Abstract
Purpose
In the chronic phase after mild traumatic brain injury (mTBI), microhaemorrhages are frequently detected on magnetic resonance imaging (MRI). It is however unclear whether microhaemorrhages are associated with functional outcome and which MRI sequence is most appropriate to address this association. We aimed to determine the association between microhaemorrhages and functional outcome in the chronic posttraumatic phase after injury with the most suitable MRI sequence to address this association.
Methods
One hundred twenty-seven patients classified with mTBI admitted to the outpatient clinic from 2008 to 2015 for persisting posttraumatic complaints were stratified according to the presence of MRI abnormalities (n = 63 (MRI+ group) and n = 64 without abnormalities (MRI− group)). For the detection of microhaemorrhages, susceptibility-weighted imaging (SWI) and T2* gradient recalled echo (T2*GRE) were used. The relation between the functional outcome (dichotomized Glasgow Outcome Scale Extended scores) and the number and localization of microhaemorrhages was analysed using binary logistic regression.
Results
SWI detected twice as many microhaemorrhages compared to T2*GRE: 341 vs. 179. Lesions were predominantly present in the frontal and temporal lobes. Unfavourable outcome was present in 67% of the MRI+ group with a significant association of total number of microhaemorrhages in the temporal cortical area on SWI (OR 0.43 (0.21–0.90) p = 0.02), with an explained variance of 44%. The number of microhaemorrhages was not correlated with the number of posttraumatic complaints.
Conclusion
An unfavourable outcome in the chronic posttraumatic phase is associated with the presence and number of microhaemorrhages in the temporal cortical area. SWI is preferably used to detect these microhaemorrhages.
Similar content being viewed by others
References
Cassidy JD, Carroll LJ, Peloso PM et al (2004) Incidence, risk factors and prevention of mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J Rehabil Med Suppl 43:S28–S60
Mcmahon P, Hricik A, Yue JK et al (2014) Symptomatology and functional outcome in mild traumatic brain injury: results from the prospective TRACK-TBI study. J Neurotrauma 31:26–33
Mott TF, McConnon ML, Rieger BP (2012) Subacute to chronic mild traumatic brain injury. Am Fam Physician 86:1045–1051
Paniak C, Reynolds S, Philips K, Toller-Lobe G, Melnyk A, Nagy J (2002) Patient complaints within 1 month of mild traumatic brain injury: a controlled study. Arch Clin Neuropsychol 17:319–334
Carroll LJ, Cassidy D, Cancelliere C et al (2014) Systematic review of the prognosis after mild traumatic brain injury in adults: cognitive, psychiatric and mortality outcomes: results of the international collaboration in mild traumatic brain injury prognosis. Arch Phys Med Rehabil 95:S152–S173
Adams JH, Doyle D, Ford I, Gennarelli TA, Graham DI, McLellan DR (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59
Liu J, Kou Z, Tian Y (2014) Diffuse axonal injury after traumatic cerebral microbleeds: an evaluation of imaging techniques. Neural Regen Res 9:1222–1230
Huang YL, Kuo YS, Tseng YC (2015) Susceptibility-weighted MRI in mild traumatic brain injury. Neurology 84:580–585
Moen KG, Skandsen T, Folvik M et al (2012) Longitudinal MRI study of traumatic axonal injury in patients with moderate and severe traumatic brain injury. J Neurol Neurosurg Psychiatry 83:1193–1200
Chung SW, Park YS, Nam TK, Kwon JT, Min BK, Hwang SN (2012) Location and clinical significance of non-hemorrhagic brain lesions in diffuse axonal injuries. J Korean Neurosurg Soc 52:377–383
Spitz G, Maller JJ, Ng A, O’Sullivan R, Ferris NJ, Ponsford JL (2013) Detecting lesions after traumatic brain injury using susceptibility weighting imaging: a comparison with fluid-attenuated inversion recovery and correlation with clinical outcome. J Neurotrauma 30:2038–2050
Skandsen T, Kvisted KA, Solhein O, Strand IH, Folvik M, Vik A (2010) Prevalence and impact of diffuse axonal injury in patients with moderate to severe traumatic brain injury: a cohort study of early magnetic resonance findings and 1-year outcome. J Neurosurg 113:556–563
Wu X, Kirov IL, Gonen O, Ge Y, Grossman RI, Lui YW (2016) MR imaging applications in mTBI: an imaging update. Radiology 279:693–707
