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Ultrasonographic Changes after Indirect Revascularization Surgery in Pediatric Patients with Moyamoya Disease
Ultrasound in Med. & Biol., Vol. -, No. -, pp. 1–8, 2016 Copyright Ó 2016 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
http://dx.doi.org/10.1016/j.ultrasmedbio.2016.07.016
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Original Contribution ULTRASONOGRAPHIC CHANGES AFTER INDIRECT REVASCULARIZATION SURGERY IN PEDIATRIC PATIENTS WITH MOYAMOYA DISEASE SHIN-JOE YEH,* SUNG-CHUN TANG,* LI-KAI TSAI,* YA-FANG CHEN,y HON-MAN LIU,y YING-AN CHEN,* YU-LIN HSIEH,* SHIH-HUNG YANG,z YU-HSUAN TIEN,x CHI-CHENG YANG,x MENG-FAI KUO,z and JIANN-SHING JENG* * Stroke Center and Department of Neurology, National Taiwan University Hospital, Taipei, Taiwan; y Department of Medical Imaging, National Taiwan University Hospital, Taipei, Taiwan; z Department of Neurosurgery, National Taiwan University Hospital, Taipei, Taiwan; and x Division of Clinical Psychology, Department of Occupational Therapy, College of Medicine, Chang-Gung University, Taoyuan, Taiwan (Received 11 February 2016; revised 9 June 2016; in final form 13 July 2016)
Abstract—The marked cerebral hypoperfusion of moyamoya disease (MMD) can be treated with encephaloduroarteriosynangiosis (EDAS), an indirect revascularization surgery. Collateral establishment after the surgery is a gradual process; thus, easy access to serial assessment is of great importance. We prospectively recruited 15 pediatric moyamoya patients who underwent EDAS surgeries on a total of 19 hemispheres. Ultrasonography of extracranial and intracranial arteries was performed pre-operatively and post-operatively at 1, 3 and 6 mo. Among the extracranial arteries, the superficial temporal artery had the most pronounced increase in flow velocity and decrease in flow resistance from 1 mo post-surgery (p , 0.01). Among the large intracranial arteries, a significant increase in peak systolic velocity was observed in the anterior cerebral artery from 3 mo post-surgery (p , 0.05). These findings indicate significant hemodynamic changes on ultrasonography in pediatric moyamoya patients after indirect revascularization surgery. (E-mail: [email protected]) Ó 2016 World Federation for Ultrasound in Medicine & Biology. Key Words: Moyamoya disease, Pediatric stroke, Encephaloduroarteriosynangiosis, Indirect revascularization, Ultrasonography.
Moyamoya disease has a progressive course (Suzuki and Takaku 1969), which makes follow-up mandatory for this disease. Cerebral angiography is the gold standard tool for diagnosis and follow-up for MMD; however, the risks of permanent neurologic deficit and radiation exposure are ongoing safety concerns (Perren et al. 2005). Ultrasound is another non-invasive tool for the evaluation of hemodynamics; however, for MMD it is reported only for baseline status (Lee et al. 2004; Ruan et al. 2006) or for evaluations conducted after direct bypass surgery (Kraemer et al. 2012; Wu et al. 2011) but not for indirect revascularization surgery. The baseline characteristics revealed by ultrasound include an increase in resistance and a decrease in flow velocity in the common carotid artery (CCA) and ICA, as well as decreased resistance and increased flow velocity in the superficial temporal artery (STA) resulting from the effects of compensation (Ruan et al. 2006). The stenotic intracranial arteries commonly exhibit low or high flow velocity (Lee et al. 2004; Ruan et al. 2006). After direct bypass surgery, the patency of the STA graft is
INTRODUCTION Moyamoya disease (MMD) is characterized by idiopathic chronic progressive stenosis or occlusion of bilateral distal internal carotid arteries (ICAs) and their major branches (Suzuki and Takaku 1969). The marked cerebral hypoperfusion in moyamoya patients usually presents as ischemic stroke (IS) or transient ischemic attack (TIA) (Scott and Smith 2009). The incidence and prevalence of MMD are higher in Asian populations (Baba et al. 2008; Chen et al. 2014; Duan et al. 2012; Han et al. 2000); nonetheless, this disease is also a major cause of pediatric stroke in Western countries (Currie et al. 2011). The ischemic events associated with MMD can be reduced by extracranial–intracranial (EC-IC) bypass surgery, including direct, indirect and combined surgeries (Bao et al. 2015).
