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

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✓ 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.

Article Information

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.
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References
  • 1.

    Barzó PMarmarou AFatouros Pet al: Magnetic resonance imaging—monitored acute blood-brain barrier changes in experimental traumatic brain injury. J Neurosurg 85:111311211996Barzó 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 DPMiller JDWard JDet al: The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47:4915021977Becker 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 GJMuizelaar JPChoi SCet al: Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg 75:6856931991Bouma 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 RZauner ATsuji Oet al: Excitatory amino acid release after severe human head trauma: effect of intracranial pressure and cerebral perfusion pressure changes in Nagai HKamiya KIshii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag1994 pp 264267Bullock 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 11:4654691988Choi 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 CELyeth BGPovlishock JTet al: A fluid percussion model of experimental brain injury in the rat. J Neurosurg 67:1101191987Dixon 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 AIDemediuk PPanter SSet al: The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244:7988001989Faden 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 PPMarmarou AKraft KA: In vivo brain water determination by T1 measurements: effect of total water content, hydration fraction, and field strength. Magn Reson Med 17:4024131991Fatouros 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 MAMarmarou A: Posttraumatic hydrocephalus following impact acceleration in the rat in Nagai HKamiya K (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag pp 3053071994Foda 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 UMarmarou A: The importance of protein content in the oedema fluid for the resolution of brain oedema. Acta Neurochir 101:1341401989Groeger 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 CCFaden AIBendall MRet al: Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 25:8438481994Hanstock 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 DABecker DPKatayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47S601992Hovda DA Becker DP Katayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47–S60 1992

    • Search Google Scholar
    • Export Citation
  • 13.

    Ito JMarmarou ABarzó Pet al: Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury. J Neurosurg 84:971031996Ito 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 JIshii MIwabuchi T: Scanning electron microscopy of the subarachnoid macrophages after subarachnoid haemorrhage and their possible role in the formation of subarachnoid fibrosis. Acta Neurochir 50:2732801979Julow 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 YBecker DPTamura Tet al: Early cellular swelling in experimental traumatic brain injury: a phenomenon mediated by excitatory amino acids. Acta Neurochir Suppl 51:2712731990Katayama 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 YBecker DPTamura Tet al: Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:8899001990Katayama 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 HSchachner M: Pharmacological properties of γ-aminobutyric acid-glutamate-, and aspartate-induced depolarization in cultured astrocytes. J Neurosci 5:329533011985Kettenmann 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 HKPang STreble DH: Excitatory amino acidstimulated uptake of 22Na+ in primary astrocyte cultures. J Neurosci 9:114111491989Kimelberg 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 HKRutledge EGoderie Set 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 15:4094161995Kimelberg 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 60:361994Klatzo 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 26:1141967Klatzo I: Neuropathological aspects of brain edema. J Neuropathol Exp Neurol 26:1–14 1967

    • Search Google Scholar
    • Export Citation
  • 22.

    Klatzo IChui EFujiwara K: Resolution of vasogenic brain edema. Adv Neurol 28:3593731980Klatzo 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 72:2292551989Kontos HA: Oxygen radicals in CNS damage. Chem Biol Interact 72:229–255 1989

    • Search Google Scholar
    • Export Citation
  • 24.

    Le Bihan DBreton ELallemand Det al: MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:4014071986Le 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 60:4214241994Marmarou A: Traumatic brain edema: an overview. Acta Neurochir Suppl 60:421–424 1994

    • Search Google Scholar
    • Export Citation
  • 26.

    Marmarou AAbd-Elfattah Foda MAvan den Brink Wet al: A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics. J Neurosurg 80:2913001994Marmarou 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 AFatouros PWard Jet al: In vivo measurement of brain water by MRI. Acta Neurochir Suppl 51:1231241990Marmarou 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 APoll WShulman Ret al: A simple gravimetric technique for measurement of cerebral edema. J Neurosurg 49:5305371978Marmarou 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 LFSmith RWShapiro HM: The outcome with aggressive treatment in severe head injuries. Part I. The significance of intracranial pressure monitoring. J Neurosurg 50:20251979Marshall 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 JDBecker DPWard JDet al: Significance of intracranial hypertension in severe head injury. J Neurosurg 47:5035161977Miller 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 PHillered LOlsson Yet al: Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab 13:1831921992Nilsson 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 JHockwald GCravioto Het al: Distribution of intraventricular horseradish peroxidase in normal and hydrocephalic cat brains. J Neuropathol Exp Neurol 31:4544631972Ogata 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 HJGraham RSpatz Met al: Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J Neurosurg 46:24351977Reulen 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 22:9599691993Siesjö 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 DLThoenen HAguayo AJ (eds): Neurodegenerative Disorders: Mechanisms and Prospects for Therapy. Chichester, UK: John Wiley & Sons1991 pp 3559Siesjö 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 BKKatsura KMellegard P: Acidosis-related brain damage. Prog Brain Res 96:23481993Siesjö BK Katsura K Mellegard P: Acidosis-related brain damage. Prog Brain Res 96:23–48 1993

    • Search Google Scholar
    • Export Citation
  • 37.

    Suzuki SIshii MOttomo Met al: Changes in the subarachnoid space after experimental subarachnoid haemorrhage in the dog: scanning electron microscopic observation. Acta Neurochir 39:1141977Suzuki 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 DGBushell MC: The spatial mapping of translational diffusion coefficients by the NMR imaging technique. Phys Med Biol 30:3413441985Taylor 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 AWAndersen BJClarke GDet al: Cerebral energy metabolism following fluid-percussion brain injury in cats. J Neurosurg 68:5946001988Unterberg 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
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