Microsurgical Bypass for Complex Intracranial Aneurysms in the Endovascular Era: Insights from a High-Volume Referral Center
Abstract
1. Introduction
2. Materials and Methods
2.1. Eligibility Criteria
2.2. Data Collection
2.3. Statistical Analysis
3. Results
3.1. Patient Inclusion and Baseline Demographics
3.2. Indication for Bypass Surgery and Treatment Strategy
3.3. Aneurysm Occlusion, Bypass Patency, and Clinical Outcome
3.4. Illustrative Cases
3.4.1. Case 14—Giant Thrombosed MCA Bifurcation Aneurysm
3.4.2. Case 15—PICA Dissection Fusiform Aneurysm
3.4.3. Case 19—Dissected Fusiform AICA Aneurysm
4. Discussion
4.1. Key Findings
4.2. Role of Direct Bypass Surgery in Aneurysmal Management
4.3. Microvascular Training and Proficiency
4.4. Starting from Scratch
4.5. Strengths and Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
aSAH | Aneurysmal Subarachnoid Hemorrhage |
WFNS | World Federation of Neurosurgical Societies |
mFISHER | Modified Fisher grade |
ICG | Indocyanine Green |
CTA | Computed Tomography Angiography |
MRA | Magnetic Resonance Angiography |
DSA | Digital Subtraction Angiography |
CT | Computed Tomography |
IQR | Interquartile Range |
MCA | Middle Cerebral Artery |
M2 | Second segment of the Middle Cerebral Artery |
M3 | Third Segment of the Middle Cerebral Artery |
ATA | Anterior Temporal Artery |
PcomA | Posterior Communicating Artery |
PICA | Posterior Inferior Cerebellar Artery |
IC-IC | Intracranial-Intracranial |
EC-IC | Extracranial-Intracranial |
STA | Superficial Temporal Artery |
OA | Occipital Artery |
AICA | Anterior Inferior Cerebellar Artery |
mRS | Modified Rankin Scale |
FU | Follow-up |
References
- Etminan, N.; Chang, H.S.; Hackenberg, K.; de Rooij, N.K.; Vergouwen, M.D.I.; Rinkel, G.J.E.; Algra, A. Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: A systematic review and meta-analysis. JAMA Neurol. 2019, 76, 588–597. [Google Scholar] [CrossRef] [PubMed]
- Volovici, V.; Verploegh, I.S.; Satoer, D.; Vrancken Peeters, N.J.M.C.; Sadigh, Y.; Vergouwen, M.D.I.; Schouten, J.W.; Bruggeman, G.; Pisica, D.; Yildirim, G.; et al. Outcomes Associated with Intracranial Aneurysm Treatments Reported as Safe, Effective, or Durable: A Systematic Review and Meta-Analysis. JAMA Netw. Open 2023, 6, e2331798. [Google Scholar] [CrossRef]
- Roy, D.; Milot, G.; Raymond, J. Endovascular treatment of unruptured aneurysms. Stroke 2001, 32, 1998–2004. [Google Scholar] [CrossRef]
- Molyneux, A.J.; Kerr, R.S.; Yu, L.M.; Clarke, M.; Sneade, M.; Yarnold, J.A.; Sandercock, P. International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: A randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005, 366, 809–817. [Google Scholar] [CrossRef]
- Spetzler, R.F.; Roski, R.A.; Schuster, H.; Takaoka, Y. The Role of EC-IC in the Treatment of Giant Intracranial Aneurysms. Neurol. Res. 1980, 2, 345–359. [Google Scholar] [CrossRef]
