DOI QR코드

DOI QR Code

Myelin Content in Mild Traumatic Brain Injury Patients with Post-Concussion Syndrome: Quantitative Assessment with a Multidynamic Multiecho Sequence

  • Roh-Eul Yoo (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Seung Hong Choi (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Sung-Won Youn (Department of Radiology, Daegu Catholic University Medical Center) ;
  • Moonjung Hwang (GE Healthcare Korea) ;
  • Eunkyung Kim (Department of Radiology, Rehabilitation Medicine, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Byung-Mo Oh (Department of Radiology, Rehabilitation Medicine, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Ji Ye Lee (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Inpyeong Hwang (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Koung Mi Kang (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Tae Jin Yun (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Ji-hoon Kim (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Chul-Ho Sohn (Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine)
  • Received : 2021.03.30
  • Accepted : 2021.08.28
  • Published : 2022.02.01

Abstract

Objective: This study aimed to explore the myelin volume change in patients with mild traumatic brain injury (mTBI) with post-concussion syndrome (PCS) using a multidynamic multiecho (MDME) sequence and automatic whole-brain segmentation. Materials and Methods: Forty-one consecutive mTBI patients with PCS and 29 controls, who had undergone MRI including the MDME sequence between October 2016 and April 2018, were included. Myelin volume fraction (MVF) maps were derived from the MDME sequence. After three dimensional T1-based brain segmentation, the average MVF was analyzed at the bilateral cerebral white matter (WM), bilateral cerebral gray matter (GM), corpus callosum, and brainstem. The Mann-Whitney U-test was performed to compare MVF and myelin volume between patients with mTBI and controls. Myelin volume was correlated with neuropsychological test scores using the Spearman rank correlation test. Results: The average MVF at the bilateral cerebral WM was lower in mTBI patients with PCS (median [interquartile range], 25.2% [22.6%-26.4%]) than that in controls (26.8% [25.6%-27.8%]) (p = 0.004). The region-of-interest myelin volume was lower in mTBI patients with PCS than that in controls at the corpus callosum (1.87 cm3 [1.70-2.05 cm3] vs. 2.21 cm3 [1.86-3.46 cm3]; p = 0.003) and brainstem (9.98 cm3 [9.45-11.00 cm3] vs. 11.05 cm3 [10.10-11.53 cm3]; p = 0.015). The total myelin volume was lower in mTBI patients with PCS than that in controls at the corpus callosum (0.45 cm3 [0.39-0.48 cm3] vs. 0.48 cm3 [0.45-0.54 cm3]; p = 0.004) and brainstem (1.45 cm3 [1.28-1.59 cm3] vs. 1.54 cm3 [1.42-1.67 cm3]; p = 0.042). No significant correlation was observed between myelin volume parameters and neuropsychological test scores, except for the total myelin volume at the bilateral cerebral WM and verbal learning test (delayed recall) (r = 0.425; p = 0.048). Conclusion: MVF quantified from the MDME sequence was decreased at the bilateral cerebral WM in mTBI patients with PCS. The total myelin volumes at the corpus callosum and brainstem were decreased in mTBI patients with PCS due to atrophic changes.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science ICT and Future Planning (NRF-2020R1A2C2008949, NRF-2020R1A4A1018714); Creative Pioneering Researchers Program through Seoul National University; Institute for Basic Science (IBSR006-A1); the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (2017R1D1A1B04034838); and the Korea Medical Device Development Fund grant funded by the Korea government (the Ministry of Science and ICT, South Korea; the Ministry of Trade, Industry and Energy; the Ministry of Health and Welfare, Republic of Korea; and the Ministry of Food and Drug Safety) (project no. 9991007218, KMDF_PR_20200901_0086). This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. NRF-2021R1A4A1028713).

