There was no significant difference between the age of patients in the blast and nonblast groups, 28.54 ± 7.73 and 31.08 ± 8.76 years (p = 0.06), respectively. Similarly, both groups had completed, on average, a little more than 5 months (p = 0.14) of their deployment tour when the trauma occurred. However, the mean number of deployments was significantly greater for the blast group, with 1.99 and 1.71 deployments, respectively (p = 0.02). The nonblast group had a greater mean number of days between injury and postinjury eye examination (44.58 days) than the blast group (40.88 days) (p = 0.002). All patients had visual acuity correctable to 20/20 at distance and at near with mean spherical equivalent manifest refraction of −0.48 ± 1.86D and −0.63 ± 2.37D for the right eye and the left eye, respectively.
Visual Symptoms and Dysfunctions
Chi-square analyses compared the visual symptoms and diagnoses of patients with mTBI resulting from blast and nonblast mechanisms during different stages after the injury. The results are summarized in Table 3. The prevalence of visual symptoms did not differ significantly between injury mechanism and postinjury stage, except for eye pain and diplopia. Eye pain was higher during the acute/subacute stage after a blast event (χ2 = 6.41; p = 0.04), and diplopia tended to be higher during the chronic ≤ 1-year period after a nonblast injury (χ2 = 7.17; p = 0.03). Overall, the data showed a very high frequency of visual symptoms and visual dysfunctions. The majority of the visual symptoms and deficits were related to oculomotor problems. The most common visual symptoms were subjective visual complaints (79%), blurred vision at near (66%), reading problems (62%), eye strain (53%), and light sensitivity (40%). The most common visual dysfunctions were posttrauma vision syndrome (37%), accommodative deficit (32%), vergence deficit (26%), vertical deviation (24%), version deficit (24%), visual field defect (22%), and diplopia (20%). Accommodative insufficiency, convergence insufficiency, and defective pursuit eye movements accounted for the majority of the accommodative (83%), vergence (88%), and version (57%) problems, respectively. In addition, we found a very high prevalence of headaches (87%) and dizziness (83%), which can result from visual and oculomotor deficits. Dizziness was more common in individuals who have experienced a blast-induced mTBI event (blast, 87.2% vs. nonblast, 75.9%; χ2 = 6.27; p = 0.04). Similarly, headaches were more common in individuals who have experienced a blast-induced mTBI event (blast, 91.5% vs. nonblast, 78.3%); however, this difference was not statistically significant.
Table 4 summarizes the mean (SD) of the oculomotor functions measured in the study. There were no statistically significant differences (ANOVA) for the measured oculomotor functions in terms of mechanism of injury and stage after injury. However, the data showed that, on average, relative to expected normative values,18 there was higher near vertical phoria (0.50 ± 1.33 PD), reduced near negative fusional vergence break (15.66 ± 7.82 PD), receded near point of convergence (8.35 cm), decreased stereoacuity (52 sec arc), and reduced positive relative accommodation (−1.80 ± 0.87D).
Table 5 summarizes the prevalence of ocular diagnoses during the initial eye examination after the mTBI event. The occurrence of ocular diagnoses in the mTBI sample was very low when compared with visual dysfunctions, regardless of the mechanism of injury. However, the blast group showed higher frequencies for dry eye (p = 0.003), retinopathies (p = 0.014), and optic neuropathies (p = 0.018) than the nonblast group. A total of 23 subjects had documented preexisting ocular diagnoses (i.e., anisocoria, ptosis, retinal breaks/detachments, visual field defect, and dry eyes), therefore were not included in the above analysis. However, these patients were included in the study because the ocular conditions do not affect the results of other visual functions.
The current study analyzed visual dysfunctions and symptoms of war fighters who experienced an mTBI event while conducting military operations in Iraq and Afghanistan. These visual deficits were documented during a comprehensive neuro-optometric examination at LRMC. The main objective of the study was to compare, at different stages after the injury, visual deficits and symptoms resulting from blast or nonblast mTBI events. Consistent with previous reports, we found a high frequency of visual dysfunctions and associated visual symptoms.6,7,9–11,26 However, there were no significant differences in visual symptoms between any of the postinjury stages or injury mechanisms (blast vs. nonblast), except for diplopia and eye pain. Similarly, headaches and dizziness were more common in patients who experienced mTBI from a blast event. However, only dizziness was significantly higher in the blast-related group (p = 0.04). This is the first report describing visual sequelae exclusively in war fighters with mTBI and taking into account different injury mechanisms. Because no difference was found in terms of visual sequelae between the subgroups (blast vs. nonblast), this finding suggests that research addressing the assessment and management of mTBI visual sequelae resulting from civilian nonblast events may be relevant to military personnel in combat who sustain blast-induced mTBI.
