Signal changes on magnetic resonance perfusion images with arterial spin labeling after carotid endarterectomy
- Department of Neurosurgery, Kyushu Rosai Hospital, Kitakyushu, Japan
- Department of Cerebrovascular Disease, Kyushu Rosai Hospital, Kitakyushu, Japan
- Department of Neurosurgery, Fukuoka Children's Hospital, Fukuoka, Japan
- Department of Clinical Chemistry and Laboratory Medicine, Kyusyu University Hospital, Fukuoka, Japan
Department of Cerebrovascular Disease, Kyushu Rosai Hospital, Kitakyushu, Japan
DOI:10.4103/2152-7806.196322Copyright: © 2016 Surgical Neurology International This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Takafumi Shimogawa, Takato Morioka, Tetsuro Sayama, Sei Haga, Tomoaki Akiyama, Kei Murao, Yuka Kanazawa, Yoshihiko Furuta, Ayumi Sakata, Shuji Arakawa. Signal changes on magnetic resonance perfusion images with arterial spin labeling after carotid endarterectomy. 21-Dec-2016;7:
How to cite this URL: Takafumi Shimogawa, Takato Morioka, Tetsuro Sayama, Sei Haga, Tomoaki Akiyama, Kei Murao, Yuka Kanazawa, Yoshihiko Furuta, Ayumi Sakata, Shuji Arakawa. Signal changes on magnetic resonance perfusion images with arterial spin labeling after carotid endarterectomy. 21-Dec-2016;7:. Available from: http://surgicalneurologyint.com/surgicalint_articles/signal-changes-on-magnetic-resonance-perfusion-images-with-arterial-spin-labeling-after-carotid-endarterectomy/
Background:Cerebral hyperperfusion after carotid endarterectomy (CEA) is defined as an increase in ipsilateral cerebral blood flow (CBF). Practically, however, prompt and precise assessment of cerebral hyperperfusion is difficult because of limitations in the methodology of CBF measurement during the perioperative period. Arterial spin labeling (ASL) is a completely noninvasive and repeatable magnetic resonance perfusion imaging technique that uses magnetically-labelled blood water as an endogenous tracer. To clarify the usefulness of ASL in the management of cerebral hyperperfusion, we investigated signal changes by ASL with a single 1.5-s post-labeling delay on visual inspection.
Methods:Thirty-two consecutive patients who underwent CEA were enrolled in this retrospective study.
Results:On postoperative day 1, 22 (68.8%) and 4 (12.5%) patients exhibited increased ASL signals bilaterally (Group A) and on the operated side (Group B), respectively. Follow-up ASL showed improvement in these findings. Six (18.8%) patients showed no change (Group C). There was no apparent correlation between ASL signals on postoperative day 1 and the preoperative hemodynamic state, including the cerebrovascular reserve (P = 0.2062). Three (9.4%) patients developed cerebral hyperperfusion syndrome (two in Group A and one in Group B). Coincidence in the localization of increased ASL signals and electroencephalographic abnormalities was noted in these patients.
Conclusion:Visual analysis of ASL with a single post-labeling delay overestimates CBF and cannot identify patients at risk of cerebral hyperperfusion syndrome probably because of the strong effect of the shortened arterial transit time immediately after CEA. However, ASL may be used as for screening.
Keywords: Arterial spin labeling, carotid endarterectomy, cerebral hyperperfusion, cerebral hyperperfusion syndrome
Cerebral hyperperfusion after carotid endarterectomy (CEA) is defined as a major increase in ipsilateral cerebral blood flow (CBF) after surgical repair of carotid stenosis that is well beyond the metabolic demands of the brain tissue.[
Among the various CBF studies performed to date, SPECT has been widely used in Japan to assess the cerebral hemodynamic state and quantify the regional CBF and hemodynamic reserve by measuring the patient's cerebrovascular reactivity (CVR) to acetazolamide loading.[
A new magnetic resonance (MR) perfusion imaging technique with arterial spin labeling (ASL) was recently developed to assess the regional CBF without the need for contrast administration.[
In this report, we demonstrate the chronological changes in ASL signals with a single PLD of 1.5 s immediately after CEA, and compare these findings with preoperative clinical conditions and hemodynamic states. A previous study reported signal changes on ASL with a single PLD of 1.5 s at 3 months postoperatively.[
Thirty-two consecutive patients with ipsilateral ICA stenosis underwent CEA at Kyushu Rosai Hospital from November 2011 to April 2016. The inclusion criteria for CEA used in our institute are carotid stenosis of ≥70% or 50–69% with repeated ischemic cerebrovascular events, activities of daily living corresponding to a modified Rankin Scale (mRS) score of ≤2 in asymptomatic patients and 3 or 4 in symptomatic patients with repeated ischemic cerebrovascular events, small or no infarction on MR imaging, and absence of major occlusive disease (≥70% in diameter) distal to the carotid stenosis. Thirty-one of the 32 patients were men, and 1 was a woman. The mean age of the patients was 73.0 years (range, 46–85 years). We reviewed all medical records. Informed consent was obtained from all the patients.
