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Mean diffusivity in the amygdala correlates with anxiety in pediatric TBI

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Abstract

Traumatic brain injury (TBI) and orthopedic injury (OI) patients are prone to anxiety and mood disorders. In the present study, we integrated anatomical and diffusion tensor neuroimaging to investigate structural properties of the amygdala and hippocampus, gray matter regions implicated in anxiety and mood disorders. Children and adolescents were evaluated during the late sub-acute phase of recovery following trauma resulting from either moderate to severe TBI or OI. Mean diffusivity (MD) of the amygdala and hippocampus was elevated following TBI. An interaction of hemisphere, structure, and group revealed that MD of the right amygdala was elevated in females with TBI. Self-reported anxiety scores were not related to either volume or microstructure of the hippocampus, or to volume or fractional anisotropy of the amygdala. Left amygdala MD in the TBI group accounted for 17.5% of variance in anxiety scores. Anxiety symptoms may be mediated by different mechanisms in patients with TBI or OI.

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References

  • Baker, S. P., O’Neill, B., Haddon, W., & Long, W. B. (1974). The Injury Severity Score: a method for desccribing patients with multiple injuries and evaluation of emergency care. Journal of Trauma, 14, 187–196.

    Google Scholar 

  • Basser, P. J. (1995). Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR in Medicine, 8(7–8), 333–344.

    CAS  Google Scholar 

  • Beauchamp, M. H., Ditchfield, M., Maller, J. J., Catroppa, C., Godfrey, C., Rosenfeld, J. V., et al. (2011). Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury. International Journal of Developmental Neuroscience, 29(2), 137–143.

    Article  PubMed  CAS  Google Scholar 

  • Bendlin, B. B., Ries, M. L., Lazar, M., Alexander, A. L., Dempsey, R. J., Rowley, H. A., et al. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. NeuroImage, 42(2), 503–514.

    Article  PubMed  Google Scholar 

  • Bigler, E. D., Abildskov, T. J., Wilde, E. A., McCauley, S. R., Li, X., Merkley, T. L., et al. (2010). Diffuse damage in pediatric traumatic brain injury: a comparison of automated versus operator-controlled quantification methods. NeuroImage, 50(3), 1017–1026.

    Article  PubMed  Google Scholar 

  • Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., et al. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry, 36(4), 545–553.

    Article  PubMed  CAS  Google Scholar 

  • Birmaher, B., Brent, D., Chiappetta, L., Bridge, J., Monga, S., & Baugher, M. (1999). Psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED): a replication study. Journal of the American Academy of Child and Adolescent Psychiatry, 38(10), 1230–1236.

    Article  PubMed  CAS  Google Scholar 

  • Bloom, D. R., Levin, H. S., Ewing-Cobbs, L., Saunders, A. E., Song, J., Fletcher, J. M., et al. (2001). Lifetime and novel psychiatric disorders after pediatric traumatic brain injury. Journal of the American Academy of Child and Adolescent Psychiatry, 40(5), 572–579.

    Article  PubMed  CAS  Google Scholar 

  • Bock, A. S., Olavarria, J. F., Leigland, L. A., Taber, E. N., Jespersen, S. N., & Kroenke, C. D. (2010). Diffusion tensor imaging detects early cerebral cortex abnormalities in neuronal architecture induced by bilateral neonatal enucleation: an experimental model in the ferret. Frontiers in Systems Neuroscience, 4. doi:10.3389/fnsys.2010.00149.

  • Bombardier, C. H., Fann, J. R., Temkin, N. R., Esselman, P. C., Barber, J., & Dikmen, S. S. (2010). Rates of major depressive disorder and clinical outcomes following traumatic brain injury. JAMA, 303(19), 1938–1945.

    Article  PubMed  CAS  Google Scholar 

  • Brown, G., Chadwick, O., Shaffer, D., Rutter, M., & Traub, M. (1981). A prospective study of children with head injuries, III: psychiatric sequelae. Psychological Medicine, 11(1), 63–78.

    Article  PubMed  CAS  Google Scholar 

  • Campbell-Sills, L., Simmons, A. N., Lovero, K. L., Rochlin, A. A., Paulus, M. P., & Stein, M. B. (2011). Functioning of neural systems supporting emotion regulation in anxiety-prone individuals. NeuroImage, 54(1), 689–696.

