Predicting Outcome 12 Months after Mild Traumatic Brain Injury in Patients Admitted to a Neurosurgery Service

Torgeir Hellstrøm, Tobias Kaufmann, Nada Andelic, Helene L Soberg, Solrun Sigurdardottir, Eirik Helseth, Ole A Andreassen, Lars T Westlye, Torgeir Hellstrøm, Tobias Kaufmann, Nada Andelic, Helene L Soberg, Solrun Sigurdardottir, Eirik Helseth, Ole A Andreassen, Lars T Westlye

Abstract

Objective: Accurate outcome prediction models for patients with mild traumatic brain injury (MTBI) are key for prognostic assessment and clinical decision-making. Using multivariate machine learning, we tested the unique and added predictive value of (1) magnetic resonance imaging (MRI)-based brain morphometric and volumetric characterization at 4-week postinjury and (2) demographic, preinjury, injury-related, and postinjury variables on 12-month outcomes, including global functioning level, postconcussion symptoms, and mental health in patients with MTBI.

Methods: A prospective, cohort study of patients (n = 147) aged 16-65 years with a 12-month follow-up. T1-weighted 3 T MRI data were processed in FreeSurfer, yielding accurate cortical reconstructions for surface-based analyses of cortical thickness, area, and volume, and brain segmentation for subcortical and global brain volumes. The 12-month outcome was defined as a composite score using a principal component analysis including the Glasgow Outcome Scale Extended, Rivermead Postconcussion Questionnaire, and Patient Health Questionnaire-9. Using leave-one-out cross-validation and permutation testing, we tested and compared three prediction models: (1) MRI model, (2) clinical model, and (3) MRI and clinical combined.

Results: We found a strong correlation between observed and predicted outcomes for the clinical model (r = 0.55, p < 0.001). The MRI model performed at the chance level (r = 0.03, p = 0.80) and the combined model (r = 0.45, p < 0.002) were slightly weaker than the clinical model. Univariate correlation analyses revealed the strongest association with outcome for postinjury factors of posttraumatic stress (Posttraumatic Symptom Scale-10, r = 0.61), psychological distress (Hospital Anxiety and Depression Scale, r = 0.52), and widespread pain (r = 0.43) assessed at 8 weeks.

Conclusion: We found no added predictive value of MRI-based measures of brain cortical morphometry and subcortical volumes over and above demographic and clinical features.

Keywords: cortical thickness; outcome; prediction; traumatic brain injury; volumetric analysis.

Figures

Figure 1
Figure 1
Flow diagram of mild traumatic brain injury (MTBI).
Figure 2
Figure 2
Association between predicted and observed outcome. (A) Imaging model mean squared error (MSE): 4.05, (B) clinical model MSE: 2.58, and (C) model with imaging + clinical data MSE: 2.91.