Address correspondence to: Jiann-Shing Jeng, Department of Neurology, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei 100, Taiwan. E-mail: [email protected] 1
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associated with increased flow velocity and decreased resistance in the STA on ultrasound (Wu et al. 2011); however, the exact changes in the ultrasound images after indirect revascularization surgery remain unclear. Encephaloduroarteriosynangiosis (EDAS) surgery is one kind of indirect revascularization surgery, particularly for pediatric moyamoya patients using STA as a feeding artery. We hypothesized that the STA should exhibit significant changes on ultrasonography after EDAS compared with the pre-operative state. Thus, we compared ultrasonographic parameters between the preand post-operative states on the operated side to characterize serial changes in the extracranial and intracranial arteries after EDAS in moyamoya patients. In addition, because progression of MMD may confound the postoperative changes, we compared the hemodynamic parameters on the operated side with those for the contralateral non-operated side at serial time points. METHODS Patients Between July 2012 and July 2014, consecutive pediatric moyamoya patients (,20 y of age) who had been diagnosed by cerebral angiography and were scheduled to undergo EDAS at the National Taiwan University Hospital were prospectively enrolled for this study. All but one patient had not undergone surgery for MMD before being enrolled; the exception had undergone EDAS on one side, and so this hemisphere was excluded from analysis because of a lack of pre-operative ultrasonographic data. All patients underwent follow-up angiography (cerebral angiography or magnetic resonance angiography) after EDAS to check for collateral establishment and disease progression. The demographic characteristics, neurologic events, angiographic findings and surgical complications of each patient were recorded. This study was approved by the Institutional Ethics Committee, and all enrolled patients and their parents gave informed consent. Ultrasonographic assessment In the present study, ultrasonographic examination was arranged before surgery and at 1, 3 and 6 mo afterward. The extracranial and transcranial ultrasound studies were performed using a color-coded ultrasound system (IE33, Philips Medical Systems, Bothell, WA, USA). These ultrasound examinations were performed by one neurologic ultrasound technician. Extracranial ultrasound study. Extracranial arteries were assessed using an 11-3 MHz linear-array transducer. For the extracranial arteries, we measured peak systolic velocity, end-diastolic velocity, resistance index and flow volume of the CCA, ICA, external carotid artery (ECA) and STA. The ICA was measured 1.5–2 cm above the
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carotid bifurcation, and the ECA was assessed at the proximal ECA segment before the branching of the superior thyroid artery. The STA was analyzed at the common STA segment at the level of the ear. The flow volume of each vessel was calculated from the time-averaged mean flow velocity of the cross-sectional area of the individual vessel; this formula has been built into the ultrasound software. The mean flow velocity was calculated from the mean of all instant velocities within the spectrum over the heart cycle. In terms of the diameter of each vessel for calculation of cross-sectional area, we measured the diameter between inner luminal walls at end-diastole; we measured once for each vessel because pediatric patients were unable to tolerate prolonged examinations. Transcranial color-coded sonography. Transcranial color-coded sonography (TCCS) was performed using a 5-1 MHz phased-array probe with angle correction. For the intracranial arteries, we measured peak systolic velocity, mean flow velocity and pulsatility index of the anterior cerebral artery (ACA), middle cerebral artery (MCA) M1 and M2 segments and posterior cerebral artery (PCA) on color Doppler images. The formula for determining mean flow velocity is built into the ultrasound software, and these data were automatically displayed. The highest flow velocity along the course of the individual vessel was recorded. Statistical analysis Categorical variables are presented as percentages, and continuous or discrete variables as means 6 standard deviations. Student’s paired t-test was used for univariate analysis between groups. First, we compared the hemodynamic parameters between the pre- and post-operative states. Cerebral hemispheres without complete postoperative follow up at these time points were excluded. Second, we compared the hemodynamic parameters on the operated side with those for the contralateral non-operated side after excluding patients who had undergone surgery on the contralateral side. Two-tailed p values , 0.05 were considered to indicate statistical significance. Data management and analysis were performed using Small Stata software (StataCorp LP, College Station, TX, USA). RESULTS Basic characteristics of these patients Among the 15 patients enrolled in the study (Table 1), the mean age was 10.4 6 4.6 y (range: 5–19 y), which included 11 males and 4 females. EDAS was performed on 19 cerebral hemispheres. Six of these also underwent indirect revascularization surgeries in addition to EDAS, including multiple-burr-hole surgery (MBH) (n 5 3), encephaloperiosteosynangiosis (EPS) (n 5 2) and encephalomyosynangiosis (EMS) (n 5 1). The most common
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Table 1. Characteristics of the 15 patients with moyamoya disease Patient
1
Age (y)/sex Hemispheres enrolled in analysis Other indirect revascularization surgeries in addition to EDAS Pre-op presentations, IS or TIA Epilepsy Developmental delay Headache Pre-op IQ score 30-d post-op ipsilateral IS Post-op IQ score
13/F L
2
3
12/M 10/M R, L R
MBH
4
5
6
7
5/M L, R
13/M L
7/F L
5/M L
EPS
EMS
MBH
IS, TIA
TIA
TIA
IS, TIA
(2)
(1) (1)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(1) (2)
(2) 86 (2)
(2) 124 (2)
(2) 117 (2)
(2)
(2) 126 (2) 117
130
(2)
IS, TIA IS, TIA
8
9
10
11/M 19/F 18/F L R L
11
12
13
14
15
6/M L,R
13/M R
14/M L
5/M L, R
5/M R
EPS
MBH
TIA
TIA
(2) IS, TIA
IS
IS, TIA IS, TIA IS, TIA
(1) (1)
(1) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) 131 (2)
(2) 60 (2)
(2) 105 (2)
(1) 110 (2)
(1) 122 (2)
(2) 78 (2)
(1) 123 (2)
(2)
(2) 89 (2)
(2) 107 (2)
114
54
103
109
123
95
120
95
108
(1)
EDAS 5 encephaloduroarteriosynangiosis; EMS 5 encephalomyosynangiosis; EPS 5 encephaloperiosteosynangiosis; IS 5 ischemic stroke; MBH 5 multiple-burr-hole surgery; TIA 5 transient ischemic attack.
clinical presentation was TIA (n 5 12, 80%), followed by IS (n 5 9, 60%), epilepsy (n 5 4, 27%), headache (n 5 3, 20%) and developmental delay (n 5 2, 13%). One patient (7%) without symptom was diagnosed because of a positive family history. The pre-operative IQ scores were mostly average to superior. The duration of symptoms before EDAS surgery
was shorter for patients who presented with ischemic stroke/TIA (2.4 6 3.1 y) and longer for patients who manifested epilepsy (4.8 6 3.9 y). The 30-d rate of post-operative ipsilateral ischemic stroke was 5% (1 event/19 operations). During follow-up periods of 18–44 mo, there were no other recurrent ISs. Only one patient had more than three
Fig. 1. Serial hemodynamics of extracranial arteries determined using ultrasonography after indirect revascularization surgery compared with pre-operative state. (a) STA. (b) ECA. (c) ICA. ECA 5 external carotid artery; ICA 5 internal carotid artery; STA 5 superficial temporal artery.
