Literature Reviews
Anterior and Posterior Ethmoidal Artery Ligation in Anterior Skull Base Meningiomas: A Review on Microsurgical Approaches Cecchini Giulio
Key words Anterior skull base meningioma - Arterial ligation - Meningioma - Olfactory groove meningioma -
Abbreviations and Acronyms AEA: Anterior ethmoidal artery ECA: External carotid artery ICA: Internal carotid artery MMA: Middle meningeal artery PEA: Posterior ethmoidal artery Departments of Neurology and Neuropsychiatry Sciences, University of Bari and University of Marche, Bari, Italy To whom correspondence should be addressed: Cecchini Giulio, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.06.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
INTRODUCTION Anterior skull base neurosurgical lesions are mainly represented by meningiomas (20). Resection of these highly vascular benign neoplasms is often complicated by significant blood loss. In meningiomas of the olfactory groove and planum sphenoidale, the vascularity is derived from dural, transosseous, and pial supply, the former being most conspicuous (15, 20). Arterial feeding, in fact, is derived for the most part from dural branches of internal carotid artery (ICA) including ethmoidal arteries from the ophthalmic branch. Nevertheless, giant anterior skull base meningiomas also receive collaterals from the meningeal branches of the ICA, middle meningeal artery (MMA) with its frontal and sphenoidal branches, and distal maxillary artery with its sphenopalatine branch. Because of all these anastomoses, two facts are derived: 1. Anterior skull base meningioma vascularity is complex and may require
- OBJECTIVE:
Anterior skull base neoplastic and vascular lesions can receive significant blood supply from the anterior and posterior ethmoidal artery. Although useful in preoperative embolization of middle meningeal artery branches, endovascular techniques for the occlusion of anterior ethmoidal artery expose the parent vessel, the ophthalmic artery, to possible embolic complications, which can cause loss of vision. When dealing with anterior fossa giant meningiomas, moreover, it is not always possible to gain direct intracranial access to anterior ethmoidal arteries because of dimensions and invasiveness of these neoplasms. The aim of this review is to illustrate the anterior and posterior ethmoidal artery anatomy and the microsurgical approaches for extracranial ligation.
- METHODS:
We performed a literature review of the relevant microsurgical anatomy of these arteries; particular attention is given to anterior cranial fossa and medial orbital wall anatomy.
- RESULTS:
Our research found two surgical sites of arterial occlusion that can be best exposed with five microsurgical approaches.
- CONCLUSIONS:
A combination of different surgical and endovascular techniques before resection of hypervascular giant olfactory groove and planum sphenoidale meningiomas should always be considered. Microsurgical extracranial ligation of anterior and sometimes posterior ethmoidal arteries provides a safe and feasible option to limit blood loss during anterior skull base surgery. various surgical techniques to be managed. Arteries that supply the margins of the superior orbital fissure may be recruited to supply tumors in the region including the anterior branch of the MMA, the recurrent meningeal branches of the ophthalmic and lacrimal arteries, the meningeal branches of the ICA, the tentorial branch of the meningohypophyseal trunk, the anterior branch of the inferolateral trunk, and the terminal branches of the internal maxillary artery. 2. The presence of multiple anastomoses puts vision at high risk when endovascular embolization is performed (5, 21, 25). The role of preoperative endovascular embolization remains controversial. It has been shown to reduce intraoperative blood loss, surgery time, and, hence, blood transfusion (6, 19). However, only complete
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
embolization seems to give good results. Moreover, safe embolization is often limited by dangerous anastomoses between external carotid artery (ECA) and ICA branches or an aberrant origin of the MMA from the ophthalmic artery or vice versa. Embolization of anterior ethmoidal artery (AEA) and posterior ethmoidal artery (PEA) is usually dangerous because of possible retrograde migration of particles, which can result in blindness from occlusion of the ophthalmic artery (5). Although not inducing complete de-vascularization of anterior skull base meningiomas, endovascular embolization of the anterior branch of MMA has led to better results (19). In this paper we illustrate microsurgical relevant anatomy of anterior and posterior ethmoidal arteries and microsurgical approaches for extracranial and intracranial ligation. These techniques have become a
www.WORLDNEUROSURGERY.org
1
LITERATURE REVIEWS CECCHINI GIULIO
useful adjunct in reducing vascularization and facilitate removal of a partially embolized anterior skull base meningioma where ECA branches have already been taken down. RELEVANT MICROSURGICAL ANATOMY The ethmoidal arteries originate from the distal ophthalmic artery in the orbit (Figure 1). They arise beneath the superior oblique muscle and then pass medially through the anterior and posterior ethmoidal foramen at the lamina papyracea of the medial orbital wall to enter the ethmoid sinus and travel respectively in the anterior and posterior ethmoidal canals to reach the dura besides the cribriform plate (15, 16). After passing through the anterior ethmoidal foramen together with the anterior ethmoidal nerve, the AEA runs in the roof of the ethmoidal sinus and crosses the floor of the anterior cranial fossa near the cribriform plate giving rise to the anterior falx artery (see Figure 1). The PEA crosses the cribriform plate near its posterior edge, a few millimeters anterior to the orbital end of the optic canal.
