Middle cerebral artery bifurcation aneurysms: an anatomic classification scheme for planning optimal surgical strategies.

Surgical Anatomy and Technique

Middle Cerebral Artery Bifurcation Aneurysms: An Anatomic Classification Scheme for Planning Optimal Surgical Strategies BACKGROUND: Changing landscapes in neurosurgical training and increasing use of endovascular therapy have led to decreasing exposure in open cerebrovascular neurosurgery. To ensure the effective transition of medical students into competent practitioners, new training paradigms must be developed. OBJECTIVE: Using principles of pattern recognition, we created a classification scheme for middle cerebral artery (MCA) bifurcation aneurysms that allows their categorization into a small number of shape pattern groups. METHODS: Angiographic data from patients with MCA aneurysms between 1995 and 2012 were used to construct 3-dimensional models. Models were then analyzed and compared objectively by assessing the relationship between the aneurysm sac, parent vessel, and branch vessels. Aneurysms were then grouped on the basis of the similarity of their shape patterns in such a way that the in-class similarities were maximized while the total number of categories was minimized. For each category, a proposed clip strategy was developed. RESULTS: From the analysis of 61 MCA bifurcation aneurysms, 4 shape pattern categories were created that allowed the classification of 56 aneurysms (91.8%). The number of aneurysms allotted to each shape cluster was 10 (16.4%) in category 1, 24 (39.3%) in category 2, 7 (11.5%) in category 3, and 15 (24.6%) in category 4. CONCLUSION: This study demonstrates that through the use of anatomic visual cues, MCA bifurcation aneurysms can be grouped into a small number of shape patterns with an associated clip solution. Implementing these principles within current neurosurgery training paradigms can provide a tool that allows more efficient transition from novice to cerebrovascular expert.

Chad W. Washington, MS, MPHS, MD* Tao Ju, PhD‡ Gregory J. Zipfel, MD* Ralph G. Dacey, Jr, MD* *Department of Neurological Surgery, and ‡Department of Computer Science and Engineering, Washington University in St. Louis, Missouri Portions of this work were presented as a topic in the Honored Guest Lecture presented by Dr Dacey at the 2012 Congress of Neurological Surgeons Annual Meeting; October 6-10, 2012; Chicago, Illinois. Correspondence: Chad W. Washington, MS, MPHS, MD, Washington University School of Medicine, Department of Neurological Surgery, 660 S. Euclid Ave, Campus Box 8057, St. Louis, MO 63110. E-mail: [email protected] Received, May 27, 2013. Accepted, November 7, 2013. Published Online, November 12, 2013. Copyright © 2013 by the Congress of Neurological Surgeons.

KEY WORDS: Cerebral aneurysm, Cerebrovascular surgery, Neurosurgical training Operative Neurosurgery 10:145–155, 2014

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ost neurosurgeons consider middle cerebral artery (MCA) aneurysms to be surgical lesions. They make up 20% to 25% of intracranial aneurysms and represent a significant component of cerebrovascular surgery.1 However, although the overall number of cerebral aneurysms being treated continues to increase, since the publication of the International WHAT IS THIS BOX? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code above links to Supplemental Digital Content from this article.

OPERATIVE NEUROSURGERY

ABBREVIATIONS: DSA, digital subtraction angiography; MCA, middle cerebral artery Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).

DOI: 10.1227/NEU.0000000000000250

Subarachnoid Aneurysm Trial,2 the proportion of them treated by surgical clipping is declining.3-5 In addition, neurosurgical trainees are having less exposure to open aneurysm surgery as a result of work hour restrictions.6,7 These limitations have had and will continue to have a significant impact on neurosurgical training. The goal of neurosurgical residency programs is to provide an educational atmosphere that allows the transition of medical students into independent, competent practitioners, ie, from novice to proficient to expert surgeons.8 In the most basic sense, differences distinguishing experts from novices revolve around the ability of an expert to complete a task faster and more accurately than novices.9 There can obviously be a wide spectrum