Cerebral blood flow measurements
Arterial spin labeling measurements
Routine MR imaging and ASL perfusion imaging were performed using a 3T-MR unit (Signa HDxt 3.0T version 23; GE Healthcare, Milwaukee, WI, USA). ASL was prepared using a three-dimensional (3D) spiral fast-spin echo sequence with background suppression for perfusion imaging covering the entire brain. A pulsed continuous scheme was employed. Other acquisition parameters were as follows: Four arms with 1004 points in each spiral arm, phase encoding in the z direction = 32, section thickness = 4 mm, Time to repeat (TR) = 4728 (AUTO) s, post-label wait = 1.525 s (1.5 s), and number of excitation (NEX) = 3. The acquisition time was 2 min 22 s.
All patients underwent preoperative ASL examination with routine MR examination. In all patients, a second ASL examination was performed on postoperative day 1 (POD1); i.e., immediately after extubation of the orotracheal tube. At that time, routine MR imaging was also performed to rule out the appearance of perioperative de novo ischemic events. Follow-up ASL was performed when needed. The timing of follow-up ASL varied in this study. Evaluation of decreased or increased ASL signals was based on visual inspection by two experienced radiologists who were blind to the clinical and imaging data. No differences in the radiologists’ interpretations were noted on independent assessments.
Single photon emission computed tomography measurements
Using SPECT (Headtome SET-031; Shimadzu Co., Kyoto, Japan), CBF was semiquantitatively measured before and 15 min after intravenous injection of 10 mg/kg of acetazolamide (ACZ) on separate days at an interval of 2 to 3 days. Regions of interest were placed automatically in the target area (e.g. in the middle cerebral artery [MCA] territory) using commercially available software (E. CAM Signature; Toshiba Medical, Tokyo, Japan/GMS7700R). The CVR to ACZ was calculated as follows: CVR (%) =100 × (CBFACZ − CBFREST)/CBFREST, where CBFREST and CBFACZ represent CBF before and after intravenous injection of ACZ, respectively. A CVR of <20% was considered to be a reduced CVR according to a previous report.[
Twenty-nine patients underwent preoperative SPECT imaging at rest. In 24 patients, CVR was assessed with an ACZ challenge. Of these 24 patients, 21 were assessed with IMP-SPECT and 3 with ECD-SPECT.
Twenty-nine of the 32 patients underwent routine EEG recording preoperatively and on POD1. Follow-up EEG was performed in 3 patients who developed CHS. Routine EEG recordings were obtained from an 18-channel digital EEG machine (Neurofax; Nihon-Kohden, Tokyo, Japan) with electrode placement according to the International EEG 10-20 system. The EEG recordings were performed for at least 30 min for each patient at rest.
Perioperative management of patients
Twenty-eight patients underwent CEA more than 1 month after the last ischemic event, and 4 patient underwent CEA urgently. All CEA procedures were performed under an operative microscope with the use of internal shunts.