- Jafar, J.J.; Russell, S.M.; Woo, H.H. Treatment of Giant Intracranial Aneurysms with Saphenous Vein Extracranial-to-Intracranial Bypass Grafting: Indications, Operative Technique, and Results in 29 Patients. Neurosurgery 2002, 51, 138–144. [Google Scholar] [CrossRef]
- Kai, Y.; Hamada, J.; Morioka, M.; Yano, S.; Mizuno, T.; Kuroda, J.; Todaka, T.; Takeshima, H.; Kuratsu, J. Treatment Strategy for Giant Aneurysms in the Cavernous Portion of the Internal Carotid Artery. Surg. Neurol. 2007, 67, 148–155. [Google Scholar] [CrossRef]
- Zhu, W.; Tian, Y.L.; Zhou, L.F.; Song, D.L.; Xu, B.; Mao, Y. Treatment Strategies for Complex Internal Carotid Artery (ICA) Aneurysms: Direct ICA Sacrifice or Combined with Extracranial-to-Intracranial Bypass. World Neurosurg. 2011, 75, 476–484. [Google Scholar] [CrossRef]
- EC/IC Bypass Study Group. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results Int. Randomized Trial. N. Engl. J. Med. 1985, 313, 1191–1200. [CrossRef]
- Powers, W.J.; Clarke, W.R.; Grubb, R.L.; Videen, T.O.; Adams, H.P.; Derdeyn, C.P.; COSS Investigators. Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: The Carotid Occlusion Surgery Study randomized trial. JAMA 2011, 306, 1983–1992. [Google Scholar] [CrossRef]
- Ma, Y.; Wang, T.; Wang, H.; Amin-Hanjani, S.; Tong, X.; Wang, J.; Tong, Z.; Kuai, D.; Cai, Y.; Ren, J.; et al. Extracranial-Intracranial Bypass and Risk of Stroke and Death in Patients With Symptomatic Artery Occlusion: The CMOSS Randomized Clinical Trial. JAMA 2023, 330, 704–714. [Google Scholar] [CrossRef]
- Agha, R.A.; Sohrabi, C.; Mathew, G.; Franchi, T.; Kerwan, A.; O’nEill, N.; Thoma, A.; Beamish, A.J.; Noureldin, A.; Rao, A.; et al. The PROCESS 2020 Guideline: Updating Consensus Preferred Reporting of Case Series in Surgery (PROCESS) Guidelines. Int. J. Surg. 2020, 84, 231–235. [Google Scholar] [CrossRef]
- Sano, H.; Inamasu, J.; Kato, Y.; Satoh, A.; Murayama, Y.; Murayama, Y. Modified World Federation of Neurosurgical Societies subarachnoid hemorrhage grading system. Surg. Neurol. Int. 2016, 7 (Suppl. S18), S502–S503. [Google Scholar] [CrossRef]
- Frontera, J.A.; Claassen, J.; Schmidt, J.M.; Wartenberg, K.E.; Temes, R.; Connolly, E.S.; Macdonald, R.L.; Mayer, S.A. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: The modified Fisher scale. Neurosurgery 2006, 59, 21–27; Discussion 21. [Google Scholar] [CrossRef]
- Bonita, R.; Beaglehole, R. Recovery of motor function after stroke. Stroke 1988, 19, 1497–1500. [Google Scholar] [CrossRef]
- Matano, F.; Tanikawa, R.; Kamiyama, H.; Ota, N.; Tsuboi, T.; Noda, K.; Miyata, S.; Matsukawa, H.; Murai, Y.; Morita, A. Surgical Treatment of 127 Paraclinoid Aneurysms with Multifarious Strategy: Factors Related with Outcome. World Neurosurg. 2016, 85, 169–176. [Google Scholar] [CrossRef]
