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Surgical Anatomy for Control of Ethmoidal Arteries During Extended Endoscopic Endonasal or Microsurgical Resection of Vascular Anterior Skull Base Meningiomas
Perspectives Commentary on: Anterior and Posterior Ethmoidal Artery Ligation in Anterior Skull Base Meningiomas: A Review on Microsurgical Approaches by Cecchini World Neurosurg 84:1161-1165, 2015
Surgical Anatomy for Control of Ethmoidal Arteries During Extended Endoscopic Endonasal or Microsurgical Resection of Vascular Anterior Skull Base Meningiomas Mohamed El-Fiki
M
eningiomas represent about 13%e20% of brain tumors; skull base meningiomas represent about 44%. Anterior skull base meningiomas are supplied from anterior or posterior ethmoidal arteries (branches of the ophthalmic artery), as in olfactory groove (10%) and tuberculum sellae and planum sphenoidale (13%) meningiomas, or middle meningeal arteries, as in sphenoid ridge meningiomas 17% (9, 13, 23). In addition to anastomosis between the middle meningeal artery and the ophthalmic artery, the middle meningeal artery may arise from the ophthalmic artery, or the ophthalmic artery may arise from the middle meningeal artery in rare cases (11, 12, 15, 33). Collaterals from the meningeal branches of the internal carotid arteries, frontal or sphenoid branches of the middle meningeal arteries, and the sphenopalatine branch of the distal maxillary artery may share in the secondary arterial supply of midline anterior skull base meningiomas (olfactory groove, planum sphenoidale, and tuberculum sellae). This rich arterial network predisposes anterior skull base lesions to high vascularity in many cases, especially meningiomas and arteriovenous malformations. Anterior skull base meningiomas may be approached through transcranial (bicoronal subfrontal, oblique subfrontal, interhemispheric, or classic pterional transsylvian approaches) or extended endonasal minimally invasive approaches. Operating in a less vascular field may be achieved if the feeding anterior and posterior ethmoidal arteries are controlled preoperatively or early during the operation (29). Hypertrophied feeding ethmoidal vessels passing through sclerosed foramina are difficult to control early in the setting of edematous brain or a huge tumor with difficult retraction during open transcranial microsurgery.
Keywords Anterior skull base meningioma - Arterial ligation - Meningioma - Olfactory groove meningioma -
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Abbreviations and Acronyms CSF: Cerebrospinal fluid CT: Computed tomography
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The vessels may be hard to control during an endoscopic transnasal approach when they are embedded in hyperostotic sclerosed bone. They may be better controlled intracranially or extracranially via microsurgical or endoscopic approaches rather than with endovascular embolization, which carries a risk of blindness induced by retrograde spilling of embolization material onto the ophthalmic arteries, which are the main stems of the ethmoidal vessels. Anterior skull base meningiomas, especially olfactory groove meningiomas because of their subfrontal origin, usually reach huge sizes before symptoms attract the attention of a keen treating physician in many developing and developed countries. Chemotherapy so far is futile (19, 20, 25). Large tumors usually parasitize additional blood supply from neighboring arteries. At this stage, surgical extirpation is the only option if the tumors have grown beyond the critical radiosurgical limiting size (17). A major challenge for successful resections of these meningiomas, whether using open microsurgical or endoscopic approaches, is the proper control of the arterial supply through the anterior or posterior ethmoidal arteries. Most studies have shown wide anatomic and radiologic aberrations of the ethmoidal arteries, such as passing over the roof of the frontal recess or the posterior ethmoidal sinus, together with lamellar variability and possible incoherence that may hinder the surgeon’s ability to identify the artery. In suspected highly vascularized anterior basal meningiomas, digital subtraction angiography is required together with computed tomography (CT) angiography before embarking on embolization or operation. Manjila et al. (14) studied the anatomic variations of the ethmoidal foramina in anthropology specimens. They used
Department of Neurosurgery, University of Alexandria, Alexandria, Egypt To whom correspondence should be addressed: Mohamed El-Fiki, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 6:1532-1535. http://dx.doi.org/10.1016/j.wneu.2015.07.029
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a Lynch or transcaruncular approach in 3 patients as safe feasible approaches for control of these vessels before open or endoscopic resection of meningiomas that did not receive embolization or received only partial embolization. The duration between embolization and surgery is not yet standardized to avert reopening of arteries that received embolization and the formation of new vasculature, which may neutralize the embolization effect (7, 18). Preoperative embolization of highly vascular anterior cranial fossa meningiomas is feasible but is not without hazards, including ophthalmic artery iatrogenic extension of embolization (21, 22). Thorough knowledge of the microsurgical and endoscopic anatomy of ethmoidal arteries and possible safe clipping sites is a prerequisite for proper selection of the surgical approach and surgical planning and safe execution of complete removal. The success of surgery substantially depends on the surgeon’s intelligent choice of a familiar approach for a particular tumor site and blood supply. Unnecessarily occluding bridging and drainage veins might be catastrophic. The posterior ethmoidal artery arises from the proximal first segment of the ophthalmic artery. Arising from the distal intraorbital third segment of the ophthalmic artery, the anterior ethmoidal arteries penetrate the lamina papyracea, into the roof of the ethmoid sinuses where it gives off its dorsal nasal artery and through the cribriform plate close to the crista galli to the intracranial opening of the anterior ethmoidal canal to form the anterior falx artery (14). In a cadaver study (3), the anterior ethmoidal foramen was about 32 mm to the right of the middle point of the nasofrontal suture and 34 mm to the left. It was 12.3 mm anterior to the posterior foramen, which was 7.1 mm more anterior to the distal opening of the right optic canal and 7.3 mm on the left. In an anatomic endoscopic study (1), the posterior ethmoidal artery was a mean 11.08 mm (range, 8e16 mm) anterior to the optic canal, whereas the anterior ethmoidal artery was a mean 13 mm (range, 10e17 mm) more anterior to the posterior ethmoidal artery. It was mainly found between the superior and middle lamellae (1, 3). In an endoscopic study in Chinese adults, the distance from the columella to the anterior ethmoidal artery measured 62.71 mm 2.18 on the right side and 63.38 mm 1.69 on the left. The distance between the columella and the posterior ethmoidal artery was 70.91 mm 1.99 on the right and 71.79 mm 1.95 on the left (10). The right posterior ethmoidal artery diameter was 0.66 mm 0.21, and the left posterior ethmoidal artery diameter was 0.63 mm 0.19. The anterior ethmoidal arteries were generally thicker than the posterior ethmoidal artery (0.92 mm 0.2 on the right and 0.88 mm 0.15 on the left) (8). In another study, the diameter of the anterior ethmoidal artery was 6e10 mm (32). The anterior ethmoidal artery runs between the second and third lamellae (where it is identified endoscopically at least in 90% of cases) or through the suprabulbar recess to the anterior ethmoidal canal with the anterior ethmoidal nerves and veins (8, 22, 27, 32). The anterior ethmoidal arteries are always single. They were absent in 2 of 30 sides. In such cases, the posterior ethmoidal arteries ran anteriorly and interiorly divided through the crista galli suture to supply the anterior ethmoidal territory. The persistently present anterior ethmoidal canal was 7e10 mm in length and was dehiscent in its proximal or distal part in one third of cases.
