European Journal of Radiology 71 (2009) 450–455
Intracranial cerebral artery stenosis with associated coronary artery and extracranial carotid artery stenosis in Turkish patients Ozlem Alkan a,∗ , Osman Kizilkilic a , Tulin Yildirim a , Hakan Atalay b a
Department of Radiology, Baskent University, Faculty of Medicine, Ankara, Turkey Department of Cardiovascular Surgery, Baskent University, Faculty of Medicine, Ankara, Turkey Received 29 November 2007; received in revised form 30 April 2008; accepted 2 May 2008
Abstract Purpose: Although it has been demonstrated that there is a high prevalence of extracranial carotid artery stenosis (ECAS) in patients with severe coronary artery disease, intracranial cerebral artery stenosis (ICAS) is rarely mentioned. We evaluated the prevalence of ICAS in patients with ECAS having elective coronary artery bypass grafting (CABG) surgery to determine the relations between ICAS, ECAS and atherosclerotic risk factors. Methods: We retrospectively reviewed the digital subtraction angiography findings of 183 patients with ECAS ≥ 50% preparing for CABG surgery. The analyses focused on the intracranial or extracranial location and degree of the stenosis. The degree of extracranial stenoses were categorized as normal, <50%, 50–69%, 70–89%, and 90–99% stenosis and occluded. The degree of intracranial stenosis was classified as normal or ≤25%, 25–49%, and ≥50% stenosis and occluded. Traditional atherosclerotic risk factors were recorded. Results: ECAS < 70% in 42 patients and ECAS ≥ 70% in 141 patients. ICAS was found in 51 patients and ICAS ≥ 50% in 30 patients. Regarding risk factors, we found hypertension in 135 patients, diabetes mellitus in 91 patients, hyperlipidemia in 84 patients, and smoking in 81 patients. No risk factor was significant predictors of intracranial atherosclerosis. The severity of ICAS was not significantly associated with that of the ECAS. Conclusions: We found ICAS in 27.8% of the patients with ECAS > 50% on digital subtraction angiography preparing for CABG. Therefore a complete evaluation of the neck vessels with magnetic resonance or catheter angiography seems to be indicated as well as intracranial circulation for the risk assessment of CABG. © 2008 Elsevier Ireland Ltd. All rights reserved. Keywords: Extracranial carotid artery stenosis; Intracranial cerebral artery stenosis; Digital subtraction angiography; CABG
1. Introduction Coronary artery bypass grafting (CABG) surgery is a frequent surgical procedure that may be associated with neurologic complications. Risk factors of CABG-associated neurologic complications include hypertension, carotid stenosis, previous stroke, diabetes mellitus, and age ≥ 65 years . Cerebral ischemia during the CABG may be induced by hypotension–hypoperfusion, intraoperative embolization, or most probably, by the combination of some of these factors . Stroke is an important complication affecting the outcome after CABG surgery. Carotid stenosis is
Corresponding author at: Baskent University, Adana Teaching and Medical Research Center, Department of Radiology, 01250 Yuregir, Adana, Turkey. Tel.: +90 322 327 27 27; fax: +90 322 327 12 70. E-mail address: [email protected]
(O. Alkan). 0720-048X/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2008.05.006
recognized as a major risk factor for stroke after CABG . Intracranial atherosclerosis is one of the main causes of ischemic stroke worldwide and frequently occurs in the setting of widespread vascular disease . Thus, intracranial cerebral artery involvement may be expected in patients with coronary artery disease, and an intracranial cerebral artery stenosis (ICAS) also may be a risk factor for stroke after CABG . We hypothesized that patients preparing for elective CABG would have an ICAS of varying degrees, depending on age, sex, severity of extracranial carotid artery stenosis (ECAS), hypertension, diabetes mellitus, hyperlipidemia, peripheral vascular disease, and smoking. 2. Materials and methods Patient selection: Patients in our practice with a diagnosis of carotid stenoses greater than 50% on Doppler analysis
