Contribution of vasogenic and cellular edema to traumatic brain swelling measured by diffusion-weighted imaging

Pál Barzó M.D., Ph.D. 1 , Anthony Marmarou Ph.D. 1 , Panos Fatouros Ph.D. 1 , Koji Hayasaki M.D., Ph.D. 1 and Frank Corwin M.S. 1
View More View Less
  • 1 Division of Neurosurgery and Department of Radiology, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

✓ The contribution of brain edema to brain swelling in cases of traumatic brain injury remains a critical problem. The authors believe that cellular edema, the result of complex neurotoxic events, is the major contributor to brain swelling and that vasogenic edema, secondary to blood-brain barrier compromise, may be overemphasized. The objective of this study, therefore, was to quantify temporal water content changes and document the type of edema that forms during the acute and late stages of edema development following closed head injury (CHI). The measurement of brain water content was based on magnetic resonance imaging—determined values of tissue longitudinal relaxation time (T1-weighted imaging) and their subsequent conversion to percentage of water, whereas the differentiation of edema formation (cellular vs. vasogenic) was based on the measurement of the apparent diffusion coefficient (ADC) by diffusion-weighted imaging.

A new impact-acceleration model was used to induce CHI. Thirty-six adult Sprague—Dawley rats were separated into two groups: Group I, control (six animals); and Group II, trauma (30 animals). Fast ADC measurements (localized, single-voxel) were obtained sequentially (every minute) up to 1 hour postinjury. The T1-weighted images, used for water content determination, and the diffusion-weighted images (ADC measurement with conventional diffusion-weighted imaging) were obtained at the end of the 1st hour postinjury and on Days 1, 3, 7, 14, 28, and 42 in animals from the trauma and control groups.

In the animals subjected to trauma, the authors found a significant increase in ADC (10 ± 5%) and brain water content (1.3 ± 0.9%) during the first 60 minutes postinjury. This is consistent with an increase in the volume of extracellular fluid and vasogenic edema formation as a result of blood-brain barrier compromise. This transient increase, however, was followed by a continuing decrease in ADC that began 40 to 60 minutes postinjury and reached a minimum value on Days 7 to 14 (10 ± 3% reduction). Because the water content of the brain continued to increase during the first 24 hours postinjury (1.9 ± 0.9%), it is suggested that the decreased ADC indicated cellular edema formation, which started to develop soon after injury and became dominant between 1 and 2 weeks postinjury.

The study provides supportive evidence that cellular edema is the major contributor to posttraumatic swelling in diffuse CHI and defines the onset and duration of the increase in cellular volume.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address reprint requests to: Anthony Marmarou, Ph.D., Division of Neurosurgery, P.O. Box 508, Medical College of Virginia Station, Sanger Hall, Room 8004, 1101 East Marshall Street, Richmond, Virginia 23298.
  • 1.

    Barzó P, , Marmarou A, & Fatouros P, et al: Magnetic resonance imaging—monitored acute blood-brain barrier changes in experimental traumatic brain injury. J Neurosurg 85:11131121, 1996 Barzó P, Marmarou A, Fatouros P, et al: Magnetic resonance imaging—monitored acute blood-brain barrier changes in experimental traumatic brain injury. J Neurosurg 85:1113–1121, 1996

    • Search Google Scholar
    • Export Citation
  • 2.

    Becker DP, , Miller JD, & Ward JD, et al: The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47:491502, 1977 Becker DP, Miller JD, Ward JD, et al: The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47:491–502, 1977

    • Search Google Scholar
    • Export Citation
  • 3.

    Bouma GJ, , Muizelaar JP, & Choi SC, et al: Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg 75:685693, 1991 Bouma GJ, Muizelaar JP, Choi SC, et al: Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg 75:685–693, 1991

    • Search Google Scholar
    • Export Citation
  • 4.

    Bullock R, , Zauner A, & Tsuji O, et al: Excitatory amino acid release after severe human head trauma: effect of intracranial pressure and cerebral perfusion pressure changes, in Nagai H, , Kamiya K, & Ishii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag, 1994, pp 264267 Bullock R, Zauner A, Tsuji O, et al: Excitatory amino acid release after severe human head trauma: effect of intracranial pressure and cerebral perfusion pressure changes, in Nagai H, Kamiya K, Ishii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag, 1994, pp 264–267

    • Search Google Scholar
    • Export Citation
  • 5.

