Prior to the assessment, P.F.C. self-reported a total score of 41 on the postconcussion symptom scale (PCSS).8 During all DLS conditions, P.F.C. maintained his balance for the maximum test duration of 30 seconds. P.F.C. was most sensitive to starts and stops of visual motion (optic flow) and occasionally stumbled out of DLS at the beginning and end of these conditions (see Video, Supplemental Digital Content 1, Pretreatment DLS Performance During Optic Flow, http://links.lww.com/JNPT/A17). P.F.C. did not reach the 30-second maximum duration for any of the SLS conditions (Figure 2).
P.F.C. demonstrated increased reaction times during symbol recognition and matching tests when compared to nonconcussed individuals. He averaged 591 ± 65 ms per response on the DLS symbol recognition test with no optic flow (compared to our average normative values of 443 ± 79 ms). There was no significant difference in symbol recognition reaction times with the addition of optic flow and gait. During DLS with no optic flow, P.F.C.'s symbol matching reaction time average was 998 ± 291 ms (compared to our average normative values of 765 ± 93 ms). There was no change in symbol matching performance with the addition of optic flow or gait. Across all Stroop conditions, P.F.C. averaged an accuracy rate of 85 ± 10% (compared to our average normative values of 96 ± 4%).
Gait deviations were not observed during unperturbed conditions. Consistent with previous reports, gait deviations (ie, cross-over steps, stumbling, and veering from a straight path) and step width variability increased dramatically during platform and visual perturbations (Figure 3).20 P.F.C. had difficulty adapting to visual perturbations and often drifted to the lateral borders of the treadmill (see Video, Supplemental Digital Content 1, Pretreatment Gait During Visual Perturbations, http://links.lww.com/JNPT/A17). He ended the VR-based assessment with no change in his PCSS total score of 41.
In addition to the VR-based assessment, measures of agility (4 square step test21) and dynamic postural balance (Y-balance test22) were performed outside of the CAREN. These are common clinical measures and provided a comparison of VR-based measures to clinical measures performed with minimal cost or setup. Furthermore, neither the tests nor their components were part of the intervention and were considered untrained motor tasks. P.F.C.'s average 4 square step test time was 7.11 ± 0.5 seconds (normative values: 4.93 ± 1.0 s). His normalized composite Y-balance score was 91.5 ± 1.2 (normative values: 93.5 ± 7.0).
P.F.C. was most intolerant to visual perturbations and was observed to stumble when motion in the scene stopped (see Video, Supplemental Digital Content 1, Pretreatment DLS Performance During Optic Flow, http://links.lww.com/JNPT/A17). This behavior was consistent with reports of a destabilizing effect from optical flow in people with visual vertigo.23 P.F.C. also demonstrated decreased SLS balance in the CAREN, which corroborated SLS measures performed during the occupational therapist evaluation. When combined with his high motion sensitivity quotient, these assessment results were consistent with a diagnostic classification of postconcussive disequilibrium with visual vertigo.10
These impairments restricted P.F.C.'s ability to perform activities of daily living and prevented him from returning to duty. Therefore, physical therapist-directed, VR-based interventions that focused on visual motion stimulation/adaptation, balance, dual-task performance, and military-specific skills were developed to meet the following goals:
1. eliminate visual vertigo,
2. improve walking balance,
3. improve static balance,
4. decrease reaction and processing times, and
5. full return to duty.
Progress toward these goals was monitored throughout treatment and assessed during a comprehensive posttherapy assessment. Measures such as the motion sensitivity quotient administered by other providers were also monitored.
P.F.C. attended six 1-hour treatment sessions over 3 weeks and a reassessment 2 days (postinjury day 63) after his final treatment. Treatment progression was informed by P.F.C.'s tolerance and ability to perform during challenges without large increases in symptoms (see Table, Supplemental Digital Content 2, Rehabilitation Treatment Progression, http://links.lww.com/JNPT/A18). The duration of most treatment bouts was restricted to 10 minutes as this was the maximum duration of the VR environments. P.F.C. documented his symptoms before and after each treatment session using the PCSS.
All sessions began with warm-up postural balance activities in a nondescript wooded scene (“Wooded Country” application) with a centered walking path bordered by vertical posts. P.F.C. maintained stance positions during blocks of pseudorandom anterior-posterior and medial-lateral visual perturbations.20 Deviations from the intended stance position were recorded as errors and P.F.C. was instructed to recover quickly (see Video, Supplemental Digital Content 1, DLS Training With Visual Perturbations, http://links.lww.com/JNPT/A17). He was allowed to rest between bouts until his symptoms subsided and he felt he could continue. As errors were minimized, P.F.C. was challenged with progressively less supportive stance positions (ie, SLS and SLS on foam).
