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Modified “Extended” Suboccipital Subtonsillar Clipping of a Ruptured Proximal Pica Aneurysm: Technical Note with Relevant Anatomical Demonstration
Case Report
Modified “Extended” Suboccipital Subtonsillar Clipping of a Ruptured Proximal Pica Aneurysm: Technical Note with Relevant Anatomical Demonstration Alberto Di Somma1, Palomares Cancela Caro2, Magdalena Olivares Blanco2, Teresa Somma1, Antonio Lo´pez-Gonza´lez2, Alvaro Campero3, Juan Emmerich4, Javier Ma´rquez-Rivas2
Key words Cranial base surgery - PICA aneurysms - Proximal PICA aneurysms - Suboccipital subtonsillar - Vascular control - Vascular surgery -
Abbreviations and Acronyms CT: Computed tomography PICA: Posterior inferior cerebellar artery VA: Vertebral artery From the 1Division of Neurosurgery, School of Medicine, Università degli Studi di Napoli “Federico II,” Naples, Italy; 2 Department of Neurosurgery, Hospital Universitario Virgen del Rocío, Sevilla, Spain; 3Department of Neurological Surgery, Hospital Padilla, Tucumán, Argentina; and 4School of Medicine, National University of La Plata, La Plata, Argentina To whom correspondence should be addressed: Alberto Di Somma, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 117:301-308. https://doi.org/10.1016/j.wneu.2018.06.019 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
INTRODUCTION Aneurysms of the posterior inferior cerebellar artery (PICA) are rare.1-3 Surgery is challenging because of the deep location and intimate relation of the PICA with the medulla and lower cranial nerves. The development and implementation of endovascular therapy have led to a less-invasive approach to cerebrovascular disease, and indications for surgery have been progressively confined.4-6 Although endovascular treatment of intracranial aneurysms is used increasingly as an alternative to surgery, specific results related to the management of PICA aneurysms with these techniques are not well established, especially if the clinical presentation is a ruptured aneurysm.7,8 Different approaches can be used to treat these lesions surgically depending on their anatomic location and morphology, with the paramedian suboccipital craniotomy
- BACKGROUND
AND IMPORTANCE: Lesions located lateral to the lower brainstem, such as proximal posterior inferior cerebellar artery (PICA) aneurysms, are surgically challenging. We report a case of a patient with a left proximal PICA aneurysm that was successfully clipped via a so-called “extended” suboccipital subtonsillar approach, which allowed us to obtain proper vascular control without removal of the atlas. The anatomy relevant for this approach has been studied.
- METHODS:
Three adult cadaveric heads were studied. The relevant neurovascular anatomy related to this approach was exposed. Hence, this technique was applied on the patient herewith reported.
- CASE
PRESENTATION: A 60-year-old man with sudden onset of severe headache, nausea, and vomiting was admitted to our hospital. Computed tomography of the brain showed diffuse subarachnoid hemorrhage, mainly distributed at the level of the perimesencephalic cisterns. Cerebral angiography revealed a 3-mm aneurysm arising at the origin of the left PICA. The aneurysm was considered unsuitable for coil embolization, so it was treated via a “modified” posterolateral suboccipital subtonsillar route. The modification consisted of accomplishing proper proximal vascular control at the extracranial segment of the vertebral artery (V3), without the need of further removal of the posterior portion of the atlas. The patient was discharged neurologically intact.
- CONCLUSIONS:
The technique we suggested allowed no unnecessary removal of bone, with no need to drill the occipital condyle or remove the atlas, offered proper proximal vascular control in the early stage of the surgical procedure, and limited the quantity of temporary vascular clips inside the intracranial surgical field.
the most common approach used.3,9,10 In such cases, proximal control of the vertebral artery (VA) generally is reached directly in the intradural space or by removing the posterior portion of the atlas and/or drilling the occipital condyle, thus localizing the VA in its extracranial course.11,12 However, both surgical maneuvers have some surgical drawbacks. If on one hand removal of the posterior portion of the atlas and/or drilling the occipital condyle may add some risks of bleeding, unnecessary bone removal, and prolonged surgical time, on the other hand localizing the VA directly in its intradural course, and using temporal clipping accordingly, could reduce the intradural surgical field space.
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In this paper, we report a case of ruptured proximal PICA aneurysm that was treated via a modified “extended” posterolateral suboccipital subtonsillar approach. The modification consisted in the exposure of the extracranial segment of the VA without the need of further bone removal. This technique allowed an appropriate proximal vascular control in the early stage of the surgical procedure without narrowing the surgical field with multiple vascular clips (intradurally) or removing further bone. Moreover, in order to highlight the main anatomic structures related to the proposed approach, a dedicated cadaveric demonstration was performed.
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Figure 1. (A) Posterior view of the cerebellum and craniovertebral junction. Dotted green lines indicate the site of proximal vascular control that can be achieved at the level of V3 segment of the vertebral artery. The blue arrow shows the surgical pathway along the posterior inferior cerebellar artery that should be followed backwards, i.e., starting from the tonsillomedullary segment, to reach the origin of the PICA (blue circle [B]). (B) The tonsil has
METHODS Three adult cadaveric heads, fixed with formaldehyde and injected with colored silicone, were studied. Extensive exposure of the posterior fossa anatomy was performed to provide some key aspects that are relevant when performing the modified “extended” suboccipital subtonsillar approach.
Relevant Intracranial Anatomy of the Modified “Extended” Suboccipital Subtonsillar Approach The anatomy of the posterior fossa is detailed widely in the pertinent literature.13-15 Focusing on the relevant anatomy for the surgical approach herewith presented, we will discuss details of some portions of the VA and the PICA (Figure 1).
