Miller, Kelly J. MPH; Ivins, Brian J. MPS; Schwab, Karen A. PhD
THE well-being of US Armed Forces' members is of critical importance, with ramifications for military readiness as well as overall public health. Among the risks faced by military personnel, during peacetime as well as wartime, is traumatic brain injury (TBI). An investigation of soldiers recently returned from combat in Iraq by Terrio et al1 found that 22.8% had sustained a TBI, and that most of these were mild. An investigation by Hoge et al2 found that nearly 15% of returned combat soldiers had sustained a mild TBI (MTBI), similar to the 12% rate of MTBI among Iraq and Afghanistan combat veterans found by Schneiderman et al.3
Mild TBI can be followed by physical, cognitive, and behavioral symptoms in the weeks immediately after the injury. Most patients recover completely from postconcussive symptom complaints within 3 months of MTBI.4 However, there is evidence suggesting that, in a minority of individuals, symptoms may persist for 6 months or even longer.5–7 No one is certain why symptoms persist after MTBI in some individuals, or to what degree the postinjury symptoms may be attributable to the MTBI as opposed to other medical conditions or problems (eg, migraines, psychiatric disorders, posttraumatic stress disorder [PTSD]) that may result in similar complaints. A possible factor that has not been extensively explored is the potential cumulative effect of multiple MTBIs.
Much of the research on the effects of repetitive TBI comes from sports medicine literature. Findings among these investigations have varied. A prospective study found that among college football players who sustained 2 MTBIs within the same season, symptom endorsement after the second injury did not differ significantly from symptom endorsement after the first injury.8 Along similar lines, a 6-year prospective examination of football players found that those with multiple MTBIs during the study period did not endorse significantly more symptoms than players with 1 MTBI.9 A study by Wall et al10 also found that there was no significant difference in the number of postconcussive symptoms endorsed by jockeys with multiple concussions, and jockeys with a single concussion. Iverson et al11 also found no evidence of cumulative effect of a history of concussion; there were no symptom differences detected among athletes reporting no concussions, athletes reporting a single concussion, and those reporting multiple concussions.
Other sports studies have found evidence of increased symptom complaints among athletes with multiple MTBIs. A study of college football players by Collins et al12 found that players who sustained multiple concussions during the playing season reported more symptoms than those who had a single concussion during the same time period. Another NCAA football study found that longer symptom duration was associated with multiple concussions,13 as did an investigation of collegiate athletes.14
There may be unique features of sports-related injuries including specific mechanisms of injury, as well as the overall capacity of athlete populations to recover from injury, that limit the extent to which findings from sports studies can be applied to mild TBI generally. Although sports concussion and MTBI are often defined similarly, a consensus panel on sport concussion stated that the terms sports concussion and mild TBI “refer to different injury constructs and should not be used interchangeably.”15 It was also acknowledged by the panel that that the majority of sports concussions (80%-90%) resolve within 7 to 10 days, and are characterized by absence of abnormalities on standard structural neuroimaging studies.
The potential cumulative effect of MTBI has not been examined in soldiers, a group for whom both the short- and long-term impact of MTBI has become a particular concern.2,3 The purpose of this article was to explore the effect of multiple MTBI on subjective symptom complaints in a peacetime sample of active duty US Army soldiers. On the basis of prior investigations that have implicated multiple concussions in the persistence of symptom complaints, we hypothesized that soldiers who sustained an MTBI within a year of testing and who had a prior lifetime history of MTBI would have greater endorsement of postconcussive symptoms than those soldiers with only 1 MTBI sustained within 1 year of testing. These soldiers with MTBI were also compared with a matched group of soldiers who reported no TBI, who provided a “background level” of symptom experience among soldiers without brain injury.
MATERIALS AND METHODS
A computerized self-report questionnaire was administered to a convenience sample of 2337 active-duty US Army soldiers at Fort Bragg, North Carolina, who were surveyed between December 1999 and December 2000 (prior to the beginning of US combat operations in Afghanistan and Iraq) as part of a larger institutional review board–approved study examining the consequences of brain injury among paratroopers. Soldiers were recruited for testing through their respective units, and participants provided written consent. The questionnaire asked the soldiers to report whether they had ever experienced a head injury; the number of injuries they experienced; and to provide details on up to 6 separate previous head injury occurrences including the month and year of each injury, severity, and whether they were hospitalized. The soldiers were instructed to include injuries that were not medically attended and those that were. These injuries could include, but were not limited to, those that resulted in loss of consciousness (LOC). For injuries that did not result in LOC, the soldiers were asked to report whether they experienced any alteration of consciousness (AOC), such as being dazed or confused, at the time of injury. Traumatic brain injury was defined as a head injury for which any LOC or any alteration of mental state without LOC was reported.