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
When passing through the anterior and posterior ethmoidal canals in the lateral wall and in the roof of the ethmoid sinus, the AEA and the PEA usually travel in a bony canal, requiring careful bone removal to endoscopically expose, identify, and control the vessels (29). The most relevant microsurgical landmarks when dealing with AEA are located in the lamina papyracea of the medial orbital wall (Figure 2). Understanding the bony medial orbital wall anatomy is the first step in successfully choosing and performing the orbital approach. In three of the four orbital walls, bones are arranged in pairs, with the exception of the medial wall. This wall is, in fact, composed by sphenoid, lacrimal, ethmoid bones, and the frontal process of the maxilla. The largest component of the medial wall is the orbital plate of the ethmoid bone, which articulates superiorly with the medial edge of the orbital plate of the frontal bone. The articulation between these plates forms the anterior and posterior ethmoidal canals (see Figure 2). These canals help dividing the orbital area into bulbar, retrobulbar, and apical parts. The orbital plate of the ethmoid bone is the thinnest
Figure 1. A posterosuperior intraorbital view of the bulb, optic nerve, ophthalmic artery, and ethmoidal arteries passing through the anterior and posterior ethmoidal canal to reach the cribriform plate and enter the anterior falx.
2
www.SCIENCEDIRECT.com
part of the orbit (0.2e0.4 mm) and is called lamina papyracea. The major microsurgical landmark here is the lacrimal crest, the anterior demarcation of the nasolacrimal duct (see Figure 2) (8, 16, 22). The “rule of seven” can be useful to remember the location of the foramen in the medial orbital wall: the anterior ethmoidal canal is on average 21 mm posterior to the lacrimal crest or to the medial orbital ridge, the posterior ethmoidal canal is about 14 mm posterior to the anterior canal, and the optic canal is on average 7 mm posterior to the posterior canal (see Figure 2) (16). There is considerable variability among these foramen: In a series of cadavers, the anterior ethmoid foramen was found to be absent in 16% of cases, whereas the posterior ethmoid foramen was multiple in 30%. Nevertheless, the anterior ethmoid foramen has never been found below the fronto-ethmoid suture (7, 12). MICROSURGICAL APPROACHES TO ETHMOIDAL ARTERIES A review of the available literature on the topic has been carried out, with the aim to identify the best surgical approaches to perform preoperative microsurgical occlusion of AEA and PEA. A Medline search was conducted using the key words “anterior ethmoidal artery” and “posterior ethmoidal artery,” yielding 89 articles; additionally, reference lists of recent publications cited another 5 papers on the topic. Certain inclusion criteria were set arbitrarily in order to review papers dealing with microsurgical techniques of ethmoidal artery identification and occlusion. Only reports written in English were considered. Our research has finally selected two surgical sites of arterial occlusion that can be best exposed through five microsurgical approaches (Table 1). The medial orbital wall with its ethmoidal foramen is the first surgical site. Exposure can be obtained by a Lynch approach, transcaruncular approach, or subperiostal subperiorbital dissection after a bicoronal flap. The cribriform plate is the second surgical site, and a subfrontal extradural corridor or subfrontal intradural approach brings it into view. Both techniques can
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.06.005
LITERATURE REVIEWS CECCHINI GIULIO
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
Figure 2. The medial wall of the orbit. The frontoethmoidal suture guides the subperiorbital dissection to the anterior and posterior ethmoidal foramen. The main bony landmarks are highlighted.
be performed through a number of craniotomies. The indications to choose the first or the second surgical site are not the same. Exposure of the Medial Orbital Wall The skull base surgeon should be familiar with orbital surgery. Extracranial surgical access to the AEA and PEA can be difficult to obtain, and methods to approaching them have undergone numerous iterations, both surgical and endoscopic (11).
The first way to expose the medial orbital wall is the Lynch approach. Traditionally, R. C. Lynch described this approach in 1921 (13). A vertical incision of about 3 cm is performed about midway between the medial orbital canthus and nasal bridge. Dissection is carried out medial to the medial canthal tendon and deep to the lacrimal apparatus, following the medial orbital wall and identification of the frontoethmoidal suture line. The identification of this bony landmark is a
key step to follow during dissection. The lower extent of this dissection should always be the lacrimal sac. Once the frontoethmoidal suture is identified, posterior dissection along this line will guide to the AEA at an average distance of 20e25 mm. Scarring is usually minimal, especially if plastic surgery techniques are applied, including a Zplasty (9). The main drawback is represented by possible damage to the lacrimal drainage apparatus. The transcaruncular approach has been described, with different variants, for the treatment of medial orbital wall fractures, medial wall and orbital apex neoplastic lesions, and ligation of ethmoidal arteries (10, 14, 18, 24). The incision is performed on the lateral one third of the caruncle. A thick avascular fibrous tissue is encountered: This is the insertion of the medial palpebral ligament anteromedially, the medial orbital septum and the Horner’s muscle posteromedially, and the Tenon’s capsule laterally. The avascular plane between the Horner muscle (medially) and orbital septum (laterally) leads to the frontoethmoidal suture, the primary landmark for this procedure. Careful lateral retraction of the globe is obtained, and posterior dissection through the medial orbital wall is continued following the frontoethmoidal suture line in a
Table 1. Pros and Cons of Surgical Approaches to the Ligation of Ethmoidal Arteries Anatomic Site
Surgical Approach
Medial orbital wall
Lynch
Time saving No brain retraction Short trajectory
Eyelid scar Risk for orbital hematoma Risk for orbital structure damage
Transcaruncular
No eyelid scar No brain retraction Short trajectory
Risk for orbital hematoma Epiphora Ophthalmic surgery technique Risk for orbital structures damage Learning curve
Subperiosteal Subperiorbital
Familiarity No additional scar Easy AEA occlusion
Risk for infratrochlear and supraorbital nerve damage Risk for orbital hematoma PEA not always visible
Subfrontal extradural
Familiarity No additional scar No orbital access
Brain retraction Only for small lesions Usually incomplete devascularization
Subfrontal intradural
Familiarity No additional scar No orbital access
Brain retraction Usually incomplete devascularization Needs partial debulking
Cribriform plate
Pros
Cons
AEA, anterior ethmoidal artery; PEA, posterior ethmoidal artery.