After CEA, general anesthesia with propofol was continued under controlled ventilation until the next morning. Blood pressure was maintained at <130 mm Hg (systolic) and <90 mm Hg (diastolic) in all patients using intravenous nicardipine. Immediately after extubation, all patients underwent routine MR imaging examination including ASL, as described above. In patients with increased ASL signals, arterial blood pressure was more closely monitored and strict control of blood pressure using intravenous nicardipine and diltiazem and an oral angiotensin II receptor blocker was continued until POD7. Diagnosis of CHS was based on the appearance of clinical symptoms and EEG abnormalities that could explain the clinical findings in addition to evidence of increased ASL signals. In Case 5, postoperative ECD-SPECT was also performed to confirm the cerebral hyperperfusion. Functional outcomes were assessed at discharge using the mRS.[
Relationship between preoperative arterial spin labeling signals and preoperative single photon emission computed tomography
Arterial spin labeling signals on postoperative day 1 and their chronological course
On POD1, 22 (68.8%) of 32 patients exhibited increased ASL signals on both sides (Group A) [
(a) Group A (Case 6): Preoperative (Preop.) perfusion images with arterial spin labeling (ASL) showed decreased signals in the affected hemisphere (white dotted arrows) (upper panel). Postoperative (Postop.) ASL on postoperative day 1 (POD1) showed increased signals in both hemispheres (white arrows) (lower panel). (b) Group B (Case 24): Preoperative ASL showed decreased signals in the affected hemisphere (white dotted arrows) (upper panel). ASL on POD1 showed increased signals only in the operated hemisphere (white arrows) (lower panel). (c) Group C (Case 29): Preoperative ASL showed decreased signals in both hemispheres (upper panel). ASL on POD1 showed no increased signals (lower panel)
Four (12.5%) patients demonstrated increased ASL signals only on the operated side (Group B) [
Six (18.8%) patients showed no change in their postoperative ASL signals compared with the preoperative ASL images (Group C) [
Relationship between arterial spin labeling signals on postoperative day 1 and pre and postoperative clinical conditions
Preoperatively, 13 of 22 patients in Group A were asymptomatic or had a history of transient ischemic attack or transient monocular blindness. Nine patients had experienced small but symptomatic infarctions. The preoperative mRS score was 0 in 13 patients, 1 in 8 patients, 2 in 1 patient. Their mRS scores did not change postoperatively except one (Case 16; improved).
In contrast, all patients in Groups B and C had old infarctions. In Group B, the preoperative mRS score was 1 in 2 patients and 3 in 2 patients. In Group C, the preoperative mRS score was 1 in 2 patients, 2 in 2 patients, 3 in 1 patient, and 4 in 1 patient. The mRS scores in Groups B and C did not change postoperatively.
Relationship between arterial spin labeling signals on postoperative day 1 and preoperative hemodynamic state
There was no apparent correlation between the ASL signals on POD1 and the preoperative hemodynamic state, as indicated by preoperative ASL, CBF detected by SPECT at rest, and CVR. Among 22 patients in Group A, the preoperative ASL signals exhibited an ipsilateral decrease in 13 patients, no decrease in 8, and a contralateral decrease in 1 with contralateral internal carotid artery occlusion. Preoperative SPECT imaging showed an ipsilateral decrease in the CBF in seven patients and no decrease in twelve. CVR impairment was observed on the ipsilateral side in 7 of 15 patients, bilaterally in 3, and on the contralateral side in 1 with contralateral ICA occlusion. Four patients demonstrated no CVR impairment.
In 4 patients in Group B, the preoperative ASL signals exhibited an ipsilateral decrease in 3 patients and no decrease in 1. Preoperative SPECT images showed an ipsilateral decrease in the CBF in 2 patients, a bilateral decrease in one, and no decrease in one. CVR impairment was observed on the ipsilateral side in 3 patients, and 1 patient demonstrated no CVR impairment.
In 6 patients in Group C, the preoperative ASL signals exhibited an ipsilateral decrease in 3 patients and no decrease in 3. Preoperative SPECT images showed an ipsilateral decrease in the CBF in 4 patients and no decrease in 2. CVR impairment was observed on the ipsilateral side in 5 of the 6 patients.
Conversely, in 15 patients with impaired ipsilateral CVR, increased ASL signals on POD1 were seen on both sides in 7 patients and unilaterally in 3. However, in the remaining 5 patients, increased ASL signals were not seen. In 5 patients without ipsilateral CVR impairment, increased ASL signals on POD1 were seen on both sides in 4 patients and unilaterally in 1. The lack of a correlation between the ASL signals on POD1 and CVR was statistically significant (P = 0.2062, Chi-square test using JMP Pro 10.0.2 [SAS Institute Inc., Cary, NC, USA]).