MTBI was defined as a head injury accompanied by any LOC of 20 minutes or less or any AOC. These characteristics are largely consistent with the criteria for MTBI established by the Centers for Disease Control and Prevention (CDC)16 and the American Congress of Rehabilitation Medicine,17 except that the CDC and American Congress of Rehabilitation Medicine criteria specify 30 or fewer minutes of LOC, and also include memory dysfunction or posttraumatic amnesia criteria. Posttraumatic amnesia was ultimately not used as criteria for MTBI in this investigation; however, because of the fact that posttraumatic amnesia was difficult to establish with self-report instruments. Thus, reports of AOC and LOC were used to establish the presence of MTBI.
Soldiers completed the Post MTBI Symptom checklist, developed by Cicerone and Kalmar,18 in which they were asked to rate their experience with each of 22 symptoms within the 2-week period before testing on a 5-point scale. From the 22 symptoms on the inventory, we selected for examination in this study the following core set of symptoms, which have been used in other studies of post-TBI symptoms:1,19,20 headache; dizziness; fatigue/loss of energy; irritability; sleep difficulty; poor concentration/attention problems/distractibility; decision making difficulty; slowed thinking/difficulty with organization or finishing tasks; forgetfulness; and poor frustration tolerance/easily overwhelmed. This list is also similar to the symptoms used in the International Classification of Diseases, Tenth Revision, criteria for postconcussive syndrome.21 Soldiers were asked to classify each symptom according to its impact in the 2 weeks before testing on a 5-point severity scale, with the following categories: none, mild, moderate, severe, and very severe (see Table, Supplemental Digital Content 1, Postconcussive symptoms and rating scale, available at http://links.lww.com/JHTR/A63).
The threshold for “symptomatic” in this investigation was an endorsement of at least moderate for a particular symptom, as it represented the point at which the symptom caused a disruption of normal daily activities. A threshold was established because we were interested in ascertaining the degree to which symptoms represented a significant problem in the soldiers' daily lives, and because it is not uncommon for symptoms to be endorsed to some degree by healthy people22,23 and individuals without TBI.24,25 We examined 3 categories of symptom endorsement in our analyses: (1) no symptoms, (2) 1 or 2 symptoms, and (3) 3 or more symptoms. These 3 categories were not inherent in the format of the questionnaire, but we established them as variables of interest because we deemed that they represented practical distinctions in terms of the impact on the soldiers. There were few soldiers who endorsed more than 3 symptoms in this small sample, and thus it seemed reasonable to combine into 1 group those who endorsed 3 or more. Numbers of soldiers who endorsed 1 and 2 symptoms were small, and we deemed that combining them into a single category was warranted because of the relative similarity in the difficulty their symptom(s) were likely to pose for them.
Data were analyzed using IBM SPSS Statistics 19.0.0 for Windows. Statistical analyses consisted of χ2 tests, with a significance level at P ≤ .05, to determine independent/dependent relationships between variables of interest.
The total number of soldiers who underwent testing as part of the Fort Bragg study was 2337. The overall lifetime rate of TBI (any severity) among these soldiers was 40.6% (n = 948). It is notable, however, that paratroopers had significantly higher prevalence of any TBI (43.3%) than nonparatrooper soldiers (28.6%; P = .000; χ2 = 31.79; df = 1). A study by Ivins et al26 found that parachute-related TBI accounted for this difference. All of soldiers in this study were paratroopers, by selection criteria.
In order for soldiers reporting TBI to be selected for participation in this study, their TBI(s) could not have exceeded mild severity, and the most recent injury must have occurred within 12 months of testing. Additional selection criteria included age of 35 years or less, enlisted military rank (E1-E9), and paratrooper status (see Table, Supplemental Digital Content 2, Selection of study participants, available at http://links.lww.com/JHTR/A63). There were 101 selected soldiers who reported only 1 MTBI; this group was defined as “One MTBI” for the purposes of this study. The One MTBI group was compared with soldiers who reported sustaining 1 or more additional MTBI during their lifetimes (n = 123), defined as the “Two+ MTBI” group. One MTBI and Two+ MTBI groups were also compared with a matched control group of “No TBI” soldiers. A random sample of 224 soldiers without TBI was selected from the 1002 who met the matching criteria of age, grade/rank, and paratrooper status. Like soldiers with MTBI, soldiers in the No MTBI group were considered to be symptomatic if they endorsed any of the 10 criteria symptoms at a moderate or higher level.
