Abstract
Background:
Women in the U.S. military are now authorized to serve in direct combat occupations. This may increase their risk of combat injuries, such as concussion, in future conflicts. Knowledge of sex differences in health profiles after concussion is paramount for military medical planning efforts. The purpose of this study was to assess sex-related differences in health profiles among U.S. military personnel following deployment-related concussion.
Materials and Methods:
We conducted a retrospective study of service members who sustained a concussion during combat deployment between 2004 and 2013. Postinjury diagnoses were abstracted from outpatient encounters in electronic health records for 24 months after concussion. We used hierarchical clustering to identify clusters, termed “health profiles,” and logistic regression to determine whether sex predicted membership in the health profiles.
Results:
The study sample included 346 women and 4536 men with deployment-related concussion. Five postinjury health profiles were identified and classified as no morbidity, back pain, tinnitus/memory loss, posttraumatic stress disorder/postconcussion syndrome, and multimorbidity. Women relative to men had higher odds of membership in the back pain (odds ratio [OR] = 1.32; 95% confidence interval [CI] = 1.05–1.67) and multimorbidity profiles (OR = 1.44; 95% CI = 1.03–2.00) and lower odds than men in the tinnitus/memory loss profile (OR = 0.62; 95% CI = 0.42–0.91).
Conclusions:
Postinjury health profiles among U.S. service members differ by sex following deployment-related concussion, particularly with a higher burden of multimorbidity among women than men, which may require interdisciplinary care. Women also had higher odds of membership in the back pain profile and lower odds in the tinnitus/memory loss profile than men. To prepare for future military operations where women may have greater exposure to combat, continued research elucidating health-related sex differences after deployment-related concussion is imperative.
Introduction
Historically, women in the U.S. military were excluded from participation in ground combat and served only in combat support roles. 1,2 With the blurred battle lines of asymmetric warfare during the post-9/11 overseas contingency operations (OCOs) in Iraq and Afghanistan, and the predominant use of improvised explosive devices by insurgents, women in combat support occupations became frequent casualties of attack. 3 This resulted in the highest number of injured U.S. military women relative to any other conflict. 4 In 2013, the Department of Defense lifted its combat exclusion policy for women, allowing women to serve in all military occupations. 1 As a result of this policy change, women may be at increased risk of combat injuries, such as concussion, in future conflicts. 5
Concussion, or mild traumatic brain injury (TBI), was one of the most common injuries during the recent military operations in Iraq and Afghanistan, 6,7 often resulting from blast weaponry that was frequently used by enemy forces. 8,9 In one study, concussion was diagnosed in over 40% of service members injured by a blast, 10 and nearly one in five of all deployed military personnel reported a probable concussion incident. 11 There is a growing body of literature on sex differences in outcomes among military personnel with concussion. 12 Compared with men, women with a history of concussion have more outpatient visits 13 and higher frequency of multisensory 14 and psychological impairments 15,16 but lower rates of alcohol misuse. 17 –19 Two studies of suicidal ideation among veterans with concussion found no sex differences. 20,21 Furthermore, concussion has been linked to posttraumatic stress disorder (PTSD), an anxiety disorder associated with an array of negative health consequences that often occurs more frequently in women than men. 16,22
The neurologic, psychological, and physical conditions resulting from concussion can co-occur, and multimorbidity (i.e., co-occurrence of two or more health conditions) has been shown to negatively impact quality of life. 23 Postconcussion syndrome (PCS) is defined by a constellation of symptoms that can occur following concussion, including sleep problems, anxiety, depressed mood, dizziness, and headaches. 6 Women have been found to report more postconcussion symptoms than men. 24,25 The polytrauma clinical triad (PCT) refers to the simultaneous presence of concussion, pain, and psychological symptoms, and it has been described in military veterans with concussion. 26 –29 Lew et al. 26 reported a 42% prevalence of PCT in veterans, with back pain the most prevailing pain symptom. Pugh et al. 29 identified that PCT was common in both men and women in the Department of Veterans Affairs (VA) system, but they did not examine sex differences. As more women are included in direct combat occupations, they may be at increased risk of concussion in future military operations. Knowledge of sex differences in both individual and co-occurring symptoms can lead to refinements in care and improved treatment outcomes. 5
The effects of concussion in the military have been shown to potentially last years. 30 With women occupying a more active role in future combat operations, it is imperative to examine sex differences in the burden of concussion and related morbidity on the military health care system for the purposes of medical planning, resource allocation, and treatment of women veterans. 12 The purpose of this study was to assess sex differences in postinjury health profiles among U.S. military personnel following deployment-related concussion.
