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FEATURE ARTICLE – PUBLIC ACCESS

Veterans with Traumatic Brain Injury–related Ocular Injury and Vision Dysfunction: Recommendations for Rehabilitation

Winkler, Sandra L. PhD, OTR/L1∗; Finch, Dezon PhD1; Wang, Xinping PhD2; Toyinbo, Peter PhD1; Marszalek, Jacob PhD3; Rakoczy, Chrystyna M. OD1; Rice, Candice E. OD4; Pollard, Kendra OD5; Rhodes, Matthew A. OD6; Eldred, Kia OD7; Llanos, Imelda OTR/L1; Peterson, Michael OD8; Williams, Michael PhD9; Zuniga, Esteban MA9; White, Helen MBA10; Delikat, Jemy MOT1; Ballistrea, Lisa DPT1; White, Keith MD1; Cockerham, Glenn C. MD11,12

Author Information
Optometry and Vision Science: January 2022 - Volume 99 - Issue 1 - p 9-17
doi: 10.1097/OPX.0000000000001828
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Abstract

FU1

Increasingly, vision function–related symptoms are recognized as possible long-term sequelae of traumatic brain injury (TBI), which may not be surprising considering that 70% of the sensory processing capacity of the brain is related to vision.1–3 Visual sequelae associated with combat and TBI include closed eye and optic nerve injury (blindness, visual field loss, low vision), orbital fracture or eye muscle injury (diplopia, restricted eye movement, strabismus), eyelid injury (disfigurement, exposure, dry eye), brain focal contusion/hemorrhage (central or peripheral visual field loss), and diffuse brain injury (convergence insufficiency, reduced accommodation, fixation instability, impaired saccades and pursuits, nystagmus).4 Ocular injuries as a percentage of total injuries in combat have increased from 2% in World Wars I and II to 7% in the Vietnam War and 13% in the Gulf War.5,6 Between 2001 and 2017, the average annual incidence of eye injury in the military was 15,681, with 304 hospitalized and 298 at high risk of blindness. During that same period, there were 4394 annual TBI cases without injury to the eye but with visual dysfunction. The total cost of TBI-related visual dysfunction is $1.9 billion annually in 2017 U.S. dollars.5 Veterans with blast-related TBIs report significantly decreased visual quality of life and score the same or worse than other study groups with cataract, thyroid eye disease, or optic neuropathy.6

More than 65% of patients with TBI treated in the Department of Veterans Affairs (VA) Polytrauma Network System of Care report vision problems.1,7 Recognizing the need for specialized services related to returning veterans with polytrauma, the Veterans Health Administration established the Polytrauma/TBI System of Care in 2004 to ensure that returning war veterans with loss of limb and other severe and lasting injuries had access to the best of both modern medicine and integrative holistic therapies. Veterans Health Administration Directive 2008-065, “Performance of Traumatic Brain Injury Specific Ocular Health and Visual Functioning Examinations for Polytrauma Rehabilitation Center Patients,” mandated that all patients with a diagnosis of TBI admitted to one of the five inpatient level 1 polytrauma rehabilitation centers must have a TBI-specific ocular health and visual functioning examination performed by an optometrist or ophthalmologist.8 The mandate provided a template that specified a history of symptoms, a complete clinical examination, and patient recommendations and treatment plan.

Since the 2008 Directive, several studies2,5,6,8–10 have identified the prevalence and symptoms of veterans with TBI-related vision and ocular dysfunction. A 2014 VA Quality Enhancement Research Initiative Evidence-based Synthesis Project1 investigated TBI incidence and prevalence (13 studies) and the types of visual dysfunction (4 studies) among individuals with TBI (veterans, active-duty military, and civilians). Prevalence varied by symptom and study: the prevalence of visual field deficit ranged from 0 to 39%, and convergence dysfunction ranged from 11 to 63%. Variation was attributed to different levels of severity of TBI, setting (inpatient vs. outpatient), and protocols that treated only patients with current symptoms. A systematic review and meta-analysis11 of 22 publications used random-effects models to calculate combined prevalence estimates for the outcomes associated with TBI-related vision dysfunction. A systematic review10 found that accommodative dysfunction was the most frequent (42.8%), followed by convergence insufficiency (36.3%) and visual field loss (18.2%).