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were referred for carotid angiography or carotid magnetic resonance angiography. During the 5 years between December 2002 and March 2007, 655 patients were admitted into our hospital and underwent transfemoral intra-arterial four-vessel cerebral angiography. Among these, 183 consecutive patients associated with severe coronary artery disease preparing for CABG surgery on the basis of coronary angiography were included in this study. Patients without severe coronary artery disease were excluded from this study. To prevent contrast material overload, we did not do a carotid angiography or a coronary angiography. This retrospective study was approved by the institutional review board of the University. Written informed consent was obtained from all patients. Clinical assessments: Clinical information was obtained from the medical records at our hospital. We investigated the presence or absence of hypertension, diabetes mellitus, hyperlipidemia, peripheral vascular disease, and the habit of smoking. Hypertension (previously diagnosed and treated or systolic pressure > 140 mm Hg and/or diastolic pressure > 90 mm Hg, and categorized as successfully treated or untreated), diabetes (previously diagnosed and treated or fasting glucose >126 mg/dL, and categorized as type 1 and type 2), hyperlipidemia (previously diagnosed and treated, fasting serum cholesterol >240 mg/dL, or low-density lipoprotein cholesterol >160 mg/dL), and smoking (current smoker or ex-smoker who quit within 5 years of the study, and the amounts smoked were recorded as pack-years) were noted. Prior history of stroke or transient ischemic attack was recorded. Ischemic strokes were classified in the following categories: large-vessel stroke, small-vessel stroke, cardioembolic stroke, other cause, and undetermined cause. We also collected information about the history of intermittent claudication, rest pain, ulceration/minor tissue loss or gangrene. Vascular assessments: Angiography was performed on all 183 patients. The angiographic examinations were performed by a single neuroradiologist (OK). All were accomplished without complication. Selective intra-arterial digital subtraction angiography (DSA) was performed via a unilateral femoral approach under local anesthesia using a standard Seldinger technique, by automatic injection of 4–8 mL/sn of iohexol (Omnipaque 240) per injection. The total volume of contrast used was 120 mL. Automated radiation dose was noted after each procedure from the machine and the average radiation dose was 524 mGy. Average six series were obtained per patient. The DSA runs were obtained at 3–4 frames/s to late venous phase by using a matrix of 1024 × 1024, 30 cm FOV. Arch aortogram, selective common carotid artery, subclavian artery, and both vertebral artery (VA) injection images were obtained. Standard anteroposterior and lateral views of the extracranial and intracranial circulations were obtained routinely. Oblique projections were acquired when needed to clarify significant findings. All images were viewed by two neuroradiologists (OA and OK, working in consensus) on a digital work-station. Locations of stenosis were categorized as being in the intracranial or extracranial vessels. Intracranial segments were defined as those at or above the precavernous or upper petrous carotid artery in the anterior circulation. For the vertebral artery, the distinction was made at the
point where the artery pierced the dura at the level of foramen magnum. North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria were used for carotid stenosis calculations: [(Dn − Ds )/Dn ] × 100, where Dn is normal diameter and Ds are stenosed diameter. The degree of ECAS and stenosis in the extracranial segment of the vertebral artery was classified as normal, <50%, 50–69%, 70–89%, and 90–99% stenosis (near occlusion), or occluded. Intracranial stenosis was measured by using a previously described technique . This measurement was based on the ratio of the narrowest diameter on any projection to that of the portion of the artery nearest the stenosis that is judged to be normal. The proximal portion of the artery is the first choice for the normal segment. However, when the stenosis involved the proximal portion of the artery or the evidence suggested significant atherosclerotic disease, the distal segment of the artery beyond the stenosis was used. When tandem intracranial lesions were present, the percentage of stenosis in both sites was measured and the more severe stenosis was selected. The degree of stenosis in the intracranial segment of the internal carotid artery, stenosis in the intracranial segment