Acta Neurochir (2015) 157:1849–1854 DOI 10.1007/s00701-015-2579-1 CASE REPORT - VASCULAR Specific and helpful intraoperative indocyanine green videoangiography finding of blood blister-like aneurysm of internal carotid artery Moon-Soo Han 1 & Sung-Pil Joo 1 & Seung-Hoon Jung 1 & Tae-Sun Kim 1 Received: 23 March 2015 / Accepted: 3 September 2015 / Published online: 16 September 2015 # Springer-Verlag Wien 2015 Abstract Background Blood blister-like aneurysms (BBAs) account for 0.5–2.0 % of ruptured intracranial aneurysms. Because of their rarity, the natural history and pathophysiology of such aneurysms are not fully understood. We present two patients with BBAs treated with Bemsheets-covered clipping and discuss their pathophysiological characteristics, through the intraoperative and specific indocyanine green (ICG) video angiography (VA) findings. Case report A 34-year-old male and a 53-year-old female were admitted to our emergency room with suddenly reduced levels of consciousness. Brain imaging studies demonstrated a blood blister-like aneurysm of the supraclinoid segment of the right ICA. Craniotomy and an attempt of surgical clipping were performed. ICG-VA showed the filling defect of dye in aneurysm in the operative field. The BBAs were clipped after being covered by Bemsheets (Kawamoto Corporation, Osaka, Japan) and then confirmed by the ICG-VA. Postoperatively, both patients showed transient neurological deficit due to vasospasms and recovered to their normal statuses within a few months after their respective operations. Conclusions ICG-VA showed the filling defect of dye in BBAs, w hich sup ported that BBAs have been a pseudoaneurysm. In addition, although not routinely recommended in the treatment of BBAs, we believe that Bemsheetcovered clipping is a safe and effective treatment option for BBAs. * Tae-Sun Kim taesun1963@yahoo.co.kr 1 Department of Neurosurgery, Chonnam National University Research Institute of Medical Sciences, Chonnam National University Hospital & Medical School, 42, Jebong-ro, Donggu Gwangju 501-757, Republic of Korea Keywords Blood blister-like aneurysm . Pseudoaneurysm . Indocyanine green . Internal carotid artery . Surgery Background Blood blister-like aneurysms (BBAs) account for 0.5–2.0 % of ruptured intracranial aneurysms and unusually lead to high morbidity and mortality rates as compared with typical ruptured saccular aneurysms of the internal carotid artery (ICA) [10, 14, 17, 23]. Because of their rarity, the natural history and pathophysiology of BBAs are not fully understood. The main hypothesis is that BBAs arise from dissection of vessel walls [4, 6], but the pathophysiological studies should be performed through biopsy or autopsy. Most often, these lesions appear on the dorsal wall of the supraclinoid portion of the ICA, which presents as a fragile wall with a poorly defined, broad-based, ambiguous neck. Given these characteristics, BBAs have been considered as pseudoaneurysms [6, 24], so the treatment of BBAs is always challenging. Although the use of endovascular treatment is increasing, endovascular coil embolization alone may be insufficient to prevent the recurrence or re-bleeding of BBAs [14, 17]. Also, surgical clipping has remained challenging, resulting in significant rates of morbidity and mortality. Recently, microscope-integrated near-infrared indocyanine green (ICG) videoangiography (VA) has been introduced in neurosurgery. It has been proven that intraoperative ICG-VA may help surgeons to evaluate cerebral vessels visible in the surgical field. In addition, ICG-CA helps surgeons to obtain a real-time diagnosis of the degree of aneurysm occlusion and vessel patency, including perforating arteries based on the timing of fluorescence with the dye [2, 3, 5, 13, 18, 19, 25]. In this paper, we describe two patients with subarachnoid hemorrhage (SAH) caused by ruptured BBAs that were treated with Bemsheets-covered clipping. In addition, this is the 1850 first report of specific finding of ICG-VA of BBAs, which can help reveal the pathophysiology and establish the neurosurgical strategy in treating BBAs. Case reports Case 1 In December of 2013, a 34-year-old male who lost consciousness, which was recovered shortly, was admitted to our emergency room. Except for severe a headache, there was