Skip to main content
Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging 7/2006

01.07.2006 | Original article

Loss of neuronal integrity: a cause of hypometabolism in patients with traumatic brain injury without MRI abnormality in the chronic stage

verfasst von: Tohru Shiga, Katsunori Ikoma, Chietsugu Katoh, Hirotaka Isoyama, Tetsuaki Matsuyama, Yuji Kuge, Hiroyuki Kageyama, Tomoya Kohno, Satoshi Terae, Nagara Tamaki

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 7/2006

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Traumatic brain injury (TBI) causes brain dysfunction in many patients. However, some patients have severe brain dysfunction but display no abnormalities on magnetic resonance imaging (MRI). There have been some reports of hypometabolism even in such patients. The purpose of this study was to investigate the relationship between metabolic abnormality and loss of neuronal integrity in TBI patients with some symptoms but without MRI abnormalities.

Methods

The study population comprised ten patients with TBI and ten normal volunteers. All of the patients were examined at least 1 year after the injury. 15O-labelled gas PET and [11C]flumazenil (FMZ) positron emission tomography (PET) were carried out. The cerebral metabolic rate of oxygen (CMRO2) and binding potential (BP) images of FMZ were calculated. Axial T2WI, T2*WI and FLAIR images were obtained. Coronal images were added in some cases.

Results

All of the patients had normal MRI findings, and all showed areas with abnormally low CMRO2. Low uptake on BP images was observed in six patients (60%). No lesions that showed low uptake on BP images were without low CMRO2. On the other hand, there were 14 lesions with low CMRO2 but without BP abnormalities.

