Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms

Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms

Journal of Clinical Neuroscience xxx (2016) xxx–xxx Contents lists available at ScienceDirect Journal of Clinical Neuroscience journal homepage: www...

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Journal of Clinical Neuroscience xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn

Clinical Study

Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms Eberval Gadelha Figueiredo a,⇑, Leonardo C. Welling b, Mark C. Preul c, Gabriel Reis Sakaya a, Iuri Neville a, Robert F. Spetzler c, Manoel Jacobsen Teixeira a a b c

Division of Neurological Surgery, University of Sao Paulo, Rua Maestro Cardim 808, CEP 01323-001 Sao Paulo, Brazil State University of Ponta Grossa, Parana, Brazil Barrow Neurological Institute, Phoenix, AZ, USA

a r t i c l e

i n f o

Article history: Received 20 May 2015 Accepted 19 July 2015 Available online xxxx Keywords: Anterior circulation aneurysms Cerebral aneurysm Minipterional craniotomy Pterional craniotomy Surgical technique

a b s t r a c t The pterional approach was described in the 1970s and has become the most utilized cranial approach with many variations described, including the minipterional technique. Although described recently as an alternative to the pterional approach for anterior circulation aneurysms, to our knowledge a large series of cases using the minipterional approach in both ruptured and unruptured aneurysms has not been described. We present our clinical experience with the minipterional craniotomy in more than 100 ruptured and unruptured anterior circulation aneurysms. The results of 86 consecutive patients with 102 ruptured non-giant, anterior circulation aneurysms treated with early surgery utilizing the minipterional craniotomy were analyzed. Postoperative angiography was carried out in all cases. Outcome results were classified as excellent in 67 (77.9%), and good in seven (8.1%), while 16 (13.9%) patients died. The minipterional technique provides adequate surgical exposure and excellent outcomes for both ruptured and unruptured anterior circulation aneurysm clipping. It constitutes a safe and effective alternative to the pterional approach, with equivalent or potentially better aesthetic and functional outcomes. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction The pterional craniotomy (PT) is one of the most utilized cranial approaches. It is highly versatile and constitutes a paradigm against which alternative surgical techniques to the same anatomical targets or cranial regions have been tested [1–7]. The PT, however, has inherent disadvantages, including functional and esthetic complications. Recent studies have demonstrated alterations in mandibular function, incidence of chronic pain, and alterations in the facial sensation [8–19]. As surgical technique and technology evolve, emphasis has been placed not only on treating the pathology, but also upon improving functional outcome, cosmetic results, and quality of life [1–7,20]. These new considerations require further refinements in surgical techniques. Many surgical modifications have been described to minimize the size of the PT [12,14] in an effort to decrease tissue trauma. However, many of these variations do not offer similar surgical exposure, nor do they improve operative results.

We have described a modification of the PT, termed the minipterional craniotomy (MPT). This approach provides similar transsylvian surgical exposure as conventional PT, as demonstrated by previous anatomical studies [1,4,5]. The MPT reduces the extent of dissection of the temporalis muscle and decreases the size of the craniotomy. The bone flap includes the lateral aspect of the sphenoid, part of the frontal bone inferior to the superior temporal line, and a minimal portion of the temporal bone [1,4,5]. This technique has increasingly gained neurosurgical acceptance worldwide. However, there is little clinical evidence of the benefits and the safety of this new technique. At the time of writing, few papers have been published describing the clinical application and results of the MPT generally or to treat specific pathology or anatomical targets [20,21]. Therefore, safety and effectiveness of the MPT craniotomy are still a matter of debate. In order to investigate aspects of clinical safety of the MPT and its surgical effectiveness, the authors present their clinical experience with more than 100 ruptured and unruptured anterior circulation aneurysms. To our knowledge, this is the largest series using the MPT technique for craniotomy published to date, and certainly for a specific pathology.

