Anatomic study and clinical significance of extended endonasal anterior skull base surgery
Correspondence Address: Source of Support: This work was supported by Key Project of Medical Research of Nanjing Military Region, China (NO. 06Z50), Conflict of Interest: None DOI: 10.4103/0028-3886.144451
Source of Support: This work was supported by Key Project of Medical Research of Nanjing Military Region, China (NO. 06Z50), Conflict of Interest: None
Objective: This study is to investigate the anatomical relationship of endonasal approach for anterior skull base surgery, and to determine the boundaries between anterior basicranial craniotomy and the security of operative techniques. Materials and Methods: A total of 10 adult dry skulls and 13 adult cadaveric heads processed by formalin were examined under operating microscope. The micro-anatomic structures of the turbinate, sphenoid sinus, ethmoid sinus, anterior ethmoidal artery, posterior ethmoidal artery and anterior skull base were observed. Artificial anatomy was performed and the deep-seated regions of the surgical approach were observed under operating microscope and endoscope. Results: Examined from the intracranial and intranasal aspects, it was found that the middle turbinate, uncinate process, ethmoid bulla, lamina papyracea, anterior ethmoid canal, posterior ethmoid canal, prominence of the optic canal and opticocarotid recess were all important anatomic landmarks for surgery. The horizontal distances between medial orbital wall on both sides at the level of crista galli, anterior ethmoid canal, and posterior ethmoid canal were (22.31 ± 3.08) mm, (23 ± 2.93) mm, and (26.25 ± 2.88) mm, respectively. The distance between the double optic canal cranial opening was (14.67 ± 3.82) mm. Conclusions: During the endonasal approach for anterior skull base surgery, full advantage of the surgical corridor made by the middle turbinate resection should be taken. To control intraoperative bleeding, it is critical to identify anterior and posterior ethmoidal artery. Identification and protection of medial orbital wall and the optic nerve, and controlling the ranges of anterior basicranial craniotomy are of great importance for surgical safety.
Keywords: Anterior skull base, endonasal approach, ethmoidal artery, microsurgery surgical anatomy
Over the last decade, with the development of extended endonasal approaches, skull base surgery has increased probabilities of resection of a variety of skull base lesions. In 1987, endonasal and transsphenoidal surgery for pituitary adenoma was introduced by Griffith.  Since then, a number of pioneers of endonasal skull base surgeries subsequently emerged and the endonasal approach has greatly developed. For example, the practice of endonasal approach for resection of ethmoidal labyrinths has lasted for one century, and there is certain understanding of anatomical relations about this approach.  When using endonasal approach for anterior skull base surgery, the lamina cribrosa planum sphenoidale or tuberculum sellae is opened. The endonasal approach is mainly used to remove olfactory groove meningiomas and tuberculum sellae meningiomas. Compared with craniotomy, endonasal approach avoids brain retraction and greatly reduces direct injury to intracranial nerves and blood vessels. In recent years, with the continuous progresses of ethmoid sinus anatomy and operation equipment, the researches on expanded endonasal approach for anterior skull base surgery are developing rapidly. According to Casiano et al.,  nasal endoscope assisted endonasal approach surgery can be used to safely handle most cases of olfactory neuroblastoma that invaded anterior skull base. And, the resection area of nasal endoscope-assisted endonasal approach is not less than that of the cranio-facial combined approach. Fernandez Miranda et al., and Liu et al.,applied this approach in the treatment of olfactory groove meningiomas. , Padhye et al.,  successfully removed anterior cranial fossa meningiomas by using this endoscopic endonasal approach. Kassam et al., , managed lesions in midline anterior skull base in children. Patel et al.,  performed a resection of a huge osteoblastoma with nasal endoscope assisted endonasal approach surgery. Lee et al.,  treated tumors in the orbital apex with this approach. Faggin et al.  used endoscopic microsurgery-combined transethmoid operation to treat children with pituitary lesions and achieved good operation effects. They pointed that compared to traditional craniotomy, endonasal approach had distinct advantages of less complications and short hospitalization time.
The anatomical relation of endonasal approach for anterior skull base surgery is complicated and the operation is hard to be managed. As a result, a series of basic scientific observations have been focused on the applied anatomy. ,, However, prevention of bleeding during surgery and delayed postoperative bleeding is rarely studied.  Identification of anatomical landmarks and their relations during endonasal approach is important for bleeding control. Thus, in this study, we have performed endonasal approach in skull and cadaveric head specimens. The microanatomic structures were examined.
A total of 10 dry skulls (20 sides) and 13 cadaveric heads (26 sides) processed by formalin were enrolled in this study. The specimens were all of adults (age 20-70 years) of Han from South China. They died of other reasons but not with brain diseases, and no obvious abnormalities were detected. The study plan was approved by the medical ethics committee of Fuzhou General Hospital, Fujian Medical University, China.