- Matsukawa, H.; Miyata, S.; Tsuboi, T.; Noda, K.; Ota, N.; Takahashi, O.; Takeda, R.; Tokuda, S.; Kamiyama, H.; Tanikawa, R. Rationale for Graft Selection in Patients with Complex Internal Carotid Artery Aneurysms Treated with Extracranial to Intracranial High-Flow Bypass and Therapeutic Internal Carotid Artery Occlusion. J. Neurosurg. 2018, 128, 1753–1761. [Google Scholar] [CrossRef]
- Yoon, S.; Burkhardt, J.K.; Lawton, M.T. Long-Term Patency in Cerebral Revascularization Surgery: An Analysis of a Consecutive Series of 430 Bypasses. J. Neurosurg. 2019, 131, 80–87. [Google Scholar] [CrossRef]
- Molyneux, A.J.; Birks, J.; Clarke, A.; Sneade, M.; Kerr, R.S. 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, 691–697. [Google Scholar] [CrossRef] [PubMed]
- Aboukais, R.; Verbraeken, B.; Leclerc, X.; Gautier, C.; Vermandel, M.; Bricout, N.; Lejeune, J.P.; Menovsky, T. Protective STA-MCA Bypass to Prevent Brain Ischemia during High-Flow Bypass Surgery: Case Series of 10 Patients. Acta Neurochir. 2019, 161, 1207–1214. [Google Scholar] [CrossRef] [PubMed]
- Endo, H.; Fujimura, M.; Shimizu, H.; Endo, T.; Omodaka, S.; Inoue, T.; Sato, K.; Niizuma, K.; Tominaga, T. Optimal Timing of Extracranial-Intracranial Bypass with Microsurgical Trapping for Ruptured Blister Aneurysms of the Internal Carotid Artery. World Neurosurg. 2020, 136, e567–e577. [Google Scholar] [CrossRef]
- Lam, J.; Ravina, K.; Rennert, R.C.; Russin, J.J. Cerebrovascular Bypass for Ruptured Aneurysms: A Case Series. J. Clin. Neurosci. 2021, 85, 106–114. [Google Scholar] [CrossRef]
- Murai, Y.; Matano, F.; Shirokane, K.; Tateyama, K.; Koketsu, K.; Nakae, R.; Sekine, T.; Mizunari, T.; Morita, A. Lesion Trapping with High-Flow Bypass for Ruptured Internal Carotid Artery Blood Blister-Like Aneurysm Has Little Impact on the Anterior Choroidal Artery Flow: Case Series and Literature Review. World Neurosurg. 2021, 153, e226–e236. [Google Scholar] [CrossRef]
- Peeters, S.M.; Colby, G.P.; Kim, W.J.; Bae, W.I.; Sparks, H.; Reitz, K.; Tateshima, S.; Jahan, R.; Szeder, V.; Nour, M.; et al. Proximal Internal Carotid Artery Occlusion and Extracranial-Intracranial Bypass for Treatment of Fusiform and Giant Internal Carotid Artery Aneurysms. World Neurosurg. 2023, 180, e494–e505. [Google Scholar] [CrossRef]
- Wolfswinkel, E.M.; Ravina, K.; Rennert, R.C.; Landau, M.; Strickland, B.A.; Chun, A.; Wlodarczyk, J.R.; Abedi, A.; Carey, J.N.; Russin, J.J. Cerebral Bypass Using the Descending Branch of the Lateral Circumflex Femoral Artery: A Case Series. Oper. Neurosurg. 2022, 22, 364–372. [Google Scholar] [CrossRef]
- Chen, Y.; Chen, P.; Duan, G.; Li, R.; Li, Z.; Guo, G. Extracranial-Intracranial Bypass Surgery for Intracranial Aneurysm of the Anterior Cerebral Circulation: A Systematic Review and Meta-Analysis. Front. Neurol. 2023, 14, 1174088. [Google Scholar] [CrossRef]
- Esposito, G.; Amin-Hanjani, S.; Regli, L. Role of and Indications for Bypass Surgery After Carotid Occlusion Surgery Study (COSS)? Stroke 2016, 47, 282–290. [Google Scholar] [CrossRef]
