|Year : 2019 | Volume
| Issue : 3 | Page : 773-779
Use of our protocol of multimodality tools to aid in the safe microsurgical clipping of unruptured anterior circulation aneurysms
Satish Kannan1, Yasuhiro Yamada2, Kyosuke Miyatani2, Takao Teranishi2, Arun Reddy Marathi3, Krishna Mohan4, Tsukasa Kawase2, Yoko Kato2
1 Department of Neurosurgery, Institute of Neurosciences and Spinal Disorders, MGM Health Care, Chennai, Tamil Nadu, India
2 Department of Neurosurgery, Bantane Hospital, Fujita Health University, Nagoya, Japan
3 Department of Neurosurgery, Prathima Hospitals, Hyderabad, Telangana, India
4 Department of Neurosurgery, KIMS, Nellore, Andhra Pradesh, India
|Date of Web Publication||2-Aug-2019|
Institute of Neurosciences and Spinal Disorders, MGM Health Care, Chennai, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Objectives: The aim of this study is to analyze the effectiveness of our protocol of the use of multimodality tools, namely indocyanine green-dual image video angiography, neuroendoscope, neuromonitoring with motor-evoked potential, micro-Doppler in the microsurgical clipping of unruptured anterior circulation aneurysms, operated at our institute from January 2016 to December 2018. Materials and Methods: We performed a retrospective analysis of all cases of unruptured anterior circulation aneurysms, operated at Fujita Health University Banbuntane-Hotokukai Hospital, Japan, from January 2016 to December 2018. We assessed outcome at immediate postoperative, at discharge, and at 3 months follow-up by defining permanent morbidity as drop in Modified Rankin Scale (MRS) by 1 at 3 months follow-up and transient morbidity as temporary deficit that improved at discharge or follow-up. Postoperative events, namely seizures, infection that did not affect/change. Preoperative MRS and discharge timing were excluded. We concluded poor outcome as MRS ≥3 and good outcome as MRS <3 (0–2). All patients had a minimum of 3 months follow-up before outcome conclusion. Results: In 2016, a total of 98 cases were operated with no mortality or permanent morbidity (i.e., change in preoperative MRS), only transient morbidity was seen in (two cases) 2.04%. In 2017, a total of 119 cases were operated with no mortality or morbidity. In 2018, a total of 130 cases were operated with no mortality or permanent morbidity, only transient morbidity 0.7%. Summarizing from January 2016 to December 2018, a total of 347 cases of anterior circulation aneurysms were operated. Mostly, in the female sex (73.3%), the most common was middle cerebral artery aneurysm (39.1%). The mean size was 5.3 mm with no mortality or permanent morbidity with only transient morbidity in 0.9%. No poor outcome (MRS ≥3) was seen in our series. Conclusion: In our center for most unruptured anterior circulation aneurysms, microsurgical clipping is the treatment of choice. We believe our protocol of the intra-operative usage of multimodality tools have aided in the safe microsurgical clipping and have consistently resulted in good operative outcomes. Hence, we recommend and continue to use our Fujita-Bantane Protocol in all cases of micro-surgical clipping of aneurysms to consistently achieve good operative outcomes.
Keywords: Anterior circulation aneurysms, dual image video angiography, incidental aneurysms, indo-cyanine green, motor-evoked potentials, neuro-endoscope, neuro-monitoring, safe clipping, surgical outcome, unruptured aneurysms
|How to cite this article:|
Kannan S, Yamada Y, Miyatani K, Teranishi T, Marathi AR, Mohan K, Kawase T, Kato Y. Use of our protocol of multimodality tools to aid in the safe microsurgical clipping of unruptured anterior circulation aneurysms. Asian J Neurosurg 2019;14:773-9
|How to cite this URL:|
Kannan S, Yamada Y, Miyatani K, Teranishi T, Marathi AR, Mohan K, Kawase T, Kato Y. Use of our protocol of multimodality tools to aid in the safe microsurgical clipping of unruptured anterior circulation aneurysms. Asian J Neurosurg [serial online] 2019 [cited 2019 Nov 20];14:773-9. Available from: http://www.asianjns.org/text.asp?2019/14/3/773/263967
| Introduction|| |
Advances in neuro-imaging and its widespread use for screening has led to an increase in the rate of diagnosis of un-ruptured intracranial aneurysms (UIAs) commonly known as Incidental Aneurysms. Although incidental cerebral aneurysms are common, the management is controversial., As reports from large-scale retrospective and prospective cohort studies have concluded that the risk of rupture associated with small UIAs is extremely low. These studies included data primarily from the Caucasian populations in North America and Europe, but the incidence of rupture is higher in Japan and Finland than in other regions.,, This difference in the rupture risk might be induced by differences in racial or genetic backgrounds.