Phase 1 training included activities focused on the habituation24 of visual vertigo symptoms through repetitive optokinetic stimulation25 and gaze stabilization challenges24,26 in a city scene (“New York, NY” application). Optic flow of the scene matched P.F.C.'s treadmill walking speed (1.1 m/s). This scene contained buildings, streets, vehicles, and people that acted as distracters and added destabilizing effects23 in the visual field. Gaze stabilization and visual scanning tasks were made more challenging by increasing the frequency of objects and the head/neck/eye excursions needed to maintain sight of the objects (see Video, Supplemental Digital Content 1, Gait With Visual Scanning, http://links.lww.com/JNPT/A17). As P.F.C. progressed, challenges such as visual scanning, Stroop, and visual perturbations were performed simultaneously (see Video, Supplemental Digital Content 1, Gait With Random Complex Visual Tasks, http://links.lww.com/JNPT/A17). The number of tasks and length of bouts increased with P.F.C.'s tolerance and success on the challenges.
Phase 2 training scenarios contained activities such as weapon handling and targeting to approximate P.F.C.'s military duties. He was placed in a virtual environment resembling an Iraqi city with a replica M4 rifle of realistic size, shape, and weight (D-Boys Airsoft, Wanchai, Hong Kong). Custom electronics were added to the rifle, which allowed registration of trigger pulls and the broadcast of weapon fire sounds. Initial training began with standing while scanning and shooting targets as the environment simulated moving in a convoy at approximately 18 mph (see Video, Supplemental Digital Content 1, Targeting in Stance, http://links.lww.com/JNPT/A17). As P.F.C. progressed, the speed of the optic flow was increased and physical perturbations (ie, platform movement) were added. The final training scenario consisted of P.F.C. identifying and engaging targets while walking (see Video, Supplemental Digital Content 1, Targeting During Gait, http://links.lww.com/JNPT/A17) with the platform moving to simulate unstable terrain.
During initial treatment sessions, P.F.C.'s symptoms were easily provoked, requiring multiple rest breaks. Over the course of treatment, his symptoms steadily improved (Figure 4), allowing longer training bouts without rest. On treatment day 3, the VR-based treatments no longer exacerbated his symptoms. At reassessment (postinjury day 63), he reported a PCSS score of 1 associated with a persistent, occipital headache (1/10 pain, described as “poking”).
The reduction of visual vertigo symptoms was evident during reassessment. Specifically, P.F.C. was able to maintain DLS with sudden starts and stops of optic flow (see Video, Supplemental Digital Content 1, Posttreatment DLS Performance During Optic Flow, http://links.lww.com/JNPT/A17), showed markedly reduced gait deviations during medial-lateral visual perturbations (see Video, Supplemental Digital Content 1, Posttreatment Gait During Visual Perturbations, http://links.lww.com/JNPT/A17) and decreased step width variability (Figure 3). The reduction of visual vertigo symptoms was reflected in improvements on the motion sensitivity test with a quotient of 0 (no motion sensitivity) the day after his last VR-based treatment.
P.F.C. also showed improvement on measures of static and dynamic balance. He increased all SLS times and reached a maximum of 30 seconds on all but the “eyes closed on foam” condition where he improved from 2.8 ± 1.1 to 6.8 ± 0.7 seconds (Figure 2). His normalized composite Y-balance score increased by 25.5% to 114.7 ± 6.0 (normal controls: 93.5 ± 7.0), which was well above our minimum detectable change value of 3.8%. Improvements in dynamic agility were also observed on the 4 square step test where he had a 21.9% reduction in time to 5.6 ± 0.6 seconds (minimum detectable change: 7.8%).
P.F.C. demonstrated gains on all executive function and dual-task tests. His average symbol recognition reaction time during DLS with no optic flow decreased by 231 ms to 360 ± 44 ms, falling within the normal range for nonconcussed individuals. Reductions in symbol recognition reaction time were also seen during DLS with optic flow (151 ms) and gait (77 ms). During DLS with no optic flow, his symbol matching reaction time decreased by 125 ms to 873 ± 174 ms. A reduction in symbol matching reaction times was also measured during DLS with optic flow (133 ms) and gait (126 ms). However, these improvements were not sufficient to bring times within the normal nonconcussed range. His accuracy rate across all Stroop conditions improved from 85 ± 10% to a combined average of 98 ± 4%.
