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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury
10
OTHER HEALTH OUTCOMES
Traumatic brain injury (TBI) is an important cause of death worldwide and contributes to a considerable number of deaths and disability in the United States. The Centers for Disease Control and Protection has estimated that about 50,000 of the 1.4 million people who sustain a TBI in the United States will die as a direct consequence (NCIP, 2008). This section examines mortality and premature death in people who have a TBI.
MORTALITY AND TRAUMATIC BRAIN INJURY
PRIMARY STUDIES
Mortality and Traumatic Brain Injury in Military Populations
That head injuries reduce life expectancy has been posited since World War I. Medical records of Bavarian World War I veterans who were patients at a head-injury center were analyzed in 1964–1966 (Walker et al., 1971) (see Chapter 5 for a description of the military cohorts). The head-injury center was established in 1916, and many of the 5,500 men who sustained head injuries in World War I were followed for up to 50 years (Credner, 1930). About 1,000 records were randomly selected, and death certificates were sought from social-welfare offices in Bavaria and West Germany. Vital statistics were obtained for 647 cases and matched with those of 616 uninjured Bavarian World War I decorated veterans, who were able to be traced because they received pensions. Veterans were excluded if they were born before 1880 or died before the age of 35 years, if death dates were unknown, or if records were incomplete. Both penetrating TBI and nonpenetrating TBI were identified; posttraumatic epilepsy was also assessed. Compared with the general population of German men who were at least 35 years old in 1925, those with head injuries had 1.8% more deaths than expected. In 1965, 73% of the veterans with TBI had survived from the age of 35 years to the age of 65 years compared with 80% of those without TBI. Life expectancy of veterans with TBI was about 4 years shorter than that of those without TBI. Posttraumatic epilepsy had the greatest effect on life expectancy after the age of 50 years. Weiss et al. (1982) used data from the same cohort through 1972 to assess life expectancy and correlate it with the severity of injury. By 1972, 77% of TBI veterans (497 of 647) and 78% of control veterans (483 of 616) had died. When TBI was categorized as shallow (nonpenetrating or penetrating less 3 cm; 314 veterans) or deep (penetration greater than 3 cm, perforating wounds, or wounds of ventricle or brainstem; 283 veterans), those with deep wounds
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had slighter higher mortality between the ages of 45 and 60 years, but the difference was not significant (p = 0.6). Similar results were seen when cases were divided by severity of coma (p > 0.6).
Confirming the results of Walker et al., Weiss and colleagues (1982) found that mortality was nonsignificantly (p = 0.08) higher in older TBI veterans with posttraumatic epilepsy than in older TBI veterans without posttraumatic epilepsy; moreover, posttraumatic epilepsy had a marked effect in reducing life expectancy (p = 0.01) in veterans with TBI compared with control veterans. Men with TBI were more likely to die of cerebrovascular disease than the controls (19% vs 12%; p = 0.01), particularly men younger than 60 years old (p = 0.015), but that difference did not correlate with the severity of the TBI.
Corkin et al. (1984) continued work begun by Teuber and colleagues in 1948 on a cohort of 190 World War II veterans with penetrating TBI. Corkin et al. (1984) compared those veterans with a control group of 106 veterans who had peripheral nerve injury, matched for age at injury, years of formal education, and preinjury intelligence-test scores. As of 1983, 28.4% of the veterans with penetrating TBI and 17.0% of those with peripheral nerve injury had died—a statistically significant difference (p = 0.03). However, when veterans with head injuries were categorized by whether they had posttraumatic epilepsy, only those with epilepsy had significantly higher mortality than the controls (p = 0.0002). Such factors as the site of the brain lesion, age at injury, and preinjury and postinjury intelligence scores did not affect survival, although veterans with more education lived longer.
Rish and colleagues (1983) followed 1,127 male Vietnam veterans who had penetrating head injuries for 15 years. Over the 15-year period, 90 deaths (8%) had occurred: 46 in the first year after injury, 9 during the second year, and then 1–4 per year. Most deaths occurred early in the first year after trauma and were the result of the injury or coma sequelae. After 3 years, compared mortality in the head-injured Vietnam veteran population approached the norm, according to actuarial projections for North American men 21–35 years old. Length of coma was the best predictor of long-term outcome, and posttraumatic epilepsy was not a significant factor in mortality in the first 15 years, although each seizure event carried its own inherent risk.
Mortality and Traumatic Brain Injury in Civilian Populations
Mortality in TBI patients can be studied from the time of injury, from the time of discharge from inpatient acute-care hospitals, or from the time of admission into or discharge from inpatient rehabilitation. Rates in cohorts of patients at those different points of entry into a study will be different. For example, rates in patients from the time of injury will be greatest because they include early deaths. In contrast, survivors of the acute phase who are studied during rehabilitation are likely to have lower mortality.