Patients and Methods
Study sample
The study sample for this retrospective analysis was obtained from the Expeditionary Medical Encounter Database (EMED) and included U.S. service members with a single concussion injury event documented during combat deployment between 2004 and 2013; service members with multiple concussions documented in the EMED were excluded. 7,31 The EMED is a deployment health database that maintains clinical records of military personnel wounded in-theater during post-9/11 OCOs. These records are reviewed by certified nurse coders who assign diagnostic codes to patients’ injuries (e.g., International Classification of Diseases, 9th Revision, Clinical Modification [ICD-9-CM] 32 and Injury Severity Score [ISS]). 33 The study sample included only service members in combat support roles 34 who had at least one ICD-9-CM code in the Military Health System Data Repository (MDR) during the 24-month follow-up period. The final study population included 4882 service members (346 women and 4536 men). This study was approved by the Naval Health Research Center Institutional Review Board (NHRC.2003.0025).
Measures
Concussion
Consistent with previous research, 7 concussion was identified from the EMED via ICD-9-CM codes 850.0 (concussion with no loss of consciousness [LOC]), 850.11 (concussion with LOC of 30 minutes or less), 850.5 (concussion with LOC of unspecified duration), or 850.9 (concussion, unspecified). Service members with other TBI ICD-9 codes were excluded (i.e., 800–801.9, 803–804.9, 850.12, 851–854).
Covariates
Demographic and injury-specific variables of interest included age, service branch (Army, Marine Corps, or Navy), previous combat deployment (yes or no), injury mechanism (battle, blast; battle, nonblast; or nonbattle), LOC (yes, no, or unknown), and ISS. Age was calculated as the difference between date of concussion and date of birth. Deployment records from the Defense Manpower Data Center were used to determine previous deployment to Iraq, Afghanistan, or Kuwait. ISS is a measure that summarizes the overall severity of multiple injuries sustained by a patient and was categorized as mild to moderate (ISS 1–8) or serious to severe (ISS 9+). 33
Health outcomes
Physical and mental health outcomes of interest were obtained from the MDR as ICD-9-CM codes for 24 months postinjury. The following health conditions and corresponding ICD-9-CM codes associated with concussion were identified: hearing loss, unspecified (389.9); hyperacusis (388.42); tinnitus (388.3); dizziness (784.0); headache (780.4); memory loss, not otherwise specified (780.93); vertigo (438.85); acute stress reaction, unspecified (308.9); anxiety/irritability (300); depression (311); sleep disturbance (780.5); insomnia (780.52); blurred vision, not otherwise specified (368.8); and photophobia (368.13). 35 After careful consideration by subject matter experts, the following conditions and codes were also included in the analysis: PTSD (309.81); PCS (310.20); back pain (719.45, 719.65, 719.85, 719.95, 721.91, 720.0, 720.2, 721.2, 721.3, 721.41, 721.42, 721.5, 721.6, 722.10, 722.11, 722.31, 722.32, 722.51, 722.52, 722.72, 722.73, 722.92, 722.93, 724.01–.03, 724.1–.6, 737.10, 737.19, 737.20, 737.29, 737.30, 737.34, 737.39, 737.41–.43, 738.4, 738.6, 739.2–.4, 739.5, 756.11, 756.12, 846.0–.3, 846.8, 846.9, 847.2, 847.3, 848.5, 953.1–.3, 953.5, 956.0); neck pain (721.0, 721.1, 722.0, 722.4, 722.71, 722.91, 723.0–.5, 723.7–.9, 738.2, 739.1, 756.2, 847.0, 953.0, 953.4, 954.0, 957.0); and substance use (291, 292.0–292.1, 292.3–292.9, 303, 304, 305.0, 305.2–305.7, and 305.9).
