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Unilateral Basal Interhemispheric Approach Through the Sphenoid Sinus to Retrochiasmatic and Intrasellar Craniopharyngiomas: Surgical Technique and Results
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Unilateral Basal Interhemispheric Approach Through the Sphenoid Sinus to Retrochiasmatic and Intrasellar Craniopharyngiomas: Surgical Technique and Results Takayuki Matsuo, Kensaku Kamada, Tsuyoshi Izumo, Izumi Nagata
Key words Craniopharyngioma - Skull base surgery - Transsphenoidal root - Unilateral basal interhemispheric approach -
Abbreviations and Acronyms DI: Diabetes insipidus EETSA: Endoscopic endonasal transsphenoidal approach MRI: Magnetic resonance imaging OT: Open transcranial microscope-based techniques TSA: Transsphenoidal approach Department of Neurosurgery, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan To whom correspondence should be addressed: Takayuki Matsuo, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.02.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION The first surgery plays a significant role in treating craniopharyngioma, and whether or not total tumor resection is possible at the initial surgery is closely related to the patient’s outcome (17, 25, 26). Incomplete removal during the first surgery is associated with an increased postoperative recurrence rate (10, 17, 24, 28, 35). Many surgical techniques have been reported, aimed toward complete removal of craniopharyngioma (5, 6, 12, 15, 18, 20, 23, 33, 34, 36, 37). With the basal interhemispheric approach, the tumor is removed via 3 routes (i.e., the prechiasmatic space, the lamina terminalis between the anterior communicating artery and the optic chiasm, and the lamina terminalis superior to the anterior communicating artery), but one of the factors making tumor removal with this approach difficult is narrowing of the prechiasmatic space (28, 35). We report a technique that allows a wide space to be secured for sufficient tumor removal by drilling holes into the planum
- OBJECTIVE:
In the treatment of craniopharyngioma, complete surgical removal offers the best chance of cure and recurrence prevention. The basal interhemispheric approach involves problems with difficulty resecting tumors in the retrochiasmatic space located behind the optic chiasm and inability to resect, under direct view, tumors extending into the sella turcica. We report our approach via the sphenoid sinus devised to resolve these problems.
- METHODS:
A unilateral basal interhemispheric approach is planned for tumor resection. In cases in which the prechiasmatic space is too narrow to be utilized or the tumor has extended into the sella turcica, the prechiasmatic space is expanded by shaving the sphenoid surface and the tuberculum sellae. If the tumor inside the sella turcica needs to be removed, the anterior wall of the sella turcica also is shaved to permit tumor resection.
- RESULTS:
This technique was applied to 7 cases in total (in 3 cases to achieve prechiasmatic space expansion and in 4 cases for intrasellar tumor resection). Gross total removal was achieved in 6 cases and subtotal removal in 1. Of the 6 cases with preoperative visual field defects, 5 showed alleviation of these defects. The 5 patients with partial hypopituitarism developed complete panhypopituitarism postoperatively. All 7 patients have not suffered from postoperative cerebrospinal fluid leakage and meningitis.
- CONCLUSIONS:
This approach allowed a working space to be secured even in cases with a narrow prechiasmatic space, allowing tumor freeing from the lower plane of the optic nerve and safe resection of the intrasellar tumor.
sphenoidale and the tuberculum sellae and making use of the sphenoid sinus space. With this technique, tumor resection under direct vision is made possible, even for tumors that have extended into the sella turcica (such tumors are often left incompletely resected when the basal interhemispheric approach is used), by drilling into the anterior wall of the sella turcica. SURGICAL TECHNIQUE Craniotomy Procedure A coronal skin incision is made within the hairline, and a U-shaped pericranial flap is created so that it can be utilized when the opened frontal sinus is closed. A burr hole is created at 3 sites, with the burr hole closest to the base being created with a high-speed drill for esthetic purposes (Figure 1). The inner table of the frontal
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sinus is sufficiently drilled to secure a working space closer to the frontal skull base and to minimize the dead space formed at the time of cranioplasty. During this step, the frontal sinus mucosa is kept intact, if possible, and coagulation and shrinkage of the natural orifice are induced. Disinfection is performed within the frontal sinus, and the dead cavity is filled with pericranial flap and fibrin glue before closure of the head. To prevent injury of the bilateral frontal lobes, we usually adopt a unilateral approach. With this approach, the mobility of the cerebral falx needs to be secured. For this purpose, the crista galli is sufficiently resected via the epidural route.