Mortality in Patients from Time of Injury or Admission into Acute-Care Hospitals
Brown et al. (2004) carried out a study to determine whether mortality from TBI was affected by the severity of the injury. Their population-based retrospective cohort study identified all Olmsted County, Minnesota, residents who had a diagnosis indicative of a potential TBI, and they reviewed the medical records from the Rochester Epidemiology Project for 1985–1999 (see Chapter 5). The review confirmed 1,448 cases of TBI—164 (11%) moderate to severe and 1,284 (80%) mild. There were 68 deaths in the moderate-to-severe TBI group. The Kaplan–
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Meier estimated 30-day case-fatality rate was 29.3% (95% CI, 22.0–35.9). The 68 deaths, compared with mortality in the 1990 Minnesota white population, were significantly more than the 12.8 expected (relative risk [RR], 5.29; 95% confidence interval [CI], 4.11–6.17); but the 14 deaths in those with moderate or severe TBI who survived for the first 6 months after injury did not differ significantly from the 12.7 expected (RR, 1.10; 95% CI, 0.60–1.85; p = 0.72). There were 78 deaths in the mild-TBI group, and the Kaplan–Meier estimated 30-day case-fatality rate was 0.2% (95% CI, 0.0–0.4). Over the full followup period, the 78 deaths were significantly greater than the 58.8 expected (RR, 1.33; 95% CI, 1.05–1.65; p = 0.012); but the 69 deaths in the people with mild cases who survived 6 months after injury were not significantly different from the 58.6 expected (RR, 1.18; 95% CI, 0.92–1.49; p = 0.173).
Mortality in Patients Discharged from Acute-Care Hospitals
Selassie et al. (2005) studied a representative sample of 3,679 TBI patients within a year of their discharge from any of 62 acute-care hospitals in South Carolina in 1999–2000 to document mortality within 15 months of discharge. Patients were stratified on the basis of TBI severity and hospital size. Of the sample, 3,371 (91.6%) were alive, and 308 (8.4%) had died within about 15 months of their discharge. Deaths were confirmed by using the Social Security Death Index (SSDI) and were classified as TBI-related or not. Of the 308 deaths, 17% were classified as TBI-related, and 63% of them occurred within the first 3 months after discharge, compared with 47% of the non-injury-related deaths. Findings indicate that the older the person, the higher the likelihood of early death. Males were more likely than females to die after TBI hospitalization if they were younger than 35 years old or older than 54 years old, but mortality was higher in females in the age range of 35–54 years. The authors also report that the severity of the TBI influenced mortality, as did the place of treatment. Patients who were treated in hospitals with trauma centers were less likely to die within 15 months after hospital discharge than patients treated in hospitals without trauma centers.
Mortality in Patients Admitted into or Discharged from Rehabilitation Centers
In a retrospective cohort study, Baguley et al. (2000) assessed mortality in 476 people who had sustained severe TBI over a 10-year period compared with an age- and sex-matched sample of the general Australian population. Patients with TBI, resulting primarily from closed head trauma due to motor-vehicle collisions, were admitted into a rehabilitation hospital 1986–1996. Twenty-seven of the 476 patients with TBI had died by August 1997, for a mortality rate of 5.7%. The median interval between injury and death was 17 months (range, 45 days–108 months after injury). Mortality in the TBI group was significantly associated with a lower level of functional independence on the basis of the Functional Assessment Measure (p < 0.001) slightly significantly with male sex (p < 0.078), with greater age (38 vs 32 years of age; p < 0.055), and with a premorbid psychiatric history (p < 0.064), but not significantly with a history of premorbid substance abuse (p < 0.308). In the general-population sample, the mortality rate was 1.5%. A Fisher’s exact test indicated that significantly more people (p < 0.001) with TBI died (compared with the general population), with most deaths occurring in the first 12 months after injury. The leading causes of deaths were cardiorespiratory events (8 of 27) and infection (6 of 27). The study is limited by the short followup period of about 5 years, the use of data from only one state in Australia, and the lack of functional assessment of and preinjury data on 52% of the deceased and 22% of the living TBI patients.
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Harrison-Felix et al. (2004) studied 2,178 patients with moderate to severe TBI identified in the Traumatic Brain Injury Model Systems (TBIMS) national database, which covers 15 TBIMS rehabilitation centers. Most of the TBIs resulted from motor-vehicle crashes (62%) or acts of violence (20%). The study participants had a mean age of 37 years, 76% were men, 60% were white, and 37% had severe TBI on the basis of 24-hour postinjury Glasgow Coma Scale (GCS) scores. Using vital-status information obtained from the SSDI the authors identified 161 deaths in 2,178 people with TBI who were followed for 17 days–12.8 years after injury for a mortality rate of 7.4%. Compared with age-, sex-, and race-specific mortality rates for the general population, the authors found that individuals with TBI were at twice greater risk of death than those in the general population (95% CI, 1.69–2.31). The median interval between injury and death was 2 years; 38 of the 161 deaths occurred between rehabilitation discharge and 1 year after injury. Life expectancy was reduced by 5–9 years (average, 7 years), depending on age at injury, race, and sex.
Long-term survival of severely injured TBI patients was also studied by Ratcliff and colleagues (2005), who reviewed medical records of 640 TBI patients discharged from a rehabilitation hospital in Pennsylvania during 1974–1984 and during 1988–1989. Most of the injuries resulted from motor-vehicle crashes (66.6%), and falls were next most common cause (16.4%). There were 464 males and 176 females in the TBI population, and their mean age was 37 years. Vital status as of 1997 was determined by using the SSDI. There were 126 deaths, for a standardized mortality ratio (SMR), relative to the expected mortality in the Pennsylvania population, of 2.78 (p = 0.0001). An increased risk of early death was associated with a known history of alcohol abuse (SMR, 6.10; p = 0.0001), substance abuse (SMR, 8.00; p = 0.0264), and other personal or social problems (SMR, 7.03; p = 0.0001). A criminal record or history of psychiatric disorder and years of followup did not modify mortality.
