The Serial Change of Cerebral Hemodynamics by Vascular Territory after Extracranial-Intracranial Bypass Surgery in Patients with Atherosclerosis of Cerebral Arteries

죽상 동맥 경화성 뇌혈관 폐색 환자에서의 두개외강-내강 우회로술 후의 혈관 영역별 연속 혈류역학 변화

  • Hong, Il-Ki (Department of Nuclear Medicine, Asan Medial Center, Ulsan University School of Medicine) ;
  • Kim, Jae-Seung (Department of Nuclear Medicine, Asan Medial Center, Ulsan University School of Medicine) ;
  • Ahn, Jae-Sung (Department of Neurosurgery, Asan Medial Center, Ulsan University School of Medicine) ;
  • Kwon, Sun-Uck (Department of Neurology, Asan Medial Center, Ulsan University School of Medicine) ;
  • Im, Ki-Chun (Department of Nuclear Medicine, Asan Medial Center, Ulsan University School of Medicine) ;
  • Lee, Jai-Hyuen (Department of Nuclear Medicine, Asan Medial Center, Ulsan University School of Medicine) ;
  • Moon, Dae-Hyuk (Department of Nuclear Medicine, Asan Medial Center, Ulsan University School of Medicine)
  • 홍일기 (울산대학교 의과대학 서울아산병원 핵의학과) ;
  • 김재승 (울산대학교 의과대학 서울아산병원 핵의학과) ;
  • 안재성 (울산대학교 의과대학 서울아산병원 신경외과) ;
  • 권순억 (울산대학교 의과대학 서울아산병원 신경과) ;
  • 임기천 (울산대학교 의과대학 서울아산병원 핵의학과) ;
  • 이재현 (울산대학교 의과대학 서울아산병원 핵의학과) ;
  • 문대혁 (울산대학교 의과대학 서울아산병원 핵의학과)
  • Published : 2008.02.29

Abstract

Purpose: To assess the effect of extracranial-intracranial (EC-IC) bypass surgery on hemodynamic improvement, we evaluated serial regional cerebral hemodynamic change of the middle cerebral artery (MCA) in symptomatic patients with atherosclerotic occlusion of the internal carotid artery (ICA) or MCA using $^{99m}Tc$-ECD acetazolamide stress brain perfusion SPECT (Acetazolamide SPECT). Materials and Methods: The patients who had suffered a recent stroke with atherosclerotic ICA or MCA occlusion underwent EC-IC bypass surgery and Acetazolamide SPECT at 1 week before and three to six months after surgery. For image analysis, attenuation corrected images were spatially normalized to SPECT templates with SPM2. Anatomical automated labeling was applied to calculate mean counts of each Volume-Of-Interest (VOI). Seven VOIs of bilateral frontal, parietal, temporal regions of the MCA territory and the ipsilateral cerebellum were defined. Using mean counts of 7 VOIs, cerebral perfusion index and perfusion reserve index were calculated. Results: Seventeen patients (M:F =12:5, mean age $53{\pm}2yr$) were finally included in the analysis. The cerebral blood flow of the parietal region increased at 1 week (p = 0.003) and decreased to the preoperative level at 3-6 months (p = 0.003). The cerebrovascular reserve of the frontal and parietal regions increased significantly at 1 week after surgery (p<0.01) and improved further at 3-6 months. Conclusion: Cerebrovascular reserve of the MCA territory was significantly improved at early postoperative period after EC-IC bypass and kept improved state during long-term follow-up, although cerebral blood flow did not significantly improved. Therefore, cerebrovascular reserve may be a good indicator of postoperative hemodynamic improvement resulted from bypass effect.