There was also no apparent correlation between ASL signals on POD1 and patency of the anterior communicating artery-A1 portion of the anterior cerebral artery (ACOM-A1) and the ipsilateral posterior communicating artery (PCOM) on MR angiography. The ACOM-A1 was not patent in only 2 patients in Group A. The ipsilateral PCOM was patent in 17 of 22 patients in Group A, 3 of 4 patients in Group B, and 3 of 6 patients in Group C.
Development of cerebral hyperfusion syndrome
Three out of 32 (9.4%) patients exhibited CHS. These 3 patients were Case 5 and Case 18 in Group A, and Case 23 in Group B. The detailed clinical courses and hemodynamic as well as EEG findings of Case 5 and Case 23 are described below as representative cases because the clinical profiles and EEG findings of Case 18 were quite similar to those of Case 5.
Case 5 (Group A)
An 83-year-old man presented with asymptomatic severe stenosis of the right ICA. He had a history of smoking, hypertension, hyperlipidaemia, aortic regurgitation, and chronic heart failure. His neurological examination revealed no remarkable findings. 3D-CTA revealed severe stenosis of the right ICA at the bifurcation of the common carotid artery [
Case 5 (Group A). (a) Preoperative three-dimensional computed tomographic angiography (3D-CTA) revealed severe stenosis of the right internal carotid artery (ICA) at the bifurcation of the common carotid artery. (b) Preoperative magnetic resonance perfusion image with arterial spin labeling (ASL) showed decreased signals in the right middle cerebral artery (MCA) territory (white dotted arrows). (c) Single-photon emission computed tomography with N-isopropyl-[123I] b-iodoamphetamine at rest demonstrated mild reduction of cerebral blood flow in the right MCA territory (white dotted arrows). (d) With acetazolamide loading, impairment of cerebrovascular reserve in the right anterior cerebral artery (ACA) and MCA territories was noted (white dotted arrows). (e) On POD1, diffusion-weighted imaging failed to reveal any de novo ischemic lesions. (f) ASL on POD1 clearly showed increased signals in the bilateral ACA and MCA territories, especially on the right side (white arrows). (g) Electroencephalography on POD1 showed slow-wave activities in the bilateral frontal regions (Fp1, Fp2, F3, and F4 of International EEG 10-20 system, black lines) with poorly organized background activities. Asterisks indicate motion artefact due to restless confusion. (h) ASL on POD14 showed disappearance of the increased signals. The preoperative decreased ASL signals in the right MCA territory were also improved. (i) Postoperative 3D-CTA confirmed that the ICA stenosis was improved
On POD1 after CEA, the patient exhibited mildly restless confusion and a talkative state. Although no de novo ischemic events were observed on diffusion-weighted imaging [
Case 23 (Group B)
A 46-year-old man presented with transient weakness of his right limbs. He had a history of smoking, hypertension, hyperlipidemia, diabetes mellitus, atrial fibrillation, and chronic heart failure. He had no abnormal neurological findings, although he had an old infarction in the white matter of the left frontal lobe. 3D-CTA revealed severe stenosis of the left ICA [
Case 23 (Group B). (a) Three-dimensional computed tomographic angiography revealed severe stenosis of the left internal carotid artery. (b) Preoperative arterial spin labeling (ASL) showed decreased signals in the left middle cerebral artery (MCA) territory. (c) Preoperative single-photon emission computed tomography (SPECT) image with 99mTc-ethylcysteinate dimer (ECD) demonstrated reduction of cerebral blood flow in the left MCA territory. (d) Acetazolamide challenge depicted impairment of cerebrovascular reactivity in the left MCA territory. (e) On POD1, diffusion-weighted imaging failed to reveal de novo ischemic events, although an old infarction in the white matter of the left frontal lobe was observed. (f) ASL clearly demonstrated increased signals in the operated left hemisphere. A perfusion defect of the old infarction lesion in the white matter of the left frontal lobe was prominent because the ASL signal in the left hemisphere was increased. (g) Electroencephalography on POD1 showed atypical triphasic waves in the left frontotemporal region (Fp1, F3, and F7, black lines) on diffuse slow-wave activities. (h) ECD-SPECT on POD2 still demonstrated hyperperfusion in the left MCA territory. (i) ASL on POD8 showed no laterality in the ASL signals
