Traumatic brain injury (TBI) is a major cause of mortality and disability, and is classified as mild, moderate, or severe (1, 2). Mild TBI accounts for 70%–90% of all TBI and approximately 15% of patients have disabling symptoms at 1 year after injury (3–5). Conventional computed tomography and magnetic resonance imaging (MRI) are known to have limitations in the evaluation of neural injury in patients with mild TBI (6–9). In contrast, diffusion tensor imaging (DTI) is able to detect injury of neural tracts in patients with mild TBI (10–15). This includes damage to the corticospinal tract, medial lemniscus, fornix, cerebellar peduncle, cingulum and corpus callosum (10–15). However, little is known about injury of the optic radiation (OR) (13).
The prevalence of visual dysfunction in patients with TBI has been reported in approximately 50% of cases (16–19). This includes injury to the OR, and homonymous visual field defects have been reported in approximately 30% of patients with TBI (20, 21). DTI provides 3-dimensional reconstruction for evaluation of the OR (22, 23). This neuroimaging technique has been applied to OR injury in various brain pathologies (24–26), but there are only a few reports in patients with TBI (13, 27, 28).
In this study, we report on patients with mild TBI who showed OR injury as demonstrated by DTI.
Two patients who complained of a visual field defect after TBI and 9 age-matched normal control subjects (5 males and 4 females; mean age: 49.22 years, range: 44–56) with no history of neurologic disease were recruited for this study. All subjects provided signed informed consent, and our institutional review board approved the study protocol.
Patient 1 was a 52-year-old woman who had suffered head trauma resulting from a pedestrian car accident. The patient experienced loss of consciousness for 30 minutes and posttraumatic amnesia for 4 hours at the time of head trauma; The Glasgow Coma Scale (29) score was 15 when the patient arrived at the hospital. Patient 2 was a 56-year-old woman who had suffered head trauma resulting from a car accident. The patient did lose consciousness nor develop posttraumatic amnesia; the Glasgow Coma Scale score was 15 when the patient arrived at the hospital. No specific abnormality was observed on brain MRI (T1, T2, and fluid-attenuated inversion recovery images) performed at 2.5 years (patient 1) with 1 year (patient 2) after onset (Fig. 1A). Peripheral field defects were detected with automated (Humphrey) visual field testing in both patients (Fig. 1B).
Diffusion Tensor Imaging
A 6-channel head coil on a 1.5 T Philips Gyroscan Intera (Philips, Ltd, Best, the Netherlands) with single-shot echo-planar imaging was used for acquisition of DTI data. For each of the 32 noncollinear diffusion sensitizing gradients, we acquired 70 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 × 96, reconstructed to matrix = 192 × 192 matrix, field of view = 240 × 240 mm2, TR = 10,398 milliseconds, TE = 72 milliseconds, parallel imaging reduction factor (SENSE factor) = 2, EPI factor = 59 and b = 1,000 s/mm2, NEX = 1, slice gap = 0, and a slice thickness of 2.5 mm. Fiber tracking was performed using the fiber assignment continuous tracking algorithm implemented within the DTI task card software (Philips Extended MR WorkSpace 2.6.3). Each of the DTI replications was intraregistered to the baseline “b0” images to correct for residual eddy-current image distortions and head motion effect, using a diffusion registration package (Philips Medical Systems, Best, Netherlands). For reconstruction of the OR, we set the seed ROI on the lateral geniculate nucleus on the color map, and the target ROI was placed on the bundle of OR at the posterior one-third portion between the lateral geniculate nucleus and the occipital pole (24, 27). Fiber tracking was performed using a fractional anisotropy (FA) threshold of >0.15 and a direction threshold of <27°. We measured the FA value, apparent diffusion coefficient (ADC) value, and voxel number of each OR. DTI parameter values showing more than 2 standard deviations (SDs) of that of normal control values were defined as abnormal.
Regarding the configuration of OR, the total volume of OR was decreased in the right OR of both patients compared with those of normal controls; in contrast, the left ORs were divided into 2 parts in both patients (Figs. 1C, D). A summary of the FA, ADC values, and voxel number of the OR of patients and controls is shown in Table 1. The voxel numbers of both ORs in both patients were more than 2 SDs lower than that of normal control subjects. The ADC value of the right OR in patient 2 was more than 2 SDs higher than that of normal control subjects.