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WASHINGTON ET AL

ranging from novice to proficient practitioner to expert.10 During an individual’s training, the rate of this transition is related to a number of factors such as innate ability, environment, and perhaps most important, exposure time. In fact, a number of studies assessing the components necessary for achieving and maintaining a level of expert performance have found that deliberate practice over an extended period of time (10-20 years) is necessary.10,11 Therefore, with the progressive decline in exposure to cerebral aneurysm clippings, new methods must be developed to provide the appropriate degree of training. The creation of such techniques has become a focus of organized neurological surgery, and efforts to implement virtual reality and simulation technologies into resident training are being explored.12,13 In consideration of this problem, one can look to other training domains requiring a high degree of expertise with minimal margin for error: training of military personnel, of pilots, and in other medical fields. Many of these programs have effectively implemented training modules based on the principle of “perceptive learning” to bridge the gap between novice and expert.9-11,14-17 A basic definition of perceptual learning is the following: improvement of an individual to extract information from his or her environment as a result of deliberate practice. In terms of visual stimuli, this refers to pattern recognition. Within the medical field, training modules implementing pattern recognition methods have proved to be effective in teaching anatomy, analysis of x-ray images, and surgical techniques.14,15,17 Currently, a number of imaging modalities are used in cerebrovascular surgery: digital subtraction angiography (DSA), computed tomographic angiography, and magnetic resonance angiography. Of these, DSA is perhaps the most well established in its ability to provide information on the anatomic characteristics of aneurysms, and it continues to be used significantly for training and treatment planning.18 As angiography techniques have improved, there has been a significant interest in analyzing the morphological features of aneurysms and their impact on the risk of rupture.19-25 Thus far, however, there has been a very limited analysis of how these features affect operative strategy.26,27 We believe that pattern recognition is an important attribute of the competent neurovascular surgeon and that efficient use of the information provided in 3-dimensional (3-D) DSA can be expanded. The current hypothesis is that objective morphological attributes of MCA aneurysms exist that allow their categorization into a relatively small number of shape pattern groups and furthermore that these shape patterns can predict the optimal clip solution.

rotational angiography imaging protocol. Imaging parameters were rotation speed of 45 per second, frame rate of 30 frames per second, and field of view of 49 cm. This provided on average a 1024 · 1024 · 130-slice image volume with a 0.29-mm pixel resolution. With the use of a combination of automated, semiautomated, and manual segmentation methods provided in the imaging software packages Osirix (version 4.1.2, Pixmeo, Geneva, Switzerland) and Seg-3-D (version 2.1; Center for Integrative Biomedical Computing, University of Utah, Salt Lake City, Utah), regions of interest were segmented. Anatomically, the regions were bound proximally by the internal carotid artery at the level of the ophthalmic artery origin and distally by the transition of the M2 to M3 division of the MCA. These segmentations allowed the creation of 3-D models viewable using the 3-D Volume Rendering module provided in Osirix. Models were constructed by the first author.

Development of Classification Rules Each 3-D model created was evaluated and categorized by 2 reviewers (C.W.W. and R.G.D.). Before classification, the following terms were defined (see Video 1, Supplemental Digital Content 1, http://links.lww.com/NEU/A610, which demonstrates the aspects of the different aneurysm classifications and potential clip solutions for each category): 1. Vessel projection: vector with direction defined by vessel flow and origin at the parent/branch vessel intersection (Figure 1). 2. Side-wall aneurysm: projection of the aneurysm is perpendicular to the projection vector of the parent vessel (Figure 1). 3. End-wall aneurysm: the projection of the aneurysm is parallel to the projection vector of the parent vessel (Figure 2). 4. Branch angle: the angle between the projection vectors of the parent and branch vessel within the branch plane. Each branch vessel has an associated angle (Figure 2). 5. Branch plane: 2-dimensional plane defined by the projection vectors of branch vessels (Figure 3). 6. Width plane: 2-dimensional plane defined by the long axis of the aneurysm neck and the projection of the aneurysm. Clip application tends to occur within this plane (Figure 3).

PATIENTS AND METHODS Study Population and 3-D Model Creation Patients were retrospectively selected from all patients who underwent craniotomy for clipping of a MCA bifurcation aneurysm from 1995 through 2012. Further inclusion criteria included the availability of the raw 3-D DSA data. Angiography data were acquired with the Artis Zee flat-detector biplane system (Siemens AG, Erlangen, Germany) using the Siemens 5sDSA

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FIGURE 1. The dark arrows represent projection vectors of the aneurysm, parent vessel, and branch vessels. The M1 vector originates at the internal carotid artery bifurcation and projects to the middle cerebral (MCA) bifurcation. The M2 branch projections represent the direction of these vessels as they originate from the MCA bifurcation. Sidewall aneurysms are those with a projection perpendicular to the direction of flow of the parent vessel.

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MCA ANEURYSM ANATOMIC CLASSIFICATION SCHEME

FIGURE 2. End-wall aneurysms are those in which the projections of the aneurysm and the parent vessel are parallel. The branch angles are defined between the branch and parent vessel projections.

Aneurysm shape patterns were then analyzed and compared objectively by assessing the relationship among the aneurysm sac, parent vessel, and branch vessels (Table 1). Specifically, aneurysm sacs were classified as either sidewall or end-wall types. Branches vessels were analyzed by comparing their relative diameters and branch angles. Finally, the relative orientation of the width plane to the branch plane was assessed. With the use of the above definitions and comparison criteria, aneurysms were grouped together on the basis of the similarity of their shape patterns. After the grouping of the aneurysms, a classification scheme was created that maximized the in-class similarities while minimizing the total number of categories. For each category a proposed clip strategy was developed.

