The recurrent aneurysm is an intriguing entity. Its occurrence depends on the interplay between hemodynamic stresses, aneurysm anatomy, and packing density of coils. Its incidence depends on how it is measured and, from the neurosurgeons’ perspective, how often the patients are referred for surgery. Because of the risk of rehemorrhage, recurrent aneurysms must be prevented with aggressive initial treatment, identified with diligent surveillance angiography, and treated when found. Despite the fact that half of our surgically explored recurrent aneurysms have extruded coils and aneurysm walls appear degraded, the recurrence problem remains less than expected. We have not detected any significant increases in coil recurrences despite the growth in endovascular market share. Surgical management of previously coiled aneurysms is a new and evolving neurosurgical challenge that will continue to change as novel technologies are introduced into clinical practice. Most recurrent aneurysms are amenable to surgical therapy but require advanced microsurgical expertise.
Despite the negative results of the Carotid Occlusion Surgery Study, a prospective, randomized, controlled trial that failed to show a benefit of superficial temporal artery-middle cerebral artery bypass compared with medical management in patients carefully selected on the basis of positron emission tomography scans and oxygen extraction, bypass surgery has been widely embraced as an important treatment for complex aneurysms. As discussed with recurrent aneurysms after coiling, bypass techniques combined with parent artery trapping or occlusion are important in the treatment of complex aneurysms, particularly those without a favorable endovascular option. Despite all of its advances, endovascular technology has yet to introduce an endovascular bypass that can challenge open microsurgical bypass.
Bypass surgery for aneurysms has gone through an evolution from extracranial-to-intracranial (EC-IC) bypass to intracranial-to-intracranial (IC-IC) bypass. The superficial temporal artery-middle cerebral artery bypass as championed by Yaşargil18 is the prototypical bypass the redirects extracranial flow to the intracranial circulation with a single end-to-side anastomosis on the brain surface that is relatively simple and technically feasible for many neurosurgeons. In response to flow limitations of this bypass, second-generation bypasses also rely on EC-IC redirection of flow but use high-flow interposition grafts (ie, saphenous vein or radial artery grafts) connected to donor sites in the patient’s neck.19-34 EC-IC bypasses are susceptible to problems associated with harvesting donor vessels, inadequate donor caliber, mismatch between donor and recipient, neck incisions, graft length, and vulnerability of the bypass to external trauma, all of which are solved with a third generation of bypasses that are entirely intracranial. Reconstructive bypasses revascularize intracranial arteries with other intracranial arteries, without contribution from extracranial donor arteries. These IC-IC bypasses are simple, elegant, and more anatomic than their EC-IC counterparts.35-38 IC-IC bypasses require no harvest of extracranial donors, spare patients a neck incision, shorten any interposition grafts, are protected within the cranium, and use caliber-matched donor and recipient arteries. The development of an array of IC-IC bypasses represents an important advance in bypass surgery for brain aneurysms.
These bypasses are categorized into 4 types of intracranial arterial reconstruction: in situ bypass, reimplantation, reanastomosis, and intracranial bypass grafts (Figure 3). In situ bypass brings donor and recipient arteries together with a side-to-side anastomosis along their parallel course without interposition graft (eg, PICA-PICA). Reimplantation reattaches an aneurysm branch artery to normal parent or branch artery end to side after occluding the aneurysm, often by trapping (eg, PICA reimplantation onto the proximal vertebral artery). After trapping and excising an aneurysm, reanastomosis brings the normal arterials ends together with an end-to-end anastomosis. Intracranial bypass grafts use interposition grafts to revascularize a branch artery from a distant donor site and require 2 anastomoses. These bypasses are performed in 4 anatomic sites: sylvian fissure for middle cerebral artery aneurysms, callosal cistern for anterior cerebral artery aneurysms, cisterna magna for PICA aneurysms, and the carotid and crural cisterns for basilar apex aneurysms. IC-IC bypass is particularly useful for unanticipated bypasses because they do not require the preparation of the extracranial donor vessel or a cervical donor site.
Despite many advantages, these bypasses have their own issues. They are technically more difficult that EC-IC bypasses, often in deep, constrained fields. Whereas EC-IC bypass requires temporary occlusion of a single recipient artery during anastomosis, IC-IC bypass requires temporary occlusion of 2 vessels, putting 2 vascular territories at risk of ischemia and postoperative occlusion. Nonocclusive bypass techniques like excimer laser-assisted nonocclusive anastomosis eliminate this temporary occlusion time, but occlusion time is well tolerated, usually causes mild ischemia, and is not associated with complications. A comparison of EC-IC and IC-IC bypasses demonstrated equivalent results, with aneurysm obliteration rates of 97% and 98%, bypass patency rates of 89% and 94%, and good neurological outcomes (Glasgow Outcome Scale score, 4-5 at late follow-up) of 89% and 91%, respectively. With results like these, IC-IC bypasses are increasingly popular and, in our aneurysm practice, account for nearly half of our bypass cases (65 bypasses, 47%; Table 3).