Common surgical instruments were provided by the hospital. The other instruments include: Microscope (Zhongtian Optical Instrument Co., Ltd. Zhenjiang, China), endoscope (Pv 430 Aesclup Neuroendoscopy, AESCULAP, Inc. -Berlin, Germany), FinePix S5600 digital camera (FUJIFILM Corporation Tokyo, Japan), vernier calipers with a precision of 0.02 mm (Ningbo Great Wall Precision Industrial Co., Ltd Ningbo, China).
Dry skull anatomy
The anterior ethmoid sinus, posterior ethmoid sinus, and anterior basicranial bone were opened. Anatomical relationship between anterior ethmoid canal, posterior ethmoid canal, sphenoid sinus, ethmoid sinus, and lamina cribrosa were observed.
Antiseptic cadaveric cranial anatomy
The craniums of 10 cadaveric heads were sawed away along the l. 0 cm horizontal lines between superciliary ridge and superior margin of the external occipital protuberance, succeeded by removal of brain tissues. The location of anterior ethmoidal artery and posterior ethmoidal artery throughout the anterior skull base and their relationship with the duramater and lamina cribrosa were observed from intracranial aspect. The anterior basicranial bone was moved with the opening of the anterior and posterior ethmoid sinus. The adjacent relationship of ethmoid sinus and optic canal was investigated and the distance was measured. Anterior and posterior ethmoidal arteries were identified and the anatomical relations of their courses to ethmoid roof and the lamina papyracea were observed. The relationship between anterior ethmoid artery, posterior ethmoidal artery, and ophthalmic artery was detected. Observation of lateral boundary of operation field was taken from intranasal aspects and intracranial aspects. The lateral wall of ethmoid sinus and sphenoid sinus was confirmed, and the distance between medial orbital wall and optic canal was measured.
Simulation of expanded endonasal approach for anterior skull base surgery
The other three antiseptic cadaveric heads were fixed on the autopsy table to imitate the endoscopic endonasal transsphenoidal approach. The structures of middle turbinate, uncinate process and sphenoethmoidal recess were identified under microscope. Sphenoid sinus ostium was identified and the internal structures of the sphenoid sinus were observed by using endoscope. Anterior ethmoidal artery was exposed after removing the middle turbinate, uncinate process and anterior wall of ethmoid bulla. Anterior ethmoid sinus was cleaned backward along the lamina cribrosa. Basal lamellae of the middle turbinate were removed, and then posterior ethmoidal artery was revealed by opening of posterior ethmoid sinus backward along the ethmoid roof. Prominence of the optic canal and the prominence of internal carotid artery were searched backward. Lamina cribrosa and anterior basicranial bone were opened upward and the olfactory nerve was found and isolated from lamina cribiosa. The region around midline anterior skull base was exposed and observed subsequently.
The ethmoid canals of the dry skulls
Ethmoid canal is a bony pipeline in the ethmoid sinus with two portals at both ends. The swelled ends serve as anatomical landmarks for ethmoid canal and facilitate the detection. Generally, anterior ethmoid canal is distributed from the lamina papyracea toward anteromedial part of ethmoid sinus while posterior ethmoid canal is distributed from the lamina papyracea toward the posteromedial part of ethmoid sinus. However, there were certain variations in the courses of anterior and posterior ethmoid canals [Figure 1]. Anterior ethmoid canal might locate in the bony plate of anterior ethmoid roof, between the bone plate and ethmoid mucous membrane, or in anterior ethmoid cells, as observed in six sides, 10 sides, and four sides of the specimens. There were 2 sides with the middle ethmoid canal between the anterior and posterior ethmoid canal. The course of this middle ethmoid canal was similar to that of posterior ethmoid canal. Posterior ethmoid canal located in the bony plate of posterior ethmoid roof, between the bone plate and ethmoid mucous membrane, or in posterior ethmoid cells, as observed in six sides, 10 sides and two sides of the specimens. Two sides of skull specimens in this study were without posterior ethmoid canal. Posterior ethmoid sinus could be divided into four types according to the relationship between the positions of ethmoid sinus back wall and optic canal. These four types and the frequency of each type were as follows: Anterocanal type (20%), semicanal type (45%), whole-canal type (20%), and sella turcica type (15%). Identical pneumatization on both sides accounted for 60%, while diverse pneumatization accounted for 40%.