On POD1, the patient was found to have motor aphasia. Diffusion-weighted imaging failed to reveal de novo ischemic events, although T2 shine-through of the old infarction in the white matter of the left frontal lobe was observed [
Preoperative ASL signals with a single PLD of 1.5 s mostly coincided with the CBF map on resting SPECT, supporting the findings of previous reports.[
The incidence of post-CEA hyperperfusion detected with SPECT reportedly ranges from 0.5 to 40.0%.[
In the present study, we measured ASL signals immediately after extubation on POD1 because general anesthesia using propofol was continued until the morning of POD1. Twenty-two (68.8%) and 4 (12.5%) of the 32 patients exhibited increased ASL signals bilaterally and on the operated side, respectively. Follow-up ASL showed improvement in these findings. The higher incidence of transiently increased ASL signals in our study is apparently attributed to the shortening of the ATT not only to the increased CBF. Immediately after CEA, improvement in anterograde ICA perfusion on the operated side and no need for slow streaming collaterals resulted in shortening of the ATT not only in the ipsilateral hemisphere but also in the contralateral hemisphere.
Previous authors have clearly demonstrated that patients with poor preoperative CVR have a potentially increased risk of post-CEA hyperperfusion.[
To overcome these shortcomings of ASL with a single PLD and to achieve quantitative measurements of CBF and ATT, a multiple-PLD ASL approach has been used.[
In the present study, 3 patients (Case 5 and Case 18 in Group A, Case 23 in Group B) developed CHS. In Case 5 and 18, on POD1, increased ASL signals were noted on both the sides, and EEG showed slow-wave activities in the bilateral frontal regions with poorly organized background activities, indicating diffuse dysfunction, especially in the bilateral frontal regions. Disinhibition of the bilateral frontal lobes caused by cerebral hyperperfusion explained the patient's restlessness. In our previous report,[
In Case 23, atypical triphasic waves were observed in the frontal region of the ipsilateral side. Atypical triphasic waves are now generally accepted as one of the EEG features in patients with nonconvulsive status epilepticus, although there is still argument against true ictal discharges.[
In these three cases, coincidence in the localization of the increased ASL signals and EEG abnormalities was noted. We speculate that the pathophysiological mechanism of CHS is not straightforward and that the marked increase in the CBF on the ipsilateral side was not the sole factor involved in the development of CHS. Increased flow velocity (i.e. shortening of the ATT) could be an additional factor, as measured with transcranial Doppler by previous authors.[
Because a limitation of our study is the small number of patients (n = 32), further studies in a large cohort should be conducted with a more sophisticated ASL method. We recently developed dual PLD method, instead of single PLD method that we used in this study.[
In conclusion, owing to the effect of the ATT, ASL with a single PLD does not accurately reflect the CBF value and cannot identify patients at risk of CHS. However, ASL is completely noninvasive and can be performed as a part of routine MR imaging examination. Furthermore, ASL can promptly evaluate post-CEA hemodynamic changes, including both an increased CBF and shortening of the ATT. Although a more sophisticated ASL method should be explored, ASL with a single PLD may be used as screening test for cerebral hyperperfusion at present.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
The authors thank Dr. Hiroyuki Nomiyama and Dr. Seitaro Shin for interpreting the SPECT and ASL images.