no specific history of head trauma or medical illness. In neurological examination, he showed a confused mentality with a Glasgow Coma Scale (GCS) of 13/15 and a Hunt and Hess grade of II. There were no abnormal laboratory findings. A non-contrasted brain computed tomography (CT) scan showed a subarachnoid hemorrhage (SAH) (Fig. 1a). Conventional four-vessel angiography confirmed a 4-mm-sized blister-like aneurysm of the supra-clinoid segment of the right ICA (Fig. 1b, c, d). There were no other aneurysms or vascular malformations that could be related to the SAH. Endovascular treatment seemed to be unsuitable due to the broad-based aneurysmal neck and small morphology. A right fronto-temporal craniotomy and an attempt of surgical clipping were performed. Fig. 1 a Initial brain CT showed SAH. b, c, d Conventional fourvessel angiography and 3D angiogram demonstrate a blood blister-like aneurysm dilation at the dorsal wall of the supraclinoid segment of right ICA. The size is 4 mm Acta Neurochir (2015) 157:1849–1854 During the operation, an extremely thin and defective walled aneurysm was seen and part of the bulging wall seemed to have a hemorrhage within it (Fig. 2a). Before clipping, the ICG-VA was performed and revealed the filling defect of dye in aneurysm (Fig. 2b). After the temporary clip was applied on the proximal ICA, the aneurysm and arterial wall were then covered thinly with Bemsheets to prevent the clip from slipping, and then a Sugita-6 clip was applied parallel to the arterial wall (Fig. 2c) so that the clip blades could cover the arterial wall beyond the lesion. ICG-VA was performed again to confirm the patency of parent artery and perforators (Fig. 2d). After the surgery, the patient exhibited paraparesis. A follow-up brain CT angiogram showed vasospasms in both ACAs. The patient’s symptoms gradually improved through 3-H therapy. A follow-up angiography 2 weeks later revealed a good patency of the ICA and the obliteration of the aneurysm (Fig. 2e, f). The patient had no residual motor deficit and had returned to normal activities in 3 months after the surgery. Case 2 In February of 2014, a 53-year-old female presented with SAH. She showed a drowsy mentality, with a Hunt and Acta Neurochir (2015) 157:1849–1854 1851 Fig. 2 Intra-operative findings. a In situ blister-like aneurysm. b Specific ICG-VA finding of BBA that has filling defect of dye in aneurysm (arrow). c Bemsheets covers the aneurysm before clipping. d ICG-VA was performed after clipping, confirming intact blood flow of the ICA and perforating arteries. e, f A follow-up angiography revealed good patency and no significant vasospasm Hess grade of II. Brain CT angiogram scan showed Fisher grade IV SAH and a 3-mm-sized blister-like aneurysm of the supraclinoid segment of the left ICA (Fig. 3). The patient has a humpback, so that the conventional fourvessel angiography could not be performed. A left fronto-temporal craniotomy was performed to attempt surgical clipping. During the operation, an extremely thin walled aneurysm having a hemorrhage within it was seen and an aneurysmal dome was defected (Fig. 4a). Through the ICG-VA, we were able to see the filling defect of dye in the aneurysm (Fig. 4b). The aneurysm and arterial wall were covered thinly with Bemsheets and then a Sugita clip was applied parallel to the arterial wall using the same method as in case 1 (Fig. 4c). ICG-VA was performed again, showing the intact blood flow of the ICA and perforating arteries (Fig. 4d). Five days after the SAH, the patient suffered aphasia and a confused mental state. A follow-up brain CT angiogram revealed vasospasms at both ACAs, MCAs, and PCAs. The patient’s symptoms have gradually improved through the 3-H treatment. A follow-up brain CT angiogram several days later revealed the obliteration of the aneurysm, no migration of the aneurismal clip, and improvement of vasospasm (Fig. 4e, f). At the 3-month follow-up check-up, the patient was doing well and her neurological examination was normal. 