with TBI were older than those who had non-TBI trauma (77.1 (standard deviation (sd) 7.3) years vs. 75.3 (sd 6.8) years, p<0.001). Falls were the most common cause of injury but were more prevalent among patients with TBI (78.5% vs 43.2%, p<0.001). ISS scores were higher among individuals with TBI, with more than double the number of individuals falling into the highest injury severity category (ISS >24) (16.7% vs. 8.2%, p<0.001). Mean follow-up in the TBI cohort was 1,490.7 (standard deviation (sd) 1,099.4) days compared to 1,566.4 (sd 1,127.1) days in the non-TBI trauma cohort (p=0.14).
Table 1.
Characteristics of patients aged ≥65 years treated for isolated traumatic brain injury (TBI) or non-TBI trauma at the R Adams Cowley Shock Trauma center 1997-2008, n=1,902
| Characteristics | Non-TBI Trauma Cohort, n=1,050 | Isolated TBI, n=852 | p-value1 |
|---|---|---|---|
| Age, mean (SD) | 75.5 (7.5) | 77.1 (7.3) | <0.001 |
| Follow up in days, mean (SD) | 1566.4 (1127.1) | 1490.7 (1099.4) | 0.14 |
| Male, n (%) | 526 (50.10) | 425 (49.9) | 0.93 |
| Race, n (%) | 0.21 | ||
| White | 829 (79.0) | 679 (79.7) | |
| African-American | 176 (16.8) | 125 (14.7) | |
| Other | 45 (4.3) | 48 (5.6) | |
| Admission year, n (%) | <0.001 | ||
| 1997-2000 | 314 (29.9) | 264 (31.0) | |
| 2001-2004 | 375 (35.7) | 368 (43.2) | |
| 2005-2008 | 361 (34.4) | 220 (25.8) | |
| Glasgow Coma Scale Score, n (%) | <0.001 | ||
| ≥14 | 977 (93.0) | 657 (77.1) | |
| 9-13 | 28 (2.7) | 115 (13.5) | |
| <9 | 41 (3.9) | 76 (8.9) | |
| Head AIS | <0.001 | ||
| 0 | 930 (88.6) | 0 | |
| 1,2 | 120 (11.4) | 0 | |
| 3 | 0 | 190 (22.3) | |
| 4 | 0 | 520 (61.0) | |
| 5 | 0 | 142 (16.7) | |
| Injury Severity Score, n (%) | <0.001 | ||
| 9-15 | 741 (70.6) | 182 (21.4) | |
| 16-24 | 225 (21.4) | 528 (62.0) | |
| >24 | 86 (8.2) | 142 (16.7) | |
| Injury cause, n (%) | <0.001 | ||
| Falls | 454 (43.2) | 669 (78.5) | |
| Motor vehicle crash | 390 (37.1) | 143 (16.8) | |
| Other accidents/injuries | 180 (17.1) | 21 (2.5) | |
| Assault | 16 (1.5) | 18 (2.1) | |
| Comorbid disease, n (%) | |||
| Alcohol dependence | 29 (2.8) | 32 (3.8) | 0.22 |
| Alzheimer’s disease | 9 (0.9) | 17 (2.0) | 0.03 |
| Arrhythmia | 14 (1.3) | 16 (1.9) | 0.34 |
| History of Cancer | 24 (2.3) | 19 (2.2) | 0.94 |
| Cerebrovascular disease | 4 (0.4) | 14 (1.6) | 0.005 |
| Depression | 39 (3.7) | 30 (3.5) | 0.82 |
| Diabetes | 178 (17.0) | 146 (17.1) | 0.92 |
| Hypertension | 261 (24.9) | 214 (25.1) | 0.90 |
| Ischemic Heart Disease | 12 (1.1) | 19 (2.2) | 0.06 |
| Parkinson disease | 13 (1.2) | 11 (1.3) | 0.92 |
| Seizure disorder | 10 (1.0) | 19 (2.2) | 0.02 |
p-values from Student’s T-test for continuous variables and Chi-square tests for categorical variables
Table 2 reports SMRs (with 95% CI) for TBI overall and by cause of death compared to the Maryland general population. The all-cause SMR was 8.1 (95% CI; 7.4, 9.0). The highest SMRs were observed for accidents (29.9; 95% CI 20.0, 44.6) and cerebrovascular disease (16.1; 95% CI 12.5, 20.6).
Table 2.