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ipsilateral TIAs, and thus, he later underwent ipsilateral EPS. Overall, these patients had significantly fewer ischemic events and stationary IQ scores after indirect revascularization surgery compared with the pre-operative state. Postsurgical angiography revealed that 82% of the hemispheres were Matsushima grade A or B, indicating good collateral establishment (Matsushima et al. 1992). Temporal alteration of hemodynamics in hemispheres that underwent indirect bypass surgery The ultrasonographic features of extracranial and intracranial arteries are illustrated in Figures 1 and 2. Among the extracranial arteries, the STA exhibited the most pronounced hemodynamic changes after indirect bypass surgery (Fig. 1). From 1 mo after surgery, we observed a significant increase in end-diastolic velocity (139% increase, p , 0.01) and flow volume (99% increase, p , 0.01) in the STA, as well as a decrease in resistance index (15% decrease, p , 0.01), compared with the pre-operative state. These changes plateaued at 3 mo post-surgery (97% increase in peak-systolic veloc-
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ity, p , 0.01; 386% increase in end-diastolic velocity, p , 0.01; 168% increase in flow volume, p , 0.01; 22% decrease in flow resistance, p , 0.01). The ECA exhibited patterns similar to those of the STA. In contrast, the ICA had a gradual decrease in flow and increase in resistance index, particularly 6 mo post-surgery. Among the intracranial arteries, the ACA exhibited the most pronounced temporal changes after indirect bypass surgery. In 11 hemispheres (58%), ACA flow could not be detected before the surgery. The ACA exhibited a significant increase in peak systolic velocity 3 mo post-surgery (75% increase, p 5 0.04) (Fig. 2). The MCA and PCA both exhibited a tendency toward a gradual decrease in flow velocity. Difference between arteries on operated and nonoperated contralateral sides We then compared the ultrasonographic results of the hemisphere that underwent surgery with those of the contralateral hemisphere that did not undergo surgery to provide a side-by-side comparison of hemodynamic properties. EDAS on the contralateral hemisphere was often performed
Fig. 2. Serial hemodynamics of intracranial arteries determined using transcranial Doppler after indirect revascularization surgery compared with pre-operative state. (a) ACA. (b) MCA. (c) PCA. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery; PCA 5 posterior cerebral artery.
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within 6 mo of the first EDAS in these cases. Once the contralateral hemisphere was operated, it was excluded from the analysis. Therefore, a total of 14 contralateral hemispheres were analyzed pre-surgery and the first month after operation, 11 hemispheres were analyzed the third month and 5 hemispheres were analyzed the sixth month. Among the extracranial arteries (Fig. 3), the STA exhibited the most pronounced side differences in all parameters (peak systolic and end-diastolic velocities, resistance index and flow amount) in this side-by-side comparison, between the first and sixth months post-surgery. The ECA exhibited significant side differences only at the third month post-surgery. The ICA on the operated side had lower velocity than that on the contralateral side before surgery, and this situation persisted until 6 mo post-surgery. Among the intracranial arteries (Fig. 4), the MCA exhibited differences in the side-by-side comparison after surgery. The MCA on the operated side exhibited a trend toward lower peak systolic velocity, compared with the contralateral side (74 cm/s vs. 148.5 cm/s, p 5 0.05), at 3 mo post-surgery. Serial ultrasonographic changes of a case with MMD after EDAS surgery In Figure 5 are serial ultrasonographic findings for a 5y-old boy with MMD who underwent EDAS. Compared with the pre-operative state, there were increases in peak systolic (from 88 to 173 cm/s) and end-diastolic (from 16
5
to 83 cm/s) velocities, a decrease in resistance index (from 0.82 to 0.52) and an increase in flow volume (from 11 to 61 mL/min) of the STA 1 mo post-surgery (Fig. 5a). The flow velocity and flow volume of the STA plateaued at the third month. The ipsilateral MCA exhibited slow flow velocity with dampened waveforms before surgery. At 6 mo after EDAS, peak systolic flow velocity of the ipsilateral MCA decreased from 49 to 44 cm/s, and flow resistance increased from 0.34 to 0.79 (Fig. 5b). The ipsilateral ACA was undetectable before the surgery; however, it became detectable 6 mo post-surgery (Fig. 5b). Flow velocity of the ipsilateral PCA was very high before surgery and dropped dramatically 1 mo postsurgery, followed by a slight increase 3 mo post-surgery. DISCUSSION This study revealed significant changes in hemodynamic parameters as manifest in the temporal and spatial patterns observed in the ultrasonographic results after indirect revascularization surgery on pediatric moyamoya patients. Among the extracranial arteries, the STA exhibited the most pronounced hemodynamic changes. Among the intracranial arteries, the temporal changes in the ACA were the most pronounced. The significant hemodynamic changes in the STA detected by ultrasound after indirect revascularization
Fig. 3. Differences in extracranial arteries between operated side and contralateral non-operated side before and after indirect revascularization surgery on ultrasonography. (a) STA. (b) ECA. (c) ICA. ECA 5 external carotid artery; ICA 5 internal carotid artery; STA 5 superficial temporal artery.
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Fig. 4. Differences in intracranial arteries between operated side and contralateral non-operated side before and after indirect revascularization surgery on ultrasonography. (a) ACA. (b) MCA. (c) PCA. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery; PCA 5 posterior cerebral artery.