The mean receded near point of convergence (8.35 cm) and decreased stereoacuity (52 sec arc) found here are consistent with the overall high frequency of convergence insufficiency. Similarly, the reduced positive relative accommodation (−1.80 ± 0.87D) is consistent with the high prevalence of accommodative insufficiency found in this population. There are only three studies quantifying oculomotor functions in patients with mTBI. Although two of these studies used the same mTBI criteria applied in the present study (i.e., loss of consciousness ≤30 min, posttraumatic amnesia ≤24 h, any alteration of mental state, Glasgow Coma Scale score from 13 to 15), the studies were conducted in relatively small samples of civilian nonblast (N = 32)27 and military blast (N = 40)7 mTBI patients. Consistent with the present study, the mean values for near point of convergence, stereoacuity, near exophoria, and vertical deviations were elevated, whereas the positive fusional vergence break was reduced in both of the previous studies. There were small discrepancies in the values compared with those two studies, which could be explained by the difference in sample size. However, the two prospective studies and the current study show a high frequency of light sensitivity and saccadic dysfunction. The third retrospective study conducted within the Department of Veterans Affairs (VA) used the same criteria for mTBI diagnosis but in a larger population.28 This study, of 50 blast and 50 nonblast patient records, also found a high frequency of visual symptoms as well as saccadic, accommodative, and convergence dysfunction. In addition, the present study is in agreement with the results of a recent study describing chronic (>12 months) visual dysfunctions in veterans after blast-induced mTBI.29 Magone et al.29 found that the most common visual complaints were photophobia (55%) and reading difficulties (32%), which correlate with the 58% and 36%, respectively, found in the Chronic > 1 year subgroup of the current study.
We also found a large frequency of vertical deviation, corroborating an observation previously reported in samples of nonblast and blast mTBI patients.7,27 An individual with a vertical deviation may tilt the head to help mechanically align the eyes, which, in turn, may disrupt the fluid of the inner ear, resulting in dizziness and balance disorders.30,31 Furthermore, vertical deviation in TBI patients can be associated with lightheadedness, diplopia, poor depth perception, eye pain, headaches, reading difficulties, and blurred vision at near.30,31 Consequently, the correction of vertical deviation with prisms before initiating any other rehabilitation modality can positively impact the mTBI patient’s overall rehabilitation outcome and quality of life.
The period of natural recovery after mTBI is reported to be as long as 1 to 2 years after injury; however, symptoms may persist after therapy.32 The fact that nearly one-third of all the patients in the present study sought care for postconcussion syndrome with visual sequelae more than a year after the injury emphasizes the importance of persistent visual sequelae and the continuous need for specialized vision rehabilitation care in the military and, subsequently, in VA medical treatment facilities.
The overall lack of significant differences between blast and nonblast mTBI groups in visual symptoms and dysfunctions is consistent with other studies that document that psychological and cognitive deficits in veterans with mTBI are not significantly different based on the injury mechanism.33,34 Luethcke et al.34 also found that, during the acute postinjury stage, there were no differences between injury mechanism (blast vs. nonblast) in the concussive and psychological symptoms, including vision, balance, memory, concentration, sleep, hearing, and irritability. Similarly, another study by Belanger et al.4 showed that cognitive sequelae of mTBI were not different based on the injury mechanism with an average of 2 years after injury. In addition, they found a marginally increased incidence of reported PTSD symptoms among blast-injured participants. This is in agreement with the finding of higher frequency of PTSD in the blast population documented in the present study. Behavioral data from this study will be reviewed in a separate manuscript currently in preparation.
The frequency of ocular diagnosis in this mTBI population was relatively small; however, dry eye was the most common diagnosis among these war fighters, with a higher frequency in the blast group (p = 0.003). The diagnosis of dry eye was recently reported by Cockerham et al.35 in 32% of veterans with mTBI evaluated between 1 and 60 months after injury. Although in a lower frequency (7 vs. 32%), the present study is in agreement with findings of Cockerham et al.35 that there is a threefold increase in the frequency of dry eye in individuals who sustained an mTBI from a blast injury when compared with a nonblast event. They also found that age and time after injury were not predictors of dry eye.
Recently, Goodrich et al.36 completed a Delphi study with the intent of developing clinical guidelines and improving the consistency of visual examinations of veterans with mTBI. The Delphi study recommended a set of clinical guidelines composed of 17 history questions and an 11-item examination to diagnose mTBI. The procedures and associated methodology recommended in the Delphi study were the same used in the present study to assess oculomotor functions (i.e., accommodation, vergence, and version eye movements). Ten of the 11 recommended examination testing on the Delphi study overlap with the present study, including the distance and near cover test, pursuit and saccades testing, accommodation, near point of convergence, phorias, fixation, stereopsis, and light sensitivity/photophobia. In addition, 11 of the 17 Delphi-recommended history questions were included in the present study and proven significant to guide the assessment and to determine the accurate diagnosis (i.e., date of injury, loss of consciousness, alteration of mental state, eye pain, change in vision, light sensitivity, double vision, blur vision at distance or near, reading issues, headaches after near tasks). The results from the present study suggests that the Delphi study recommendations of clinical guidelines could be adopted by both the VA and the Department of Defense to ensure a continuum of care as war fighters transition their eye care between these federal treatment facilities.