Age and sex adjusted standardized mortality ratio (SMR) and 95% confidence interval (CI) by cause of death among patients aged ≥65 years treated for isolated traumatic brain injury (TBI) or non-TBI trauma at the R Adams Cowley Shock Trauma center 1997-2008
| Cause of disease | Observed deaths in TBI cohort | SMR for TBI (95% CI) | Observed deaths non-TBI trauma cohort | SMR for non-TBI trauma (95% CI) |
|---|---|---|---|---|
| Heart disease | 107 | 6.7 (5.6, 8.2) | 102 | 5.8 (4.8, 7.1) |
| Cancer | 70 | 6.4 (5.1, 8.1) | 67 | 5.3 (4.2, 6.8) |
| Cerebrovascular disease | 62 | 16.1 (12.5, 20.6) | 24 | 5.7 (3.8, 8.5) |
| Chronic lower respiratory disease | 12 | 4.4 (2.5, 7.8) | 23 | 7.6 (5.0, 11.4) |
| Influenza and pneumonia | 15 | 9.0 (5.4, 14.9) | 14 | 7.8 (4.6, 13.2) |
| Alzheimer's disease | 13 | 8.5 (4.9, 14.6) | 10 | 6.1 (3.3, 11.4) |
| Septicemia | 10 | 7.8 (4.2, 14.6) | 13 | 9.2 (5.3, 15.8) |
| Accidents | 24 | 29.9 (20.0, 44.6) | 14 | 15.6 (9.2, 26.3) |
| Overall | 420 | 8.1 (7.4, 9.0) | 388 | 6.7 (6.1, 7.4) |
Table 2 also presents SMRs among the non-TBI trauma cohort compared to the Maryland general population. The all-cause SMR was 6.7 (95% CI; 6.1, 7.4). The highest SMRs were observed for accidents (15.6; 95% CI 9.2, 26.3) and septicemia (9.2; 95% CI 5.3, 15.8).
Before adjustment and compared to the non-TBI trauma cohort, TBI was associated with an increased risk of mortality (HR 1.39; 95% CI 1.21, 1.60) (Supplemental Table S1 and Figure 1). However, in the fully adjusted Cox regression model adjusted for age, injury severity score, history of cerebrovascular disease, and injury mechanism and compared to the non-TBI trauma cohort, TBI was no longer associated with increased risk of all-cause mortality (HR 1.03; 95% CI 0.87, 1.23). There were no significant associations between TBI and mortality in our fully adjusted models of cause-specific mortality.
Figure.
Survival among Adults aged 65 years and Older with Traumatic Brain Injury (TBI) or non-TBI trauma, adjusted for age, injury severity score, history of cerebrovascular disease, and injury mechanism, n=1,902
GCS may be in the causal pathway between TBI and mortality and was consequently excluded from our main models.23, 24 To assess the contribution of GCS to post-discharge mortality, we added it to our models and reran them. TBI was not associated with increased risk of all-cause mortality (HR 0.98; 95% CI 0.82, 1.18).
Discussion
In this large study of older adults treated for traumatic injury at an urban trauma center, individuals with TBI were at greatly increased risk of mortality compared to their peers. These results are consistent with studies that have used a standard population or individuals without trauma as the comparison group.4, 14, 15 However, when we isolated the impact of TBI on mortality from that of any traumatic injury, we found no difference in mortality between injured groups after adjusting for covariates. Thus, our hypothesis that older adults with TBI would have increased mortality relative to older adults with non-TBI trauma was not supported.
Our study suggests that injured older adults are a vulnerable population at increased risk of mortality, especially from cerebrovascular events and injuries, when compared to their age and sex-adjusted peers. Among older adults, injury in general but not specifically TBI may have a causal link to the observed increased rates of death and cause specific mortality. Experiencing injuries may also be a marker of increased mortality risk rather than a precipitating event.25, 26
Relative to a non-TBI trauma cohort and adjusting for age and other factors, older adults who sustained TBI were not at increased risk of mortality. Only two prior studies conducted in mixed age populations made comparisons with a non-TBI injured cohort, yet results are not consistent with ours.2, 27 In contrast with our study, these two studies did not describe or control for injury severity in their final models. Thus, in addition to the significantly older age of our cohort, results from those studies may not be comparable with ours.
Older adults with TBI or other injuries were much more likely to die of accidental causes compared with their age- and sex-adjusted general population peers. Furthermore, falls were associated with increased risk of mortality in both TBI and other traumatically injured populations, consistent with prior work.2, 3, 28 Given the increased risk of repeat falls, mortality among these individuals may have also been fall-related, although we did not explicitly test this hypothesis in this study.29 Also of interest was our finding that mechanism of injury, in particular falls, was highly significant in our models. This suggests that falling captures individual characteristics which may include frailty, sarcopenia, and polypharmacy that are unmeasured in this study but contribute to increased mortality risk.29
This study was conducted at a single site that is the primary adult resource center for the state of Maryland. Our study population may have had more severe injury or medical complexity compared to the general trauma population, impacting generalizability. Importantly, data used in this study are over 10 years old. It is possible that individuals are now surviving more severe injuries which could impact long-term mortality trends. Thus, replication of this study using newer data may be warranted.
This study provides evidence that, among older adults, moderate and severe injuries are associated with increased subsequent post-discharge mortality risk. Specifically, older injured adults are at high risk of death from accidental and therefore preventable causes.
Supplementary Material
Supplementary Table S1 contains two tables: Table 1: Crude and adjusted hazard ratio (HR) with 95% confidence interval (CI) for the association between isolated traumatic brain injury (TBI) and death, comparing to the non-TBI trauma cohort and Table 2. Standardized Mortality Ratio (SMR) Sample Calculation.
Acknowledgements
Conflicts of Interest and Source of Funding: Dr. Albrecht was supported by AHRQ grant 1K01HS024560. The authors declare no conflicts of interest.
Sponsor’s Role: The sponsor had no role in the design, implementation, or interpretation of this study.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplementary Table S1 contains two tables: Table 1: Crude and adjusted hazard ratio (HR) with 95% confidence interval (CI) for the association between isolated traumatic brain injury (TBI) and death, comparing to the non-TBI trauma cohort and Table 2. Standardized Mortality Ratio (SMR) Sample Calculation.