] Stroke Cerebropasc Dis 1992;2:240-243
© 1992 National Stroke Association
Recovery of Cortical Blood Flow and Dementia After Superficial Temporal-Middle Cerebral Artery Bypass in a Patient with Severe Carotid Occlusive Lesions: A Two-Year Follow-Up Study 'Yoshiyasu Tsuda, 3K. Yamada, 3T. Hayakawa, IF. Hirakawa, 'Y, Ayada, 2M. Ohkawa, 2M. Tanabe, and IH. Matsuo
The effect of superficial temporal-middle cerebral artery (ST-MCA) bypass for enhancing cerebral circulation is controversial (1-3), and its prophylactic effect is questioned by the cooperative study (4). We studied a patient who had hemodynamically severe occlusive lesions of the left carotid artery, presenting with several transient ischemic attacks (TIAs) accompanied by dementia prior to the bypass surgery. After the bypass, he showed improved cortical flow, cognitive ability, and disappearance of neurological deficits.
Case Report A 58-year-old man who had had two TIAs in 3 years presented with right hemiparesis, right-hand hypesthesia, and dysarthria of 7 hand 12 h duration, respectively. Two months prior to admission, he had experienced a transient episode of right-hand tremor with motor aphasia. Subsequently, he developed disorientation and disturbances of memory and cognition that were noted by his wife. At admission, he
From the ISecond Department of Internal Medicine and 2Department of Radiology, Kagawa Medical School, Miko-cho, Kagawa, and the 3Department of Neurosurgery, Osaka University Medical School, Osaka, Japan. Presented at the 16th Salzburg Conference of the Cerebrovascular Research Group of the World Federation of Neurology, which was a satellite symposia of the Second World Congress of Stroke sponsored by the International Stroke Society, Washington, DC, September 8-12,1992. Address correspondence and reprint requests to Dr. Y. Tsuda at Second Department of Internal Medicine, Kagawa Medical School, 1750-1 Ikenobe, Miko-cho, Kagawa 761-07, Japan . 240
/ STROKE CEREBROVASCDIS, VOL. 2, NO.4, 1992
complained of right-hand hypesthesia and dysarthria, presenting cognitive impairments with memory disturbances, disorientation, and dyscalculia.
Diagnostic Evaluation The patient was examined by computed tomography (CT), 1.5-T magnetic resonance imaging (MRI) (Gyroscan SIS, Philips), and carotid angiography. The regional cerebral blood flow (rCBF) was evaluated preoperatively, and 2, 9, and 20 months postoperatively by 1231 N-isopropyl-p-iodoamphetamine (IMP) single-photon emission computed tomography (SPECT) using a rotating scintillation camera (GCA-90B, Toshiba, Japan) equipped with a LEGP collimator (full width at half maximum was 12.4 mm) sampled for 20-30 min after intravenous injection of 222 MBq IMP.
Mental Ability Evaluations The mental abilities of the patient were evaluated preoperatively, 0, 1.5, and 20 months postoperatively, using the dementia rating scale of Hasegawa et al. (5) (HDRS). This dementia rating scale is a useful bedside method of scoring cognitive impairment and consists of six subtests to measure orientation (7.5 points), recent and remote memories (8.0 points), general information (5.5 points), calculation (4.0 points), memory recall (4.0 points), and memorization (3.5 points). The maximum score is 32.5 points, with scores less than 20.0 points reflecting cognitive impairment (6).
16th SALZBURGCONFERENCE
Figure 1. Pre- (left) alldpostoperative (right) bilateral carotid allgiography of the patient.
R
Preop erative Stlldy Carotid angiography showed the left carotid siphon occlusion (shown by a large arrow in Fig. 1, left), accompanying a stenosis at the stem of the left anterior cerebral artery (shown by a small arrow in Fig. 1, left), with collaterals from the anterior communicating artery. CT (Fig. 2a) and T2-weighted MRIs (Fig. 2b, up-
per part) showed left temporo-occipital borderzone infarction. In addition, the Tl-weighted MRIs at day 18 post-onset showed an enhanced small lesion with Gd-DTPA at the left periventriculum, suggesting an occurrence of recent cerebral. infarction (Fig. 2b, lower part). The rCBF images by 123I_IMP SPECT preoperatively showed an extensive hypoperfusion
Figure 2. A: Cl'scan ofday 3 post-TIAonset. B: MRIimages Ofday 18 afterollsetofTIAillthepatient (upper half, T2-weiglrted images; lowerhalf, Tl-uieighted images witll enhancement by Gd-DTPA).