Figure 2. Relevant anatomic relationships of the intracranial vertebral artery (V4) with the surrounding neurovascular structures, anterior (A) and posterior (B) view. Once inside the dura mater, the V4 ascends from the lower lateral to the upper anterior surface of the medulla and joins its mate of the opposite side near the pontomedullary junction to form the basilar
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been retracted superolaterally to expose the surface of the medulla as well as the origin of the PICA and its anteromedullary segment. Suboccipit., suboccipital; Bivent., biventricul; Lat., laterally; Med., medullary; Seg., segment; Vert. A., vertebral artery; Cer., cervical; CN XI, accessory cranial nerve; C1 and C2, first 2 cervical nerve roots; Cor., cortical; CN XII, hypoglossal nerve. Ant., anterior.
The VA (one per side) is schematically divided into 4 segments, from its origin from the subclavian artery (V1) to the intradural join with the contralateral VA (V4).16 The third segment (V3) is intimately related to the foramen magnum and craniovertebral junction and, together with the intracranial VA, is extremely relevant during this modified route. It extends
artery. The artery ascends anterior to the cranial nerves IX to XII. CN XII, hypoglossal nerve; P.I.C.A., posterior inferior cerebellar artery; Vert. A., vertebral artery; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XI, accessory nerve. (Adapted from Campero et al.16)
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Figure 3. (A) Preoperative computed tomography (CT) scan showing posterior fossa subarachnoid hemorrhage. (B) Angio-CT evaluation revealed a small aneurysm coming from the anterior medullary segment of the left posterior cerebellar artery. (C) Cerebral digital subtraction angiography,
from the foramen in the transverse process of the atlas to the site of passage through the dura mater. The V3 is divided in 3 portions: a vertical portion that ascends through the transverse processes of C1, a horizontal portion that courses in the groove on the upper surface of the posterior arch of the atlas, and an oblique portion that penetrates the dura mater. In the modified “extended” suboccipital subtonsillar approach, the proximal control can be achieved in between the horizontal and oblique portions in the initial stage of the surgical procedure. Subsequently, the VA enters the dura lateral to the cervicomedullary junction (V4), courses superior, anterior, and medial to reach the front of the medulla, and joins its mate from the opposite side to form the basilar artery.
performed 2 weeks after bleeding, confirmed the presence of the left PICA aneurysm. (DeF) Three-dimensional reconstructions in different perspectives showing the vascular anatomy of the proximal left PICA aneurysm. White arrow, aneurysm.
The PICA (one per side) is the largest branch of the VA and it generally arises at any point along the intradural course of the VA. However, it has to be stressed that an extracranialeextradural origin from the VA has been described in the main literature.17 In such cases, the PICA arises from the third segment of the VA, about 1 cm proximal to the place at which the VA enters the dura and does not send extradural branches; it progresses parallel to the VA and the first cervical nerve and subsequently pierces the dura. Intradurally, the PICA remains lateral and posterior to the brainstem, without sending branches to the anterior brainstem. The PICA is divided into 5 segments: 1) anterior medullary, 2) lateral medullary, 3) tonsillomedullary 4) telovelotonsillar, and 5) cortical segments. The relevant anatomy for
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this modified extended subtonsillar approach involves mainly the first 3 segments of the PICA. The anterior medullary portion lies anterior to the medulla. It begins at the origin of the PICA anterior to the medulla and extends backward to the hypoglossal rootlets to the level of a rostrocaudal line through the most prominent part of the inferior olive that marks the boundary between the anterior and lateral surfaces of the medulla. This is the segment that was affected by the aneurysm in this case. The lateral medullary segment begins where the artery passes the most prominent point of the olive and ends at the level of the origin of the glossopharyngeal, vagus, and accessory rootlets. The tonsillomedullary portion begins where the PICA passes posterior to the glossopharyngeal, vagus, and accessory nerves and
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Figure 4. (A and B) Postoperative computed tomography evaluation showing no surgical-related complications. (C and D) Three-dimensional reconstructions of the paramedian suboccipital subtonsillar approach have
extends medially across the posterior aspect of the medulla near the caudal half of the tonsil. For the main interest of the surgical variation herewith proposed, some details
of the hypoglossal nerve should be reviewed. The hypoglossal nerve result from as a series of rootlets that exits the brainstem along the anterior margin of the caudal two-thirds of the olive in the
Figure 5. (A) Left paramedian suboccipital subtonsillar exposure of the extracranial vertebral artery in the suboccipital triangle. (B). Temporary clip can be applied without narrowing the intracranial surgical space. VA,
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been provided. (E) Postoperative cerebral digital subtraction angiography confirmed complete occlusion of the aneurysm, with patency of the surrounding arteries.
preolivary sulcus. The hypoglossal rootlets, in their course from the preolivary sulcus to the hypoglossal canal, pass often posterior to the VA. The relation of the origin and proximal part of the PICA to the
vertebral artery, V3; Atlas, posterior portion of C1; Fdm, dura mater of the foramen magnum; PFdm, posterior fossa dura mater.
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Figure 6. (A) Intraoperative pictures showing the subtonsillar route to the anterior medullary segment of the left posterior cerebellar artery. Identification of the tonsillomedullary segment of both posterior inferior cerebellar arteries (PICAs). Asterisks indicate the tonsillomedullary segment of the posterior inferior cerebellar artery. (B). Dissection of the left PICA thus reaching its lateral medullary segment, being in close relationship with lower cranial nerve roots. Double
hypoglossal rootlets differs significantly. The PICA arises either rostral or caudal or at the level of the hypoglossal rootlets. The initial segment of the PICA has a variable course in relation to the hypoglossal rootlets. The most common course is for the PICA to arise from the VA and pass directly posteriorly around or between the hypoglossal rootlets (Figure 2).18,19 CASE REPORT A 60-year-old man with hypertension, previous ischemic heart disease, and hepatitis B viruserelated cirrhosis was admitted to our emergency department (Hospital Virgen del Rocio, Sevilla, Spain) after a mild head trauma. A computed tomography (CT) scan of the brain
asterisk indicates the lateral medullary segment of the left posterior inferior cerebellar artery. (C) Exposure of the aneurysm arising from the anterior medullary segment of the left PICA. Plus sign indicates the anterior medullary segment of the left posterior inferior cerebellar artery. (D) Clipping of the aneurysm with patency of the surrounding vessels. Med, medulla; Tonsil, left cerebellar tonsil; An, aneurysm.
