Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T06:03:42.593Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuroanatomic correlates of CVLT–C performance following pediatric traumatic brain injury

Published online by Cambridge University Press:  21 October 2005

CYNTHIA F. SALORIO ,
BETH S. SLOMINE ,
MARCO A. GRADOS ,
ROMA A. VASA ,
JAMES R. CHRISTENSEN  and
JOAN P. GERRING
CYNTHIA F. SALORIO
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, Maryland
BETH S. SLOMINE
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland
MARCO A. GRADOS
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland
ROMA A. VASA
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland
JAMES R. CHRISTENSEN
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland
JOAN P. GERRING
Affiliation:
Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland
Get access Rights & Permissions [Opens in a new window]

Abstract

Traumatic brain injury (TBI) frequently results in memory problems, and the degree of memory impairment is related to injury severity and is commonly associated with lesions in frontal and temporal brain areas. This study examined the relationship among injury severity, brain lesions, and memory in children with moderate to severe TBI using Donders' (1999) 5-factor model of performance on the California Verbal Learning Test–Children's Version (CVLT–C). Seventy-six children underwent magnetic resonance imaging (MRI) scans 3 months post-TBI and testing 1 year post-TBI. Results showed injury severity (Glasgow Coma Scale) was not predictive of performance on 4 of the 5 factors. Volume of frontal and/or temporal brain lesions was significantly predictive of performance on 3 of the 5 factors. Unexpectedly, lesion volume outside these areas (extra-frontotemporal) was predictive of performance on all 5 factors. In contrast, Verbal IQ at 1 year was most strongly associated with preinjury factors (socioeconomic status and special education involvement), although extra-frontotemporal lesions also contributed to the variability in this measure. Results suggest that in children with moderate to severe TBI, extra-frontal/temporal lesions are predictive of memory outcome 1 year postinjury above and beyond initial severity or frontal/temporal contusions. This finding may relate to widespread diffuse axonal injury, which potentially disconnects brain circuits mediating memory following moderate to severe TBI. (JINS, 2005, 11, 686–696.)

Keywords

TBI (Traumatic brain injury)MemoryChildrenMagnetic resonance imagingDiffuse brain injuryNeuropsychological test
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 11 , Issue 6 , October 2005 , pp. 686 - 696
Copyright
© 2005 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, J.H., Doyle, D., Ford, I., Gennarelli, T., Graham, D.I., & McLellan, D.R. (1989). Diffuse axonal injury in head injury: Definition, diagnosis and grading. Histopathology, 15, 49–59.Google Scholar
Adams, J.H., Jennett, B., McLellan, D.R., Murray, L.S., & Graham, D.I. (1999). The neuropathology of the vegetative state after head injury. Journal of Clinical Pathology, 52, 804–806.Google Scholar
Alexander, M.P., Stuss, D.T., & Fansabedian, N. (2003). California Verbal Learning Test: Performance by patients with focal frontal and non-frontal lesions. Brain, 126, 1493–1503.Google Scholar
American Psychiatric Association (1987). Diagnostic and Statistical Manual of Mental Disorders (Revised–3rd ed.). Washington, DC: American Psychiatric Association Press.
Auerbach, S.H. (1986). Neuroanatomical correlates of attention and memory disorders in traumatic brain injury: An application of neurobehavioral subtypes. Journal of Head Trauma Rehabilitation, 1, 1–12.Google Scholar
Blatter, D.D., Bigler, E.D., Gale, S.D., Johnson, S.C., Anderson, C.V., & Burnett, B.M. (1997). MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: Correlation with neuropsychological outcome. American Journal of Neuroradiology, 18, 1–10.Google Scholar
Blumbergs, P.C., Scott, G., Manavis, J., Wainwright, H., Simpson, D.A., & McLean, A. (1994). Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet, 344, 1055–1056.Google Scholar
Catroppa, C. & Anderson, V. (2002). Recovery in memory function in the first year following TBI in children. Brain Injury, 16, 369–384.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1994). California Verbal Learning Test–Children's Version. San Antonio, TX: Psychological Corporation.