Conclusion

These results indicate that there are metabolic abnormalities in TBI patients with some symptoms after brain injury but without abnormalities on MRI. Some of the hypometabolic lesions showed low BP, indicating a loss of neuronal integrity. Thus, FMZ PET may have potential to distinguish hypometabolism caused by neuronal loss from that caused by other factors.
Literatur
1.
Zurück zum Zitat Thurman D, Guerrero J. Trends in hospitalization associated with traumatic brain injury. JAMA 1999;282(10):954–7CrossRefPubMed Thurman D, Guerrero J. Trends in hospitalization associated with traumatic brain injury. JAMA 1999;282(10):954–7CrossRefPubMed
2.
Zurück zum Zitat Sander AM, Kreutzer JS, Rosenthal M, Delmonico R, Young ME. A multicenter longitudinal investigation of return to work and community integration following traumatic brain injury. J Head Trauma Rehabil 1996;11:70–84CrossRef Sander AM, Kreutzer JS, Rosenthal M, Delmonico R, Young ME. A multicenter longitudinal investigation of return to work and community integration following traumatic brain injury. J Head Trauma Rehabil 1996;11:70–84CrossRef
3.
Zurück zum Zitat Maziere M, Prenant C, Sastre J, Crouzel M, Comar D, Hantraye P, et al. 11C-R[O-15]-1788 et 11C-flunitrazepam, deux coordinats pour l’etude par tomographie par positons des sites de liaison des benzodiazepines. C R Seances Acad Sci III 1983;296(18):871–6PubMed Maziere M, Prenant C, Sastre J, Crouzel M, Comar D, Hantraye P, et al. 11C-R[O-15]-1788 et 11C-flunitrazepam, deux coordinats pour l’etude par tomographie par positons des sites de liaison des benzodiazepines. C R Seances Acad Sci III 1983;296(18):871–6PubMed
4.
Zurück zum Zitat Haglund MM, Berger MS, Kunkel DD, Franck JE, Ghatan S, Ojemann GA. Changes in gamma-aminobutyric and somatostatin in epileptic cortex associated with low-grade gliomas. J Neurosurg 1992;77:209–16PubMedCrossRef Haglund MM, Berger MS, Kunkel DD, Franck JE, Ghatan S, Ojemann GA. Changes in gamma-aminobutyric and somatostatin in epileptic cortex associated with low-grade gliomas. J Neurosurg 1992;77:209–16PubMedCrossRef
5.
Zurück zum Zitat Wolf HK, Roos D, Blumcke I, Pietsch T, Wiestler OD. Perilesional neurochemical changes in focal epilepsies. Acta Neuropathol (Berl) 1996;91:376–84CrossRef Wolf HK, Roos D, Blumcke I, Pietsch T, Wiestler OD. Perilesional neurochemical changes in focal epilepsies. Acta Neuropathol (Berl) 1996;91:376–84CrossRef
6.
Zurück zum Zitat Rudolf J, Sobesky J, Grond M, Heiss WD. Identification by positron emission tomography of neuronal loss in acute vegetative state. Lancet 2000;355(9198):115–6CrossRefPubMed Rudolf J, Sobesky J, Grond M, Heiss WD. Identification by positron emission tomography of neuronal loss in acute vegetative state. Lancet 2000;355(9198):115–6CrossRefPubMed
7.
Zurück zum Zitat Nakagawara J, Sperling B, Lassen NA. Incomplete brain infarction of reperfused cortex may be quantitated with iomazenil. Stroke 1997;28(1):124–32PubMed Nakagawara J, Sperling B, Lassen NA. Incomplete brain infarction of reperfused cortex may be quantitated with iomazenil. Stroke 1997;28(1):124–32PubMed
8.
Zurück zum Zitat Heiss WD, Graf R, Wienhard K. Relevance of experimental ischemia in cats for stroke management: a comparative reevaluation. Cerebrovasc Dis 2001;11(2):73–81CrossRefPubMed Heiss WD, Graf R, Wienhard K. Relevance of experimental ischemia in cats for stroke management: a comparative reevaluation. Cerebrovasc Dis 2001;11(2):73–81CrossRefPubMed
9.
Zurück zum Zitat Heiss WD, Kracht LW, Thiel A, Grond M, Pawlik G. Penumbral probability thresholds of cortical flumazenil binding and blood flow predicting tissue outcome in patients with cerebral ischaemia. Brain 2001;124(Pt 1):20–9CrossRefPubMed Heiss WD, Kracht LW, Thiel A, Grond M, Pawlik G. Penumbral probability thresholds of cortical flumazenil binding and blood flow predicting tissue outcome in patients with cerebral ischaemia. Brain 2001;124(Pt 1):20–9CrossRefPubMed
10.
Zurück zum Zitat Heiss WD, Kracht L, Grond M, Rudolf J, Bauer B, Wienhard K, et al. Early [11C]flumazenil/H2O positron emission tomography predicts irreversible ischemic cortical damage in stroke patients receiving acute thrombolytic therapy. Stroke 2000;31(2):366–9PubMed Heiss WD, Kracht L, Grond M, Rudolf J, Bauer B, Wienhard K, et al. Early [11C]flumazenil/H2O positron emission tomography predicts irreversible ischemic cortical damage in stroke patients receiving acute thrombolytic therapy. Stroke 2000;31(2):366–9PubMed
