Mo d i f i c at i o n s to platinum coils have been proposed. Evaluation of the new HydroSoft coil in a canine model of bifurcation aneurysm
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1 See the corresponding editorial in this issue, pp J Neurosurg 111:11 16, 2009 Evaluation of the new HydroSoft coil in a canine model of bifurcation aneurysm Laboratory investigation To m o y u k i Ts u m o t o, M.D., Ya s u n a r i Ni i m i, M.D., a n d Al e j a n d r o Be r e n s t e i n, M.D. Center for Endovascular Surgery, Beth Israel Hyman Newman Institute for Neurology and Neurosurgery, Roosevelt Hospital, New York Object. The present study was designed to evaluate the new HydroSoft coil as a finishing coil in a canine model of a wide-necked, high-flow bifurcation aneurysm. Methods. Nine experimental aneurysms were created. The aneurysm dome was first embolized with bare platinum coils and HydroCoils, and then the remaining neck portion was embolized with HydroSoft coils to obtain maximum aneurysm occlusion. Follow-up angiography was performed at 1 and 3 months, and histopathological analysis was performed after the 3-month follow-up angiography. Results. One hundred twenty-five HydroSoft coils were deployed into 9 aneurysms without any technical problem. The mean volume % of the bare platinum coils, HydroCoils, and HydroSoft coils were 23.0 ± 15.9, 63.0 ± 23.5, and 13.9 ± 8.9%, respectively. The mean aneurysm volumetric occlusion rate was 45.9%. At the 3-month follow-up angiography, 8 of 9 aneurysms remained stable and had not recanalized. Microscopically, most aneurysms showed complete endothelialization and thick neointima formation at the neck surface with no thrombus present. Conclusions. The HydroSoft coil appears feasible as a finishing coil based on the results of this animal study. HydroSoft coils inserted at the neck of the aneurysm may help induce neointima formation, which may lead to less coil compaction and aneurysm recanalization in clinical practice. (DOI: / JNS08855) Ke y Wo r d s endovascular treatment embolization intracranial aneurysm HydroCoil HydroSoft coil canine Abbreviations used in this paper: CCA = common carotid artery; GDC = Guglielmi Detachable Coil. J Neurosurg / Volume 111 / July 2009 Mo d i f i c at i o n s to platinum coils have been proposed to reduce the tendency of coils to compact in wide-necked and large aneurysms. These modifications include the addition of biomaterials such as collagen coatings or filaments, basement membrane proteins, growth factors, cellular elements, or bioabsorbable polymers. 3,8 10,13,14 One such modified platinum coil, the HydroCoil (Microvention Terumo, Inc.), has been introduced clinically. 1,4,7 The HydroCoil is a hybrid hydrogelplatinum detachable coil device. The device consists of a synthetic polymeric hydrogel attached to a platinum coil. This hydrogel swells to its maximum predetermined diameter in ~ 20 minutes in blood, thereby increasing the volumetric filling. 6 In our previous experimental study in canine bifurcation aneurysms, compared with bare platinum coils (GDC), HydroCoil use resulted in significantly denser coil packing, less midterm follow-up coil compaction, and thicker neointimal tissue at the neck of the lesion. 16 The use of HydroCoils was associated with less aneurysm recurrence in 1 clinical study, particularly in small and large aneurysms. 7 However, there were some technical considerations in using this coil in the clinical setting. Although investigators in the HydroCoil for Endovascular Aneurysm Occlusion study 2 discovered a reduced recurrence rate when the final coil was a HydroCoil, this coil was originally designed to pack the dome of the aneurysm. Because of its relative stiffness secondary to the gel coating and the time restriction to deploy the HydroCoil into the aneurysm, deployment of the HydroCoil at the neck and parent vessel interface can be problematic. To overcome the drawbacks of the HydroCoil as a finishing coil, the new HydroSoft coil (Microvention Terumo, Inc.) was developed. This new coil is softer, contains less hydrogel, swells more slowly than the existing HydroCoil, and expands to fill up to 70% more volume than a 10 system bare platinum coil, which enables repositioning and retrieval without time restriction. This HydroSoft coil can be deployed at the aneurysm neck as a finishing coil. The present study was designed to evaluate the HydroSoft coil as a finishing coil in a wide-necked highflow bifurcation aneurysm model in canines. 11