At the conclusion of the re-assessment, P.F.C. was discharged from Physical Therapy services at the Military Performance Laboratory with the recommendation to perform a driving test. He was able to return to duty, but was restricted from driving until after passing an on-road driving test conducted 3 weeks later. On a follow-up phone interview conducted by the treating physical therapist 2 months after discharge, P.F.C. reported returning to full duty. He participated in physical training to include regular calisthenics and 4-mile runs. His only complaint was of continued headaches, which were provoked by “jarring” activities such as jumping jacks and the “bouncing” of his helmet during runs. The headaches were effectively treated with medication (Celebrex [celecoxib]). He returned to playing soccer and even participated in 2 tandem skydiving jumps. He requalified on all required weapon systems and returned to driving military vehicles. P.F.C. was promoted to Specialist (E4) just before attending training exercise in preparation for combat deployment. P.F.C. expressed confidence in his ability to perform his duties once deployed, with the caveat that he has a supply of medication to manage headaches.
Our assessment and intervention used visual, vestibular, proprioceptive, and cognitive challenges during functional tasks (stance and gait). With mTBI populations, visual-vestibular challenges are commonly used to assess postural balance.26,27 These challenges can be delivered through high-end VR systems like the CAREN, automated force-platform systems like the Smart Balance Master (NeuroCom, Inc, Clackamas, Oregon),26,28 or low cost solutions like the foam- and-dome.29 However, a key benefit of the CAREN system compared with other more commonly used systems is the ability to manipulate the physical and visual environment during both stance and gait. During visual-vestibular challenges, P.F.C. exhibited symptoms and functional deficits consistent with visual vertigo, including reduction in postural balance with visual stimuli during static stance (see Video, Supplemental Digital Content 1, Pretreatment DLS Performance During Optic Flow, http://links.lww.com/JNPT/A17). Balance during gait was also negatively influenced by visual perturbations, illustrating his dependence on visual inputs (see Video, Supplemental Digital Content 1, Pretreatment Gait During Visual Perturbations, http://links.lww.com/JNPT/A17). Vertigo may derive from a mismatch in central nervous system integration resulting in sensory conflict, as visual, vestibular, and proprioceptive inputs are used to perceive physical motion.30 Postural control becomes difficult when the central nervous system is not able to reconcile this conflict through the proper inhibition of competing inputs. This causes the perception of self-motion in response to object motion in the environment. Although a diagnosis of visual vertigo matched P.F.C.'s complaints of visual motion intolerance, it did not adequately explain balance deficits with static visual fields. Specifically, P.F.C. demonstrated times below normal for SLS during both eyes open and closed conditions (Figure 2). These impairments were most consistent with postconcussive disequilibrium10 and needed to be treated together with the visual vertigo.
P.F.C.'s functional impairments were addressed with specific challenges combined with conventional vestibular rehabilitation techniques. These techniques included postural stability training, gaze stabilization exercises24,26 at mid and distant ranges, optokinetic stimulation/habituation,24,26 and military-specific training. We feel the CAREN system is a robust rehabilitation environment, that is, ideally suited to deliver these multiple intervention modalities. The warm-up exercises included static balance challenges with progressively reduced bases of support, combined with random visual perturbations. Phase 1 training included walking while visually scanning and locating objects in the environment (people, vehicles, and signs) that were called out by the treating physical therapist. As these objects were located, P.F.C. had to maintain his gaze on the object until it disappeared from the field of view (see Video, Supplemental Digital Content 1, Gait With Visual Scanning, http://links.lww.com/JNPT/A17). This required P.F.C. to turn his head in all directions similar to cervical/vestibular ocular reflex habituation techniques.24,26 In general, head movements, and not any specific vestibular rehabilitation technique, may have contributed significantly to the decrease in P.F.C.'s visual vertigo symptoms.24 Yet, we believe that the VR environment added realism to the treatment intervention that may be difficult to recreate while performing similar vestibular exercises on a treadmill in the clinic. For example, within the CAREN, P.F.C. could track randomly shifting objects while stabilizing his gaze at various distances. Furthermore, the optic flow and visual parallax that is natural as people walk toward objects was easily reproduced in the CAREN.