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
www.WORLDNEUROSURGERY.org
3
LITERATURE REVIEWS CECCHINI GIULIO
subperiorbital fashion, until AEA is encountered at a distance of about 20e25 mm from the lacrimal crest. Gentle lateral retraction and deeper posterior dissection leads to the exposure of the PEA after about another 14 mm. This is a more demanding procedure because of the small caliber of the vessel and, most important, the proximity of the orbital apex. Caruncule closure is obtained using 5-0 or 6-0 Vicryl sutures. The bicoronal flap, which is more familiar to neurosurgeons, may be extended caudally over the superior orbital rim (28). Two main points must be considered when performing this approach: First, the supraorbital nerve has to be freed from its notch; frequent ossification of the notch leads to the presence of a supraorbital canal, in which the nerve passes (4). To preserve this sensitive nerve, a small craniotomy can be performed or gentle careful removal of the anterior wall of the supraorbital canal can be obtained by using a high-speed drill or a small rongeur (3). Second, the periorbita is thinner than the periosteum, requiring a careful dissection, in particular at the anterior orbital rim (16). Exposure of the Cribriform Plate The exposure of the ethmoidal arteries at the cribriform plate is more familiar to brain surgeons than the orbital approaches, but it is not always possible to achieve. Numerous craniotomies have been described to accomplish a subfrontal approach: Frontal unilateral, frontal bilateral, pterional trans-sylvian, fronto-orbital unilateral, and fronto-orbital bilateral are among the most commonly used (1, 2, 20). Subfrontal approaches to ethmoidal arteries can be easily achieved only when dealing with relatively small lesions. We feel that performing a single-piece craniotomy or retracting posteriorly the frontal lobes with a giant anterior skull base meningioma could lead to significant brain damage due to manipulation before reaching the ethmoidal vessels. The standard approach has been represented by the subfrontal intradural access, with the argument that adequate proximal exposure of AEA can only be obtained by resecting the inferior part of the lesion and coagulating the feeding vessels above the
4
www.SCIENCEDIRECT.com
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
cribriform plate. With this technique, obviously, we do not devascularize the tumor before reaching it but after partial debulking. DISCUSSION When dealing with highly vascular meningiomas, the surgeon should always try to interrupt blood supply as early as possible. This can be relatively easy with convexity meningioma. In the case of cribriform plate or olfactory groove meningiomas, access to the main arterial supply may require entering in a different anatomic compartment: the orbit. The AEA and PEA exposure at the cribriform plate is not always possible because of the dimensions of these neoplasms. Exposure at the medial orbital wall is, in case of giant meningiomas, a safe and relatively simple procedure. It adds about 20 minutes to be achieved bilaterally. Few papers have focused on this topic, and in almost all cases preoperative microsurgical extracranial AEA and PEA closure is suggested (17, 27, 28). On the other hand, endoscopic occlusion of AEA at the anterior ethmoidal canal through an endonasal approach is less versatile and not always feasible (14, 29). In my opinion, this kind of approach is technically demanding because of multiple arterial and osseous variations and generally requires specific endoscopic endonasal skills (23). Preoperative imaging can be useful in defining surgical planning. Digital subtraction angiography (DSA) clarifies the whole vasculature of the lesion and can help with endovascular closure of MMA branches. Its invasive nature, however, may limit its clinical application. Because of the abundant anastomoses among AEA, PEA, and collateral branches from MMA and ICA, endovascular embolization puts the ophthalmic artery and vision at risk (5, 15, 25). When using computed tomography scan, identification of AEA can be achieved indirectly through bony landmarks, in particular coronal reconstructions (7, 26). Limits of extracranial microsurgical closure of AEA and PEA at the medial orbital wall are represented by possible orbital complications: Extreme care should be taken when dissecting periorbita to avoid damaging the lacrimal