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, and Psychiatry, 69, 210–216.Google Scholar
Donders, J. (1999). Structural equation analysis of the California Verbal Learning Test–Children's Version in the standardization sample. Developmental Neuropsychology, 15, 395–406.Google Scholar
Donders, J. & Minnema, M.T. (2004). Performance discrepancies on the California Verbal Learning Test–Children's Version (CVLT–C) in children with traumatic brain injury. Journal of the International Neuropsychological Society, 10, 482–488.Google Scholar
Eslinger, P.G. & Damasio, A.R. (1985). Severe disturbance of higher cognition after frontal lobe ablation: Patient EVR. Neurology, 35, 1731–1741.Google Scholar
Ewing-Cobbs, L., Levin, H.S., & Fletcher, J.M. (1998). Neuropsychological sequelae after pediatric traumatic brain injury. In M. Ylvisaker (Ed.), Traumatic brain injury rehabilitation: Children and adolescents (2nd ed.) (pp. 11–26). Boston: Butterworth-Heinimann.
Ewing-Cobbs, L., Levin, H.S., Fletcher, T.M., Miner, M.E., & Eisenberg, H.M. (1990). The Children's Orientation and Amnesia Test: Relationship to severity of acute head injury and to recovery of memory. Neurosurgery, 27, 683–691.Google Scholar
Geddes, J.F., Hackshaw, A.K., Vowles, G.H., Nickols, C.D., & Whitwell, H.L. (2001). Neuropathology of inflicted head injury in children. I. Patterns of brain damage. Brain, 124, 1290–1298.Google Scholar
Gentry, L.R., Godersky, J.C., & Thompson, B. (1988). MR imaging of head trauma: Review of the distribution and radiopathologic features of traumatic lesions. American Journal of Neuroradiology, 150, 663–672.Google Scholar
Gerring, J., Brady, K., Chen, A., Quinn, C., Herskovits, E., Bandeen-Roche, K., Denckla, M.B., & Bryan, R.N. (2000). Neuroimaging variables related to development of secondary attention deficit hyperactivity disorder after closed head injury in children and adolescents. Brain Injury, 14, 205–218.Google Scholar
Gerring, J.P., Brady, K.D., Chen, A., Vasa, R., Grados, M., Bandeen-Roche, K.J., Bryan, R.N., & Denckla, M.B. (1998). Premorbid prevalence of ADHD and development of secondary ADHD after closed head injury. Journal of the American Academy of Child and Adolescent Psychiatry, 37, 647–654.Google Scholar
Giedd, J.N., Blumenthal, J., & Jeffries, N.O. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861–863.Google Scholar
Grados, M.A., Slomine, B.S., Gerring, J.P., Vasa, R., Bryan, N., & Denckla, M.B. (2001). Depth of lesion model in children and adolescents with moderate to severe traumatic brain injury: Use of SPGR MRI to predict severity and outcome. Journal of Neurology, Neurosurgery, and Psychiatry, 70, 350–358.Google Scholar
Hoffman, N., Donders, J., & Thompson, E.H. (2000). Novel learning abilities after traumatic head injury in children. Archives of Clinical Neuropsychology, 1, 47–58.Google Scholar
Hollingshead, A. (1975). Four Factor Index of Social Status. Unpublished manuscript, Department of Sociology, Yale University.
ISG Technologies (1995). Allegro software. Toronto, Canada: ISG Technologies.