References

    1. Andelic N, Sigurdardottir S, Brunborg C, Roe C. Incidence of hospital-treated traumatic brain injury in the Oslo population. Neuroepidemiology (2008) 30(2):120–8.10.1159/000120025
    1. Carroll LJ, Cassidy JD, Peloso PM, Borg J, von Holst H, Holm L, et al. Prognosis for mild traumatic brain injury: results of the WHO collaborating centre task force on mild traumatic brain injury. J Rehabil Med (2004) 36(43 Suppl):84–105.10.1080/16501960410023859
    1. Cassidy JD, Carroll LJ, Peloso PM, Borg J, von Holst H, Holm L, et al. 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 (2004) 36(43 Suppl):28–60.10.1080/16501960410023732
    1. Sigurdardottir S, Andelic N, Roe C, Jerstad T, Schanke AK. Post-concussion symptoms after traumatic brain injury at 3 and 12 months post-injury: a prospective study. Brain Inj (2009) 23(6):489–97.10.1080/02699050902926309
    1. Studerus-Germann AM, Thiran JP, Daducci A, Gautschi OP. Diagnostic approaches to predict persistent post-traumatic symptoms after mild traumatic brain injury – a literature review. Int J Neurosci (2016) 126(4):289–98.10.3109/00207454.2015.1033620
    1. Siman R, Giovannone N, Hanten G, Wilde EA, McCauley SR, Hunter JV, et al. Evidence that the blood biomarker SNTF predicts brain imaging changes and persistent cognitive dysfunction in mild TBI patients. Front Neurol (2013) 4:190.10.3389/fneur.2013.00190
    1. Silverberg ND, Gardner AJ, Brubacher JR, Panenka WJ, Li JJ, Iverson GL. Systematic review of multivariable prognostic models for mild traumatic brain injury. J Neurotrauma (2015) 32(8):517–26.10.1089/neu.2014.3600
    1. King NS. A systematic review of age and gender factors in prolonged post-concussion symptoms after mild head injury. Brain Inj (2014) 28(13–14):1639–45.10.3109/02699052.2014.954271
    1. Stulemeijer M, van der Werf S, Borm GF, Vos PE. Early prediction of favourable recovery 6 months after mild traumatic brain injury. J Neurol Neurosurg Psychiatry (2008) 79(8):936–42.10.1136/jnnp.2007.131250
    1. Ponsford J, Cameron P, Fitzgerald M, Grant M, Mikocka-Walus A, Schonberger M. Predictors of postconcussive symptoms 3 months after mild traumatic brain injury. Neuropsychology (2012) 26(3):304–13.10.1037/a0027888
    1. Jacobs B, Beems T, Stulemeijer M, van Vugt AB, van der Vliet TM, Borm GF, et al. Outcome prediction in mild traumatic brain injury: age and clinical variables are stronger predictors than CT abnormalities. J Neurotrauma (2010) 27(4):655–68.10.1089/neu.2009.1059
    1. Lingsma H, Yue JK, Maas AI, Steyerberg EW, Manley GT, TRACK-TBI Investigators . Outcome prediction after mild and complicated mild traumatic brain injury: external validation of existing models and identification of new predictors using the TRACK-TBI pilot study. J Neurotrauma (2014) 32(2):83–94.10.1089/neu.2014.3384
    1. McCauley SR, Wilde EA, Miller ER, Frisby ML, Garza HM, Varghese R, et al. Preinjury resilience and mood as predictors of early outcome following mild traumatic brain injury. J Neurotrauma (2013) 30(8):642–52.10.1089/neu.2012.2393
    1. Losoi H, Silverberg ND, Waljas M, Turunen S, Rosti-Otajarvi E, Helminen M, et al. Resilience is associated with outcome from mild traumatic brain injury. J Neurotrauma (2015) 32(13):942–9.10.1089/neu.2014.3799
    1. Kumar RG, Bracken MB, Clark AN, Nick TG, Melguizo MS, Sander AM. Relationship of preinjury depressive symptoms to outcomes 3 mos after complicated and uncomplicated mild traumatic brain injury. Am J Phys Med Rehabil (2014) 93(8):687–702.10.1097/PHM.0000000000000077
    1. Stulemeijer M, Vos PE, Bleijenberg G, van der Werf SP. Cognitive complaints after mild traumatic brain injury: things are not always what they seem. J Psychosom Res (2007) 63(6):637–45.10.1016/j.jpsychores.2007.06.023
    1. Dischinger PC, Ryb GE, Kufera JA, Auman KM. Early predictors of postconcussive syndrome in a population of trauma patients with mild traumatic brain injury. J Trauma (2009) 66(2):289–96; discussion 96–7.10.1097/TA.0b013e3181961da2