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During endoscopic exposure, the surgeon may localize the artery parallel to the ethmoid sinus roof, as it curves along the cribriform plate posterolateral to anteromedial at an angle of 60 to the lamina papyracea. It may be found in the roof of the frontal recess or the roof of the posterior ethmoid sinus in a few cases. A 30 rigid endoscope is preferred for clipping or a curved Ligaclip with 0 scope. It is more accessible in a well-pneumatized sinus (32). It is recommended to assess ethmoid pneumatization by CT to decrease the risk of injuring the artery (27). Minimally invasive extended endonasal approaches allow early control of the feeding ethmoidal arteries. However, these endoscopic approaches are demanding and require sharpened surgical skill and an adequate learning curve to minimize postoperative complications (9). Visualization of the lamina papyracea in the medial orbital wall allows the anterior ethmoidal foramina and canal to be identified for safe early coagulation and division of the anterior ethmoidal arteries extracranially. The anterior ethmoidal artery is sought posterior to the anterior face of the ethmoidal bulla. The smaller posterior ethmoidal artery is looked for at the junction of the roof of the sphenoid and posterior ethmoid sinus. White et al. (31) recognized 3 safe sites for control of the anterior ethmoidal artery before resection in the presence of a vascular anterior skull base lesion through a single flap fronto-orbital craniotomy instead of the classic pterional or subfrontal approaches: 1) the anterior ethmoidal foramen at the lamina papyracea of the medial orbital wall, 2) the anterior ethmoid canal at the lateral ethmoid wall, and 3) intracranial extradural at the cribriform plate. The open lamina papyracea clipping site was previously described in a bicoronal intracranial extradural approach (16). Extracranial open bilateral anterior and posterior ethmoidal artery ligation may be performed through Lynch incision exposure down to the periosteum of the medial orbital walls. The frontoethmoidal suture is followed bluntly for about 22 mm posterior to the lacrimal crest, and the posterior ethmoidal artery is encountered about 15 mm posterior to the anterior ethmoidal artery (14). The extracranial transcaruncular approach entails an incision just lateral to the caruncle, identifying the lacrimal fossa and following the avascular facial plans posteromedially to the frontoethmoidal suture. The periosteum is incised bilaterally to allow a posterior subperiosteal dissection trajectory to the anterior ethmoidal arteries. In a paper recently published in WORLD NEUROSURGERY, the authors reviewed microsurgical anatomy literature pertinent to extracranial ligation of the anterior and posterior ethmoidal arteries and identified 2 possible control sites. They applied their findings in 5 approaches during exposure of anterior cranial fossa basal meningiomas. The results apply to an endoscopic rather than an open approach, although both may be used interchangeably (26). Early arterial ligation is an added advantage in endoscopic transnasal approaches to anterior skull base meningiomas (29). The frontal recess, the anterior ethmoidal artery, and the posterior ethmoidal artery were suggested as constant landmarks in the extended endoscopic transnasal approach to the anterior skull base (32). The authors preferred endoscopic approaches, which are more amenable to small or medium-sized lesions at the present stage of surgical expertise. Schroeder (24) found no advantage of an endoscopic approach over craniotomy in surgery of small or
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medium-sized olfactory groove, planum sphenoidale, and tuberculum sellae meningiomas compared with the eyebrow approach because the trauma to the nasal cavity, paranasal sinuses, and skull base is greater, and there is increased risk of cerebrospinal fluid (CSF) leak. Discussion about the merits of the authors’ findings is warranted in relation to different approaches and how the authors’ technique can be implemented in each individual case. Experience shall illustrate how frequently visual compromise might be encountered using the authors’ suggested open microsurgical technique compared with currently practiced endovascular, endonasal endoscopic or transcranial approaches. The direct anatomic endoscopic approach avoids traversing significant neurovascular structures, obviating consequences of brain retraction. Proper understanding of the endoscopic anatomy of anterior ethmoidal arteries is a prerequisite for endoscopic clipping of these arteries during endonasal resection or as preoperative preparation of an intracranial approach. An extra-axial midline anterior skull base tumor such as a meningioma expands upward and laterally, displacing important midline structures away from the base and creating a safe natural corridor for their endoscopic resection through an extended endonasal approach. Limited working space through the endoscopic dural opening and the difficulty of attaining proper repair with CSF leak and possible infective complications or tension pneumocephalus limits widespread application of endoscopic minimally invasive procedures. Supporters claim lower mortality and morbidity compared with transcranial routes with equal surgical resectability. Staged and redo extended endonasal resections may be considered to handle large or huge lesions (5). The posterior ethmoidal artery is more vulnerable during exposure for planum sphenoidale meningiomas, whereas the anterior and the posterior