Jaffe, K., Fay, G., Polissar, N.L., Martin, K., Shurtleff, H., Rivara, J.B., & Winn, H.R. (1993). Severity of pediatric traumatic brain injury and neurobehavioral recovery at one year—A cohort study. Archives of Physical Medicine and Rehabilitation, 74, 587–595.Google Scholar
Jaffe, K.M., Fay, G.C., Polissar, N.L., Martin, K.M., Shurtleff, H., Rivara, J., & Winn, H.R. (1992). Severity of pediatric traumatic brain injury and neurobehavioral recovery at one year—A cohort study. Archives of Physical Medicine and Rehabilitation, 73, 540–547.Google Scholar
Jaffe, K.M., Polissar, N.L., Fay, G.C., & Liao, S. (1995). Recovery trends over three years following pediatric traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 76, 17–26.Google Scholar
Janowsky, J.S., Shimamura, A.P., Kritchevsky, M., & Squire, L.R. (1989). Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behavioral Neuroscience, 103, 548–560.Google Scholar
Kauffman, P.M., Fletcher, J.M., Levin, H.S., Miner, M.E., & Ewing-Cobbs, L. (1993). Attentional disturbance after pediatric closed head injury. Journal of Child Neurology, 8, 348–353.Google Scholar
Levin, H.S., Amparo, E.G., Eisenberg, H.M., Miner, M.E., High, W.M., Ewing-Cobbs, L., Fletcher, J.M., & Guinto, F.C. (1989). Magnetic resonance imaging after closed head injury in children. Neurosurgery, 24, 223–227.Google Scholar
Levin, H.S., Culhane, K.A., Fletcher, J.M., Mendelsohn, D.B., Lilly, M.A., Harward, H., Chapman, S.B., Bruce, D.A., Bertolino-Kusnerik, L., & Eisenberg, H.M. (1994). Dissociation between delayed alternation and memory after pediatric head injury: Relationship to MRI findings. Journal of Child Neurology, 9, 81–89.Google Scholar
Levin, H.S., Culhane, K.A., Mendelsohn, D., Lilly, M.A., Bruce, D., Flethcher, J.M., Chapman, S.B., Harward, H., & Eisenberg, H.M. (1993). Cognition in relation to magnetic resonance imaging in head-injured children and adolescents. Archives of Neurology, 50, 897–905.Google Scholar
Levin, H.S., Eisenberg, H.M., Wigg, N.R., & Kobayashi, K. (1982). Memory and intellectual ability after head injury in children and adolescents. Neurosurgery, 11, 668–673.Google Scholar
Levin, H.S., Fletcher, J.M., Kufera, J.A., Harward, H., Lilly, M.A., Medelsohn, D., Bruce, D., & Eisenberg, H.M. (1996). Dimensions of cognition measured by the Tower of London and other cognitive tasks in head-injured children and adolescents. Developmental Neuropsychology, 12, 17–34.Google Scholar
Levin, H.S., High, W.M., Ewing-Cobbs, L., Fletcher, J.M., Eisenberg, H.M., Miner, M.E., & Goldstein, F.C. (1988). Memory functioning during the first year after closed head injury in children and adolescents. Neurosurgery, 22, 1043–1052.Google Scholar
Levin, H.S., Song, J., Ewing-Cobbs, L., Chapman, S.B., & Mendelsohn, D. (2001). Word fluency in relation to severity of closed head injury, associated frontal brain lesions, and age at injury in children. Neuropsychologia, 39, 122–131.Google Scholar
Levin, H.S., Song, J., Scheibel, R.S., Fletcher, J.M., Harward, H., Lilly, M., & Goldstein, F. (1997). Concept formation and problem-solving following closed head injury in children. Journal of the International Neuropsychological Society, 3, 598–607.Google Scholar
Mandzia, J.L., Black, S.E., McAndrews, M.P., Grady, C., & Graham, S. (2004). fMRI differences in encoding and retrieval of pictures due to encoding strategy in the elderly. Human Brain Mapping, 21, 1–14.Google Scholar
Massagli, T.L., Michaud, L.J., & Rivara, F.P. (1996). Association between injury indices and outcome after severe traumatic brain injury in children. Archives of Physical Medicine and Rehabilitation, 77, 125–132.Google Scholar
Medana, I.M. & Esiri, M.M. (2003). Axonal damage: A key predictor of outcome in human CNS diseases. Brain, 126, 515–530.Google Scholar
Mendelsohn, D., Levin, H.S., Bruce, D., Lilly, M., Harward, H., Culhane, K.A., & Eisenberg, H.M. (1992). Late MRI after head injury in children: Relationship to clinical features and outcome. Child's Nervous System, 8, 445–452.Google Scholar