The purposes of this study were to understand how the VA's current system of care emerged and to use lessons learned to create a standardized and successful system of vision care that could be implemented within both the VA and community care. We accomplished this by analyzing data generated by the directive to identify patterns of service delivery, including access to and utilization of health care services by veterans with TBI-related ocular injuries and visual dysfunction. The rationale for the study was trifold. First, knowledge of utilization patterns should provide opportunities to structure services so that care can be available outside of the five VA Polytrauma Rehabilitation Centers, thereby increasing access to care in the communities where many of these veterans now reside. Second, the clinical knowledge base created by clinicians during the post-9/11 era, if not adequately captured, would be lost not only to the next generation of clinicians treating service members in future conflicts but also to nonspecialized clinicians currently treating Operation Enduring Freedom/Operation Iraqi Freedom veterans in community versus specialty center settings. Finally, systematic examination of vision function–related rehabilitation outcomes will provide evidence to amend and update practice guidelines for the management of TBI. The research questions asked the following: (1) What specific recommendations were made by the optometrists and ophthalmologists performing the examinations, and (2) what were the relationships between the recommendations and the demographic variables, comorbidity, severity of TBI injury, specific visual and ocular symptoms, and geographical access to vision-related services?

METHODS

The study was approved by the institutional review boards of the University of South Florida and the University of Florida and the Research and Development Committees of the James A Haley VA Hospital and the North Florida South Georgia Veterans Health System. Using a retrospective design, 2458 veterans who had served in the Operation Enduring Freedom or Operation Iraqi Freedom conflicts, had received inpatient or outpatient care at one of the five VA Polytrauma Rehabilitation Centers between January 1, 2008, and December 31, 2017, and had received the mandated evaluation were identified.8 All analyses were performed within the secure VA's informatics and computing infrastructure environment.

The first step in understanding how the mandated evaluation affected the health care utilization of these 2458 veterans was to identify the recommendations made by the optometrists and ophthalmologists performing the examinations. The researchers used natural language processing algorithms to extract recommendations from the text of the evaluation clinical notes. For reliability and validity, two annotators independently identified recommendation key words in the patients' notes. Disagreements between the annotators were adjudicated by an optometry expert, for example, whether prism was an optometry or rehabilitation recommendation or both/either. Agreement statistics were calculated. Annotation and adjudication continued until a 0.7 correlation agreement between annotators was achieved. A rule-based algorithm was constructed that sorted the key words (e.g., orientation, o and m, O&M, blind rehab, tint, advanced blind rehab, and blind rehabilitation) into three categories: rehabilitation, glasses/contacts, or imaging/photography/tests. The frequencies of recommendations by category were stratified by the five polytrauma rehabilitation centers to show variation across evaluating facilities.

The second step in understanding how the mandated examination affected utilization was to determine how the recommendation categories were influenced by demographic variables, visual symptoms, comorbidity, severity of TBI injury, geographic access to care, and the evaluating polytrauma rehabilitation center. The visual symptoms were specific to the history section of the mandated evaluation. Comorbidities were calculated based on work conducted by Pugh et al.12 with the veteran and military TBI population. Glasgow Coma Scale values at the time of injury (abstracted from the Defense and Veterans Eye Injury and Vision Registry) were used as a proxy for severity of TBI.13 For patients with missing Glasgow Coma Scale scores, severity of TBI was extrapolated from the VA Functional Status Outcomes Database Functional Independence Measure score. For patients with missing Glasgow Coma Scale and Functional Independence Measure scores, the research team conferred on severity of TBI in veterans' individual electronic medical records. Previous studies indicated that geographic distance barriers negatively impact utilization of inpatient and outpatient services, leading to a sevenfold decrease in use of VA services by Operation Enduring Freedom/Operation Iraqi Freedom veterans.14 Thus, access measured as distance and travel time to the treating facility were included as covariates and used to map the relationship of the veterans' home zip code at the time the evaluation was performed to the treating facility. Initially, Student t tests and χ2 analyses were conducted to identify demographic and clinical characteristic factors univariately associated with each clinic category. Three logistic regression models (one for each category) using forward stepwise selection were fit to identify factors independently associated (at P < .05).