The availability of a wide array of bypasses has advanced contemporary aneurysm practice. Although bypasses have a role in the management of dolichoectactic, dissecting, thrombotic, calcified, and recurrent aneurysms, their role in the management of giant aneurysms demonstrates their transformative impact. In the past, deep hypothermic circulatory arrest was used to convert an unclippable aneurysm into a clippable one by collapsing it, eliminating risk of intraoperative rupture, and permitting aggressive manipulation, even entrance into the aneurysm to remove thrombus and to create a supple neck.27,39-43 However, hypothermic circulatory arrest incurs significant operative morbidity. Cannulation of the femoral vessels can cause dissections, occlusions, and compromise of distal circulation; prolonged circulatory arrest is associated with cerebral ischemic injury and poor neurological outcomes; and heparinization, slowing of the coagulation cascade by hypothermia, and trauma to red blood cells and platelets by the cardiopulmonary bypass pump contribute to postoperative bleeding complications. These risks have resulted in declining use of hypothermic circulatory arrest.44 Instead, indirect aneurysm occlusion with a bypass has become a more acceptable alternative, with indirect occlusion consisting of proximal occlusion, distal occlusion, or trapping. This strategy has important advantages. The bypass can be performed with predictable ischemia times, cerebroprotection, and relatively low complication rates. The dangers of direct attack are avoided, including perforator dissection and preservation around clips. Clips are applied to afferent and efferent arteries, avoiding pathological tissues at the neck that can cause clip slippage, intraoperative rupture, and branch artery occlusions. Endovascular techniques can be used for indirect aneurysm occlusion, allowing the adequacy of a surgical bypass to be tested before permanent occlusion and allowing staged aneurysm occlusion with safe use of heparinization or optimization of hemodynamics in the intensive care unit. A heavy reliance on bypass techniques for giant aneurysms (38% in our experience with 141 giant aneurysms) resulted in good outcomes in 81% and represents an important advance in microsurgery for aneurysms.44
Even in an era with excellent endovascular options, bypass techniques can make open microsurgery a better therapeutic option, as demonstrated by PICA aneurysms. A prevailing attitude among the endovascular community is that the PICA is expendable with minimal morbidity. PICA occlusion can be a significant complication, and although cerebellar infarcts may be tolerable in some cases, more often, they cause secondary deterioration from edema and brainstem compression and require urgent decompressive craniectomy.45-51 Bypass techniques offer an alternative to this deconstructive approach, enabling a constructive approach that preserves the PICA with direct clipping or replaces flow with bypass when sacrificed.52,53 Reconstructive options for PICA revascularization include PICA-PICA bypass, PICA reimplantation, PICA reanastomosis, and interposition grafts that use the vertebral artery as a donor. The cisterna magna is a favorable working space to perform these bypasses, and our results have demonstrated high patency rates and low stroke rates. Distal aneurysms are particularly amenable to a constructive approach, and in our experience with 29 distal PICA aneurysms, we performed bypasses in 7 patients. Endovascular experiences use little or no bypass surgery, and cerebellar infarctions suggest that angiographic assessments of collateral circulation are unreliable or that bypasses were not performed aggressively enough. PICA aneurysms are difficult to treat endovascularly because of unusual morphology, aberrant branching, distal location, small caliber of the parent artery, tortuosity, and angulations that preclude coiling. The ability to perform a bypass should make microsurgery the primary treatment option, or at least the next option when endovascular coiling fails, rather than deliberate PICA occlusion.