The primary limitation of the current study is its retrospective nature. The data were not collected with the intention of further analysis; therefore, there is likely variation in the testing procedures and the history taken during the patient encounter. Second, the lack of a control cohort and the fact that not all subjects had a baseline eye examination with oculomotor assessment prevent the accurate estimation of visual deficits resulting from a deployment injury; therefore, the number of subjects who had preexisting oculomotor dysfunctions might lead to an overestimation of visual sequelae associated to the injury. Third, this study did not assess the cumulative effect of past mTBI/concussion since some of the patient histories indicated prior mild head injury.
Future research should investigate preinjury and postinjury oculomotor functions through predeployment baselines for a large number of war fighters. This should include a cohort of war fighters that deployed but did not sustain a head injury to assess if factors associated to the deployment contribute to visual deficits (e.g., stress, PTSD, environmental).
Consistent with previous reports, this study documents the high frequency of visual dysfunctions and associated visual symptoms in war fighters with mTBI. However, overall, there were no significant differences in visual sequelae and symptoms between stages after injury and the injury mechanism (i.e., blast vs. nonblast). The results of the current study, coupled with previous studies suggesting that there is no difference in symptoms based on time after injury or mechanism of combat injury (blast vs. nonblast), suggest that research addressing the assessment and management of mTBI visual sequelae resulting from civilian nonblast event may be relevant to military personnel in combat resulting primarily from a blast event.
The fact that nearly one-third of all patients in the present study had significant visual sequelae and complaints more than a year after the injury emphasizes the concern of persistent visual sequelae and the continuous need for specialized vision rehabilitation care by military and VA eye care providers. The findings of the present study correlate with the clinical guidelines (17 history questions and 11-item examination procedures) recommended in the Delphi study and highlight the need for these clinical guidelines to be adopted by both the VA and the Department of Defense to improve the consistency of visual examinations of military personnel with mTBI and ensure a continuum of care as war fighters transition their eye care between these treatment facilities.
Sponsored in part by the appointment to the Postgraduate Research Participation Program at the U.S. Army Aeromedical Research Laboratory administered by the Oak Ridge Institute of Science and Education through an interagency agreement, the U.S. Department of Energy and the U.S. Army Medical Research and Materiel Command.
The views, opinions, and/or findings contained in this report are those of the author(s) and should not be construed as an official Department of the Army position, policy, or decision, unless so designated by other official documentation.
Received May 9, 2015; accepted October 16, 2015.
3. Hoge CW, McGurk D, Thomas JL, et al. Mild traumatic brain injury
in U.S. soldiers returning from Iraq. N Engl J Med 2008;358:453–63.
4. Belanger HG, Kretzmer T, Yoash-Gantz R, et al. Cognitive sequelae of blast
-related versus other mechanisms of brain trauma. J Int Neuropsychol Soc 2009;15:1–8.
5. Sutter P. Rehabilitation and management of visual dysfunction
following traumatic brain injury. In: Ashley MJ, Krych DK, eds. Traumatic Brain Injury Rehabilitation. New York, NY: CRC Press; 1995;187–219.
6. Capó-Aponte JE, Tarbett AK, Urosevich TG, et al. Effectiveness of computerized oculomotor vision screening in a military
population: pilot study. J Rehabil Res Dev 2012;49:1377–98.
7. Capó-Aponte JE, Urosevich TG, Temme LA, et al. Visual dysfunctions and symptoms during the subacute stage of blast
-induced mild traumatic brain injury
. Mil Med 2012;177:804–13.
8. Okie S. Traumatic brain injury in the war zone. N Engl J Med 2005;352:2043–7.
9. Brahm KD, Wilgenburg HM, Kirby J, et al. Visual impairment and dysfunction in combat-injured servicemembers with traumatic brain injury. Optom Vis Sci 2009;86:817–25.
10. Goodrich GL, Kirby J, Cockerham G, et al. Visual function in patients of a polytrauma rehabilitation center: a descriptive study. J Rehabil Res Dev 2007;44:929–36.
11. Stelmack JA, Frith T, Van Koevering D, et al. Visual function in patients followed at a Veterans Affairs polytrauma network site: an electronic medical record review. Optometry 2009;80:419–24.