revealed subarachnoid blood, predominantly in the perimesencephalic cisterns. Accordingly, we decided to hospitalize the patient in the Division of Neurosurgery for further diagnostic tests. Findings of the neurologic examination were normal, with a Glasgow Coma Scale score of 15/15 points. To rule out the presence of a cerebral aneurysm, an angio-CT scan was performed the day of the admission that demonstrated an uncertain image located at the level of the proximal left posterior inferior cerebellar artery aneurysm. Further neuroradiologic investigation was performed by means of a cerebral digital subtraction angiography that showed the presence of a possible aneurysm located at the level of the anteromedullary segment of the left posterior inferior cerebellar artery
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but difficult to comprehensively characterize and to confirm with certainty, due to the recent bleeding. Accordingly, because of the excellent clinical condition, it was decided to repeat the angiography 14 days later. The subsequent cerebral angiography clearly showed the presence of a 3-mm left PICA aneurysm arising from its most proximal segment, i.e., the anteromedullary segment (Figure 3). A standard endovascular treatment or even a stent-assisted coiling were excluded by the interventional radiologists due to the high risk of PICA occlusion with such peculiar aneurysm location and projection. After careful consideration of many factors, including patient age, general clinical conditions, and aneurysm size, it was decided to treat the aneurysm by using a
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Figure 7. (A) Panoramic view of the surgical field after aneurysm clipping. (B) Closure technique used for this case with synthetic sutureable dura mater (C) covered by another layer of no sutured dural substitute. (D) A
left paramedian suboccipital subtonsillar approach 3 weeks after the patient’s admittance. A postoperative arteriogram showed proper placement of the clip, obliteration of the aneurysm, and the patency of the VA and PICA. Neither postoperative infection nor cerebrospinal fluid leak was detected. The postoperative course was characterized by slight and temporary dysphagia. A postoperative CT scan demonstrated the resolution of the subarachnoid hemorrhage without any other neurosurgical complications, and the patient was discharged 10 days after surgery (Figure 4). Surgical Technique The patient was placed in the prone position and the head, flexed downwards 10 e15 , and was stabilized by means of a
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titanium mesh has been placed to cover the skull base defect and the dead space has been filled with fibrin glue. Med, medulla; Tonsil, cerebellar tonsil; PFdm, dura mater of the posterior fossa.
3-points MayfieldeKees skeletal fixation headrest. A slightly curved vertical incision 4 cm behind the left mastoid bone and extending from the superior nuchal line down to the level of C-4 was performed. Muscles were detached and retracted up to the exposure of the occipital bone. A paramedian left suboccipital craniotomy was extended from the midline medially to the sigmoidal sinus laterally, including the foramen magnum. The left condyle was exposed. The transverse process of the atlas was palpated and exposed approximately 1 cm below the tip of the mastoid and through the suboccipital triangle, which is formed medially by the rectus capitis posterior major muscle, superolaterally by the superior oblique, and inferolaterally by the inferior oblique muscle. It is in this triangle where the
horizontal segment of the third portion of the extracranial VA (V3) usually runs, within a groove on the lamina of the atlas. After the suboccipital triangle was revealed, the complex venous compartment around V3 (the suboccipital cavernous sinus) was visualized. The V3 was then exposed extradurally, under full visualization, so a temporary clip could be applied when it was needed (Figure 5). After obtaining proper exposure of the V3 segment of the VA, we opened the dura mater and cerebrospinal fluid was drained from the cisterna magna to relax the brain. Afterwards, the left PICA was followed backwards, i.e., from the tonsillomedullary segment to the anteromedullary one, by elevating the homolateral cerebellar tonsil. Accordingly, following the PICA in the
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CASE REPORT ALBERTO DI SOMMA ET AL.
subtonsillar corridor, we recognized a lateral projecting aneurysm proximal to the origin of the PICA. Thereafter, the arachnoid membrane was sharply dissected to expose the aneurysm sac and a curved titanium aneurysm clip was placed (Figure 6). At the end of the procedure, normal blood flow in the left PICA and VA was checked by the use of the micro-Doppler ultrasound probe. The closure technique used for this case included synthetic suturable dura mater covered by a layer of no suturable dural substitute; a titanium mesh was placed to cover the skull base defect, and the dead space was filled with Fibrin glue (Figure 7). DISCUSSION The PICA has the most complex and variable course among all arteries of the posterior circulation. Hence, proximal PICA aneurysms could be considered as are a unique subset of posterior circulation aneurysm, representing from 0.5% to 3% of all intracranial aneurysms.20 Surgery for such vascular diseases may disclose particular problems due to deep aneurysm location and its intimate relationship with the lower brainstem and lower cranial nerves. The complexities involved in the surgical approach to the PICA aneurysms relate to the narrow corridor limited by the brainstem, petrous occipital bones, and multiple neurovascular structures occupying the cerebellomedullary and cerebellopontine cisterns.21 In many centers, proximal PICA aneurysms commonly are treated with a far-lateral suboccipital craniotomy and surgical clipping of the aneurysm. More extensive skull base approaches such as the lateral suboccipital, transcondylar, extremelateral transcondylar, far-lateral, and transpharyngeal-transclival have been described as well.9,22-24 In contrast, endovascular management increasingly is used as an alternative to surgery but specific endovascular outcomes of PICA aneurysms are not well established. The surgical option tends to reveal unique difficulties because of complex neurovascular anatomy and its close relationship with the lower brainstem and lower cranial nerves. For many years, controversy has raged over the advantages and disadvantages of the various surgical routes
MODIFIED SUBOCCIPITAL APPROACH FOR PICA ANEURYSM
to approach such lesions depending on their anatomic location and morphology. Together with the selection of the proper surgical route, management of proximal PICA aneurysms requires appropriate vascular control, as with any neurovascular procedure. In particular, the proximal vascular control can be achieved via identification of the VA through the dentate ligament, intracranially, or by means of removing the posterior portion of the atlas thus allowing extracranial control of the VA. However, both surgical maneuvers have some surgical drawbacks. As a matter of fact, if on one hand removal of the posterior portion of the atlas may add some risks of bleeding, unnecessary bone removal, and prolonged surgical time, on the other hand when localizing the VA directly in the intracranial space its vascular control by means of vascular clips may tighten the surgical space (the intradural surgical space). Given such a background, with this brief technical report we intended to share a modified posterolateral paramedian suboccipital subtonsillar approach with the aim of refining the vascular control over the VA via a suboccipital subtonsillar approach. The modification consisted of accomplishing proper proximal vascular control at the level of the extracranial segment of the VA without the need of further removal of the posterior portion of the atlas. The advantages of such technical adjunct can be summarized as follow: 1) localization and dissection of the extracranial VA before opening the dura, thus allowing for an early proximal vascular control in the V3 segment of the VA; 2) no need for removal of the posterior portion of the atlas and/or occipital condyle drilling, thus avoiding wasting surgical time and/or venous bone bleeding; 3) avoid narrowing the surgical space with temporary clip applied on the intracranial VA; and 4) the possibility of contralateral clipping of the intracranial VA, without narrowing the surgical space. In the present article, we have intended to afford an additional technical aspect to the surgeon’s armamentarium related to the difficult management of proximal PICA aneurysms. Relevant anatomical demonstration has been provided as well. However, it has to be stressed that a multimodality approach tailored to the specific aneurysm in the specific patient currently still stands as the better approach for such kind of pathologies.