    Choi DW: Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11:465469, 1988 Choi DW: Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11:465–469, 1988

    • Search Google Scholar
    • Export Citation
  • 6.

    Dixon CE, , Lyeth BG, & Povlishock JT, et al: A fluid percussion model of experimental brain injury in the rat. J Neurosurg 67:110119, 1987 Dixon CE, Lyeth BG, Povlishock JT, et al: A fluid percussion model of experimental brain injury in the rat. J Neurosurg 67:110–119, 1987

    • Search Google Scholar
    • Export Citation
  • 7.

    Faden AI, , Demediuk P, & Panter SS, et al: The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244:798800, 1989 Faden AI, Demediuk P, Panter SS, et al: The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244:798–800, 1989

    • Search Google Scholar
    • Export Citation
  • 8.

    Fatouros PP, , Marmarou A, & Kraft KA: In vivo brain water determination by T1 measurements: effect of total water content, hydration fraction, and field strength. Magn Reson Med 17:402413, 1991 Fatouros PP, Marmarou A, Kraft KA: In vivo brain water determination by T1 measurements: effect of total water content, hydration fraction, and field strength. Magn Reson Med 17:402–413, 1991

    • Search Google Scholar
    • Export Citation
  • 9.

    Foda MA, & Marmarou A: Posttraumatic hydrocephalus following impact acceleration in the rat, in Nagai H, & Kamiya K (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag, pp 305307, 1994 Foda MA, Marmarou A: Posttraumatic hydrocephalus following impact acceleration in the rat, in Nagai H, Kamiya K (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag, pp 305–307, 1994

    • Search Google Scholar
    • Export Citation
  • 10.

    Groeger U, & Marmarou A: The importance of protein content in the oedema fluid for the resolution of brain oedema. Acta Neurochir 101:134140, 1989 Groeger U, Marmarou A: The importance of protein content in the oedema fluid for the resolution of brain oedema. Acta Neurochir 101:134–140, 1989

    • Search Google Scholar
    • Export Citation
  • 11.

    Hanstock CC, , Faden AI, & Bendall MR, et al: Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 25:843848, 1994 Hanstock CC, Faden AI, Bendall MR, et al: Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 25:843–848, 1994

    • Search Google Scholar
    • Export Citation
  • 12.

    Hovda DA, , Becker DP, & Katayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47S60, 1992 Hovda DA, Becker DP, Katayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47–S60, 1992

    • Search Google Scholar
    • Export Citation
  • 13.

    Ito J, , Marmarou A, & Barzó P, et al: Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury. J Neurosurg 84:97103, 1996 Ito J, Marmarou A, Barzó P, et al: Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury. J Neurosurg 84:97–103, 1996

    • Search Google Scholar
    • Export Citation
  • 14.

    Julow J, , Ishii M, & Iwabuchi T: Scanning electron microscopy of the subarachnoid macrophages after subarachnoid haemorrhage and their possible role in the formation of subarachnoid fibrosis. Acta Neurochir 50:273280, 1979 Julow J, Ishii M, Iwabuchi T: Scanning electron microscopy of the subarachnoid macrophages after subarachnoid haemorrhage and their possible role in the formation of subarachnoid fibrosis. Acta Neurochir 50:273–280, 1979

    • Search Google Scholar
    • Export Citation
  • 15.

    Katayama Y, , Becker DP, & Tamura T, et al: Early cellular swelling in experimental traumatic brain injury: a phenomenon mediated by excitatory amino acids. Acta Neurochir Suppl 51:271273, 1990 Katayama Y, Becker DP, Tamura T, et al: Early cellular swelling in experimental traumatic brain injury: a phenomenon mediated by excitatory amino acids. Acta Neurochir Suppl 51:271–273, 1990

    • Search Google Scholar
    • Export Citation
  • 16.

    Katayama Y, , Becker DP, & Tamura T, et al: Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889900, 1990 Katayama Y, Becker DP, Tamura T, et al: Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889–900, 1990

    • Search Google Scholar
    • Export Citation
  • 17.