    Article  PubMed  Google Scholar 

  • Carrion, V. G., Weems, C. F., Ray, R., & Reiss, A. L. (2002). Toward an empirical definition of pediatric PTSD: the phenomenology of PTSD symptoms in youth. Journal of the American Academy of Child and Adolescent Psychiatry, 41(2), 166–173.

    Article  PubMed  Google Scholar 

  • Cederberg, D., & Siesjö, P. (2010). What has inflammation to do with traumatic brain injury? Child’s Nervous System, 26(2), 221–226.

    Article  PubMed  Google Scholar 

  • Di Stefano, G., Bachevalier, J., Levin, H. S., Song, J. X., Scheibel, R. S., & Fletcher, J. M. (2000). Volume of focal brain lesions and hippocampal formation in relation to memory function after closed head injury in children. Journal of Neurology, Neurosurgery & Psychiatry, 69(2), 210–216.

    Article  Google Scholar 

  • Ewing-Cobbs, L., Prasad, M. R., Swank, P., Kramer, L., Cox, C. S., Jr., Fletcher, J. M., et al. (2008). Arrested development and disrupted callosal microstructure following pediatric traumatic brain injury: relation to neurobehavioral outcomes. NeuroImage, 42(4), 1305–1315.

    Article  PubMed  Google Scholar 

  • Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.

    Article  PubMed  CAS  Google Scholar 

  • Gerring, J. P., Slomine, B., Vasa, R. A., Grados, M., Chen, A., Rising, W., et al. (2002). Clinical predictors of posttraumatic stress disorder after closed head injury in children. Journal of the American Academy of Child and Adolescent Psychiatry, 41(2), 157–165.

    Article  PubMed  Google Scholar 

  • Grados, M. A., Vasa, R. A., Riddle, M. A., Slomine, B. S., Salorio, C., Christensen, J., et al. (2008). New onset obsessive-compulsive symptoms in children and adolescents with severe traumatic brain injury. Depression and Anxiety, 25(5), 398–407.

    Article  PubMed  Google Scholar 

  • Hajek, C. A., Yeates, K. O., Gerry Taylor, H., Bangert, B., Dietrich, A., Nuss, K. E., et al. (2010). Relationships among post-concussive symptoms and symptoms of PTSD in children following mild traumatic brain injury. Brain Injury, 24(2), 100–109.

    Article  PubMed  Google Scholar 

  • Hasan, K., & Narayana, P. (2005). DTI parameter optimization at 3.0 T: potential application in entire normal human brain mapping and multiple sclerosis research. MedicaMundi, 49.

  • Holbrook, T., Hoyt, D., Coimbra, R., Potenza, B., Sise, M., & Anderson, J. (2005). High rates of acute stress disorder impact quality-of-life outcomes in injured adolescents: mechanism and gender predict acute stress disorder risk. Journal of Trauma Injury, Infection and Critical Care, 59(5), 1126–1130.

    Article  Google Scholar 

  • Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841.

    Article  PubMed  Google Scholar 

  • Johansen-Berg, H., Gutman, D. A., Behrens, T. E. J., Matthews, P. M., Rushworth, M. F. S., Katz, E., et al. (2008). Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cerebral Cortex, 18(6), 1374–1383.

    Article  PubMed  CAS  Google Scholar 

  • Jonovska, S., Jengic, V., Kvesic, A., Pavlovic, E., Zupancic, B., Galic, G., et al. (2008). The quality of life during the treatment of long bone fractures in children and adolescents. Collegium Antropologicum, 32(4), 1121–1127.

    PubMed  Google Scholar 

  • Jorge, R. E., Robinson, R. G., Moser, D., Tateno, A., Crespo-Facorro, B., & Arndt, S. (2004). Major depression following traumatic brain injury. Archives of General Psychiatry, 61(1), 42–50.

    Article  PubMed  Google Scholar 

  • Jorge, R. E., Acion, L., Starkstein, S. E., & Magnotta, V. (2007). Hippocampal volume and mood disorders after traumatic brain injury. Biological Psychiatry, 62(4), 332–338.

    Article  PubMed  Google Scholar 

  • Kantarci, K., Petersen, R. C., Boeve, B. F., Knopman, D. S., Weigand, S. D., O’Brien, P. C., et al. (2005). DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology, 64(5), 902–904.