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CONCLUSIONS This modified approach allowed for avoiding unnecessary cervical spine bone removal, i.e., no need to drill the occipital condyle or remove the atlas, offered proper proximal vascular control in the early stage of the surgical procedure, and limited the quantity of temporary vascular clips in the intracranial surgical field, thus preventing possible instruments crowding in a relatively narrow space. The relevant anatomy pertinent to this case has been illustrated and discussed. With this contribution, we aimed to report some specific technical issues regarding the difficult surgical management of proximal posterior inferior cerebellar artery aneurysms. REFERENCES 1. Foster MT, Herwadkar A, Patel HC. Posterior inferior cerebellar artery/vertebral artery subarachnoid hemorrhage: a comparison of saccular vs dissecting aneurysms. Neurosurgery. 2018;82: 93-98. 2. Lehto H, Kivisaari R, Niemelä M, Dashti R, Elsharkawy A, Harati A, et al. Seventy aneurysms of the posterior inferior cerebellar artery: anatomical features and value of computed tomography angiography in microneurosurgery. World Neurosurg. 2014;82:1106-1112. 3. Viswanathan GC, Menon G, Nair S, Abraham M. Posterior inferior cerebellar artery aneurysms: operative strategies based on a surgical series of 27 patients. Turk Neurosurg. 2014;24:30-37. 4. Awad AJ, Mascitelli JR, Haroun RR, De Leacy RA, Fifi JT, Mocco J. Endovascular management of fusiform aneurysms in the posterior circulation: the era of flow diversion. Neurosurg Focus. 2017;42: E14. 5. Srinivasan VM, Ghali MGZ, Reznik OE, Cherian J, Mokin M, Dumont TM, et al. Flow diversion for the treatment of posterior inferior cerebellar artery aneurysms: a novel classification and strategies. J Neurointerv Surg. 2018;10:663-668. 6. Xu F, Hong Y, Zheng Y, Xu Q, Leng B. Endovascular treatment of posterior inferior cerebellar artery aneurysms: a 7-year single-center experience. J Neurointerv Surg. 2017;9:45-51. 7. Korja M, Kivisaari R, Rezai Jahromi B, Lehto H. Size and location of ruptured intracranial aneurysms: consecutive series of 1993 hospitaladmitted patients. J Neurosurg. 2017;127:748-753. 8. Song J, Park JE, Chung J, Lim YC, Shin YS. Treatment strategies of ruptured posterior inferior cerebellar artery aneurysm according to its segment. Surg Neurol Int. 2017;8:155. 9. Bertalanffy H, Sure U, Petermeyer M, Becker R, Gilsbach JM. Management of aneurysms of the vertebral artery-posterior inferior cerebellar artery
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complex. Neurol Med Chir (Tokyo). 1998;38(suppl): 93-103.
supracondylar, and paracondylar extensions of the far-lateral approach. J Neurosurg. 1997;87:555-585.
and posterior inferior cerebellar arteries. Neurosurg Focus. 2005;19:E4.
10. Hudgins RJ, Day AL, Quisling RG, Rhoton AL, Sypert GW, Garcia-Bengochea F. Aneurysms of the posterior inferior cerebellar artery. A clinical and anatomical analysis. J Neurosurg. 1983;58: 381-387.
16. Campero A, Rubino P, Rothon A. Anatomy of the vertebral artery. In: George B, Bruneau M, Spetzler RF, eds. Pathology and Surgery Around the Vertebral Artery. Paris: Springer-Verlag Paris; 2011: 29-40.
22. Nanda A, Konar S, Bir SC, Maiti TK, Ambekar S. Modified far lateral approach for posterior circulation aneurysms: an institutional experience. World Neurosurg. 2016;94:398-407.
11. Tayebi Meybodi A, Lawton MT, Feng X, Benet A. Posterior inferior cerebellar artery reimplantation: buffer lengths, perforator anatomy, and technical limitations. J Neurosurg. 2016;125:909-914.
17. Fine AD, Cardoso A, Rhoton AL. Microsurgical anatomy of the extracranial-extradural origin of the posterior inferior cerebellar artery. J Neurosurg. 1999;91:645-652.
12. Rodríguez-Hernández A, Lawton MT. Anatomical triangles defining surgical routes to posterior inferior cerebellar artery aneurysms. J Neurosurg. 2011;114:1088-1094.
18. Matsushima K, Matsuo S, Komune N, Kohno M, Lister JR. Variations of occipital artery-posterior inferior cerebellar artery bypass: anatomic consideration. Oper Neurosurg (Hagerstown). 2018;14: 563-571.