ethmoidal arteries are at risk approaching olfactory groove meningiomas. Preoperative radiologic visualization of the anterior ethmoidal arteries is feasible with noninvasive coronal CT angiography. Supraorbital pneumatization facilitates CT visualization of the course and ensures easier clipping but increases the risk of iatrogenic injury of the anterior ethmoidal artery. The anterior ethmoidal canal may be identified in 40%, the anterior ethmoidal sulcus is clearly identified in 98%, and the bony anterior ethmoidal foramen is evident in 100% of CT angiographies (28). The anterior ethmoidal foramen appears as a notch of the medial wall of the orbit, whereas the anterior ethmoidal groove displays a focal funneling in the olfactory fossa. Endoscopic closure with a vascularized nasoseptal flap decreases CSF leak (30). Proper clipping of the anterior ethmoidal arteries avoids retraction and intraorbital hematoma that may predispose to ophthalmologic complications. Most ethmoidal foramina (78%) are situated along the frontoethmoidal suture; 22% are within 6 mm. An equal percentage of posterior ethmoidal foramina (78%) is
REFERENCES 1. Abuzayed B, Tanriover N, Gazioglu N, Sanus GZ, Ozlen F, Biceroglu H, Kafadar AM, Eraslan BS, Akar Z: Endoscopic endonasal anatomy and approaches to the anterior skull base: a
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along the suture, and 4% are outside it, again within 6 mm. An accessory ethmoidal foramen was identified in 26% of studied orbits (10). The mean distances between the frontoethmoidal suture and the anterior ethmoid foramen, the posterior ethmoid foramen, and the accessory foramen—when present—were 2.1 mm 0.5, 2.0 mm 1.5, and 2.3 mm 1.2. The distances from the suture to the anterior ethmoidal, posterior ethmoidal, and accessory ethmoidal foramina were 1.2 to 3.32 mm, 1.02 to 5.76 mm, and 1.1 to 3.65 mm. An angled 30 Ligaclip allows adequate visualization of the anterior ethmoidal artery during clipping, rather than a straight Ligaclip if a 0 endoscope is used. It is recommended to clip the artery in the orbit rather than at the ethmoidal roof because of the closeness of the artery to the cranial base, which was <5 mm in 90% of cases (2). Al-Mefty preferred the endoscopic approach for olfactory groove meningioma because it allows early control of the ethmoidal arteries. He cautioned surgeons to expect difficulty in large tumors that reach the planum or the tuberculum, and he advised careful dissection of the adherent carotid complex vasculature (6). Other authors preferred transcranial approaches, such as the pterional approach (4). They stressed its advantage for early identification of the posterior carotid vascular complex and the adjacent optic apparatus, frontal sinus conservation, less brain retraction, and familiarity to most neurosurgeons. Kleiber et al. (12) preferred the minimally invasive transglabellar approach through an inter-eyebrow incision and a 3-cm bone flap in the frontal sinus to expose the midline skull base in 24 totally removed meningiomas with 12.5% incidence of CSF leak and 4% incidence of meningitis. These authors did not discuss in detail how they handled the anterior ethmoidal artery in vascular lesions. In conclusion, the ethmoidal arteries may be controlled via an intracranial or extracranial approach, in the orbit or in the ethmoidal roof through microsurgical or endoscopic approaches rather than endovascular embolization, which carries a remote risk of spilling embolic material onto the ophthalmic arteries. A thorough knowledge of the microsurgical and endoscopic anatomy of ethmoidal arteries and possible safe clipping sites is a prerequisite for proper selection of the surgical approach and surgical planning as well as safe execution of complete removal of vascular anterior skull base meningiomas. The success of surgery substantially depends on the surgeon’s intelligent choice of a familiar approach for a particular tumor site and blood supply based on adequate radiologic evaluation. Unnecessarily occluding bridging and drainage veins might be catastrophic. Hypertrophied ethmoidal vessels passing through sclerosed basal foramina are difficult to control early in a transcranial approach or through the ethmoid sinus roof in endoscopic exposures at the skull base. These vessels instead may be approached extracranially in the orbit away from the thickened sclerosed tumor or infiltrated invaded skull base.
neurosurgeon’s viewpoint. J Craniofac Surg 21: 529-537, 2010.
study [in Portuguese]. Braz J Otorhinolaryngol 77: 33-38, 2011.
2. Araujo Filho BC, Pinheiro-Neto CD, Ramos HF, Voegels RL, Sennes LU: Endoscopic ligation of the anterior ethmoidal artery: a cadaver dissection
3. Avcı E, Aktüre E, Seçkin H, Uluç K, Bauer AM, Izci Y, Morcos JJ, Bas¸kaya MK: Level I to III craniofacial approaches based on Barrow
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classification for treatment of skull base meningiomas: surgical technique, microsurgical anatomy, and case illustrations. Neurosurg Focus 30: E5, 2011.
giant olfactory groove or planum sphenoidale meningiomas: 3 illustrative cases with a review of the literature on surgical techniques. Neurosurg Focus 35:E13, 2013.
25. Schulz C, Mathieu R, Kunz U, Mauer UM: Treatment of unresectable skull base meningiomas with somatostatin analogs. Neurosurg Focus 30: E11, 2011.
4. Bitter AD, Stavrinou LC, Ntoulias G, Petridis AK, Dukagjin M, Scholz M, Hassler W: The role of the pterional approach in the surgical treatment of olfactory groove meningiomas: a 20-year experience. J Neurol Surg B Skull Base 74:97-102, 2013.