One MTBI and Two+ MTBI groups were divided into subgroups according to time since injury for the purpose of symptom analysis. This was done to enable examination of soldiers in 2 distinct intervals of postinjury recovery: within 3 months since injury, the interval during which recovery from MTBI is typically expected,27 and the postinjury period of 3 months. In this investigation, we defined the “Recent” subgroup to include soldiers who sustained their sole, or most recent MTBI up to and including 3 months before testing, and “Post–3 month” subgroup to include soldiers who sustained their sole, or most recent MTBI more than 3 months to 12 months before testing. Among soldiers in the Recent group, the mean time since injury was an average of 1.6 months. For the Post–3 month group, the mean time since injury was 6.6 months.
One MTBI, Two+ MTBI, and No TBI groups were generally similar with respect to demographic and injury-related characteristics (Table 1). The only statistically significant difference found was in the percentage nonwhite between the Post–3 month, Two+ MTBI group (27.4%), and the No TBI group (40.6%; P = .03; χ2 = 4.59; df = 1). There were no significant differences in demographic characteristics between One MTBI and Two+ MTBI groups, in either time since injury group. Most of the injuries in this study were jump-related (74% overall; 74.3% for One MTBI and 73.2% for Two+ MTBI). This factor differentiates the soldiers in this study from other military populations. Specific mechanism of injury data for non–jump-related injuries (motor vehicle accidents, falls, etc) were not collected.
No data were collected on whether soldiers had combat exposure, for example, deployment in the Persian Gulf War (August 1990 to February 1991). However, most soldiers in this study (80%) were 25 years old or younger at the time of testing in 1999 and 2000, and thus were too young to have served in the Army during the Gulf War. The oldest of the sampled soldiers were 35 years old, ruling out combat in earlier military conflicts. Although it is possible that a small number of the soldiers in this study may have been deployed in the Gulf War, combat exposure is not believed to have been a significant factor in the symptom reporting in this sample. Many of the participants had occupations in combat-related career fields, which included infantry, combat engineer, field artillery, and air defense artillery. Combat-related occupations typically carry a higher exposure to injury agents, but it should be noted that a “career field related to combat” does not indicate that soldiers had combat exposure or combat-related injury.
Soldiers were asked to report up to 6 lifetime injuries; the range of number of injuries reported in this MTBI study group was 1 to 5. In the Recent group, 53.6% had 1 MTBI only, whereas 40% of the Post–3 month soldiers had sustained 1 MTBI only. Table 2 shows the distribution of number of MTBIs among soldiers with 2 or more MTBIs, which were similar for both time since injury groups. For both the Recent and Post–3 month groups, the majority reported 2 only (71.8% and 70.2%, respectively).
Because soldiers were asked to report on injuries that occurred over their lifetimes, there was a wide range of intervals between injuries among those who reported 2 or more MTBIs. For these soldiers, the interval between the injury that occurred within 1 year of testing and the next most recent injury ranged from as short as 1 month, to as long as 25.8 years. Table 2 shows the distribution of intervals between injuries. As with the number of lifetime MTBIs, there were no significant differences in interval distributions between Recent and Post–3 month soldiers.
Table 3 shows symptom endorsement comparisons of Recent and Post–3 month soldiers in both time since injury groups, and No TBI soldiers.
In the Recent group, there was a significant difference in symptom endorsement between soldiers with 1 MTBI and those with 2 or more MTBIs. Individuals with 1 MTBI predominantly reported either no symptoms, or 1 or 2 symptoms. In the Two+ MTBI group, however, most (66.7%) reported 3 or more symptoms, compared with 28.9% in the Recent One MTBI group and 19.6% in the No TBI group reporting 3 or more symptoms. In total, 79.5% of the Two+ MTBI group reported at least 1 symptom, compared with 57.8% in the One MTBI group and 42.4% in the No TBI group. The median number of symptoms in the Two+ MTBI group was 4, whereas the median for the One MTBI group was 1.
In the Post–3 month group, no significant differences in symptom prevalence were observed between MTBI subgroups. One MTBI and Two+ MTBI groups endorsed a median of 1 and 2 symptoms, respectively.
There were significant symptom endorsement differences between the No TBI controls and 3 of the 4 MTBI subgroups: Recent Two+ MTBI, Post–3 month One MTBI, and Post–3 month Two+ MTBI. Only the No TBI versus Recent One MTBI comparison fell short of statistical significance (P = .156; χ2 = 3.71; df = 2).