- Volovici, V.; Cenzato, M.; Meling, T.R.; EXPERVASC. The European Expertise Network for Open Microvascular Surgery. Lancet Neurol. 2024, 23, 1187. [Google Scholar] [CrossRef] [PubMed]
- Volovici, V.; Verploegh, I.S.C.; Vos, J.C.; Delwel, E.J.; Bijvoet, H.W.C.; van Putten, E.H.P.; Schouten, J.W.; Avezaat, C.J.J.; Dirven, C.M.F.; Dammers, R. Can young vascular neurosurgeons become proficient in microsurgical clip reconstruction in the endovascular era? A Rotterdam cohort spanning 2 decades with propensity score matching for complexity. World Neurosurg. 2020, 144, e780–e788. [Google Scholar] [CrossRef]
- Dindelegan, G.C.; Dammers, R.; Oradan, A.V.; Vinasi, R.C.; Dindelegan, M.; Volovici, V. The Double Stitch Everting Technique in the End-to-Side Microvascular Anastomosis: Validation of the Technique Using a Randomized N-of-1 Trial. J. Reconstr. Microsurg. 2021, 37, 421–426. [Google Scholar] [CrossRef]
No. | Age at Treatment | Sex | Type bypass (Donor-Receiver) | Double Barrel | aSAH WFNS Grade | mFISHER Grade | Rupture Status | Location | Size and Morphology | Previous Treatments | Indication Bypass Treatment | Aneurysm Exclusion |
---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | 58 | M | EC-IC (STA-MCA) | Yes | - | - | Recanalized | MCA bif | Giant, saccular (partially thrombosed) | 3x Coiled | Aneurysm rest | Clip reconstruction |
2 | 67 | F | IC-IC (Intermediate M2-ATA) | No | III | I | Ruptured | MCA bif | Small, saccular | None | Intermediate M2 branch from aneurysm sac | Clip reconstruction |
3 | 32 | F | IC-IC (Temporo-occipital-Temporo-occipital) | No | I | I | Ruptured, dissection | Temporo-occipital artery | Small, saccular | None | M4 branch rescue | Excision |
4 | 69 | F | EC-IC (STA-MCA) | Yes | - | - | Unruptured | MCA bif | Large, saccular (partially thrombosed, calcified base) | None | Not amenable to endovascular therapy | Clip reconstruction |
5 | 61 | F | EC-IC (STA-MCA) | No | II | III | Ruptured, dissection | MCA bif | Large, saccular | None | Not amenable to endovascular therapy | Clip reconstruction |
6 | 65 | F | EC-IC (STA-MCA) | Yes | - | - | Unruptured | MCA bif | Giant, saccular (partially thrombosed, calcified base) | None | Not amenable to endovascular therapy | Clip reconstruction |
7 | 51 | M | IC-IC (PICA-PICA) | No | I | II | Ruptured, dissection | PICA | Small, fusiform | None | Parent vessel (PICA) occlusion | Trapping, coiling |
8 | 64 | F | EC-IC (STA-MCA) | No | - | - | Unruptured | M2 | Small, bilobar (partially thrombosed, calcified base) | None | Parent vessel (M2) occlusion | Clip reconstruction |
9 | 48 | F | EC-IC (OA-PICA) | No | - | - | Recanalized | PICA | Neck remnant, growth | 1x Coiled | Neck remnant growth and recanalization | Trapping, coiling |
10 | 45 | F | IC-IC (M2 superior-M1) | No | V | I | Ruptured | MCA bif | Very large, saccular (partially thrombosed, calcified base) | None | M2 trunk occlusion | Excision |