15. Manjunath KY: Anomalous origin of the middle meningeal artery—a review. J Anat Soc India 50: 179-183, 2001.
26. Sekhar LN, Tariq F, Ferreira M: What is the best approach to resect an anterior midline skull base meningioma in 2011? Microsurgical transcranial, endonasal endoscopic, or minimal access cranial? World Neurosurg 77:621-622, 2012.
5. Cavallo M, Messina A, Cappabianca P, Esposito F, de Divitiis E, Gardner P, Tschabitscher M: Endoscopic endonasal surgery of the midline skull base: anatomical study and clinical considerations. Neurosurg Focus 19:E2, 2005. 6. De Monte F, McDermott MW, Al-Mefty O, eds. Al-Mefty’s Meningiomas. 2nd ed. New York: Thieme Medical Publishers; 2011. 7. Dowd CF, Halbach VV, Higashida RT: Meningiomas: the role of preoperative angiography and embolization. Neurosurg Focus 15:E10, 2003. 8. Erdogmus S, Govsa F: The anatomic landmarks of ethmoidal arteries for the surgical approaches. J Craniofac Surg 17:280-285, 2006. 9. Honig S, Trantakis C, Frerich B, Sterker I, Kortmann RD, Meixensberger J: Meningiomas involving the sphenoid wing outcome after microsurgical treatment—a clinical review of 73 cases. Cent Eur Neurosurg 71:189-198, 2010. 10. Kazak Z, Celik S, Ozer MO, Govsa F: Threedimensional evaluation of the danger zone of ethmoidal foramens on the frontoethmoidal suture line on the medial orbital wall. Surg Radiol Anat 25:218-223, 2015. 11. Kimball D, Kimball H, Tubbs RS, Lukas M: Variant middle meningeal artery origin from the ophthalmic artery: a case report. Surg Radiol Anat 37:105-108, 2015. 12. Kleiber JC, Roemer S, Duntze J, Eap C, Theret E, Rousseaux P, Litre F: Transglabellar approach for resection of anterior midline skull base meningiomas: technical note. Acta Neurochir (Wien) 156: 2283-2287, 2014. 13. Liu Q, Rhoton AL Jr: Middle meningeal origin of the ophthalmic artery. Neurosurgery 49:401-406; discussion 406-407 2001. 14. Manjila S, Cox EM, Smith GA, Corriveau M, Chhabra N, Johnson F, Geertman RT: Extracranial ligation of ethmoidal arteries before resection of
16. McDermott MW, Rootman J, Durity FA: Subperiosteal, subperiorbital dissection and division of the anterior and posterior ethmoid arteries for meningiomas of the cribriform plate and planum sphenoidale: technical note. Neurosurgery 36: 1215-1219, 1995. 17. Nanda A, Jawahar A, Sathyanarayana S: Microsurgery for potential radiosurgical skull base lesions: a retrospective analysis and comparison of results. Skull Base 13:131-138, 2003. 18. Nania A, Granata F, Vinci S, Pitrone A, Barresi V, Morabito R, Settineri N, Tomasello F, Alafaci C, Longo M: Necrosis score, surgical time, and transfused blood volume in patients treated with preoperative embolization of intracranial meningiomas. Analysis of a single-centre experience and a review of literature. Clin Neuroradiol 24:29-36, 2013. 19. Newton HB: Hydroxyurea chemotherapy in the treatment of meningiomas. Neurosurg Focus 23: E11, 2007. 20. Norden AD, Drappatz J, Wen PY: Advances in meningioma therapy. Curr Neurol Neurosci Rep 9:231-240, 2009. 21. Perrini P, Cardia A, Fraser K, Lanzino G: A microsurgical study of the anatomy and course of the ophthalmic artery and its possibly dangerous anastomoses. J Neurosurg 106:142-150, 2007. 22. Raper MS, Starke RM, Henderson F, Ding D, Simon S, Evans AJ, Jane AJ, Liu KC: Preoperative embolization of intracranial meningiomas: efficacy, technical considerations, and complications. AJNR Am J Neuroradiol 35:1798-1804, 2014. 23. Rockhill J, Mrugala M, Chamberlain MC: Intracranial meningiomas: an overview of diagnosis and treatment. Neurosurg Focus 23:E1, 2007. 24. Schroeder HW: Indications and limitations of the endoscopic endonasal approach for anterior cranial base meningiomas. World Neurosurg 82(6 Suppl):S81-S85, 2014.
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27. Simmen D, Raghavan U, Briner HR, Manestar M, Schuknecht B, Groscurth P, Jones NS: The surgeon’s view of the anterior ethmoid artery. Clin Otolaryngol 31:187-191, 2006. 28. Souza SA, de Souza MM, Gregório LC, Ajzen S: Anterior ethmoidal artery evaluation on coronal CT scans. Braz J Otorhinolaryngol 75:101-106, 2009. 29. Ung TH, Waziri AE, Ramakrishnan VR: Preoperative ethmoid artery ligation facilitates resection of large sub-frontal meningiomas. Am J Otolaryngol 35:424-426, 2014. 30. Verillaud B, Bresson D, Sauvaget E, Mandonnet E, Georges B, Kania R, Herman P: Transcribriform and transplanum endoscopic approach for skullbase tumors. Eur Ann Otorhinolaryngol Head Neck Dis 130:233-236, 2013. 31. White DV, Sincoff EH, Abdulrauf SI: Anterior ethmoidal artery: microsurgical anatomy and technical considerations. Neurosurgery 56(2 Suppl): 406-410, 2005. 32. Yang YX, Lu QK, Liao JC, Dang RS: Morphological characteristics of the anterior ethmoidal artery in ethmoid roof and endoscopic localization. Skull Base 19:311-317, 2009. 33. Zong Y, Li X, Jiang Y, Xu J, Li J: Transnasal approach to the anterior skull base: an endoscopic anatomic study. J Craniofac Surg 25:1041-1043, 2014.