We explored possible confounders that might have affected these findings, including the influence of MTBI severity, and, for those with 2 or more MTBIs, the number of previous MTBIs as well as the length of time between the 2 most recent MTBIs. Significant differences were not found in regard to injury severity (LOC versus altered consciousness; see Table, Supplemental Digital Content 3, Exploratory analysis of injury severity, available at http://links.lww.com/JHTR/A63), 2 versus 3 or more MTBIs, or interval between TBIs (see Table, Supplemental Digital Content 4, Exploratory analysis of number of, and interval between MTBIs, available at http://links.lww.com/JHTR/A63). Low cell counts may have limited the power to detect significant differences.
To further explore potential confounding factors, we repeated symptom analyses excluding those soldiers whose short interval between injuries, or higher number of injuries, might have disproportionately affected the outcome. In the Recent group, we selected those who had more than 1 year separating their 2 most recent MTBIs (n = 29) and compared them to the 45 soldiers in the One MTBI group. The difference in symptom endorsement remained (69% Two+ MTBIs versus 28.9% One MTBIs with 3 or more symptoms; P = .002; χ2 = 12.20; df = 2). Similarly, we compared symptom endorsement among soldiers with only 2 injuries (n = 28) with that of the One MTBI group, and found that the significant difference in proportions endorsing 3 or more symptoms also remained (64.3% of the Two MTBI group, versus 28.9% of the One MTBI group; P = .01; χ2 = 9.13; df = 2). This suggests that the finding of more symptoms with the Recent Two+ MTBI group was not likely to have been disproportionately influenced by soldiers with a high number of injuries, or a shorter interval between injuries.
The findings of this study indicate that having at least 1 previous mild TBI may make a difference in the likelihood of postconcussive symptoms in the early months following a subsequent mild injury. This is not a longitudinal study, but the similarity in symptom endorsement among soldiers 3 months postinjury suggests that initially increased difficulties experienced as a result of multiple MTBI may diminish as time since injury increases, to a level comparable with that experienced by individuals with 1 MTBI.
In this investigation, the proportion of symptomatic soldiers without TBI was significantly lower overall than that of the MTBI groups. Nonetheless, 42.4% of the soldiers without TBI reported having at least 1 symptom, and 19.6% reported 3 or more. Postconcussive symptoms include problems such as headache, fatigue, and irritability, which are not peculiar to TBI and may be endorsed by individuals without brain injury for a variety of reasons.11 Studies of persons without TBI have found high rates of postconcussive-type symptoms, including 63% to 82% of a college student sample reporting difficulty with concentration, tiredness, and impatience,22 and 59% reporting poor concentration and forgetfulness in a general population.23 The lower symptom rate in the current study may be explained by the higher symptomatic threshold used in this investigation, in which problems had to have caused a moderate or higher level of disruption to their normal daily activities to be counted.
Existing literature on multiple MTBI and symptoms is scant. Some sports-related concussion studies found no differences in reported symptoms between athletes with single and multiple MTBI, whereas this investigation found symptom differences between MTBI groups for recently injured soldiers. One possible explanation may be differences between the groups in willingness to report symptoms. There is a characteristic reluctance on the part of athletes to report symptoms,28 because of not recognizing the potential seriousness of the injury, or out of concern that they may be removed from play. However, it is unknown whether soldiers are more likely than athletes to report lingering symptoms. Another explanation may be differences in injury severity. The mild TBIs sustained by the participants in this study, which were accompanied by LOC for 36%, may have been more severe overall than those typically sustained on the playing field. There is some agreement among researchers of sports-related MTBI that sports injuries are predominantly minor and usually without accompanying LOC,29 and that postinjury problems tend to resolve within 7 to 10 days in 80% to 90% of cases.15,30 However, we are unable to determine if there were actual severity differences between the participants in the current study and those in sports-related concussion studies.
In this study, soldiers with MTBI reported difficulty with at least 1 symptom at rates ranging between 58% and 80%, which are higher than those reported in other studies of MTBI (32%-44%).25,31,32 This is despite the fact that factors such as female sex,5,6,33 older age,25,33,34 lower education, and comorbidity,6 which have been found to be associated with postconcussive symptoms, are notably underrepresented in our population, with its preponderance of males (97%) who are young (maximum age = 35 years; 91% aged 30 years or less), educated at a high school level or higher (95%), and in generally good physical health. Nonetheless, as mentioned earlier, this population of soldiers may have had injuries that were more serious, within the mild spectrum, than those sustained by other individuals. Preexisting emotional problems and expectation of symptom difficulty following brain injury are additional factors that have been linked to postconcussive symptoms;6,35–37 the extent to which these factors may be present in our population of soldiers is unknown.