J STROKECEREBROVASCDIS, VOL.2, NO.4,
1992
241
16111 SALZBURGCONFERENCE
Figure 3.
rCBF images by 12JI_IMP SPECTofthepatient. A: Preoperative. B: Two 1II0nl11s postoperative. C: Nine monthspostoperative.
D : Twenty-one months postoperative.
area in the left anterior-parietal cortex (Fig. 3A). The scores of HROS at days 3 and 5 post-onset showed apparent mental deterioration in this patient, i.e., 8.5 and 6.5 points, respectively, which mainly consisted of disturbances of orientation, calculation, memory recall, and memorization. There was a slight recovery at days 8 and 10, i.e., 10.5 and 17.0 points, respectively, although this was still under the normal range of more than 20.0 points (Fig. 4). Although the scores ofHORS improved spontaneously within normal ranges of more than 20.0 points,
:3 2 _5-1r--
-
-
-
-
-
i.e., from 17.0 to 28.5 points 2.5 months after onset, the patient was believed to have a good indication for ST-MCA bypass from the hemodynamic point of view, because the brain damage on CT and MRI was minimal, whereas collaterals via the anterior communicating artery were marginal due to a severe stenosis at the stem of the left anterior cerebral artery. In addition, an extensive hypoperfused area on rCBF was observed by 123I-IMP SPECT (Fig.3A). The hemodynamic instability in this patient was thought to be correctable. The bypass surgery was performed 3
-
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Figure 4. Sequential changes of tilescores on the dementia rating scale of Hasegawa (HDRS), sllOrtly after onsetand pre- and postoperatively in tile patient.
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J STROKECEREBROVASCDIS, VOL. 2, NO.4, 1992
II
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2 4
(after onse t)
16tlz SALZBURGCONFERENCE
weeks after the successful endarterectomy of an occlusive plaque at the stem of the left external carotid artery.
Postoperative Study After surgery, the patient's right-hand hypesthesia disappeared, and dysarthric speech became fluent. His orientation improved, and he could calculate well at this time . However, the HDRS scores worsened slightly from 28.5 preoperatively to 25.0 and 21.0 points, respectively, 0 and 1.5 months postoperatively (Fig. 4). Postoperative cerebral angiography showed a good filling into the left MCA from the ipsilateral superficial temporal artery (Fig. 1, right). CT and T2weighted MRI showed the left periventricular lesion, in addition to the lesion in the left temporo-occipital borderzone area. The rCBF images by 123I_IMP SPECT showed a gradual and good recovery of the blood flow in the left anteroparietal and parietotemporal cortex (shown by arrows in Figs. 3B, C, and 0, respectively), 2, 9,and 21 months postoperatively. Subsequently, the scores of HDRS returned to a maximum score of 32.5 points 20 months postoperatively (Fig. 4).
Discussion Although the necessity of the bypass surgery is still unclear in most cases-its prophylactic effect for the occurrence of subsequent cerebral infarction in particular being questioned by the cooperative study (4)- the improvement of rCBF after ST-MCA bypass has been reported in some studies (1-3). Baron et al. (1) reported a case with hemodynamic instability showing TIAs with blood pressure changes, which might have been an absolute indication for the bypass, considering the pre- and postoperative findings of rCBF and cerebral oxygen metabolism. In our 2year follow-up study, bypass surgery corrected the cognitive impairment, improved neurological deficits, and three-dimensional cortical blood flow without showing any worsened signs in a case with severe carotid occlusive lesions. Nielsen et al. (7) reported the improvement of neuropsychological abilities, i.e., verbal sequential thinking for repetition, verbal learning, and mental arithmetic, in patients with reversible
ischemic neurological deficit after the bypass surgery, particularly in the left-hemisphere patients, which was in accordance with the postoperative findings in our patient. The temporary mental deterioration in our patient, which was shown as slightly worsened scores of HDRS up to 1.5 months after the bypass, returned to a normal level 20 months after the operation . With respect to such a transient deterioration, Heros et al. (8) reported temporary neurological deteriorations, such as TIA or more prolonged deficits, which improved 2 weeks or more after the bypass. They speculated that hyperperfusion of chronically ischemic brain tissue and shifts in the watershed region resulting from the new flow pattern after the bypass were the etiology of these temporary deficits. This might explain the short-term temporary fluctuation of the HDRS scores observed in our patient.