Citation: World Neurosurg. (2015) 84, 6:1532-1535. http://dx.doi.org/10.1016/j.wneu.2015.07.029 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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Surgical Anatomy for Control of Ethmoidal Arteries During Extended Endoscopic Endonasal or Microsurgical Resection of Vascular Anterior Skull Base Meningiomas Mohamed El-Fiki
M
eningiomas represent about 13%e20% of brain tumors; skull base meningiomas represent about 44%. Anterior skull base meningiomas are supplied from anterior or posterior ethmoidal arteries (branches of the ophthalmic artery), as in olfactory groove (10%) and tuberculum sellae and planum sphenoidale (13%) meningiomas, or middle meningeal arteries, as in sphenoid ridge meningiomas 17% (9, 13, 23). In addition to anastomosis between the middle meningeal artery and the ophthalmic artery, the middle meningeal artery may arise from the ophthalmic artery, or the ophthalmic artery may arise from the middle meningeal artery in rare cases (11, 12, 15, 33). Collaterals from the meningeal branches of the internal carotid arteries, frontal or sphenoid branches of the middle meningeal arteries, and the sphenopalatine branch of the distal maxillary artery may share in the secondary arterial supply of midline anterior skull base meningiomas (olfactory groove, planum sphenoidale, and tuberculum sellae). This rich arterial network predisposes anterior skull base lesions to high vascularity in many cases, especially meningiomas and arteriovenous malformations. Anterior skull base meningiomas may be approached through transcranial (bicoronal subfrontal, oblique subfrontal, interhemispheric, or classic pterional transsylvian approaches) or extended endonasal minimally invasive approaches. Operating in a less vascular field may be achieved if the feeding anterior and posterior ethmoidal arteries are controlled preoperatively or early during the operation (29). Hypertrophied feeding ethmoidal vessels passing through sclerosed foramina are difficult to control early in the setting of edematous brain or a huge tumor with difficult retraction during open transcranial microsurgery.
Keywords Anterior skull base meningioma - Arterial ligation - Meningioma - Olfactory groove meningioma -
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Abbreviations and Acronyms CSF: Cerebrospinal fluid CT: Computed tomography
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The vessels may be hard to control during an endoscopic transnasal approach when they are embedded in hyperostotic sclerosed bone. They may be better controlled intracranially or extracranially via microsurgical or endoscopic approaches rather than with endovascular embolization, which carries a risk of blindness induced by retrograde spilling of embolization material onto the ophthalmic arteries, which are the main stems of the ethmoidal vessels. Anterior skull base meningiomas, especially olfactory groove meningiomas because of their subfrontal origin, usually reach huge sizes before symptoms attract the attention of a keen treating physician in many developing and developed countries. Chemotherapy so far is futile (19, 20, 25). Large tumors usually parasitize additional blood supply from neighboring arteries. At this stage, surgical extirpation is the only option if the tumors have grown beyond the critical radiosurgical limiting size (17). A major challenge for successful resections of these meningiomas, whether using open microsurgical or endoscopic approaches, is the proper control of the arterial supply through the anterior or posterior ethmoidal arteries. Most studies have shown wide anatomic and radiologic aberrations of the ethmoidal arteries, such as passing over the roof of the frontal recess or the posterior ethmoidal sinus, together with lamellar variability and possible incoherence that may hinder the surgeon’s ability to identify the artery. In suspected highly vascularized anterior basal meningiomas, digital subtraction angiography is required together with computed tomography (CT) angiography before embarking on embolization or operation. Manjila et al. (14) studied the anatomic variations of the ethmoidal foramina in anthropology specimens. They used
Department of Neurosurgery, University of Alexandria, Alexandria, Egypt To whom correspondence should be addressed: Mohamed El-Fiki, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 6:1532-1535. http://dx.doi.org/10.1016/j.wneu.2015.07.029
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.07.029
PERSPECTIVES
a Lynch or transcaruncular approach in 3 patients as safe feasible approaches for control of these vessels before open or endoscopic resection of meningiomas that did not receive embolization or received only partial embolization. The duration between embolization and surgery is not yet standardized to avert reopening of arteries that received embolization and the formation of new vasculature, which may neutralize the embolization effect (7, 18). Preoperative embolization of highly vascular anterior cranial fossa meningiomas is feasible but is not without hazards, including ophthalmic artery iatrogenic extension of embolization (21, 22). Thorough knowledge of the microsurgical and endoscopic anatomy of ethmoidal arteries and possible safe clipping sites is a prerequisite for proper selection of the surgical approach and surgical planning and safe execution of complete removal. The success of surgery substantially depends on the surgeon’s intelligent choice of a familiar approach for a particular tumor site and blood supply. Unnecessarily occluding bridging and drainage veins might be catastrophic. The posterior ethmoidal artery arises from the proximal first segment of the ophthalmic artery. Arising from the distal intraorbital third segment of the ophthalmic artery, the anterior ethmoidal arteries penetrate the lamina papyracea, into the roof of the ethmoid sinuses where it gives off its dorsal nasal artery and through the cribriform plate close to the crista galli to the intracranial opening of the anterior ethmoidal canal to form the anterior falx artery (14). In a cadaver study (3), the anterior ethmoidal foramen was about 32 mm to the right of the middle point of the nasofrontal suture and 34 mm to the left. It was 12.3 mm anterior to the posterior foramen, which was 7.1 mm more anterior to the distal opening of the right optic canal and 7.3 mm on the left. In an anatomic endoscopic study (1), the posterior ethmoidal artery was a mean 11.08 mm (range, 8e16 mm) anterior to the optic canal, whereas the anterior ethmoidal artery was a mean 13 mm (range, 10e17 mm) more anterior to the posterior ethmoidal artery. It was mainly found between the superior and middle lamellae (1, 3). In an endoscopic study in Chinese adults, the distance from the columella to the anterior ethmoidal artery measured 62.71 mm 2.18 on the right side and 63.38 mm 1.69 on the left. The distance between the columella and the posterior ethmoidal artery was 70.91 mm 1.99 on the right and 71.79 mm 1.95 on the left (10). The right posterior ethmoidal artery diameter was 0.66 mm 0.21, and the left posterior ethmoidal artery diameter was 0.63 mm 0.19. The anterior ethmoidal arteries were generally thicker than the posterior ethmoidal artery (0.92 mm 0.2 on the right and 0.88 mm 0.15 on the left) (8). In another study, the diameter of the anterior ethmoidal artery was 6e10 mm (32). The anterior ethmoidal artery runs between the second and third lamellae (where it is identified endoscopically at least in 90% of cases) or through the suprabulbar recess to the anterior ethmoidal canal with the anterior ethmoidal nerves and veins (8, 22, 27, 32). The anterior ethmoidal arteries are always single. They were absent in 2 of 30 sides. In such cases, the posterior ethmoidal arteries ran anteriorly and interiorly divided through the crista galli suture to supply the anterior ethmoidal territory. The persistently present anterior ethmoidal canal was 7e10 mm in length and was dehiscent in its proximal or distal part in one third of cases.