RESULTS Complete 3-D DSA data were acquired and used to construct 3-D models for 61 MCA bifurcation aneurysms. From the analysis of the shape patterns, 4 categories were created that allowed the classification of 56 aneurysms (92%). The number of aneurysms allotted to each shape cluster was as follows: 10 (16.4%) in category 1, 24 (39.3%) in category 2, 7 (11.5%) in category 3, and 15 (24.6%) in category 4. Shape Cluster Characteristics In shape category 1 (Figure 3A and Figure 4A), aneurysms arose from the side wall of an M2 branch that was significantly larger than the other M2 branch and was in nearly straight continuation from the distal M1 (see Video 1 and Table 2). The optimal clip strategy for this aneurysm uses either a straight or a gently curved clip placed across the neck of the aneurysm


parallel to the larger of the M2 branches while sparing the smaller branch (Figure 4B). In shape category 2 (Figure 3B and Figure 5A), aneurysms arose from the distal M1 bifurcation as end-wall-type aneurysms. In this class, the M2 branch vessels had relatively equivalent diameters and acute branch angles (# 90). The major axis of the aneurysm neck (width plane) in this class paralleled the branch plane. With this, the optimal clip strategy is either an angled or right-angled clip placed parallel to this long axis between the 2 conduits of the M2s (Figure 5B). In shape category 3 (Figure 3C and Figure 6A), aneurysms were similar to category 2 in that aneurysms were end-wall-type lesions with relatively symmetric branch vessels projecting at acute angles (# 90). The difference in this pattern is that the width plane and branch plane were perpendicular. As a result, the optimal clip strategy uses a “shank” clip28 applied parallel to the major axis of the aneurysm neck, which again is perpendicular to the M2 branch vessels (Figure 6B). With this strategy, the shank portion of the clip captures the proximal fundus of the neck while the clip tips capture the distal portion. In shape category 4 (Figure 3D and Figure 7A), aneurysms were end-wall-type lesions with branch vessels of relatively equal size; however, the branch angles were not acute (. 90). This resulted in branch vessels projecting posterior and lying next to the M1 parent vessel within the sylvian fissure. The aneurysms also tended to be larger, incorporating the origin of the branch vessels. Therefore, although the aneurysm neck is parallel to the M2 branches, the optimal clip strategy is more complicated than that found in categories 1 and 2. The aneurysm is decompressed with temporary clips and needle aspiration, allowing precise application of aneurysm clip(s), which preserves the conduit between the M1 and its major divisions (Figure 7B). Of the 61 aneurysms analyzed, 5 (8%) could not be successfully categorized by the proposed classification scheme. These aneurysms were defined by very unique morphologies. Three of the 5 aneurysms were best described as fusiform dilatations of the MCA artery with or without a saccular component. The remaining 2 aneurysms involved a trifurcating MCA artery. Similar to their morphologies, each of these aneurysms had a singularly unique clip strategy, not limited to but including bypass.

DISCUSSION This study introduces a novel shape-based classification scheme for MCA bifurcation aneurysms. Using specific and subjectively defined definitions in the anatomic analysis of 61 aneurysms, we identified 4 unique shape patterns allowing the accurate categorization of . 90% of these aneurysms. Furthermore, for each category, an optimal clip strategy has been proposed. Use of this categorization scheme has the ability to hasten cerebrovascular surgery education by providing novice neurosurgeons insight into the cognitive processes used by experts in their operative planning. Past studies analyzing aneurysm geometry have focused primarily on differences between ruptured and unruptured



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FIGURE 3. The branch plane (blue) is the 2-dimensional plane defined by the parent vessel and branch vessel projection vectors (black arrows). The width plane (yellow) is defined by the aneurysm projection vector (red arrow) and the major axis of the aneurysm neck (red bar). In categories 1 (A), 2 (B), and 4 (D), the branch plane and width planes are parallel. Category 3 (C) is unique in that the branch plane and width plane are perpendicular.

aneurysms. Hassan et al21 analyzed 53 aneurysmal geometric formations using computational flow dynamic modeling and described 3 shape categories: sidewall, sidewall with branch vessel, and end-wall aneurysms. The flow patterns were found to be significantly different, and although the categories were not predictive of rupture, they correlated with location of rupture. TABLE 1. Classification Factors for Shape Pattern Analysis Category 1 Category 2 Category 3 Category 4