apparatus and trochlea of the superior oblique muscle. Into the orbit, if coagulation is used, it should be bipolar, not monopolar. Caution must be applied to carefully secure AEA during ligation to prevent vessel retraction into the periorbita with possible hematoma and subsequent visual compromise. Experience shall illustrate how frequent visual compromise might be encountered using the open microsurgical techniques compared with currently practiced endovascular, endonasal endoscopic, or transcranial approaches. CONCLUSIONS Extracranial microsurgical closure of AEA and PEA may be helpful for large meningiomas of the anterior skull base that have a documented blood supply from these arteries. During preoperative planning, multiple techniques should be considered to reduce the arterial supply: endovascular, endoscopic, and microsurgical and, among them, extracranial and intracranial. Extracranial techniques require an accurate knowledge of orbital anatomy and microsurgical landmarks. Preoperative planning is the key factor to achieve a good final result. In expert hands, the techniques described could be useful and timesaving. REFERENCES 1. Adappa ND, Lee JYK, Chiu AG, Palmer JN: Olfactory groove meningioma. Otolaryngol Clin North Am 44:965-980; ix, 2011. 2. Alexiou GA, Gogou P, Markoula S, Kyritsis AP: Management of meningiomas. Clin Neurol Neurosurg 112:177-182, 2010. 3. Al-Mefty O: Supraorbital-pterional approach to skull base lesions. Neurosurgery 21:474-477, 1987. 4. Barker L, Naveed H, Adds PJ, Uddin JM: Supraorbital notch and foramen: positional variation and relevance to direct brow lift. Ophthal Plast Reconstr Surg 29:e67-e70, 2013. 5. Bendszus M, Monoranu CM, Schütz A, Nölte I, Vince GH, Solymosi L: Neurologic complications after particle embolization of intracranial meningiomas. AJNR Am J Neuroradiol 26:1413-1419, 2005. 6. Bendszus M, Rao G, Burger R, Schaller C, Scheinemann K, Warmuth-Metz M, Hofmann E, Schramm J, Roosen K, Solymosi L: Is there a benefit of preoperative meningioma embolization? Neurosurgery 47:1306-1311; discussion 1311-1312, 2000.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.06.005
LITERATURE REVIEWS CECCHINI GIULIO
7. Ding J, Sun G, Lu Y, Yu B, Li M, Li L, Li G, Peng Z, Zhang X: Evaluation of anterior ethmoidal artery by 320-slice CT angiography with comparison to three-dimensional spin digital subtraction angiography: initial experiences. Korean J Radiol 13:667-673, 2012. 8. Erdogmus S, Govsa F: The anatomic landmarks of ethmoidal arteries for the surgical approaches. J Craniofac Surg 17:280-285, 2006. 9. Esclamado RM, Cummings CW: Z-plasty modification of the Lynch incision. Laryngoscope 99: 986-987, 1989. 10. Graham SM, Thomas RD, Carter KD, Nerad JA: The transcaruncular approach to the medial orbital wall. Laryngoscope 112:986-989, 2002. 11. Harrison DF: Surgical approach to the medial orbital wall. Ann Otol Rhinol Laryngol 90(5 Pt 1): 415-419, 1981. 12. Kirchner JA, Yanagisawa E, Crelin ES: Surgical anatomy of the ethmoidal arteries. A laboratory study of 150 orbits. Arch Otolaryngol 74:382-386, 1961. 13. Lynch RC: The technique of a radical frantal sinus operation which has given me the best results. Laryngoscope 31:1-5, 1921. 14. Manjila S, Cox EM, Smith GA, Corriveau M, Chhabra N, Johnson F, Geertman RT: Extracranial ligation of ethmoidal arteries before resection of giant olfactory groove or planum sphenoidale meningiomas: 3 illustrative cases with a review of the literature on surgical techniques. Neurosurg Focus 35:E13, 2013.
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
the dural arteries. Neurosurgery 56 (2 Suppl): 211-251, 2005.
role of preoperative embolization in meningioma management. Neurosurg Focus 35:E17, 2013.
17. 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: 1215-1218; discussion 1218-1219, 1995.
26. Souza SA, Souza MM, Gregório LC, Ajzen S: Anterior ethmoidal artery evaluation on coronal CT scans. Braz J Otorhinolaryngol 75:101-106, 2009.
18. Morera E, Artigas C, Ferrán L, Ferrén L, Trobat F, Tomás M: Transcaruncular electrocoagulation of anterior ethmoidal artery for the treatment of severe epistaxis. Laryngoscope 121:446-450, 2011. 19. 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, 2014. 20. Ojemann R: Meningiomas. Neurosurg Clin N Am 1:181-197, 1990. 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. Rhoton AL: The anterior and middle cranial base. Neurosurgery 51 (4 Suppl):S273-S302, 2002. 23. Schroeder HW: Indications and limitations of the endoscopic endonasal approach for anterior cranial base meningiomas. World Neurosurg 82 (6 Suppl):S81-S85, 2014.
15. Martins C, Costa E Silva IE, Campero A, Yasuda A, Aguiar LR, Tatagiba M, Rhoton A: Microsurgical anatomy of the orbit: the rule of seven. Anat Res Int 2011:468727, 2011.
24. Shorr N, Baylis HI, Goldberg RA, Perry JD: Transcaruncular approach to the medial orbit and orbital apex. Ophthalmology 107:1459-1463, 2000.
16. Martins C, Yasuda A, Campero A, Ulm AJ, Tanriover N, Rhoton A: Microsurgical anatomy of
25. Singla A, Deshaies EM, Melnyk V, Toshkezi G, Swarnkar A, Choi H, Chin LS: Controversies in the
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
27. Ung TH, Waziri AE, Ramakrishnan VR: Preoperative ethmoid artery ligation facilitates resection of large sub-frontal meningiomas. Am J Otolaryngol 35:424-426, 2014.
28. White DV, Sincoff EH, Abdulrauf SI: Anterior ethmoidal artery: microsurgical anatomy and technical considerations. Neurosurgery 56 (2 Suppl):406-410; discussion 406-410, 2005.
29. Yang Y-X, Lu Q-K, Liao J-C, Dang R-S: Morphological characteristics of the anterior ethmoidal artery in ethmoid roof and endoscopic localization. Skull Base 19:311-317, 2009.