11 | 70 | M | EC-IC (STA-MCA) | No | - | - | Unruptured | MCA bif | Large, saccular (partially thrombosed, calcified base) | None | Not amenable to endovascular therapy | Trapping |
12 | 46 | F | EC-IC (STA-MCA) | Yes | N/A | N/A | Ruptured | PcomA | Small, neck remnant | 1x Coiled | Neck remnant rupture and ICA dissection during endovascular retreatment | Trapping |
13 | 51 | F | EC-IC (STA-MCA) | No | - | - | Recanalized | MCA bif | Large, saccular (partially thrombosed) | 1x Flow Diverter | Aneurysm rest | Clip reconstruction |
14 | 63 | M | EC-IC (STA-MCA) | No | - | - | Unruptured | MCA bif | Giant, saccular (thrombosed, calcified base) | None | Not amenable to endovascular therapy | Trapping |
15 | 44 | F | IC-IC (PICA-PICA) | No | II | II | Ruptured, dissection | PICA | Blood-blister aneurysm | None | Not amenable to endovascular therapy | Excision |
16 | 29 | M | IC-IC (Callosomarginal-Callosomarginal) | No | V | III | Ruptured, dissection | Callosomarginal artery | Small, saccular | None | Traumatic aneurysm | Trapping |
17 | 60 | F | IC-IC (PICA-PICA) | No | I | II | Ruptured, dissection | PICA | Small, saccular | None | Not amenable to endovascular therapy | Excision |
18 | 65 | M | EC-IC (STA-MCA) | No | - | - | Unruptured | MCA bif | Giant, saccular (partially thrombosed) | None | Not amenable to endovascular therapy | Clip reconstruction |
19 | 35 | F | EC-IC (OA-AICA) | Yes | II | II | Ruptured, dissection | AICA | Very small, fusiform | None | Parent vessel (AICA) occlusion | Trapping |
20 | 62 | F | IC-IC (PICA-PICA) | No | - | - | Recanalized | PICA | Small neck remnant | 2x coiled | Not amenable to endovascular therapy | Trapping |
Patient | Aneurysm Occlusion | Intraoperative Bypass Patency | Postoperative Bypass Patency | FU Bypass Patency/FU Duration (mo) | mRS Discharge | mRS FU 6 Months | mRS Last Available FU/FU Duration (mo) | Procedure-Related Hypoperfusion | Procedure-Related Permanent Morbidity | Procedure-Related Mortality |
---|---|---|---|---|---|---|---|---|---|---|
1 | Total occlusion | Yes | Yes | Yes/7 | 4 | 3 | 2/94 | Yes | Yes | No |
2 | Total occlusion | Yes | Yes | Yes/1 | 3 | N/A | 1/2 | No | No | No |
3 | Total occlusion | Yes | Yes | Yes/3 | 0 | 0 | 0/10 | No | No | No |
4 | Total occlusion | Yes | Yes | Yes/4 | 1 | N/A | 1/13 | No | No | No |
5 | Neck rest | Yes | Yes | Yes/5 | 1 | 1 | 0/24 | No | No | No |
6 | Total occlusion | Yes | Yes | Yes/0 | 4 | N/A | 3/2 | Yes | No | No |
7 | Total occlusion | Yes | Yes | Yes/21 | 3 | 3 | 2/58 | No | No | No |
8 | Total occlusion | Yes | Yes | Yes/2 | 1 | 0 | 0/10 | No | No | No |
9 | Total occlusion | Yes | Yes | Yes/6 | 0 | 0 | 0/54 | No | No | No |
10 | Total occlusion | Yes | Yes | Yes/33 | 4 | 3 | 3/33 | No | No | No |
11 | Total occlusion | Yes | Yes | Yes/0 | 3 | N/A | N/A | No | No | No |
12 | Total occlusion | No | No | No | 5 | 4 | 3/14 | No | No | No |
13 | Total occlusion | Yes | Yes | Yes/15 | 0 | 1 | 0/12 | No | No | No |
