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(Stroke. 1997;28:584-587.)
© 1997 American Heart Association, Inc.

Articles

Specific Changes in Human Brain After Hypoglycemic Injury

Masayuki Fujioka, MD; Kazuo Okuchi, MD; Ken-Ichiro Hiramatsu, MD; Toshisuke Sakaki, MD; Syouji Sakaguchi, MD; Yoshinobu Ishii, MD

From the Departments of Neurosurgery (M.F., K.O., K.-I.H., T.S.) and Radiology (S.S.), Nara Medical University, and Department of Medicine, Keioh Hospital (Y.I.), Nara, Japan.

Correspondence to Masayuki Fujioka, MD, Department of Neurosurgery, Emergency and Critical Care Medical Center, Nara Prefectural Nara Hospital, 1-30-1, Hiramatsu-cho, Nara, 631, Japan. E-mail RXL00203{at}niftyserve.or.jp

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Very few reports are available on serial changes in the human brain after severe hypoglycemic injury. The aim of this study was to investigate sequential neuroradiological changes in brains of patients after hypoglycemic coma compared with those after cardiac arrest previously studied with the same methods.

Methods We repeatedly studied CT scans and MR images obtained at 1.5 T in four vegetative patients after profound hypoglycemia associated with diabetes mellitus.

Results In all patients, consecutive CT scans showed symmetrical, persistent low-density lesions with transient enhancement in the caudate and lenticular nuclei and transient enhancement in the cerebral cortex 7 to 14 days after onset. Serial MR images consistently revealed symmetrical lesions of persistent hyperintensity and hypointensity on T1- and T2-weighted images, respectively, in the caudate and lenticular nuclei, cerebral cortex, substantia nigra, and/or hippocampus from 8 days to 12 months after onset.

Conclusions Repeated MR images revealed specific lesions in the bilateral basal ganglia, cerebral cortex, substantia nigra, and hippocampus, which suggests the particular vulnerability of these areas to hypoglycemia in the human brain. We speculate that the localized lesions represent tissue degeneration, including some combination of selective neuronal death, proliferation of astrocytic glial cells, paramagnetic substance deposition, and/or lipid accumulation. The absence of localized hemorrhages on MR images in hypoglycemic encephalopathy is in marked contrast to the presence of regional minor hemorrhages in postischemic-anoxic encephalopathy.

Key Words: brain injuries • diabetes mellitus • heart arrest • hypoglycemia • magnetic resonance imaging

	Introduction

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Hypoglycemic coma induces a purely neuronal lesion of the neocortex (layers 2 and 3), the hippocampus (neurons in the subiculum and the CA1 region and granule cells at the crest of the dentate gyrus), and the dorsolateral crescent of the caudoputamen in rat brains.¹ The accumulation of excitatory amino acids, but not simply glucose starvation of the neuron, seems to play an important pathogenetic role.^{2 3} The experimental neurochemical and morphological changes in hypoglycemic brain damage differ from those in transient forebrain or global brain ischemia even though both insults affect the whole brain critically, leading to energy failure and selective neuronal death in certain areas vulnerable to each insult.⁴ In particular, intracellular acidosis accompanies cerebral ischemia but not hypoglycemia. Profound hypoglycemia causes tissue alkalosis resulting from the ammonia formation from deamination of amino acids, the consumption of metabolic acids, and the absence of lactic acid formation.²

In the human brain, we noted symmetrical lesions in the basal ganglia, thalami, and/or substantia nigra with minor hemorrhage on MR images after cardiac arrest.^{5 6} We also suggested the possibility of hyperglycemic, hyperosmotic cerebrovascular endothelial injury in a diabetic patient.⁷ However, very few reports are available on the serial changes in the human brain after severe hypoglycemic injury with coma. We investigated neuroradiological changes with time in the brains of patients who remained in a persistent vegetative state after hypoglycemic coma and compared the results with those of patients after cardiac arrest as previously studied using the same methods.⁶

	Subjects and Methods

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This study included subjects satisfying the following criteria: (1) no apparent history of diseases possibly influencing head MR images other than diabetes mellitus; (2) first and pure hypoglycemic coma (blood glucose level <2.5 mmol/L and no clinical or laboratory evidence of hypotension, hypothermia, hypoxia, acidosis, infection, intoxication, or epilepsy on admission); and (3) systemic condition sufficiently stable to withstand multiple neuroimaging studies without any cardiorespiratory dysfunction or seizure activity. We encountered four such patients at Nara Medical University Hospital or affiliated institutions during the period December 1994 to January 1996 (Table). Persistent vegetative state was diagnosed in accordance with the published criteria of the American Neurological Association.⁸