Sidewall vs end-wall aneurysm Equivalent branch vessel diameters vs asymmetrical diameters Branch angles # 90 vs . 90 Width plane is parallel vs perpendicular to branch plane


Dhar and colleagues29 reviewed the morphological characteristics of 45 aneurysms and found that “aneurysm angle” (defined as the angle between the major projection axis of the aneurysm and the plane of the neck) was a significant predictor of aneurysm rupture. Baharoglu et al20 reported similar findings from their study using 3-D modeling and computational flow dynamics to analyze 116 sidewall aneurysms. They found that increasing in-flow angle (angle between the major axis of the aneurysm and medial axis of parent vessel) led to increased intra-aneurysmal flow velocity and was significantly increased in ruptured aneurysms. Lin and colleagues22 implemented a similar morphological analysis of 132 MCA aneurysms and found that increasing in-flow angle was significantly associated with ruptured vs unruptured aneurysms. In contradistinction, Baharoglu et al19 compared the morphological features of 271 aneurysms and found that in-flow angle was associated with rupture in only sidewall- but not bifurcation-type aneurysms.




FIGURE 4. A, category 1 shape pattern is distinguished by the presence of a sidewall aneurysm, asymmetrical M2 branch vessels, the larger M2 being a continuation of the M1 parent vessel, and parallel width and branch planes. B, the clip solution for this category is placement of a gently curved clip parallel to the larger of the M2 branch vessel. The curve allows complete closure of the aneurysm neck while sparing the smaller branch vessel.

With such interest in morphological parameters and the impact these have on a patient’s clinical course, tools for the quantitative analysis of cerebral aneurysm imaging data continue to be developed. Piccinelli et al30 presented a semiautomated framework for the characterization of cerebrovascular geometry, the vascular modeling toolkit. Using a set of sophisticated mathematical concepts (including Voroni diagrams, wave propagation theory, and centerline geometry), they were able to deconstruct complex vasculature into a set of individual components. This breakdown into basic structures allows the rapid calculation of geometric characteristics such as branch angles, curvature, and torsion. Use of anatomic factors to plan operative strategy is not an original concept. Through his experience, Yas ̧argil31 noted that for MCA bifurcation aneurysms the direction of the fundus projection could be classified by 3 principal directions: anterosuperior, toward the sylvian fissure; posterior, between the M2s; and inferior, toward the insula. Identification of the unique projection of an aneurysm can help to improve the surgeon’s understanding of the relationship of the aneurysm to the superior and inferior MCA trunks during dissection. From their experience treating . 1300 MCA bifurcation aneurysms, Dashti et al32 expanded on this idea of classifying on the basis of fundus projection to define 5 types: intertruncal, inferior, lateral, insular, and complex. They use this categorization to tailor patient positioning and microsurgical

approach. More recently, Lawton27 described a generalized classification for MCA aneurysms. He described 5 types that are based on the projection of the aneurysm dome relative to the M1 segment projection arc: lateral type, inferior tilt, superior tilt, posterior tilt, and anterior tilt. Surgeons are able to use this scheme to plan a safe route of dissection that avoids the dome of the aneurysm. These classifications, based on a wide breadth of experience, are based on very similar principles and are particularly useful in planning a microsurgical approach. However, they do not provide insight into appropriate clip strategy. With a purpose more closely related to our study, a categorization scheme for MCA aneurysms was defined by Kumar et al26 to help guide surgeons in choosing a clipping strategy. In their analysis of 141 patients who underwent clipping, MCA bifurcation aneurysms were divided into 5 subtypes related to morphological features. This classification was defined as follows: type 1 (simple), aneurysm arising from distal projection of M1 but with no extension to M1 proximally; type 2 (central type), aneurysm arising from distal M1 but with neck extending into M1 proximally; type 3 (complicated type), branch vessel arising at the neck of the aneurysm; type 4 (complex), aneurysm neck involving M2 branches; and type 5, blister aneurysm. With increasing complexity from type 1 to 4, the likelihood of the clipping strategy requiring multiple clips increased from 0% to

TABLE 2. Shape Cluster Characteristics Category 1 Sidewall aneurysm arising from the M1/M2 junction

Category 2 End-wall aneurysm arising from the distal M1

Asymmetrical M2 branch vessel Symmetrical M2 branch vessel diameters diameters Larger M2 is a continuation of the M1 Branch angles # 90 parent vessel Width plane is parallel to the branch Width plane is parallel to the plane branch plane


Category 3

Category 4

End-wall aneurysm arising from the distal M1

End-wall aneurysm arising from the distal M1

Symmetrical M2 branch vessel diameters Branch angles # 90

Symmetrical M2 branch vessel diameters Branch angles . 90

Width plane is perpendicular to the branch plane

Width plane is parallel to the branch plane



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FIGURE 5. A, category 2 aneurysms are defined by end-wall aneurysms, symmetrical branch vessels, branch angles # 90, and the width plane parallel to the branch plane. B, the optimal clip solution uses a rightangled clip placed across the aneurysm neck that is parallel to both the width and branch planes.

