American Journal of Neuroradiology 23:1356-1358, September 2002
© 2002 American Society of Neuroradiology
Case Report
BRAIN
Prominent Matched Hypoperfusion in an Intact Cerebellum after a Solitary Middle Cerebellar Peduncle Infarct
Masashi Takasawaa,b,
Kazuo Kitagawaa,b,
Toshiho Ohtsukia,b,
Naohiko Okua,c,
Kazuo Hashikawaa,c,
Saburo Sakodaa,
Masatsugu Horib and
Masayasu Matsumotoa,b
a Department of Neurology and Cerebrovascular Disease, Osaka University Hospital, Osaka, Japan
b Division of Strokology, Department of Internal Medicine and Therapeutics, Osaka University Graduate School of Medicine, Osaka, Japan
c Department of Nuclear Medicine, Osaka University Graduate School of Medicine, Osaka, Japan
Address reprint requests to Masashi Takasawa, MD, Division of Strokology, Department of Internal Medicine and Therapeutics, Osaka University Graduate School of Medicine, 2-2, Yamadaoka, Suita City, Osaka, 565-0871, Japan
 |
Abstract
|
|---|
Summary: We examined the cerebellar metabolism of a 61-year-old
man with a small infarct in the left middle cerebellar peduncle
and an intact cerebellum. Positron emission tomographic images
obtained 28 days after onset showed prominent hypoperfusion
and hypometabolism (almost 50% below the normal level) in the
left cerebellar hemisphere. This case report shows that neural
deafferentation may cause prominent hypometabolism without morphologic
changes in the cerebellum. An arrest in synaptic activity may
be the most important factor for the adaptive decrease in oxygen
metabolism seen in ischemic brain.
|
Introduction
|
|---|
Cerebral blood flow and oxygen metabolism can be measured by
using positron emission tomography (PET), thanks to the high
spatial resolution and accurate quantitation characteristics
of this technique. Intensive examination of patients with acute
stroke has shown that the threshold of oxygen metabolism required
for tissue survival in an ischemic condition is approximately
50% of the normal level (
1–
4). In other words, the brain
has an intrinsic adaptive mechanism against ischemic insults
that involves a reduction in oxygen metabolism. Cerebral vasodilatation
and an increased uptake of oxygen are well known to be adaptive
responses of the brain to a reduction in perfusion pressure
(
5,
6). However, the mechanism for the adaptive decrease in
oxygen metabolism has not been previously discussed. Because
a 50% reduction in oxygen metabolism in the surviving tissue
is unexpectedly high and almost identical to the effect of hypothermia
at 32°C (
7), the elucidation of this adaptive response is
important for improving our understanding of the pathophysiology
of acute stroke and the development of novel therapeutic strategies.
The disconnection of synaptic circuits may be an important component
of this mechanism, because electrical activity is arrested,
but energy metabolism is preserved in the penumbra tissue (
4,
8).
In humans, a reduction in oxygen metabolism without any morphologic change occurring after supratentorial infarction is known as crossed cerebellar diaschisis (9). This form of hypometabolism is presumably caused by an interruption in the cerebropontocerebellar pathway. Because the degree of oxygen metabolism reduction varies between 0 and 37% according to the size and location of the supratentorial infarction (10, 11), it remains uncertain to what degree the disconnection of synaptic circuits reduces oxygen metabolism in the intact brain. We had the opportunity to examine cerebellar circulation and metabolism in a case with a solitary middle cerebellar peduncle infarct, in which most afferent and efferent fibers to the cerebellum were disconnected.
|
Case Report
|
|---|
A 61-year-old, right-handed man suddenly presented with severe
gait unsteadiness and vomiting. Hypertension and impaired glucose
tolerance had been diagnosed when the patient was 50 years old,
but the patient did not undergo treatment. The diagnosis of
cerebellar infarction was made on the basis of neurologic findings
at another hospital. He was transferred to our hospital 3 weeks
after onset. A neurologic examination performed at admission
showed left-sided ataxia and ataxic speech. Both the nose-finger-nose
test and the pronation-supination test performances were clumsy
on the left side. No signs of ipsilateral facial palsy, hearing
loss, trigeminal sensory loss, or Horner syndrome were observed.
After admission, the neurologic findings did not deteriorate,
and the patient showed gradual improvement. Informed consent
to participate in this study was obtained from the patient and
his family.