⇑ Corresponding author. Tel.: +55 11 3141 9550. E-mail address: [email protected] (E.G. Figueiredo). http://dx.doi.org/10.1016/j.jocn.2015.07.032 0967-5868/Ó 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032

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E.G. Figueiredo et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx

2. Materials and methods 2.1. Patients One hundred and two aneurysms were consecutively operated on at the Division of Neurological Surgery of the University of Sao Paulo and Estadual University of Ponta Grossa, Brazil, between August 2005 and July 2013. Surgical indication for the MPT technique included patients harboring non-giant ruptured and unruptured anterior circulation aneurysms. Patients presenting with hematomas with significant mass effect have been preferentially operated on using a conventional PT craniotomy and were not included in the analysis. Ruptured aneurysms were treated as soon as clinical conditions allowed. Ophthalmic artery (OphA) aneurysms were operated on by conventional PT, rather than MPT. Demographic data, including sex, age, Fisher grade, Hunt–Hess (HH) scale grade, and aneurysm location and size were analyzed. Intraoperative events, including aneurysm bleeding and need for converting MPT to traditional PT were evaluated. Postoperative angiogram was performed in all patients before discharge to evaluate the postsurgical state (clipping outcome) of the aneurysms. Clinical and surgical complications, including neurological deficits, intracranial hemorrhage, vasospasm, postoperative infection, cerebrospinal fluid (CSF) leakage, and hydrocephalus were assessed. Modified Rankin Scale (mRS) score at 6 months was used as the outcome index. Scores 0–1 were considered as excellent, 2–3 as good, and 4–5 as bad outcomes.

Fig. 2. Intraoperative photograph showing subperiosteal dissection of the temporalis muscle leaving a cushion of muscle to facilitate closure.

2.2. Surgical technique An arcuate scalp incision began 1 cm above the base of the zygomatic arch at the anterior border of the hairline. It was extended superiorly and curved gradually toward the ipsilateral midpupillary line (Fig. 1). The scalp opening was then reflected ventrally. As previously described, an interfascial dissection technique was carried out to avoid injury to the frontalis branch of the facial nerve [21]. The temporalis fascia was incised between the superior and inferior temporal lines, leaving behind a myofascial cuff for reapproximation at the end of the procedure (Fig. 2). The muscular flap was dissected subperiosteally and retracted caudally and posteriorly (Fig. 2). The muscle was retracted until the pterion had been exposed. These procedures limit the extension of dissection and retraction of the temporalis muscle. A burr hole was placed superior to the pterion, under the linea temporalis. The osteotomy proceeded inferior and ventrally along the superior temporal line, and as it reached the fronto-zygomatic suture, it curved sharply to the temporal bone. Next, the osteotomy was

Fig. 3. Intraoperative photograph showing osteotomies. The entire bone flap is located under the superior temporal line.

directed posterior and superiorly along the temporal and parietal bones to connect with the initial burr hole. Thus, the bone flap included the lateral aspect of the sphenoid, part of the frontal bone inferior to the superior temporal line, and a minimal portion of the temporal and parietal bones (Fig. 3). The sphenoid ridge was drilled away until its base was flattened. The medial limit of the drilling was the emergence of the meningo-orbital artery at the superior orbital fissure. Shaving the sphenoid ridge down to the depth of the superior orbital fissure permitted a more flattened trajectory to the circle of Willis. The dura was opened in a semilunar fashion with the base of the flap directed toward the base of the skull (Fig. 4). Next, the inferolateral aspect of the frontal lobe, Sylvian fissure, and superior temporal gyrus were exposed. The Sylvian fissure was visualized beyond the anterior ascendant ramus, which superficially corresponds to the pterion. A microsurgical dissection of the Sylvian fissure was performed as usual and the lesions were approached using conventional microsurgical techniques. Figure 5 illustrates the microsurgical view provided by the MPT approach. 3. Results

Fig. 1. Intraoperative photograph showing planned skin incision for stepwise surgical dissection using the minipterional craniotomy technique.

A total of 86 patients with 102 aneurysms were evaluated with 16 patients harboring two aneurysms. Ten patients had bilateral

Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032

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E.G. Figueiredo et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx

Table 1 Clinical presentation of 86 patients with anterior circulation aneurysms operated with the minipterional craniotomy Clinical presentation

Patients (n)

Ruptured aneurysm Unruptured aneurysm

37 49

Hunt–Hess grade 1 2 3 4

7 15 12 13

Fisher grade 1 2 3 4

4 9 12 12

Hydrocephalus Yes No

74 12

Fig. 4. Intraoperative photograph showing the bone flap has been removed to show the dura underneath. Table 2 Surgical timing after subarachnoid hemorrhage of 37 anterior circulation ruptured aneurysms operated with the minipterional craniotomy Surgical timing <5 days 6–10 days >10 days

Patients (n) 30 03 04

Table 3 Location of 102 anterior circulation aneurysms operated with the minipterional craniotomy Aneurym location

Fig. 5. Intraoperative microsurgical view showing the dura has been opened and the Sylvian fissure has been split.