목적: 내경동맥 또는 중대뇌동맥의 죽상 동맥 경화증 환자에서의 두개외강-내강 우회로술(이하 우회로술) 후의 연속적인 혈류 역학적 변화를 $^{99m}Tc$-ECD 아세타졸아마이드 부하 뇌혈류 단일 광자 방출 전산화 단층 촬영(이하 아세타졸아마이드 부하 SPECT)으로 평가하여 중대뇌 동맥의 각 분지별 영역에 대한 우회로술의 혈류역학적 개선효과를 알아보고자 하였다. 대상 및 방법: 전향적 방법으로 최근 3개월 내에 혈관 폐색성 징후가 발생하여 우회로술을 시행받은 환자를 대상으로 수술 전과 수술 1 주 후, 3-6 개월 후에 아세타졸아마이드 부하 SPECT를 시행하였다. 영상 분석을 위해 SPM의 SPECT 표준 뇌에 공간 정규화한 후 Anatomical Automated Labeling으로 중대뇌동맥의 지배를 받는 양측 전두, 측두, 두정 영역에 관심 구역을 설정하여 각 관심 영역별로 뇌혈류 지표(PI; $C_{region}/C_{ipsilateral\;cerebellum}$) 및 뇌혈관 예비능 지표$((PI_{acetazolamide}-PI_{basal})/PI_{basal})$로 정하여 이들 지표의 수술 전후 변화를 평가하였다. 결과한 측에 성공적인 우회로술을 시행한 환자 17 명(남:여=12:5, 나이 $53{\pm}2$세)을 분석하였다. 전체적으로 뇌혈류는 수술 1 주 후 유의하게 증가하나 3-6 개월 후 감소하여 수술 이전의 수준으로 유지되었으며 ($1.01{\pm}0.09{\rightarrow}1.06{\pm}0.09}{\rightarrow}1.02{\pm}0.10,\;p=0.005$) 뇌 혈관 예비능은 수술 1 주 후 유의하게 증가한 이후 유의하지는 않으나, 3-6개월 이후까지 계속 호전되었다($-0.14{\pm}0.05{\rightarrow}-0.07{\pm}0.04{\rightarrow}0.05{\pm}0.05,\;p=0.004$). 각 뇌 영역별로 뇌혈류는 두정 영역에서 수술 직후 증가하였다가($1.12{\pm}0.09{\rightarrow}1.18{\pm}0.09,\;p=0.003$) 수술 3-6개월 이후 감소하여($1.12{\pm}0.09,\;p=0.003$) 수술 이전의 수준으로 유지되었다. 뇌혈관 예비능은 수술 측의 전두 영역($-0.15{\pm}0.07{\rightarrow}0.08{\pm}0.05$), 두정 영역($-0.16{\pm}0.07{\rightarrow}-0.07{\pm}0.05$)에서 모두 수술 직후 유의하게 증가하였고(p<0.01) 이후 유의하지는 않으나 3-6개월까지 계속 호전되었다. 결론: 성공적인 우회로술 후 뇌혈류는 전체적으로 유의한 변화가 없었으나 뇌혈관 예비능은 중대뇌동맥 영역 전체에 걸쳐 수술 후 단기간에 유의한 호전을 보였으며 장기간 유지되었다. 따라서 뇌혈관 예비능의 호전여부는 우회로술에 의해 증가된 뇌관류압을 평가할 수 있는 중요한 지표로 생각되며 향후 우회로술에 의한 뇌졸중 재발방지 효과를 알아보기 위해 뇌혈관 예비능의 변화와 예후와의 상관관계에 대한 연구가 필요하리라 생각된다.

