Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury

Restricted access

✓ The objective of this study was to use diffusion-weighted magnetic resonance imaging (DWI) to help detect the type of edema that develops after experimental trauma and trauma coupled with hypotension and hypoxia (THH). Reduction in the apparent diffusion coefficients (ADCs) is thought to represent cytotoxic edema. In a preliminary series of experiments, the infusion edema model and middle cerebral artery occlusion models were used to confirm the direction of ADC change in response to purely extracellular and cytotoxic edema, respectively. The ADCs increased (p < 0.05) in the case of extracellular edema and decreased (p < 0.001) in cytotoxic edema.

Following these initial experiments, a new impact acceleration model was used to induce traumatic brain injury. Thirty-six adult Sprague-Dawley rats were separated into four groups: sham, trauma alone, hypoxia and hypotension (HH), and THH. Following trauma, a 30-minute insult of hypoxia (PaO2 of 40 mm Hg) and hypotension (mean arterial blood pressure (MABP) of 30 mm Hg) were imposed and the animals were resuscitated. The DWI was carried out at four 1-hour intervals postinjury, and MABP, intracranial pressure (ICP), cerebral perfusion pressure (CPP), and cerebral blood flow (CBF) were monitored. The ADCs in the control and HH groups remained unchanged. The ADCs in the THH group rapidly decreased from a control level of 0.68 ± 0.05 × 10−3 mm2/second to 0.37 ± 0.09 3 10−3 mm2/second by 3 hours posttrauma (p < 0.001). In this group, the decreased CBF and CPP during secondary insult remained low despite resuscitation, with the ICP increasing to 56 6 7 mm Hg by 3 hours. In the trauma alone group, the rise in ICP reached a maximum value (28 ± 3 mm Hg) at 30 minutes with a significant and sustained increase in CBF despite a gradual decrease in CPP. The ADCs in this group were not significantly reduced. The data lead the authors to suggest that the rise in ICP following severe trauma coupled with secondary insult in this model is predominately caused by cytotoxic edema and that ischemia plays a major role in the development of brain edema after head injury.

Article Information

Contributor Notes

Address reprint requests to: Anthony Marmarou, Ph.D., Division of Neurosurgery, P.O. Box 508, MCV Station, 1101 East Marshall Street, Richmond, Virginia 23298.
Headings
References
  • 1.

    Benveniste HDHedlund LWJohnson GA: Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 23:7467541992Benveniste HD Hedlund LW Johnson GA: Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 23:746–754 1992

    • Search Google Scholar
    • Export Citation
  • 2.

    Busza ALAllen KLvan Bruggen Net al: Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke 23:160216121992Busza AL Allen KL van Bruggen N et al: Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke 23:1602–1612 1992

    • Search Google Scholar
    • Export Citation
  • 3.

    Ebisu TNaruse SHorikawa Yet al: Discrimination between different types of white matter edema with diffusion-weighted MR imaging. J Magn Reson Imaging 3:8638681993Ebisu T Naruse S Horikawa Y et al: Discrimination between different types of white matter edema with diffusion-weighted MR imaging. J Magn Reson Imaging 3:863–868 1993

    • Search Google Scholar
    • Export Citation
  • 4.

    Gotoh OAsano TKoide Tet al: Ischemic brain edema following occlusion of the middle cerebral artery in the rat. I: the time courses of the brain water, sodium and potassium contents and blood-brain-barrier permeability to 125I-albumin. Stroke 16:1011091985Gotoh O Asano T Koide T et al: Ischemic brain edema following occlusion of the middle cerebral artery in the rat. I: the time courses of the brain water sodium and potassium contents and blood-brain-barrier permeability to 125I-albumin. Stroke 16:101–109 1985

    • Search Google Scholar
    • Export Citation
  • 5.

    Ishige NPitts LHBerry Iet al: The effects of hypovolemic hypotension on high-energy phosphate metabolism of traumatized brain in rats. J Neurosurg 68:1291361988Ishige N Pitts LH Berry I et al: The effects of hypovolemic hypotension on high-energy phosphate metabolism of traumatized brain in rats. J Neurosurg 68:129–136 1988

    • Search Google Scholar
    • Export Citation
  • 6.