1. Akiyama T, Morioka T, Shimogawa T, Haga S, Sayama T, Kanazawa Y. Arterial spin-labeling magnetic resonance perfusion imaging with dual postlabeling delay in internal carotid artery steno-occlusion: Validation with digital subtraction angiography. J Stroke Cerebrovasc Dis. 2016. pii: S1052-
2. Alsop DC, Detre JA. Multisection cerebral blood flow MR imaging with continuous arterial spin labeling. Radiology. 1998. 208: 410-6
3. Ances BM, McGarvey ML, Abrahams JM, Maldjian JA, Alsop DC, Zager EL. Continuous arterial spin labeled perfusion magnetic resonance imaging in patients before and after carotid endarterectomy. J Neuroimaging. 2004. 14: 133-8
4. Coutts SB, Hill MD, Hu WY, Sutherland GR. Hyperperfusion syndrome: Toward a stricter definition. Neurosurgery. 2003. 53: 1053-69
5. Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA. Arterial spin-labeling in routine clinical practice, part 1: Technique and artifacts. AJNR Am J Neuroradiol. 2008. 29: 1228-34
6. Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA. Arterial spin-labeling in routine clinical practice, part 2: Technique and artifacts. AJNR Am J Neuroradiol. 2008. 29: 1235-41
7. Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA. Arterial spin-labeling in routine clinical practice, part 3: Technique and artifacts. AJNR Am J Neuroradiol. 2008. 29: 1428-35
8. Detre JA, Alsop DC, Vives LR, Maccotta L, Teener JW, Raps EC. Noninvasive MRI evaluation of cerebral blood flow in cerebrovascular disease. Neurology. 1998. 50: 633-41
9. Fujimoto S, Toyoda K, Inoue T, Hirai Y, Uwatoko T, Kishikawa K. Diagnostic impact of transcranial color-coded real-time sonography with echo contrast agents for hyperperfusion syndrome after carotid endarterectomy. Stroke. 2004. 35: 1852-6
10. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T. Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol. 2007. 67: 273-82
11. Haga S, Morioka T, Shimogawa T, Akiyama T, Murao K, Kanazawa Y. Arterial spin labeling perfusion magnetic resonance image with dual postlabeling delay: A correlative study with acetazolamide 123I-Iodoanphetamine single-photon emission computed tomography. J Stroke Cerebrovasc Dis. 2016. 25: 1-6
12. Hamamura T, Morioka T, Sayama T, Mukae N, Arakawa S, Maeda H. Cerebral hyperperfusion syndrome associated with non-convulsive status epilepticus following superficial temporal artery-middle cerebral artery anastomosis – A case report. Neurol Med Chir. 2010. 50: 1099-104
13. Hayashi K, Horie N, Suyama K, Nagata I. Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg. 2012. 78: 447-54
14. Helle M, Norris DG, Rüfer S, Alfke K, Jansen O, van Osch MJ. Superselective pseudocontinuous arterial spin labeling. Magn Reson Med. 2010. 64: 777-86
15. Helle M, Rüfer S, van Osch MJ, Nabavi A, Alfke K, Norris DG. Superselective arterial spin labeling applied for flow territory mapping in various cerebrovascular diseases. J Magn Reson Imaging. 2013. 38: 496-503
16. Hirooka R, Ogasawara K, Sasaki M, Yamadate K, Kobayashi M, Suga Y. Magnetic resonance imaging in patients with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy. J Neurosurg. 2008. 108: 1178-83
17. Hosoda K, Kawaguchi T, Shibata Y, Kamei M, Kidoguchi K, Koyama J. Cerebral vasoreactivity and internal carotid artery flow help to identify patients at risk for hyperperfusion after carotid endarterectomy. Stroke. 2001. 32: 1567-73
18. Hosoda K. The Significance of Cerebral Hemodynamics Imaging in Carotid Endarterectomy: A Brief Review. Neurol Med Chir. 2015. 55: 782-8
19. Iwanaga T, Harada M, Kubo H, Funakoshi Y, Kunikane Y, Matsuda T. Operator-bias-free Comparison of Quantitative Perfusion Maps Acquired with Pulsed-continuous Arterial Spin Labeling and Single-photon-emission Computed Tomography. Magn Reson Med Sci. 2014. 13: 239-49
20. Jorgensen LG, Schroeder TV. Defective cerebrovascular autoregulation after carotid endarterectomy. Eur J Vasc Surg. 1993. 7: 370-9