The studies by Brown et al. (2004) and Ratcliff et al. (2005) indicate that functional status at time of discharge from rehabilitation is a leading indicator of later survival time, although severity of injury and other demographic variables, such as age at time of injury, are not.
Shavelle and Strauss (2000) published two mortality studies of people with TBI who received services from the California Department of Developmental Services and survived at least 12 months after injury. The department serves the severely disabled, including those with developmental disabilities and those with long-term cognitive deficits. In nonambulatory patients, observed mortality exceeded expected mortality by a factor of 16.6 in 15- to 29-year-olds and 7.3 in 30- to 44-year-olds. In patients who were more ambulatory, the SMR was 2.5 for 15- to 29-year-olds who could walk with support or could walk unsteadily for at least 10 feet and 2.7 for those who could walk well alone for at least 20 feet.
SECONDARY STUDIES
The committee identified 12 secondary studies, as discussed below. Several studies used cohort designs to examine mortality in people who have TBI. The people studied have been only patients with TBI; that is, there have been no external comparison groups. The best of the studies have followed patients from the time of TBI. Others have examined subsets of the universe of patients with TBI, such as those admitted into rehabilitation hospitals, in which case the more selective nature of the population (survivors of the acute period who enter rehabilitation) may
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lead to death rates different from that in the whole universe of TBI patients who survive the acute period.
Six population-based studies were identified; most found consistent results regarding TBI and increased mortality (Harris et al., 2003; Hukkelhoven et al., 2003; Engberg and Teasdale, 2004; Lu et al., 2005; Flaada et al., 2007; Winqvist et al., 2007;).
Using data from the Rochester Epidemiology Project (see Chapter 5), Flaada and colleagues (2007) compared the observed number of deaths after TBI with the expected number of deaths. Mortality within 6 months increased with age in both moderate and severe TBI cases. Mortality in moderate and severe cases was 40 times that in mild cases independently of age. Among those surviving at least 6 months, 10-year mortality differed from expected only in the adult cases.
Lu et al. (2005) studied mortality associated with TBI in 1984–1996 to determine whether mortality had been decreasing. The study population consisted of 1,839 severely head-injured patients, whose data were extracted retrospectively from the Traumatic Brain Injury Data Bank (635 patients), the Medical College of Virginia (382), and clinical-trial databases in the United States (822). People with penetrating head injuries and treatment groups in the clinical-trial databases were excluded. Of the 1,839 patients with severe TBI, 526 died, for a mortality rate of 28.6%. Over the period 1984–1996, mortality from severe TBI fell from 39% to 27%. After adjustment for a variety of factors—including age, admission motor score, and pupillary response—the difference remained significant (p < 0.05).
Engberg and Teasdale (2004) conducted a population-based study of 389 patients identified in the national hospital register in Denmark who had cranial fractures or traumatic cerebral lesions. The mortality rate was assessed 15 years or more after injury. The acute and subacute mortality rate was 27% in those who sustained cerebral lesions and 4% in those who sustained cranial fracture.
Harris et al. (2003) assessed mortality after head injury in 13,908 people identified through the New York State Trauma Registry from January 1, 1994, to December 31, 1995. The overall mortality rate in all age groups was 14.7% (range, 5.6–30.2%). The authors found an increased mortality rate with increased age: 10.9% at ages 0–30 years, 12.4% at ages 31–50 years, and 21.3% at age above 50 years.
Winqvist et al. (2007) assessed mortality related to TBI by using the Northern Finland Birth Cohorts. One cohort is made up of people born in 1966 in two provinces in Finland and followed over a 34-year period. The authors identified 457 subjects who sustained their first ever TBI during 1966–2000, 78.1% of whom had sustained mild TBIs, including concussions and skull fractures. Nearly 10% had sustained moderate to severe TBIs, including brain contusions, intracranial hematomas, and diffuse traumatic axonal injuries. The authors found that the annual mortality in people with TBI was 14 per 100,000. Mortality related to TBI accounted for 12% of the total mortality in this group.
Hukkelhoven et al. (2003) analyzed individual patient data from four prospective studies (three multicenter randomized clinical trials and one prospective series with closed TBI) to assess mortality and outcome related to TBI. The mean mortality rate ranged from 23% to 40% in the four studies; the mean proportion with an unfavorable outcome ranged from 43% to 60%.
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The authors found that mortality increased with age from 21% in those 35 years old and younger to 72% in those 65 years old and older.
Five secondary studies assessed mortality related to TBI in hospitalized patients (Miller and Jennett, 1968; Fearnside et al., 1993; Lai et al., 1998; Gomez et al., 2000; Pentland et al., 2005). Many of the study populations consisted of consecutive series of patients admitted to hospitals with TBI. The studies found consistent results regarding TBI and increased mortality.
