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Imaging of the Inflammatory Response in Reperfusion Injury After Transient Imaging of the Inflammatory Response in Reperfusion Injury After Transient Cerebral Ischemia in Rats: Correlation of SPIO-enhanced MR Images with Histopathology Jinna Kim Department of Medicine The Graduate School, Yonsei University Imaging of the Inflammatory Response in Reperfusion Injury After Transient Cerebral Ischemia in Rats: Correlation of SPIO-enhanced MR Images with Histopathology Directed by Professor Dong Ik Kim The Doctoral Dissertation submitted to the Department of Medicine, the Graduate School of Yonsei University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Jinna Kim December 2006 This certifies that the Doctoral Dissertation of Jinna Kim is approved. ---------------------------------- Thesis Supervisor : Dong Ik Kim ---------------------------------- Tae Seung Kim ---------------------------------- Dong Goo Kim ---------------------------------- Jong Doo Lee ---------------------------------- Ji Hoe Heo The Graduate School Yonsei University December 2006 감사의 글 신경방사선학에 입문하며 시작한 이 연구는 진리탐구에 대한 또 하나의 도전이였기에 작은 결실이지만 감사하게 겸손히 받아들이려 합니다. 오래 전부터 존경하는 은사님이 되어 주셨고 본 연구 중에도 변함없이 가르침과 지원을 아끼지 않으신 김동익 지도 교수님께 감사드립니다. 뇌신경계를 공부하게 되면서 가까운 곳에서 항상 크고 작은 도움을 주시고 조언을 아끼지 않으시는 이종두 교수님과 허지회 교수님께 감사드립니다. 또한 깊은 통찰력으로 자상한 가르침을 주신 김태승 교수님과 김동구 교수님께 감사드립니다. 실험연구의 선배로서 기초를 마련하여 주시고 이끌어주신 이승구 교수님과 김동준 교수님, 그리고 판독실의 김응엽 교수님께 감사드립니다. 긴 시간동인 연구의 방향을 제시하여 주시고 항상 지켜봐 주신 이종은 교수님과 해부학교실의 안수경 선생님, 김사현 선생님, 늦은 밤에도 좋은 MR 영상을 얻도록 도와주신 김윤국 선생님, 김세영 선생님께도 깊은 감사를 드립니다. 제게 생명 주신 하나님, 항상 큰 딸을 믿고 지켜봐 주시는 부모님, 힘든 병원 생활 속에서도 따뜻한 쉼터가 되어주는 친구 자경, 자영이에게도 감사합니다. 밤 늦게 들어오는 아내를 항상 응원해 주고 가장 좋은 친구가 되어주는 사랑하는 남편과 아들 현민에게도 마음 속 깊이 사랑과 고마움을 전합니다. 저 자 씀 Table of contents Abstract ······················································································································ 1 I. INTRODUCTION ································································································· 3 II. MATERIALS AND METHODS ········································································ 6 1. Animal preparation ································································································ 6 2. Administration of contrast material and MR imaging acquisition ······················ 7 3. Image analysis ····································································································· 8 4. Histopathology ···································································································· 9 III. RESULTS ············································································································ 11 1. MR imaging findings after reperfusion ······························································· 11 2. Histopathologic findings ···················································································· 16 3. Correlation with BBB disruption ········································································ 20 IV. DISCUSSION ······································································································ 22 V. CONCLUSION ····································································································· 28 REFERENCES ·········································································································· 30 Abstract (in Korean) ································································································· 37 i List of figures Fig. 1. In vivo assessment of macrophage infiltration by SPIO-enhanced MR imamaging at various stages of reperfusion ·················································· 12 Fig. 2. Overall lesion volume and the volume of hypointense area on T2*-weighted MR images at various stages of reperfusion ················································· 14 Fig. 3. Mean signal intensities of the hyperintense and hypointense areas on T2*- weighted MR images at various stages of reperfusion ·································· 15 Fig. 4. Histologic section with Prussian blue stain 3 days after reperfusion ············ 17 Fig. 5. Histologic section stained for ED-1 3 days after reperfusion ······················· 18 Fig. 6. Comparison of stained sections with Prussian blue solution and ED-1 3 days after reperfusion ···························································································· 19 Fig. 7. Relationship between SPIO-induced signal loss and breakdown of the BBB 3 days after reperfusion ···················································································· 21 ii Abstract Imaging of the Inflammatory Response in Reperfusion Injury After Transient Cerebral Ischemia in Rats: Correlation of SPIO-enhanced MR Images with Histopathology Jinna Kim Department of Medicine The Graduate