View this table: [in this window] [in a new window]   Table 1. Clinical Features of Four Patients With Transient Profound Hypoglycemia

CT scanning was performed with 10-mm cuts displayed on a 512x512 matrix. All patients underwent precontrast CT scanning daily for the first 3 days (days 1 through 3) and thereafter repeatedly every 2 to 10 days for 4 months after onset and at given times between 5 and 12 months. Postcontrast CT scanning was performed in all patients every 3 to 10 days for the first 2 months. MRI at 1.5 T was performed twice per patient. The timing of MRI is indicated in Fig 1. Axial and coronal T1- and T2-weighted sequences were obtained with the use of a spin-echo technique (repetition time [TR]=500 or 200 ms and echo time [TE]=20 ms for the short TR/TE images; TR=2000 ms and TE=100 ms for the long TR/TE images). Other imaging parameters included 5- or 7-mm slice thickness without an intersection gap, matrix size 256x256 or 192x256, and 25-cm field of view.

View larger version (62K): [in this window] [in a new window]   Figure 1. Specific changes with time on MRI; serial changes on high-field MR images in each patient. These specific changes in the bilateral basal ganglia, cerebral cortex, substantia nigra, and hippocampus are considered to reflect tissue degeneration, including some combination of selective neuronal death, proliferation of astrocytic glial cells, paramagnetic substance deposition, and/or lipid accumulation but not infarct (pannecrosis) or hemorrhage. T1WI indicates T1-weighted image; T2WI, T2-weighted image.

	Results

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Both the CT scans and MR images of our patients illustrated unique changes with time in the basal ganglia, cerebral cortex, hippocampus, and substantia nigra bilaterally (Table, Figs 1 and 2). Sequential CT scans showed symmetrical, persistent low-density lesions with transient enhancement in the caudate and lenticular nuclei and transient enhancement of the cerebral cortex predominantly in the parietal and occipital regions 7 to 14 days after onset in all cases (Table, Fig 2). Fig 1 shows the serial changes on high-field MR images in each patient. The most common pattern was consistent hyperintensity and hypointensity on both initial and second T1- and T2-weighted images, respectively, in the bilateral caudate and lenticular nuclei, cerebral cortex, substantia nigra, and hippocampus. The cerebral cortex lesions appeared in laminar form and were most conspicuous in the insular and parieto-occipital cortices. Serial CT scans and MR images showed diffuse brain edema in the acute stage (within 1 week of onset) in cases 1 and 4 and showed diffuse brain atrophy in the chronic stage (from 2 weeks to 12 months after onset) in all cases.

View larger version (86K): [in this window] [in a new window]   Figure 2. Patient 2. Postcontrast CT scans obtained on day 10 (A, B) reveal enhanced lesions in the bilateral occipital and parietal cerebral cortices. MR images on days 18 (C, D, E, F, G) and 50 (H, I, J, K, L) show persistent hyperintense and hypointense lesions on T1-weighted (C, E, G, H, I, K) and T2-weighted (D, F, J, L) images, respectively, in the bilateral caudate and lenticular nuclei, cerebral cortices (E, G, H; arrows), and substantia nigra (K, L; arrows) and show hypointensity and hyperintensity in the bilateral hippocampus (C, D, G, K, L).

	Discussion

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To the best of our knowledge, this is the first study in which multiple CT scanning and high-field MRI were used to focus on chronological changes in the brain of patients who remained in a persistent vegetative state after hypoglycemic coma.

Hypoglycemic Encephalopathy
Hypoglycemic insult predominantly affects cerebral gray matter, as noted in previous CT studies.⁹ MRI has been studied in detail in only two cases of transient profound hypoglycemia followed by severe amnesia.^{10 11} Chalmers et al¹⁰ and Boeve et al¹¹ showed MR image abnormalities of hyperintensity on only T1- or T2-weighted images in the hippocampus and temporal and occipital gray matter but not in the caudate and lenticular nuclei or substantia nigra.