Fearnside et al. (1993) conducted a prospective study of 315 consecutive patients with severe TBI admitted to Westmead Hospital in Sydney, Australia. Severe TBI was defined as a GCS of no more than 8 within 6 hours after injury or deterioration to this level within 48 hours after injury. The authors found that GCS was inversely related to mortality. The correlation coefficient between mortality and GCS was 0.418 (t = 8.14; p < 0.005).
Gomez and colleagues (2000) studied outcomes in a cohort of 810 patients with severe closed head injuries who were consecutively admitted to a hospital in Spain in 1987–1996. Severe head injury was defined as a GCS at admission of no more than 8 or deterioration to this level 48 hours after injury. At 6 months after injury, the overall mortality rate was 50.3%. In general, older patients had worse outcomes: the mortality rate reached 77% in the subgroup of 142 patients over 55 years old, but it was 37.5% in patients 46–55 years old.
Miller and Jennett (1968) evaluated mortality in a consecutive series of 400 patients with depressed fracture of the skull who were treated in the neurosurgical division of the Institute of Neurological Sciences in Glasgow during 1956–1967. The authors found that the cases were associated with a significant increase in mortality (p < 0.005).
Lai et al. (1998) conducted a retrospective study to evaluate long-term outcomes related to severe TBI in 70 patients admitted to a surgical intensive-care unit over a 29-month period. At 1 year after injury, the overall mortality was 50%.
Pentland (Pentland et al., 2005) assessed mortality in a cohort of 1,871 patients with mild, moderate, and severe TBI admitted to a regional head-injury unit in Scotland between 1981 and mid-2002. Of the 1,871, 93 had severe TBI, 205 moderate, and 1,573 mild. Fifty-seven patients died during the initial admission into the unit (42 with severe TBI, 8 with moderate, and 7 with mild). During subsequent years, 340 patients died (six had severe TBI, 33 moderate, and 301 mild).
Studies in the Sports-Injury Literature
To study the influence of intense physical training on life expectancy, Bianco et al. (2007) examined male athletes born in 1860–1930 who had been inducted into various halls of fame: baseball (154), ice hockey (130), tennis (83), football (81), boxing (81), track and field (59), basketball (58), swimming (37), and wrestling (32). Because boxing is characterized by repetitive blows to the head, numbers of bouts and rounds were scrutinized. Median life expectancy of all the samples was 76.0 years; boxers had the lowest median life expectancy (73.0 years), and no differences were found by number of rounds or bouts.
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SUMMARY AND CONCLUSIONS
There is clear evidence of increased mortality in the acute phase after TBI and for some time afterward in both military and civilian populations with moderate to severe TBI. In the military literature, posttraumatic epilepsy in patients who initially survive penetrating head injuries is associated with an increased risk of death and about a 5-year decrease in life expectancy. In the civilian literature, studies in Minnesota suggest that although there is clear evidence of increased mortality in the first 6 months after injury, there is no evidence of increased mortality in patients with TBI beyond 6 months, regardless of severity. Studies of the subset of more severely injured patients who survive initial hospitalization and require inpatient rehabilitation demonstrate a worse prognosis, consistent with the greater degree of residual compromise: mortality some 2–7 times higher than in age- and sex-matched comparison populations.
The committee has reviewed 10 primary studies and 12 secondary studies of TBI and mortality and has found consistent results.
The committee concludes, on the basis of its evaluation, that there is sufficient evidence of a causal relationship between penetrating TBI and premature mortality in survivors of the acute injury.
The committee concludes, on the basis of its evaluation, that there is sufficient evidence of an association between moderate or severe TBI and premature mortality in the subset of patients who are admitted into or discharged from rehabilitation centers or receive disability services.
The committee concludes, on the basis of its evaluation, that there is inadequate/insufficient evidence to determine whether an association exists between surviving 6 months or more after sustaining a mild, moderate, or severe TBI and premature mortality.