1852 Acta Neurochir (2015) 157:1849–1854 Fig. 3 a Initial CT showed diffuse, Fisher grade IV SAH. b, c Brain CT angiogram showed an irregularity of the anterior wall of the left ICA Fig. 4 Intra-operative findings. a In situ blister-like aneurysm (note the lack of aneurysm dome). b Specific ICG-VA finding of BBA that has filling defect of dye in aneurysm (arrow). c Bemsheets wraps the aneurysm before clipping. d ICG-VA was performed after clipping, confirming intact blood flow of the ICA and perforating arteries. e, f A follow-up brain CT angiogram revealed no migration of the aneurismal clip and improvement of vasospasm Acta Neurochir (2015) 157:1849–1854 Discussion BBAs are rare, accounting for 0.5–2.0 % of ruptured intracranial aneurysms, but are clinically important because they can cause a SAH [10, 14, 17, 23]. The pathophysiology of BBAs is not fully understood. Some studies suggest that BBAs are not true aneurysms. BBAs consist of a fragile fibrin layer in a focal wall defect with the absence of an internal elastic lamina and media [6, 12]. Merely blood clots of fenestrations found in the internal elastic lamina of affected carotid arteries [22], and organization and growth of the blood clots on the focal wall defect [1]. These segments are believed to undergo major dynamic changes depending on blood pressure and sheer stress. Consequentially, these are caused secondary to a subadventitial dissection of the ICA, which may represent a possible mechanism of BBAs’ formation. These pathophysiological characteristics are considered as a pseudoaneurysm [6, 24] and therefore treatment strategies used for other typical types of aneurysms cannot be applied for BBAs. In our patients, intraoperative ICG-VA showed the filling defect of dye in aneurysms. This demonstrates that organized blood clots were on the focal wall defect. These intraoperative ICG-VA findings support previous pathophysiological studies and could support that BBA is a pseudoaneurysm radiologically instead of taking a biopsy of the lesion or performing an autopsy to confirm the pathophysiological feature. Treatment of BBAs remains challenging due to their small size, broad-based morphology, and fragile thin wall, making them prone to rupture during microsurgery [26]. Various treatment strategies have been developed to deal with BBAs. The treatment modality should be tailored to not only the pseudoaneurysm but also the affected ICA vascular wall in order to prevent re-bleeding and regrowth. Proposed pathogenesis and ICG-VA finding of BBAs support that BBAs are a pseudoaneurysm, so endovascular coil embolization alone has been associated with a high intraprocedural rupture rate [17] and should not be considered as a first option. Fig. 5 ICG-VA could distinguish the pseudoaneurysmal wall from the normal internal carotid artery wall (line transitional zone) 1853 Surgical treatment has the advantage of enabling direct observation of the vascular lesion. Although intraoperative rupture has been demonstrated to occur during dissection, during clip closure, and after slipping-off the clip [15, 21], these problems have been managed using various methods, including trapping or occlusion, clipping on wrapping material [8, 16], suturing the tear [7, 26], and clipping with an encircling clip [9, 20]. Some authors have emphasized that clip blades are applied parallel to the ICA, taking part of the normal carotid wall beyond the lesion [1, 12, 15, 21]. However, clipping, either directly or on a wrapping material, may compromise the patency of the parent artery and injure branching vessels and perforators resulting in ischemia [11]. Ogawa et al. [15] reported ischemic complications in a patient with ICA stenosis after BBAs clipping. As illustrated by our patients, we were able to preserve the parent artery and perforator arteries through the ICG-VA. Especially, before BBA clipping, we could distinguish the pseudoaneurysmal wall from the normal internal carotid artery wall by using ICG-VA. So, confirming the transitional zone (Fig. 5), we could perform the Bemsheetscovered clipping in the appropriate location, preventing a slipping-off of the clip and ICA stenosis. After clipping, through the ICG-VA, we could confirm the intact blood flow of the ICA and perforating arteries Conclusions Intraoperative ICG-VA revealed the filling defect of dye in aneurysm, supporting that BBAs are pseudoaneurysms. It also helps to reduce perioperative aneurysm rupture and ischemic complications, consequently improving patient outcome in BBA cases. 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