surgery are somewhat similar to those observed after direct bypass surgery (Kraemer et al. 2012; Wu et al. 2011). The parameters of the STA and ECA that underwent significant post-operative changes compared with pre-operative values were flow velocities (peak systolic and end-diastolic) and resistance after direct bypass surgery (Kraemer et al. 2012) or indirect revascularization surgery (present study). The increase in flow volume was largely attributed to the increased flow velocity, especially the end-diastolic velocity. Because it is the donor artery in indirect revascularization surgeries, the increased flow in the STA can be caused by the establishment of intracranial collaterals. However, the two procedures differ with respect to the speed of collateral establishment. In this study, the hemodynamic plateau after indirect revascularization surgery occurred at 3 mo, whereas the plateau after direct bypass surgery occurs as early as 1 wk post-surgery (Wu et al. 2011). This difference in these temporal profiles indicates that there
are differences in the revascularization process between indirect revascularization and direct bypass. The present study revealed that the ICA on the operated side underwent a gradual decrease in flow after indirect bypass surgery, which may be related to progressive stenosis of the ICA or decreased demand from the ICA. Previous angiographic studies have reported acceleration in the progression of ICA stenosis after bypass surgery (Huang et al. 2009). Furthermore, a decrease in demand from the ICA may also occur after the establishment of collaterals. Our findings also revealed significant temporal changes in the hemodynamic parameters of the ACA after indirect bypass surgery, which manifested as increased flow velocity and decreased resistance. In addition, the ACAs of the 11 hemispheres were undetectable before the operation, and there was only one hemisphere with an undetectable ACA 6 mo after indirect revascularization surgery. If the ACA were occluded by a thrombus,
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Fig. 5. Ultrasonographic findings for a 5-y-old moyamoya patient who underwent encephaloduroarteriosynangiosis surgery on the left side: (a) Carotid Doppler study revealing serial changes in the left superficial temporal artery. (b) Transcranial Doppler study revealing pre-operative MCA, as well as post-operative left MCA and ACA 6 mo after encephaloduroarteriosynangiosis. The ACA was undetected before the operation. The MCA was detected at a depth of 45–46 mm, and the ACA, at a depth of 74 mm. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery.
it would not open again after the surgery. Thus, the failure to detect the ACA before surgery probably indicated very low flow in the ACA, which was likely to be missed in detection. After indirect revascularization surgery, the ACA was detected because of the increased flow, which probably came from collateral vessels. This phenomenon also indicates that indirect revascularization surgery may improve perfusion in the ACA territory. Furthermore, even though the flow velocity of the MCA trunk decreased after surgery, there were significantly fewer ipsilateral ISs or TIAs after surgery. This indicates that the collaterals played a more important role than the MCA trunk in supplying MCA territory in moyamoya patients. Another study using perfusion SPECT reported that EDAS can improve perfusion in the MCA territory (Song et al. 2012). However, it was difficult to prove progressive stenosis of the MCA with TCCS because the diameter of the MCA cannot be measured. In addition, the PCA had abnormally high flow velocity before surgery that decreased after indirect bypass surgery. This change in the PCA may result from a decrease in the need for compensation from the PCA or progressive stenosis of the PCA (Huang et al. 2009). Previous literature on ultrasonographic changes after combined direct bypass surgery and encephalomyosynangiosis (EMS) in children with moyamoya children indicated ultrasonographic changes correlated well with angiography (Perren et al. 2005). They used power Doppler imaging to detect low flow of neoangiogenesis and concluded that the degree of neoangiogenesis on ultrasound had a good correlation with that on angiography. We used color Doppler instead of power Doppler in this
study, which might have reduced sensitivity in detecting low flow, especially in the pre-operative state. The present study had several limitations. First, the number of cases was small as MMD is a rare disease. Second, the first follow-up was conducted 1 mo post-surgery, which made it impossible to clarify when the earliest hemodynamic changes occurred after indirect revascularization surgery. Third, in terms of measurement of flow volume, the diameter of each vessel was measured at end-diastole, which would result in an underestimate flow volume. Fourth, six cases also underwent indirect revascularization surgeries in addition to EDAS; therefore, these changes were not purely secondary to EDAS surgery. However, these features can represent the changes after indirect revascularization surgeries and are more compatible with real-world conditions. The strength of this study lies in the fact that it is the first study to use ultrasonography to visualize sequential as well as spatial changes in hemodynamic parameters after successful indirect revascularization surgery. In the future, for any moyamoya patient, post-operative ultrasonographic changes that deviate from the pattern outlined in this study may indicate inadequate revascularization, and further angiographic investigation will be warranted. CONCLUSIONS This study found that ultrasonography is effective in revealing temporal and spatial changes in hemodynamic parameters after indirect revascularization surgery. Regular follow-up of moyamoya patients after indirect revascularization surgery, particularly in the first 3 mo, is
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suggested for the early confirmation of revascularization status. Acknowledgments—This study was supported in part by a grant from the National Science Council and Ministry of Science and Technology, Taiwan (MOST 103-2321-B-002-033). The funding source had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
REFERENCES Baba T, Houkin K, Kuroda S. Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 2008;79:900–904. Bao XY, Duan L, Yang WZ, Li DS, Sun WJ, Zhang ZS, Zong R, Han C. Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China. Cerebrovasc Dis 2015;39:75–81. Chen PC, Yang SH, Chien KL, Tsai IJ, Kuo MF. Epidemiology of moyamoya disease in Taiwan: A nationwide population-based study. Stroke 2014;45:1258–1263. Currie S, Raghavan A, Batty R, Connolly DJ, Griffiths PD. Childhood moyamoya disease and moyamoya syndrome: A pictorial review. Pediatr Neurol 2011;44:401–413. Duan L, Bao XY, Yang WZ, Shi WC, Li DS, Zhang ZS, Zong R, Han C, Zhao F, Feng J. Moyamoya disease in China: Its clinical features and outcomes. Stroke 2012;43:56–60. Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, Choi SG, Doh JO, Han JW, Jung S, Kang SD, Kim DJ, Kim HI, Kim HD, Kim MC, Kim SC, Kim SC, Kim Y, Kwun BD, Lee BG, Lim YJ, Moon JG, Park HS, Shin MS, Song JH, Suk JS, Yim MB. A cooperative study: Clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976– 1994). The Korean Society for Cerebrovascular Disease. Acta Neurochir (Wien) 2000;142:1263–1273.