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TABLE 10.1 TBI and Mortality
Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
Baguley et al., 2000
Cohort composed of clinical case series
Patients with TBI admitted to Brain Injury Rehabilitation Service, Westmead Hospital, New South Wales, Australia, 1986–1996; cases had survived through admission into rehabilitation facility; comparison group: expected mortality in age- and sex-matched Australian population in 1997
Severe; 97% closed, 3% penetrating
Mortality by August 1997 (mean, 5 years after trauma; range, 8 mo–11 years after trauma); ascertained by New South Wales vital-statistics search
476 patients, mean duration of followup 64 mo; 97% closed head injury, 3% penetrating head injury; 62% MVC, 21% falls or hit by object, 12% assault, 4% sports-related
None
Missing FAM, preinjury information on substance abuse, psychiatric history from patients admitted before 1990 on 52% of the deceased, 22% of the living; no multivariate analysis
27 of 476 (5.7%; 95% CI, 0.037–0.083) dead (median, 17 mo after trauma; range, 45 day–9 years 2 mo after trauma); expected mortality rate, 1.5% (CI, 0.006–0.03) (p<0.001 by Fisher’s exact test)
Contributing factors: low FAM on discharge (p < 0.001), being male (p = 0.078), greater age (p = 0.055), prior psychiatric morbidity (p = 0.064), but not prior substance abuse (p = 0.308) by x2 or t test
Cause of death: cardiorespiratory arrest
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
(30%), infection (22%)
Brown et al., 2004
Population-based retrospective cohort from Rochester Epidemiology Project
Any Olmsted County, MN, resident with medically attended TBI, 1985–1999 (N = 45,831); random 15.7% sample of TBI patients (N = 7,175) reviewed; 1,448 met inclusion criteria; comparison group: age- and sex-specific 1990 white Minnesotans
Documented concussion with LOC; PTA; neurologic signs of brain injury and/or intracerebral, subdural, or epidural hematoma; cerebral hemorrhage or contusion; brain stem injury; penetrating head injury; skull fracture; or postconcussive syndrome
Vital status through 2002 from medical records, state death tapes
Age 35.3 years for moderate–severe, 26.8 years for mild; mean followup, 7.4 years
Age, sex for mortality analysis; age, sex, year of TBI with Cox proportional-hazards model for comparison of moderate–severe vs mild
Unique database on medical care of county’s entire population; cohort not generalizable beyond Olmsted County—few minority-group members (96% white), all care in only 2 institutions
Mortality in moderate–severe: 68 deaths in 164 cases; overall risk of death increased compared with expected, RR, 5.29 (95% CI, 4.11–6.71) by long-rank statistic; 30-day CFR, 29.3% by Kaplan–Meier, risk increased compared with expected, RR, 5.29 (95% CI, 4.11–6.71); 14 deaths in those surviving ≥6 mo, no increase in risk, RR 1.10 (95% CI, 0.60–1.85)
Moderate or severe (11%): skull fracture, intracranial hematoma, brain contusion, penetrating head injury, brain stem injury, or severe complications (neurosurgery, CNS infection,
Mortality in mild: 78 deaths in 1,284 cases; overall risk of death increased compared with expected, RR, 1.33 (95% CI, 1.05–1.65); 9 deaths in first 6 mo (CFR, 0.2%), no
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
subarachnoid hemorrhage, hydrocephaly, CSF leak)
difference from expected 69 deaths in those surviving 6 mo; risk of death not increased compared with expected, RR, 1.18 (95% CI, 0.92–1.49)
Mild (89%): LOC, PTA, postconcussive symptoms, focal neurologic signs
Comparison of moderate–severe with mild: risk of death increased in first 6 mo, RH, 5.18 (95% CI, 3.65–7.30) by Cox proportional-hazards model; no difference ≥6 mo, RH, 1.04 (95% CI, 0.57–1.88)
Corkin et al., 1984
Prospective cohort (World War II veterans assembled at NYU by Teuber in 1948)
All WWII veterans with penetrating head injury from Teuber series (n = 190); excludes few with nonpenetrating head injury; 106 WWII controls with peripheral nerve injuries matched for age, education, preinjury AGCT (85% of controls in Teuber series with such injuries)
Penetrating, at least 3 years after trauma
Mortality to 5/1/1983 as function of various factors
Mortality: 54 of 190 (28.4%) with penetrating head injury dead vs 18 of 106 (17.0%), significant difference by Kaplan–Meier (p = 0.03); those with PT epilepsy (n = 82) more likely to be dead than those without (n = 91) or controls (p = 0.0002); PT epilepsy (p = 0.003), lower education (p = 0.02) associated with death by Cox
Cox proportional regression adjusted for age at injury, years of education, difference in AGCT (preinjury vs 10 years after trauma)
Vital status could not be determined on only one subject (treated as alive); no cause-of-death data collected
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
Harrison-Felix et al., 2004
Retrospective cohort from 15 TBIMS centers
2,178 TBI patients ≥16 years old completing inpatient rehabilitation in 1988–2000; sample is 2,140 who survived >1 year after trauma; comparison group: US age- and sex-specific mortality in 1994
Age 37.4 years, 76% male, 60% white
Mortality from SSA Death Index through 2001
Mortality: 123 of 2,140; median, 2 years; overall, SMR, 2.00 (95% CI, 1.69–2.31); <1 year after trauma, 38 deaths; ≥1 year after trauma, 123 deaths, SMR, 1.95 (95% CI, 1.61–2.29); life expectancy, average reduction, 7 years, depending on age at injury, sex, race, with range 5–9 years
Age, sex, race in determining SMRs from federal statistics for 2000; Cox proportional hazards for those surviving >1 year