References

  1. Coronado VG, Xu L, Basavaraju SV, McGuire LC, Wald MM, Faul MD, et al. Surveillance for traumatic brain injury-related deaths--United States, 1997-2007. MMWR Surveill Summ 2011;60:1-32 
  2. Daneshvar DH, Riley DO, Nowinski CJ, McKee AC, Stern RA, Cantu RC. Long-term consequences: effects on normal development profile after concussion. Phys Med Rehabil Clin N Am 2011;22:683-700, ix  https://doi.org/10.1016/j.pmr.2011.08.009
  3. McMahon P, Hricik A, Yue JK, Puccio AM, Inoue T, Lingsma HF, et al. Symptomatology and functional outcome in mild traumatic brain injury: results from the prospective TRACK-TBI study. J Neurotrauma 2014;31:26-33  https://doi.org/10.1089/neu.2013.2984
  4. Corso P, Finkelstein E, Miller T, Fiebelkorn I, Zaloshnja E. Incidence and lifetime costs of injuries in the United States. Inj Prev 2006;12:212-218  https://doi.org/10.1136/ip.2005.010983
  5. Spinos P, Sakellaropoulos G, Georgiopoulos M, Stavridi K, Apostolopoulou K, Ellul J, et al. Postconcussion syndrome after mild traumatic brain injury in Western Greece. J Trauma 2010;69:789-794  https://doi.org/10.1097/TA.0b013e3181edea67
  6. Alves W. Natural history of post-concussive signs and symptoms. Phys Med Rehabil: State Art Rev 1992;6:21-32 
  7. 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  https://doi.org/10.1089/neu.2007.0241
  8. Bendlin BB, Ries ML, Lazar M, Alexander AL, Dempsey RJ, Rowley HA, et al. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 2008;42:503-514  https://doi.org/10.1016/j.neuroimage.2008.04.254
  9. Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007;130:2508-2519  https://doi.org/10.1093/brain/awm216
  10. Levin HS, Wilde E, Troyanskaya M, Petersen NJ, Scheibel R, Newsome M, et al. Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J Neurotrauma 2010;27:683-694  https://doi.org/10.1089/neu.2009.1073
  11. Andica C, Hagiwara A, Hori M, Nakazawa M, Goto M, Koshino S, et al. Automated brain tissue and myelin volumetry based on quantitative MR imaging with various in-plane resolutions. J Neuroradiol 2018;45:164-168  https://doi.org/10.1016/j.neurad.2017.10.002
  12. Hagiwara A, Hori M, Cohen-Adad J, Nakazawa M, Suzuki Y, Kasahara A, et al. Linearity, bias, intrascanner repeatability, and interscanner reproducibility of quantitative multidynamic multiecho sequence for rapid simultaneous relaxometry at 3 T: a validation study with a standardized phantom and healthy controls. Invest Radiol 2019;54:39-47  https://doi.org/10.1097/RLI.0000000000000510
  13. Hagiwara A, Hori M, Kamagata K, Warntjes M, Matsuyoshi D, Nakazawa M, et al. Myelin measurement: comparison between simultaneous tissue relaxometry, magnetization transfer saturation index, and T1w/T2w ratio methods. Sci Rep 2018;8:10554 
  14. Hagiwara A, Hori M, Yokoyama K, Takemura MY, Andica C, Kumamaru KK, et al. Utility of a multiparametric quantitative MRI model that assesses myelin and edema for evaluating plaques, periplaque white matter, and normal-appearing white matter in patients with multiple sclerosis: a feasibility study. AJNR Am J Neuroradiol 2017;38:237-242  https://doi.org/10.3174/ajnr.A4977
  15. Warntjes JBM, Persson A, Berge J, Zech W. Myelin detection using rapid quantitative MR imaging correlated to macroscopically registered luxol fast blue-stained brain specimens. AJNR Am J Neuroradiol 2017;38:1096-1102  https://doi.org/10.3174/ajnr.A5168
  16. Hagiwara A, Kamagata K, Shimoji K, Yokoyama K, Andica C, Hori M, et al. White matter abnormalities in multiple sclerosis evaluated by quantitative synthetic MRI, diffusion tensor imaging, and neurite orientation dispersion and density imaging. AJNR Am J Neuroradiol 2019;40:1642-1648  https://doi.org/10.3174/ajnr.A6209
  17. Dixon CE, Taft WC, Hayes RL. Mechanisms of mild traumatic brain injury. J Head Trauma Rehabil 1993;8:1-12  https://doi.org/10.1097/00001199-199309000-00003
  18. World Health Organization. ICD-10: international statistical classification of diseases and related health problems. Geneva: World Health Organization, 2004 
  19. Riedy G, Senseney JS, Liu W, Ollinger J, Sham E, Krapiva P, et al. Findings from structural MR imaging in military traumatic brain injury. Radiology 2016;279:207-215  https://doi.org/10.1148/radiol.2015150438
  20. King NS, Crawford S, Wenden FJ, Moss NE, Wade DT. The Rivermead post concussion symptoms questionnaire: a measure of symptoms commonly experienced after head injury and its reliability. J Neurol 1995;242:587-592  https://doi.org/10.1007/BF00868811