Symptoms that can follow TBI are associated with other problems relevant to soldiers, notably PTSD38–40 and depression.25 In this investigation, the potential interaction of PCS and PTSD is mitigated by the fact that this is a study of a peacetime military population, tested in 1999 and 2000. As such, this study provides a profile of symptom experienced during peacetime, both for soldiers with and without TBI, which may be useful for symptom comparison with soldiers deployed in combat theaters, who would be influenced by factors such as PTSD, depression, and pain. A recent study by Lew et al41 of veterans returning from combat in Iraq and Afghanistan found that persistent postconcussive symptoms, PTSD, and chronic pain occurred most often in combination with one another, with 42.1% diagnosed with all 3 conditions simultaneously. Postconcussive symptoms was defined as 3 or more symptoms lasting longer than 3 months, and was present in 66.8% of veterans.41 This proportion is substantially higher than the 41.5% endorsing 3 or more symptoms in this study (One and Two+ MTBI groups combined), indicating either some important difference in the MTBIs sustained by the combat soldiers as compared with their noncombatant counterparts, and/or a comorbidity effect involving other factors, such as PTSD and chronic pain.
Because this is a study of self-reported symptoms, malingering is a possible explanation for high rates of symptom reporting. However, there are several reasons why soldiers may have been unlikely to have exaggerated their reporting of symptoms. Soldiers cannot hold the government liable for their injuries; therefore, motivation for compensation was unlikely to be a factor. Additionally, this was a noncombatant group of soldiers, sampled and tested prior to September 11, 2001, and thus would not have had been motivated to exaggerate claims to avoid war duty. Finally, concerns about potential career ramifications of seeking treatment among this population of largely elite, highly motivated paratroopers might have resulted in a tendency to underreport rather than over report symptoms.
This study is strengthened by the presence of a noninjured control group, which is often lacking in analysis of postconcussive symptoms. However, there are several limitations to note in this study, including its use of self-reported injury data. Although self-report of TBI history is useful in studies of mild TBI, because many individuals who sustain an MTBI do not seek medical treatment,34 the fact that injuries were not clinically verified increases the likelihood of injury misclassification. The predominance of paratroopers in this study limits the extent to which findings can be generalized to other military and civilian populations. Low numbers within the time since injury subgroups limit the power of some analyses to detect differences between groups. As a cross-sectional study and not a longitudinal one, caution should be exercised in drawing any conclusions about the course of symptom experience over time.
Given the suggestive nature of the findings of this study, it would be helpful to investigate whether the finding of increased symptom reporting in the first few months after injury for those with 2 or more MTBIs would be replicated in other studies. Specifically, this investigation characterizes MTBI and postconcussive symptoms in a peacetime military population. With findings from this study as a noncombatant comparison, it would be beneficial to investigate symptoms of multiple MTBI in other samples of soldiers who have experienced combat-related TBI, to delineate differences in symptom experience that may be associated with combat injuries and comorbidities. Further research aimed at more sensitively ascertaining the relationship between subsequent injury and increased short-term symptoms would also be useful. Ideally, a prospective study design could enable comparison of the symptom experience between initial and subsequent injury. This would mitigate limitations such as retrospective recall and reporting of MTBI, as well as the wide range of intervals between injuries that were seen in this study.
Our findings indicate that past experience of MTBI may be a risk factor for increased symptom difficulties for several months after injury. When evaluating patients for mild TBI, clinicians should ascertain a patient's TBI history and be aware that even a mild TBI in the past may impact a patient's likelihood of experiencing postconcussive symptoms in the period of up to several months following the injury.
This study adds to existing literature on mild TBI by characterizing postconcussive symptom problems both within and after the acute postinjury period of up to 3 months. Unlike some sports studies that detected no difference in the acute period between those with single mild TBIs and those with additional MTBIs, we found that postconcussive symptoms were significantly more prevalent in the acute period among soldiers with 2 or more lifetime MTBIs than in soldiers who had reported 1 injury only. This study provides further support that the sequelae of mild TBI can present significant problems for some patients, and suggests that additional TBI may explain why some individuals have longer periods of symptoms in the acute period.
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mild traumatic brain injury; military; multiple TBI; postconcussive symptoms; soldier
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