    Ito UOhno KNakamura Ret al: Brain edema during ischemia and after restoration of blood flow. Measurement of water, sodium, potassium content and plasma protein permeability. Stroke 10:5425471979Ito U Ohno K Nakamura R et al: Brain edema during ischemia and after restoration of blood flow. Measurement of water sodium potassium content and plasma protein permeability. Stroke 10:542–547 1979

    • Search Google Scholar
    • Export Citation
  • 7.

    Johansson BBLinder LE: Hypertension and brain oedema: an experimental study on acute and chronic hypertension in the rat. J Neurol Neurosurg Psychiatry 44:4024061981Johansson BB Linder LE: Hypertension and brain oedema: an experimental study on acute and chronic hypertension in the rat. J Neurol Neurosurg Psychiatry 44:402–406 1981

    • Search Google Scholar
    • Export Citation
  • 8.

    Kita HMarmarou A: The cause of acute brain swelling after the closed head injury in rats. Acta Neurochir 60 (Suppl):4524551994Kita H Marmarou A: The cause of acute brain swelling after the closed head injury in rats. Acta Neurochir 60 (Suppl): 452–455 1994

    • Search Google Scholar
    • Export Citation
  • 9.

    Knight RAOrdidge RJHelpern JAet al: Temporal evolution of ischemic damage in rat brain measured by proton nuclear magnetic resonance imaging. Stroke 22:8028081991Knight RA Ordidge RJ Helpern JA et al: Temporal evolution of ischemic damage in rat brain measured by proton nuclear magnetic resonance imaging. Stroke 22:802–808 1991

    • Search Google Scholar
    • Export Citation
  • 10.

    Marmarou A: Traumatic brain edema: an overview. Acta Neurochir 60 (Suppl):4214241994Marmarou A: Traumatic brain edema: an overview. Acta Neurochir 60 (Suppl):421–424 1994

    • Search Google Scholar
    • Export Citation
  • 11.

    Marmarou AFoda MAEvan den Brink Wet al: A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics. J Neurosurg 80:2913001994Marmarou A Foda MAE 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
  • 12.

    Marmarou AWard JYoung HFet al: Impact of ICP instability and hypotension on outcome in patients with severe head trauma. J Neurosurg 75 (Suppl):59661991Marmarou A Ward J Young HF et al: Impact of ICP instability and hypotension on outcome in patients with severe head trauma. J Neurosurg 75 (Suppl):59–66 1991

    • Search Google Scholar
    • Export Citation
  • 13.

    Miller JDCorales RL: Brain edema as a result of head injury: fact or fallacy? in de Vlieger Mde Lange SBeks JWF (eds): Brain Edema. New York: John Wiley & Sons1981 pp 99115Miller JD Corales RL: Brain edema as a result of head injury: fact or fallacy? in de Vlieger M de Lange S Beks JWF (eds): Brain Edema. New York: John Wiley & Sons 1981 pp 99–115

    • Search Google Scholar
    • Export Citation
  • 14.

    Mintorovitch JMoseley MEChileuitt Let al: Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn Reson Med 18:39501991Mintorovitch J Moseley ME Chileuitt L et al: Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn Reson Med 18:39–50 1991

    • Search Google Scholar
    • Export Citation
  • 15.

    Moseley MECohen YMintorovitch Jet al: Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med 14:3303461990Moseley ME Cohen Y Mintorovitch J et al: Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med 14:330–346 1990

    • Search Google Scholar
    • Export Citation
  • 16.

    Narayan RKGreenberg RPMiller JDet al: Improved confidence of outcome prediction in severe head injury. A comparative analysis of the clinical examination, multimodality evoked potentials, CT scanning, and intracranial pressure. J Neurosurg 54:7517621981Narayan RK Greenberg RP Miller JD et al: Improved confidence of outcome prediction in severe head injury. A comparative analysis of the clinical examination multimodality evoked potentials CT scanning and intracranial pressure. J Neurosurg 54:751–762 1981

    • Search Google Scholar
    • Export Citation
  • 17.