The present neuroradiological data can be interpreted as follows. First, specific and symmetrical hypoglycemic brain damage was demonstrated neuroradiologically in the human brain after hypoglycemic coma. Second, these hypoglycemic lesions were shown to be distributed bilaterally in the basal ganglia, hippocampus, cerebral cortex, and/or substantia nigra but not in the thalamus, suggesting the particular vulnerability or resistance of individual areas in the human brain to hypoglycemia. Third, the localized hypoglycemic lesions of persistent hyperintensity and hypointensity on serial T1- and T2-weighted high-field MR images, respectively, and of consistent low density on consecutive CT scans were neuroradiologically thought to represent tissue degeneration, including some possible combination of selective neuronal loss,^{2 12} proliferation of astrocytic glial cells,¹² paramagnetic substance deposition,¹³ and/or lipid accumulation.¹⁴

The specific lesions on serial CT and MR images noted in our patients appear unlikely to represent the following three entities neuroradiologically. (1) Nonhemorrhagic cerebral infarcts of all ages exhibit hypointensity and hyperintensity on T1- and T2-weighted images, respectively, relative to normal parenchyma.¹⁵ (2) The signal intensity of hemorrhagic brain tissue changes with time according to the process of hemoglobin degradation.¹⁶ (3) Ectopic calcifications appear hyperintense and hypointense on T1- and T2-weighted MR images, respectively, but as high-density lesions on CT scans.¹⁷ These findings are in agreement with several animal and human pathological studies in which uncomplicated, profound hypoglycemia with coma resulted in selective neuronal loss and astrogliosis without infarcts or vascular lesions in the hippocampus, basal ganglia, and cerebral cortex.^{1 2 12 18} Only histological examination, however, would resolve this issue.

Comparison With Post–Cardiac Arrest Encephalopathy
We previously studied eight vegetative patients resuscitated from cardiac arrest using multiple CT scanning and high-field MRI at 1.5 T.⁶ In seven of the eight patients, consecutive CT scans showed symmetrical, persistent low-density lesions in the bilateral caudate, lenticular, and/or thalamic nuclei 2 to 6 days following reperfusion after cardiac arrest. However, MR images demonstrated minor hemorrhages localized in these areas and/or substantia nigra.

Our neuroradiological studies suggest two major differences between hypoglycemic and ischemic encephalopathies: (1) serial MR images showed minor hemorrhages in the localized lesions of ischemic encephalopathy but not of hypoglycemic encephalopathy, and (2) symmetrical thalamic lesions of abnormal intensity on CT and MR images exist in post–cardiac arrest encephalopathy but seem absent in hypoglycemic encephalopathy. The mechanisms underlying these differences could not be elucidated precisely by our study, but we speculate that differences in the mechanisms of selective damage exist between transient hypoglycemic and ischemia/reperfusion injuries in the human brain.

We think that tissue acidosis leading to alterations of cerebrovascular permeability is definitively related to minor hemorrhages on MR images observed in ischemic but not hypoglycemic brain injuries. Intracellular acidosis appears to contribute to cell death¹⁹ and leads to a poor outcome in patients after cardiopulmonary resuscitation.²⁰ The inability to produce lactic acid during hypoglycemia is thought to account for the fact that infarction is not seen in controlled experimental conditions producing a pure hypoglycemic insult to the brain.¹ Öztas et al²¹ reported that normothermic hypoglycemia in rats resulted in few cases of any noticeable increase in blood-brain barrier permeability and that their light microscopic study detected no significant bleeding. Recently, Kristián et al¹⁸ reported that, although pure hypoglycemia causes a "nonvascular" lesion, the lesion is aggravated by acidosis and transformed into infarction accompanied by perivascular erythrocytes in the caudoputamen. The precise mechanism leading to thalamic lesions in ischemic encephalopathy but not in hypoglycemic coma remains unclear. The present result is, however, consistent with several animal experiments that demonstrate prominent neuronal destruction in the nucleus reticularis thalami in the rat after cardiac arrest but no cell necrosis in the thalamus after hypoglycemic brain damage.^{1 22 23} The following factors may be related to the result in our studies that thalamic lesions exist in ischemic encephalopathy but not in hypoglycemic coma. First, excitatory amino acids in neurotransmitter mechanisms are implicated in the development of both ischemic and hypoglycemic brain damage.⁴ However, the predominant release of aspartate into the extracellular fluid in hypoglycemia differs from the rise in extracellular glutamate in ischemia.^{3 4} Second, unlike ischemia, energy failure is only moderate during hypoglycemia because of the remaining glucose supply and oxidation of endogenous nonglucose fuels by the brain.⁴ In particular, after 30 minutes of hypoglycemia, the ATP level is much higher in the thalamus (45% of control values) than in the cerebral cortex (23%), striatum (27%), and hippocampus (17%) in rats.²² This heterogeneous regional ATP level also may be related to the absence of thalamic lesions in hypoglycemia.

	Acknowledgments

 
We thank T. Taoka, MD, Y. Nishimura, MD, and Y. Imai, MD, for thoughtful neuroradiological comments and great assistance. We are grateful to K. Fujioka and M. Onoue for their secretarial help.

Received July 19, 1996; revision received November 21, 1996; accepted November 21, 1996.

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