2 T. Tsumoto, Y. Niimi, and A. Berenstein Methods This prospective study was conducted in 9 male dogs. One experienced neurosurgeon (TT) constructed all experimental bifurcation aneurysms after sufficient training. All animal experiments were conducted in accordance with the policies of the Institutional Animal Care and Use Committee at St. Luke s Roosevelt Hospital Center Animal Care Facility. All surgical and endovascular procedures were performed with the animals in a state of general anesthesia. The dogs were 3 4 years old, weighed kg each, and were maintained on a standard laboratory diet. Anesthesia was induced with thiopental (15 20 mg/kg), followed by endotracheal intubation, and maintained with isoflurane 1 3% via the endotracheal tube. The neck was prepared and draped in the usual sterile fashion. Heart rate, blood pressure, O 2 saturation, electrocardiogram, and depth of anesthesia were monitored intraoperatively. Aneurysm Construction The details of bifurcation aneurysm construction have been described previously. 5,15 In brief, after a 10-cm midline incision is made in the neck, a 6-cm venous segment is excised from the right external jugular vein. The distal segment of the divided left CCA is swung to the right through a tunnel made behind the trachea. A partial end-to-side anastomosis of the left CCA to the proximal arteriotomy of the right CCA is created using interrupted monofilament 6-0 Prolene sutures. The venous segment is then sutured to the notch formed by the anastomosis of both CCAs. The open end of the grafted vein segment is then ligated with 6-0 Prolene sutures to create a bifurcation aneurysm. After the bifurcation aneurysm was completed, a sidewall aneurysm was created on the right CCA distal to a bifurcation aneurysm for control. Embolization of Aneurysm To minimize the effects of a tissue reaction from surgery and all the aneurysms to maturate, endovascular treatment was performed at least 4 weeks after aneurysm construction. For the purpose of testing the behavior of the coils during embolization, we treated the aneurysms by simulating clinical practice. A 50-U/kg heparin bolus was administered intravenously after a 5-Fr guiding catheter (Envoy; Cordis) was advanced 3-cm proximal to the aneurysm neck. Selective CCA angiograms were obtained to confirm the patency of the aneurysm in multiple projections. A microcatheter (Excelsior1018; Boston Scientific-Target Therapeutic) was advanced through the guiding catheter and the tip of the microcatheter was placed at the center of the aneurysm. The dome of the aneurysm was filled with HydroCoils (HydroCoil size 10, 14, or 18) after the first bare platinum coils formed a retaining basket. After packing with HydroCoils in the dome of the aneurysm, the remaining neck portion was embolized with HydroSoft 10 coils to obtain maximum aneurysm occlusion. During the procedure, HydroCoils were switched to HydroSoft coils arbitrarily by the 2 operators (AB and TT). Groups were not embolized with only bare platinum coils or HydroCoils, because we had already tested these groups in the same model before. 16 Angiographic Analysis Aneurysm packing density volumetric occlusion was determined angiographically immediately after embolization. The theoretical volumetric occlusion was estimated based on the volume of the aneurysm and the volume of the implanted devices. To obtain these calculations, the aneurysm dome and length and a radiopaque calibration marker (dime = 18 mm) were measured using calipers. Before embolization the aneurysm volumes were determined from the dome and length measurements of the lesions. The shape of the lesions was assumed to be elliptical, and the volumes were determined using the following equation: aneurysm volume = (4/3) π (length/2) (dome/2) 2 A theoretical volumetric occlusion was determined by dividing the sum of the volumes of all devices that were implanted by the aneurysm volume. The volume of the coils was estimated using the following formula: volume of coils = π (OD/2) 2 L where OD is the outside diameter of the coils (Microplex size 18, mm; MicroPlex size 10, mm; Hydro- Coil size 14, mm when hydrated; and HydroCoil size 18, mm when hydrated; HydroCoil size 10, mm when hydrated; HydroSoft size 10, mm when hydrated) and L represents the total length of the coils implanted into the aneurysm. Follow-up angiograms were obtained to assess potential aneurysm recanalization at 1 and 3 months after aneurysm construction. All follow-up angiograms were compared with angiograms obtained immediately after embolization to assess interval changes in coil configuration and aneurysm filling. Macroscopic