INTRADURAL PROCEDURE The bridging vein is preserved as far as possible. The olfactory nerve is abraded up
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Figure 1. Craniotomy and intradural procedure. Burr hole is created at 3 sites.
to a level of the olfactory trigon before applying traction load to the olfactory nerve, allowing sufficient mobility to be secured. Then, this nerve is fixed on the cribriform plate with a combination of Surgicel (Ethicon, North Ryde, New South Wales, Australia) and fibrin glue for the purpose of protection. If the mobility of the cerebral falx is insufficient, greater mobility with a wider range can be achieved with incision of the tip of the cerebral falx. If a sufficient opening can be made, brain retractor use can potentially be minimized. Routes for Tumor Removal Difficulties encountered during tumor removal include preservation of the
UNILATERAL BASAL INTERHEMISPHERIC APPROACH
perforators of the anterior and posterior communicating arteries and abrasion of the optic nerve, hypothalamus, and pituitary stalk from the tumor. With the basal interhemispheric approach, tumor removal is usually achieved via 3 routes, i.e., the prechiasmatic space, the lamina terminalis between the anterior communicating artery and the optic chiasm, and the lamina terminalis superior to the anterior communicating artery (Figures 2A-2C). Because this approach allows sufficient space to be secured in front of the optic chiasms, if the tumor is small, it can be removed without opening the lamina terminalis. If the tumor has extended upward or a sufficient space cannot be secured in front of the optic chiasm, the lamina terminalis needs to be opened. If there is a space enabling an incision of the lamina terminalis to be made from under the anterior communicating artery, this space is to be utilized. However, in cases requiring incision of the lamina terminalis from above the anterior communicating artery, care needs to be taken to preserve the perforators of the hypothalamic and subcallosal arteries, and others, with particular attention given to avoidance of injury to the largest hypothalamic artery (Figure 2C). Which one of these three routes is selected depends on the features of individual cases. If the prechiasmatic space is too narrow to be used for tumor removal from the lower plane of the optic chiasm or if the presence of the tumor within the sella turcica makes direct vision surgery impossible, the area from the planum sphenoidale to the tuberculum sellae and the anterior wall of sella turcica is partially removed with a diamond drill to secure a space in front of the
Figure 2. Routes for tumor removal. (A) The prechiasmatic space. (B) The lamina terminalis between the anterior communicating artery and the optic chiasm. (C) The lamina terminalis superior to the anterior communicating
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optic chiasm via the sphenoid sinus (Figures 3A-3C). If necessary, the falciform fold is incised. Utilization of the thus-created space allows the tumor to be removed from the sella turcica under direct vision. In cases in which the prechiasmatic space has expanded or narrowed, this route also allows tumor removal from the inferior plane of the optic nerve (Figures 3D and 3E). In cases in which the sphenoid sinus has developed, a particularly wide space can be secured with this route, facilitating utilization of an endoscope through this space to identify the inferior plane of the optic nerve and to free the tumor from this plane. However, if this route is selected, the sphenoid sinus needs to be opened, thus requiring postoperative reconstruction of the sphenoid sinus. To prepare for such postoperative reconstruction, it is essential 1) to preserve the dura mater of the sphenoid surface as far as possible so that it can later be used for closure of the communication between the opened sphenoid sinus and the intracranial cavity, and 2) to avoid damaging the sphenoid sinus mucosa at the time of drilling. Upon completion of tumor removal, the opened portion of the planum sphenoidale needs to be closed from within the skull using galea, fibrin glue, and the preserved dura mater from the opened planum sphenoidale (Figures 4A and 4B). Freeing from the Surrounding Tissue When a tumor is surrounded by important structures and the space for manipulation or the surgeon’s visual field is restricted, sufficient tumor decompression is the first surgical procedure for tumor removal or
artery. OC, optic chiasm; T, tumor; Acom, anterior communicating artery; HTA, hypothalamic artery.