100%, respectively. It was also noted that strategies for specific types could be generalized. Type 2 could use shank clipping to avoid the need for multiple clips; type 3 requires the use of a fenestrated clip to maintain patency of branch vessels; and type 4 needs a complex application of multiple clips to reconstruct the bifurcation of the MCA. The results from this analysis demonstrate that MCA aneurysms may be classified on the basis of basic anatomic principles into a small number of shape patterns with the wide variability of

MCA bifurcation aneurysms captured. The classification strategy presented by Kumar et al26 is similar in theory; however, this scheme expands this idea by creating multiple criteria for each shape pattern, which provides more accurate grouping of aneurysms. These criteria allow rapid, objective categorization without the need for advanced geometrical analysis. In addition, the cognitive process used by experienced cerebrovascular surgeons to develop clip solutions has been deconstructed. With this categorization scheme, it has been shown that clipping

FIGURE 6. A, category 3 aneurysms are shaped similar to category 2 aneurysms with end-wall aneurysms, symmetrically branching vessels, and branch angles # 90. B, however, because the width plane and branch planes lie perpendicular to one another, the clip solution must be modified so that a shank clip is placed across the aneurysm neck lying perpendicular to the M2 branch vessels.





FIGURE 7. A, shape category 4 is characterized by a more complex relationship between the aneurysm, branch vessels, and parent vessel. In this group, although the aneurysm is an end-wall type and the branch vessels are relatively symmetric, the branch angle is . 90. This causes the M2 vessels to project more posterior toward the M1 parent vessel. B, in addition, these aneurysm tend to be larger and to encompass the origins of the branch vessels. As a result, the clip solution requires the use of temporary clips and needle aspiration. The decompressed aneurysm can then be clipped in such a way that ensures patency of the M1/M2 branch vessel conduits.

principles can be applied to these general shapes to guide surgical strategy. For example, accurate identification of category 3 aneurysms in the proposed system would prevent a surgeon from inappropriately placing a curved clip, potentially leaving a remnant, or placing a clip parallel to the MCA bifurcation plane (ie, perpendicular to the aneurysm neck), which is more likely to result in branch vessel stenosis (Figures 8A and 8B). As a result of advances in endovascular techniques, modern paradigms for the treatment of cerebral aneurysms have led to

a marked decline in open surgical clipping. Simon et al4 examined the percentage of cerebral aneurysms treated with surgical clipping in 1996 vs 2006 in a cohort of Medicare patients and found that surgical clipping declined from 80% to 33%. A similar finding was noted by Andaluz and Zuccarello,5 who analyzed the Nationwide Inpatient Sample and found that the proportion of surgical clippings declined from 52% in 1993 to 34% in 2003. In conjunction with these findings, overall surgical exposure in residency has declined since the implementation of duty hour restrictions by the Accreditation Council for Graduate Medical

FIGURE 8. A, appropriate categorization of aneurysms preoperatively can help prevent the inappropriate application of a clip solution. For example, here a curved clip will leave a significant residual aneurysm neck, whereas, a right-angled clip would be forced inferiorly (B), resulting in encroachment of the M1/M2 bifurcation.




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Education. Evidence for this was provided by McCall et al7 in their intradepartmental assessment of neurosurgery resident case volume. They found that case load in non-chief-level residents decreased on average by 45% when comparing pre-duty hour years with post-duty hour years. In a larger nationwide cohort of surgical residents, Kairys et al6 found that decreased work hours affected the surgical experience of not only junior residents but also chief residents. In the years following work hour restrictions, they found that the chief resident case load declined by 8%. To combat the impact of decreasing exposure, 2 potential options exist: increasing resident training time or modifying the current training scheme to provide exposure outside the operating room. Others have demonstrated evidence that the use of pattern recognition techniques can be implemented successfully for medical and surgical training.14,15,17 We believe that the information presented here can be implemented in such a way that the training gap created by declining exposure can be effectively bridged. There are limitations to the study. Analysis was limited to aneurysms for which 3-D data were available. From these data, the proposed categories were created, and although these definitions are specific, not all aneurysms can be definitively placed into a particular category. For example, it is possible that an aneurysm could fall within the spectrum of both shape category 2 and shape category 4. Second, the retrospective nature of the study does not allow validation of the clip solutions with intraoperative data. The clip strategies defined were developed from the experiences and opinions of the senior neurosurgery authors (R.G.D. and G.J.Z.). To further validate the proposed categorizations, we are now prospectively analyzing the ability of the preoperative classification to predict the ultimate clip solution. Finally, the concepts presented here are not intended to fully encompass every factor that must be evaluated when planning the operative strategy needed to treat MCA bifurcation aneurysms. Other considerations such as rupture status, presence of calcifications and/or intraluminal thrombus, and surgical accessibility of the aneurysm must be considered. Beyond application of the categorization scheme to aid in resident training, we envision additional future directions. First, there are plans to analyze other aneurysm locations to develop similar categorization schemes that are specifically designed to guide optimal clip solutions. Second, it is believed that modeling this cognitive process into an automated shape analysis algorithm is imminently feasible. The software needed for this automation is currently available and implements the principles of machine learning and facial recognition. Preliminary results,33 although not presented here, are encouraging and demonstrate that computerized shape analysis may play a role in future surgical tools.