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During endoscopic exposure, the surgeon may localize the artery parallel to the ethmoid sinus roof, as it curves along the cribriform plate posterolateral to anteromedial at an angle of 60 to the lamina papyracea. It may be found in the roof of the frontal recess or the roof of the posterior ethmoid sinus in a few cases. A 30 rigid endoscope is preferred for clipping or a curved Ligaclip with 0 scope. It is more accessible in a well-pneumatized sinus (32). It is recommended to assess ethmoid pneumatization by CT to decrease the risk of injuring the artery (27). Minimally invasive extended endonasal approaches allow early control of the feeding ethmoidal arteries. However, these endoscopic approaches are demanding and require sharpened surgical skill and an adequate learning curve to minimize postoperative complications (9). Visualization of the lamina papyracea in the medial orbital wall allows the anterior ethmoidal foramina and canal to be identified for safe early coagulation and division of the anterior ethmoidal arteries extracranially. The anterior ethmoidal artery is sought posterior to the anterior face of the ethmoidal bulla. The smaller posterior ethmoidal artery is looked for at the junction of the roof of the sphenoid and posterior ethmoid sinus. White et al. (31) recognized 3 safe sites for control of the anterior ethmoidal artery before resection in the presence of a vascular anterior skull base lesion through a single flap fronto-orbital craniotomy instead of the classic pterional or subfrontal approaches: 1) the anterior ethmoidal foramen at the lamina papyracea of the medial orbital wall, 2) the anterior ethmoid canal at the lateral ethmoid wall, and 3) intracranial extradural at the cribriform plate. The open lamina papyracea clipping site was previously described in a bicoronal intracranial extradural approach (16). Extracranial open bilateral anterior and posterior ethmoidal artery ligation may be performed through Lynch incision exposure down to the periosteum of the medial orbital walls. The frontoethmoidal suture is followed bluntly for about 22 mm posterior to the lacrimal crest, and the posterior ethmoidal artery is encountered about 15 mm posterior to the anterior ethmoidal artery (14). The extracranial transcaruncular approach entails an incision just lateral to the caruncle, identifying the lacrimal fossa and following the avascular facial plans posteromedially to the frontoethmoidal suture. The periosteum is incised bilaterally to allow a posterior subperiosteal dissection trajectory to the anterior ethmoidal arteries. In a paper recently published in WORLD NEUROSURGERY, the authors reviewed microsurgical anatomy literature pertinent to extracranial ligation of the anterior and posterior ethmoidal arteries and identified 2 possible control sites. They applied their findings in 5 approaches during exposure of anterior cranial fossa basal meningiomas. The results apply to an endoscopic rather than an open approach, although both may be used interchangeably (26). Early arterial ligation is an added advantage in endoscopic transnasal approaches to anterior skull base meningiomas (29). The frontal recess, the anterior ethmoidal artery, and the posterior ethmoidal artery were suggested as constant landmarks in the extended endoscopic transnasal approach to the anterior skull base (32). The authors preferred endoscopic approaches, which are more amenable to small or medium-sized lesions at the present stage of surgical expertise. Schroeder (24) found no advantage of an endoscopic approach over craniotomy in surgery of small or
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medium-sized olfactory groove, planum sphenoidale, and tuberculum sellae meningiomas compared with the eyebrow approach because the trauma to the nasal cavity, paranasal sinuses, and skull base is greater, and there is increased risk of cerebrospinal fluid (CSF) leak. Discussion about the merits of the authors’ findings is warranted in relation to different approaches and how the authors’ technique can be implemented in each individual case. Experience shall illustrate how frequently visual compromise might be encountered using the authors’ suggested open microsurgical technique compared with currently practiced endovascular, endonasal endoscopic or transcranial approaches. The direct anatomic endoscopic approach avoids traversing significant neurovascular structures, obviating consequences of brain retraction. Proper understanding of the endoscopic anatomy of anterior ethmoidal arteries is a prerequisite for endoscopic clipping of these arteries during endonasal resection or as preoperative preparation of an intracranial approach. An extra-axial midline anterior skull base tumor such as a meningioma expands upward and laterally, displacing important midline structures away from the base and creating a safe natural corridor for their endoscopic resection through an extended endonasal approach. Limited working space through the endoscopic dural opening and the difficulty of attaining proper repair with CSF leak and possible infective complications or tension pneumocephalus limits widespread application of endoscopic minimally invasive procedures. Supporters claim lower mortality and morbidity compared with transcranial routes with equal surgical resectability. Staged and redo extended endonasal resections may be considered to handle large or huge lesions (5). The posterior ethmoidal artery is more vulnerable during exposure for planum sphenoidale meningiomas, whereas the anterior and the posterior ethmoidal arteries are at risk approaching olfactory groove meningiomas. Preoperative radiologic visualization of the anterior ethmoidal arteries is feasible with noninvasive