We further examined the rehabilitation recommendation category to learn more about which VA vision rehabilitation clinics were veterans were referred to. Possible clinics included the following: blind outpatient/blind rehabilitation outpatient specialist, blind inpatient/blind rehabilitation center, vision impairment services team coordinator, vision impairment services outpatient rehabilitation and advanced blind rehabilitation, orthoptics, advanced low vision, intermediate low vision/intermediate low-vision care, low-vision care, occupational therapy, and physical therapy (for vestibular treatment). Key words from the rehabilitation recommendations (with the guidance of the expert panel) were mapped to the VA clinics. The frequencies of rehabilitation recommendations by clinic were stratified by evaluating the polytrauma rehabilitation center.

RESULTS

Description of Cohort

We identified 20,268 unique patients (with and with no TBI) who served in the Operation Enduring Freedom/Operation Iraqi Freedom conflicts. Approximately 12% of the 20,268 (2458 unique patients) were treated at a VA Polytrauma Rehabilitation Center between January 1, 2008, and December 31, 2017, and administered the mandated examination. Study participants had an average of nine comorbidities, with a mean age of 37 years. They were 95% male, 10% Hispanic, 78% White, and 11% African American. Fig. 1 shows the residences of patients on the date the mandated examination was administered. Unique patients are color coded to indicate which polytrauma rehabilitation center performed the mandated evaluation. Fig. 2 reports dates of the mandated examinations by year and treating polytrauma rehabilitation center.

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FIGURE 1:
Location of veterans' home residence (by zip code centroid) on the date of mandated examination, color coded by evaluating polytrauma rehabilitation center.
F2
FIGURE 2:
Mandated evaluations performed by year and by site.

Recommendations by Category

Table 1 displays the number of veterans who received recommendations by category (rehabilitation, glasses/contacts, and imaging/photography/tests) and by treating facility. The total number of referral recommendations (3387) exceeded the total number of veterans in the study cohort (2458), because some veterans received referrals for more than one category. As an example, of the cohort of 2458 patients with mandated examinations, rehabilitation was recommended for 581 (23.6%) during the 10-year study period. More than 50% of the cohort was referred for further testing and/or glasses, not mutually exclusive. Less than 25% were referred for vision rehabilitation. Variation across sites was found, with Tampa recommending further testing and glasses/contacts for the highest percentage of veterans, whereas San Antonio recommended vision rehabilitation for the highest percentage of veterans. Adjusted analyses showed that photosensitivity was the only symptom that was a significant predictor of recommendation to all three categories of recommendation.

TABLE 1 - Number and column percentages show the percent of veterans who received a recommendation per site
Recommendation category Total (n = 2458) Minneapolis (n = 321) Palo Alto (n = 275) Richmond (n = 388) San Antonio (n = 134) Tampa (n = 1340)
Imaging, photograph 1426 (58.0) 143 (44.6) 125 (45.5) 51 (13.1) 16 (11.9) 1091 (81.4)
Glasses/contacts 1380 (56.1) 154 (48.8) 67 (24.4) 120 (30.9) 55 (41.0) 984 (73.4)
Rehabilitation 581 (23.6) 68 (21.2) 99 (36.0) 121 (31.2) 80 (59.7) 213 (15.9)
Percent is calculated as 100 times number of veterans with recommendation in the category/total number of veterans in the center who received a referral. Column percentages do not add up to 100 because some veterans had multiple recommendations from one or more categories.