Yuh EL, Mukherjee P, Lingsma HF et al (2013) Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury. Ann Neurol 73:224–235
Park JH, Park SW, Kang SH, Nam TK, Min BK, Hwang SN (2009) Detection of traumatic cerebral microbleeds by susceptibility-weighted image of MRI. J Korean Neurosurg Soc 46:365–369
Chastain CA, Oyoyo UE, Zipperman M et al (2009) Predicting outcomes of traumatic brain injury by imaging modality and injury distribution. J Neurotrauma 26:1183–1196
Geurts BH, Andriessen TM, Goraj BM, Vos PE (2012) The reliability of magnetic resonance imaging in traumatic brain injury lesion detection. Brain Inj 26:1439–1450
Kristman VL, Borg J, Godbolt AK et al (2014) Methodological issues and research recommendations for prognosis after mild traumatic brain injury: results of the international collaboration on mild traumatic brain injury prognosis. Arch Phys Med Rehabil 95:S265–S277
Cassidy JD, Cancelliere C, Caroll LJ et al (2014) Systematic review of self-reported prognosis in adults after mild traumatic brain injury: results of the International Collaboration on Mild Traumatic Brain Injury Prognosis. Arch Phys Med Rehabil 95:S132–S151
De Koning ME, Gareb B, El Moumni M et al (2016) Subacute posttraumatic complaints and psychological distress in trauma patients with or without mild traumatic brain injury. Injury 47:2041–2047
Wilson JT, Pettigrew LE, Teasdale GM (1998) Structured interviews for the Glasgow outcome scale and the extended Glasgow outcome scale: guidelines for their use. J Neurotrauma 15:573–585
Van der Horn HJ, de Haan S, Spikman JM, de Groot JC, van der Naalt J (2017) Clinical relevance of microhemorrhagic lesions in subacute mild traumatic brain injury. https://doi.org/10.1007/s11682-017-9743-6
Akiyama Y, Miyata K, Harada K et al (2009) Susceptibility-weighted magnetic resonance imaging for the detection of cerebral microhemorrhage in patients with traumatic brain injury. Neurol Med Chir (Tokyo) 49:97–99
Ayaz M, Boikov AS, Haacke EM, Kido DK, Kirsch WM (2010) Imaging cerebral microbleeds using susceptibility weighted imaging: one step toward detecting vascular dementia. J Magn Reson Imaging 31:142–148
Liu W, Liu R, Sun W et al (2012) Different impacts of blood pressure variability on the progression of cerebral microbleeds and white matter lesions. Stroke 43:2916–2922
Dacey R, Dikmen S, Temkin N, Mclean A, Armsden G, Winn HR (1991) Relative effects of brain and non-brain injuries on neuropsychological and psychosocial outcome. J Trauma 31:217–222
Benedictus MR, Spikman JM, van der Naalt J (2010) Cognitive and behavioral impairment in traumatic brain injury related to outcome and return to work. Arch Phys Med Rehabil 91:1436–1441
Tong KA, Ashwal S, Holshouser BA et al (2004) Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol 56:36–50
Toth A, Kornyei B, Kovacs N et al. (2017) Both hemorrhagic and non-hemorrhagic traumatic MRI lesions are associated with the microstructural damage of the normal appearing white matter. Behav Brain Res https://doi.org/10.1016/j.bbr.2017.02.039
Toth A, Kovacs N, Tamas V et al (2016) Microbleeds may expand acutely after traumatic brain injury. Neurosci Lett 617:207–212
Messori A, Polonara G, Mabiglia C, Salvolini U (2003) Is haemosiderin visible indefinitely on gradient-echo MRI following traumatic intracerebral hemorrhage? Neuroradiology 45:881–886
Wäljas M, Iverson GL, Lange RT et al (2015) A prospective biopsychosocial study of the persistent post- concussion symptoms following mild traumatic brain injury. J Neurotrauma 32:534–547
Silverberg ND, Gardner AJ, Brubacher JR, Panenka WJ, Li JJ, Iverson GL (2015) Systematic review of multivariable prognostic models for mild traumatic brain injury. J Neurotrauma 32:517–526
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This study was not funded.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
de Haan, S., de Groot, J.C., Jacobs, B. et al. The association between microhaemorrhages and post - traumatic functional outcome in the chronic phase after mild traumatic brain injury. Neuroradiology 59, 963–969 (2017). https://doi.org/10.1007/s00234-017-1898-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-017-1898-8