Volume -, Number -, 2016 Huang AP, Liu HM, Lai DM, Yang CC, Tsai YH, Wang KC, Yang SH, Kuo MF, Tu YK. Clinical significance of posterior circulation changes after revascularization in patients with moyamoya disease. Cerebrovasc Dis 2009;28:247–257. Kraemer M, Schuknecht B, Jetzer AK, Yonekawa Y, Khan N. Postoperative changes in the superficial temporal artery and the external carotid artery duplex sonography after extra-intracranial bypass surgery in European moyamoya disease. Clin Neurol Neurosurg 2012;114:930–934. Lee YS, Jung KH, Roh JK. Diagnosis of moyamoya disease with transcranial Doppler sonography: Correlation study with magnetic resonance angiography. J Neuroimaging 2004;14:319–323. Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients—Comparison between the results of indirect and direct revascularization procedures. Neurosurgery 1992;31:401–405. Perren F, Meairs S, Schmiedek P, Hennerici M, Horn P. Power Doppler evaluation of revascularization in childhood moyamoya. Neurology 2005;64:558–560. Ruan LT, Duan YY, Cao TS, Zhuang L, Huang L. Color and power Doppler sonography of extracranial and intracranial arteries in Moyamoya disease. J Clin Ultrasound 2006;34:60–69. Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med 2009;360:1226–1237. Song YS, Oh SW, Kim YK, Kim SK, Wang KC, Lee DS. Hemodynamic improvement of anterior cerebral artery territory perfusion induced by bifrontal encephalo(periosteal)synangiosis in pediatric patients with moyamoya disease: A study with brain perfusion SPECT. Ann Nucl Med 2012;26:47–57. Suzuki J, Takaku A. Cerebrovascular ‘‘moyamoya’’ disease: Disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969;20:288–299. Wu M, Huang Z, Zhang D, Wang L, Sun J, Wang S, Zhao Y, Zhao J. Color Doppler hemodynamic study of the superficial temporal arteries in superficial temporal artery–middle cerebral artery (STA–MCA) bypass surgery for moyamoya disease. World Neurosurg 2011;75: 258–263.
http://dx.doi.org/10.1016/j.ultrasmedbio.2016.07.016
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Original Contribution ULTRASONOGRAPHIC CHANGES AFTER INDIRECT REVASCULARIZATION SURGERY IN PEDIATRIC PATIENTS WITH MOYAMOYA DISEASE SHIN-JOE YEH,* SUNG-CHUN TANG,* LI-KAI TSAI,* YA-FANG CHEN,y HON-MAN LIU,y YING-AN CHEN,* YU-LIN HSIEH,* SHIH-HUNG YANG,z YU-HSUAN TIEN,x CHI-CHENG YANG,x MENG-FAI KUO,z and JIANN-SHING JENG* * Stroke Center and Department of Neurology, National Taiwan University Hospital, Taipei, Taiwan; y Department of Medical Imaging, National Taiwan University Hospital, Taipei, Taiwan; z Department of Neurosurgery, National Taiwan University Hospital, Taipei, Taiwan; and x Division of Clinical Psychology, Department of Occupational Therapy, College of Medicine, Chang-Gung University, Taoyuan, Taiwan (Received 11 February 2016; revised 9 June 2016; in final form 13 July 2016)
Abstract—The marked cerebral hypoperfusion of moyamoya disease (MMD) can be treated with encephaloduroarteriosynangiosis (EDAS), an indirect revascularization surgery. Collateral establishment after the surgery is a gradual process; thus, easy access to serial assessment is of great importance. We prospectively recruited 15 pediatric moyamoya patients who underwent EDAS surgeries on a total of 19 hemispheres. Ultrasonography of extracranial and intracranial arteries was performed pre-operatively and post-operatively at 1, 3 and 6 mo. Among the extracranial arteries, the superficial temporal artery had the most pronounced increase in flow velocity and decrease in flow resistance from 1 mo post-surgery (p , 0.01). Among the large intracranial arteries, a significant increase in peak systolic velocity was observed in the anterior cerebral artery from 3 mo post-surgery (p , 0.05). These findings indicate significant hemodynamic changes on ultrasonography in pediatric moyamoya patients after indirect revascularization surgery. (E-mail: [email protected]) Ó 2016 World Federation for Ultrasound in Medicine & Biology. Key Words: Moyamoya disease, Pediatric stroke, Encephaloduroarteriosynangiosis, Indirect revascularization, Ultrasonography.
Moyamoya disease has a progressive course (Suzuki and Takaku 1969), which makes follow-up mandatory for this disease. Cerebral angiography is the gold standard tool for diagnosis and follow-up for MMD; however, the risks of permanent neurologic deficit and radiation exposure are ongoing safety concerns (Perren et al. 2005). Ultrasound is another non-invasive tool for the evaluation of hemodynamics; however, for MMD it is reported only for baseline status (Lee et al. 2004; Ruan et al. 2006) or for evaluations conducted after direct bypass surgery (Kraemer et al. 2012; Wu et al. 2011) but not for indirect revascularization surgery. The baseline characteristics revealed by ultrasound include an increase in resistance and a decrease in flow velocity in the common carotid artery (CCA) and ICA, as well as decreased resistance and increased flow velocity in the superficial temporal artery (STA) resulting from the effects of compensation (Ruan et al. 2006). The stenotic intracranial arteries commonly exhibit low or high flow velocity (Lee et al. 2004; Ruan et al. 2006). After direct bypass surgery, the patency of the STA graft is
INTRODUCTION Moyamoya disease (MMD) is characterized by idiopathic chronic progressive stenosis or occlusion of bilateral distal internal carotid arteries (ICAs) and their major branches (Suzuki and Takaku 1969). The marked cerebral hypoperfusion in moyamoya patients usually presents as ischemic stroke (IS) or transient ischemic attack (TIA) (Scott and Smith 2009). The incidence and prevalence of MMD are higher in Asian populations (Baba et al. 2008; Chen et al. 2014; Duan et al. 2012; Han et al. 2000); nonetheless, this disease is also a major cause of pediatric stroke in Western countries (Currie et al. 2011). The ischemic events associated with MMD can be reduced by extracranial–intracranial (EC-IC) bypass surgery, including direct, indirect and combined surgeries (Bao et al. 2015).