Finally, our intervention extended beyond conventional therapies to address impairments that limited and restricted the performance of military-specific duties. Targets were presented throughout the environment requiring P.F.C. to pivot his trunk/head to visually scan while looking down rifle sights. Vertical platform oscillations were added to increase realism by simulating a bumpy ride at high speeds. With P.F.C.'s input, we were able to quickly adapt and increase the challenge of tasks by increasing optic flow speed and adding physical perturbations. These challenges matched a large component of mission readiness, which requires an individual to be prepared to perform rapid simultaneous physical and cognitive tasks.
Throughout all procedures, P.F.C. was instructed to accurately report his symptoms verbally and via the formal PCSS documentation. He openly communicated episodes of activity intolerance and his need to rest and recover before continuing. This was important, as we sought to provide slight symptom provocation during treatment challenges to promote adaptation, rather than send P.F.C. in to crisis. As evident by P.F.C.'s PCSS reporting, symptoms no longer worsened during the intervention and began to improve after treatment day 3 (Figure 4). He also reported a corresponding reduction in use of medication for symptom management.
Several factors beyond the specific CAREN intervention may have contributed to the positive outcomes observed in this patient. These include positive expectations, patient motivation, enjoyment of the treatment tasks, and spontaneous natural recovery.2,3 However, all of these factors were available prior to the start of CAREN-based treatment, yet his symptoms worsened with complexities resembling postconcussive disequilibrium with visual vertigo.10 The specific etiology of P.F.C.'s worsening symptoms and resistance to conventional therapy was not known. Persistent postconcussive symptoms may be related to multiple factors including neuropathology, psychopathology, secondary gain in the form of consciously reduced effort or malingering, and any combination thereof.4 He may have been predisposed to a longer recovery secondary to previous head trauma associated with reported multiple head impacts during sports and at least 2 episodes of loss of consciousness following trauma. Neurologic imaging evidence of changes in bilateral frontal cortical white matter was consistent with reports of prior trauma. P.F.C. showed no signs of consciously reducing effort or malingering and all symptoms were consistent with the stated mechanism of injury. Furthermore, P.F.C. communicated specific goals of returning to his unit so that he could deploy, and was enthusiastic about trying Physical Therapy in the CAREN.
Previous authors have described VR interventions emphasizing self-directed activity without the “constraint of having a therapist present.”12 Our experience suggests rehabilitation within a VR environment is most effective when directed by a therapist. Specifically, treatment modalities can be quickly adapted to the patient in a manner specific to their functional limitations and personal and professional roles. The assessment and intervention described herein was based on common clinical techniques and targeted specific impairments to produce positive functional change. The successful integration of these multiple treatment techniques within the CAREN speaks to their collective importance in managing the complex symptomatology of individuals with mTBI and not just the delivery tool. Virtual-reality-based interventions to promote movement and increase function can be delivered via sophisticated computerized systems to family friendly games on inexpensive gaming consoles12 in the clinic. Thus, interventions based on techniques outlined in this case are currently accessible to clinicians and patients. Our VR-based assessment and intervention provides a partial groundwork for future clinical care of patient populations using VR applications.
We thank our CAREN application designer, Michael Vernon, for his technical expertise in the development of treatment applications; Mustafa Shinta for data collection assistance; Dr Tedesco-Evans and Mrs Marina LeBlanc for the patient referral; and all the providers at Brooke Army Medical Center's traumatic brain injury service for their support.
1. Sosin DM, Sniezek JE, Thurman DJ. Incidence of mild and moderate brain injury in the United States, 1991. Brain Inj. 1996;10(1):47–54.
2. Alexander MP. Mild traumatic brain injury: pathophysiology, natural history, and clinical management. Neurology. 1995;45(7):1253–1260.
3. Binder LM, Rohling ML, Larrabee GJ. A review of mild head trauma. Part I: meta-analytic review of neuropsychological studies. J Clin Exp Neuropsychol. 1997;19(3):421–431.
4. Ruff R. Two decades of advances in understanding of mild traumatic brain injury. J. Head Trauma Rehabil. 2005;20(1):5–18.
5. Ruff RM, Camenzuli L, Mueller J. Miserable minority: emotional risk factors that influence the outcome of a mild traumatic brain injury. Brain Inj. 1996;10(8):551–565.
6. Catena RD, Van Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2007;176:23–31.
7. Parker TM, Osternig LR, Van Donkelaar P, Chou L-S. Gait stability following concussion. Med Sci Sports Exerc. 2006;38(6):1032–1040.