CONCLUSION The present study demonstrates that with the use of anatomic visual cues, MCA bifurcation aneurysms can be grouped into a small number of shape patterns. These patterns in turn can be recognized and used to develop appropriate clip solutions. Implementing these principles within current training paradigms can provide a tool that


allows more efficient transition from novice to cerebrovascular expert. As exposure to aneurysm clipping declines, the need for such applications will grow increasingly necessary. The onus is on neurosurgeons to maintain the specialty’s degree of excellence in microsurgical treatment of cerebral aneurysms. Disclosure 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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22. Lin N, Ho A, Gross BA, et al. Differences in simple morphological variables in ruptured and unruptured middle cerebral artery aneurysms. J Neurosurg. 2012;117 (5):913-919. 23. Sadatomo T, Yuki K, Migita K, Taniguchi E, Kodama Y, Kurisu K. Morphological differences between ruptured and unruptured cases in middle cerebral artery aneurysms. Neurosurgery. 2008;62(3):602-609; discussion 602-609. 24. Xiang J, Natarajan SK, Tremmel M, et al. Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke. 2011;42(1):144-152. 25. Sadatomo T, Yuki K, Migita K, Taniguchi E, Kodama Y, Kurisu K. Evaluation of relation among aneurysmal neck, parent artery, and daughter arteries in middle cerebral artery aneurysms, by three-dimensional digital subtraction angiography. Neurosurg Rev. 2005;28(3):196-200. 26. Kumar MV, Karagiozov KL, Chen L, et al. A classification of unruptured middle cerebral artery bifurcation aneurysms that can help in choice of clipping technique. Minim Invasive Neurosurg. 2007;50(3):132-139. 27. Lawton MT. Seven Aneurysms: Tenets and Techniques for Clipping. New York: Thieme; 2011. 28. Osawa M, Obinata C, Kobayashi S, Tanaka Y. Newly designed bayonet clips for complicated aneurysms: technical note. Neurosurgery. 1995;36(2):425-426; discussion 426-427. 29. Dhar S, Tremmel M, Mocco J, et al. Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery. 2008;63(2):185-196; discussion 196-197. 30. Piccinelli M, Veneziani A, Steinman DA, Remuzzi A, Antiga L. A framework for geometric analysis of vascular structures: application to cerebral aneurysms. IEEE Trans Med Imaging. 2009;28(8):1141-1155. 31. Yas a̧ rgil MG. Microneurosurgery. Stuttgart, Germany: Georg Thieme Verlag;; 1987. 32. Dashti R, Hernesniemi J, Niemela M, et al. Microneurosurgical management of middle cerebral artery bifurcation aneurysms. Surg Neurol. 2007;67(5): 441-456. 33. Dacey R, Washington C, Ju T, Zipfel G. Patterns of occurrence and surgical solutions across the spectrum of saccular and fusiform middle cerebral artery aneurysms. Paper presented at: Congress of Neurological Surgeons; October 6-10, 2012; Chicago, IL.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).

COMMENTS

I

n a retrospective review of 7 years of aneurysm clipping data, the authors have developed a succinct, simple stratification scheme for middle cerebral artery (MCA) aneurysms with a goal to help learning (clipping) skills, which are on the wane. They have nicely documented the immediate problem in training residents to properly and safely clip aneurysms: diminishing case volume as a result of the advent of interventional techniques to secure aneurysms and reduced experience in the operating room foisted on the specialty by Council for Graduate Medical Education work hour restrictions. This categorization of MCA lesions is most timely and appropriate because at present they are the aneurysms least likely to be able to be safely obliterated by interventional techniques.1 The authors note that others before them have classified MCA aneurysms using different schemes, but they were often aimed at identifying the optimal surgical approach. The authors propose using their classification scheme to speed learning by simplifying clipping strategy. Taking advantage of advanced 3-dimensional reconstruction techniques to help refine the classification scheme, they put great thought into simplifying the classification scheme to allow a quicker transition from a resident who has never clipped an MCA aneurysm to an advanced cerebrovascular surgeon. The authors are to be


congratulated for bringing these valuable techniques in perceptual learning tested in other “real-world” disciplines to the cerebrovascular surgery realm. I look forward to seeing their future work using automated shape analysis algorithms and computer simulation to further aid in clipping strategies. Paul J. Camarata Kansas City, Kansas