School, Yonsei University (Directed by Professor Dong Ik Kim) Reperfusion by recanalization of the occluded artery after acute ischemic stroke may result in microscopic cellular damage, and acute inflammatory responses have been thought to play a central role in ischemia-reperfusion injury. The purpose of this study was to determine if the accumulation of macrophages could be seen in vivo in a reperfusion animal model after focal cerebral ischemia using superparamagnetic iron oxide (SPIO)-enhanced magnetic resonance (MR) imaging, and to correlate the spatial distribution of SPIO-induced MR signal alterations with histopathologic 1 findings. One-hour transient occlusion of the middle cerebral artery was produced in adult male Sprague-Dawley rats. We injected SPIO particles at different time points after reperfusion and performed three-dimensional (3-D) T2*-weighted MR images with gradient-echo sequence 24 hours later. After the acquisition of MR imaging, a specimen was obtained. Macrophages were detected with Prussian blue and immunohistochemical staining. Histochemical iron detection was compared with T2* signal abnormalities. At days 3 and 4 post-reperfusion, focal areas of signal loss indicating local accumulation of SPIO particles appeared at the center of the damaged brain. Areas of signal loss corresponded to local accumulation of iron-laden macrophages in histologic sections, and SPIO-induced signal loss indicated active macrophage transmigration into the reperfused brain. SPIO-enhanced MR imaging demonstrated through in vivo monitoring that macrophages participate in reperfusion injury at early stages of injury development. SPIO-enhanced MR imaging can be a useful tool to examine the inflammatory mechanisms involved in reperfusion brain injury. Key words: acute ischemic stroke, reperfusion, inflammation, macrophage, magnetic resonance imaging 2 Imaging of the Inflammatory Response in Reperfusion Injury After Transient Cerebral Ischemia in Rats: Correlation of SPIO-enhanced MR Images with Histopathology Jinna Kim Department of Medicine The Graduate School, Yonsei University (Directed by Professor Dong Ik Kim) I. INTRODUCTION Recently, reperfusion by recanalization of occluded arteries has proven the most effective therapy for acute ischemic stroke in humans. Aggressive therapeutic trials have studied the effectiveness of intravenous, intra-arterial, mechanical, or combined thrombolysis for the treatment of hyperacute cerebral infarcts.1-3 In light of these 3 advances, elucidation of the pathophysiological events that complicate early cerebral reperfusion is essential. Although reperfusion can save ischemic tissue by rapid restoration of cerebral blood flow, microscopic cellular injury after reperfusion may occur by various mechanisms. The adverse effects of reperfusion diminish the net positive effect on clinical outcome and independently increase the risk of decline in stroke patients.4-6 Reperfusion injury has been defined in numerous ways that implicate secondary hemodynamic disturbances, enhancement of inflammatory responses, excess production of oxygen free radicals, glutamatergic excitotoxicity, apoptosis, and breakdown of the blood-brain barrier (BBB) as factors that contribute to reperfusion injury.4,7-13 In all of them, it has been well documented that profound inflammatory responses are evoked and that immune mediators produced by the inflammatory cells contribute to reperfusion cellular injury.7-9 Recent studies have demonstrated that superparamagnetic iron oxide (SPIO) particles taken up by macrophages in the mononuclear phagocyte system enable in vivo monitoring of macrophage infiltration by magnetic resonance (MR) imaging in the experimental ischemic rat brain.14-19 The purpose of the present study was to visualize early activation and accumulation of macrophages in an experimental reperfusion animal model by means of SPIO- enhanced MR imaging, to evaluate the clinical usefulness of SPIO-enhanced MR 4 imaging for the assessment of inflammatory responses in reperfusion brain injury, and to correlate the spatial distribution of SPIO-induced MR signal alterations with histopathologic findings. 5 II. MATERIALS & METHODS 1. Animal preparation Animal experiments were approved by the Committee for the Care & Use of Laboratory Animals at the Yonsei University College of Medicine. Adult male Sprague-Dawley rats weighing 300 to 350 g were subjected to transient middle cerebral artery occlusion (MCAO). Animals were anesthetized with 100 mg/kg body weight ketamine chloride (Ketalar; Yuhan yanghang, Seoul, Korea) and 10 mg/kg body weight xylazine hydrochloride (Rompun; Bayer Korea, Seoul, Korea) administered intraperitoneally. During anesthesia, rectal temperature was maintained at 36.5 o C to 37.5 o C by a heating pad. Ischemia
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