Fig. 3 uses a circular bar chart to illustrate Table 1 data. Bars are shaded by recommendation category and grouped by evaluating facility. A longer bar indicates more veterans received a recommendation. Fig. 4 shows the overlap in categories of recommendations for the total cohort (Table 1, column 2). Table 2 and Figs. 5A to C show demographic and clinical variables significantly associated with referral for rehabilitation (Fig. 5A), glasses/contacts (Fig. 5B), and imaging/photographs/videos/tests (Fig. 5C).

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FIGURE 3:
Circular bar charts of the percentage of veterans with recommendations by category by polytrauma rehabilitation centers. (A) Minnesota, (B) Palo Alto, (C) Richmond, (D) San Antonio, and (E) Tampa polytrauma rehabilitation centers.
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FIGURE 4:
Venn diagram veterans who received recommendations for one, two, or all three categories of recommendations.
TABLE 2 - Demographic and clinical variables significantly associated with recommendations per category of recommendation
Rehabilitation Glasses Imaging, photographs, videos, tests
c Statistic 0.689 0.792 0.761
Variable OR P OR P OR P
Age (per 10 y) 0.84 <.001 1.21 <.001
Floaters 0.74 .02 1.54 .001
Photosensitivity 1.32 .03 1.67 <.001 1.63 .002
Blurred vision 2.10 <.001
Double vision 1.29 .02
Decreased visual field 1.34 .02 0.75 .03
Decreased night vision 1.48 .01
Balance problems/dizziness 1.36 .02
Difficulty reading 1.63 .001 1.52 .001
Dry eye 1.44 .003
Headache 1.36 .02
Ocular pain 1.34 .05
Comorbidity count 1.02 .15 1.02 .09 0.97 .01
Non-Tampa site 3.94 <.01 0.46 <.001 0.21 <.001
Access in minutes from facility (per 30 min) 1.00 .94 0.89 .073 1.03 .78
Access in miles from facility (per 20 miles) 1.01 .91 1.07 .084 0.98 .79
OR = odds ratio.

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FIGURE 5:
(A) Factors significantly associated with a rehabilitation recommendation (vestibular, low vision, blind rehabilitation, and low vision + blind rehabilitation). (A) Minnesota, (B) Palo Alto, (C) Richmond, (D) San Antonio, and (E) Tampa polytrauma rehabilitation centers. (B) Factors significantly associated with a recommendation for glasses or contacts. (C) Factors significantly associated with imaging, photography, or test recommendation.

Rehabilitation Recommendations

Table 3 shows the rehabilitation recommendations by type of rehabilitation clinic by evaluating center. Many key words from the evaluation recommendations mapped to more than one clinic; therefore, five groups were created: (1) referrals based on key words definitively mapped to blind rehabilitation (inpatient and outpatient) or to (2) low vision, (3) key words mapped to both blind rehabilitation and low vision, (4) key words mapped to vestibular treatment typically treated by physical therapy and sometimes occupational therapy, and (5) key words mapped to occupational therapy. The fifth group, occupational therapy, may have included non–vision-related referrals. Of the 2458 veterans who received the mandated examination, 581 (23.6%) received some type of vision rehabilitation referral. Fig. 6 graphs the Table 3 data showing recommendations per rehabilitation clinic for the first four groups defined previously, within and across evaluating polytrauma rehabilitation centers.

