Early Nonischemic Oxidative Metabolic Dysfunction Leads to Chronic Brain Atrophy in Traumatic Brain Injury

Overview

Journal J Cereb Blood Flow Metab

Publisher Sage Publications

Specialties Cardiology & Vascular Diseases
Endocrinology
Neurology

Date 2009 Dec 24

PMID 20029449

Citations 61

Authors

Yueqiao Xu

David L McArthur

Jeffry R Alger

Maria Etchepare

David A Hovda

Thomas C Glenn

Sungcheng Huang

Ivo Dinov

Paul M Vespa

Affiliations

Soon will be listed here.

Abstract

Chronic brain atrophy after traumatic brain injury (TBI) is a well-known phenomenon, the causes of which are unknown. Early nonischemic reduction in oxidative metabolism is regionally associated with chronic brain atrophy after TBI. A total of 32 patients with moderate-to-severe TBI prospectively underwent positron emission tomography (PET) and volumetric magnetic resonance imaging (MRI) within the first week and at 6 months after injury. Regional lobar assessments comprised oxidative metabolism and glucose metabolism. Acute MRI showed a preponderance of hemorrhagic lesions with few irreversible ischemic lesions. Global and regional chronic brain atrophy occurred in all patients by 6 months, with the temporal and frontal lobes exhibiting the most atrophy compared with the occipital lobe. Global and regional reduction in cerebral metabolic rate of oxygen (CMRO(2)), cerebral blood flow (CBF), oxygen extraction fraction (OEF), and cerebral metabolic rate of glucose were observed. The extent of metabolic dysfunction was correlated with the total hemorrhage burden on initial MRI (r=0.62, P=0.01). The extent of regional brain atrophy correlated best with CMRO(2) and CBF. Lobar values of OEF were not in the ischemic range and did not correlate with chronic brain atrophy. Chronic brain atrophy is regionally specific and associated with regional reductions in oxidative brain metabolism in the absence of irreversible ischemia.

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References

Wu H, Huang S, Hattori N, Glenn T, Vespa P, Hovda D . Subcortical white matter metabolic changes remote from focal hemorrhagic lesions suggest diffuse injury after human traumatic brain injury. Neurosurgery. 2004; 55(6):1306-15. DOI: 10.1227/01.neu.0000143028.08719.42. View

Okauchi M, Hua Y, Keep R, Morgenstern L, Xi G . Effects of deferoxamine on intracerebral hemorrhage-induced brain injury in aged rats. Stroke. 2009; 40(5):1858-63. PMC: 2674519. DOI: 10.1161/STROKEAHA.108.535765. View

Verger K, Junque C, Levin H, Jurado M, Bartres-Faz D, Barrios M . Correlation of atrophy measures on MRI with neuropsychological sequelae in children and adolescents with traumatic brain injury. Brain Inj. 2001; 15(3):211-21. DOI: 10.1080/02699050010004059. View

Feeney D, Baron J . Diaschisis. Stroke. 1986; 17(5):817-30. DOI: 10.1161/01.str.17.5.817. View

Coles J, Cunningham A, Salvador R, Chatfield D, Carpenter A, Pickard J . Early metabolic characteristics of lesion and nonlesion tissue after head injury. J Cereb Blood Flow Metab. 2009; 29(5):965-75. DOI: 10.1038/jcbfm.2009.22. View

Shattuck D, Leahy R . BrainSuite: an automated cortical surface identification tool. Med Image Anal. 2002; 6(2):129-42. DOI: 10.1016/s1361-8415(02)00054-3. View

Kidwell C, Saver J, Starkman S, Duckwiler G, Jahan R, Vespa P . Late secondary ischemic injury in patients receiving intraarterial thrombolysis. Ann Neurol. 2002; 52(6):698-703. DOI: 10.1002/ana.10380. View

Levin H, Benavidez D, Verger-Maestre K, Perachio N, Song J, Mendelsohn D . Reduction of corpus callosum growth after severe traumatic brain injury in children. Neurology. 2000; 54(3):647-53. DOI: 10.1212/wnl.54.3.647. View

Langlois J, Kegler S, Butler J, Gotsch K, Johnson R, Reichard A . Traumatic brain injury-related hospital discharges. Results from a 14-state surveillance system, 1997. MMWR Surveill Summ. 2003; 52(4):1-20. View

10.

Wilde E, Hunter J, Newsome M, Scheibel R, Bigler E, Johnson J . Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. J Neurotrauma. 2005; 22(3):333-44. DOI: 10.1089/neu.2005.22.333. View

11.

Levine B, Kovacevic N, Nica E, Cheung G, Gao F, Schwartz M . The Toronto traumatic brain injury study: injury severity and quantified MRI. Neurology. 2008; 70(10):771-8. DOI: 10.1212/01.wnl.0000304108.32283.aa. View

12.

Dinov I, Van Horn J, Lozev K, Magsipoc R, Petrosyan P, Liu Z . Efficient, Distributed and Interactive Neuroimaging Data Analysis Using the LONI Pipeline. Front Neuroinform. 2009; 3:22. PMC: 2718780. DOI: 10.3389/neuro.11.022.2009. View

13.

Coles J, Fryer T, Smielewski P, Rice K, Clark J, Pickard J . Defining ischemic burden after traumatic brain injury using 15O PET imaging of cerebral physiology. J Cereb Blood Flow Metab. 2004; 24(2):191-201. DOI: 10.1097/01.WCB.0000100045.07481.DE. View

14.

Ng K, Mikulis D, Glazer J, Kabani N, Till C, Greenberg G . Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Arch Phys Med Rehabil. 2008; 89(12 Suppl):S35-44. DOI: 10.1016/j.apmr.2008.07.006. View

15.

Yount R, Raschke K, Biru M, Tate D, Miller M, Abildskov T . Traumatic brain injury and atrophy of the cingulate gyrus. J Neuropsychiatry Clin Neurosci. 2002; 14(4):416-23. DOI: 10.1176/jnp.14.4.416. View

16.

MacKenzie J, Siddiqi F, Babb J, Bagley L, Mannon L, Sinson G . Brain atrophy in mild or moderate traumatic brain injury: a longitudinal quantitative analysis. AJNR Am J Neuroradiol. 2002; 23(9):1509-15. PMC: 7976797. View

17.

Marcoux J, McArthur D, Miller C, Glenn T, Villablanca P, Martin N . Persistent metabolic crisis as measured by elevated cerebral microdialysis lactate-pyruvate ratio predicts chronic frontal lobe brain atrophy after traumatic brain injury. Crit Care Med. 2008; 36(10):2871-7. DOI: 10.1097/CCM.0b013e318186a4a0. View

18.

Bergsneider M, Hovda D, McArthur D, Etchepare M, Huang S, Sehati N . Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability. J Head Trauma Rehabil. 2001; 16(2):135-48. DOI: 10.1097/00001199-200104000-00004. View

19.

Kidwell C, Saver J, Mattiello J, Starkman S, Vinuela F, Duckwiler G . Thrombolytic reversal of acute human cerebral ischemic injury shown by diffusion/perfusion magnetic resonance imaging. Ann Neurol. 2000; 47(4):462-9. View

20.

Vespa P, Miller C, McArthur D, Eliseo M, Etchepare M, Hirt D . Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med. 2007; 35(12):2830-6. PMC: 4347945. View