13. Kawashima M, Rhoton AL, Tanriover N, Ulm AJ, Yasuda A, Fujii K. Microsurgical anatomy of cerebral revascularization. Part II: posterior circulation. J Neurosurg. 2005;102:132-147.
19. Matsushima K, Yagmurlu K, Kohno M, Rhoton AL. Anatomy and approaches along the cerebellar-brainstem fissures. J Neurosurg. 2016; 124:248-263.
14. Matsushima T, Natori Y, Katsuta T, Ikezaki K, Fukui M, Rhoton AL. Microsurgical anatomy for lateral approaches to the foramen magnum with special reference to transcondylar fossa (supracondylar transjugular tubercle) approach. Skull Base Surg. 1998;8:119-125.
20. Salcman M, Rigamonti D, Numaguchi Y, Sadato N. Aneurysms of the posterior inferior cerebellar artery-vertebral artery complex: variations on a theme. Neurosurgery. 1990;27:12-20 [discussion: 20-21].
15. Wen HT, Rhoton AL, Katsuta T, de Oliveira E. Microsurgical anatomy of the transcondylar,
21. Krayenbuhl N, Guerrero C, Krisht AF. Technical strategies to approach aneurysms of the vertebral
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23. Shi X, Qian H, Singh KC, Zhang Y, Zhou Z, Sun Y, et al. Surgical management of vertebral and basilar artery aneurysms: a single center experience in 41 patients. Acta Neurochir (Wien). 2013;155:1087-1093. 24. Rohde V, Schaller C, Hassler W. The extreme lateral transcondylar approach to aneurysms of the vertebrobasilar junction, the vertebral artery, and the posterior inferior cerebellar artery. Skull Base Surg. 1994;4:177-180.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 31 May 2018; accepted 2 June 2018 Citation: World Neurosurg. (2018) 117:301-308. https://doi.org/10.1016/j.wneu.2018.06.019 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.06.019
Modified “Extended” Suboccipital Subtonsillar Clipping of a Ruptured Proximal Pica Aneurysm: Technical Note with Relevant Anatomical Demonstration Alberto Di Somma1, Palomares Cancela Caro2, Magdalena Olivares Blanco2, Teresa Somma1, Antonio Lo´pez-Gonza´lez2, Alvaro Campero3, Juan Emmerich4, Javier Ma´rquez-Rivas2
Key words Cranial base surgery - PICA aneurysms - Proximal PICA aneurysms - Suboccipital subtonsillar - Vascular control - Vascular surgery -
Abbreviations and Acronyms CT: Computed tomography PICA: Posterior inferior cerebellar artery VA: Vertebral artery From the 1Division of Neurosurgery, School of Medicine, Università degli Studi di Napoli “Federico II,” Naples, Italy; 2 Department of Neurosurgery, Hospital Universitario Virgen del Rocío, Sevilla, Spain; 3Department of Neurological Surgery, Hospital Padilla, Tucumán, Argentina; and 4School of Medicine, National University of La Plata, La Plata, Argentina To whom correspondence should be addressed: Alberto Di Somma, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 117:301-308. https://doi.org/10.1016/j.wneu.2018.06.019 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
INTRODUCTION Aneurysms of the posterior inferior cerebellar artery (PICA) are rare.1-3 Surgery is challenging because of the deep location and intimate relation of the PICA with the medulla and lower cranial nerves. The development and implementation of endovascular therapy have led to a less-invasive approach to cerebrovascular disease, and indications for surgery have been progressively confined.4-6 Although endovascular treatment of intracranial aneurysms is used increasingly as an alternative to surgery, specific results related to the management of PICA aneurysms with these techniques are not well established, especially if the clinical presentation is a ruptured aneurysm.7,8 Different approaches can be used to treat these lesions surgically depending on their anatomic location and morphology, with the paramedian suboccipital craniotomy
- BACKGROUND
AND IMPORTANCE: Lesions located lateral to the lower brainstem, such as proximal posterior inferior cerebellar artery (PICA) aneurysms, are surgically challenging. We report a case of a patient with a left proximal PICA aneurysm that was successfully clipped via a so-called “extended” suboccipital subtonsillar approach, which allowed us to obtain proper vascular control without removal of the atlas. The anatomy relevant for this approach has been studied.
- METHODS:
Three adult cadaveric heads were studied. The relevant neurovascular anatomy related to this approach was exposed. Hence, this technique was applied on the patient herewith reported.
- CASE
PRESENTATION: A 60-year-old man with sudden onset of severe headache, nausea, and vomiting was admitted to our hospital. Computed tomography of the brain showed diffuse subarachnoid hemorrhage, mainly distributed at the level of the perimesencephalic cisterns. Cerebral angiography revealed a 3-mm aneurysm arising at the origin of the left PICA. The aneurysm was considered unsuitable for coil embolization, so it was treated via a “modified” posterolateral suboccipital subtonsillar route. The modification consisted of accomplishing proper proximal vascular control at the extracranial segment of the vertebral artery (V3), without the need of further removal of the posterior portion of the atlas. The patient was discharged neurologically intact.
- CONCLUSIONS:
The technique we suggested allowed no unnecessary removal of bone, with no need to drill the occipital condyle or remove the atlas, offered proper proximal vascular control in the early stage of the surgical procedure, and limited the quantity of temporary vascular clips inside the intracranial surgical field.
the most common approach used.3,9,10 In such cases, proximal control of the vertebral artery (VA) generally is reached directly in the intradural space or by removing the posterior portion of the atlas and/or drilling the occipital condyle, thus localizing the VA in its extracranial course.11,12 However, both surgical maneuvers have some surgical drawbacks. If on one hand removal of the posterior portion of the atlas and/or drilling the occipital condyle may add some risks of bleeding, unnecessary bone removal, and prolonged surgical time, on the other hand localizing the VA directly in its intradural course, and using temporal clipping accordingly, could reduce the intradural surgical field space.