of the vertebral artery, and stenosis in the basilar artery were classified as normal or ≤25%, 25–49%, ≥50% stenosis and occlusion. The cardiac angiography was performed by cardiologists. Statistical analyses: The results are expressed as percentages. Univariate analyses were performed to assess the association between the prevalence of ICAS with the possible risk factors and severity of ECAS. All variables were analyzed using Pearson χ2 test, Fisher’s χ2 test, or Mantel–Haenszel χ2 test as appropriate. The t-test was utilized to compare ages. A multiple logistic regression analysis was used to estimate independent effects of the predictive variables on the cerebral arterial occlusive lesions. The analysis was repeated for the extracranial carotid artery and intracranial arteries, with each abnormality as a dependent variable and with background characteristics including possible risk factors as independent variables. The level significance was set at p < 0.05 for all statistical analyses. Data were analyzed through SPSS software (Statistical Package for the Social Sciences, Version 11.0, SPSS Inc., Chicago, IL, USA). 3. Results The patient group included 132 men and 51 women (mean age, 65.8 ± 8.4 years; age range, 46–85 years). Of the patients with ECAS, 42 (23%) had stenosis of 50–69%, 56 (30.6%) had stenosis of 70–89%, 46 (25.1%) had stenosis of 90–99%, and 39 (21.3%) had occlusion. ECAS of more than 70% narrowing were detected in 77% of the subjects. In 51 patients with ICAS, we found 57 intracranial vessels with stenosis. Twenty-four patients (13.1%) with intracranial cerebral artery stenosis displayed stenosis of >50%, and 6 patients displayed occlusion (3.3%), and stenosis of 25–49% was observed in 21 of the patients. The petrocavernous segment of the internal carotid artery was the most commonly involved site (36 vessels, 63.1%), followed by the basilar artery (7 vessels, 12.2%), the intracranial segment of the vertebral artery (7 vessels, 12.2%), the supraclinoid segment of internal carotid artery (5 vessels, 8.7%), the M2 segment of middle cerebral
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artery (1 vessel, 1.7%), and the A2 segment of the anterior cerebral artery (1 vessel, 1.7%). The distribution of ICAS by site and severity is shown in Table 1. The severity of ICAS was not significantly associated with the severity of ECAS. The severity and prevalence of ICAS and ECAS are summarized in Table 2. Seven patients had tandem lesions of the internal carotid artery (defined as stenosis of extracranial segment >70%, stenosis of intracranial segment >50%) (Fig. 1A and B). Among the 92 patients with extracranial vertebral artery stenosis (50.3%), 25 (13.7%) had stenosis of <50%, 10 (5.5%) had stenosis of 50–69%, 14 (7.7%) had stenosis of 70–89%, 13 (7.1%) had stenosis of 90–99%, and 30 (16.4%) had occlusion. Among the 135 patients with hypertension (73.7%), 40 had well-controlled disease. Among the 91 patients with diabetes in 91 (49.7%), 35 had well-controlled disease and 80 had type 2. Eighty-four patients (45.9%) had hyperlipidemia, 81 (44.2%) had smoking, and 53 (28.9%) had peripheral vascular disease. Of these, 44 patients (83%) had intermittent claudication ranging from mild to severe (categories I–III according the Rutherford classification) and the remaining 9 patients (17%) had rest pain, ulceration/minor tissue loss or gangrene, which was defined as critical limb ischemia (categories IV–VI). Prior history of stroke/transient ischemic attack was found in 50 patients (27.3%). Of the 50 cerebral infarctions, 35 were large-vessel stroke, 15 were small-vessel stroke. According to univariate analyses, risk factors such as hypertension, diabetes, hypercholesterolemia, smoking, and hyperlipidemia were not significant predictors of intracranial atherosclerosis. Smoking was the predictive factor for ECAS (p < 0.5). Other risk factors were not significant predictors for ECAS. Multiple logistic regression analyses revealed that