The ethmoidal artery of cadaveric heads
Ophthalmic artery went forward along the orbit after passing through the orbital opening [Figure 2]. Ophthalmic artery branched into anterior and posterior ethmoidal arteries successively, which then entered the corresponding ethmoidal foramen, respectively. As observed from the superior aspect, ophthalmic artery together with the anterior and posterior ethmoidal artery showed the shape of "F" in eight sides of specimens. In two sides of specimens, anterior and posterior ethmoidal arteries were branched simultaneously from ophthalmic artery, and the three arteries showed the shape of "K". This "K"-shaped distribution could be divided into three subtypes of K1 type, K2 type, and K3 type. In K1 type, both the ethmoidal arteries were branched simultaneously before the anterior ethmoidal foramen. In K2 type, ethmoidal arteries were branched between the anterior and posterior ethmoidal foramen. In K3 type, ethmoidal arteries were branched behind the posterior ethmoidal foramen. There were two sides of specimens with K1 type, six sides with K2 type and four sides with K3 type.
Anterior and posterior ethmoidal arteries were located in the ethmoidal sinus after entering into the corresponding ethmoid canal though anterior and posterior ethmoidal foramen, respectively. The anterior and posterior ethmoidal arteries entered the nose via the corresponding ethmoid canal, supplied the ethmoidal sinuses, and entered the skull to supply meninges. Anterior ethmoidal artery was divided into nasal septal branch, lateral nasal branch, nasal dorsal branch, dural branch and lamina cribrosa branch. Posterior ethmoidal artery was divided into nasal septal branch, lateral nasal branches and lamina cribrosa branch [Figure 3].
The operating view field of skull base surgery
The medial walls of both orbits were the lateral boundaries of endonasal transsphenoidal and transethmoidal skull base surgery. If this boundary was exceeded, the lamina papyracea would be damaged, the fat in the orbits would spill over, and the optic nerve would be injured. The distance between medial orbital walls on both sides was different as a result of the diverse measuring locations adopted. The distances measured in the middle of crista galli, anterior, and posterior ethmoid canal were (22.31 ± 3.08) mm (range 18.7-27.4 mm), (23 ± 2.93) mm (range 19.7-28.1 mm), and (26.25 ± 2.88) mm (range 21.9-31.4 mm). The distance between medial margins of the cranial openings of the bilateral optic canals was (14.67 ± 3.82) mm (range 9.8-2.1 mm). These four groups of distances gradually broadened from the crista galli to posterior ethmoid canal and then narrowed after the posterior ethmoid canal. The data indicates that the operating field of the anterior skull base is relatively broad in the front, quite broad in the middle while rather narrow in the back [Figure 4]. At the back of anterior skull base, opticocarotid recess in the lateral wall of sphenoid sinus was the anatomical landmark for identifying the bilateral cranial opening of bilateral optic canals [Figure 5]. This location represents the pneumatized inner cavity of anterior clinoid process.
The findings of simulated endonasal anterior skull base surgery
After the nasal cavity was opened, the structure of middle turbinate, uncinate process and sphenoethmoidal recess was identified under microscope and sphenoidal ostium was found. Anterior ethmoid sinus was exposed by resection of middle turbinate, uncinate process and anterior wall of ethmoid bulla. After the anterior ethmoid sinus was cleaned, anterior ethmoidal artery could be found by examining from the front to posterior-superior part . After the basal lamellae of the middle turbinate were removed and the posterior ethmoid sinus was opened backward along the ethmoid roof, the posterior ethmoidal artery was found. The prominence of optic canal and prominence of internal carotid artery were found when searching backward [Figure 6].
The midline expanded endonasal approach to the cranial base can be broadly divided into four approaches along rostrocaudal axis: Transcribriform approach, transrubercular/transplanum approach, transsellar approach, and transclival approach,  among which, the first two are related to anterior skull base operations. Jho and Ha  examined the exposure range of three endonasal anterior skull base surgery approaches on six cadaveric heads. They found that the exposure range of the anterior skull base in the middle turbinectomy approach was the largest, followed by paraseptal approach. Middle meatal approach only exposed 2/3 the width of olfactory groove. Thus, the middle meatal approach was suitable for the treatment of cerebrospinal fluid leakage in the olfactory groove. In this study, we also analyzed the surgical approach made by middle turbinectomy and found that resection of middle turbinate achieved good exposure view to anterior skull base. Our results suggest that the middle turbinate is not only an important anatomic landmark, but also a structure that has to be removed while extending the surgical approach. The distances between the medial orbital wall on both sides at crista galli level and at planum sphenoidale were 24 mm (range 22-29 mm) and 27 mm (range 24-30 mm) as reported by Jho and Ha.  The distance between the optic nerves was 18 mm (range 15-22 mm). Our data showed that distances between medial orbital wall on both sides at the crista galli level and at the planum sphenoidale were relatively shorter than those reported by Jho and Ha.  This difference might be caused by racial difference. Jho and Ha reported that, by this middle turbinectomy approach, lesions (that were 2 cm in width) in the midline anterior skull base could be resected. Cook et al.  adopted paraseptal approach and they suggested that this approach could handle anterior skull base meningiomas with a diameter no more than 3 cm. The anatomical results in this study suggest that, endonasal approach for resection of anterior skull base tumor under the microscope is suitable for small range lesions in the midline anterior skull base. We suggest that the lesion diameter should be no more than 2.5 cm.