    Kettenmann H, & Schachner M: Pharmacological properties of γ-aminobutyric acid-glutamate-, and aspartate-induced depolarization in cultured astrocytes. J Neurosci 5:32953301, 1985 Kettenmann H, Schachner M: Pharmacological properties of γ-aminobutyric acid-glutamate-, and aspartate-induced depolarization in cultured astrocytes. J Neurosci 5:3295–3301, 1985

    • Search Google Scholar
    • Export Citation
  • 18.

    Kimelberg HK, , Pang S, & Treble DH: Excitatory amino acidstimulated uptake of 22Na+ in primary astrocyte cultures. J Neurosci 9:11411149, 1989 Kimelberg HK, Pang S, Treble DH: Excitatory amino acidstimulated uptake of 22Na+ in primary astrocyte cultures. J Neurosci 9:1141–1149, 1989

    • Search Google Scholar
    • Export Citation
  • 19.

    Kimelberg HK, , Rutledge E, & Goderie S, et al: Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 15:409416, 1995 Kimelberg HK, Rutledge E, Goderie S, et al: Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 15:409–416, 1995

    • Search Google Scholar
    • Export Citation
  • 20.

    Klatzo I: Evolution of brain edema concepts. Acta Neurochir Suppl 60:36, 1994 Klatzo I: Evolution of brain edema concepts. Acta Neurochir Suppl 60:3–6, 1994

    • Search Google Scholar
    • Export Citation
  • 21.

    Klatzo I: Neuropathological aspects of brain edema. J Neuropathol Exp Neurol 26:114, 1967 Klatzo I: Neuropathological aspects of brain edema. J Neuropathol Exp Neurol 26:1–14, 1967

    • Search Google Scholar
    • Export Citation
  • 22.

    Klatzo I, , Chui E, & Fujiwara K: Resolution of vasogenic brain edema. Adv Neurol 28:359373, 1980 Klatzo I, Chui E, Fujiwara K: Resolution of vasogenic brain edema. Adv Neurol 28:359–373, 1980

    • Search Google Scholar
    • Export Citation
  • 23.

    Kontos HA: Oxygen radicals in CNS damage. Chem Biol Interact 72:229255, 1989 Kontos HA: Oxygen radicals in CNS damage. Chem Biol Interact 72:229–255, 1989

    • Search Google Scholar
    • Export Citation
  • 24.

    Le Bihan D, , Breton E, & Lallemand D, et al: MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401407, 1986 Le Bihan D, Breton E, Lallemand D, et al: MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407, 1986

    • Search Google Scholar
    • Export Citation
  • 25.

    Marmarou A: Traumatic brain edema: an overview. Acta Neurochir Suppl 60:421424, 1994 Marmarou A: Traumatic brain edema: an overview. Acta Neurochir Suppl 60:421–424, 1994

    • Search Google Scholar
    • Export Citation
  • 26.

    Marmarou A, , Abd-Elfattah Foda MA, & van den Brink W, et al: A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics. J Neurosurg 80:291300, 1994 Marmarou A, Abd-Elfattah Foda MA, van den Brink W, et al: A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics. J Neurosurg 80:291–300, 1994

    • Search Google Scholar
    • Export Citation
  • 27.

    Marmarou A, , Fatouros P, & Ward J, et al: In vivo measurement of brain water by MRI. Acta Neurochir Suppl 51:123124, 1990 Marmarou A, Fatouros P, Ward J, et al: In vivo measurement of brain water by MRI. Acta Neurochir Suppl 51:123–124, 1990

    • Search Google Scholar
    • Export Citation
  • 28.

    Marmarou A, , Poll W, & Shulman R, et al: A simple gravimetric technique for measurement of cerebral edema. J Neurosurg 49:530537, 1978 Marmarou A, Poll W, Shulman R, et al: A simple gravimetric technique for measurement of cerebral edema. J Neurosurg 49:530–537, 1978

    • Search Google Scholar
    • Export Citation
  • 29.