Conflict of interest statement: The manuscript comprises original unpublished work and is not under consideration for publication elsewhere. The author declares that he has no competing interests or financial and personal relationship that may bias this work. No funding has been received for this work. Received 30 April 2015; accepted 3 June 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.06.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
5
Anterior and Posterior Ethmoidal Artery Ligation in Anterior Skull Base Meningiomas: A Review on Microsurgical Approaches Cecchini Giulio
Key words Anterior skull base meningioma - Arterial ligation - Meningioma - Olfactory groove meningioma -
Abbreviations and Acronyms AEA: Anterior ethmoidal artery ECA: External carotid artery ICA: Internal carotid artery MMA: Middle meningeal artery PEA: Posterior ethmoidal artery Departments of Neurology and Neuropsychiatry Sciences, University of Bari and University of Marche, Bari, Italy To whom correspondence should be addressed: Cecchini Giulio, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.06.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
INTRODUCTION Anterior skull base neurosurgical lesions are mainly represented by meningiomas (20). Resection of these highly vascular benign neoplasms is often complicated by significant blood loss. In meningiomas of the olfactory groove and planum sphenoidale, the vascularity is derived from dural, transosseous, and pial supply, the former being most conspicuous (15, 20). Arterial feeding, in fact, is derived for the most part from dural branches of internal carotid artery (ICA) including ethmoidal arteries from the ophthalmic branch. Nevertheless, giant anterior skull base meningiomas also receive collaterals from the meningeal branches of the ICA, middle meningeal artery (MMA) with its frontal and sphenoidal branches, and distal maxillary artery with its sphenopalatine branch. Because of all these anastomoses, two facts are derived: 1. Anterior skull base meningioma vascularity is complex and may require
- OBJECTIVE:
Anterior skull base neoplastic and vascular lesions can receive significant blood supply from the anterior and posterior ethmoidal artery. Although useful in preoperative embolization of middle meningeal artery branches, endovascular techniques for the occlusion of anterior ethmoidal artery expose the parent vessel, the ophthalmic artery, to possible embolic complications, which can cause loss of vision. When dealing with anterior fossa giant meningiomas, moreover, it is not always possible to gain direct intracranial access to anterior ethmoidal arteries because of dimensions and invasiveness of these neoplasms. The aim of this review is to illustrate the anterior and posterior ethmoidal artery anatomy and the microsurgical approaches for extracranial ligation.
- METHODS:
We performed a literature review of the relevant microsurgical anatomy of these arteries; particular attention is given to anterior cranial fossa and medial orbital wall anatomy.
- RESULTS:
Our research found two surgical sites of arterial occlusion that can be best exposed with five microsurgical approaches.
- CONCLUSIONS:
A combination of different surgical and endovascular techniques before resection of hypervascular giant olfactory groove and planum sphenoidale meningiomas should always be considered. Microsurgical extracranial ligation of anterior and sometimes posterior ethmoidal arteries provides a safe and feasible option to limit blood loss during anterior skull base surgery. various surgical techniques to be managed. Arteries that supply the margins of the superior orbital fissure may be recruited to supply tumors in the region including the anterior branch of the MMA, the recurrent meningeal branches of the ophthalmic and lacrimal arteries, the meningeal branches of the ICA, the tentorial branch of the meningohypophyseal trunk, the anterior branch of the inferolateral trunk, and the terminal branches of the internal maxillary artery. 2. The presence of multiple anastomoses puts vision at high risk when endovascular embolization is performed (5, 21, 25). The role of preoperative endovascular embolization remains controversial. It has been shown to reduce intraoperative blood loss, surgery time, and, hence, blood transfusion (6, 19). However, only complete
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
embolization seems to give good results. Moreover, safe embolization is often limited by dangerous anastomoses between external carotid artery (ECA) and ICA branches or an aberrant origin of the MMA from the ophthalmic artery or vice versa. Embolization of anterior ethmoidal artery (AEA) and posterior ethmoidal artery (PEA) is usually dangerous because of possible retrograde migration of particles, which can result in blindness from occlusion of the ophthalmic artery (5). Although not inducing complete de-vascularization of anterior skull base meningiomas, endovascular embolization of the anterior branch of MMA has led to better results (19). In this paper we illustrate microsurgical relevant anatomy of anterior and posterior ethmoidal arteries and microsurgical approaches for extracranial and intracranial ligation. These techniques have become a
www.WORLDNEUROSURGERY.org
1
LITERATURE REVIEWS CECCHINI GIULIO
useful adjunct in reducing vascularization and facilitate removal of a partially embolized anterior skull base meningioma where ECA branches have already been taken down. RELEVANT MICROSURGICAL ANATOMY The ethmoidal arteries originate from the distal ophthalmic artery in the orbit (Figure 1). They arise beneath the superior oblique muscle and then pass medially through the anterior and posterior ethmoidal foramen at the lamina papyracea of the medial orbital wall to enter the ethmoid sinus and travel respectively in the anterior and posterior ethmoidal canals to reach the dura besides the cribriform plate (15, 16). After passing through the anterior ethmoidal foramen together with the anterior ethmoidal nerve, the AEA runs in the roof of the ethmoidal sinus and crosses the floor of the anterior cranial fossa near the cribriform plate giving rise to the anterior falx artery (see Figure 1). The PEA crosses the cribriform plate near its posterior edge, a few millimeters anterior to the orbital end of the optic canal.