We investigated the configuration and DTI parameters of the OR in patients who showed visual field defects after mild TBI. According to our findings, the configuration of both ORs in both patients was abnormal compared with those of normal controls. In addition, the voxel numbers of both ORs in both patients were decreased and the ADC value of the left OR in patient 2 was increased without change of FA value in both patients. FA value represents the degree of directionality of microstructures (axon, myelin, and microtubule), and ADC value indicates the magnitude of water diffusion (30). In contrast, the voxel number is determined by the number of neural fibers contained within a neural tract (31). Therefore, the decrement of tract volume of both ORs in both patients suggested decreased neural fibers of the OR. In addition, the increased ADC value of the left OR in patient 2 indicated mild injury of a neural tract or local cell death as did the finding of the left ORs dividing into 2 parts in both patients.
A number of reports using DTI have documented OR damage in patients with TBI (13, 27, 28). Kwon and Jang (27) described a patient with OR injury on DTI after epidural hematoma in the left temporoparietal lobe. The patient complained of right homonymous hemianopia, which was confirmed by automated visual field testing. Although no abnormality was found on conventional MRI, DTI demonstrated decreased fiber density along the midpoint of the left OR. FA values around the injury site were decreased and ADC values were increased compared with controls, consistent with neuronal injury. After head trauma, Yeo et al (28) reported a patient with right homonymous hemianopia and discontinuation of the left OR on DTI due to hemorrhage in the left occipital lobe after head trauma. Huang et al (13) studied a group of military and civilian patients who sustained mild TBI. Abnormalities were detected in the ORs of some of these patients but clinical findings, including visual field results, were not reported.
In conclusion, we documented injury of the ORs using DTI in 2 patients who showed visual field abnormalities after mild TBI. Our results suggest that DTI may be a useful technique in patients with mild TBI complaining of visual field loss. Further studies involving a large number of patients are needed to verify and confirm our findings.
STATEMENT OF AUTHORSHIP
Category 1: a. Conception and design: S. H. Jang; b. Acquisition of data: J. P. Seo; c. Analysis and interpretation of data: J. P. Seo. Category 2: a. Drafting the manuscript: S. H. Jang and J. P. Seo; b. Revising it for intellectual content: S. H. Jang. Category 3: a. Final approval of the completed manuscript: S. H. Jang and J. P. Seo.
This work was supported by the DGIST R&D Program of the Ministry of Science, ICT and Future Planning (15-BD-0401).
1. Elisevich KV, Ford RM, Anderson DP, Stratford JG, Richardson PM. Visual abnormalities with multiple trauma. Surg Neurol. 1984;22:565–575.
2. De Kruijk JR, Twijnstra A, Leffers P. Diagnostic criteria and differential diagnosis of mild traumatic brain injury. Brain Inj. 2001;15:99–106.
3. Rutherford WH, Merrett JD, McDonald JR. Symptoms at one year following concussion from minor head injuries. Injury. 1979;10:225–230.
4. McLean A Jr, Temkin NR, Dikmen S, Wyler AR. The behavioral sequelae of head injury. J Clin Neuropsychol. 1983;5:361–376.
5. Ruff RM. Mild traumatic brain injury and neural recovery: rethinking the debate. NeuroRehabilitation. 2011;28:167–180.
6. Hofman PA, Stapert SZ, van Kroonenburgh MJ, Jolles J, de Kruijk J, Wilmink JT. MR imaging, single-photon emission CT, and neurocognitive performance after mild traumatic brain injury. AJNR Am J Neuroradiol. 2001;22:441–449.
7. Borg J, Holm L, Cassidy JD, Peloso PM, Carroll LJ, von Holst H, Ericson K. Diagnostic procedures in mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J Rehabil Med. 2004;43 suppl:61–75.
8. Hughes DG, Jackson A, Mason DL, Berry E, Hollis S, Yates DW. Abnormalities on magnetic resonance imaging seen acutely following mild traumatic brain injury: correlation with neuropsychological tests and delayed recovery. Neuroradiology. 2004;46:550–558.
9. Shenton ME, Hamoda HM, Schneiderman JS, Bouix S, Pasternak O, Rathi Y, Vu MA, Purohit MP, Helmer K, Koerte I, Lin AP, Westin CF, Kikinis R, Kubicki M, Stern RA, Zafonte R. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 2012;6:137–192.
10. Bazarian JJ, Zhong J, Blyth B, Zhu T, Kavcic V, Peterson D. Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J Neurotrauma. 2007;24:1447–1459.