TABLE 3 - Veterans with rehabilitation recommendations by rehabilitation clinic and evaluating facility
Total cohort (N = 2458) Minneapolis (n = 321) Palo Alto (n = 275) Richmond (n = 388) San Antonio (n = 134) Tampa (n = 1340)
Clinic(s) 581 (23.6) 68 (21.2) 99 (36.0) 121 (31.2) 80 (59.7) 213 (15.9)
 Blind rehabilitation 253 (37.2) 23 (33.8) 68 (68.7) 90 (74.4) 70 (87.5) 2 (0.9)
 Low vision 23 (3.4) 0 (0.0) 14 (14.1) 2 (1.7) 2 (2.5) 5 (2.4)
 Blind rehabilitation/low vision 382 (56.2) 46 (67.6) 65 (65.7) 69 (57.0) 25 (31.3) 177 (83.1)
 Vestibular (OT/PT) 22 (3.2) 1 (1.5) 1 (1.0) 0 (0.0) 1 (1.3) 19 (8.9)
 OT* 399 (16.2) 49 (72.1) 67 (24.4) 70 (18.0) 26 (19.4) 187 (14.0)
*May include OT referrals not related to vision therapy. OT = occupational therapy; PT = physical therapy.

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FIGURE 6:
Circular bar charts of the percentage of veterans with recommendations to specific rehabilitation clinics.

DISCUSSION

Anecdotally, vision problems tend to be the most sensitive sign of TBI and typically the last to recover in patients. Patients report that “until my vision was corrected, I really didn't move on in therapy,” and “I couldn't see what the therapist wanted me to do—it was hazy and blurred.” Other veterans did not realize they had vision dysfunction but complained of not being able to follow the football during a game on TV. There was no existing system of care to accommodate the post-9/11 service members returning home to the United States for medical treatment for TBI and other blast-related injuries. This article reports on VA service delivery and utilization for veterans with TBI-related ocular injury and vision dysfunction that emerged after an unpredicted need that was met by dedicated clinicians using resources available at the time.

Variation in referrals for rehabilitation, glasses, and further testing was found. This is not surprising because each of the polytrauma rehabilitation centers evolved independently of the others. The variation in delivery of vision rehabilitation was at least partly attributed to how patient care was uniquely delivered by the VA Polytrauma Rehabilitation Centers and the VA Blind Rehabilitation Service at each polytrauma rehabilitation center site. The VA Polytrauma System of Care, created in 2004, provides comprehensive specialized services related to veterans with TBI and polytrauma, that is, those with a significant associated secondary injury. The VA Blind Rehabilitation Service Continuum of Care, established in 2006, consists of inpatient blind rehabilitation centers, vision impairment services in outpatient rehabilitation programs, advanced low-vision clinics, intermediate low-vision clinics, vision impairment services team coordinators, and blind rehabilitation outpatient service specialists. The variation, albeit unavoidable at the time, now, two decades later, poses a challenge to the standardization of VA care and precludes a clear pathway to treatment.

Overall, the data suggest a need for more standardized accounting of key symptoms and diagnostic testing protocols. In addition, the current service-delivery model may be outdated in that it does not adequately address both the TBI and the related ocular injuries and visual dysfunctions incurred by military personnel serving during the 9/11 and post-9/11 conflicts. In addition, the current delivery model demonstrates a lack of understanding about how the visual system works. There are two visual systems to consider for vision rehabilitation. The afferent system transmits sensory information from the eyes to the brain. Damage to the afferent system causes “visual impairment” that cannot be repaired. Instead, patients are trained to compensate for their remaining visual system. Patients with moderate to severe TBI typically have visual impairment. The efferent system transmits sensory information from the brain to the eyes. Damage to the efferent system causes visual “dysfunction.” Typically, patients with mild to moderate TBI have damage to the efferent system and can be retrained or rehabilitated to at least age-appropriate norms. These differentiations are important for the move toward clinical guidelines for community-based care. See Table 4 for a summary of the VA service delivery models in actual practice, contributed by the optometrists and ophthalmologists performing the mandated examinations at each of the five polytrauma rehabilitation centers. These variations in service delivery models explain at least some of the variance in referrals.