    Article  PubMed  CAS  Google Scholar 

  • Kaufman, J., Birmaher, B., Brent, D., Rao, U. M. A., Flynn, C., Moreci, P., et al. (1997). Schedule for affective disorders and schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988.

    Article  PubMed  CAS  Google Scholar 

  • Kim, M. J., & Whalen, P. J. (2009). The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. Journal of Neuroscience, 29(37), 11614–11618.

    Article  PubMed  CAS  Google Scholar 

  • Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain, 130(10), 2508–2519.

    Article  PubMed  Google Scholar 

  • Langer, D. A., Wood, J. J., Bergman, R. L., & Piacentini, J. C. (2010). A multitrait-multimethod analysis of the construct validity of child anxiety disorders in a clinical sample. Child Psychiatry and Human Development, 41(5), 549–561.

    Article  PubMed  Google Scholar 

  • Langlois, J., Rutland-Brown, W., & Thomas, K. (2005). The incidence of traumatic brain injury among children in the United States: differences by race. The Journal of Head Trauma Rehabilitation, 20(3), 229–238.

    Article  PubMed  Google Scholar 

  • Le Bihan, D. (2003). Looking into the functional architecture of the brain with diffusion MRI. Nature Reviews Neuroscience, 4(6), 469–480.

    Article  PubMed  Google Scholar 

  • Levi, R. B., Drotar, D., Yeates, K. O., & Taylor, H. G. (1999). Posttraumatic stress symptoms in children following orthopedic or traumatic brain injury. Journal of Clinical Child Psychology, 28(2), 232–243.

    Article  PubMed  CAS  Google Scholar 

  • Levin, H., Wilde, E., Chu, Z., Yallampalli, R., Hanten, G., Li, X., et al. (2008). Diffusion tensor imaging in relation to cognitive and functional outcome of traumatic brain injury in children. The Journal of Head Trauma Rehabilitation, 23(4), 197–208.

    Article  PubMed  Google Scholar 

  • Luis, C. A., & Mittenberg, W. (2002). Mood and anxiety disorders following pediatric traumatic brain injury: a prospective study. Journal of Clinical and Experimental Neuropsychology, 24(3), 270–279.

    Article  PubMed  Google Scholar 

  • Maller, J. J., Thomson, R. H. S., Lewis, P. M., Rose, S. E., Pannek, K., & Fitzgerald, P. B. (2010). Traumatic brain injury, major depression, and diffusion tensor imaging: making connections. Brain Research Reviews, 64(1), 213–240.

    Article  PubMed  Google Scholar 

  • Manassis, K., Tannock, R., & Monga, S. (2009). Anxious by maternal—versus self-report: are they the same children? Journal of the Canadian Academy of Child and Adolescent Psychiatry=Journal de l’Academie canadienne de psychiatrie de l’enfant et de l’adolescent, 18(2), 103–109.

    PubMed  Google Scholar 

  • Max, J., Robin, D., Lindgren, S., Smith, W., Sato, Y., Mattheis, P., et al. (1997). Traumatic brain injury in children and adolescents: psychiatric disorders at two years. Journal of the American Academy of Child and Adolescent Psychiatry, 36(9), 1278–1285.

    Article  PubMed  CAS  Google Scholar 

  • Max, J., Koele, S., Smith, W., Sato, Y., Lindgren, S., Robin, D., et al. (1998). Psychiatric disorders in children and adolescents after severe traumatic brain injury: a controlled study. Journal of the American Academy of Child and Adolescent Psychiatry, 37(8), 832–840.

    Article  PubMed  CAS  Google Scholar 

  • Max, J., Keatley, E., Wilde, E. A., Bigler, E. D., Levin, H. S., Schachar, R. J., et al. (2011). Anxiety disorders in children and adolescents in the first six months after traumatic brain injury. The Journal of Neuropsychiatry and Clinical Neurosciences, 23(1), 29–39.

    Article  PubMed  Google Scholar 

  • Monk, C. S. (2008). The development of emotion-related neural circuitry in health and psychopathology. Development and Psychopathology, 20, 1231–1250.

    Article  PubMed  Google Scholar 

  • Mukherjee, P., & McKinstry, R. C. (2006). Diffusion tensor imaging and tractography of human brain development. Neuroimaging Clinics of North America, 16(1), 19–43.