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In this paper, we report a case of ruptured proximal PICA aneurysm that was treated via a modified “extended” posterolateral suboccipital subtonsillar approach. The modification consisted in the exposure of the extracranial segment of the VA without the need of further bone removal. This technique allowed an appropriate proximal vascular control in the early stage of the surgical procedure without narrowing the surgical field with multiple vascular clips (intradurally) or removing further bone. Moreover, in order to highlight the main anatomic structures related to the proposed approach, a dedicated cadaveric demonstration was performed.
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Figure 1. (A) Posterior view of the cerebellum and craniovertebral junction. Dotted green lines indicate the site of proximal vascular control that can be achieved at the level of V3 segment of the vertebral artery. The blue arrow shows the surgical pathway along the posterior inferior cerebellar artery that should be followed backwards, i.e., starting from the tonsillomedullary segment, to reach the origin of the PICA (blue circle [B]). (B) The tonsil has
METHODS Three adult cadaveric heads, fixed with formaldehyde and injected with colored silicone, were studied. Extensive exposure of the posterior fossa anatomy was performed to provide some key aspects that are relevant when performing the modified “extended” suboccipital subtonsillar approach.
Relevant Intracranial Anatomy of the Modified “Extended” Suboccipital Subtonsillar Approach The anatomy of the posterior fossa is detailed widely in the pertinent literature.13-15 Focusing on the relevant anatomy for the surgical approach herewith presented, we will discuss details of some portions of the VA and the PICA (Figure 1).
Figure 2. Relevant anatomic relationships of the intracranial vertebral artery (V4) with the surrounding neurovascular structures, anterior (A) and posterior (B) view. Once inside the dura mater, the V4 ascends from the lower lateral to the upper anterior surface of the medulla and joins its mate of the opposite side near the pontomedullary junction to form the basilar
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been retracted superolaterally to expose the surface of the medulla as well as the origin of the PICA and its anteromedullary segment. Suboccipit., suboccipital; Bivent., biventricul; Lat., laterally; Med., medullary; Seg., segment; Vert. A., vertebral artery; Cer., cervical; CN XI, accessory cranial nerve; C1 and C2, first 2 cervical nerve roots; Cor., cortical; CN XII, hypoglossal nerve. Ant., anterior.
The VA (one per side) is schematically divided into 4 segments, from its origin from the subclavian artery (V1) to the intradural join with the contralateral VA (V4).16 The third segment (V3) is intimately related to the foramen magnum and craniovertebral junction and, together with the intracranial VA, is extremely relevant during this modified route. It extends
artery. The artery ascends anterior to the cranial nerves IX to XII. CN XII, hypoglossal nerve; P.I.C.A., posterior inferior cerebellar artery; Vert. A., vertebral artery; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XI, accessory nerve. (Adapted from Campero et al.16)
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Figure 3. (A) Preoperative computed tomography (CT) scan showing posterior fossa subarachnoid hemorrhage. (B) Angio-CT evaluation revealed a small aneurysm coming from the anterior medullary segment of the left posterior cerebellar artery. (C) Cerebral digital subtraction angiography,
from the foramen in the transverse process of the atlas to the site of passage through the dura mater. The V3 is divided in 3 portions: a vertical portion that ascends through the transverse processes of C1, a horizontal portion that courses in the groove on the upper surface of the posterior arch of the atlas, and an oblique portion that penetrates the dura mater. In the modified “extended” suboccipital subtonsillar approach, the proximal control can be achieved in between the horizontal and oblique portions in the initial stage of the surgical procedure. Subsequently, the VA enters the dura lateral to the cervicomedullary junction (V4), courses superior, anterior, and medial to reach the front of the medulla, and joins its mate from the opposite side to form the basilar artery.
performed 2 weeks after bleeding, confirmed the presence of the left PICA aneurysm. (DeF) Three-dimensional reconstructions in different perspectives showing the vascular anatomy of the proximal left PICA aneurysm. White arrow, aneurysm.
The PICA (one per side) is the largest branch of the VA and it generally arises at any point along the intradural course of the VA. However, it has to be stressed that an extracranialeextradural origin from the VA has been described in the main literature.17 In such cases, the PICA arises from the third segment of the VA, about 1 cm proximal to the place at which the VA enters the dura and does not send extradural branches; it progresses parallel to the VA and the first cervical nerve and subsequently pierces the dura. Intradurally, the PICA remains lateral and posterior to the brainstem, without sending branches to the anterior brainstem. The PICA is divided into 5 segments: 1) anterior medullary, 2) lateral medullary, 3) tonsillomedullary 4) telovelotonsillar, and 5) cortical segments. The relevant anatomy for
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this modified extended subtonsillar approach involves mainly the first 3 segments of the PICA. The anterior medullary portion lies anterior to the medulla. It begins at the origin of the PICA anterior to the medulla and extends backward to the hypoglossal rootlets to the level of a rostrocaudal line through the most prominent part of the inferior olive that marks the boundary between the anterior and lateral surfaces of the medulla. This is the segment that was affected by the aneurysm in this case. The lateral medullary segment begins where the artery passes the most prominent point of the olive and ends at the level of the origin of the glossopharyngeal, vagus, and accessory rootlets. The tonsillomedullary portion begins where the PICA passes posterior to the glossopharyngeal, vagus, and accessory nerves and
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Figure 4. (A and B) Postoperative computed tomography evaluation showing no surgical-related complications. (C and D) Three-dimensional reconstructions of the paramedian suboccipital subtonsillar approach have
extends medially across the posterior aspect of the medulla near the caudal half of the tonsil. For the main interest of the surgical variation herewith proposed, some details
of the hypoglossal nerve should be reviewed. The hypoglossal nerve result from as a series of rootlets that exits the brainstem along the anterior margin of the caudal two-thirds of the olive in the
Figure 5. (A) Left paramedian suboccipital subtonsillar exposure of the extracranial vertebral artery in the suboccipital triangle. (B). Temporary clip can be applied without narrowing the intracranial surgical space. VA,
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been provided. (E) Postoperative cerebral digital subtraction angiography confirmed complete occlusion of the aneurysm, with patency of the surrounding arteries.
preolivary sulcus. The hypoglossal rootlets, in their course from the preolivary sulcus to the hypoglossal canal, pass often posterior to the VA. The relation of the origin and proximal part of the PICA to the
vertebral artery, V3; Atlas, posterior portion of C1; Fdm, dura mater of the foramen magnum; PFdm, posterior fossa dura mater.