smoking was the significant and independent predictor of ECAS. Table 3 shows correlations between risk factors and occlusive lesions in cerebral arteries. 4. Discussion CABG provides definite clinical advantages in patients with coronary artery disease. However, patients who undergo CABG are subject to marked hemodynamic fluctuations; a change in body temperature, a rapid reduction in hematocrit, and a loss of pulsatile flow. Therefore, CABG surgery may be associated with neurological complications. The incidence of such complications is 0.4–5.7% for stroke, 10–28% for delirium, and 33–83% for persistent cognitive dysfunction and behavioral change . ECAS is well known to increase the operative risk of stroke. To reduce the stroke rate, many institutions perform routine preoperative assessment of the carotid arteries before CABG surgery . Carotid endarterectomy or angioplasty/stenting is recommended if the stenosis is significant . Intracranial atherosclerosis carries a risk of stroke of 8–22% per annum and may have varying degrees of risk based on the location and severity of the stenosis. There are at least four proposed mechanisms of stroke caused by intracranial stenosis: hypoperfusion, thromboembolic occlusion distal to the site of stenosis, thrombosis at the site of stenosis, occlusion of small penetrating arteries. Intracranial stenosis as a cause for stroke/transient ischemic attack is suggested by a history of recurrent symptoms or infarcts in the same vascular territory or infarcts in the classic watershed distribution. Typical locations for intracranial atherosclerotic stenosis are petrous and cavernous siphon segments of the ICA, the middle cerebral artery, the paracranial and intracranial vertebral arteries, and the
Table 1 Distribution of ICAS by site and severity <50%
Petrocavernous Basilar artery Intracranial vertebral artery Supraclinoid MCA M2 ACA A2
20 (35%) 3 (5.2%) 2 (3.5%) 1 (1.7%) – –
15 (26.3%) 4 (7%) 3 (5.2%) 2 (3.5%) – –
1 (1.7%) – 2 (3.5%) 2 (3.5%) 1 (1.7%) 1 (1.7%)
36 (63.1%) 7 (12.2%) 7 (12.2%) 5 (8.7%) 1 (1.7%) 1 (1.7%)
MCA, middle cerebral artery; ACA, anterior cerebral artery.
Table 2 Severity and prevalence of carotid atherosclerosis ICAS
Normal <50% >50% Occlusion
25 (13.6%) 5 (2.7%) 10 (5.4%) 2 (1.1%)
37 (20.2%) 10 (5.4%) 7 (3.8%) 2 (1.1%)
37 (20.2%) 3 (1.6%) 4 (2.1%) 2 (1.1%)
33 (18.03%) 3 (1.6%) 3 (1.6%) –
132 (72.1%) 21 (11.4%) 24 (13.1%) 6 (3.3%)
ECAS, extracranial carotid artery stenosis; ICAS, intracranial cerebral artery stenosis.
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Fig. 1. A 72-year-old woman presented with unstable angina. She had right hemiparesis due to a stroke 2 months earlier. Her risk factors included diabetes mellitus and hypertension. (A) Lateral left common carotid angiography shows high-grade stenosis of the bulb segment of the left internal carotid artery and (B) anteroposterior intracranial angiogram shows occlusion of the distal segment of the left internal carotid artery.
basilar artery. In NASCET, the infraclinoid portion of the ICA was affected seven times more often than the supraclinoid portion . Although most studies performed in patients preparing CABG are restricted to ECAS, ICAS are rarely mentioned. In this study, we used DSA to evaluate the neck vessels as well as the intracranial circulation. DSA provides excellent visualization of the intracranial vasculature and can detect occlusive changes not only in the extracranial but also in the intracranial
arteries. Our study showed ECAS ≥ 70% in 141 patients (77%) and ICAS ≥ 50% in 30 patients (16.4%). Seven patients had tandem lesions of the internal carotid artery. Several studies have classified ECAS and ICAS in patients with coronary artery disease [5,9–15] (Table 4). Previous studies in preparing CABG have reported frequencies of intracranial atherosclerosis varying from 13% to 71%. This variability may be explained by differences in the definition of stenosis, the patient characteristics, radiologic examination method, and the sample size. Uehara et al.  showed that the possibility of atherosclerosis in the intracranial arteries should be considered in aged ischemic heart disease patients. According to Yoon et al. , 30.3% of their patients undergoing CABG had an ICAS, which could increase the risk of neurologic complications. Uehara et al.  showed that the prevalence of extracranial and intracranial carotid artery stenoses in Japanese patients scheduled for CABG is considerably high and preoperative evaluation of cranial arteries is recommended, particularly in patients with peripheral vascular disease and infarcts in the basal ganglia. Uekita et al.  noted that serious coronary artery lesions were commonly accompanied by latent atherosclerotic lesions in the cervical and intracranial arteries besides