The overall prevalence of UIAs in the Japanese population was 3.2%. The prevalence in women was higher than that in men (4.4% vs. 2.5%). The prevalence increased with age in both genders. Although the prevalence of intracranial aneurysms is low, aneurysmal rupture causing subarachnoid hemorrhage (SAH) can be devastating, with morbidity and mortality rates around 25% and 40%, respectively.,, The Un-ruptured Cerebral Aneurysm Study (UCAS) showed that the natural course of unruptured cerebral aneurysms varies according to the size, location, and shape of the aneurysm. The risk for rupture was significantly higher for aneurysms that were 7 mm or larger, aneurysms of the anterior communicating artery (A-Com A) and the internal carotid (IC)-posterior communicating artery (P-ComA), aneurysms with a daughter sac as independent factors. The International Study of UIAs trial and the UCAS stratified the risk of rupture for UIAs according to aneurysm size, with higher risk for aneurysms that were 7 mm or larger.
In this study, we analyze the effectiveness of our protocol of the usage of multimodality tools, namely indo-cyanine green-dual image video angiography (ICG-DIVA), neuroendoscope, neuromonitoring (motor-evoked potential [MEP]), micro-Doppler in the safe micro-surgical clipping of anterior circulation aneurysms, performed at our institute from 2016 to 2018.
| Materials and Methods|| |
We performed a retrospective analysis of all cases of unruptured anterior circulation aneurysms operated at Fujita Health University Banbuntane-Hotokukai Hospital, Japan, from January 2016 to December 2018 [Table 1]. Along with the UCAS recommendations, cases that showed aneurysmal growth on serial imaging was taken up for surgical treatment.
Preoperative imaging included two-dimensional and three-dimensional (3D) computed tomography angiography, computational fluid dynamics study demonstrating wall pressure, wall shear stress suggesting impending rupture. Magnetic resonance imaging & 3D digital subtraction angiography if indicated. We classified Permanent Morbidity as drop in Modified Rankin Scale (MRS) by 1 at 3 months follow-up and Transient Morbidity-as temporary deficit that improved at discharge or follow-up. Postoperative events, namely seizures, infection that did not affect/change discharge timing were excluded. We concluded poor outcome as MRS ≥3, good outcome as MRS <3 (0–2). In our hospital, all neurovascular surgeries are performed with OPMI Pentero Microscope (Carl Zeiss, Oberkochen, Germany) with infrared 800 camera for ICG-VA. The MINIRC-2000K (Mizuho Co., Ltd., Nagoya, Japan) NIR camera mounted on the microscope for DIVA. Right angled rigid endoscope (Machida, Japan) for endoscopic evaluation. Micro-Doppler ultrasound (DVM 4300, Hadeco, Japan). All surgeries were performed under general anesthesia for induction, followed by propofol sedation. No muscle relaxant agents were used after induction to facilitate MEP monitoring.
Intra-operative protocol as depicted in [Flowchart 1].
In 2016, a total of 98 cases of anterior circulation aneurysms were operated with majority being females (72.4%). Most common was middle cerebral artery (MCA) aneurysm 41.8%, followed by IC-P-Com aneurysm. Mean size was 4.8 mm with no mortality or permanent morbidity, only transient morbidity was seen in (2 cases) 2.04% [Table 2].
In 2017, a total of 119 cases of anterior circulation aneurysms were operated with majority being females (73.1%). Most common was MCA aneurysm 41.1%, followed by IC-P-Com aneurysm. Mean size was 6 mm approximately with no mortality or morbidity [Table 2].
In 2018, a total of 130 cases of anterior circulation aneurysms were operated with majority being females (74.6%). The most common was MCA aneurysm 34.6%, followed by A-Com aneurysm. The mean size was 5.1 mm approximately with no mortality or permanent morbidity, only transient morbidity 0.7% [Table 2].
| Results|| |
Summarizing from January 2016 to December 2018, a total of 347 cases of anterior circulation aneurysms were operated with majority being females (73.3%), most common was MCA aneurysm 39.1%. The mean size was 5.3 mm with no mortality or permanent morbidity, and transient morbidity in 0.9%. No poor outcome (MRS ≥3) was seen in our series [Table 3].