coronal CT angiography. Supraorbital pneumatization facilitates CT visualization of the course and ensures easier clipping but increases the risk of iatrogenic injury of the anterior ethmoidal artery. The anterior ethmoidal canal may be identified in 40%, the anterior ethmoidal sulcus is clearly identified in 98%, and the bony anterior ethmoidal foramen is evident in 100% of CT angiographies (28). The anterior ethmoidal foramen appears as a notch of the medial wall of the orbit, whereas the anterior ethmoidal groove displays a focal funneling in the olfactory fossa. Endoscopic closure with a vascularized nasoseptal flap decreases CSF leak (30). Proper clipping of the anterior ethmoidal arteries avoids retraction and intraorbital hematoma that may predispose to ophthalmologic complications. Most ethmoidal foramina (78%) are situated along the frontoethmoidal suture; 22% are within 6 mm. An equal percentage of posterior ethmoidal foramina (78%) is
REFERENCES 1. Abuzayed B, Tanriover N, Gazioglu N, Sanus GZ, Ozlen F, Biceroglu H, Kafadar AM, Eraslan BS, Akar Z: Endoscopic endonasal anatomy and approaches to the anterior skull base: a
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along the suture, and 4% are outside it, again within 6 mm. An accessory ethmoidal foramen was identified in 26% of studied orbits (10). The mean distances between the frontoethmoidal suture and the anterior ethmoid foramen, the posterior ethmoid foramen, and the accessory foramen—when present—were 2.1 mm 0.5, 2.0 mm 1.5, and 2.3 mm 1.2. The distances from the suture to the anterior ethmoidal, posterior ethmoidal, and accessory ethmoidal foramina were 1.2 to 3.32 mm, 1.02 to 5.76 mm, and 1.1 to 3.65 mm. An angled 30 Ligaclip allows adequate visualization of the anterior ethmoidal artery during clipping, rather than a straight Ligaclip if a 0 endoscope is used. It is recommended to clip the artery in the orbit rather than at the ethmoidal roof because of the closeness of the artery to the cranial base, which was <5 mm in 90% of cases (2). Al-Mefty preferred the endoscopic approach for olfactory groove meningioma because it allows early control of the ethmoidal arteries. He cautioned surgeons to expect difficulty in large tumors that reach the planum or the tuberculum, and he advised careful dissection of the adherent carotid complex vasculature (6). Other authors preferred transcranial approaches, such as the pterional approach (4). They stressed its advantage for early identification of the posterior carotid vascular complex and the adjacent optic apparatus, frontal sinus conservation, less brain retraction, and familiarity to most neurosurgeons. Kleiber et al. (12) preferred the minimally invasive transglabellar approach through an inter-eyebrow incision and a 3-cm bone flap in the frontal sinus to expose the midline skull base in 24 totally removed meningiomas with 12.5% incidence of CSF leak and 4% incidence of meningitis. These authors did not discuss in detail how they handled the anterior ethmoidal artery in vascular lesions. In conclusion, the ethmoidal arteries may be controlled via an intracranial or extracranial approach, in the orbit or in the ethmoidal roof through microsurgical or endoscopic approaches rather than endovascular embolization, which carries a remote risk of spilling embolic material onto the ophthalmic arteries. A thorough knowledge of the microsurgical and endoscopic anatomy of ethmoidal arteries and possible safe clipping sites is a prerequisite for proper selection of the surgical approach and surgical planning as well as safe execution of complete removal of vascular anterior skull base meningiomas. The success of surgery substantially depends on the surgeon’s intelligent choice of a familiar approach for a particular tumor site and blood supply based on adequate radiologic evaluation. Unnecessarily occluding bridging and drainage veins might be catastrophic. Hypertrophied ethmoidal vessels passing through sclerosed basal foramina are difficult to control early in a transcranial approach or through the ethmoid sinus roof in endoscopic exposures at the skull base. These vessels instead may be approached extracranially in the orbit away from the thickened sclerosed tumor or infiltrated invaded skull base.
neurosurgeon’s viewpoint. J Craniofac Surg 21: 529-537, 2010.
study [in Portuguese]. Braz J Otorhinolaryngol 77: 33-38, 2011.
2. Araujo Filho BC, Pinheiro-Neto CD, Ramos HF, Voegels RL, Sennes LU: Endoscopic ligation of the anterior ethmoidal artery: a cadaver dissection
3. Avcı E, Aktüre E, Seçkin H, Uluç K, Bauer AM, Izci Y, Morcos JJ, Bas¸kaya MK: Level I to III craniofacial approaches based on Barrow
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PERSPECTIVES
classification for treatment of skull base meningiomas: surgical technique, microsurgical anatomy, and case illustrations. Neurosurg Focus 30: E5, 2011.
giant olfactory groove or planum sphenoidale meningiomas: 3 illustrative cases with a review of the literature on surgical techniques. Neurosurg Focus 35:E13, 2013.
25. Schulz C, Mathieu R, Kunz U, Mauer UM: Treatment of unresectable skull base meningiomas with somatostatin analogs. Neurosurg Focus 30: E11, 2011.
4. Bitter AD, Stavrinou LC, Ntoulias G, Petridis AK, Dukagjin M, Scholz M, Hassler W: The role of the pterional approach in the surgical treatment of olfactory groove meningiomas: a 20-year experience. J Neurol Surg B Skull Base 74:97-102, 2013.
15. Manjunath KY: Anomalous origin of the middle meningeal artery—a review. J Anat Soc India 50: 179-183, 2001.
26. Sekhar LN, Tariq F, Ferreira M: What is the best approach to resect an anterior midline skull base meningioma in 2011? Microsurgical transcranial, endonasal endoscopic, or minimal access cranial? World Neurosurg 77:621-622, 2012.