Keywords

References

  1. Klijn CJ, Kappelle LJ, Tulleken CA, van Gijn J. Symptomatic carotid artery occlusion. A reappraisal of hemodynamic factors. Stroke 1997;28:2084-93 https://doi.org/10.1161/01.STR.28.10.2084
  2. Klijn CJM, Kappelle LJ. Symptomatic carotid artery occlusion: Extracranial Intracranial Bypass and other treatment options. In: Chaturvedi S, Rothwell PM, eds. Carotid artery stenosis: Current and emerging treatments. Boca Raton: Taylor & Francis; 2005. p. 277-86
  3. Sundt TM, Meyer FB. Sundt's Occlusive Cerebrovascular disease. 2nd ed. Philadelphia: Elsevier Science Health Science div; 1994. p. 489-511
  4. Group TEIBS. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med 1985;313:1191-200 https://doi.org/10.1056/NEJM198511073131904
  5. Ausman JI, Diaz FG. Critique of the extracranial-intracranial bypass study. Surg Neurol 1986;26:218-21 https://doi.org/10.1016/0090-3019(86)90152-7
  6. Day AL, Rhoton AL, Jr., Little JR. The extracranial-intracranial bypass study. Surg Neurol 1986;26:222-6 https://doi.org/10.1016/0090-3019(86)90153-9
  7. Mendelowitsch A, Taussky P, Rem JA, Gratzl O. Clinical outcome of standard extracranial-intracranial bypass surgery in patients with symptomatic atherosclerotic occlusion of the internal carotid artery. Acta Neurochir (Wien) 2004;146:95-101 https://doi.org/10.1007/s00701-003-0154-7
  8. Schmiedek P PA, Leinsinger G, Kirsch CM, Einhupl K. Improvement of cerebrovascular reserve capacity by EC-IC arterial bypass surgery in patients with ICA occlusion and hemodynamic cerebral ischemia. J Neurosurg 1994;81:236-44 https://doi.org/10.3171/jns.1994.81.2.0236
  9. Matthias H, Alexander B, Winfried U, Jiirgen M. Cerebral blood flow and cerebrovascular reserve 5 years after EC-IC bypass. Neurosurg Rev 1991;14:275-8 https://doi.org/10.1007/BF00383261
  10. Batjer HHD, M D Sr; Purdy, P D; Mickey, B; Bonte, F J; Samson, D. Improvement in regional cerebral blood flow and cerebral vasoreactivity after extracranial-intracranial arterial bypass. Neurosurgery 1988;22:913-9 https://doi.org/10.1227/00006123-198805000-00020
  11. Takagi Y, Hashimoto N, Iwama T, Hayashida K. Improvement of oxygen metabolic reserve after extracranial-intracranial bypass surgery in patients with severe haemodynamic insufficiency. Acta Neurochir (Wien) 1997;139(1):52-6; discussion 6-7 https://doi.org/10.1007/BF01850868
  12. Vorstrup S, Brun B, Lassen NA. Evaluation of the cerebral vasodilatory capacity by the acetazolamide test before EC-IC bypass surgery in patients with occlusion of the internal carotid artery. Stroke 1986;17:1291-8 https://doi.org/10.1161/01.STR.17.6.1291
  13. Norihiko K, Kohei H, Toru I, IhnHo C, Naofumi M. Use of I-123 IMP brain SPET to predict outcome following STA-MCA bypass surgery: cerebral blood flow but not vasoreactivity is a predictive parameter. Eur J Nucl Med Mol Imaging 1998;V25:1637-42
  14. Kuroda S, Kamiyama H, Abe H, Houkin K, Isobe M, Mitsumori K. Acetazolamide test in detecting reduced cerebral perfusion reserve and predicting long-term prognosis in patients with internal carotid artery occlusion. Neurosurgery 1993;32:912-8; discussion 8-9 https://doi.org/10.1227/00006123-199306000-00005
  15. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002;15:273-89 https://doi.org/10.1006/nimg.2001.0978
  16. So Y, Lee HY, Kim SK, Lee JS, Wang KC, Cho BK, et al. Prediction of the clinical outcome of pediatric moyamoya disease with postoperative basal/acetazolamide stress brain perfusion SPECT after revascularization surgery. Stroke 2005;36(7):1485-9 https://doi.org/10.1161/01.STR.0000170709.95185.b1
  17. Crowell RM, Ogilvy CS, Choi IS, Gress DR. Direct brain revascularization. In: Schmidek HH, Sweet WH, eds. Operative Neurosurgical Techniques. Vol 1: W.B. Saunders; 1995. p. 909-28
  18. Tulleken CA, Verdaasdonk RM. First clinical experience with Excimer assisted high flow bypass surgery of the brain. Acta Neurochir (Wien) 1995;134(1-2):66-70 https://doi.org/10.1007/BF01428506
  19. Tulleken CAF, Verdaasdonk RM, Mansvelt Beck RJ, Mali WPTM. The modified excimer laser-assisted high-flow bypass operation. Surg Neurol 1996;46:424-9 https://doi.org/10.1016/S0090-3019(96)00096-1
  20. Umemura A, Yamada K, Masago A, Kanda Y, Matsumoto T, Shimazu N. Hemodynamic flow patterns evaluated by transcranial color-coded duplex sonography after STA-MCA bypass for internal carotid artery occlusion. Cerebrovasc Dis 2002;14(3-4):143-7 https://doi.org/10.1159/000065671
  21. Iwama TMH, Nobuo MD; Takagi, Yasushi MD; Tsukahara, Tetsuya MD; Hayashida, Kohei MD. Predictability of Extracranial/Intracranial Bypass Function: A Retrospective Study of Patients with Occlusive Cerebrovascular Disease. Neurosurgery 1997;40:53-60 https://doi.org/10.1097/00006123-199701000-00011
  22. Selman WR, Lust WD, Ratcheson RA. Cerebral blood flow. In: Wilkins RH, Rengachary SS, eds. Neurosurgery. Vol 2: McGraw-Hill; 1996. p. 1997-2010
  23. Kim JS, Moon DH, Kim GE, Cho YP, Kim JS, Ryu JS, et al. Acetazolamide stress brain-perfusion SPECT predicts the need for carotid shunting during carotid endarterectomy. J Nucl Med 2000;41:1836-41
  24. HY Lee DL, JC Paeng, CW Oh, MJ Cho, JK Chung, MC Lee. The efficacy of Quantitative Analysis of Basal/Acetazolamide SPECT Using SPM and Statistical Probabilistic Brain Atlas in Patients with Internal Carotid Artery Stenosis. Korean J Nucl Med 2002;36:357-67
  25. JS Eo CO, YK Kim, EK Park, WW Lee, SE Kim. Hemodynamic Outcome of Successful Bypass Surgery in Patients with Atherosclerotic Cerebrovascular Disease: A study with Acetazolamide and 99mTc-ECD SPECT. Korean J Nucl Med 2006;40:293-301