According to de Divitiis et al.,  in the treatment of tuberculum sellae meningiomas, the anterior boundary of craniotomy window was between planum sphenoidale and posterior ethmoidal artery, posterior boundary was the upper part of anterior sellar wall, and, the lateral boundary was the opticocarotid recess. While dealing with olfactory groove meningiomas, the anterior boundary was the back wall of frontal sinus, the posterior boundary was posterior ethmoidal artery, and the lateral boundary was the medial orbit walls on both sides. It was of great importance to identify and protect the boundary structures. In addition, the width in one case of anterior basicranial meningioma was 3.8 cm, and in another case it was 6 cm.  We suppose that it is extremely difficult to resect the lesion that is close to the lateral boundary in these two cases through endonasal anterior skull base surgery. And, the operation risk in these two cases is relatively high. Additionally, it is difficult to protect important structures when performing endonasal anterior skull base surgery in these two cases. Thus, cases like these two should better be excluded from this endonasal approach.
Ohnishi et al.,  studied endonasal microsurgery of the ethmoid sinus in 190 cases and suggested that handling of anterior and posterior ethmoidal artery and the protection of lamina papyracea and optic canal were very important. Furthermore, optic nerve damage occurred frequently in endonasal ethmoid sinus surgery.  Therefore, identification and protection of optic canal is very important during endonasal approaches. There are about 13 kinds of variations in the adjacent relationships among the optic canal medial wall, ethmoid sinus and sphenoid sinus, with most of them showing in the form of optic canal prominence. And, the more pneumatized the posterior ethmoid sinus is, the more obvious the optic canal prominence is.  Our study found that, the course of the prominence of optic canal and the prominence of internal carotid artery was crossed. The prominence of optic canal went from the back toward the anterior-lateral, while the prominence of internal carotid artery went from the posterosuperior toward lateral-inferior direction. These two prominences could exist simultaneously or individually. Prominence of optic canal and prominence of internal carotid artery could be used as a group of anatomic landmarks and as cross references during surgery. They could be identified comprehensively by their morphologies and adjacent anatomical landmarks. Our results were consistent with the anatomic study by Selcuk et al.,  suggesting that protection of the prominence of optic canal, prominence of internal carotid artery and tuberculum sellae are of great significance.
The anatomic structure of ethmoid sinus is complicated and the corridor of endonasal approach for anterior skull base operation is rather narrow. So only a little intraoperative bleeding can lead to poor visibility, especially when the operation is combined with endoscope. Anterior and posterior ethmoidal arteries are the main arteries of this area. With some variations in their positions, identifying them during surgery is of certain difficulty. Ohnishi et al.,  reported that, identification of anterior ethmoidal artery in the anterior ethmoid sinus was very important for the prevention of complications. Our study found that, while treating the anterior skull base lesions in the anterior ethmoid sinus, hemorrhage was mainly related to the intrasinus segment of the ethmoid artery and the lamina cribrosa branch of the anterior ethmoidal artery. Moreover, we found that the main trunks of anterior and posterior ethmoidal arteries went along or nearby the bony plate of ethmoid roof laterally. After opening the ethmoidal bulla and when cleaning the upward mucous membrane, careful attention should be paid. Once the anterior and posterior ethmoidal arteries were indentified, the skull base was reached. As the distance between posterior ethmoidal foramen and optic canal orbital opening was 5.1 mm (2.0-8.4 mm),  so the posterior ethmoidal artery and anterior optic nerve canal were mural references. Both anterior and posterior ethmoidal artery can be used as constant marks for endonasal anterior skull base surgery.
In this paper, dissection was performed with combined microscopic and endoscopic techniques. Anatomical structure of the skull base was observed and measured in the intracranial aspect and the intranasal aspect, respectively. We found that, during endonasal anterior skull base surgery, the structures of the nasal cavity, sphenoid sinus, ethmoid sinus and skull base were identified. And, the surgical corridor made by the middle turbinate resection should be taken. It was important to identify anterior and posterior ethmoidal arteries and then control the bleeding as quickly as possible. a Anterior and posterior ethmoidal artery could be used as good land marks for identification of the ethmoid sinus roof and the medial wall of orbit and also as constant marks for endonasal anterior skull base surgery. Prominence of the optic canal and the prominence of the internal carotid artery could be used as a group of anatomic landmarks and they were mutual references in operation. To ensure surgical safety, the optic canal and the medial wall of orbit should be not exceeded while performing extended endonasal anterior skull base surgery. Our study provides experimental data for conducting extended endonasal anterior skull base surgery in the future.
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