References 1. Baron JC, Bousser MG, Rey A, Guillard A, Comar D, Castaigne P. Reversal of focal "misery-perfusion syn drome" by extra-intracranial arterial bypass in hemodynamic cerebral ischemia. A case study with 150 positron emission tomography. Stroke 1981;12:454-9. 2. Tsuda Y,Kimura K,Iwata Y,et al. Improvement of cerebral blood flow and/or CO 2 reactivity after superficial temporal artery-middle cerebral artery bypass in patients with transient ischemic attacks and watershedzone infarctions. Surg NellroI1984;22:595-604 . 3. Vorstrup S, Lassen NA, Henriksen L. et at CBF before and after extra cranial-intracranial bypass surgery in patients with ischemic cerebrovascular disease studied with I33Xe-inhalation tomography. Stroke 1985;16: 616-25. 4. The EC/IC Bypass Study Group. Failure of extracranialintracranial arterial bypa ss to reduce the risk of ischemic stroke. Results of an international randomized trial. N EllgIJ Med 1985;313 :1191-1200. 5. Hasegawa K, Inoue K, Moriya K. An investigation of dementia rating scale for the elderly. Seishin lgaku (Tokyo) 1974;16:965-9.
6. Fukuda H, Kobayashi S, Okada T, Tsunematsu T. Frontal white matter lesions and dementia in lacunar infarction . Stroke 1990;21 :1143-9. 7. Nielsen H, Hojer-Pederson E, Gulliksen G, Haase J, Enevoldsen E. Reversible ischemic neurological defecit and minor strokes before and after EC/IC bypass surgery. Acta Neurol Scand 1986;73 :615-8. 8. Heros RC, Scott RM, Kistler [P, Ackerman RH, Conner ES. Temporary neurological deterioration after extracranial-intracranial bypass. Neurosurgery 1984;15: 17885.
J STROKE CEREBROVASC DIS, VOL.2. NO.4, 1992
243
© 1992 National Stroke Association
Recovery of Cortical Blood Flow and Dementia After Superficial Temporal-Middle Cerebral Artery Bypass in a Patient with Severe Carotid Occlusive Lesions: A Two-Year Follow-Up Study 'Yoshiyasu Tsuda, 3K. Yamada, 3T. Hayakawa, IF. Hirakawa, 'Y, Ayada, 2M. Ohkawa, 2M. Tanabe, and IH. Matsuo
The effect of superficial temporal-middle cerebral artery (ST-MCA) bypass for enhancing cerebral circulation is controversial (1-3), and its prophylactic effect is questioned by the cooperative study (4). We studied a patient who had hemodynamically severe occlusive lesions of the left carotid artery, presenting with several transient ischemic attacks (TIAs) accompanied by dementia prior to the bypass surgery. After the bypass, he showed improved cortical flow, cognitive ability, and disappearance of neurological deficits.
Case Report A 58-year-old man who had had two TIAs in 3 years presented with right hemiparesis, right-hand hypesthesia, and dysarthria of 7 hand 12 h duration, respectively. Two months prior to admission, he had experienced a transient episode of right-hand tremor with motor aphasia. Subsequently, he developed disorientation and disturbances of memory and cognition that were noted by his wife. At admission, he
From the ISecond Department of Internal Medicine and 2Department of Radiology, Kagawa Medical School, Miko-cho, Kagawa, and the 3Department of Neurosurgery, Osaka University Medical School, Osaka, Japan. Presented at the 16th Salzburg Conference of the Cerebrovascular Research Group of the World Federation of Neurology, which was a satellite symposia of the Second World Congress of Stroke sponsored by the International Stroke Society, Washington, DC, September 8-12,1992. Address correspondence and reprint requests to Dr. Y. Tsuda at Second Department of Internal Medicine, Kagawa Medical School, 1750-1 Ikenobe, Miko-cho, Kagawa 761-07, Japan . 240
/ STROKE CEREBROVASCDIS, VOL. 2, NO.4, 1992
complained of right-hand hypesthesia and dysarthria, presenting cognitive impairments with memory disturbances, disorientation, and dyscalculia.