Photography and Histological Analysis The animals were killed after the 3-month follow-up angiograms were obtained. The walls of the carotid arteries were longitudinally opened to expose the lumen of the aneurysm necks, which were digitally photographed from the lumen side in close-up mode. The aneurysms were fixed in 10% formaldehyde and sent to an outside facility (CV Path Institute, Inc.) where they were cut into sections. The specimens were studied after H & E staining. The thickness of the aneurysm neck tissue was determined by drawing a vertical line from the surface of the neointima to the surface of the closest coil with the aid of digital morphometry software (SPOTSoftware). Results All aneurysms were patent, and no intraaneurysmal thrombi were observed at the time of treatment. The mean dimensions of the aneurysms were as follows: length, ± 3.10 mm; diameter, ± 2.00 mm; and volume, 1.12 ± 0.46 ml. The mean aneurysm neck size was 7.03 ± 1.51 mm. 12 J Neurosurg / Volume 111 / July 2009
3 Evaluation of the HydroSoft coil in a canine bifurcation aneurysm Embolization Findings A total of 125 HydroSoft coils were deployed into 9 bifurcation aneurysms. Figure 1 displays the proportion of coils used in each case. Bare platinum coils were used to form a basket within the aneurysm, HydroCoils were used to pack the dome of the aneurysm, and HydroSoft coils were used to pack the neck as a finishing coil. The mean volume % of those coils was 23.0 ± 15.9, 63.0 ± 23.5, and 13.9 ± 8.9%, respectively. Aneurysm volumetric occlusion rates ranged from 19.9 to 85.7% by volume with a mean of 45.9%. Angiographic Findings Eight of 9 aneurysms had 100% occlusion immediately after the embolization, with no occlusion of the parent vessel or outflow vessel, and 1 aneurysm (Case 1) was intentionally occluded to only 90%. In 3 of 9 procedures, obvious clot formation was recognized immediately after the procedure. At the 1-month angiographic follow-up, 8 of 9 aneurysms remained 100% occluded and 1 aneurysm (Case 1) was unchanged and stable at 90% occlusion. At the 3-month follow-up, 8 of 9 aneurysms remained stable and had not recanalized (Table 1; Fig. 2A D). In 1 of the 8 aneurysms (Case 6), which had been 100% occluded at 1 month, there was a small amount of coil compaction (Fig. 3A D). The aneurysm that was intentionally occluded to 90% was unchanged at 3 months. Adverse events such as coil protrusion, parent artery occlusion, and obvious clot formation were not seen on follow-up angiography at either time point. Macroscopic and Histological Findings After the 3-month follow-up, 6 of 9 animals were killed for histological evaluation. The 3 remaining animals were kept alive for long-term follow-up. Macroscopically, the aneurysm necks were covered with thick white connective tissue (Fig. 2E). Microscopically, most aneurysms showed complete endothelialization and neointima formation (mean thickness ± mm) at the neck surface and no thrombus present. The aneurysm domes also showed marked organization consisting of smooth muscle cells within a proteoglycan matrix, mild neoangiogenesis, and minimal inflammation consisting of lymphocytes, macrophages, and giant cells. No fibrin or platelet thrombus was seen within the aneurysms (Fig. 2F and G). In Case 6, a small cleft between the coils and the aneurysmal wall was recognized macroscopically and microscopically (Fig. 3E). Discussion Clinically, the HydroCoil is used as a filling coil and is not considered a finishing coil because of its relative stiffness, the time restriction associated with its deployment, and its expansion that may protrude toward the lumen. The present study in relatively large and widenecked canine bifurcation aneurysms demonstrated that the new HydroSoft coil is a feasible finishing coil. After packing the aneurysm dome with HydroCoils, we embolized the remaining neck portion with HydroSoft coils J Neurosurg / Volume 111 / July 2009 Fig. 1. Graph demonstrating the proportion of coils used in each case. The mean volume % of bare platinum coils, HydroCoils, and HydroSoft coils was 23.0 ± 15.9, 63.0 ± 23.5, and 13.9 ± 8.9%, respectively. to obtain aneurysm occlusion. Without time restriction, multiple repositioning of the HydroSoft coil at the neck of the aneurysm was possible, similar to bare platinum finishing coils. We were able to pack the aneurysm necks uniformly with HydroSoft coils even though the average neck diameter was relatively wide (> 7 mm). In angiographic follow-up, adverse events such as coil protrusion, parent artery occlusion, and obvious clot formation