During the initial part of the study, MEP monitoring was done on a selective basis mostly for MCA, IC-P-Com, IC-Acho aneurysms, etc. AS the protocol evolved, we have used it for almost all the cases as mentioned above. Now it has become a routine for all cases. Suture removal was done on the 7th postoperative day, the average in-hospital stay was 12–14 days.
| Discussion|| |
Although the estimated 3% prevalence of intracranial aneurysms is low, aneurysm rupture causing SAH can be devastating, with morbidity and mortality rates around 25% and 40%, respectively.,, Despite recent improvements in surgical and medical management of aneurysmal SAH, the overall mortality rate produced by this disease is still high (approximately 40%–50%). The high mortality and morbidity rates are attributed mainly to brain damage caused by a severe initial hemorrhage, early re-bleeding, and delayed cerebral ischemia related to vasospasm., During the last two decades, detection of UIAs has increased because of new and improving diagnostic technology and its routine and increased use in screening. The overall prevalence of UIAs in the Japanese population was 3.2%. The prevalence in women was higher than that in men (4.4% vs. 2.5%). Female sex is an independent risk factor for the growth of UIAs in elderly patients.,, The prevalence increased with age in both genders.,, The size is considered to be an independent risk factor.,,,,,, The management of unruptured aneurysms is controversial, currently there are no randomized controlled trials to decide on the management of UIAs. The PHASES score and the UIA treatment score (UIATS) score are currently used in decision making. The PHASES score is a 5-year rupture rate estimation model based on 8283 patients diagnosed with UIAs and 29166 patient years of follow-up and the UIATS score is a consensus-based scoring system., Neither scoring system has been satisfactorily validated on an independent large cohort and there is a conflicting reports about such scoring systems leading to over treatment and questions about their reliability on stable UIAs, growing UIAs.,
Hence, the management of UIAs should take into consideration patient characteristics such as age, sex, ethnic background, comorbidities and aneurysm characteristics such as size, shape, location, and aspect ratio.,,,,,,,,,,,, The management of aneurysms at high volume centers by experienced neurosurgical and endovascular teams has excellent results, most experts agree that micro-surgical clipping should be the first line of treatment.,
In our center, micro-surgical clipping is the first line of treatment for most unruptured anterior circulation aneurysms. We have been using the Fujita-Bantane Protocol (FB Protocol) in all our cases. After sylvian dissection and exposure of the aneurysm.
Step 1 involves preclipping ICG-DIVA. Although standard ICG-VA (ICG alone) clearly highlights vascular structures from nonvascular structures as white and black images respectively, other structures cannot be observed.,,,, ICG-DIVA provides real-time simultaneous visualization of the aneurysm, vessels and surrounding structures including brain, nerves with far better depth perception thereby facilitating better anatomical correlation. This helps in quicker and more effective decision making during surgery., DIVA images giving better anatomical correlation clearly depicted here in [Figure 1].
|Figure 1: Illustrative case of internal carotid artery aneurysm with (a-c) depicting pre-clipping microscopic, indo-cyanine green, dual image video angiography images respectively. (d-f) Depicting post clipping microscopic, indo-cyanine green, dual image video angiography images respectively. Dual image video angiography images giving better anatomical correlation clearly depicted here. (g-i) Depicting post 2nd-clipping microscopic, indo-cyanine green, dual image video angiography images respectively|
Click here to view
Step 2 involves preclipping neuro-endoscopic evaluation. The neuro-endoscope, with its better illumination, higher magnification, extended viewing angles can provide real-time assessment about the hidden perforators, key neurovascular structures which are not visible under the dead angles of the microscope.,,, Additional technological advancements have made the neuro-endoscope not only as an diagnostic tool but also capable of assisting angiographic evaluation and guiding clipping procedure as shown in [Figure 2].,,,,
|Figure 2: Illustrative case of internal carotid-posterior communicating aneurysm (a and b) depicting preclipping microscopic, dual image video angiography images respectively. (c) Is endoscopic view depicting posterior communicating and perforators, not seen in microscopic view. (d and e) Depicting post-clipping microscopic, dual image video angiography images respectively. (f) Is endoscopic view showing posterior communicating preserved and complete obliteration of the aneurysm|
Click here to view
The Step 1 and Step 2 are repeated as per requirements. Continuous transcranial MEP monitoring is done during the procedure; initially, MEP monitoring was done on a case-to-case basis. Now has become a routine in all cases. Direct (cortical) MEP is sensitive in detecting ischemic stress to descending motor pathways during aneurysm surgery. Recently, increased use of combined trans-cranial and direct MEP monitoring is being practiced with better sensitivity and specificity as a part of multimodality monitoring during aneurysm surgery.,,, Micro-Doppler is used as an optional modality on a case-to-case basis, if additional information is required about the patency of the parent vessel or perforators.