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Figure 3. Transsphenoidal root. (A, B, C) The planum sphenoidale to the tuberculum sellae and the anterior wall of sella turcica is drilled with a diamond drill to secure a space in front of the optic chiasm via the sphenoid sinus. Arrow head, drilling line; arrow, dural incision line; star, dural flap. (D, E) The space thus created allows the tumor to be removed from the sella turcica under direct vision. OC, optic chiasm; T, tumor; PS, planum sphenoidale; SS, sphenoid sinus; S, sella turcica.
for securing sufficient space for tumor dissection from the surrounding tissue. If the tumor is located above the third ventricle, adhesion is often mild. In such cases, easy orientation for dissection of the upper tumor plane is possible if manipulation is advanced backward from the upper median plane of the tumor, which has undergone internal decompression, toward the midbrain aqueduct while checking cerebrospinal fluid outflow. Adequate care must be taken when the tumor is freed from the hypothalamus located lateral to the tumor. The manipulation for freeing the tumor from the hypothalamus involves gently pulling the tumor free, rather than
manipulating the brain so as to free it from the tumor. Using a spatula, these maneuvers are cautiously carried out to ensure that the gliosis layer is left as intact as possible on the freed brain surface. When the tumor is free from the optic nerve, care needs to be taken to avoid injury of the blood vessels around the optic nerve, and the manipulations used to free this nerve should be made with meticulous attention to the subarachnoid membrane. The pituitary stalk can easily be identified on the basis of the longitudinally arranged blood vessels. Whether or not the pituitary stalk should be preserved is determined based on the features of individual cases, but it is resected in
Figure 4. (A, B) After tumor removal, the opened sphenoid sinus needs to be closed from within the skull using galea, fibrin glue, and the preserved dura mater. G, galea.
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cases in which removal of the entire tumor is judged to be feasible. Even if the tumor has extended toward the prepontine cistern, the Lilienquist membrane often serves as a partition between the basilar artery and its perforators if the patient has not previously undergone surgery. Under such circumstances, the tumor in that area is not directly nourished by these vessels. Thus, there is little risk of injuring these vessels if the tumor is resected paying close attention to the subarachnoid membrane. CLINICAL MATERIAL Seven patients with craniopharyngiomas underwent surgery via this approach. In 3 patients, the objective was enlargement of the prechiasmatic space. In the other 4 patients, the objective was removal of the tumor from inside the sella turcica. The clinical features are detailed in Table 1. The degree of resection was determined using the results of follow-up enhanced magnetic resonance imaging (MRI) within 48 hours after surgery. A gross total excision was achieved in 6 patients, whereas only subtotal removal was possible in 1. All 7 patients have not suffered from postoperative cerebrospinal fluid leakage or meningitis. Partial anterior pituitary dysfunction and diabetes insipidus (DI)
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Table 1. Summary of 7 Patients Who Underwent a Basal Interhemispheric Approach With Transsphenoidal Root Case Number
Sex
Age
M
15
1
Maximum Diameter (mm)/Type
Tumor Location
31.4 Multicystic
Initial Hormonal Insufficiency
SS
APHY, DI
Visual
Other
BLH
2
F
4
32.1 Solid and cyst
SS þ S
DI
BLH
3
F
45
40.2 Solid and cyst
SS þ S
ACTHY, TSHY, DI
BLH
4
M
12
45.1 Multicystic
SS þ S
APH, DI
Left LH
5
M
58
38.2 Solid
SS
ACTHY, TSHY, DI
BLH
6
M
32
34.5 Cystic
SS
ACTHY, DI
Right BLH
7
M
47
36.6 Solid and cyst
SS þ S
ACTHY, TSHY, DI
Normal
Hydrocephalus/dementia
M, male; F, female; SS, suprasellar; S, sellar; APH, anterior panhypopituitarism; DI, Diabetes insipidus; BLH, bilateral hemianopsia; ACTH, adrenocorticotropic hormone; TSH, thyroid stimulating hormone; LH, lateral hemianopsia.
was present in all cases on admission (Table 1). Complete panhypopituitarism developed postoperatively in the 5 patients with partial hypopituitarism (Table 2). Visual field defects were seen in 6 patients preoperatively, and 5 of them showed alleviation of these defects.