    1. Meares S, Shores EA, Taylor AJ, Batchelor J, Bryant RA, Baguley IJ, et al. Mild traumatic brain injury does not predict acute postconcussion syndrome. J Neurol Neurosurg Psychiatry (2008) 79(3):300–6.10.1136/jnnp.2007.126565
    1. Meares S, Shores EA, Taylor AJ, Batchelor J, Bryant RA, Baguley IJ, et al. The prospective course of postconcussion syndrome: the role of mild traumatic brain injury. Neuropsychology (2011) 25(4):454–65.10.1037/a0022580
    1. Sheedy J, Harvey E, Faux S, Geffen G, Shores EA. Emergency department assessment of mild traumatic brain injury and the prediction of postconcussive symptoms: a 3-month prospective study. J Head Trauma Rehabil (2009) 24(5):333–43.10.1097/HTR.0b013e3181aea51f
    1. Haagsma JA, Scholten AC, Andriessen TM, Vos PE, Van Beeck EF, Polinder S. Impact of depression and post-traumatic stress disorder on functional outcome and health-related quality of life of patients with mild traumatic brain injury. J Neurotrauma (2015) 32(11):853–62.10.1089/neu.2013.3283
    1. McCullagh S, Oucherlony D, Protzner A, Blair N, Feinstein A. Prediction of neuropsychiatric outcome following mild trauma brain injury: an examination of the Glasgow Coma Scale. Brain Inj (2001) 15(6):489–97.10.1080/02699050010007353
    1. Hart T, Novack TA, Temkin N, Barber J, Dikmen SS, Diaz-Arrastia R, et al. Duration of posttraumatic amnesia predicts neuropsychological and global outcome in complicated mild traumatic brain injury. J Head Trauma Rehabil (2016) 31(6):E1–9.10.1097/HTR.0000000000000210
    1. Lannsjo M, Backheden M, Johansson U, Af Geijerstam JL, Borg J. Does head CT scan pathology predict outcome after mild traumatic brain injury? Eur J Neurol (2013) 20(1):124–9.10.1111/j.1468-1331.2012.03813.x
    1. Lee H, Wintermark M, Gean AD, Ghajar J, Manley GT, Mukherjee P. Focal lesions in acute mild traumatic brain injury and neurocognitive outcome: CT versus 3T MRI. J Neurotrauma (2008) 25(9):1049–56.10.1089/neu.2008.0566
    1. Jerstad T, Roe C, Ronning P, Sigurdardottir S, Nakstad P, Andelic N. Predicting functional outcome one year after traumatic brain injury with CT and MRI findings. J Neurol Res (2012) 2(4):134–44.10.4021/jnr133w
    1. Povlishock JT, Katz DI. Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehabil (2005) 20(1):76–94.10.1097/00001199-200501000-00008
    1. Yuh EL, Mukherjee P, Lingsma HF, Yue JK, Ferguson AR, Gordon WA, et al. Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury. Ann Neurol (2013) 73(2):224–35.10.1002/ana.23783
    1. Ross DE. Review of longitudinal studies of MRI brain volumetry in patients with traumatic brain injury. Brain Inj (2011) 25(13–14):1271–8.10.3109/02699052.2011.624568
    1. da Costa L, van Niftrik CB, Crane D, Fierstra J, Bethune A. Temporal profile of cerebrovascular reactivity impairment, gray matter volumes, and persistent symptoms after mild traumatic head injury. Front Neurol (2016) 7:70.10.3389/fneur.2016.00070
    1. Mild Traumatic Brain Injury Committee; American Congress of Rehabilitation Medicine; Group HIISI. Definition of mild traumatic brain injury. J Head Trauma Rehabil (1993) 8(3):86–7.10.1097/00001199-199309000-00010
    1. Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage (2004) 22(3):1060–75.10.1016/j.neuroimage.2004.03.032
    1. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron (2002) 33(3):341–55.10.1016/S0896-6273(02)00569-X
    1. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage (1999) 9(2):179–94.10.1006/nimg.1998.0395
    1. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A (2000) 97(20):11050–5.10.1073/pnas.200033797
    1. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage (2006) 31(3):968–80.10.1016/j.neuroimage.2006.01.021
    1. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, et al. Automatically parcellating the human cerebral cortex. Cereb Cortex (2004) 14(1):11–22.10.1093/cercor/bhg087
    1. Friborg O, Hjemdal O, Rosenvinge JH, Martinussen M. A new rating scale for adult resilience: what are the central protective resources behind healthy adjustment? Int J Methods Psychiatr Res (2003) 12(2):65–76.10.1002/mpr.143
    1. Friborg O, Barlaug D, Martinussen M, Rosenvinge JH, Hjemdal O. Resilience in relation to personality and intelligence. Int J Methods Psychiatr Res (2005) 14(1):29–42.10.1002/mpr.15