silent brain infarction in patients with CAD. Ohuchi et al.  found an equal incidence of intracranial and extracranial vascular lesions and recommended examination of the carotid artery as well as intracranial arteries before CABG. Bae et al.  suggest that the correlation between coronary atherosclerosis and ECAS is stronger than that between coronary atherosclerosis and ICAS and the possibility of a race-based difference should be mentioned. Takami and Masumoto  suggested that the brain MRA-based selection of off-pump CABG can contribute to prevention of stroke in neurologically high-risk patients. Goto et al.  show that women and men present for CABG surgery with different strokeassociated comorbidities and women have a higher frequency of intracranial artery stenoses. Nakamura et al.  suggested that careful vascular evaluation before and during CABG can improve surgical outcomes. The prevalence of a significant carotid stenosis in patients undergoing CABG ranges from 8.5% to 19.9%, although the definitions of significant stenosis among the studies range from 50% or greater to 80% or greater . Of the patients with ECAS in our study, 42 (23%) had stenosis of <70%, whereas stenoses >70% were found in 141 patients (77%). Severe ECAS (>70%) was higher than the previously reported rates [3,17,18]. The higher severity of ECAS and higher prevalence of ICAS in our study may be explained by the fact that we studied patients with ECAS > 50% preparing for CABG who may have had moreadvanced atherosclerotic diseases. Patients with ICAS, especially those with coexisting ECAS, are at higher risk of death or further vascular conditions . The presence of a tandem stenosis is important to decide on surgical and/or endovascular treatment . Thus, searching for intracranial lesions before CABG is just as important as searching for extracranial lesions. Intracranial angioplasty with conditional stent placement is technically feasible and clinically effective in producing a substantial reduction in long-term stroke and death.
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Table 3 Correlations between risk factors and occlusive lesions in cerebral arteries Odds ratio
ECAS Age > 70 years Male sex Hypertension Diabetes Hyperlipidemia Smoking habit PVD TIA
0.886 1.864 0.833 1.014 1.238 0.417 1.308 1.358
0.438–1.791 0.898–3.870 0.385–1.802 0.509–2.020 0.621–2.468 0.198–0.880 0.624–2.741 0.612–3.011
0.735 0.092 0.643 0.968 0.544 0.02 0.477 0.451
ICAS Age > 70 years Male sex Hypertension Diabetes Hyperlipidemia Smoking habit PVD TIA ECAS
0.839 0.789 0.976 1.040 1.046 1.882 0.970 2.281 0.467
0.429–1.643 0.389–1.600 0.465–2.048 0.545–1.985 0.547–2.002 0.959–3.697 0.477–1.974 1.147–4.536 0.226–0.967
0.609 0.511 0.949 0.905 0.892 0.064 0.934 0.522 0.078
ECAS, extracranial carotid artery stenosis; ICAS, intracranial cerebral artery stenosis; PVD, peripheral vascular disease; TIA, transient ischemic attack.
For symptomatic patients with a 50% intracranial stenoses who have failed medical therapy, balloon angioplasty with or without stenting should be considered. In patients with ICAS preparing for CABG, there is insufficient evidence to make definitive recommendations regarding endovascular therapy to prevent perioperative stroke [21,22]. However, preoperative identification of ICAS provides information regarding operative risk and avoids hypotension or dehydration during and after CABG . Additionally, preoperative vascular risk assessment can guide targeted surgical treatment options that reduce perioperative stroke in patients undergoing CABG . The previous studies have shown that the risk factors for occlusive lesions in the cervical carotid artery and intracranial arteries were different. Compared with extracranial stenoses, intracranial stenoses do not correlate as well with the typical atherosclerotic risk factors for peripheral and coronary vascular disease (i.e., male sex, hypercholesterolemia, and white race). In contrast, in certain races, other factors (e.g., Hispanic Americans, blacks, Asians, female sex, diabetes, and younger age)