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
When passing through the anterior and posterior ethmoidal canals in the lateral wall and in the roof of the ethmoid sinus, the AEA and the PEA usually travel in a bony canal, requiring careful bone removal to endoscopically expose, identify, and control the vessels (29). The most relevant microsurgical landmarks when dealing with AEA are located in the lamina papyracea of the medial orbital wall (Figure 2). Understanding the bony medial orbital wall anatomy is the first step in successfully choosing and performing the orbital approach. In three of the four orbital walls, bones are arranged in pairs, with the exception of the medial wall. This wall is, in fact, composed by sphenoid, lacrimal, ethmoid bones, and the frontal process of the maxilla. The largest component of the medial wall is the orbital plate of the ethmoid bone, which articulates superiorly with the medial edge of the orbital plate of the frontal bone. The articulation between these plates forms the anterior and posterior ethmoidal canals (see Figure 2). These canals help dividing the orbital area into bulbar, retrobulbar, and apical parts. The orbital plate of the ethmoid bone is the thinnest
Figure 1. A posterosuperior intraorbital view of the bulb, optic nerve, ophthalmic artery, and ethmoidal arteries passing through the anterior and posterior ethmoidal canal to reach the cribriform plate and enter the anterior falx.
2
www.SCIENCEDIRECT.com
part of the orbit (0.2e0.4 mm) and is called lamina papyracea. The major microsurgical landmark here is the lacrimal crest, the anterior demarcation of the nasolacrimal duct (see Figure 2) (8, 16, 22). The “rule of seven” can be useful to remember the location of the foramen in the medial orbital wall: the anterior ethmoidal canal is on average 21 mm posterior to the lacrimal crest or to the medial orbital ridge, the posterior ethmoidal canal is about 14 mm posterior to the anterior canal, and the optic canal is on average 7 mm posterior to the posterior canal (see Figure 2) (16). There is considerable variability among these foramen: In a series of cadavers, the anterior ethmoid foramen was found to be absent in 16% of cases, whereas the posterior ethmoid foramen was multiple in 30%. Nevertheless, the anterior ethmoid foramen has never been found below the fronto-ethmoid suture (7, 12). MICROSURGICAL APPROACHES TO ETHMOIDAL ARTERIES A review of the available literature on the topic has been carried out, with the aim to identify the best surgical approaches to perform preoperative microsurgical occlusion of AEA and PEA. A Medline search was conducted using the key words “anterior ethmoidal artery” and “posterior ethmoidal artery,” yielding 89 articles; additionally, reference lists of recent publications cited another 5 papers on the topic. Certain inclusion criteria were set arbitrarily in order to review papers dealing with microsurgical techniques of ethmoidal artery identification and occlusion. Only reports written in English were considered. Our research has finally selected two surgical sites of arterial occlusion that can be best exposed through five microsurgical approaches (Table 1). The medial orbital wall with its ethmoidal foramen is the first surgical site. Exposure can be obtained by a Lynch approach, transcaruncular approach, or subperiostal subperiorbital dissection after a bicoronal flap. The cribriform plate is the second surgical site, and a subfrontal extradural corridor or subfrontal intradural approach brings it into view. Both techniques can
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.06.005
LITERATURE REVIEWS CECCHINI GIULIO
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
Figure 2. The medial wall of the orbit. The frontoethmoidal suture guides the subperiorbital dissection to the anterior and posterior ethmoidal foramen. The main bony landmarks are highlighted.
be performed through a number of craniotomies. The indications to choose the first or the second surgical site are not the same. Exposure of the Medial Orbital Wall The skull base surgeon should be familiar with orbital surgery. Extracranial surgical access to the AEA and PEA can be difficult to obtain, and methods to approaching them have undergone numerous iterations, both surgical and endoscopic (11).
The first way to expose the medial orbital wall is the Lynch approach. Traditionally, R. C. Lynch described this approach in 1921 (13). A vertical incision of about 3 cm is performed about midway between the medial orbital canthus and nasal bridge. Dissection is carried out medial to the medial canthal tendon and deep to the lacrimal apparatus, following the medial orbital wall and identification of the frontoethmoidal suture line. The identification of this bony landmark is a
key step to follow during dissection. The lower extent of this dissection should always be the lacrimal sac. Once the frontoethmoidal suture is identified, posterior dissection along this line will guide to the AEA at an average distance of 20e25 mm. Scarring is usually minimal, especially if plastic surgery techniques are applied, including a Zplasty (9). The main drawback is represented by possible damage to the lacrimal drainage apparatus. The transcaruncular approach has been described, with different variants, for the treatment of medial orbital wall fractures, medial wall and orbital apex neoplastic lesions, and ligation of ethmoidal arteries (10, 14, 18, 24). The incision is performed on the lateral one third of the caruncle. A thick avascular fibrous tissue is encountered: This is the insertion of the medial palpebral ligament anteromedially, the medial orbital septum and the Horner’s muscle posteromedially, and the Tenon’s capsule laterally. The avascular plane between the Horner muscle (medially) and orbital septum (laterally) leads to the frontoethmoidal suture, the primary landmark for this procedure. Careful lateral retraction of the globe is obtained, and posterior dissection through the medial orbital wall is continued following the frontoethmoidal suture line in a
Table 1. Pros and Cons of Surgical Approaches to the Ligation of Ethmoidal Arteries Anatomic Site
Surgical Approach
Medial orbital wall
Lynch
Time saving No brain retraction Short trajectory
Eyelid scar Risk for orbital hematoma Risk for orbital structure damage
Transcaruncular
No eyelid scar No brain retraction Short trajectory
Risk for orbital hematoma Epiphora Ophthalmic surgery technique Risk for orbital structures damage Learning curve
Subperiosteal Subperiorbital
Familiarity No additional scar Easy AEA occlusion
Risk for infratrochlear and supraorbital nerve damage Risk for orbital hematoma PEA not always visible
Subfrontal extradural
Familiarity No additional scar No orbital access
Brain retraction Only for small lesions Usually incomplete devascularization
Subfrontal intradural
Familiarity No additional scar No orbital access
Brain retraction Usually incomplete devascularization Needs partial debulking
Cribriform plate
Pros
Cons
AEA, anterior ethmoidal artery; PEA, posterior ethmoidal artery.