    1. Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet (1974) 2(7872):81–4.10.1016/S0140-6736(74)91639-0
    1. Hellstrøm T, Westlye LT, Server A, Løvstad M, Brunborg C, Lund MJ, et al. Volumetric and morphometric MRI findings in patients with mild traumatic brain injury. Brain Inj (2016) 30(13–14):1683–91.10.1080/02699052.2016.1199905
    1. Kuorinka I, Jonsson B, Kilbom A, Vinterberg H, Biering-Sorensen F, Andersson G, et al. Standardised Nordic questionnaires for the analysis of musculoskeletal symptoms. Appl Ergon (1987) 18(3):233–7.10.1016/0003-6870(87)90010-X
    1. Constantino MJ, Arnkoff DB, Glass CR, Ametrano RM, Smith JZ. Expectations. J Clin Psychol (2011) 67(2):184–92.10.1002/jclp.20754
    1. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand (1983) 67(6):361–70.10.1111/j.1600-0447.1983.tb09716.x
    1. Schonberger M, Ponsford J. The factor structure of the Hospital Anxiety and Depression Scale in individuals with traumatic brain injury. Psychiatry Res (2010) 179(3):342–9.10.1016/j.psychres.2009.07.003
    1. Whelan-Goodinson R, Ponsford J, Schonberger M. Validity of the Hospital Anxiety and Depression Scale to assess depression and anxiety following traumatic brain injury as compared with the Structured Clinical Interview for DSM-IV. J Affect Disord (2009) 114(1–3):94–102.10.1016/j.jad.2008.06.007
    1. Eid J, Thayer JF, Johnsen BH. Measuring post-traumatic stress: a psychometric evaluation of symptom – and coping questionnaires based on a Norwegian sample. Scand J Psychol (1999) 40(2):101–8.10.1111/1467-9450.00105
    1. Stoll C, Kapfhammer HP, Rothenhausler HB, Haller M, Briegel J, Schmidt M, et al. Sensitivity and specificity of a screening test to document traumatic experiences and to diagnose post-traumatic stress disorder in ARDS patients after intensive care treatment. Intensive Care Med (1999) 25(7):697–704.10.1007/s001340050932
    1. Wilson JT, Pettigrew LE, Teasdale GM. Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. J Neurotrauma (1998) 15(8):573–85.10.1089/neu.1998.15.573
    1. Wilde EA, Whiteneck GG, Bogner J, Bushnik T, Cifu DX, Dikmen S, et al. Recommendations for the use of common outcome measures in traumatic brain injury research. Arch Phys Med Rehabil (2010) 91(11):1650.e–60.e.10.1016/j.apmr.2010.06.033
    1. 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(9):587–92.10.1007/BF00868811
    1. Kroenke K, Spitzer RL, Williams JB. The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med (2001) 16(9):606–13.10.1046/j.1525-1497.2001.016009606.x
    1. Nichols T, Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res (2003) 12(5):419–46.10.1191/0962280203sm341ra
    1. Paterakis K, Karantanas AH, Komnos A, Volikas Z. Outcome of patients with diffuse axonal injury: the significance and prognostic value of MRI in the acute phase. J Trauma (2000) 49(6):1071–5.10.1097/00005373-200012000-00016
    1. Zeller B, Tamnes CK, Kanellopoulos A, Amlien IK, Andersson S, Due-Tonnessen P, et al. Reduced neuroanatomic volumes in long-term survivors of childhood acute lymphoblastic leukemia. J Clin Oncol (2013) 31(17):2078–85.10.1200/JCO.2012.47.4031
    1. Rimol LM, Nesvag R, Hagler DJ, Jr, Bergmann O, Fennema-Notestine C, Hartberg CB, et al. Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biol Psychiatry (2012) 71(6):552–60.10.1016/j.biopsych.2011.11.026
    1. Johanson C, Stopa E, Baird A, Sharma H. Traumatic brain injury and recovery mechanisms: peptide modulation of periventricular neurogenic regions by the choroid plexus-CSF nexus. J Neural Transm (2011) 118(1):115–33.10.1007/s00702-010-0498-0
    1. Zhou G, Hotta J, Lehtinen MK, Forss N, Hari R. Enlargement of choroid plexus in complex regional pain syndrome. Sci Rep (2015) 5:14329.10.1038/srep14329
    1. Bigler ED, Maxwell WL. Neuroimaging and neuropathology of TBI. NeuroRehabilitation (2011) 28(2):63–74.10.3233/NRE-2011-0633
    1. Inglese M, Makani S, Johnson G, Cohen BA, Silver JA, Gonen O, et al. Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J Neurosurg (2005) 103(2):298–303.10.3171/jns.2005.103.2.0298