Statistical analysis
All statistical analyses were conducted in SAS version 9.4 (SAS Institute Inc., Cary, NC). Hierarchical cluster analysis was conducted on the medical outcome categories per previous research on diagnostic codes. 36 We used Ward’s minimum variance method to determine relevant clusters with the Trim option to remove outliers. 37 An examination of the dendrogram and pseudo T identified the ideal number of clusters, and an inclusion criterion of 50.0 (i.e., probability of each of the 19 medical outcome categories in that cluster) was used to determine relevant categories for each cluster. Identified clusters were termed “health profiles.” A cluster analysis methodology has been used previously within an injured military population and has been described in more detail elsewhere. 23 Chi square tests for categorical variables and a t-test for age were used to assess differences by sex. Multivariable logistic regression models were used to determine whether sex predicted membership in any of the postinjury health profiles. Models were adjusted for all covariates. Odds ratios (ORs) and 95% confidence intervals (CIs) were reported.
Results
The characteristics of the study sample are shown in Table 1. Most service members were injured by a blast (86.5%) and had mild-to-moderate injury severity (87.0%). Men had a higher percentage of blast injury mechanism and serious-to-severe injuries than women. Approximately, 43.2% of the sample did not have LOC with concussion, and men had a higher proportion of LOC (35.3%) than women (24.9%). More than one in five service members had documentation of a previous combat deployment, which was more prevalent in men (23.3%) than women (14.7%). Sex also differed by service branch, with a higher proportion of women (86.7%) in the Army compared with men (70.1%).
Sample Characteristics by Sex
ISS, Injury Severity Score; LOC, loss of consciousness; SD, standard deviation.
Table 2 details the results of the hierarchical cluster analysis. Overall, in 27.4% (n = 1340) of the sample, none of the health conditions were present, and these individuals were placed in a profile termed “no morbidity.” For the remaining 3542 individuals, cluster analysis was used to identify health profiles. An examination of the dendrogram and pseudo T showed that a four-cluster solution was ideal with 355 individuals (40 women, 315 men) removed as outliers in the Trim option. The resultant health profiles were termed “back pain” (28.5%), “tinnitus/memory loss” (13.4%), “PTSD/PCS” (12.5%), and “multimorbidity” (10.9%). The multimorbidity profile had six conditions that met the 50.0 relevance criterion, including insomnia, headache, memory loss, anxiety/irritability, PTSD, and back pain.
Distribution of Probabilities in the ICD-9-CM Diagnosis Categories by Postdeployment Health Profiles
Note. Diagnosis categories that did not reach the relevance criterion in any health profile are not shown (i.e., hearing loss, hyperacusis, dizziness, vertigo, acute stress reaction, depression, sleep disturbance, blurred vision, photophobia, neck pain, and substance use).
Met relevance criterion of
ICD-9-CM, International Classification of Diseases, 9th Revision, Clinical Modification; PCS, postconcussion syndrome; PTSD, posttraumatic stress disorder.
Table 3 presents the results of the multivariable logistic regression models examining the predictive effect of sex on the five identified health profiles. Women had higher odds of membership in the back pain (OR = 1.32; 95% CI = 1.05–1.67) and multimorbidity profiles (OR = 1.44; 95% CI = 1.03–2.00) compared with men. Women relative to men had significantly lower odds of membership in the no morbidity (OR = 0.55; 95% CI = 0.41–0.73) and tinnitus/memory loss profiles (OR = 0.62; 95% CI = 0.42–0.91). There were no sex differences when examining the PTSD/PCS health profile.