Maximum followup only 13 years, average 3.1 years from 1 year after trauma; 38% loss to followup; two of 17 centers did not participate, so sample less representative
Cause of injury: MVC, 62%; violence, 20%; falls, 16%; other, 2%
Severity: 37% severe (24-h max GCS ≤ 8)
ALOS: 21 days acute care, 30 days acute rehabilitation
Risk factors: higher age, unemployment at time of injury, higher DRS score at discharge
Lewin et al., 1979
Retrospective cohort
7,000 consecutive head injured patients admitted into John Radcliffe Infirmary, Oxford, 10–24 years earlier (1955–1969); of these, 479 amnesic or unconscious >1 week; additional selected series: 64 cases unconscious >1 mo admitted to this or other facility 3–25 year earlier
Severe in large part closed, but complicated by compression or penetration (traumatic or surgical for internal decompression) for 77 and 14, respectively, of 331 survivors
Vital status; for 178 (consecutive series), 28 (selected series) who died, cause of death; for 331 survivors, neurologic examination (all), test of cognitive function (217)
Overall mortality, 178 of 469 (38%)
Age, maximum central neural disability score, maximum mental disability score, duration of PTA for model
Only 2% loss to followup; developed model for predicting long-term outcome on basis of age at injury, worst category of mental and neurophysical disability, length of PT amnesia in selected series
(same population studied in book by AH Robert, 1979, with same results, but also mentioned suicide as cause of increased deaths)
Life expectancy for four neurophysical-disability patterns—“decerebrate dementia”: most <1 year, one >10 years; “athetoid pseudobulbar”: reduced only by epilepsy, drowning, inhalation of food, suicide;
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TABLE 10.2 TBI and Brain Tumors
Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
Annegers et al., 1979
Double cohort
All TBI in Olmsted County, MN, 1935–1974 survived initial trauma; no known pre-existing tumor; comparator data from previous incidence study of brain tumors in Olmsted County
Head injury with LOC, PTA, or skull fracture
Brain tumors
Four brain tumors observed (three astrocytomas, one meningioma); RR (observed/expected) not significant overall or for two tumor types
None
TBI that did not reach medical care uncounted
Expected numbers of tumors not adjusted for age or sex to match study population
Burch et al., 1987
Case–control
All brain tumors in Toronto and southern Ontario diagnosed in 1977–1981 and still resident in 1979–1982; of 328 eligible, 247 (75%) participated; comparator, matched hospital controls; of 410 controls asked to participate, 228 (56%) interviewed
Accidents, injuries that involved head (not further specified)
Brain tumors
215 matched pairs analyzed; more cases than controls reported injuries involving head (RR, 2.51; p ≤ 0.0001), but difference not significant if head injury required medical attention (RR, 1.2; p = 0.65)
Matching on basis of sex, area of residence, marital status, ±5 years of birth, date of diagnosis, date of death (if death occurred)
Excluded spongioblastomas, ependymomas, meningiomas, neuroepitheliomas, pituitary adenomas, neurilemmomas.
Recall bias, nonparticipation bias noted by authors
Carpenter et al., 1987
Nested case–control
Workers at two nuclear facilities in Oak Ridge, TN, in 1943–1977; cases
Head injury, self-reported on occupational-medicine pre-employment
Fatal primary malignancy of brain
82 primary brain malignancies: OR, 0.9 (95% CI, 0.2–4.2); for tumors of glial origin: OR, 1.4 (95% CI, 0.3–7.2)
Matched by race, sex, work site, year of birth, year of hire
Misclassification of exposures
Outcome assessed by death certificate,
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
determined by death certificate; four controls per case
assessments
excluding those who had not died of primary brain malignancy
Hochberg et al., 1984
Case–control
Cases with glioblastomas from three Boston, one Providence, one Baltimore hospitals; ≥15 years old; 160 of 231 (69%) of eligibles participated; 125 friend controls matched by 5-year age group
Severe: resulted in skull fracture or concussion, followed by complications (such as coma, intracranial hemorrhage, epilepsy, shock, or long-lasting impairment of memory, hearing, or vision; mild: well-described concussion or brief LOC without other complications
Glioblasatoma, histologically confirmed
Unmatched analysis on 160 cases and 128 controls: overall RR, 2.1 (95% CI, 1.1–4.0); severe RR, 3.8 (95% CI, 1.3–11.0); mild RR, 1.5 (95% CI, 0.7–3.3)
Stratification by age; RR adjusted (unknown for what)
Participation bias, recall bias
Risk increased with age: RR, 10.6 (95% CI, 2.1–53.3) for ≥15 years old at time of TBI
Hu et al., 1998
Case–control
Cases from six major hospitals in Heilongjiang Province, China, in 1989–1995; controls from same hospitals with nonneurologic and nonneoplastic disease
History of head trauma by self-report
Histologically confirmed primary gliomas requiring surgery
34 of 218 cases vs 10 of 416 controls reported head trauma; adjusted OR, 4.85 (95% CI, 2.52–9.44)
Matching on age (±5 years), sex, area of residence
Alcohol and skull x-rays also found as risk factors
Inskip et al., 1998
Double cohort;
All Danish residents
Concussion, fractured skull, or
Intracranial tumors of CNS
Overall SIR, 1.36 (95% CI, 1.20–1.53); ≥1 year PT
None
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
Danish population with TBI compared with Danish population without TBI