5. Cavallo M, Messina A, Cappabianca P, Esposito F, de Divitiis E, Gardner P, Tschabitscher M: Endoscopic endonasal surgery of the midline skull base: anatomical study and clinical considerations. Neurosurg Focus 19:E2, 2005. 6. De Monte F, McDermott MW, Al-Mefty O, eds. Al-Mefty’s Meningiomas. 2nd ed. New York: Thieme Medical Publishers; 2011. 7. Dowd CF, Halbach VV, Higashida RT: Meningiomas: the role of preoperative angiography and embolization. Neurosurg Focus 15:E10, 2003. 8. Erdogmus S, Govsa F: The anatomic landmarks of ethmoidal arteries for the surgical approaches. J Craniofac Surg 17:280-285, 2006. 9. Honig S, Trantakis C, Frerich B, Sterker I, Kortmann RD, Meixensberger J: Meningiomas involving the sphenoid wing outcome after microsurgical treatment—a clinical review of 73 cases. Cent Eur Neurosurg 71:189-198, 2010. 10. Kazak Z, Celik S, Ozer MO, Govsa F: Threedimensional evaluation of the danger zone of ethmoidal foramens on the frontoethmoidal suture line on the medial orbital wall. Surg Radiol Anat 25:218-223, 2015. 11. Kimball D, Kimball H, Tubbs RS, Lukas M: Variant middle meningeal artery origin from the ophthalmic artery: a case report. Surg Radiol Anat 37:105-108, 2015. 12. Kleiber JC, Roemer S, Duntze J, Eap C, Theret E, Rousseaux P, Litre F: Transglabellar approach for resection of anterior midline skull base meningiomas: technical note. Acta Neurochir (Wien) 156: 2283-2287, 2014. 13. Liu Q, Rhoton AL Jr: Middle meningeal origin of the ophthalmic artery. Neurosurgery 49:401-406; discussion 406-407 2001. 14. Manjila S, Cox EM, Smith GA, Corriveau M, Chhabra N, Johnson F, Geertman RT: Extracranial ligation of ethmoidal arteries before resection of
16. McDermott MW, Rootman J, Durity FA: Subperiosteal, subperiorbital dissection and division of the anterior and posterior ethmoid arteries for meningiomas of the cribriform plate and planum sphenoidale: technical note. Neurosurgery 36: 1215-1219, 1995. 17. Nanda A, Jawahar A, Sathyanarayana S: Microsurgery for potential radiosurgical skull base lesions: a retrospective analysis and comparison of results. Skull Base 13:131-138, 2003. 18. Nania A, Granata F, Vinci S, Pitrone A, Barresi V, Morabito R, Settineri N, Tomasello F, Alafaci C, Longo M: Necrosis score, surgical time, and transfused blood volume in patients treated with preoperative embolization of intracranial meningiomas. Analysis of a single-centre experience and a review of literature. Clin Neuroradiol 24:29-36, 2013. 19. Newton HB: Hydroxyurea chemotherapy in the treatment of meningiomas. Neurosurg Focus 23: E11, 2007. 20. Norden AD, Drappatz J, Wen PY: Advances in meningioma therapy. Curr Neurol Neurosci Rep 9:231-240, 2009. 21. Perrini P, Cardia A, Fraser K, Lanzino G: A microsurgical study of the anatomy and course of the ophthalmic artery and its possibly dangerous anastomoses. J Neurosurg 106:142-150, 2007. 22. Raper MS, Starke RM, Henderson F, Ding D, Simon S, Evans AJ, Jane AJ, Liu KC: Preoperative embolization of intracranial meningiomas: efficacy, technical considerations, and complications. AJNR Am J Neuroradiol 35:1798-1804, 2014. 23. Rockhill J, Mrugala M, Chamberlain MC: Intracranial meningiomas: an overview of diagnosis and treatment. Neurosurg Focus 23:E1, 2007. 24. Schroeder HW: Indications and limitations of the endoscopic endonasal approach for anterior cranial base meningiomas. World Neurosurg 82(6 Suppl):S81-S85, 2014.
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27. Simmen D, Raghavan U, Briner HR, Manestar M, Schuknecht B, Groscurth P, Jones NS: The surgeon’s view of the anterior ethmoid artery. Clin Otolaryngol 31:187-191, 2006. 28. Souza SA, de Souza MM, Gregório LC, Ajzen S: Anterior ethmoidal artery evaluation on coronal CT scans. Braz J Otorhinolaryngol 75:101-106, 2009. 29. Ung TH, Waziri AE, Ramakrishnan VR: Preoperative ethmoid artery ligation facilitates resection of large sub-frontal meningiomas. Am J Otolaryngol 35:424-426, 2014. 30. Verillaud B, Bresson D, Sauvaget E, Mandonnet E, Georges B, Kania R, Herman P: Transcribriform and transplanum endoscopic approach for skullbase tumors. Eur Ann Otorhinolaryngol Head Neck Dis 130:233-236, 2013. 31. White DV, Sincoff EH, Abdulrauf SI: Anterior ethmoidal artery: microsurgical anatomy and technical considerations. Neurosurgery 56(2 Suppl): 406-410, 2005. 32. Yang YX, Lu QK, Liao JC, Dang RS: Morphological characteristics of the anterior ethmoidal artery in ethmoid roof and endoscopic localization. Skull Base 19:311-317, 2009. 33. Zong Y, Li X, Jiang Y, Xu J, Li J: Transnasal approach to the anterior skull base: an endoscopic anatomic study. J Craniofac Surg 25:1041-1043, 2014.
Citation: World Neurosurg. (2015) 84, 6:1532-1535. http://dx.doi.org/10.1016/j.wneu.2015.07.029 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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