Address correspondence to: Jiann-Shing Jeng, Department of Neurology, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei 100, Taiwan. E-mail: [email protected] 1
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associated with increased flow velocity and decreased resistance in the STA on ultrasound (Wu et al. 2011); however, the exact changes in the ultrasound images after indirect revascularization surgery remain unclear. Encephaloduroarteriosynangiosis (EDAS) surgery is one kind of indirect revascularization surgery, particularly for pediatric moyamoya patients using STA as a feeding artery. We hypothesized that the STA should exhibit significant changes on ultrasonography after EDAS compared with the pre-operative state. Thus, we compared ultrasonographic parameters between the preand post-operative states on the operated side to characterize serial changes in the extracranial and intracranial arteries after EDAS in moyamoya patients. In addition, because progression of MMD may confound the postoperative changes, we compared the hemodynamic parameters on the operated side with those for the contralateral non-operated side at serial time points. METHODS Patients Between July 2012 and July 2014, consecutive pediatric moyamoya patients (,20 y of age) who had been diagnosed by cerebral angiography and were scheduled to undergo EDAS at the National Taiwan University Hospital were prospectively enrolled for this study. All but one patient had not undergone surgery for MMD before being enrolled; the exception had undergone EDAS on one side, and so this hemisphere was excluded from analysis because of a lack of pre-operative ultrasonographic data. All patients underwent follow-up angiography (cerebral angiography or magnetic resonance angiography) after EDAS to check for collateral establishment and disease progression. The demographic characteristics, neurologic events, angiographic findings and surgical complications of each patient were recorded. This study was approved by the Institutional Ethics Committee, and all enrolled patients and their parents gave informed consent. Ultrasonographic assessment In the present study, ultrasonographic examination was arranged before surgery and at 1, 3 and 6 mo afterward. The extracranial and transcranial ultrasound studies were performed using a color-coded ultrasound system (IE33, Philips Medical Systems, Bothell, WA, USA). These ultrasound examinations were performed by one neurologic ultrasound technician. Extracranial ultrasound study. Extracranial arteries were assessed using an 11-3 MHz linear-array transducer. For the extracranial arteries, we measured peak systolic velocity, end-diastolic velocity, resistance index and flow volume of the CCA, ICA, external carotid artery (ECA) and STA. The ICA was measured 1.5–2 cm above the
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carotid bifurcation, and the ECA was assessed at the proximal ECA segment before the branching of the superior thyroid artery. The STA was analyzed at the common STA segment at the level of the ear. The flow volume of each vessel was calculated from the time-averaged mean flow velocity of the cross-sectional area of the individual vessel; this formula has been built into the ultrasound software. The mean flow velocity was calculated from the mean of all instant velocities within the spectrum over the heart cycle. In terms of the diameter of each vessel for calculation of cross-sectional area, we measured the diameter between inner luminal walls at end-diastole; we measured once for each vessel because pediatric patients were unable to tolerate prolonged examinations. Transcranial color-coded sonography. Transcranial color-coded sonography (TCCS) was performed using a 5-1 MHz phased-array probe with angle correction. For the intracranial arteries, we measured peak systolic velocity, mean flow velocity and pulsatility index of the anterior cerebral artery (ACA), middle cerebral artery (MCA) M1 and M2 segments and posterior cerebral artery (PCA) on color Doppler images. The formula for determining mean flow velocity is built into the ultrasound software, and these data were automatically displayed. The highest flow velocity along the course of the individual vessel was recorded. Statistical analysis Categorical variables are presented as percentages, and continuous or discrete variables as means 6 standard deviations. Student’s paired t-test was used for univariate analysis between groups. First, we compared the hemodynamic parameters between the pre- and post-operative states. Cerebral hemispheres without complete postoperative follow up at these time points were excluded. Second, we compared the hemodynamic parameters on the operated side with those for the contralateral non-operated side after excluding patients who had undergone surgery on the contralateral side. Two-tailed p values , 0.05 were considered to indicate statistical significance. Data management and analysis were performed using Small Stata software (StataCorp LP, College Station, TX, USA). RESULTS Basic characteristics of these patients Among the 15 patients enrolled in the study (Table 1), the mean age was 10.4 6 4.6 y (range: 5–19 y), which included 11 males and 4 females. EDAS was performed on 19 cerebral hemispheres. Six of these also underwent indirect revascularization surgeries in addition to EDAS, including multiple-burr-hole surgery (MBH) (n 5 3), encephaloperiosteosynangiosis (EPS) (n 5 2) and encephalomyosynangiosis (EMS) (n 5 1). The most common
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Table 1. Characteristics of the 15 patients with moyamoya disease Patient
1
Age (y)/sex Hemispheres enrolled in analysis Other indirect revascularization surgeries in addition to EDAS Pre-op presentations, IS or TIA Epilepsy Developmental delay Headache Pre-op IQ score 30-d post-op ipsilateral IS Post-op IQ score
13/F L
2
3
12/M 10/M R, L R
MBH
4
5
6
7
5/M L, R
13/M L
7/F L
5/M L
EPS
EMS
MBH
IS, TIA
TIA
TIA
IS, TIA
(2)
(1) (1)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(1) (2)
(2) 86 (2)
(2) 124 (2)
(2) 117 (2)
(2)
(2) 126 (2) 117
130
(2)
IS, TIA IS, TIA
8
9
10
11/M 19/F 18/F L R L
11
12
13
14
15
6/M L,R
13/M R
14/M L
5/M L, R
5/M R
EPS
MBH
TIA
TIA
(2) IS, TIA
IS
IS, TIA IS, TIA IS, TIA
(1) (1)
(1) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) (2)
(2) 131 (2)
(2) 60 (2)
(2) 105 (2)
(1) 110 (2)
(1) 122 (2)
(2) 78 (2)
(1) 123 (2)
(2)
(2) 89 (2)
(2) 107 (2)
114
54
103
109
123
95
120
95
108
(1)
EDAS 5 encephaloduroarteriosynangiosis; EMS 5 encephalomyosynangiosis; EPS 5 encephaloperiosteosynangiosis; IS 5 ischemic stroke; MBH 5 multiple-burr-hole surgery; TIA 5 transient ischemic attack.