Diagnostic Evaluation The patient was examined by computed tomography (CT), 1.5-T magnetic resonance imaging (MRI) (Gyroscan SIS, Philips), and carotid angiography. The regional cerebral blood flow (rCBF) was evaluated preoperatively, and 2, 9, and 20 months postoperatively by 1231 N-isopropyl-p-iodoamphetamine (IMP) single-photon emission computed tomography (SPECT) using a rotating scintillation camera (GCA-90B, Toshiba, Japan) equipped with a LEGP collimator (full width at half maximum was 12.4 mm) sampled for 20-30 min after intravenous injection of 222 MBq IMP.
Mental Ability Evaluations The mental abilities of the patient were evaluated preoperatively, 0, 1.5, and 20 months postoperatively, using the dementia rating scale of Hasegawa et al. (5) (HDRS). This dementia rating scale is a useful bedside method of scoring cognitive impairment and consists of six subtests to measure orientation (7.5 points), recent and remote memories (8.0 points), general information (5.5 points), calculation (4.0 points), memory recall (4.0 points), and memorization (3.5 points). The maximum score is 32.5 points, with scores less than 20.0 points reflecting cognitive impairment (6).
16th SALZBURGCONFERENCE
Figure 1. Pre- (left) alldpostoperative (right) bilateral carotid allgiography of the patient.
R
Preop erative Stlldy Carotid angiography showed the left carotid siphon occlusion (shown by a large arrow in Fig. 1, left), accompanying a stenosis at the stem of the left anterior cerebral artery (shown by a small arrow in Fig. 1, left), with collaterals from the anterior communicating artery. CT (Fig. 2a) and T2-weighted MRIs (Fig. 2b, up-
per part) showed left temporo-occipital borderzone infarction. In addition, the Tl-weighted MRIs at day 18 post-onset showed an enhanced small lesion with Gd-DTPA at the left periventriculum, suggesting an occurrence of recent cerebral. infarction (Fig. 2b, lower part). The rCBF images by 123I_IMP SPECT preoperatively showed an extensive hypoperfusion
Figure 2. A: Cl'scan ofday 3 post-TIAonset. B: MRIimages Ofday 18 afterollsetofTIAillthepatient (upper half, T2-weiglrted images; lowerhalf, Tl-uieighted images witll enhancement by Gd-DTPA).
J STROKECEREBROVASCDIS, VOL.2, NO.4,
1992
241
16111 SALZBURGCONFERENCE
Figure 3.
rCBF images by 12JI_IMP SPECTofthepatient. A: Preoperative. B: Two 1II0nl11s postoperative. C: Nine monthspostoperative.
D : Twenty-one months postoperative.
area in the left anterior-parietal cortex (Fig. 3A). The scores of HROS at days 3 and 5 post-onset showed apparent mental deterioration in this patient, i.e., 8.5 and 6.5 points, respectively, which mainly consisted of disturbances of orientation, calculation, memory recall, and memorization. There was a slight recovery at days 8 and 10, i.e., 10.5 and 17.0 points, respectively, although this was still under the normal range of more than 20.0 points (Fig. 4). Although the scores ofHORS improved spontaneously within normal ranges of more than 20.0 points,
:3 2 _5-1r--
-
-
-
-
-
i.e., from 17.0 to 28.5 points 2.5 months after onset, the patient was believed to have a good indication for ST-MCA bypass from the hemodynamic point of view, because the brain damage on CT and MRI was minimal, whereas collaterals via the anterior communicating artery were marginal due to a severe stenosis at the stem of the left anterior cerebral artery. In addition, an extensive hypoperfused area on rCBF was observed by 123I-IMP SPECT (Fig.3A). The hemodynamic instability in this patient was thought to be correctable. The bypass surgery was performed 3
-
:3 I
./
oQ. 10.'
2 o-.-..;;:..---........-~-
I
Figure 4. Sequential changes of tilescores on the dementia rating scale of Hasegawa (HDRS), sllOrtly after onsetand pre- and postoperatively in tile patient.
10
T
,
d a Y 3
242
6.5 ~
I .
a
io
v,
It
2_5
I
.,...4
:
5-5
b ypas s
J STROKECEREBROVASCDIS, VOL. 2, NO.4, 1992
II
j
2 4
(after onse t)
16tlz SALZBURGCONFERENCE
weeks after the successful endarterectomy of an occlusive plaque at the stem of the left external carotid artery.