    Marshall LF, , Smith RW, & Shapiro HM: The outcome with aggressive treatment in severe head injuries. Part I. The significance of intracranial pressure monitoring. J Neurosurg 50:2025, 1979 Marshall LF, Smith RW, Shapiro HM: The outcome with aggressive treatment in severe head injuries. Part I. The significance of intracranial pressure monitoring. J Neurosurg 50:20–25, 1979

    • Search Google Scholar
    • Export Citation
  • 30.

    Miller JD, , Becker DP, & Ward JD, et al: Significance of intracranial hypertension in severe head injury. J Neurosurg 47:503516, 1977 Miller JD, Becker DP, Ward JD, et al: Significance of intracranial hypertension in severe head injury. J Neurosurg 47:503–516, 1977

    • Search Google Scholar
    • Export Citation
  • 31.

    Nilsson P, , Hillered L, & Olsson Y, et al: Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab 13:183192, 1992 Nilsson P, Hillered L, Olsson Y, et al: Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab 13:183–192, 1992

    • Search Google Scholar
    • Export Citation
  • 32.

    Ogata J, , Hockwald G, & Cravioto H, et al: Distribution of intraventricular horseradish peroxidase in normal and hydrocephalic cat brains. J Neuropathol Exp Neurol 31:454463, 1972 Ogata J, Hockwald G, Cravioto H, et al: Distribution of intraventricular horseradish peroxidase in normal and hydrocephalic cat brains. J Neuropathol Exp Neurol 31:454–463, 1972

    • Search Google Scholar
    • Export Citation
  • 33.

    Reulen HJ, , Graham R, & Spatz M, et al: Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J Neurosurg 46:2435, 1977 Reulen HJ, Graham R, Spatz M, et al: Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J Neurosurg 46:24–35, 1977

    • Search Google Scholar
    • Export Citation
  • 34.

    Siesjö BK: Basic mechanisms of traumatic brain damage. Ann Emerg Med 22:959969, 1993 Siesjö BK: Basic mechanisms of traumatic brain damage. Ann Emerg Med 22:959–969, 1993

    • Search Google Scholar
    • Export Citation
  • 35.

    Siesjö BK: The role of calcium in cell death, in Price DL, , Thoenen H, & Aguayo AJ (eds): Neurodegenerative Disorders: Mechanisms and Prospects for Therapy. Chichester, UK: John Wiley & Sons, 1991, pp 3559 Siesjö BK: The role of calcium in cell death, in Price DL, Thoenen H, Aguayo AJ (eds): Neurodegenerative Disorders: Mechanisms and Prospects for Therapy. Chichester, UK: John Wiley & Sons, 1991, pp 35–59

    • Search Google Scholar
    • Export Citation
  • 36.

    Siesjö BK, , Katsura K, & Mellegard P: Acidosis-related brain damage. Prog Brain Res 96:2348, 1993 Siesjö BK, Katsura K, Mellegard P: Acidosis-related brain damage. Prog Brain Res 96:23–48, 1993

    • Search Google Scholar
    • Export Citation
  • 37.

    Suzuki S, , Ishii M, & Ottomo M, et al: Changes in the subarachnoid space after experimental subarachnoid haemorrhage in the dog: scanning electron microscopic observation. Acta Neurochir 39:114, 1977 Suzuki S, Ishii M, Ottomo M, et al: Changes in the subarachnoid space after experimental subarachnoid haemorrhage in the dog: scanning electron microscopic observation. Acta Neurochir 39:1–14, 1977

    • Search Google Scholar
    • Export Citation
  • 38.

    Taylor DG, & Bushell MC: The spatial mapping of translational diffusion coefficients by the NMR imaging technique. Phys Med Biol 30:341344, 1985 Taylor DG, Bushell MC: The spatial mapping of translational diffusion coefficients by the NMR imaging technique. Phys Med Biol 30:341–344, 1985

    • Search Google Scholar
    • Export Citation
  • 39.

    Unterberg AW, , Andersen BJ, & Clarke GD, et al: Cerebral energy metabolism following fluid-percussion brain injury in cats. J Neurosurg 68:594600, 1988 Unterberg AW, Andersen BJ, Clarke GD, et al: Cerebral energy metabolism following fluid-percussion brain injury in cats. J Neurosurg 68:594–600, 1988

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 777 429 26
Full Text Views 325 39 4
PDF Downloads 157 30 2
EPUB Downloads 0 0 0