The goal of aneurysm surgery is to achieve satisfactory clipping such that there is no residual filling of the aneurysm, distal branch and perforator occlusion, or parent vessel stenosis. As aneurysm remnants have potential for re-growth and hemorrhage, whereas clip occlusion of a parent artery or small hidden perforators can lead to permanent neurological deficits and is a devastating complication. Thus, preserving blood flow in the branches and perforators of a parent artery is very important for successful surgery.
We believe our protocol, which has evolved over a short period of time provides all the vital information to the operating surgeon, thereby aiding in quicker and better decision making to make microsurgical clipping safe. Thus, consistently resulting in satisfactory operative outcomes and achieving the goal of aneurysm surgery.
| Conclusion|| |
In the current era of neuro-vascular surgery, most randomized controlled trials are nearing a consensus that both open micro surgical clipping and endovascular treatment are equally efficient and viable treatment options in experienced hands., Although open micro surgical clipping is the gold standard treatment in terms of aneurysm obliteration rates and rebleeding rates, it is being constantly challenged by recent technological advancements and continuously evolving endovascular treatment modalities.,,,, Most experts agree that management of aneurysms done at high volume centers by experienced neurosurgical and endovascular teams has excellent results. In most centers micro-surgical clipping is the first line of treatment for unruptured aneurysms.,
In our center for most unruptured anterior circulation aneurysms micro-surgical clipping is the treatment of choice. We believe our protocol of the intra-operative usage of multimodality tools have aided in the safe micro-surgical clipping and have consistently resulted in good operative outcomes. Hence, we recommend and continue to use our FB Protocol in all cases of micro-surgical clipping of aneurysms to consistently achieve good operative outcomes.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms – Risk of rupture and risks of surgical intervention. N Engl J Med 1998;339:1725-33.
Wiebers DO, Whisnant JP, Huston J 3rd
, Meissner I, Brown RD Jr., Piepgras DG, et al.
Unruptured intracranial aneurysms: Natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 2003;362:103-10.
Vlak MH, Algra A, Brandenburg R, Rinkel GJ. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: A systematic review and meta-analysis. Lancet Neurol 2011;10:626-36.
Bederson JB, Awad IA, Wiebers DO, Piepgras D, Haley EC Jr., Brott T, et al.
Recommendations for the management of patients with unruptured intracranial aneurysms: A statement for healthcare professionals from the stroke council of the American Heart Association. Stroke 2000;31:2742-50.
Morita A, Fujiwara S, Hashi K, Ohtsu H, Kirino T. Risk of rupture associated with intact cerebral aneurysms in the Japanese population: A systematic review of the literature from Japan. J Neurosurg 2005;102:601-6.
Harada K, Fukuyama K, Shirouzu T, Ichinose M, Fujimura H, Kakumoto K, et al.
Prevalence of unruptured intracranial aneurysms in healthy asymptomatic Japanese adults: Differences in gender and age. Acta Neurochir (Wien) 2013;155:2037-43.
Burkhardt JK, Benet A, Lawton MT. Management of small incidental intracranial aneurysms. Neurosurg Clin N
UCAS Japan Investigators, Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, et al.
The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 2012;366:2474-82.
Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 1994;25:1342-7.
Fogelholm R, Hernesniemi J, Vapalahti M. Impact of early surgery on outcome after aneurysmal subarachnoid hemorrhage. A population-based study. Stroke 1993;24:1649-54.
Kubo Y, Koji T, Kashimura H, Otawara Y, Ogawa A, Ogasawara K. Female sex as a risk factor for the growth of asymptomatic unruptured cerebral saccular aneurysms in elderly patients. J Neurosurg 2014;121:599-604.