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
www.WORLDNEUROSURGERY.org
3
LITERATURE REVIEWS CECCHINI GIULIO
subperiorbital fashion, until AEA is encountered at a distance of about 20e25 mm from the lacrimal crest. Gentle lateral retraction and deeper posterior dissection leads to the exposure of the PEA after about another 14 mm. This is a more demanding procedure because of the small caliber of the vessel and, most important, the proximity of the orbital apex. Caruncule closure is obtained using 5-0 or 6-0 Vicryl sutures. The bicoronal flap, which is more familiar to neurosurgeons, may be extended caudally over the superior orbital rim (28). Two main points must be considered when performing this approach: First, the supraorbital nerve has to be freed from its notch; frequent ossification of the notch leads to the presence of a supraorbital canal, in which the nerve passes (4). To preserve this sensitive nerve, a small craniotomy can be performed or gentle careful removal of the anterior wall of the supraorbital canal can be obtained by using a high-speed drill or a small rongeur (3). Second, the periorbita is thinner than the periosteum, requiring a careful dissection, in particular at the anterior orbital rim (16). Exposure of the Cribriform Plate The exposure of the ethmoidal arteries at the cribriform plate is more familiar to brain surgeons than the orbital approaches, but it is not always possible to achieve. Numerous craniotomies have been described to accomplish a subfrontal approach: Frontal unilateral, frontal bilateral, pterional trans-sylvian, fronto-orbital unilateral, and fronto-orbital bilateral are among the most commonly used (1, 2, 20). Subfrontal approaches to ethmoidal arteries can be easily achieved only when dealing with relatively small lesions. We feel that performing a single-piece craniotomy or retracting posteriorly the frontal lobes with a giant anterior skull base meningioma could lead to significant brain damage due to manipulation before reaching the ethmoidal vessels. The standard approach has been represented by the subfrontal intradural access, with the argument that adequate proximal exposure of AEA can only be obtained by resecting the inferior part of the lesion and coagulating the feeding vessels above the
4
www.SCIENCEDIRECT.com
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
cribriform plate. With this technique, obviously, we do not devascularize the tumor before reaching it but after partial debulking. DISCUSSION When dealing with highly vascular meningiomas, the surgeon should always try to interrupt blood supply as early as possible. This can be relatively easy with convexity meningioma. In the case of cribriform plate or olfactory groove meningiomas, access to the main arterial supply may require entering in a different anatomic compartment: the orbit. The AEA and PEA exposure at the cribriform plate is not always possible because of the dimensions of these neoplasms. Exposure at the medial orbital wall is, in case of giant meningiomas, a safe and relatively simple procedure. It adds about 20 minutes to be achieved bilaterally. Few papers have focused on this topic, and in almost all cases preoperative microsurgical extracranial AEA and PEA closure is suggested (17, 27, 28). On the other hand, endoscopic occlusion of AEA at the anterior ethmoidal canal through an endonasal approach is less versatile and not always feasible (14, 29). In my opinion, this kind of approach is technically demanding because of multiple arterial and osseous variations and generally requires specific endoscopic endonasal skills (23). Preoperative imaging can be useful in defining surgical planning. Digital subtraction angiography (DSA) clarifies the whole vasculature of the lesion and can help with endovascular closure of MMA branches. Its invasive nature, however, may limit its clinical application. Because of the abundant anastomoses among AEA, PEA, and collateral branches from MMA and ICA, endovascular embolization puts the ophthalmic artery and vision at risk (5, 15, 25). When using computed tomography scan, identification of AEA can be achieved indirectly through bony landmarks, in particular coronal reconstructions (7, 26). Limits of extracranial microsurgical closure of AEA and PEA at the medial orbital wall are represented by possible orbital complications: Extreme care should be taken when dissecting periorbita to avoid damaging the lacrimal
apparatus and trochlea of the superior oblique muscle. Into the orbit, if coagulation is used, it should be bipolar, not monopolar. Caution must be applied to carefully secure AEA during ligation to prevent vessel retraction into the periorbita with possible hematoma and subsequent visual compromise. Experience shall illustrate how frequent visual compromise might be encountered using the open microsurgical techniques compared with currently practiced endovascular, endonasal endoscopic, or transcranial approaches. CONCLUSIONS Extracranial microsurgical closure of AEA and PEA may be helpful for large meningiomas of the anterior skull base that have a documented blood supply from these arteries. During preoperative planning, multiple techniques should be considered to reduce the arterial supply: endovascular, endoscopic, and microsurgical and, among them, extracranial and intracranial. Extracranial techniques require an accurate knowledge of orbital anatomy and microsurgical landmarks. Preoperative planning is the key factor to achieve a good final result. In expert hands, the techniques described could be useful and timesaving. REFERENCES 1. Adappa ND, Lee JYK, Chiu AG, Palmer JN: Olfactory groove meningioma. Otolaryngol Clin North Am 44:965-980; ix, 2011. 