11.
Zurück zum Zitat Heiss WD, Grond M, Thiel A, Ghaemi M, Sobesky J, Rudolf J, et al. Permanent cortical damage detected by flumazenil positron emission tomography in acute stroke. Stroke 1998;29(2):454–61PubMed Heiss WD, Grond M, Thiel A, Ghaemi M, Sobesky J, Rudolf J, et al. Permanent cortical damage detected by flumazenil positron emission tomography in acute stroke. Stroke 1998;29(2):454–61PubMed
12.
Zurück zum Zitat Kuroda S, Shiga T, Ishikawa T, Houkin K, Narita T, Katoh C, et al. Reduced blood flow and preserved vasoreactivity characterize oxygen hypometabolism due to incomplete infarction in occlusive carotid artery diseases. J Nucl Med 2004;45(6):943–9PubMed Kuroda S, Shiga T, Ishikawa T, Houkin K, Narita T, Katoh C, et al. Reduced blood flow and preserved vasoreactivity characterize oxygen hypometabolism due to incomplete infarction in occlusive carotid artery diseases. J Nucl Med 2004;45(6):943–9PubMed
13.
Zurück zum Zitat Goshen E, Zwas ST, Shahar E, Tadmor R. The role of 99Tcm-HMPAO brain SPET in paediatric traumatic brain injury. Nucl Med Commun 1996;17(5):418–22PubMedCrossRef Goshen E, Zwas ST, Shahar E, Tadmor R. The role of 99Tcm-HMPAO brain SPET in paediatric traumatic brain injury. Nucl Med Commun 1996;17(5):418–22PubMedCrossRef
14.
Zurück zum Zitat Newton MR, Greenwood RJ, Britton KE, Charlesworth M, Nimmon CC, Carroll MJ, et al. A study comparing SPECT with CT and MRI after closed head injury. J Neurol Neurosurg Psychiatry 1992;55(2):92–4PubMedCrossRef Newton MR, Greenwood RJ, Britton KE, Charlesworth M, Nimmon CC, Carroll MJ, et al. A study comparing SPECT with CT and MRI after closed head injury. J Neurol Neurosurg Psychiatry 1992;55(2):92–4PubMedCrossRef
15.
Zurück zum Zitat Mattioli F, Grassi F, Perani D, Cappa SF, Miozzo A, Fazio F. Persistent post-traumatic retrograde amnesia: a neuropsychological and (18F)FDG PET study. Cortex 1996;32(1):121–9PubMed Mattioli F, Grassi F, Perani D, Cappa SF, Miozzo A, Fazio F. Persistent post-traumatic retrograde amnesia: a neuropsychological and (18F)FDG PET study. Cortex 1996;32(1):121–9PubMed
16.
Zurück zum Zitat Adriaan AL, Susan PH. Simplified reference tissue model for PET receptor studies. Neuroimage 1996;4:153–8CrossRefPubMed Adriaan AL, Susan PH. Simplified reference tissue model for PET receptor studies. Neuroimage 1996;4:153–8CrossRefPubMed
17.
Zurück zum Zitat Shiga T, Morita K, Takano A, Katoh C, Nakamura F, Tsukamoto E, et al. Clinical advantages of interictal SPECT coregistered to magnetic resonance imaging in patients with epilepsy. Clin Nucl Med 2001;26(4):334–9CrossRefPubMed Shiga T, Morita K, Takano A, Katoh C, Nakamura F, Tsukamoto E, et al. Clinical advantages of interictal SPECT coregistered to magnetic resonance imaging in patients with epilepsy. Clin Nucl Med 2001;26(4):334–9CrossRefPubMed
18.
Zurück zum Zitat Wechsler D. Manual for the Wechsler adult intelligence scale-revised (WAIS-R). San Antonio, TX: The Psychological Corporation; 1981 Wechsler D. Manual for the Wechsler adult intelligence scale-revised (WAIS-R). San Antonio, TX: The Psychological Corporation; 1981
19.
Zurück zum Zitat Folstein MF, Folstein SE, McHugh PR: Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189–98CrossRefPubMed Folstein MF, Folstein SE, McHugh PR: Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189–98CrossRefPubMed
20.
Zurück zum Zitat Muller V, Saur D, Klutmann S, Weiller C, Rother J, Clausen M. Experience with 123I-iomazenil SPECT in acute cerebral infarction. Nucl Med Commun 2002;23(12):1191–6CrossRefPubMed Muller V, Saur D, Klutmann S, Weiller C, Rother J, Clausen M. Experience with 123I-iomazenil SPECT in acute cerebral infarction. Nucl Med Commun 2002;23(12):1191–6CrossRefPubMed
21.
Zurück zum Zitat Ohyama M, Senda M, Ishiwata K, Kitamura S, Mishina M, Ishii K, et al. Preserved benzodiazepine receptors in Alzheimer’s disease measured with [C-11] flumazenil PET and I-123 iomazenil SPECT in comparison with CBF. Ann Nucl Med 1999;13(5):309–15PubMed Ohyama M, Senda M, Ishiwata K, Kitamura S, Mishina M, Ishii K, et al. Preserved benzodiazepine receptors in Alzheimer’s disease measured with [C-11] flumazenil PET and I-123 iomazenil SPECT in comparison with CBF. Ann Nucl Med 1999;13(5):309–15PubMed
22.