ILLUSTRATIVE CASES
a sufficient prechiasmatic space, followed by opening of the lamina terminalis and removal of the tumor via the space above and under the optic chiasm. Postoperative MRI showed no residual tumor (Figures 5C and 5D). Anterior panhypopituitarism and DI persisted after surgery, but the visual field defects resolved and there was no cerebrospinal fluid leakage postoperatively.
the entire tumor, including the solid lesion inside the sella turcica. Postoperative MRI showed no residual tumor (Figures 6C and 6D). Postoperatively the patient developed complete panhypopituitarism, but the visual field defects resolved after surgery and there was no cerebrospinal fluid leakage postoperatively.
DISCUSSION Case 1 The patient was a 15-year-old adolescent boy. His initial clinical manifestations were visual field defects, DI, and anterior panhypopituitarism. MRI revealed a multicystic lesion compressing the optic nerve in the suprasellar region (Figures 5A and 5B). The tumor was removed with a right unilateral basal interhemispheric approach. Because the prechiasmatic space was narrow, the sphenoid surface was shaved to open the sphenoid sinus and thereby secure
Case 2 The patient was a 4-year-old girl. Her initial manifestations were DI and visual field defects. The sphenoid sinus was poorly developed. A cystic lesion, part of which was accompanied by a solid lesion, was seen on MRI in the area from the sella turcica to the suprasellar region (Figures 6A and 6B). With a right unilateral interhemispheric approach, we drilled into the bone in the area from the sphenoid surface to the tuberculum sellae, followed by removal of
Table 2. Surgical Outcomes and Complications Case Number
Surgical Result
Follow-Up Visual (years) Improvement
CSF Leakage/ Meningitis
Hormonal Outcome
Adjuvant Therapy
1
GTR
1.5
Yes
e
APH, DI
No
2
GTR
7
Yes
e
APH, DI
No
3
GTR
1
Yes
e
APH, DI
No
4
GTR
2
Yes
e
APH, DI
No
5
GTR
3
No change
e
ACTHY, TSHY, DI
No
6
STR
8
Yes
e
APH, DI
SRS
7
GTR
8
Yes
e
APH, DI
No
GTR, gross total removal; STR, subtotal removal; APH, anterior panhypopituitarism; TSH, thyroid stimulating hormone; SRS, stereotactic radiosurgery.
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In the treatment of craniopharyngioma, whether or not gross total removal can be achieved with the first surgery determines the outcomes of patients (10, 24, 26, 28, 35). Cases with little lateral extension of a tumor located below the Monro foramen have a good indication for the anteromedian surgical approach. With the anterior approach, the optic chiasm is located in front of the tumor. To avoid this obstacle, the tumor needs to be removed via the prechiasmatic space. If this space is narrow, the lamina terminalis is opened to allow the manipulations necessary for removal of the tumor from the inferior plane of the optic chiasm, but the manipulations on the reverse side of the optic chiasm are inevitably performed in a blind fashion when an anterior approach is applied. Techniques reported to resolve this problem include the posterior petrosal approach (1, 2, 15) and the endoscopic endonasal extended transsphenoidal approach (TSA) (3, 7, 11, 13). Comparison of the Basal Interhemispheric Approach and the Other Transcranial Approach The unilateral or bilateral subfrontal approach [Samii et al. (30), Yasargil et al.
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needed to achieve sufficient lateral development comparable to that possible with the bifrontal basal interhemispheric approach reported by Shibuya et al. (31). We also cut the anterior communicating artery in 1 of our 7 cases. Furthermore, if the area from the planum sphenoidale to the tuberculum sellae is drilled to open the sphenoid sinus, a sufficient working space can be secured not only in the lateral direction but also in the anterior direction, thereby expanding the operative field.