12. Ciuffreda KJ, Han Y, Kapoor N, et al. Oculomotor consequences of acquired brain injury. In: Suchoff IB, Ciuffreda KJ, Kapoor N, eds. Visual and Vestibular Consequences of Acquired Brain Injury. Santa Ana, CA: OEP Foundation Press; 2001;77–88.
13. Ciuffreda KJ, Kapoor N. Oculomotor dysfunctions, their remediation, and reading-related problems in mild traumatic brain injury
. J Behav Optom 2007;18:72–7.
14. Ciuffreda KJ, Kapoor N, Rutner D, et al. Occurrence of oculomotor dysfunctions in acquired brain injury: a retrospective analysis. Optometry 2007;78:155–61.
15. Ciuffreda KJ, Ludlam D, Thiagarajan P. Oculomotor diagnostic protocol for the mTBI
population. Optometry 2011;82:61–3.
16. Halbauer JD, Ashford JW, Zeitzer JM, et al. Neuropsychiatric diagnosis and management of chronic sequelae of war-related mild to moderate traumatic brain injury. J Rehabil Res Dev 2009;46:757–96.
17. Stapert S, Houx P, de Kruijk J, et al. Neurocognitive fitness in the sub-acute stage after mild TBI: the effect of age. Brain Inj 2006;20:161–5.
18. Carlson N, Kurtz D. Clinical Procedures for Ocular Examination, 3rd ed. New York, NY: McGraw-Hill; 2004.
19. Goss DA. Fixation disparity. In: Eskridge JB, Amos JF, Barlett JD, eds. Clinical Procedures in Optometry. Philadelphia, PA: Lippincott William & Wilkins; 1991;716–26.
20. Maples WC, Ficklin TW. Interrater and test-retest reliability of pursuits and saccades. J Am Optom Assoc 1988;59:549–52.
21. Messé A, Caplain S, Paradot G, et al. Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury
with persistent neurobehavioral impairment. Hum Brain Mapp 2011;32:999–1011.
22. Miles L, Grossman RI, Johnson G, et al. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury
. Brain Inj 2008;22:115–22.
23. Lipton ML, Gulko E, Zimmerman ME, et al. Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury
. Radiology 2009;252:816–24.
24. Greenberg G, Mikulis DJ, Ng K, et al. Use of diffusion tensor imaging to examine subacute white matter injury progression in moderate to severe traumatic brain injury. Arch Phys Med Rehabil 2008;89:S45–50.
25. Ng K, Mikulis DJ, Glazer J, et al. Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Arch Phys Med Rehabil 2008;89:S35–44.
26. Dougherty AL, MacGregor AJ, Han PP, et al. Visual dysfunction
-related traumatic brain injury from the battlefield. Brain Inj 2011;25:8–13.
27. Hellerstein LF, Freed S, Maples WC. Vision profile of patients with mild brain injury. J Am Optom Assoc 1995;66:634–9.
28. Goodrich GL, Flyg HM, Kirby JE, et al. Mechanisms of TBI and visual consequences in military
and veteran populations. Optom Vis Sci 2013;90:105–12.
29. Magone MT, Kwon E, Shin SY. Chronic visual dysfunction
-induced mild traumatic brain injury
. J Rehabil Res Dev 2014;51:71–80.
30. Doble JE, Feinberg DL, Rosner MS, et al. Identification of binocular vision dysfunction (vertical heterophoria) in traumatic brain injury patients and effects of individualized prismatic spectacle lenses in the treatment of postconcussive symptoms: a retrospective analysis. PM R 2010;2:244–53.
31. Matheron E, Lê TT, Yang Q, et al. Effects of a two-diopter vertical prism on posture. Neurosci Lett 2007;423:236–40.
32. Rutherford WH, Merrett JD, McDonald JR. Symptoms at one year following concussion from minor head injuries. Injury 1979;10:225–30.
33. Lippa SM, Pastorek NJ, Benge JF, et al. Postconcussive symptoms after blast
and nonblast-related mild traumatic brain injuries in Afghanistan and Iraq war veterans. J Int Neuropsychol Soc 2010;16:856–66.
34. Luethcke CA, Bryan CJ, Morrow CE, et al. Comparison of concussive symptoms, cognitive performance, and psychological symptoms between acute blast
-versus nonblast-induced mild traumatic brain injury
. J Int Neuropsychol Soc 2011;17:36–45.
35. Cockerham GC, Lemke S, Glynn-Milley C, et al. Visual performance and the ocular surface in traumatic brain injury. Ocul Surf 2013;11:25–34.
36. Goodrich GL, Martinsen GL, Flyg HM, et al. U.S. Department of Veterans Affairs. Development of a mild traumatic brain injury
-specific vision screening protocol: a Delphi study. J Rehabil Res Dev 2013;50:757–68.
Keywords:© 2017 American Academy of Optometry
visual dysfunction; mild traumatic brain injury; mTBI; military; blast