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Figure 6. (A) Intraoperative pictures showing the subtonsillar route to the anterior medullary segment of the left posterior cerebellar artery. Identification of the tonsillomedullary segment of both posterior inferior cerebellar arteries (PICAs). Asterisks indicate the tonsillomedullary segment of the posterior inferior cerebellar artery. (B). Dissection of the left PICA thus reaching its lateral medullary segment, being in close relationship with lower cranial nerve roots. Double
hypoglossal rootlets differs significantly. The PICA arises either rostral or caudal or at the level of the hypoglossal rootlets. The initial segment of the PICA has a variable course in relation to the hypoglossal rootlets. The most common course is for the PICA to arise from the VA and pass directly posteriorly around or between the hypoglossal rootlets (Figure 2).18,19 CASE REPORT A 60-year-old man with hypertension, previous ischemic heart disease, and hepatitis B viruserelated cirrhosis was admitted to our emergency department (Hospital Virgen del Rocio, Sevilla, Spain) after a mild head trauma. A computed tomography (CT) scan of the brain
asterisk indicates the lateral medullary segment of the left posterior inferior cerebellar artery. (C) Exposure of the aneurysm arising from the anterior medullary segment of the left PICA. Plus sign indicates the anterior medullary segment of the left posterior inferior cerebellar artery. (D) Clipping of the aneurysm with patency of the surrounding vessels. Med, medulla; Tonsil, left cerebellar tonsil; An, aneurysm.
revealed subarachnoid blood, predominantly in the perimesencephalic cisterns. Accordingly, we decided to hospitalize the patient in the Division of Neurosurgery for further diagnostic tests. Findings of the neurologic examination were normal, with a Glasgow Coma Scale score of 15/15 points. To rule out the presence of a cerebral aneurysm, an angio-CT scan was performed the day of the admission that demonstrated an uncertain image located at the level of the proximal left posterior inferior cerebellar artery aneurysm. Further neuroradiologic investigation was performed by means of a cerebral digital subtraction angiography that showed the presence of a possible aneurysm located at the level of the anteromedullary segment of the left posterior inferior cerebellar artery
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but difficult to comprehensively characterize and to confirm with certainty, due to the recent bleeding. Accordingly, because of the excellent clinical condition, it was decided to repeat the angiography 14 days later. The subsequent cerebral angiography clearly showed the presence of a 3-mm left PICA aneurysm arising from its most proximal segment, i.e., the anteromedullary segment (Figure 3). A standard endovascular treatment or even a stent-assisted coiling were excluded by the interventional radiologists due to the high risk of PICA occlusion with such peculiar aneurysm location and projection. After careful consideration of many factors, including patient age, general clinical conditions, and aneurysm size, it was decided to treat the aneurysm by using a
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Figure 7. (A) Panoramic view of the surgical field after aneurysm clipping. (B) Closure technique used for this case with synthetic sutureable dura mater (C) covered by another layer of no sutured dural substitute. (D) A
left paramedian suboccipital subtonsillar approach 3 weeks after the patient’s admittance. A postoperative arteriogram showed proper placement of the clip, obliteration of the aneurysm, and the patency of the VA and PICA. Neither postoperative infection nor cerebrospinal fluid leak was detected. The postoperative course was characterized by slight and temporary dysphagia. A postoperative CT scan demonstrated the resolution of the subarachnoid hemorrhage without any other neurosurgical complications, and the patient was discharged 10 days after surgery (Figure 4). Surgical Technique The patient was placed in the prone position and the head, flexed downwards 10 e15 , and was stabilized by means of a
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titanium mesh has been placed to cover the skull base defect and the dead space has been filled with fibrin glue. Med, medulla; Tonsil, cerebellar tonsil; PFdm, dura mater of the posterior fossa.
3-points MayfieldeKees skeletal fixation headrest. A slightly curved vertical incision 4 cm behind the left mastoid bone and extending from the superior nuchal line down to the level of C-4 was performed. Muscles were detached and retracted up to the exposure of the occipital bone. A paramedian left suboccipital craniotomy was extended from the midline medially to the sigmoidal sinus laterally, including the foramen magnum. The left condyle was exposed. The transverse process of the atlas was palpated and exposed approximately 1 cm below the tip of the mastoid and through the suboccipital triangle, which is formed medially by the rectus capitis posterior major muscle, superolaterally by the superior oblique, and inferolaterally by the inferior oblique muscle. It is in this triangle where the
horizontal segment of the third portion of the extracranial VA (V3) usually runs, within a groove on the lamina of the atlas. After the suboccipital triangle was revealed, the complex venous compartment around V3 (the suboccipital cavernous sinus) was visualized. The V3 was then exposed extradurally, under full visualization, so a temporary clip could be applied when it was needed (Figure 5). After obtaining proper exposure of the V3 segment of the VA, we opened the dura mater and cerebrospinal fluid was drained from the cisterna magna to relax the brain. Afterwards, the left PICA was followed backwards, i.e., from the tonsillomedullary segment to the anteromedullary one, by elevating the homolateral cerebellar tonsil. Accordingly, following the PICA in the