were not noted at 1 and 3 months. Moreover, in 8 of 9 cases, the uniform coil surface formed by the HydroSoft coils remained unchanged during follow-up. Our angiographic findings were supported by histological findings. Macroscopically, the aneurysm necks were covered with relatively homogeneous thick white connective tissue, and microscopically, most showed complete endothelialization and neointima formation. These histopathological findings suggest that HydroSoft coils may foster neointima formation across the neck of the aneurysm when used as a finishing coil. There are 2 previous reports of bioactive coils evaluated in the same animal model as in the present study. In one report, the HydroCoil was evaluated, and in the other, the Matrix coil was evaluated. 12,16 Yoshino et al. 16 compared the use of HydroCoil to that of bare platinum coils. The HydroCoil group aneurysms were more densely packed than the GDC group, with a statistically significant difference (75.4 versus 39.6% occlusion). The neointima of the aneurysm neck was also significantly thicker in the HydroCoil group than in the GDC group TABLE 1: Summary of angiographic results with 3 coil types in a canine model of bifurcation aneurysm Finding GDC (%)* HydroCoil (%)* HydroSoft (%) coil packing density (mean ± SD) 39.6 ± ± ± 25.0 no. w/ recanalization at 3 mos 2 (67) 0 1 (11) no. w/ thrombus formation 0 2 (33) 3 (33) * Data from our previous study, Yoshino et al.,
4 T. Tsumoto, Y. Niimi, and A. Berenstein Fig. 2. Case 3. Representative digital subtraction angiograms obtained before (A), immediately after (B), and 1 (C) and 3 (D) months after embolization. A small amount of thrombus is recognized immediately after embolization. The aneurysm was not recanalized and was stable as 100% occlusion during the 3-month follow-up period. Macroscopic view of specimen of harvested aneurysm at 3 months (E). Thick neointimal tissue and dense edge contact is observed in this case. Low-magnification H & E stained photomicrographs showing the neck and dome of this aneurysm (F and G). Complete endothelialization and neointima formation at the neck surface is seen and no thrombus is present. The dome shows marked organization consisting of smooth muscle cells and no fibrin or platelet thrombus. (0.329 ± versus ± mm). Concerning coil compaction, no compaction was noted in the Hydro- Coil group, while 2 of 3 aneurysms recurred in the GDC group. In the evaluation of the Matrix coil by Song and colleagues 12, the neointima of the aneurysm neck was ± 0.14 mm, and 4 of 6 aneurysms recanalized. In the present study, in comparison, mean volumetric occlusion rate was 45.9% and the mean neointima of the aneurysm neck measured ± mm, more than the Matrix coil but less than the HydroCoil group. Similar to the HydroCoil aneurysm study, 8 of 9 canine aneurysms treated with HydroSoft finishing coils did not recanalize at the 3-month follow-up; 1 aneurysm demonstrated a small amount of coil compaction. Study Limitations There are several limitations to the present study. First, the switch from HydroCoils to HydroSoft coils depended on the arbitrary intraoperative decision of the 2 operators. The mean volume % of HydroCoils and HydroSoft coils used in this study was 63.0 ± 23.5 and 13.9 ± 8.9% each. However, in Case 6, only 13.0% HydroCoils was inserted into the aneurysm; this small volume of HydroCoils used may have caused coil compaction to occur in this particular case. With this in mind, we speculate that the HydroSoft coil may be more effective after first densely packing the aneurysm dome with HydroCoils, especially in larger aneurysms. Second, it was difficult to determine whether HydroSoft coils caused fewer thromboembolic complications than HydroCoils. Theoretically, the HydroSoft coil is designed to be less thrombogenic as it has less hydrogel volume and does not expand as much. In our previous HydroCoil study, obvious thrombus formation was recognized in 2 of 6 cases with the HydroCoil. Also in this HydroSoft coil study, thrombus formation was recognized in 3 of 9 cases. The apparently increased thrombogenicity of the HydroCoil and Hydro- Soft coil may depend on differences in the platelet and coagulation systems between humans and dogs. It was reported that canines have a higher tendency to develop thrombi than other species, including humans. 11 Kang et al. 7 reported that thromboembolic complications with HydroCoils was recognized in only 2 of 76 patients in their clinical study. 14 J Neurosurg / Volume 111 / July 2009