Postoperative Study After surgery, the patient's right-hand hypesthesia disappeared, and dysarthric speech became fluent. His orientation improved, and he could calculate well at this time . However, the HDRS scores worsened slightly from 28.5 preoperatively to 25.0 and 21.0 points, respectively, 0 and 1.5 months postoperatively (Fig. 4). Postoperative cerebral angiography showed a good filling into the left MCA from the ipsilateral superficial temporal artery (Fig. 1, right). CT and T2weighted MRI showed the left periventricular lesion, in addition to the lesion in the left temporo-occipital borderzone area. The rCBF images by 123I_IMP SPECT showed a gradual and good recovery of the blood flow in the left anteroparietal and parietotemporal cortex (shown by arrows in Figs. 3B, C, and 0, respectively), 2, 9,and 21 months postoperatively. Subsequently, the scores of HDRS returned to a maximum score of 32.5 points 20 months postoperatively (Fig. 4).
Discussion Although the necessity of the bypass surgery is still unclear in most cases-its prophylactic effect for the occurrence of subsequent cerebral infarction in particular being questioned by the cooperative study (4)- the improvement of rCBF after ST-MCA bypass has been reported in some studies (1-3). Baron et al. (1) reported a case with hemodynamic instability showing TIAs with blood pressure changes, which might have been an absolute indication for the bypass, considering the pre- and postoperative findings of rCBF and cerebral oxygen metabolism. In our 2year follow-up study, bypass surgery corrected the cognitive impairment, improved neurological deficits, and three-dimensional cortical blood flow without showing any worsened signs in a case with severe carotid occlusive lesions. Nielsen et al. (7) reported the improvement of neuropsychological abilities, i.e., verbal sequential thinking for repetition, verbal learning, and mental arithmetic, in patients with reversible
ischemic neurological deficit after the bypass surgery, particularly in the left-hemisphere patients, which was in accordance with the postoperative findings in our patient. The temporary mental deterioration in our patient, which was shown as slightly worsened scores of HDRS up to 1.5 months after the bypass, returned to a normal level 20 months after the operation . With respect to such a transient deterioration, Heros et al. (8) reported temporary neurological deteriorations, such as TIA or more prolonged deficits, which improved 2 weeks or more after the bypass. They speculated that hyperperfusion of chronically ischemic brain tissue and shifts in the watershed region resulting from the new flow pattern after the bypass were the etiology of these temporary deficits. This might explain the short-term temporary fluctuation of the HDRS scores observed in our patient.
References 1. Baron JC, Bousser MG, Rey A, Guillard A, Comar D, Castaigne P. Reversal of focal "misery-perfusion syn drome" by extra-intracranial arterial bypass in hemodynamic cerebral ischemia. A case study with 150 positron emission tomography. Stroke 1981;12:454-9. 2. Tsuda Y,Kimura K,Iwata Y,et al. Improvement of cerebral blood flow and/or CO 2 reactivity after superficial temporal artery-middle cerebral artery bypass in patients with transient ischemic attacks and watershedzone infarctions. Surg NellroI1984;22:595-604 . 3. Vorstrup S, Lassen NA, Henriksen L. et at CBF before and after extra cranial-intracranial bypass surgery in patients with ischemic cerebrovascular disease studied with I33Xe-inhalation tomography. Stroke 1985;16: 616-25. 4. The EC/IC Bypass Study Group. Failure of extracranialintracranial arterial bypa ss to reduce the risk of ischemic stroke. Results of an international randomized trial. N EllgIJ Med 1985;313 :1191-1200. 5. Hasegawa K, Inoue K, Moriya K. An investigation of dementia rating scale for the elderly. Seishin lgaku (Tokyo) 1974;16:965-9.
6. Fukuda H, Kobayashi S, Okada T, Tsunematsu T. Frontal white matter lesions and dementia in lacunar infarction . Stroke 1990;21 :1143-9. 7. Nielsen H, Hojer-Pederson E, Gulliksen G, Haase J, Enevoldsen E. Reversible ischemic neurological defecit and minor strokes before and after EC/IC bypass surgery. Acta Neurol Scand 1986;73 :615-8. 8. Heros RC, Scott RM, Kistler [P, Ackerman RH, Conner ES. Temporary neurological deterioration after extracranial-intracranial bypass. Neurosurgery 1984;15: 17885.
J STROKE CEREBROVASC DIS, VOL.2. NO.4, 1992
243