Miller, L.J. & Donders, J. (2003). Prediction of educational outcome after pediatric traumatic brain injury. Rehabilitation Psychology, 48, 237–241.Google Scholar
Roman, M.J., Delis, D.C., Willerman, L., Magulac, M., Demadura, T.L., de la Peña, J.L., Loftis, C. et al. (1998). Impact of pediatric traumatic brain injury on components of verbal memory. Journal of Clinical and Experimental Neuropsychology, 2, 245–258.Google Scholar
Slifer, K.J., Cataldo, M.F., Cataldo, M.D., Llorente, A.M., & Gerson, A.C. (1993). Behavior analysis of motion control for pediatric neuroimaging. Journal of Applied Behavioral Analysis, 26, 469–470.Google Scholar
Slomine, B.S., Gerring, J.P., Grados, M.A., Vasa, R., Brady, K.D., Christensen, J.R., & Denckla, M.B. (2002). Performance on measures of ‘executive function’ following pediatric traumatic brain injury. Brain Injury, 16, 759–772.Google Scholar
Squire, L.R., Haist, F., & Shimamura, A.P. (1989). The neurology of memory: Quantitative assessment of retrograde amnesia in two groups of amnesic patients. Journal of Neuroscience, 9, 828–839.Google Scholar
Stuss, D.T., Kaplan, E.F., Benson, D.F., Wier, W.S., Naeser, M.A., & Levine, H.L. (1981). Long-term effects of prefrontal leucotomy: An overview of neuropsychological residuals. Journal of Clinical Neuropsychology, 3, 13–32.Google Scholar
Talairach, T. & Tournox, P. (1988) Co-planar stereotaxic atlas of the human brain. Three dimensional proportional system: An approach to cerebral imaging. New York: Thieme Medical Publishers.
Taylor, H.G. & Allen, J. (1997). Age related differences in outcomes following childhood brain insults: An introduction and overview. Journal of the International Neuropsychological Society, 3, 555–567.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., Grados, M., Slomine, B., Herskovits, E.H., Thompson, R.E., Salorio, C., Christensen, J. et al. (2004). Neuroimaging correlates of anxiety after pediatric traumatic brain injury. Biological Psychiatry, 55, 208–216.Google Scholar
Verger, K., Junqué, C., Levin, H.S., Jurado, M.A., Pérez-Gomez, M., Bartés-Faz, D., Barrios, M. et al. (2001). Correlation of atrophy measures on MRI with neuropsychological sequelae in children and adolescents with traumatic brain injury. Brain Injury, 15, 211–221.Google Scholar
Wechsler, D. (1991). Wechsler Intelligence Scale for Children (3rd ed.). San Antonio, TX: Psychological Corporation.
Weis, S., Klaver, P., Reul, J., Elger, C., & Fernandez, G. (2004). Temporal and cerebellar brain regions that support both declarative memory formation and retrieval. Cerebral Cortex, 14, 256–267.Google Scholar
Welner, Z., Reich, W., Herjanic, B., Jung, K.G., & Amado, H. (1987). Reliability, validity, and parent–child agreement studies of the Diagnostic Interview for Children and Adolescents (DICA). Journal of the American Academy of Child and Adolescent Psychiatry, 26, 649–653.Google Scholar
Wilson, J.T. (1990) Review: The relationship between neuropsychological function and brain damage detected by neuroimaging after closed head injury. Brain Injury, 4, 349–363.Google Scholar
Yeates, K.O. (2000). Closed-head injury. In K.O. Yeates, M.D. Ris, & H.G. Taylor (Eds.), Pediatric neuropsychology: Research, theory and practice (pp. 92–116). New York: Guilford.
Yeates, K.O., Blumenstein, E., Patterson, C.M., & Delis, D.C. (1995). Verbal learning and memory following pediatric closed-head injury. Journal of the International Neuropsychological Society, 1, 78–87.Google Scholar
Yeates, K.O., Taylor, H.G., Wade, S.L., Drotar, D., Stancin, T., & Minich, N. (2002). A prospective study of short- and long-term neuropsychological outcomes after traumatic brain injury in children. Neuropsychology, 16, 514–523.Google Scholar
Zafonte, R.D., Hammond, F.M., Mann, N.R, Wood, D.L., Black, K.L, & Millis, S.R. (1996). Relationship between Glasgow coma scale and functional outcome. American Journal of Physical Medicine and Rehabilitation, 75, 364–369.Google Scholar