5 Evaluation of the HydroSoft coil in a canine bifurcation aneurysm Fig. 3. Case 6. Representative digital subtraction angiograms obtained before (A), immediately after (B), and 1 (C) and 3 (D) months after embolization. The aneurysm shows a small amount of recanalization at the 3-month follow-up. Macroscopic view of a specimen of harvested aneurysm at 3 months (E). Small cleft between the coils and the aneurysm is recognizable at the 6 and 12 o clock positions. Conclusions The HydroSoft coil appears feasible as a finishing coil based on our results in this animal study. Hydro- Soft coils at the neck of the aneurysm may help induce neointima formation, which may lead to less coil compaction and aneurysm recanalization in clinical practice. The occurrence of thromboembolic complication may be a limitation of this model. The 3-month follow-up period was relatively short; longer-term angiographic and histological follow-up results are being pursued. Disclosure This study was supported in part by Microvention Terumo, Inc. Dr. Berenstein has consulting interests in this company. References J Neurosurg / Volume 111 / July Berenstein A, Song JK, Niimi Y, Namba K, Heran NS, Brisman JL, et al: Treatment of cerebral aneurysms with Hydrogel coated platinum coils (HydroCoil): early single-center experience. AJNR Am J Neuroradiol 27: , Cloft HJ, HEAL Investigators: HydroCoil for Endovascular Aneurysm Occlusion (HEAL) study: 3-6 month angiographic follow-up results. AJNR Am J Neuroradiol 28: , Dai D, Ding YH, Danielson MA, Kadirvel R, Hunter LW, Zhan WZ, et al: Endovascular treatment of experimental aneurysms by use of fibroblast-coated platinum coils: an angiographic and histopathologic study. Stroke 38: , Deshaies EM, Adamo MA, Boulos AS: A prospective singlecenter analysis of the safety and efficacy of the HydroCoil embolization system for the treatment of intracranial aneurysms. J Neurosurg 106: , Graves VB, Ahuja A, Strother CM, Rappe AH: Canine model of terminal arterial aneurysm. AJNR Am J Neuroradiol 14: , Kallmes DF, Fujiwara NH: New expandable hydrogel-platinum coil hybrid device for aneurysm embolization. AJNR Am J Neuroradiol 23: , Kang HS, Han MH, Lee TH, Shin YS, Roh HG, Kwon OK, et al: Embolization of intracranial aneurysms with hydrogelcoated coils: results of a Korean multicenter trial. Neurosurgery 61:51 59, Murayama Y, Suzuki Y, Viñuela F, Kaibara M, Kurotobi K, Iwaki M, et al: Development of a biologically active Guglielmi detachable coil for the treatment of cerebral aneurysms: part 1 in vitro study. AJNR Am J Neuroradiol 20: , Murayama Y, Viñuela F, Suzuki Y, Akiba Y, Ulihoa A, Duckwiler GR, et al: Development of the biologically active Guglielmi detachable coil for the treatment of cerebral aneurysms: part 2 an experimental study in a swine aneurysm model. AJNR Am J Neuroradiol 20: , Murayama Y, Viñuela F, Tateshima S, Song JK, Gonzalez NR, Wallace MP: Bioabsorbable polymeric material coils for embolization of intracranial aneurysm: a preliminary experimental study. J Neurosurg 94: , Sato M, Harasaki H: Evaluation of platelet and coagulation 15
6 T. Tsumoto, Y. Niimi, and A. Berenstein function in different animal species using the xylum clot signature analyzer. ASAIO J 48: , Song JK, Niimi Y, Yoshino Y, Khoyama S, Berenstein A: Assessment of Matrix coils in a canine model of a large bifurcation aneurysm. Neuroradiology 49: , Szikora I, Wakhloo AK, Guterman LR, Chavis TD, Dawson RC 3rd, Hergenrother RW, et al: Initial experience with collagen-filled Guglielmi detachable coils for endovascular treatment of experiment aneurysms. AJNR Am J Neuroradiol 18: , Tsumoto T, Matsumoto H, Terada T, Tsuura M, Itakura T, Hamamoto T: A polyvinyl alcohol core coil containing basic fibroblast growth factor evaluated in rabbits with aneurysms induced by elastase. Neurosurgery 61: , Tsumoto T, Song JK, Niimi Y, Berenstein A: Interval change in size of venous Pouch canine bifurcation aneurysms over a 10 month period. AJNR Am J Neuroradiol 29: , Yoshino Y, Niimi Y, Song JK, Silane M, Berenstein A: Endovascular treatment of intracranial aneurysms: comparative evaluation in a terminal bifurcation aneurysm model in dogs. J Neurosurg 101: , 2004 Manuscript submitted July 7, Accepted October 23, Please include this information when citing this paper: published online March 27, 2009; DOI: / JNS Address correspondence to: Tomoyuki Tsumoto, M.D., Department of Neurosurgery, Japanese Red Cross Society, Wakayama Medical Cen ter, 4-20 Komatsubara-dori, Wakayama City , Japan. tsumoto1029@gmail.com. 16 J Neurosurg / Volume 111 / July 2009
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