hospitalized with TBI, 1977–1992 (n = 228,955); comparator, Danish population without history of TBI
other head injury
SIR, 1.15 (95% CI, 0.99–1.32); no difference by cell type
Monteiro et al., 2006
Hospital-based case–control
231 patients 30–65 years old newly diagnosed with primary brain tumors in 1999–2002, admitted into 10 hospitals in Rio de Janeiro, Brazil; 261 controls matched by age, sex, region of residence from inpatients for conditions other than brain cancer
Head injury >1year before diagnosis of brain neoplasm (cases) or hospitalization (controls) by self-report; hospitalization, amnesia, LOC used as indicators of trauma severity
New diagnosis of primary brain neoplasm, including cerebral meningiomas, brain cancer, cranial nerve tumors, benign and unspecified brain tumors
Association with prior head injury: adjusted OR, 1.49 (95% CI, 1.03–2.15)
Age, sex, education, epilepsy, alcohol consumption
Only 80% of cases confirmed histopathologically, but nonhistopathologic findings most suggestive; participation rate 94% for cases and 90% for controls; reason for hospitalization for 37.4% of controls was trauma; recall bias cannot be ruled out; information on head injury based on self-reports
By histologic type: glioma (n = 31), OR, 1.30 (95% CI, 0.71–2.35); meningioma (n = 38), OR, 1.63 (95% CI, 0.96–2.75); other with histopathology (n = 15), OR, 1.07 (95% CI, 0.52–2.21); other without histopathology (n = 23), OR, 1.92 (95% CI, 0.99–3.73)
As function of severity: hospitalized (n = 15), OR, 0.78 (95% CI, 0.37–1.64); lost consciousness (n = 22), OR, 1.03 (95% CI, 0.55–1.94); amnesia (n = 5), OR, 1.48 (95% CI, 0.38–5.83); any of these (n = 31), OR, 0.93 (95% CI, 0.54–1.60)
As function of number of head injuries: 1 (n = 74),
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
OR, 1.29 (95% CI, 0.85–1.96); >1 (n = 28), OR, 3.14 (95% CI, 1.50–6.61; (p trend = 0.004)
As function of years since head injury: 1–9 (n = 19), OR, 1.18 (95% CI, 0.73–1.89); 10–19 (n = 27), OR, 1.31 (95% CI, 1.06–1.64); 20–29 (n = 23), OR, 1.07 (95% CI, 0.91–1.27); 30–39 (n = 20), OR, 1.09 (95% CI, 0.94–1.26); ≥40 (n = 18), OR, 1.09 (95% CI, 0.96–1.24)
Nygren et al., 2001
Retrospective population-based cohort
311,006 patients hospitalized for TBI in 1965–1994 from Swedish Inpatient Register (of discharges) without current cancer vs age-, sex- and year-specific incidence rates for Swedish population
Skull trauma that survived hospitalization (ICD-7 801, 853–855; ICD-8 801, 850–854; ICD-9 801, 850–854); considered in three severity groups: concussion, severe without neurosurgery, severe with neurosurgery
Primary brain tumors occurring >1 year after trauma through 1995 found by linkage with Swedish Cancer Register, Cause of Death Register, Emigration Register
281 cases of brain tumors (55 meningiomas, 161 primary brain tumors, 65 others) observed in TBI subjects (SIR, 1.0; 95% CI, 0.9–1.2); no relationship for individual types of brain tumor or severity Suggestion of increase in group 30–44 years old at time of TBI: overall, SIR, 1.3 (95% CI, 1.0–1.7); benign meningiomas, SIR, 1.0 (95% CI, 0.5–1.8); primary brain tumors, SIR, 1.4 (95% CI, 1.0–1.8); other, SIR, 1.7 (95% CI, 0.8–3.2)
Stratification by age at injury, sex, years after trauma, severity of injury
Record-linkage design permits assembly of large sample, but limited information available on other risk factors; radiation only likely confounder for brain tumors, but no apparent problem in these negative findings; design adopted because of question of reliability of exposure recall in case–control studies of brain-tumor patients;
No suggestion of trend with
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
time since trauma (p = 0.69) or increasing age (p = 0.25)
completeness of ascertainment of meningiomas in registry of malignant diagnoses unknown
Phillips et al., 2002
Population-based case–control
200 cases newly diagnosed in January 1995–June 1998, ≥18 years old, histologic confirmation by Cancer Surveillance System at Fred Hutchinson; 400 controls, two per case matched on age ± 5 years, sex by RDD or Medicare eligibility lists; all English-speaking residents of three counties in western Washington state with telephone
History of head trauma by self-report; considered “serious” if LOC, went to ED, or hospitalized
Newly diagnosed meningiomas (intracranial); exposures before diagnosis (case applied to two controls) gathered by in-person interviews
99 cases, 142 controls with any head trauma: OR, 1.83 (95% CI, 1.28–2.62); mild, OR, 3.23 (95% CI, 1.82–5.71); severe, OR, 1.27 (95% CI, 0.82–1.98); single, OR, 1.51 (95% CI, 0.99–2.29); multiple, OR, 2.75 (95% CI, 1.48–5.08)
Age at diagnosis, sex, skull radiography, CT scanning of head; race, education left out of model when shown to have had no effect
Participation 84% in cases, 55% random-digit dialing controls, 67% in Medicare controls
Lack of blinding of interviewers to case or control status might increase potential for recall bias
Time before diagnosis: <10 years, OR, 1.39 (95% CI, 0.72–2.68;) 10–19 years, OR, 4.33 (95% CI, 1.28–2.62); ≥20 years, OR, 1.59 (95% CI, 1.09–2.31)
Cases arising less than 1 year after trauma not excluded, so tumor might have been cause of injuries or found incidentally during workup for TBI
Conditional logistic analysis with information on medical, dental exposures to radiation
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
Dose–response relationship for number of head traumas but not expected direction with “severity” of head injury (as defined)