clinical presentation was TIA (n 5 12, 80%), followed by IS (n 5 9, 60%), epilepsy (n 5 4, 27%), headache (n 5 3, 20%) and developmental delay (n 5 2, 13%). One patient (7%) without symptom was diagnosed because of a positive family history. The pre-operative IQ scores were mostly average to superior. The duration of symptoms before EDAS surgery
was shorter for patients who presented with ischemic stroke/TIA (2.4 6 3.1 y) and longer for patients who manifested epilepsy (4.8 6 3.9 y). The 30-d rate of post-operative ipsilateral ischemic stroke was 5% (1 event/19 operations). During follow-up periods of 18–44 mo, there were no other recurrent ISs. Only one patient had more than three
Fig. 1. Serial hemodynamics of extracranial arteries determined using ultrasonography after indirect revascularization surgery compared with pre-operative state. (a) STA. (b) ECA. (c) ICA. ECA 5 external carotid artery; ICA 5 internal carotid artery; STA 5 superficial temporal artery.
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ipsilateral TIAs, and thus, he later underwent ipsilateral EPS. Overall, these patients had significantly fewer ischemic events and stationary IQ scores after indirect revascularization surgery compared with the pre-operative state. Postsurgical angiography revealed that 82% of the hemispheres were Matsushima grade A or B, indicating good collateral establishment (Matsushima et al. 1992). Temporal alteration of hemodynamics in hemispheres that underwent indirect bypass surgery The ultrasonographic features of extracranial and intracranial arteries are illustrated in Figures 1 and 2. Among the extracranial arteries, the STA exhibited the most pronounced hemodynamic changes after indirect bypass surgery (Fig. 1). From 1 mo after surgery, we observed a significant increase in end-diastolic velocity (139% increase, p , 0.01) and flow volume (99% increase, p , 0.01) in the STA, as well as a decrease in resistance index (15% decrease, p , 0.01), compared with the pre-operative state. These changes plateaued at 3 mo post-surgery (97% increase in peak-systolic veloc-
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ity, p , 0.01; 386% increase in end-diastolic velocity, p , 0.01; 168% increase in flow volume, p , 0.01; 22% decrease in flow resistance, p , 0.01). The ECA exhibited patterns similar to those of the STA. In contrast, the ICA had a gradual decrease in flow and increase in resistance index, particularly 6 mo post-surgery. Among the intracranial arteries, the ACA exhibited the most pronounced temporal changes after indirect bypass surgery. In 11 hemispheres (58%), ACA flow could not be detected before the surgery. The ACA exhibited a significant increase in peak systolic velocity 3 mo post-surgery (75% increase, p 5 0.04) (Fig. 2). The MCA and PCA both exhibited a tendency toward a gradual decrease in flow velocity. Difference between arteries on operated and nonoperated contralateral sides We then compared the ultrasonographic results of the hemisphere that underwent surgery with those of the contralateral hemisphere that did not undergo surgery to provide a side-by-side comparison of hemodynamic properties. EDAS on the contralateral hemisphere was often performed
Fig. 2. Serial hemodynamics of intracranial arteries determined using transcranial Doppler after indirect revascularization surgery compared with pre-operative state. (a) ACA. (b) MCA. (c) PCA. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery; PCA 5 posterior cerebral artery.
US after indirect revascularization in moyamoya disease d S.-J. YEH et al.
within 6 mo of the first EDAS in these cases. Once the contralateral hemisphere was operated, it was excluded from the analysis. Therefore, a total of 14 contralateral hemispheres were analyzed pre-surgery and the first month after operation, 11 hemispheres were analyzed the third month and 5 hemispheres were analyzed the sixth month. Among the extracranial arteries (Fig. 3), the STA exhibited the most pronounced side differences in all parameters (peak systolic and end-diastolic velocities, resistance index and flow amount) in this side-by-side comparison, between the first and sixth months post-surgery. The ECA exhibited significant side differences only at the third month post-surgery. The ICA on the operated side had lower velocity than that on the contralateral side before surgery, and this situation persisted until 6 mo post-surgery. Among the intracranial arteries (Fig. 4), the MCA exhibited differences in the side-by-side comparison after surgery. The MCA on the operated side exhibited a trend toward lower peak systolic velocity, compared with the contralateral side (74 cm/s vs. 148.5 cm/s, p 5 0.05), at 3 mo post-surgery. Serial ultrasonographic changes of a case with MMD after EDAS surgery In Figure 5 are serial ultrasonographic findings for a 5y-old boy with MMD who underwent EDAS. Compared with the pre-operative state, there were increases in peak systolic (from 88 to 173 cm/s) and end-diastolic (from 16
5
to 83 cm/s) velocities, a decrease in resistance index (from 0.82 to 0.52) and an increase in flow volume (from 11 to 61 mL/min) of the STA 1 mo post-surgery (Fig. 5a). The flow velocity and flow volume of the STA plateaued at the third month. The ipsilateral MCA exhibited slow flow velocity with dampened waveforms before surgery. At 6 mo after EDAS, peak systolic flow velocity of the ipsilateral MCA decreased from 49 to 44 cm/s, and flow resistance increased from 0.34 to 0.79 (Fig. 5b). The ipsilateral ACA was undetectable before the surgery; however, it became detectable 6 mo post-surgery (Fig. 5b). Flow velocity of the ipsilateral PCA was very high before surgery and dropped dramatically 1 mo postsurgery, followed by a slight increase 3 mo post-surgery. DISCUSSION This study revealed significant changes in hemodynamic parameters as manifest in the temporal and spatial patterns observed in the ultrasonographic results after indirect revascularization surgery on pediatric moyamoya patients. Among the extracranial arteries, the STA exhibited the most pronounced hemodynamic changes. Among the intracranial arteries, the temporal changes in the ACA were the most pronounced. The significant hemodynamic changes in the STA detected by ultrasound after indirect revascularization
Fig. 3. Differences in extracranial arteries between operated side and contralateral non-operated side before and after indirect revascularization surgery on ultrasonography. (a) STA. (b) ECA. (c) ICA. ECA 5 external carotid artery; ICA 5 internal carotid artery; STA 5 superficial temporal artery.