    1. Chamard E, Lefebvre G, Lassonde M, Theoret H. Long-term abnormalities in the corpus callosum of female concussed athletes. J Neurotrauma (2016) 33(13):1220–6.10.1089/neu.2015.3948
    1. Sidaros A, Engberg AW, Sidaros K, Liptrot MG, Herning M, Petersen P, et al. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain (2008) 131(Pt 2):559–72.10.1093/brain/awm294
    1. Fjell AM, Westlye LT, Greve DN, Fischl B, Benner T, van der Kouwe AJ, et al. The relationship between diffusion tensor imaging and volumetry as measures of white matter properties. Neuroimage (2008) 42(4):1654–68.10.1016/j.neuroimage.2008.06.005
    1. Hou R, Moss-Morris R, Peveler R, Mogg K, Bradley BP, Belli A. When a minor head injury results in enduring symptoms: a prospective investigation of risk factors for postconcussional syndrome after mild traumatic brain injury. J Neurol Neurosurg Psychiatry (2012) 83(2):217–23.10.1136/jnnp-2011-300767
    1. Losoi H, Silverberg ND, Waljas M, Turunen S, Rosti-Otajarvi E, Helminen M, et al. Recovery from mild traumatic brain injury in previously healthy adults. J Neurotrauma (2016) 33(8):766–76.10.1089/neu.2015.4070
    1. Faux S, Sheedy J, Delaney R, Riopelle R. Emergency department prediction of post-concussive syndrome following mild traumatic brain injury – an international cross-validation study. Brain Inj (2011) 25(1):14–22.10.3109/02699052.2010.531686
    1. Chaput G, Lajoie SP, Naismith LM, Lavigne G. Pain catastrophizing correlates with early mild traumatic brain injury outcome. Pain Res Manag (2016) 2016:2825856.10.1155/2016/2825856
    1. Cancelliere C, Donovan J, Cassidy JD. Is sex an indicator of prognosis after mild traumatic brain injury: a systematic analysis of the findings of the World Health Organization collaborating centre task force on mild traumatic brain injury and the International Collaboration on Mild Traumatic Brain Injury Prognosis. Arch Phys Med Rehabil (2016) 97(2 Suppl):S5–18.10.1016/j.apmr.2014
    1. McLean SA, Kirsch NL, Tan-Schriner CU, Sen A, Frederiksen S, Harris RE, et al. Health status, not head injury, predicts concussion symptoms after minor injury. Am J Emerg Med (2009) 27(2):182–90.10.1016/j.ajem.2008.01.054
    1. Kreuter M, Sullivan M, Dahllof AG, Siosteen A. Partner relationships, functioning, mood and global quality of life in persons with spinal cord injury and traumatic brain injury. Spinal Cord (1998) 36(4):252–61.10.1038/sj.sc.3100592
    1. Chang FH, Wang YH, Jang Y, Wang CW. Factors associated with quality of life among people with spinal cord injury: application of the International Classification of Functioning, Disability and Health Model. Arch Phys Med Rehabil (2012) 93(12):2264–70.10.1016/j.apmr.2012.06.008
    1. van Veldhoven LM, Sander AM, Struchen MA, Sherer M, Clark AN, Hudnall GE, et al. Predictive ability of preinjury stressful life events and post-traumatic stress symptoms for outcomes following mild traumatic brain injury: analysis in a prospective emergency room sample. J Neurol Neurosurg Psychiatry (2011) 82(7):782–7.10.1136/jnnp.2010.228254
    1. Vikane E, Hellstrom T, Roe C, Bautz-Holter E, Assmus J, Skouen JS. Predictors for return to work in subjects with mild traumatic brain injury. Behav Neurol (2016) 2016:8026414.10.1155/2016/8026414
    1. Maas AI, Lingsma HF, Roozenbeek B. Predicting outcome after traumatic brain injury. Handb Clin Neurol (2015) 128:455–74.10.1016/B978-0-444-63521-1.00029-7
    1. Lovell MR, Collins MW, Iverson GL, Johnston KM, Bradley JP. Grade 1 or "ding" concussions in high school athletes. Am J Sports Med (2004) 32(1):47–54.10.1177/0363546503260723
    1. Ivins BJ, Schwab KA, Warden D, Harvey LT, Hoilien MA, Powell CO, et al. Traumatic brain injury in U.S. Army paratroopers: prevalence and character. J Trauma (2003) 55(4):617–21.10.1097/01.TA.0000052368.97573.D4
    1. Kristman VL, Borg J, Godbolt AK, Salmi LR, Cancelliere C, Carroll LJ, et al. 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 (2014) 95(3 Suppl):S265–77.10.1016/j.apmr.2013.04.026

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