are commonly associated with occlusive disease of intracranial arteries . We could not to determine a significant correlation between the incidence of risk factors and ICAS, as in the Uehara study . Alternatively, novel risk factors for atherosclerosis may be investigated. Recently, novel risk factors for atherosclerosis such as the presence of abdominal obesity, chronic infection, C-reactive protein, homocysteine, and insulin resistance are accepted . ICAS is clearly associated with some ethnic and geographic variables. Intracranial atherosclerosis is more common in US Hispanics, blacks, Japanese, and Chinese than in US whites . Our study found rates similar to those previously reported in Asian populations [23,25,26]. Some epidemiologic studies have shown that not only genetic factors but also environmental factors are associated with the distribution of atherosclerosis . The limitations of the present study must be mentioned. First, the best means of investigating ICAS and ECAS in this study was an intra-arterial DSA, which is invasive. Second, the study subjects were patients with >50% ECAS, and a control group
Table 4 Prevalence of ICAS and ECAS in patients preparing for CABG Author
Number of patients
Uehara et al.  Yoon et al.  Uehara et al.  Uekita et al.  Ohuchi et al.  Bae et al.  Takami and Masumoto  Goto et al.  Nakamura et al.  Our data
67 201 151 133 335 246 720 140 238 183
22.4 23.9 16.6 49.8 12.8 21.5 11.1 – 8.4 77
16.4 16.4 21.2 71.4 13.4 14.2 15.4 64 8.4 27.8
ECAS + ICAS (%) 13.9 11.1 14.6 – – – –
Examination MRA MRA MRA MRA MRA TCD + MRA MRA MRA MRA/3D-CTA DSA
MRA, magnetic resonance angiography; TCD, transcranial Doppler sonography; DSA, digital subtraction angiography; ECAS, extracranial carotid artery stenosis; ICAS, intracranial cerebral artery stenosis; 3D-CTA, three-dimensional computed tomography angiography.
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also should have been included as a reference. However, because we do not routinely do intra-arterial DSA for patients with ECAS < 50%, we could not create a control group. Because the study involved a selected population, our results cannot be generalized to all patients who undergo CABG. Third, in this study, postoperative stroke is not assessed. Further study is required to evaluate perioperative stroke in patients undergoing CABG with intracranial atherosclerosis. 5. Conclusions While the relevance of extracranial carotid stenoses in these patients is well known, data on intracranial stenoses are less clear mostly because of the lack of angiographic studies and the prevalence of screening with ultrasounds. The real prevalence of ICAS in these patients is not known and consequently, it is not clear when to investigate intracranial circulation in patients preparing for CABG. In our study, we found an ICAS in 27.8% of the patients with an ECAS > 50% on DSA preparing for CABG. Therefore, a complete evaluation of the neck vessels with magnetic resonance angiography or catheter angiography seems to be indicated as well as intracranial circulation for the risk assessment of CABG. Preoperative screening of the extracranial and intracranial carotid arteries may guide clinicians to the judicious use of endovascular therapy, which might improve the post-CABG outcomes. Acknowledgments We thank Ugur Ozkan, MD, and G¨ulsah Seydaoglu, MD, for their assistance with the statistical analyses and the preparation of the study. References  McKhann GM, Goldsborough MA, Borowicz Jr LM, et al. Predictors of stroke risk in coronary artery bypass patients. Ann Thorac Surg 1997;63(2):516–21.  Restrepo L, Wityk RJ, Grega MA, et al. Diffusion- and perfusion-weighted magnetic resonance imagings of the brain before and after coronary artery bypass grafting surgery. Stroke 2002;33(12):2909–15.  Faggioli GL, Curl GR, Ricotta JJ. The role of carotid screening before coronary artery bypass. J Vasc Surg 1990;12(6):724–9.  Arenillas JF, Candell-Riera J, Romero-Farina G, et al. Silent myocardial ischemia in patients with symptomatic intracranial atherosclerosis: associated factors. Stroke 2005;36(6):1201–6.  Yoon BW, Bae HJ, Kang DW, et al. Intracranial cerebral artery disease as a risk factor for central nervous system complications of coronary artery bypasses graft surgery. Stroke 2001;32(1):94–9.  Samuels OB, Joseph GJ, Lynn MJ, et al. A standardized method for measuring intracranial arterial stenosis. Am J Neuroradiol 2000;21(4):643–6.  Regli L, Meyer FB, Bogousslavsky J. Carotid endarterectomy. In: Ginsberg MD, Bogousslavsky J, editors. Cerebrovascular Disease: Pathophysiology, Diagnosis and Management. Malden, MA: Blackwell Science; 1998. p. 1907–30.
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