Wermer MJ, van der Schaaf IC, Algra A, Rinkel GJ. Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: An updated meta-analysis. Stroke 2007;38:1404-10.
Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms: Probability of and risk factors for aneurysm rupture. J Neurosurg 2000;93:379-87.
Ishibashi T, Murayama Y, Urashima M, Saguchi T, Ebara M, Arakawa H, et al.
Unruptured intracranial aneurysms: Incidence of rupture and risk factors. Stroke 2009;40:313-6.
Greving JP, Wermer MJ, Brown RD Jr., Morita A, Juvela S, Yonekura M, et al.
Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: A pooled analysis of six prospective cohort studies. Lancet Neurol 2014;13:59-66.
Etminan N, Brown RD Jr., Beseoglu K, Juvela S, Raymond J, Morita A, et al.
The unruptured intracranial aneurysm treatment score: A multidisciplinary consensus. Neurology 2015;85:881-9.
Ravindra VM, de Havenon A, Gooldy TC, Scoville J, Guan J, Couldwell WT, et al.
Validation of the unruptured intracranial aneurysm treatment score: Comparison with real-world cerebrovascular practice. J Neurosurg 2018;129:100-6.
Bijlenga P, Gondar R, Schilling S, Morel S, Hirsch S, Cuony J, et al.
PHASES score for the management of intracranial aneurysm: A cross-sectional population-based retrospective study. Stroke 2017;48:2105-12.
Ujiie H, Tachibana H, Hiramatsu O, Hazel AL, Matsumoto T, Ogasawara Y, et al.
Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms: A possible index for surgical treatment of intracranial aneurysms. Neurosurgery 1999;45:119-29.
Sonobe M, Yamazaki T, Yonekura M, Kikuchi H. Small unruptured intracranial aneurysm verification study: SUAVe study, Japan. Stroke 2010;41:1969-77.
Komotar RJ, Mocco J, Solomon RA. Guidelines for the surgical treatment of unruptured intracranial aneurysms: The first annual J. Lawrence pool memorial research symposium – Controversies in the management of cerebral aneurysms. Neurosurgery 2008;62:183-93.
Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: A new method for intraoperative assessment of vascular flow. Neurosurgery 2003;52:132-9.
Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, et al.
Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 2005;103:982-9.
Washington CW, Zipfel GJ, Chicoine MR, Derdeyn CP, Rich KM, Moran CJ, et al.
Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 2013;118:420-7.
Payner TD, Horner TG, Leipzig TJ, Scott JA, Gilmor RL, DeNardo AJ. Role of intraoperative angiography in the surgical treatment of cerebral aneurysms. J Neurosurg 1998;88:441-8.
Riva M, Amin-Hanjani S, Giussani C, De Witte O, Bruneau M. Indocyanine green videoangiography in aneurysm surgery: Systematic review and meta-analysis. Neurosurgery 2018;83:166-80.
Sato T, Suzuki K, Sakuma J, Takatsu N, Kojima Y, Sugano T, et al.
Development of a new high-resolution intraoperative imaging system (dual-image videoangiography, DIVA) to simultaneously visualize light and near-infrared fluorescence images of indocyanine green angiography. Acta Neurochir (Wien) 2015;157:1295-301.
Feletti A, Wang X, Tanaka R, Yamada Y, Suyama D, Kawase T, et al.
Dual-image videoangiography during intracranial microvascular surgery. World Neurosurg 2017;99:572-9.
Taniguchi M, Takimoto H, Yoshimine T, Shimada N, Miyao Y, Hirata M, et al.
Application of a rigid endoscope to the microsurgical management of 54 cerebral aneurysms: Results in 48 patients. J Neurosurg 1999;91:231-7.
Kato Y, Sano H, Nagahisa S, Iwata S, Yoshida K, Yamamoto K, et al.
Endoscope-assisted microsurgery for cerebral aneurysms. Minim Invasive Neurosurg 2000;43:91-7.
Tamaki N, Hara Y, Takaishi Y, Shimada S. Angled rigid neuroendoscope for continuous intraoperative visual monitoring: Technical note. J Clin Neurosci 2001;8:148-50.