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subtonsillar corridor, we recognized a lateral projecting aneurysm proximal to the origin of the PICA. Thereafter, the arachnoid membrane was sharply dissected to expose the aneurysm sac and a curved titanium aneurysm clip was placed (Figure 6). At the end of the procedure, normal blood flow in the left PICA and VA was checked by the use of the micro-Doppler ultrasound probe. The closure technique used for this case included synthetic suturable dura mater covered by a layer of no suturable dural substitute; a titanium mesh was placed to cover the skull base defect, and the dead space was filled with Fibrin glue (Figure 7). DISCUSSION The PICA has the most complex and variable course among all arteries of the posterior circulation. Hence, proximal PICA aneurysms could be considered as are a unique subset of posterior circulation aneurysm, representing from 0.5% to 3% of all intracranial aneurysms.20 Surgery for such vascular diseases may disclose particular problems due to deep aneurysm location and its intimate relationship with the lower brainstem and lower cranial nerves. The complexities involved in the surgical approach to the PICA aneurysms relate to the narrow corridor limited by the brainstem, petrous occipital bones, and multiple neurovascular structures occupying the cerebellomedullary and cerebellopontine cisterns.21 In many centers, proximal PICA aneurysms commonly are treated with a far-lateral suboccipital craniotomy and surgical clipping of the aneurysm. More extensive skull base approaches such as the lateral suboccipital, transcondylar, extremelateral transcondylar, far-lateral, and transpharyngeal-transclival have been described as well.9,22-24 In contrast, endovascular management increasingly is used as an alternative to surgery but specific endovascular outcomes of PICA aneurysms are not well established. The surgical option tends to reveal unique difficulties because of complex neurovascular anatomy and its close relationship with the lower brainstem and lower cranial nerves. For many years, controversy has raged over the advantages and disadvantages of the various surgical routes
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to approach such lesions depending on their anatomic location and morphology. Together with the selection of the proper surgical route, management of proximal PICA aneurysms requires appropriate vascular control, as with any neurovascular procedure. In particular, the proximal vascular control can be achieved via identification of the VA through the dentate ligament, intracranially, or by means of removing the posterior portion of the atlas thus allowing extracranial control of the VA. However, both surgical maneuvers have some surgical drawbacks. As a matter of fact, if on one hand removal of the posterior portion of the atlas may add some risks of bleeding, unnecessary bone removal, and prolonged surgical time, on the other hand when localizing the VA directly in the intracranial space its vascular control by means of vascular clips may tighten the surgical space (the intradural surgical space). Given such a background, with this brief technical report we intended to share a modified posterolateral paramedian suboccipital subtonsillar approach with the aim of refining the vascular control over the VA via a suboccipital subtonsillar approach. The modification consisted of accomplishing proper proximal vascular control at the level of the extracranial segment of the VA without the need of further removal of the posterior portion of the atlas. The advantages of such technical adjunct can be summarized as follow: 1) localization and dissection of the extracranial VA before opening the dura, thus allowing for an early proximal vascular control in the V3 segment of the VA; 2) no need for removal of the posterior portion of the atlas and/or occipital condyle drilling, thus avoiding wasting surgical time and/or venous bone bleeding; 3) avoid narrowing the surgical space with temporary clip applied on the intracranial VA; and 4) the possibility of contralateral clipping of the intracranial VA, without narrowing the surgical space. In the present article, we have intended to afford an additional technical aspect to the surgeon’s armamentarium related to the difficult management of proximal PICA aneurysms. Relevant anatomical demonstration has been provided as well. However, it has to be stressed that a multimodality approach tailored to the specific aneurysm in the specific patient currently still stands as the better approach for such kind of pathologies.
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CONCLUSIONS This modified approach allowed for avoiding unnecessary cervical spine bone removal, i.e., no need to drill the occipital condyle or remove the atlas, offered proper proximal vascular control in the early stage of the surgical procedure, and limited the quantity of temporary vascular clips in the intracranial surgical field, thus preventing possible instruments crowding in a relatively narrow space. The relevant anatomy pertinent to this case has been illustrated and discussed. With this contribution, we aimed to report some specific technical issues regarding the difficult surgical management of proximal posterior inferior cerebellar artery aneurysms. REFERENCES 1. Foster MT, Herwadkar A, Patel HC. Posterior inferior cerebellar artery/vertebral artery subarachnoid hemorrhage: a comparison of saccular vs dissecting aneurysms. Neurosurgery. 2018;82: 93-98. 2. Lehto H, Kivisaari R, Niemelä M, Dashti R, Elsharkawy A, Harati A, et al. Seventy aneurysms of the posterior inferior cerebellar artery: anatomical features and value of computed tomography angiography in microneurosurgery. World Neurosurg. 2014;82:1106-1112. 3. Viswanathan GC, Menon G, Nair S, Abraham M. Posterior inferior cerebellar artery aneurysms: operative strategies based on a surgical series of 27 patients. Turk Neurosurg. 2014;24:30-37. 4. Awad AJ, Mascitelli JR, Haroun RR, De Leacy RA, Fifi JT, Mocco J. Endovascular management of fusiform aneurysms in the posterior circulation: the era of flow diversion. Neurosurg Focus. 2017;42: E14. 5. Srinivasan VM, Ghali MGZ, Reznik OE, Cherian J, Mokin M, Dumont TM, et al. Flow diversion for the treatment of posterior inferior cerebellar artery aneurysms: a novel classification and strategies. J Neurointerv Surg. 2018;10:663-668. 6. Xu F, Hong Y, Zheng Y, Xu Q, Leng B. Endovascular treatment of posterior inferior cerebellar artery aneurysms: a 7-year single-center experience. J Neurointerv Surg. 2017;9:45-51. 7. Korja M, Kivisaari R, Rezai Jahromi B, Lehto H. Size and location of ruptured intracranial aneurysms: consecutive series of 1993 hospitaladmitted patients. J Neurosurg. 2017;127:748-753. 8. Song J, Park JE, Chung J, Lim YC, Shin YS. Treatment strategies of ruptured posterior inferior cerebellar artery aneurysm according to its segment. Surg Neurol Int. 2017;8:155. 9. Bertalanffy H, Sure U, Petermeyer M, Becker R, Gilsbach JM. Management of aneurysms of the vertebral artery-posterior inferior cerebellar artery
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 31 May 2018; accepted 2 June 2018 Citation: World Neurosurg. (2018) 117:301-308. https://doi.org/10.1016/j.wneu.2018.06.019 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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