11. Lipton ML, Gellella E, Lo C, Gold T, Ardekani BA, Shifteh K, Bello JA, Branch CA. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. J Neurotrauma. 2008;25:1335–1342.
12. Rutgers DR, Toulgoat F, Cazejust J, Fillard P, Lasjaunias P, Ducreux D. White matter abnormalities in mild traumatic brain injury: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2008;29:514–519.
13. Huang MX, Theilmann RJ, Robb A, Angeles A, Nichols S, Drake A, D'Andrea J, Levy M, Holland M, Song T, Ge S, Hwang E, Yoo K, Cui L, Baker DG, Trauner D, Coimbra R, Lee RR. Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J Neurotrauma. 2009;26:1213–1226.
14. Kasahara K, Hashimoto K, Abo M, Senoo A. Voxel- and atlas-based analysis of diffusion tensor imaging may reveal focal axonal injuries in mild traumatic brain injury—comparison with diffuse axonal injury. J Magn Reson Imaging. 2012;30:496–505.
15. Yeo SS, Jang SH. Neural reorganization following bilateral injury of the fornix crus in a patient with traumatic brain injury. J Rehabil Med. 2013;45:595–598.
16. Schlageter K, Gray B, Hall K, Shaw R, Sammet R. Incidence and treatment of visual dysfunction in traumatic brain injury. Brain Inj. 1993;7:439–448.
17. Van Stavern GP, Biousse V, Lynn MJ, Simon DJ, Newman NJ. Neuro-ophthalmic manifestations of head trauma. J Neuroophthalmol. 2001;21:112–117.
18. Kelts EA. Traumatic brain injury and visual dysfunction: a limited overview. NeuroRehabilitation. 2010;27:223–229.
19. Ripley DL, Politzer T. Vision disturbance after TBI. NeuroRehabilitation. 2010;27:215–216.
20. Suchoff IB, Kapoor N, Ciuffreda KJ, Rutner D, Han E, Craig S. The frequency of occurrence, types, and characteristics of visual field defects in acquired brain injury: a retrospective analysis. Optometry. 2008;79:259–265.
21. Brahm KD, Wilgenburg HM, Kirby J, Ingalla S, Chang CY, Goodrich GL. Visual impairment and dysfunction in combat-injured servicemembers with traumatic brain injury. Optom Vis Sci. 2009;86:817–825.
22. Staempfli P, Rienmueller A, Reischauer C, Valavanis A, Boesiger P, Kollias S. Reconstruction of the human visual system based on DTI fiber tracking. J Magn Reson Imaging. 2007;26:886–893.
23. Glass HC, Berman JI, Norcia AM, Rogers EE, Henry RG, Hou C, Barkovich AJ, Good WV. Quantitative fiber tracking of the optic radiation is correlated with visual-evoked potential amplitude in preterm infants. AJNR Am J Neuroradiol. 2010;31:1424–1429.
24. Taoka T, Sakamoto M, Nakagawa H, Nakase H, Iwasaki S, Takayama K, Taoka K, Hoshida T, Sakaki T, Kichikawa K. Diffusion tensor tractography of the Meyer loop in cases of temporal lobe resection for temporal lobe epilepsy: correlation between postsurgical visual field defect and anterior limit of Meyer loop on tractography. AJNR Am J Neuroradiol. 2008;29:1329–1334.
25. Yogarajah M, Focke NK, Bonelli S, Cercignani M, Acheson J, Parker GJ, Alexander DC, McEvoy AW, Symms MR, Koepp MJ, Duncan JS. Defining Meyer's loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain. 2009;132:1656–1668.
26. Seo JP, Choi BY, Chang CH, Jung YJ, Byun WM, Kim SH, Kwon YH, Jang SH. Diffusion tensor imaging findings of optic radiation in patients with putaminal hemorrhage. Eur Neurol. 2013;69:236–241.
27. Kwon HG, Jang SH. Optic radiation injury following traumatic epidural hematoma: diffusion tensor imaging study. NeuroRehabilitation. 2011;28:383–387.
28. Yeo SS, Kim SH, Kim OL, Kim MS, Jang SH. Optic radiation injury in a patient with traumatic brain injury. Brain Inj. 2012;26:891–895.
29. Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974;2:81–84.
30. Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci. 2008;34:51–61.
31. Jang SH, Chang CH, Lee J, Kim CS, Seo JP, Yeo SS. Functional role of the corticoreticular pathway in chronic stroke patients. Stroke. 2013;44:1099–1104.