An MR imaging examination was performed on the 24th day after onset and revealed an infarct in the left middle cerebellar peduncle (Fig 1, arrow), located within the territory of the anterior inferior cerebellar artery. MR diffusion- and perfusion-weighted images were not obtained. No definite infarcts were found in the cerebral hemisphere or the left cerebellar hemisphere on T1- or T2-weighted images. Cerebral angiography was not performed. MR angiography showed no definite stenosis and only slight atherosclerotic changes in the bilateral vertebral arteries and the basilar artery.
View larger version (54K):
[in this window]
[in a new window]
|
FIG 1. MR images obtained 24 days after symptom onset show an infarct strictly confined to the left middle cerebellar peduncle (arrow). No definite infarctions are visible in the cerebral hemisphere or the left cerebellar hemisphere on T2-weighted images. Rt., right; Lt., left.
| |
PET was performed by using a Headtome V scanner (Shimadzu Corp., Kyoto, Japan) on the 28th day after symptom onset. The PET examination was performed according to steady-state methods by using 15O-labeled gases. Regional cerebral blood flow, cerebral metabolic oxygen rate, cerebral blood volume, and oxygen extraction fraction were measured. Circular regions of interest, 20 mm in diameter, were placed on the cerebellar hemispheres in the PET images.
The PET images showed severe hypoperfusion (right, 68.9 mL/100 mg/min; left, 35.7 mL/100 mg/min) (Fig 2, arrows) and hypometabolism (right, 4.45 mL/100 mg/min; left, 2.75 mL/100 mg/min) (Fig 2, arrowheads) in the left cerebellar hemisphere. Elevated oxygen extraction fraction values, which have been shown in cases of misery perfusion (5), were not observed in bilateral cerebellar hemispheres (right, 38.6%; left, 40.5%). The standard PET parameters in the cerebelli of normal controls examined at our hospital’s PET center are 63 ± 6.5 mL/100 mg/min for cerebral blood flow (mean ± SD), 4.3 ± 0.6 mL/100 mg/min for cerebral metabolic oxygen rate, and 46 ± 4.0% for oxygen extraction fraction in a cerebellar hemisphere.
View larger version (60K):
[in this window]
[in a new window]
|
FIG 2. Positron emission tomographic images obtained 28 days after symptom onset show severe hypoperfusion (arrows) and oxygen hypometabolism (arrowheads) in the left cerebellar hemisphere. CBF, cerebral blood flow; CMRO2, cerebral metabolic oxygen rate.
| |
|
Discussion
|
|---|
Quantitative cerebral blood flow mapping by using PET has revealed
the remote effects of focal cerebral lesions in humans. The
phenomenon of cerebellar hypoperfusion and hypometabolism occurring
after supratentorial infarction, termed
crossed cerebellar diaschisis,
occurs via the cerebropontocerebellar pathway and was first
described by Baron et al (
9).
The cerebellum is linked to other parts of the brain by numerous efferent and afferent fibers that are grouped together on each side of the cerebellum into three peduncles. The middle cerebellar peduncle is the largest of the three peduncles and arises from the posterolateral region of the pons; it consists of the transverse fibers of the pons, which arise from the neurons of the pontine nuclei (12). In our patient, the interception of most efferent and afferent fibers of the cerebellar hemisphere by a middle cerebellar peduncle infarct resulted in profound hypoperfusion (almost 50% lower than the nonaffected cerebellar hemisphere) and profound hypometabolism (almost 40% lower), without any signs of morphologic change. The severity of this hypoperfusion and hypometabolism was greater than that reported previously regarding human study participants and was almost the same as the ischemic reversible threshold (4, 6, 13).
In cases of acute stroke, PET studies have been used to document the existence of a penumbra (4, 14) in which the electrocorticogram and evoked potentials vanish but the membrane potential and energy metabolism are maintained (4, 8). In this penumbra, ischemic tissue can survive for several hours under conditions of reduced oxygen consumption (almost 50% of normal) and recovers if adequate recirculation occurs (4). Surprisingly, the maximum level of oxygen consumption suppression in the penumbra is nearly identical to that in the cerebellum in the presence of a solitary middle cerebellar peduncle infarct.