1. Rodríguez-Hernández A, Sughrue ME, Akhavan S, Habdank-Kolaczkowski J, Lawton MT. Current management of middle cerebral artery aneurysms: surgical results with a “clip first” policy. Neurosurgery. 2013;72(3):415-427.

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ndovascular therapy has left a large footprint in the care of aneurysms, but on occasion there is absolutely no alternative except a surgical one. Middle cerebral artery (MCA) aneurysms have always fallen under the domain of the open neurosurgical therapist, although continued inroads to therapy endovascularly exist. This article tries to reconcile the paradox of increasing aneurysm complexity that is being addressed in today’s operating rooms with decreasing surgical training and experience. I have always been a believer that heuristic techniques represent the “fine art” of neurosurgery, and this article begins to address this “form of art” from a training standpoint; MCA aneurysms seem the most logical place to begin. The authors subdivide MCA aneurysm types into 4 category shape types: sidewall, end-wall, end-wall with additional perpendicular growth, end-wall with obtuse branch angles. I would submit that the authors have made a heroic start in linking clip classification to these potentially complex aneurysm configurations, but more work is needed. The most dangerous problem with MCA aneurysms is not so much proximal control or exposure but clip placement without distal vascular compromise. For me, from a clipping standpoint, MCA aneurysms are either simple or complex. The simple cases include (depending on size) most of the sidewall and end-wall aneurysms. The basic tenet of Charles Drake to clip aneurysms parallel and not perpendicular to flow will allow safe occlusion of these aneurysms without vascular compromise. Surgeons have their favorite instruments and vascular neurosurgeons their favorite clips, so maintaining flow and accomplishing clipping is what matters. Flow diversion, even in open surgical procedures, is what matters. Complex aneurysms, on the other hand, have several characteristics: 1 of the M2 branches is typically smaller and therefore more prone to compromise; the base of the aneurysm incorporates the distal side of the proximal M2 branch, exposing it to crimping and risk; total enlargement of the distal MCA (M1) in all dimensions (the authors end-wall with additional perpendicular growth), coupled with an obtuse branch angle; calcium and atheromatous involvement; or intraluminal clot. I am always reluctant to clip any aneurysm perpendicular to the inflow vessel (as the authors suggest for the type with end-wall with perpendicular growth) for fear of kinking the smaller of the distal M2 vessels and compromising its flow. Occasionally, this can be done, but for me this is not the rule of thumb. The most dangerous MCA aneurysms are the end-wall type with obtuse branch angles and steep neck expansion in all dimensions, especially perpendicular to the flow of the M1. These aneurysms usually require significant remodeling many times with opening and multiple clips. The rapid enlargement of the dome from its point of origin makes clipping particularly difficult. Finally, adherence of M2 branches



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themselves to the dome will preclude clipping without compromise unless these arteries are somehow freed allowing for clip placement. This is always more difficult because these arteries wander and become adherent to the fundus away from the neck of the aneurysm. With complex MCA aneurysms, there comes a time that the surgeon is better off using multiple clips. Repetitive clip applications result only in intimal damage, the potential for downstream ischemia, and if too much time is spent, a flow-no reflow phenomenon even in the face of a perfect clipping. I prefer direct clipping rather than trapping with bypass, but all vascular techniques may be needed when direct clipping coupled with bypass for the smaller vessel may be required. Opening the aneurysm also may be required, although this action increases the risk of the procedure exponentially in my mind. The authors have embarked on a journey to help younger surgeons begin dealing with some of these complex aneurysms. The clip application techniques are helpful, but other heuristic factors play a role with effective therapy. I have never been able to identify preemptively which complex MCA aneurysms will require bypass even by studying the configuration of the aneurysm preoperatively, so it is not uncommon for us to have the radial artery exposed but not harvested in the complex types. I look forward to further progress in this area and find the novel concept of “perceptual learning” intriguing. Winfield S. Fisher Birmingham, Alabama