TABLE 4 - Summary of actual service delivery across polytrauma facilities
Rehabilitation services Rehabilitation centers Network sites
Minneapolis Palo Alto Richmond San Antonio Tampa Lexington Tucson
Moderate to severe TBI
 Visual field/neglect OT OD BR, OD LV BR
 Accommodation BRCT (LV, O&M, stroke, TBI, binocular) OTVS
 Orientation and mobility VISOR BR BR
 Magnification OD, BR, LV BR, OD OD, LV
 Glarewear OD, BR OD BR, OD
 Prism visual field loss OD OD OD OD OD
 Legally/totally blind VISOR VIST VISOR BR, OTVS BR BR
Mild to moderate TBI
 Oculomotor BR
 Vergence OT OD BRCT OTVS OD, office, telehealth
 Accommodation BR, OD
 Glarewear VISOR OD, BR OTVS, LV BR, OD
 Prism ocular alignment* OD OD OD OD OD
*Fresnel and ground prism. BR = blind rehabilitation specialist; BRCT = BR cross trained; LV = low-vision specialist; OD = optometry; O&M = orientation and mobility; OT = occupational therapy; OTVS = OT vision specialist; TBI = traumatic brain injury; VISOR = vision impairment services outpatient rehabilitation; VIST = vision impairment services team.

One way the VA has responded to these challenges was to establish advanced fellowships in optometry to provide post-residency training in diagnosis, treatment, and rehabilitation of post-traumatic visual disturbances. The VA National Enterprise System for Telerehabilitation15,16 may be another option to integrate the treatment of TBI with blind rehabilitation. A question posed by this study asks, how should the delivery of vision and TBI rehabilitation services be paired at the community level? The task at hand is to take the best practices from the Polytrauma and Blind Rehabilitation Services to develop a standard of care that can be applied across the VA System of Care, to include community-based care.

This is the first known study to examine service delivery of vision rehabilitation for veterans with TBI-related vision dysfunction and ocular injury. Included in our analyses were calculations of prevalence of symptoms. Our findings were similar to symptoms identified by Capo-Aponte et al.2 in a study that examined the medical reports of 500 U.S. military personnel diagnosed with deployment-related mild TBI who had received eye care at the Landstuhl Regional Medical Center in Germany. Common visual symptoms at the acute stage were blurred vision (66%), reading problems (62%), and light sensitivity (40%), compared with the symptoms of the cohort group at the time of mandated testing at 53, 46, and 58%, respectively. In the cohort in the study by Capo-Aponte et al.,2 89% reported dizziness and 93% reported headache, compared with patients in the current study's cohort, reporting 41 and 39%, respectively. This study built on prevalence of symptoms by identifying significant relationships between symptoms and other clinic and demographic variables and health care utilization.

There were limitations. First, data were captured solely from large administrative databases; thus, the variables selected for analysis were limited to those available in administrative data sets. For example, although we identified veterans with difficulty reading, our data did not enable us to learn more specifics such as the cause of the difficulty reading. Second, this was the first time that the mandated evaluation data (described previously in Introduction) have been evaluated. The authors were able to achieve all of the study's data analysis goals, except they were unable to follow optometry follow-up referrals. The inconsistent wording used by the optometrists jeopardized the validity of the data during natural language processing. As a result, “optometry” was eliminated as a fourth category of recommendations. In the next phase of analyses, the authors plan to take a more in-depth look at optometry assessments and treatment by using natural language processing to examine treatment notes versus analysis of treatment recommendations in the mandated evaluation used for the analyses reported in this study. A third limitation is that some participants may have received rehabilitation as active-duty service members before being admitted to a VA Polytrauma Rehabilitation Center, and this study does not include data from the Department of Defense rehabilitation services.

CONCLUSIONS

The VA Polytrauma System of Care and mandated comprehensive vision evaluation were important first steps in identifying and documenting the many visual and ocular signs and symptoms associated with TBI. Before this system, vision rehabilitation meant only blind rehabilitation. This work represents another body of evidence that documents significant prevalence of visual dysfunction after TBI, dysfunction that can impact daily life, therapies, and improvement across many systems. In addition, this work goes on to objectively identify a need for next steps in TBI-related visual dysfunction, prioritizing clear pathways for a broad spectrum of treatment options within the VA and community reintegration outside the VA.

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