Preston-Martin et al., 1980
Case–control
Cases, women ≤65 years old with intracranial meningiomas identified through cancer registry living in Los Angeles County; one matched control per case from neighborhood
Head injury >2 years before interview that was medically treated by history
Meningioma, histologically confirmed
185 matched pairs analyzed: OR for head injury treated medically, 2.0 (95% CI, 1.2–3.5)
Matched by sex, race or ethnicity, year of birth (±5 years); by selecting controls from neighborhood, also matched by socioeconomic status; multivariate logistic regression
189 of 218 (87%) eligible cases interviewed; interviewers not blinded to case–control status
Differential recall bias
Preston-Martin et al., 1983
Case–control
Cases, men ≤65 years old with intracranial meningiomas identified through cancer registry living in Los Angeles County; one matched control per case from neighborhood
Head injury >2 years before diagnosis by history; severe head injury defined as LOC or permanent scar
Meningiomas, histologically confirmed
105 matched pairs analyzed with exact binomial test: serious head injury not related to boxing, OR, 1.9 (p = 0.01); boxed as sport, OR, 2.0 (p = 0.03); either boxed or had severe head injury unrelated to boxing, OR, 1.8 (95% CI, 1.1–3.2)
Matched by sex, race or ethnicity, year of birth (±5 years); by selecting controls from neighborhood, also matched by SES; multivariate logistic regression
One-sided tests of significance; differential recall bias
Preston-Martin et
Case–control
Cases, men 25–69 years old with
Serious head injury >2 years before
Gliomas and meningiomas,
272 matched pairs (202 glioma, 70 meningiomas)
Matched by sex, race or ethnicity,
277 of 478 (58%) eligible cases
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Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
al., 1989
glioma or meningioma identified through cancer registry, diagnosed in 1980–1984 in Los Angeles County; one matched neighborhood control per case
diagnosis of case that resulted in LOC, dizziness, or medical consultation
histologically confirmed
analyzed with exact binomial test
year of birth (±5 years); by selecting controls from neighborhood, also matched by SES; multivariate logistic regression
interviewed; differential recall bias less likely with different findings for meningioma and glioma
For history of serious head trauma ≥20 years before diagnosis: glioma, OR 0.8 (95% CI, 0.5–1.3); meningioma, OR 2.1 (95% CI, 1.1–5.4)
For meningiomas only, number of serious head injuries, p for trend = 0.01
Preston-Martin et al., 1998
Case–control
Cases from eight centers in six countries (Adelaide, Melbourne, Australia; Grenoble, France; Heidelberg, Germany; Toronto, Winnipeg, Canada; Stockholm, Sweden; Los Angeles, US; men, women ≥20 years old with diagnosed glioma or meningioma
Medically treated head injuries; subgroup of serious TBI: medically treated injuries that resulted in LOC, PTA, or hospitalization; also recorded participation in sports (differed by region) that could result in TBI; proxy respondents could be used if case or control unavailable
Gliomas and meningiomas
297 gliomas, 59 meningiomas
Individual and frequency matching by age and sex; some centers matched on race or geographic region; ORs computed by maximallikelihood estimates by using both conditional, unconditional logistic regression
Subject to recall bias; different methods used for matching at different centers
Glioma: any TBI, males, OR, 1.18 (95% CI, 0.94–1.48), females, OR, 1.03 (95% CI, 0.42–2.55); any serious TBI, males, OR, 1.13 (95% CI, 0.87–1.48), females, OR, 1.07 (95% CI, 0.74–1.56)
Meningioma: any TBI, males, OR, 1.49 (95% CI, 0.86–2.57), females, OR, 0.83 (95% CI, 0.54–1.28); any serious TBI, males, OR, 1.15 (95% CI, 0.57–2.34), females, OR, 0.79 (95% CI, 0.45–1.39)
Borderline increase in risk
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Reference
Study Design
Population
Type of TBI
Health Outcomes or Outcome Measures
Results
Adjustments
Comments or Limitations
for >1 TBI in men with glioma (OR, 1.52; 95% CI, .00–2.32) but not seen in women or men with meningioma
No correlation with sports participation
Risk of meningioma in men higher 15-24 years after trauma (OR, 5.35; 95% CI, 1.72–16.62)
Schlehofer et al., 1992.
Population-based case–control
226 cases in Rhein-Neckar-Odenwald area of Germany with primary brain tumors diagnosed 1987–1988; controls, 418 randomly selected from residential registers
Self-reported history of head injury requiring medical attention; obtained by interview
Primary brain tumors (ICD-9 191, 191.1, 192.0), restricted to gliomas (115), meningiomas (81), acoustic neuromas (30)
For all tumor types: 46 of 226 (20%) vs 113 of 418 (27%); RR, 0.71 (95% CI, 0.5–1.1)
Age-, sex-matching for controls
418 of 521 (72%) potential controls participated; self-reports of head trauma; no comparisons by severity or number of injuries
For gliomas: 27 cases vs 66 controls; RR, 0.70 (95% CI, 0.4–1.2)
For meningiomas: 13 cases vs 39 controls; RR, 0.52 (95% CI, 0.3–1.0)
NOTE: CI = confidence interval, CNS = central nervous system, CT = computed tomography, ED = emergency department, ICD = International Classification of Diseases, LOC = loss of consciousness, OR = odds ratio, PT = posttrauma, PTA = posttraumatic amnesia, RDD = random-digit dialing, RR = relative risk, SES = socioeconomic status, SIR = standardized incidence ratio, TBI = traumatic brain injury.
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