    Ohata KMarmarou A: Clearance of brain edema and macromolecules through the cortical extracellular space. J Neurosurg 77:3873961992Ohata K Marmarou A: Clearance of brain edema and macromolecules through the cortical extracellular space. J Neurosurg 77:387–396 1992

    • Search Google Scholar
    • Export Citation
  • 18.

    Petito CKSchaefer JAPlum F: The blood-brain barrier in experimental seizures in Pappius HMFeindel W (eds): Dynamics of Brain Edema. Berlin: Springer-Verlag1976 pp 3842Petito CK Schaefer JA Plum F: The blood-brain barrier in experimental seizures in Pappius HM Feindel W (eds): Dynamics of Brain Edema. Berlin: Springer-Verlag 1976 pp 38–42

    • Search Google Scholar
    • Export Citation
  • 19.

    Pierpaoli CRighini ALinfante Iet al: Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging and light and electron microscopic study. Radiology 189:4394481993Pierpaoli C Righini A Linfante I et al: Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging and light and electron microscopic study. Radiology 189:439–448 1993

    • Search Google Scholar
    • Export Citation
  • 20.

    Schuier FJHossmann KA: Experimental brain infarcts in cats. II. Ischemic brain edema. Stroke 11:5936011980Schuier FJ Hossmann KA: Experimental brain infarcts in cats. II. Ischemic brain edema. Stroke 11:593–601 1980

    • Search Google Scholar
    • Export Citation
  • 21.

    Sevick RJKanda FMintorovitch Jet al: Cytotoxic brain edema: assessment with diffusion-weighted MR imaging. Radiology 185:6876901992Sevick RJ Kanda F Mintorovitch J et al: Cytotoxic brain edema: assessment with diffusion-weighted MR imaging. Radiology 185:687–690 1992

    • Search Google Scholar
    • Export Citation
  • 22.

    Siesjo BK: Membrane events leading to glial swelling and brain edema in Inaba YKlatzo ISpatz M (eds): Brain Edema. Proceedings of the Sixth International Symposium November 7–10 in Tokyo. Berlin: Springer-Verlag1985 pp 200209Siesjo BK: Membrane events leading to glial swelling and brain edema in Inaba Y Klatzo I Spatz M (eds): Brain Edema. Proceedings of the Sixth International Symposium November 7–10 in Tokyo. Berlin: Springer-Verlag 1985 pp 200–209

    • Search Google Scholar
    • Export Citation
  • 23.

    Tamura AGraham DIMcCulloch Jet al: Focal cerebral ischaemia in the rat. 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1:53601981Tamura A Graham DI McCulloch J et al: Focal cerebral ischaemia in the rat. 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1:53–60 1981

    • Search Google Scholar
    • Export Citation
  • 24.

    van den Brink WASantos BOMarmarou Aet al: Quantitative analysis of blood-brain barrier damage in two models of experimental head injury in the rat. Acta Neurochir 60 (Suppl):4564581994van den Brink WA Santos BO Marmarou A et al: Quantitative analysis of blood-brain barrier damage in two models of experimental head injury in the rat. Acta Neurochir 60 (Suppl):456–458 1994

    • Search Google Scholar
    • Export Citation
  • 25.

    Yuan XQWade CEClifford CB: Suppression by traumatic brain injury of spontaneous hemodynamic recovery from hemorrhagic shock in rats. J Neurosurg 75:4084141991Yuan XQ Wade CE Clifford CB: Suppression by traumatic brain injury of spontaneous hemodynamic recovery from hemorrhagic shock in rats. J Neurosurg 75:408–414 1991

    • Search Google Scholar
    • Export Citation
TrendMD
Cited By
Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 437 355 16
Full Text Views 163 26 0
PDF Downloads 116 20 0
EPUB Downloads 0 0 0
PubMed
Google Scholar