Kalavakonda C, Sekhar LN, Ramachandran P, Hechl P. Endoscope-assisted microsurgery for intracranial aneurysms. Neurosurgery 2002;51:1119-26.
Mielke D, Malinova V, Rohde V. Comparison of intraoperative microscopic and endoscopic ICG angiography in aneurysm surgery. Neurosurgery 2014;10 Suppl 3:418-25.
Galzio RJ, Di Cola F, Raysi Dehcordi S, Ricci A, De Paulis D. Endoscope-assisted microneurosurgery for intracranial aneurysms. Front Neurol 2013;4:201.
Sharma BS, Kumar A, Sawarkar D. Endoscopic controlled clipping of anterior circulation aneurysms via keyhole approach: Our initial experience. Neurol India 2015;63:874-80.
] [Full text]
Yoshioka H, Kinouchi H. The roles of endoscope in aneurysmal surgery. Neurol Med Chir (Tokyo) 2015;55:469-78.
Yamada Y, Kato Y, Ishihara K, Ito K, Kaito T, Nouri M, et al.
Role of endoscopy in multi-modality monitoring during aneurysm surgery: A single center experience with 175 consecutive unruptured aneurysms. Asian J Neurosurg 2015;10:52.
] [Full text]
Szelényi A, Kothbauer K, de Camargo AB, Langer D, Flamm ES, Deletis V. Motor evoked potential monitoring during cerebral aneurysm surgery: Technical aspects and comparison of transcranial and direct cortical stimulation. Neurosurgery 2005;57:331-8.
Szelényi A, Langer D, Beck J, Raabe A, Flamm ES, Seifert V, et al.
Transcranial and direct cortical stimulation for motor evoked potential monitoring in intracerebral aneurysm surgery. Neurophysiol Clin 2007;37:391-8.
Motoyama Y, Kawaguchi M, Yamada S, Nakagawa I, Nishimura F, Hironaka Y, et al.
Evaluation of combined use of transcranial and direct cortical motor evoked potential monitoring during unruptured aneurysm surgery. Neurol Med Chir (Tokyo) 2011;51:15-22.
Seng LB, Yamada Y, Rajagopal N, Mohammad AA, Teranishi T, Miyatani K, et al.
Multimodality techniques in microsurgical clipping as the gold standard treatment in the management of basilar tip aneurysm: A case series. Asian J Neurosurg 2018;13:1148-57.
] [Full text]
Joo SP, Kim TS. The clinical importance of perforator preservation in intracranial aneurysm surgery: An overview with a review of the literature. Chonnam Med J 2017;53:47-55.
Molyneux A, Kerr R, International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group, Stratton I, Sandercock P, Clarke M, et al.
International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: A randomized trial. J Stroke Cerebrovasc Dis 2002;11:304-14.
McDougall CG, Spetzler RF, Zabramski JM, Partovi S, Hills NK, Nakaji P, et al.
The barrow ruptured aneurysm trial. J Neurosurg 2012;116:135-44.
Molyneux AJ, Birks J, Clarke A, Sneade M, Kerr RS. The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the international subarachnoid aneurysm trial (ISAT). Lancet 2015;385:691-7.
Thomas AJ, Ogilvy CS. ISAT: Equipoise in treatment of ruptured cerebral aneurysms? Lancet 2015;385:666-8.
Bakker NA, Veeger NJ, Van Dijk JM. ISAT: End of the debate on coiling versus clipping? Lancet 2015;385:2251.
Spetzler RF, McDougall CG, Albuquerque FC, Zabramski JM, Hills NK, Partovi S, et al.
3-year results. Neurosurg 2013;119:146-57. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23621600
. [Last accessed on 2019 Feb 22].
Spetzler RF, McDougall CG, Zabramski JM, Albuquerque FC, Hills NK, Russin JJ, et al.
The barrow ruptured aneurysm trial: 6-year results. J Neurosurg 2015;123:609-17.
Nanda A, Patra DP, Bir SC, Maiti TK, Kalakoti P, Bollam P, et al.
Microsurgical clipping of unruptured intracranial aneurysms: A single surgeon's experience over 16 years. World Neurosurg 2017;100:85-99.
Spetzler RF, Zabramski JM, McDougall CG, Albuquerque FC, Hills NK, Wallace RC, et al.
Analysis of saccular aneurysms in the barrow ruptured aneurysm trial. J Neurosurg 2018;128:120-5.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]