MPT, therefore a total of 96 MPT were performed. Twenty patients (23.3%) were male and 66 (76.7%) female. Patient age ranged from 20 to 72 years (average 49.1 years). Thirty-seven patients (43%) presented with subarachnoid hemorrhage (SAH), while 49 (57%) patients had unruptured aneurysms (Table 1). HH and Fisher grades are depicted in Table 1. Twentyfour patients (64.8%) were classified as Fisher grade 3 and 4, and 13 categorized as Fisher grade 1 and 2 (35.1%). Seven patients (18.9%) presented in HH grade 1, 15 (40.5%) in HH grade 2, two (32.4%) in HH grade 3, and three (8.1%) patients in HH grade 4. Twelve patients (32.4%) required external ventricular drainage due to acute hydrocephalus (Table 1). Thirty patients (81%) with ruptured aneurysms were operated within the first 5 days after SAH. Four patients (10.8%) were treated between days 6–10 and three aneurysms (8.2%) were clipped after 15 days (Table 2). Aneurysm location is detailed in Table 3. Posterior communicating artery (PcomA) (n = 11, 29.7%) and middle cerebral artery (MCA) aneurysms (n = 11, 29.7%) were the most common locations in the ruptured group, while MCA aneurysms comprised 44.6% (n = 29) of the unruptured lesions (Fig. 6–9, Table 3). Two OphA ruptured aneurysms were mistakenly interpreted as PComA

Aneurysms (n)

Ruptured aneurysms PcomA ChA ICA bifurcation OphA AComA MCA

11 3 0 2 10 11

Unruptured aneurysms PcomA ChA ICA bifurcation OphA artery AComA MCA Total

20 5 3 0 8 29 102

AComA = anterior communicanting artery, ChA = anterior choroidal artery, ICA = internal carotid artery, MCA = middle cerebral artery, OphA = ophthalmic artery, PcomA = posterior communicating artery.

aneurysms from the preoperative angiogram. The anterior clinoid process was drilled uneventfully and these aneurysms were clipped without additional difficulty. Thirty-four aneurysms (33.3%) were 64 mm, 58 (56.8%) measured between 5–10 mm and 10 aneurysms (9.8%) were P10 mm (Fig. 8, Table 4). Clinical outcome is depicted in Table 5. Most patients had an excellent clinical result (77.9% mRS 0 or 1), seven patients exhibited good outcome (8.1% mRS 2). Twelve patients (13.9%) died, all with ruptured aneurysms, mainly due to vasospasm and other SAH clinical complications (Table 5). Intra- and post-operative complications are detailed in Table 6. Intraoperative aneurysm bleeding occurred in five patients (4.9%), while postoperative hemorrhage was observed in three patients (2.9%) without the need for surgical evacuation. CSF leak occurred in one patient who had a large frontal sinus with additional

Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032

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Fig. 6. Internal carotid angiogram, lateral view, depicting a large posterior communicating artery aneurysm.

Fig. 9. Postoperative axial CT scan showing the clipping of the complex aneurysm in Fig. 8 though the minipterional craniotomy. Table 4 Size of the 102 anterior circulation aneurysms operated with the minipterional craniotomy Aneurysm size 4 mm 5–9 mm >10 mm

Aneurysms (n) 34 58 10

Table 5 Clinical outcome of 86 patients with anterior circulation aneurysms operated with the minipterional craniotomy Clinical outcome Fig. 7. Intraoperative photograph showing microsurgical dissection has been performed and aneurysm seen in Fig. 6 has been clipped uneventfully.

Modified Rankin Scale 0 1 2 3 4 5 Deaths

Patients (n) 57 10 7 0 0 0 12

surgery necessary to successfully treat the leak. Infection did not occur in this patient. Six patients developed late hydrocephalus that required a ventriculoperitoneal shunt. Wound infection was observed in three patients and meningitis occurred concomitantly in one of these patients. Patients were treated with reoperation and antibiotics uneventfully. Postoperative angiogram was carried out in all patients. Aneurysmal remnants were observed in two MCA and in one PcomA aneurysm. Reoperation was required in one MCA aneurysm in order to reposition the clip. In the other two cases, remnants were interpreted as not clinically relevant, although the patients had annual follow-up angiograms.