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Fig. 4. Differences in intracranial arteries between operated side and contralateral non-operated side before and after indirect revascularization surgery on ultrasonography. (a) ACA. (b) MCA. (c) PCA. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery; PCA 5 posterior cerebral artery.
surgery are somewhat similar to those observed after direct bypass surgery (Kraemer et al. 2012; Wu et al. 2011). The parameters of the STA and ECA that underwent significant post-operative changes compared with pre-operative values were flow velocities (peak systolic and end-diastolic) and resistance after direct bypass surgery (Kraemer et al. 2012) or indirect revascularization surgery (present study). The increase in flow volume was largely attributed to the increased flow velocity, especially the end-diastolic velocity. Because it is the donor artery in indirect revascularization surgeries, the increased flow in the STA can be caused by the establishment of intracranial collaterals. However, the two procedures differ with respect to the speed of collateral establishment. In this study, the hemodynamic plateau after indirect revascularization surgery occurred at 3 mo, whereas the plateau after direct bypass surgery occurs as early as 1 wk post-surgery (Wu et al. 2011). This difference in these temporal profiles indicates that there
are differences in the revascularization process between indirect revascularization and direct bypass. The present study revealed that the ICA on the operated side underwent a gradual decrease in flow after indirect bypass surgery, which may be related to progressive stenosis of the ICA or decreased demand from the ICA. Previous angiographic studies have reported acceleration in the progression of ICA stenosis after bypass surgery (Huang et al. 2009). Furthermore, a decrease in demand from the ICA may also occur after the establishment of collaterals. Our findings also revealed significant temporal changes in the hemodynamic parameters of the ACA after indirect bypass surgery, which manifested as increased flow velocity and decreased resistance. In addition, the ACAs of the 11 hemispheres were undetectable before the operation, and there was only one hemisphere with an undetectable ACA 6 mo after indirect revascularization surgery. If the ACA were occluded by a thrombus,
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Fig. 5. Ultrasonographic findings for a 5-y-old moyamoya patient who underwent encephaloduroarteriosynangiosis surgery on the left side: (a) Carotid Doppler study revealing serial changes in the left superficial temporal artery. (b) Transcranial Doppler study revealing pre-operative MCA, as well as post-operative left MCA and ACA 6 mo after encephaloduroarteriosynangiosis. The ACA was undetected before the operation. The MCA was detected at a depth of 45–46 mm, and the ACA, at a depth of 74 mm. ACA 5 anterior cerebral artery; MCA 5 middle cerebral artery.
it would not open again after the surgery. Thus, the failure to detect the ACA before surgery probably indicated very low flow in the ACA, which was likely to be missed in detection. After indirect revascularization surgery, the ACA was detected because of the increased flow, which probably came from collateral vessels. This phenomenon also indicates that indirect revascularization surgery may improve perfusion in the ACA territory. Furthermore, even though the flow velocity of the MCA trunk decreased after surgery, there were significantly fewer ipsilateral ISs or TIAs after surgery. This indicates that the collaterals played a more important role than the MCA trunk in supplying MCA territory in moyamoya patients. Another study using perfusion SPECT reported that EDAS can improve perfusion in the MCA territory (Song et al. 2012). However, it was difficult to prove progressive stenosis of the MCA with TCCS because the diameter of the MCA cannot be measured. In addition, the PCA had abnormally high flow velocity before surgery that decreased after indirect bypass surgery. This change in the PCA may result from a decrease in the need for compensation from the PCA or progressive stenosis of the PCA (Huang et al. 2009). Previous literature on ultrasonographic changes after combined direct bypass surgery and encephalomyosynangiosis (EMS) in children with moyamoya children indicated ultrasonographic changes correlated well with angiography (Perren et al. 2005). They used power Doppler imaging to detect low flow of neoangiogenesis and concluded that the degree of neoangiogenesis on ultrasound had a good correlation with that on angiography. We used color Doppler instead of power Doppler in this
study, which might have reduced sensitivity in detecting low flow, especially in the pre-operative state. The present study had several limitations. First, the number of cases was small as MMD is a rare disease. Second, the first follow-up was conducted 1 mo post-surgery, which made it impossible to clarify when the earliest hemodynamic changes occurred after indirect revascularization surgery. Third, in terms of measurement of flow volume, the diameter of each vessel was measured at end-diastole, which would result in an underestimate flow volume. Fourth, six cases also underwent indirect revascularization surgeries in addition to EDAS; therefore, these changes were not purely secondary to EDAS surgery. However, these features can represent the changes after indirect revascularization surgeries and are more compatible with real-world conditions. The strength of this study lies in the fact that it is the first study to use ultrasonography to visualize sequential as well as spatial changes in hemodynamic parameters after successful indirect revascularization surgery. In the future, for any moyamoya patient, post-operative ultrasonographic changes that deviate from the pattern outlined in this study may indicate inadequate revascularization, and further angiographic investigation will be warranted. CONCLUSIONS This study found that ultrasonography is effective in revealing temporal and spatial changes in hemodynamic parameters after indirect revascularization surgery. Regular follow-up of moyamoya patients after indirect revascularization surgery, particularly in the first 3 mo, is
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suggested for the early confirmation of revascularization status. Acknowledgments—This study was supported in part by a grant from the National Science Council and Ministry of Science and Technology, Taiwan (MOST 103-2321-B-002-033). The funding source had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
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