Zurück zum Zitat Ryvlin P, Bouvard S, Le Bars D, Mauguiere F. Transient and falsely lateralizing flumazenil-PET asymmetries in temporal lobe epilepsy. Neurology 1999;53(8):1882–5PubMed Ryvlin P, Bouvard S, Le Bars D, Mauguiere F. Transient and falsely lateralizing flumazenil-PET asymmetries in temporal lobe epilepsy. Neurology 1999;53(8):1882–5PubMed
23.
Zurück zum Zitat Juhasz C, Nagy F, Muzik O, Watson C, Shah J, Chugani HT. [11C]Flumazenil PET in patients with epilepsy with dual pathology. Epilepsia 1999;40(5):566–74PubMed Juhasz C, Nagy F, Muzik O, Watson C, Shah J, Chugani HT. [11C]Flumazenil PET in patients with epilepsy with dual pathology. Epilepsia 1999;40(5):566–74PubMed
24.
Zurück zum Zitat Kaji T, Kuge Y, Yokota C, Tagaya M, Inoue H, Shiga T, et al. Characterisation of [123I]iomazenil distribution in a rat model of focal cerebral ischaemia in relation to histopathological findings. Eur J Nucl Med Mol Imaging 2004;31(1):64–70CrossRefPubMed Kaji T, Kuge Y, Yokota C, Tagaya M, Inoue H, Shiga T, et al. Characterisation of [123I]iomazenil distribution in a rat model of focal cerebral ischaemia in relation to histopathological findings. Eur J Nucl Med Mol Imaging 2004;31(1):64–70CrossRefPubMed
25.
Zurück zum Zitat Moriwaki H, Matsumoto M, Hashikawa K, Oku N, Ishida M, Seike Y, et al. [Evaluation of 123I-iomazenil SPECT in patients with ischemic cerebrovascular disease: comparative study with 123I-IMP SPECT]. Kaku Igaku 1996;33(6):587–97PubMed Moriwaki H, Matsumoto M, Hashikawa K, Oku N, Ishida M, Seike Y, et al. [Evaluation of 123I-iomazenil SPECT in patients with ischemic cerebrovascular disease: comparative study with 123I-IMP SPECT]. Kaku Igaku 1996;33(6):587–97PubMed
26.
Zurück zum Zitat Tsuchida T, Yonekura Y, Sadato N, Takahashi N, Yamamoto K, Ishii Y. Prediction of improvement of cerebral perfusion with I-123 iomazenil SPECT. Ann Nucl Med 1999;13(4):265–8PubMedCrossRef Tsuchida T, Yonekura Y, Sadato N, Takahashi N, Yamamoto K, Ishii Y. Prediction of improvement of cerebral perfusion with I-123 iomazenil SPECT. Ann Nucl Med 1999;13(4):265–8PubMedCrossRef
27.
Zurück zum Zitat Shiozaki T, Akai H, Taneda M, Hayakata T, Aoki M, Oda J, et al. Delayed hemispheric neuronal loss in severely head-injured patients. J Neurotrauma 2001;18(7):665–74CrossRefPubMed Shiozaki T, Akai H, Taneda M, Hayakata T, Aoki M, Oda J, et al. Delayed hemispheric neuronal loss in severely head-injured patients. J Neurotrauma 2001;18(7):665–74CrossRefPubMed
28.
Zurück zum Zitat Gentry LR, Godersky JC, Thompson B. MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. AJR Am J Roentgenol 1988;150(3):663–72PubMed Gentry LR, Godersky JC, Thompson B. MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. AJR Am J Roentgenol 1988;150(3):663–72PubMed
29.
Zurück zum Zitat Adams JH. Pathology of nonmissile head injury. Neuroimaging Clin North Am 1991;397–410 Adams JH. Pathology of nonmissile head injury. Neuroimaging Clin North Am 1991;397–410
30.
Zurück zum Zitat Raghupathi R, Conti AC, Graham DI, Krajewski S, Reed JC, Grady MS, et al. Mild traumatic brain injury induces apoptotic cell death in the cortex that is preceded by decreases in cellular Bcl-2 immunoreactivity. Neuroscience 2002;110(4):605–16CrossRefPubMed Raghupathi R, Conti AC, Graham DI, Krajewski S, Reed JC, Grady MS, et al. Mild traumatic brain injury induces apoptotic cell death in the cortex that is preceded by decreases in cellular Bcl-2 immunoreactivity. Neuroscience 2002;110(4):605–16CrossRefPubMed
31.
Zurück zum Zitat Son BC, Park CK, Choi BG, Kim EN, Choe BY, Lee KS, et al. Metabolic changes in pericontusional oedematous areas in mild head injury evaluated by 1H MRS. Acta Neurochir Suppl (Wien) 2000;76:13–6 Son BC, Park CK, Choi BG, Kim EN, Choe BY, Lee KS, et al. Metabolic changes in pericontusional oedematous areas in mild head injury evaluated by 1H MRS. Acta Neurochir Suppl (Wien) 2000;76:13–6
Metadaten
Titel
Loss of neuronal integrity: a cause of hypometabolism in patients with traumatic brain injury without MRI abnormality in the chronic stage
verfasst von
Tohru Shiga
Katsunori Ikoma
Chietsugu Katoh
Hirotaka Isoyama
Tetsuaki Matsuyama
Yuji Kuge
Hiroyuki Kageyama
Tomoya Kohno
Satoshi Terae
Nagara Tamaki
Publikationsdatum
01.07.2006
Verlag
Springer-Verlag
Erschienen in
European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 7/2006
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-005-0033-y

Weitere Artikel der Ausgabe 7/2006

European Journal of Nuclear Medicine and Molecular Imaging 7/2006 Zur Ausgabe