  21. Kwon JS, Lyoo IK, Hong KS, Yeon BK, Ha KS. Development and standardization of the computerized memory assessment for Korean adults. J Korean Neuropsychiatr Assoc 2002;41:347-362 
  22. Shi H, Hu X, Leak RK, Shi Y, An C, Suenaga J, et al. Demyelination as a rational therapeutic target for ischemic or traumatic brain injury. Exp Neurol 2015;272:17-25  https://doi.org/10.1016/j.expneurol.2015.03.017
  23. Bai L, Bai G, Wang S, Yang X, Gan S, Jia X, et al. Strategic white matter injury associated with long-term information processing speed deficits in mild traumatic brain injury. Hum Brain Mapp 2020;41:4431-4441  https://doi.org/10.1002/hbm.25135
  24. Mohammadian M, Roine T, Hirvonen J, Kurki T, Posti JP, Katila AJ, et al. Alterations in microstructure and local fiber orientation of white matter are associated with outcome after mild traumatic brain injury. J Neurotrauma 2020;37:2616-2623  https://doi.org/10.1089/neu.2020.7081
  25. Bramlett HM, Dietrich WD. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol 2002;103:607-614  https://doi.org/10.1007/s00401-001-0510-8
  26. Donovan V, Kim C, Anugerah AK, Coats JS, Oyoyo U, Pardo AC, et al. Repeated mild traumatic brain injury results in long-term white-matter disruption. J Cereb Blood Flow Metab 2014;34:715-723  https://doi.org/10.1038/jcbfm.2014.6
  27. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 2003;33:366-374  https://doi.org/10.1038/ng1095
  28. Nave KA. Myelination and support of axonal integrity by glia. Nature 2010;468:244-252  https://doi.org/10.1038/nature09614
  29. Jurick SM, Bangen KJ, Evangelista ND, Sanderson-Cimino M, Delano-Wood L, Jak AJ. Advanced neuroimaging to quantify myelin in vivo: application to mild TBI. Brain Inj 2016;30:1452-1457  https://doi.org/10.1080/02699052.2016.1219064
  30. Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329  https://doi.org/10.1016/j.nurt.2007.05.011
  31. Shenton ME, Hamoda HM, Schneiderman JS, Bouix S, Pasternak O, Rathi Y, et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav 2012;6:137-192  https://doi.org/10.1007/s11682-012-9156-5
  32. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003;20:1714-1722  https://doi.org/10.1016/j.neuroimage.2003.07.005
  33. Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Rother J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004;22:1767-1774  https://doi.org/10.1016/j.neuroimage.2004.03.041
  34. Kumar R, Gupta RK, Husain M, Chaudhry C, Srivastava A, Saksena S, et al. Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric tests. Brain Inj 2009;23:675-685  https://doi.org/10.1080/02699050903014915
  35. Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 2010;74:643-650  https://doi.org/10.1212/WNL.0b013e3181d0ccdd
  36. Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, et al. Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 2011;55:1454-1460  https://doi.org/10.1016/j.neuroimage.2011.01.007
  37. Madden DJ, Bennett IJ, Song AW. Cerebral white matter integrity and cognitive aging: contributions from diffusion tensor imaging. Neuropsychol Rev 2009;19:415-435  https://doi.org/10.1007/s11065-009-9113-2
  38. Wheeler-Kingshott CA, Cercignani M. About "axial" and "radial" diffusivities. Magn Reson Med 2009;61:1255-1260  https://doi.org/10.1002/mrm.21965
  39. Wright AD, Jarrett M, Vavasour I, Shahinfard E, Kolind S, van Donkelaar P, et al. Myelin water fraction is transiently reduced after a single mild traumatic brain injury-A prospective cohort study in collegiate hockey players. PLoS One 2016;11:e0150215 
  40. Jurick SM, Hoffman SN, Sorg S, Keller AV, Evangelista ND, DeFord NE, et al. Pilot investigation of a novel white matter imaging technique in Veterans with and without history of mild traumatic brain injury. Brain Inj 2018;32:1256-1265  https://doi.org/10.1080/02699052.2018.1493225
  41. Spader HS, Dean DC, LaFrance WC, Raukar NP, Cosgrove GR, Eyerly-Webb SA, et al. Prospective study of myelin water fraction changes after mild traumatic brain injury in collegiate contact sports. J Neurosurg 2018 Apr [Epub]. https://doi.org/10.3171/2017.12.JNS171597 
  42. Harris TC, de Rooij R, Kuhl E. The shrinking brain: cerebral atrophy following traumatic brain injury. Ann Biomed Eng 2019;47:1941-1959 https://doi.org/10.1007/s10439-018-02148-2