2. Alexiou GA, Gogou P, Markoula S, Kyritsis AP: Management of meningiomas. Clin Neurol Neurosurg 112:177-182, 2010. 3. Al-Mefty O: Supraorbital-pterional approach to skull base lesions. Neurosurgery 21:474-477, 1987. 4. Barker L, Naveed H, Adds PJ, Uddin JM: Supraorbital notch and foramen: positional variation and relevance to direct brow lift. Ophthal Plast Reconstr Surg 29:e67-e70, 2013. 5. Bendszus M, Monoranu CM, Schütz A, Nölte I, Vince GH, Solymosi L: Neurologic complications after particle embolization of intracranial meningiomas. AJNR Am J Neuroradiol 26:1413-1419, 2005. 6. Bendszus M, Rao G, Burger R, Schaller C, Scheinemann K, Warmuth-Metz M, Hofmann E, Schramm J, Roosen K, Solymosi L: Is there a benefit of preoperative meningioma embolization? Neurosurgery 47:1306-1311; discussion 1311-1312, 2000.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.06.005
LITERATURE REVIEWS CECCHINI GIULIO
7. Ding J, Sun G, Lu Y, Yu B, Li M, Li L, Li G, Peng Z, Zhang X: Evaluation of anterior ethmoidal artery by 320-slice CT angiography with comparison to three-dimensional spin digital subtraction angiography: initial experiences. Korean J Radiol 13:667-673, 2012. 8. Erdogmus S, Govsa F: The anatomic landmarks of ethmoidal arteries for the surgical approaches. J Craniofac Surg 17:280-285, 2006. 9. Esclamado RM, Cummings CW: Z-plasty modification of the Lynch incision. Laryngoscope 99: 986-987, 1989. 10. Graham SM, Thomas RD, Carter KD, Nerad JA: The transcaruncular approach to the medial orbital wall. Laryngoscope 112:986-989, 2002. 11. Harrison DF: Surgical approach to the medial orbital wall. Ann Otol Rhinol Laryngol 90(5 Pt 1): 415-419, 1981. 12. Kirchner JA, Yanagisawa E, Crelin ES: Surgical anatomy of the ethmoidal arteries. A laboratory study of 150 orbits. Arch Otolaryngol 74:382-386, 1961. 13. Lynch RC: The technique of a radical frantal sinus operation which has given me the best results. Laryngoscope 31:1-5, 1921. 14. Manjila S, Cox EM, Smith GA, Corriveau M, Chhabra N, Johnson F, Geertman RT: Extracranial ligation of ethmoidal arteries before resection of giant olfactory groove or planum sphenoidale meningiomas: 3 illustrative cases with a review of the literature on surgical techniques. Neurosurg Focus 35:E13, 2013.
ARTERIAL LIGATION IN ANTERIOR SKULL BASE MENINGIOMA
the dural arteries. Neurosurgery 56 (2 Suppl): 211-251, 2005.
role of preoperative embolization in meningioma management. Neurosurg Focus 35:E17, 2013.
17. 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: 1215-1218; discussion 1218-1219, 1995.
26. Souza SA, Souza MM, Gregório LC, Ajzen S: Anterior ethmoidal artery evaluation on coronal CT scans. Braz J Otorhinolaryngol 75:101-106, 2009.
18. Morera E, Artigas C, Ferrán L, Ferrén L, Trobat F, Tomás M: Transcaruncular electrocoagulation of anterior ethmoidal artery for the treatment of severe epistaxis. Laryngoscope 121:446-450, 2011. 19. 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, 2014. 20. Ojemann R: Meningiomas. Neurosurg Clin N Am 1:181-197, 1990. 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. Rhoton AL: The anterior and middle cranial base. Neurosurgery 51 (4 Suppl):S273-S302, 2002. 23. Schroeder HW: Indications and limitations of the endoscopic endonasal approach for anterior cranial base meningiomas. World Neurosurg 82 (6 Suppl):S81-S85, 2014.
15. Martins C, Costa E Silva IE, Campero A, Yasuda A, Aguiar LR, Tatagiba M, Rhoton A: Microsurgical anatomy of the orbit: the rule of seven. Anat Res Int 2011:468727, 2011.
24. Shorr N, Baylis HI, Goldberg RA, Perry JD: Transcaruncular approach to the medial orbit and orbital apex. Ophthalmology 107:1459-1463, 2000.
16. Martins C, Yasuda A, Campero A, Ulm AJ, Tanriover N, Rhoton A: Microsurgical anatomy of
25. Singla A, Deshaies EM, Melnyk V, Toshkezi G, Swarnkar A, Choi H, Chin LS: Controversies in the
WORLD NEUROSURGERY - [-]: ---, MONTH 2015
27. Ung TH, Waziri AE, Ramakrishnan VR: Preoperative ethmoid artery ligation facilitates resection of large sub-frontal meningiomas. Am J Otolaryngol 35:424-426, 2014.
28. White DV, Sincoff EH, Abdulrauf SI: Anterior ethmoidal artery: microsurgical anatomy and technical considerations. Neurosurgery 56 (2 Suppl):406-410; discussion 406-410, 2005.
29. Yang Y-X, Lu Q-K, Liao J-C, Dang R-S: Morphological characteristics of the anterior ethmoidal artery in ethmoid roof and endoscopic localization. Skull Base 19:311-317, 2009.
Conflict of interest statement: The manuscript comprises original unpublished work and is not under consideration for publication elsewhere. The author declares that he has no competing interests or financial and personal relationship that may bias this work. No funding has been received for this work. Received 30 April 2015; accepted 3 June 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.06.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
5