Associations Between Sex and Postinjury Profile (N = 4882 a )
Note. Multivariable logistic regression was used to determine whether sex predicted membership in any of the postinjury health profiles. Models were adjusted for age, service branch, injury severity, injury mechanism, loss of consciousness, and previous deployment.
In total, 355 individuals removed during the Trim option in hierarchical cluster analysis were included in the reference group for each of the multivariable regression models.
CI, confidence interval; OR, odds ratio; PCS, postconcussion syndrome; PTSD, posttraumatic stress disorder.
Discussion
Women’s health initiatives in the U.S. military remain a priority, particularly with the recent lifting of the combat exclusion policy that may result in women being exposed to higher levels of combat in future operations. 1,5 The present study found that women relative to men had higher odds of membership in the multimorbidity and back pain health profiles following deployment-related concussion. Back pain can negatively impact a patient in a variety of ways, 38 and multimorbidity has been found to be associated with lower quality of life among service members. 23 This suggests a need for interdisciplinary teams to appropriately manage concussion to foster recovery while minimizing prolonged effects. Military medical professionals should be aware of potential sex differences when treating veterans with concussion.
The finding of sex differences in the multimorbidity profile is novel to the literature but not entirely surprising. Previous studies have found women have higher rates than men for several of the conditions that met the inclusion criterion in the multimorbidity profile. 22,24,39 An analysis from the Millennium Cohort Study found women were more likely than men to report chronic multisymptom illness after deployment, which includes general fatigue, mood and cognition abnormalities, and musculoskeletal pain. 40 A comprehensive evaluation of multimorbidity after concussion is needed to provide appropriately focused health care, particularly for women, given that it requires care in multiple primary and specialty care settings. In the initial postdeployment phase of concussion care, a model similar to the patient-centered medical home might be considered and could incorporate targeted screening for multimorbidity after deployment-related concussion. 41 The course of treatment may also involve specific case managers affiliated with neurology, psychology, and pain clinics designed to encourage utilization of specialty care. Rehabilitation specialists, such as physical therapists, should consider techniques to augment coping self-efficacy and healing imagery, which can improve patient outcomes. 42 Psychologically informed practice, to include interventions such as education to reduce fear-avoidance beliefs, quota-based exercise, and graded exposure, should be incorporated into the rehabilitation course. 43 Sequelae in women may continue beyond military service, as shown in a study by Amara et al. 44 that found higher rates of VA health care utilization in women compared with men who experienced combat-related concussions. This suggests that clinical screening tools and treatment plans must target injured women for both short- and long-term care. Considering women are the fastest growing demographic among veterans, 45 it is imperative that concussion clinical management protocols address their unique risk factors and provide care to address multimorbidity.
Back pain is ubiquitous in war-wounded military service members; almost half of all military members injured on deployment have been reported to have at least one back pain diagnosis between the time of injury and follow-up post redeployment. 46 The relationship between concussion and back pain is less clear. Mollayeva et al. found that bodily pain, such as back pain, is frequently experienced in individuals with delayed recovery following concussion, with up to 93% reporting persistent chronic symptoms. 47 Interestingly, they found no sex-related differences in pain frequency, findings that diverge from those observed in our study. It is plausible that this divergence may be explained in part by differences in study samples and injury mechanisms. Moreover, there are mixed findings on whether concussion confers a higher risk of back pain in military personnel, 26,48 which highlights the need for further research. It is possible that the association identified in the present study is reflective of a general sex-based risk of back pain among military personnel, which has been identified in at least one other study. 49
The connection between neuromusculoskeletal pain and concussion is complex. Concussion has been found to be strongly associated with pain intensity and health-related quality of life and functioning in military members. 50 However, these effects appear to be mediated by comorbidities such as PTSD, depression, anxiety, and sleep disturbance. In a study performed by Watrous et al., 46 approximately 60% of service members and veterans diagnosed with recurrent low back pain also had PTSD or depression. Military personnel with concussion have been found to have higher inflammatory biomarker levels and greater pain compared with healthy controls. 51 Although the associations between neuromusculoskeletal pain, concussion, and function are acknowledged, the interactions between physical or psychological stressors, trauma to the emotional circuitry of the brain, and protective resiliency factors are still not well understood. 52 Interestingly, individuals with chronic pain disorders and no history of head injury have previously been reported to demonstrate symptoms reflective of PCS, a finding that is likely tied to psycho-emotional etiology. 53 Furthermore, interactions between anatomical, physiological, and psychological effects of concussion may be intricately linked, especially through the hypothalamic–pituitary–adrenal axis. 54 Future studies should aim to elucidate these mechanisms.