21. Kanazawa Y, Morioka T, Arakawa S, Furuta Y, Nakanishi A, Kitazono T. Non-convulsive partial status epilepticus mimicking recurrent infarction revealed by diffusion weighted and ASL perfusion MR images. J Stroke Cerebrovasc Dis. 2015. 24: 731-8
22. Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y, Abe H. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: Can acetazolamide test predict it?. Stroke. 2001. 32: 2110-6
23. Morioka T, Sayama T, Mukae N, Hamamura T, Yamamoto K, Kido T. Nonconvulsive status epilepticus during perioperative period of cerebrovascular surgery. Neurol Med Chir. 2011. 51: 171-9
24. Morioka T, Sayama T, Shimogawa T, Mukae N, Hamamura T, Arakawa S. Electroencephalographic evaluation of cerebral hyperperfusion syndrome following superficial temporal artery-middle cerebral artery anastomosis. Neurol Med Chir. 2013. 53: 388-95
25. Moulakakis KG, Mylonas SN, Sfyroeras GS, Andrikopoulos V. Hyperperfusion syndrome after carotid revascularization. J Vasc Surg. 2009. 49: 1060-8
26. Naylor AR, Whyman M, Wildsmith JA, McClure JH, Jenkins AM, Merrick MV. Immediate effects of carotid clamp release on middle cerebral artery blood flow velocity during carotid endarterectomy. Eur J Vasc Surg. 1993. 7: 308-16
27. Noguchi T, Kawashima M, Irie H, Ootsuka T, Nishihara M, Matsushima T. Arterial spin-labeling MR imaging in moyamoya disease compared with SPECT imaging. Eur J Radiol. 2011. 80: e557-62
28. Ogasawara K, Yukawa H, Kobayashi M, Mikami C, Konno H, Terasaki K. Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning. J Neurosurg. 2003. 99: 504-10
29. Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotidendarterectomy and carotid artery stenting: Retrospective review of 4494 patients. J Neurosurg. 2007. 107: 1130-6
30. Pizzini FB, Farace P, Manganotti P, Zoccatelli G, Bongiovanni LG, Golay X. Cerebral perfusion alterations in epileptic patients during peri-ictal and post-ictal phase: PASL vs DSC-MRI. Magn Reson Imaging. 2013. 31: 1001-5
31. Reigel MM, Hollier LH, Sundt TM, Piepgras DG, Sharbrough FW, Cherry KJ. Cerebral hyperperfusion syndrome: A cause of neurologic dysfunction after carotid endarterctomy. J Vasc Surg. 1987. 5: 628-34
32. Sugino T, Mikami T, Miyata K, Suzuki K, Houkin K, Mikuni N. Arterial spin-labeling magnetic resonance imaging after revascularization of moyamoya disease. J Stroke Cerebrovasc Dis. 2013. 22: 811-6
33. Sundt TM, Sharbrough FW, Piepgras DG, Kearns TP, Messick JM, O’Fallon WM. Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy, with results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc. 1981. 56: 533-43
34. Takeuchi R, Matsuda H, Yonekura Y, Sakahara H, Konishi J. Noninvasive quantitative measurements of regional cerebral blood flow using technetium-99m-L, L-ECD SPECT activated with acetazolamide: Quantification analysis by equal-volume-split 99mTc-ECD consecutive SPECT method. J Cereb Blood Flow Metab. 1997. 17: 1020-32
35. Tanaka Y, Nagaoka T, Nair G, Ohno K, Duong TQ. Arterial spin labeling and dynamic susceptibility contrast CBF MRI in postischemic hyperperfusion, hypercapnia, and after mannitol injection. J Cereb Blood Flow Metab. 2011. 31: 1403-11
36. Uchihashi Y, Hosoda K, Zimine I, Fujita A, Fujii M, Sugimura K. Clinical application of arterial spin-labeling MR imaging in patients with carotid stenosis: Quantitative comparative study with single-photon emission CT. AJNR Am J Neuroradiol. 2011. 32: 1545-51
37. van Mook WN, Rennenberg RJ, Schurink GW, van Oostenbrugge RJ, Mess WH, Hofman PA. Cerebral hyperperfusion syndrome. Lancet Neurol. 2005. 4: 877-88
38. Van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988. 19: 604-7
39. Wang DJ, Alger JR, Qiao JX, Gunther M, Pope WB, Saver JL. Multi-delay multi-parametric arterial spin-labeled perfusion MRI in acute ischemic stroke-Comparison with dynamic susceptibility contrast enhanced perfusion imaging. Neuroimage Clin. 2013. 6: 1-7