    Article  PubMed  Google Scholar 

  • Pierpaoli, C., Jezzard, P., Basser, P. J., Barnett, A., & Di Chiro, G. (1996). Diffusion tensor MR imaging of the human brain. Radiology, 201(3), 637–648.

    PubMed  CAS  Google Scholar 

  • Pine, D. S., Guyer, A. E., & Leibenluft, E. (2008). Functional magnetic resonance imaging and pediatric anxiety. Journal of the American Academy of Child and Adolescent Psychiatry, 47(11), 1217–1221.

    Article  PubMed  Google Scholar 

  • Rauch, S., Shin, L., & Phelps, E. (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research–past, present, and future. Biological Psychiatry, 60(4), 376–382.

    Article  PubMed  Google Scholar 

  • Saatman, K. E., Duhaime, A.-C., Bullock, R., Maas, A. I. R., Valadka, A., & Manley, G. T. (2008). Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma, 25(7), 719–738.

    Article  PubMed  Google Scholar 

  • Slemmer, J. E., Zhu, C., Landshamer, S., Trabold, R., Grohm, J., Ardeshiri, A., et al. (2008). Causal role of apoptosis-inducing factor for neuronal cell death following traumatic brain injury. American Journal of Pathology, 173(6), 1795–1805.

    Article  PubMed  CAS  Google Scholar 

  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208–S219.

    Article  PubMed  Google Scholar 

  • Tasker, R., Salmond, C., Westland, A., Pena, A., Gillard, J., Sahakian, B., et al. (2005). Head circumference and brain and hippocampal volume after severe traumatic brain injury in childhood. Pediatric Research, 58(2), 302–308.

    Article  PubMed  Google Scholar 

  • Tateno, A., Jorge, R. E., & Robinson, R. G. (2004). Pathological laughing and crying following traumatic brain injury. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(4), 426–434.

    Article  PubMed  Google Scholar 

  • Teasdale, G., & Jennett, B. (1974). Assessment of coma and impaired consciousness: a practical scale. Lancet, 2, 81–84.

    Google Scholar 

  • Vasa, R. A., Gerring, J. P., Grados, M., Slomine, B., Christensen, J. R., Rising, W., et al. (2002). Anxiety after severe pediatric closed head injury. Journal of the American Academy of Child and Adolescent Psychiatry, 41(2), 148–156.

    Article  PubMed  Google Scholar 

  • Vasa, R. A., Grados, M., Slomine, B., Herskovits, E. H., Thompson, R. E., Salorio, C., et al. (2004). Neuroimaging correlates of anxiety after pediatric traumatic brain injury. Biological Psychiatry, 55(3), 208–216.

    Article  PubMed  Google Scholar 

  • Wilde, E., Bigler, E., Hunter, J., Fearing, M., Scheibel, R., Newsome, M., et al. (2007). Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate-to-severe traumatic brain injury. Developmental Medicine and Child Neurology, 49(4), 294–299.

    Article  PubMed  Google Scholar 

  • Winston, F. K., Baxt, C., Kassam-Adams, N. L., Elliott, M. R., & Kallan, M. J. (2005). Acute traumatic stress symptoms in child occupants and their parent drivers after crash involvement. Archives of Pediatrics & Adolescent Medicine, 159(11), 1074–1079.

    Article  Google Scholar 

  • Yakovlev, A. G., Knoblach, S. M., Fan, L., Fox, G. B., Goodnight, R., & Faden, A. I. (1997). Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. Journal of Neuroscience, 17(19), 7415–7424.

    PubMed  CAS  Google Scholar 

  • Zhang, X., Chen, Y. F., Jenkins, L. W., Kochanek, P. M., & Clark, R. S. B. (2005). Bench-to-bedside review: apoptosis/programmed cell death triggered by traumatic brain injury. Critical Care, 9(1), 66–75.

    Article  PubMed  CAS  Google Scholar 

  • Ziebell, J. M., & Morganti-Kossmann, M. C. (2010). Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics, 7(1), 22–30.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded by NIH-NINDS-R01-NS046308 awarded to LEC. Additional intramural funding from the Department of Pediatrics awarded to JJ.

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Correspondence to Jenifer Juranek.

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Juranek, J., Johnson, C.P., Prasad, M.R. et al. Mean diffusivity in the amygdala correlates with anxiety in pediatric TBI. Brain Imaging and Behavior 6, 36–48 (2012). https://doi.org/10.1007/s11682-011-9140-5

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