There were additional findings of interest. Interestingly, women had significantly lower odds of membership in the tinnitus/memory loss profile, which may reflect a greater tendency for men to attribute symptoms to the concussion rather than psychological reasons. Further, the most prevalent health profile was no morbidity, reflecting individuals without any of the conditions assessed in the present study. Women had lower odds of membership in this profile, which may be indicative of differences in care seeking or symptom reporting within the military population. 55 More examination is needed of the patterns of health care utilization and postconcussion symptoms in both military women and men, which could help to refine clinical practice guidelines.
This study had several strengths. Our study sample was restricted to combat support occupations only, thus accounting for the lack of women in direct combat occupations during the study period. Using cluster analysis allowed us to assess coexisting disorders rather than individual conditions alone. Accurate point-of-injury information abstracted from the EMED clinical record reduced the impact of recall bias and added more granularity to the analysis by accounting for mechanism, severity, and LOC status. There were also limitations that warrant mention. Because we restricted our population to service members with only one documented concussion event in the EMED during the study period, we could not address the potential impact of multiple concussions, including concussions that were not documented or occurred prior to the study period. It is also important to note that we did not account for preexisting health conditions, and postinjury diagnoses may not be attributable to the concussion injury event. In addition, cluster analysis classifies individuals based on probability of each assessed health condition, and thus, the true prevalence of the identified health profiles may differ. Lastly, by using ICD-9 diagnosis codes, we included treatment seekers only, and thus, those who had symptoms but did not present for care are not represented.
To the best of our knowledge, this is the first study to examine and identify sex differences in health profiles after deployment-related concussion. Overall, the findings suggest a need for targeted clinical interventions for women with concussion to address multiple symptomologies and to provide areas for future research to mitigate the long-term impact of these conditions. As more women serve in combat roles, an increase in concussions and associated morbidity among military women may be expected in future combat operations. An interdisciplinary approach to concussion management in women should be considered to maximize force readiness and improve their overall short- and long-term well-being.
Footnotes
Authors’ Contributions
A.J.M. and D.J.C. designed the study and drafted the article. J.M.Z. analyzed the data. All authors interpreted the data, critically revised the article for important intellectual content, and approved the final version to be published.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
This work was supported by the U.S. Navy Bureau of Medicine and Surgery under work unit no. 60808.
Data Availability Statement
The datasets generated and/or analyzed during the current study are not publicly available because of security protocols and privacy regulations, but they may be made available on reasonable request by the Naval Health Research Center Institutional Review Board (contact phone +1 619 553 8400).
Disclaimer
The authors are service members or employees of the U.S. Government. This work was prepared as part of their official duties. Title 17, U.S.C. §105 provides that copyright protection under this title is not available for any work of the U.S. government. Title 17, U.S.C. §101 defines a U.S. government work as work prepared by a military service member or employee of the U.S. government as part of that person’s official duties. Report No. 22–75 was supported by the U.S. Navy Bureau of Medicine and Surgery under work unit no. 60808. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the U.S. government. The study protocol was approved by the Naval Health Research Center Institutional Review Board in compliance with all applicable federal regulations governing the protection of human subjects. Research data were derived from an approved Naval Health Research Center Institutional Review Board protocol (NHRC.2003.0025).