14 | Total occlusion | Yes | Yes | Yes/4 | 1 | 0 | 0/6 | No | No | No |
15 | Total occlusion | Yes | Yes | Yes/7 | 0 | 1 | 1/6 | No | No | No |
16 | Total occlusion | Yes | Yes | Yes/1 | 2 | 2 | 1/6 | No | No | No |
17 | Total occlusion | Yes | Yes | Yes/6 | 4 | N/A | 2 | Yes | No | No |
18 | Total occlusion | N/A | Yes | Yes/4 | 1 | N/A | 0 | No | No | No |
19 | Total occlusion | Yes | Yes | Yes/5 | 1 | N/A | 1 | No | No | No |
20 | Total occlusion | Yes | Yes | Yes/0 | 6 | - | - | No | No | No |
Time Point | mRS Category | No. Patients (All, %) | No. Patients (Ruptured, %) | No. Patients (Unruptured or Recanalized, %) |
---|---|---|---|---|
n = 18 | n = 9 | n = 9 | ||
Preoperative | 0 | 7 (39) | 2 (22) | 5 (55) |
1 | 4 (22) | 1 (11) | 3 (33) | |
2 | 2 (11) | 2 (22) | 0 (0) | |
3 | 1 (5) | 0 (0) | 1 (11) | |
4 | 2 (11) | 2 (22) | 0 (0) | |
5 | 2 (11) | 2 (22) | 0 (0) | |
n = 20 | n = 10 | n = 10 | ||
Discharge | 0 | 4 (20) | 2 (20) | 2 (20) |
1 | 6 (30) | 2 (20) | 4 (40) | |
2 | 0 (0) | 0 (0) | 0 (0) | |
3 | 3 (15) | 2 (20) | 1 (10) | |
4 | 5 (25) | 3 (30) | 2 (20) | |
5 | 1 (5) | 1 (10) | 0 (0) | |
6 | 1 (5) | 0 (0) | 1 (10) | |
n = 12 | n = 7 | n = 5 | ||
6 months FU | 0 | 4 (33) | 1 (14) | 3 (60) |
1 | 3 (25) | 2 (28) | 1 (20) | |
2 | 0 (0) | 0 (0) | 0 (0) | |
3 | 1 (8) | 1 (14) | 0 (0) | |
4 | 4 (33) | 3 (43) | 1 (10) | |
5 | 0 (0) | 0 (0) | 0 (0) | |
6 | 0 (0) | 0 (0) | 0 (0) | |
n = 18 | n = 10 | n = 8 | ||
Median last FU duration (mo, IQR) | 13 (10–33) | 12 (10–54) | 19 (10–33) | |
Last FU | 0 | 7 (39) | 2 (20) | 5 (62) |
1 | 5 (28) | 4 (40) | 1 (12) | |
2 | 3 (17) | 2 (20) | 1 (12) | |
3 | 3 (17) | 2 (20) | 1 (12) | |
4 | 0 (0) | 0 (0) | 0 (0) | |
5 | 0 (0) | 0 (0) | 0 (0) | |
6 | 0 (0) | 0 (0) | 0 (0) |
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Sadigh, Y.; Haasdijk, E.J.; Dammers, R.; Volovici, V. Microsurgical Bypass for Complex Intracranial Aneurysms in the Endovascular Era: Insights from a High-Volume Referral Center. J. Clin. Med. 2025, 14, 6027. https://doi.org/10.3390/jcm14176027
Sadigh Y, Haasdijk EJ, Dammers R, Volovici V. Microsurgical Bypass for Complex Intracranial Aneurysms in the Endovascular Era: Insights from a High-Volume Referral Center. Journal of Clinical Medicine. 2025; 14(17):6027. https://doi.org/10.3390/jcm14176027
Chicago/Turabian StyleSadigh, Yasmin, Eva Joëlle Haasdijk, Ruben Dammers, and Victor Volovici. 2025. "Microsurgical Bypass for Complex Intracranial Aneurysms in the Endovascular Era: Insights from a High-Volume Referral Center" Journal of Clinical Medicine 14, no. 17: 6027. https://doi.org/10.3390/jcm14176027
APA StyleSadigh, Y., Haasdijk, E. J., Dammers, R., & Volovici, V. (2025). Microsurgical Bypass for Complex Intracranial Aneurysms in the Endovascular Era: Insights from a High-Volume Referral Center. Journal of Clinical Medicine, 14(17), 6027. https://doi.org/10.3390/jcm14176027