Disconnection of the efferent and afferent fibers to the cerebellum suppressed the level of oxygen metabolism by approximately 40% in the present study. These findings seem to agree with previous findings of autoradiography that entorhinotomy in experimental animals causes a 30% to 45% reduction in glucose metabolism in the hippocampus (15). Because the cerebral metabolic oxygen rate threshold for irreversible injury in the ischemic brain has been found to be approximately 40% to 50% of normal (16), the adaptive decrease in oxygen consumption in the penumbra may be ascribed to the disconnection of synaptic circuits, although other mechanisms, such as the inhibition of protein synthesis, could also preserve oxygen consumption (17).
|
Conclusion
|
|---|
The mechanism by which EEG and electrical activity is suppressed
remains uncertain, but suppression of the conduction action
potential in the axons of afferent fibers under ischemic conditions
(
18) may be important for functional depression. The present
study suggests that disconnection of the synaptic circuit into
the ischemic brain may further reduce the cerebral metabolic
oxygen rate threshold for irreversible injury.
|
Acknowledgments
|
|---|
The authors thank the staff of the Department of Nuclear Medicine
and the Cyclotron staff of Osaka University Medical School Hospital
for technical support in performing the studies and R. Morimoto
and S. Imoto for administrative assistance.
|
References
|
|---|
- Baron JC, Rougemont D, Bousser MG, Lebrun-Grandie P, Iba-Zizen MT, Chiras J. Local CBF, oxygen extraction fraction (OEF), and CMRO2: prognostic value in recent supratentorial infarction in humans.
J Cereb Blood Flow Metab1983; 3[suppl 1]
:S1
–S2
- Powers WJ, Grubb RL Jr, Darriet D, Raichle ME. Cerebral blood flow and cerebral metabolic rate of oxygen requirements for cerebral function and viability in humans.
J Cereb Blood Flow and Metab1985; 5
:600
–608[Medline]
- Ackerman RH, Lev MH, Mackay BC, et al. PET studies in acute stroke: findings and relevance to therapy.
J Cereb Blood Flow Metab1989; 9[suppl 1]
:S359
- Heiss WD. Ischemic penumbra: evidence from functional imaging in man.
J Cereb Blood Flow Metab2000; 20
:1276
–1293[Medline]
- Baron JC, Bousser MG, Rey A, Guillard A, Comar D, Castaigne P. Reversal of focal "misery-perfusion syndrome" by extra-intracranial arterial bypass in hemodynamic cerebral ischemia.
Stroke1981; 12
:454
–459[Abstract/Free Full Text]
- Powers WJ, Press AW, Grubb RL Jr, Gado M, Raichle ME. The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation.
Ann Intern Med1987; 106
:27
–35
- Metz C, Holzschuh M, Bein T, et al. Moderate hypothermia in patients with severe head injury: cerebral and extracerebral effects.
J Neurosurg1996; 85
:533
–541[Medline]
- Baron JC. Perfusion thresholds in human cerebral ischemia: historical perspective and therapeutic implications.
Cerebrovasc Dis2001; 11[suppl 1]
:2
–8
- Baron JC, Bousser MG, Comar D, Castaigne P. "Crossed cerebellar diaschisis" in human supratentorial brain infarction.
Trans Am Neurol Assoc1980; 105
:459
–461
- Martin WR, Raichle ME. Cerebellar blood flow and metabolism in cerebral hemisphere infarction.
Ann Neurol1983; 14
:168
–176[Medline]
- Pantano P, Baron JC, Samson Y, Bousser MG, Derouesne C, Comar D. Crossed cerebellar diaschisis: further studies.
Brain1986; 109
:677
–694[Abstract/Free Full Text]
- Carpenter MB, Sutin J. The cerebellum. In: Carpenter MB, Sutin J, eds.
Human Neuroanatomy. 8th ed. Baltimore: Lippincott William & Wilkins;1983
:474
–492
- Heiss WD, Kracht L, Grond M, et al. Early [11C] flumazenil/H2O positron emission tomography predicts irreversible ischemic cortical damage in stroke patients receiving acute thrombolytic therapy.
Stroke2000; 31
:366
–369[Abstract/Free Full Text]
- Astrup J, Siesjo BK, Symon L. Thresholds in cerebral ischemia - the ischemic penumbra.
Stroke1981; 12
:723
–725[Free Full Text]
- Jorgenesen MB, Wright DC. The effect of unilateral and bilateral removal of the entorhinal cortex on the glucose utilization in various hippocampal regions in the rat.
Neurosci Lett1988; 87
:227
–232[Medline]
- Enblad P, Frykholm P, Valtysson J, et al. Middle cerebral artery occlusion and reperfusion in promates monitored by microdialysis and sequential positron emission tomography.
Stroke2001; 32
:1574
–1580[Abstract/Free Full Text]
- Hossmann KA. Viability thresholds and the penumbra of focal ischemia.
Ann Neurol1994; 36
:557
–565[Medline]
- Stys PK. Anoxic and ischemic injury of myelinated axons in CNS white matter: from mechanistic concepts to therapeutics.
J Cereb Blood Flow Metab1998; 18
:2
–25[Medline]
Received August 20, 2002;
accepted after revision March 18, 2002.
TOP
Abstract
Introduction