Flow diverters introduce an endovascular option for selected giant and complex aneurysms, with excellent results reported for those along the carotid artery in the cavernous and paraclinoid segments. However, flow diversion is not the easy answer in all giant and complex aneurysms because of the following limitations. First, results with aneurysms in the middle cerebral artery and posterior circulation have been poor, with high rates of perforator infarction and hemorrhage thought to be due to “jailed” perforators and inflow into aneurysms without outflow (“ball-valve” effect), respectively.54,55 Second, deployment is technically challenging and may not be possible in aneurysms associated with tortuous vasculature, diminutive parent arteries, and acute angles between afferent and efferent arteries. Third, flow diverters require the use of aspirin and Plavix and therefore are restricted to unruptured aneurysms. Finally, the high cost of these devices limits their widespread application. In contrast, open surgical bypass remains a technique that is applicable to most aneurysms, regardless of aberrant aneurysm or parent artery anatomy, can be performed in patients with ruptured and unruptured aneurysms alike, is inexpensive, and is part of a durable cure for complex and giant aneurysms that are trapped. Flow diverters are changing the management of these aneurysms and have diminished noticeably the indications for surgical bypass for petrocavernous and paraclinoid aneurysms. As technology evolves and expands the endovascular armamentarium, indications for bypass are expected to decrease but not vanish; therefore, bypass proficiencies should be maintained and surgical solutions practiced as part of multidisciplinary teams.
In contrast to endovascular therapy for aneurysms that has decentralized out of tertiary centers and into community hospitals, microsurgical therapy has increasingly centralized in tertiary centers. This trend, driven mainly by the proliferation of endovascular technology and practitioners, is decreasing the number of open aneurysm surgeons and increasing the complexity of aneurysms referred for microsurgical management. Centralization of aneurysm microsurgery has produced important advances in aneurysm outcomes, and historically, high-volume surgeons innovate new techniques and tools. Tertiary centers are equipped to apply multimodality approaches and to use the most sophisticated resources. In addition, the evidence is clear that patient morbidity and mortality are lower when complex procedures are performed at high-volume centers and by high-volume neurosurgeons.
Volume-outcome relationships have been demonstrated for aneurysms, with drops in mortality and morbidity seen in high-volume centers.56,57 Although large administrative data sets can be difficult to interpret because they lack detailed neurological outcome data, these large-cohort power analyses might not otherwise be feasible with single-provider or single-institution sources. In an analysis of pediatric aneurysms in the Nationwide Inpatient Sample, we found clear relationships between hospital-level aneurysm volume and outcomes of interest: discharge disposition, which is a surrogate for functional outcome and neurological status, and complication rates. Pediatric aneurysm patients have better discharge and complications profiles at higher-volume hospitals (Figure 4A and 4B). As demonstrated by these data, it is not uncommon to observe an initial decrement in outcomes going from the lowest quartile to the next, which is generally thought to be due to transfer practices that bias toward better outcomes. Data for both adults and children demonstrate that the odds of discharge to home without supportive services are improved at high-volume centers (Figure 4B). Interestingly, volume-outcome relationships are not universal for all procedures, as seen with pediatric endovascular interventions. These findings support the decentralization of endovascular therapy and the centralization of open microsurgical therapy for aneurysms.
With aneurysm patients, it is appropriate to manage their high acuity, treat their complex lesions, and maximize their outcomes through specialization, experience, and expertise that are available at the hospital-wide level. For a variety of cerebrovascular procedures, not only do high-volume surgeons at high-volume centers have lower mortality rates and lower complication rates, but patients have shorter lengths of stay and hospitals gain important economic advantages. Hospital and surgeon volume-outcome effects are independent and the hospital-related effect is greater, implying that the ecosystem of care supersedes a surgeon’s technical expertise. Specialized nursing care, diagnostic services, and a team of providers likely account for improved outcomes at high-volume centers.
The trend toward centralized aneurysm surgery is favorable and should progress even further. Bypass proficiency provides a useful explanation. Sundt et al62 reported a threshold effect for bypass surgery, with approximately 20 bypass operations needed to achieve a patency rate >90%. With centralization, >75% of aneurysm centers in the United States perform bypass with sufficient volume to meet this threshold. However, some of these centers require more than a decade to reach the threshold. Therefore, centralization benefits patients and aneurysm surgeons by concentrating case volume and improving outcomes, and further centralization may be needed to maximize these volume-outcome effects. Large metropolitan areas might be better served to further reduce the number of centers of excellence, and regions might be better served to develop networks for transferring patients within the region.
Endovascular techniques unleashed strong extrinsic forces that provoked reactive changes in aneurysm surgery. Open microsurgery must now compete with endovascular therapies, forcing surgery to become less invasive, more appealing to patients, lower risk, and efficacious for complex aneurysms, particularly those unfavorable for or failing with endovascular therapy. Open aneurysm surgery has advanced by embracing minimalism. Minimally invasive approaches tailor the surgical exposure to the patient’s unique anatomy, selecting the smallest possible craniotomy that still provides adequate exposure. The development of an array of IC-IC bypasses is another important advance that makes microsurgery a competitive option for complex and recurrent aneurysms. Trends centralizing aneurysm surgery in tertiary centers optimize results achievable with open microsurgery.
The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
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