4. Discussion Fig. 8. Axial CT angiography shows a large and multilobulated middle cerebral artery aneurysm.

Yasargil was primarily responsible for refining and popularizing PT [19,21–23] However, PT requires complete reflection of the

Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032

E.G. Figueiredo et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx Table 6 Postoperative and clinical complications of 102 anterior circulation aneurysms operated with the minipterional craniotomy Complications

Aneurysm (n)

Intraoperative bleeding Yes No

05 97

Intracranial hemorrhage Yes No

3 99

CSF leak Yes No

01 101

Clinical vasospasm Yes No

34 68

Radiological vasospasm Yes No

16 86

Postoperative hydrocephalus Yes No

06 96

Infection Yes No

03 99

CSF = cerebrospinal fluid.

temporal muscle and exposes often unnecessarily large, uninvolved areas of the brain parenchyma. Furthermore, adverse cosmetic and functional outcomes are relatively common, despite several modifications devised to prevent atrophy of the temporalis muscle [8–10,13,17,19,21,24]. As microsurgery technique advanced, new refinements were required [1,4,5]. Contemporary neurosurgery requires that tradition must be evaluated and challenged, especially to evaluate effectiveness and patient outcomes. New technologies and techniques, such as image guidance systems, endoscopes, endovascular procedures and advances in anesthesia have posed new challenges [3,5]. These advances, along with accurate knowledge of the surgical anatomy and early microsurgical training, have increased the level of confidence among many neurosurgeons who now routinely employ smaller surgical openings. In addition, laboratory anatomical studies have importantly contributed to surgical technique refinements [1,4,5] MPT was first described by Figueiredo et al. who demonstrated that anatomical and surgical exposure were similar to that provided by the conventional PT approach [1,4,5]. In the MPT technique the pterion is the landmark for determining the posterior and distal limits of the craniotomy. Exposure and dissection of only the segment proximal to the pterion optimize exposure of the transsylvian anatomy. Thus, the two main features of the standard PT technique — the extensive drilling of the lateral aspect of the sphenoid wing and the wide opening of the Sylvian fissure — are also possible in the MPT [1,4,5]. Therefore, anatomical surgical exposures are similar between the PT and MPT. The lateral supraorbital approach described by Hernesniemi et al. is another craniotomy proposed to operate on intracranial lesions located in the sellar and suprasellar regions, in the Sylvian fissure and in the retrosellar regions such as the superior part of the basilar artery and interpeduncular fossa. The short skin incision dos not reach the front of the ear like the incision when using the standard pterional approach [25]. According to Salma et al. from an anatomic point of view, when comparing pterional and lateral supraorbital approaches both provide similar exposure to the sellar, suprasellar, and anterior communicating artery areas. The pterional approach provides better exposure of the retrosellar area