8. Lovell M. The neurophysiology and assessment of sports-related head injuries. Phys Med Rehabil Clin N Am. 2009;20(1):39–53, vii-viii.
9. Williams G, Robertson V, Greenwood K. Measuring high-level mobility after traumatic brain injury. Am J Phys Med Rehabil. 2004;83(12):910–920.
10. Gottshall KR, Hoffer ME. Tracking recovery of vestibular function in individuals with blast-induced head trauma using vestibular-visual-cognitive interaction tests. J Neurol Phys Ther. 2010;34(2):94–97.
11. McComas J, Sveistrup H. Virtual reality applications for prevention, disability awareness, and physical therapy rehabilitation in neurology: our recent work. J Neurol Phys Ther. 2002;26(2):55–61.
12. Flynn S, Palma P, Bender A. Feasibility of using the Sony PlayStation 2 gaming platform for an individual poststroke: a case report. J Neurol Phys Ther. 2007;31(4):180–189.
13. van der Eerden WJ, Otten E, May G, Even-Zohar O. CAREN–computer assisted rehabilitation environment. Stud Health Technol Inform. 1999;62:373–378.
14. Holden MK. Virtual environments for motor rehabilitation: review. Cyberpsychol Behav. 2005;8(3):187–211. Discussion 212–219.
15. Cox DJ, Davis M, Singh H, et al. Driving rehabilitation for military personnel recovering from traumatic brain injury using virtual reality driving simulation: a feasibility study. Mil Med. 2010;175(6):411–416.
16. Bisson E, Contant B, Sveistrup H, Lajoie Y. Functional balance and dual-task reaction times in older adults are improved by virtual reality and biofeedback training. Cyberpsychol Behav. 2007;10(1):16–23.
17. Jang SH, You SH, Hallett M, et al. Cortical reorganization and associated functional motor recovery after virtual reality in patients with chronic stroke: an experimenter-blind preliminary study. Arch Phys Med Rehabil. 2005;86(11):2218–2223.
18. Akin FW, Davenport MJ. Validity and reliability of the Motion Sensitivity Test. J Rehabil Res Dev. 2003;40(5):415–421.
19. Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18(6):643–662.
20. McAndrew PM, Dingwell JB, Wilken JM. Walking variability during continuous pseudo-random oscillations of the support surface and visual field. J Biomech. 2010;43(8):1470–1475.
21. Whitney SL, Marchetti GF, Morris LO, Sparto PJ. The reliability and validity of the Four Square Step Test for people with balance deficits secondary to a vestibular disorder. Arch Phys Med Rehabil. 2007;88(1):99–104.
22. Plisky PJ, Rauh MJ, Kaminski TW, Underwood FB. Star Excursion Balance Test as a predictor of lower extremity injury in high school basketball players. J Orthop Sports Phys Ther. 2006;36(12):911–919.
23. Chang CP, Hain TC. A theory for treating dizziness due to optical flow (visual vertigo). CyberPsychol Behav. 2008;11(4):495–498.
24. Clendaniel RA. The effects of habituation and gaze stability exercises in the treatment of unilateral vestibular hypofunction: a preliminary results. J Neurol Phys Ther. 2010;34(2):111–116.
25. Guerraz M, Yardley L, Bertholon P, et al. Visual vertigo: symptom assessment, spatial orientation and postural control. Brain. 2001;124(Pt 8):1646–1656.
26. Alsalaheen BA, Mucha A, Morris LO, et al. Vestibular rehabilitation for dizziness and balance disorders after concussion. J Neurol Phys Ther. 2010;34(2):87–93.
27. Kaufman KR, Brey RH, Chou LS, Rabatin A, Brown AW, Basford JR. Comparison of subjective and objective measurements of balance disorders following traumatic brain injury. Med Eng Phys. 2006;28(3):234–239.
28. Riemann BL, Guskiewicz KM. Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train. 2000;35(1):19–25.
29. Guskiewicz KM, Perrin DH, Gansneder BM. Effect of mild head injury on postural stability in athletes. J Athl Train. 1996;31(4):300–306.
30. Keshner EA, Kenyon RV. Postural and spatial orientation driven by virtual reality. Stud Health Technol Inform. 2009;145:209–228.
mild traumatic brain injury; postconcussive syndrome military; rehabilitation; virtual reality; visual vertigo
Supplemental Digital Content
© 2011 Neurology Section, APTA