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he authors reviewed angiographic data from 61 middle cerebral artery aneurysms over a 17-year period. They constructed 3-dimensional models that were then analyzed, and 56 of the aneurysms were classified into 4 categories based on similar patterns. This elegant study is an excellent first step to synthesizing the cognitive planning that more experienced surgeons perform almost unconsciously when choosing clip types and configuration for middle cerebral artery aneurysms. It might have been of interest to readers if the authors had elaborated on the 5 cases that did not fall neatly into one of the 4 defined categories. I agree that this type of modeling could be an important tool in the training of neurosurgical residents as the number of open surgical cases continue to dwindle. The authors should be congratulated on this article, and I look forward to their analysis of other aneurysm types. Cargill H. Alleyne, Jr Augusta, Georgia

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iddle cerebral artery (MCA) bifurcation aneurysms are often wide necked and may involve 1 or both branches of the bifurcation. Although double stent-assisted coiling has been a great advance, the problem of angiographic occurrence represents a major limitation. Surgical clipping is still the most efficient treatment for MCA bifurcation aneurysms. The goal of surgical treatment is to completely clip the neck without neck remnants while preserving normal flow of branches of bifurcation. Regarding the diversity of aneurysm morphology, anatomy, and hemodynamic characteristics, the optimal clip strategy is required to adequately reconstruct the normal anatomy and is often unique for each case of an MCA bifurcation aneurysm. The authors introduce a novel shape-based classification scheme for MCA bifurcation aneurysms by assessing the relationship among the aneurysm sac, parent vessel, and branch vessels. MCA bifurcation aneurysms were subdivided into 4 categories: sidewall, end-wall with acute branch angles, end-wall with perpendicular plane, and end-wall with


obtuse branch angles. The authors also proposed an optimal clip strategy for each category. This study might provide a good tool in the training of neurosurgical residents. However, because of the limited number of patients, the morphological analysis in this study does not account for surgical accessibility with respect to the operator. Ruptured MCA bifurcation aneurysms were usually associated with an irregular wall and less spherical geometry. Additionally, branch vessel adherence to the aneurysms sac is a critical factor. For these complex aneurysms, multiple clipping strategies and remodeling are common. Although useful for training purposes, additional methods using emerging technologies in surgical simulation will be increasingly beneficial in gaining experience in open cerebrovascular surgical techniques. These emerging technologies will be increasingly important in the endovascular era when open microsurgical experience is becoming more difficult to attain. Xu Feng Nicholas C. Bambakidis Cleveland, Ohio

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he rapid growth of neuroendovascular techniques has changed the way we approach the standard treatment of cerebral aneurysms. In many centers, the proportion of cerebral aneurysms that are treated surgically has declined, and those that are treated surgically are often more complex. As a result, the open surgical experience of neurosurgical trainees has suffered. We congratulate the authors on their approach to this problem. The authors introduced a novel shape-based classification for middle cerebral artery bifurcation aneurysms. They present a retrospective analysis of 61 middle cerebral artery bifurcation aneurysms that were treated with surgical clip obliteration over a 17-year period. These aneurysms were modeled with 3-dimensional software, and a total of 56 were used for classification. On the basis of selected angiographic factors (side wall vs end-wall aneurysms, relative size of the branching M2 branches, branch angles, and the width plane in relation to the branch plane), the aneurysms were classified into 4 subtypes, and an “optimal” clip strategy was proposed. The authors concluded that, “Implementing these principles within current neurosurgery training paradigms can provide a tool that allows more efficient transition from novice to cerebrovascular expert.” This is an excellent article. It is timely and provides useful insight into the highly intuitive process of microsurgical aneurysm clipping. As the authors point out, this type of expertise can take many years to develop. We agree that characterizing this experience into a scheme may allow others to incorporate these techniques into their own practice more quickly. There is certainly more work to be done. This article is by no means comprehensive. Instead, it is the opinion of mature cerebrovascular practitioners based on careful analysis of their surgical experience. The absolute number of aneurysms is small, but the strategies are distilled from many years of surgical practice. And although the article focuses only on surgical strategies, a similar analysis could be performed with endovascular options in mind. Indeed, it may be useful to use such 3-dimensional model analysis as a means for comparison between surgical and endovascular alternatives. We look forward to further work to correlate the strategies put forth in this article with actual clinical data and outcomes. Moreover, it would be interesting to see how the strategies of this group compare with those from other highly experienced practitioners. It is likely that there would be some common trends but also some significant and equally effective approaches.




The authors successfully translate their experience into realistic classification system that is accessible to novice practitioners and can be studied, practiced, and modeled. It is not a substitute for experience but provides an excellent distillation of 3-dimensional surgical anatomy and heuristic information. As simulation becomes a more important part of training, systems such as these can be used to form the basis of surgical aneurysm clipping simulators. The present article represents a major contribution to


the education of in-training neurosurgeons. We hope that the proposed classification will be adopted by multiple institutions to confirm its validity. William Ashley Wael Hassaneen Maywood, Illinois



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