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[26]. This difference was not observed in anatomical studies comparing pterional and minipterional craniotomies [1]. The MPT technique has gained acceptance worldwide. Many surgeons have used it with assumed excellent results, including us. However to our knowledge there are no large series in the literature to document its clinical outcomes and results. Therefore, its safety and effectiveness in treating anterior circulations aneurysms have not been verified until now. Series analysis, such as the 102 analyzed consecutive unruptured and rupture intracranial aneurysms treated by MPT craniotomy presented here are therefore essential to gauge efficacy. Our findings confirm the data from anatomical studies [1,4,5]. In this study, no surgical restrictions were observed. There was no need to enlarge the craniotomy in order to clip the aneurysms. When intraoperative bleeding occurred (4.9%), the aneurysm was secured without need for additional maneuvers. No permanent morbidity was noticed in this series, including the unruptured aneurysms. Aphasia was observed in one patient with one MCA aneurysm, but this was transient and the patient fully recovered after a few days. This series included both ruptured (43%) and unruptured aneurysms (57%). Most of the hemorrhages were classified as Fisher grade 3 or 4 (64.8%), although patients with Fisher grade 1 and 2 (35.2%) were also represented. Most of the patients who presented with ruptured aneurysms were categorized as HH grade 2 or 3. These data demonstrate that this series is representative of the general population with ruptured aneurysms. Additionally, the majority (81%) of the aneurysms were treated within the first 5 days after SAH. Only 8.2% of the lesions were treated after 15 days following bleeding. Morbidity due to SAH complications, such as vasospasm and hydrocephalus, were present in this analysis, reflecting the general SAH population. The International Subarachnoid Hemorrhage Trial has shown a rate of death or dependence of 23.9% [27], which is congruent with our own rate for ruptured aneurysms (25.5%). Furthermore, in the unruptured aneurysm group no death or dependence was found. Additionally, most of aneurysms were midsized (5–9 mm) comprising 56.8% of the cases. However, small (64 mm) and large (P10 mm) aneurysms were also present, at 33.3% and 9.8%, respectively. Even though OphA aneurysms (n = 2) were underrepresented in this study, which reflects our inclusion criteria, all other common locations for aneurysm occurrence in the anterior circulation were included in this series. We have deliberately avoided operating on OphA aneurysms using the MPT due to the theoretical risk of jeopardizing drilling of the anterior clinoid process with a smaller opening. However, our experience with these two cases demonstrated that the MPT may also be employed to treat non-giant paraclinoid aneurysms. Limitations or restrictions were not noted when treating PcomA, MCA, internal carotid artery bifurcation, anterior choroidal artery or anterior communicating artery aneurysms as well. Clinical results are reflected to a great degree in adequate surgical exposure. Excellent outcome was achieved in 77.9% of the patients, with good outcome results in 8.1% of the cohort. Twelve patients (13.9%) died due to clinical complications of SAH. No deaths were observed in the group of patients with unruptured aneurysms. These results may partially reflect the high percentage (57%) of unruptured lesions in this patient group. On the other hand, these data also positively reinforce the clinical safety of the MPT craniotomy. Patel et al. [28] found that in up to 34.8% of patients, opening of the frontal sinus occurs after PT, even though only a minority of patients will develop CSF leak. One case of CSF leak occurred in our series in a patient with a large frontal sinus. This event was easily treated and there was no postoperative infection.

Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032

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Postoperative angiograms showed aneurysmal remnants in two MCA and in one PcomA aneurysm, with only one MCA aneurysm requiring additional treatment. This data clearly demonstrates the effectiveness of this technique in completely obliterating aneurysms. Therefore, the MPT is a safe and effective alternative to the PT technique that can ensure complete occlusion of the aneurysm. Caplan et al. have recently, described their surgical experience with 82 unruptured anterior circulation aneurysms [20]. They conclude that MPT is a worthwhile alternative to the standard PT. No surgical or anatomical restrictions or suboptimal exposure were found when applying MPT in this group of patients. Our experience differs from that of Caplan and co-authors in many aspects [20,21]. First, we have employed the MPT approach to operate on both ruptured and unruptured anterior circulation aneurysms. Second, we have also successfully operated on anterior communicating artery aneurysms. Third, we have not operated on carotid OphA aneurysms due to the theoretical risk of jeopardizing the drilling of the anterior clinoid process when using a smaller opening. Nonetheless, two cases of carotid artery ophthalmic aneurysms, interpreted as PcomA aneurysms from the preoperative angiogram, were operated on without additional difficulty. Fourth, we have performed postoperative angiograms in all patients to document complete obliteration of the aneurysmal sac. The complete occlusion of the lesion was not documented in Caplan’s paper [20,21]. This data is mandatory to demonstrate the effectiveness of the MPT technique. The cosmetic benefits of MPT over the classical PT have been documented in a prospective and randomized study (unpublished data) and were not included in this analysis. Advantages of the MPT craniotomy include less extensive dissection of the temporalis muscle, shorter operation time and shorter hospital stay. Certainly the anatomic data from laboratory studies supports such studies [1–7]. The potential psychological benefits of a smaller area of scalp and muscle incision, craniotomy, and less visible scar were not objectively evaluated, however these were relevant concerns of patients.

5. Conclusion MPT technique optimizes a balance between effective microsurgical exposure and the size of craniotomy. It provides adequate surgical exposure and excellent outcomes for both ruptured and unruptured anterior circulation aneurysm clipping. It ensures complete obliteration of the aneurysm sac with satisfactory, if not excellent, outcomes in morbidity and mortality. It constitutes a safe and effective alternative to the classical PT approach, with potentially better functional and esthetic outcomes.

Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.

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Please cite this article in press as: Figueiredo EG et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.07.032