Figure 5. Case 1. Preoperative coronal (A) and sagittal (B) T1-weighted post-Gd magnetic resonance imaging studies showing retrochiasmatic multicystic craniopharyngioma. Postoperative coronal (C) and sagittal (D) T1-weighted post-Gd (gadolinium enhanced) magnetic resonance imaging studies showing gross total resection of the tumor.
(36)] is simple, does not require opening of the interhemispheric fissure, and has been used extensively. However, as compared to the interhemispheric approach, this strategy has several disadvantages, including the relatively narrow operative field, difficulty in opening the entire lamina terminalis, and the intense retraction of the frontal lobe, which is required (31-34). Shibuya et al. (31) compared the bifrontal basal interhemispheric approach (32) with unilateral approaches such as the pterional one used in surgery for large craniopharyngiomas, reporting that the basal interhemispheric approach was superior to other approaches in terms of preservation of the perforator and pituitary stalk and avoidance of bilateral hypothalamus injuries. They also highlighted the importance of visualizing the lateral aspect of the tumor via the interhemispheric approach (33), stating that favorable outcomes were
obtained by lateral expansion, achieved by cutting the anterior communicating artery in cases in which this artery was an obstacle to lateral expansion. Yasui et al. (37) reported a unilateral basal interhemispheric approach. According to their report, this approach is advantageous in that there is less injury of the bridging vein, and the opening of the interhemispheric fissure is small, allowing the operative time to be shortened and less brain damage to occur. Furthermore, they reported that their approach allows the upper part of the tumor extending into the third ventricle to be checked from a lower angle. Basically, we adopt the unilateral basal interhemispheric approach, involving incision of the unilateral dura mater, an approach similar to that reported by Yasui et al. (37). However, we have modified this approach by sufficiently resecting the crista galli and cutting the falx tip as
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Comparison of the Basal Interhemispheric Approach and the TSA Another possible strategy for accessing a craniopharyngioma from the inferior plane of the optic nerve is the TSA. Comparison of the TSA and basal interhemispheric approach reveals the former to be superior in terms of the manipulation for freeing the area from the inferior to the posterior plane of optic chiasm. This approach is advantageous in that the risk of perforator injury (from the posterior communicating artery, P1, etc.) or postoperative cranial nerve palsy is lower than with the posterior petrosal approach and other lateral or posterior approaches aimed at viewing the optic chiasm from its inferior plane. Komotar et al. (21) reviewed 88 reports involving 3470 cases and made comparisons among the endoscopic endonasal transsphenoidal, transsphenoidal purely microscope-based, and open transcranial microscope-based (OT) techniques. They concluded that the endoscopic endonasal transsphenoidal technique was safer and more effective for craniopharyngioma surgery than the other approaches. Consideration must, however, be given as the pterional approach was used for many of the OT group cases. Incomplete tumor removal due to poor sellar visualization was listed as one of the reasons for the low gross total resection rate in the OT group. If the transsphenoidal route we propose is adopted, a tumor located inside the sella turcica can be removed under direct vision. This supports the likelihood of improving the gross total resection rate with the OT technique. Reconstruction of Skull Base The technique presented herein, i.e., securing the space for manipulations by opening the planum sphenoidale and utilizing the sphenoid sinus, is expected to provide a valid operative procedure in cases
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beyond the dorsum sellae, adhesions with surrounding tissues developed after previous surgery, etc., and blood vessels have become incorporated into the tumor (8, 9, 29). Our approach is promising as a technique that is both safe and effective for treating craniopharyngiomas extending into the sella turcica and for resection of craniopharyngiomas affecting the inferior plane of the optic nerve where a sufficient prechiasmatic space cannot be secured. CONCLUSIONS
Figure 6. Case 2. Preoperative coronal (A) and sagittal (B) T1-weighted post-Gd (gadolinium enhanced) magnetic resonance imaging studies showing a cystic craniopharyngioma, part of which was accompanied by a solid lesion in the area from the sella turcica to the suprasellar region. Postoperative coronal (C) and sagittal (D) T1-weighted post-Gd magnetic resonance imaging studies showing gross total resection of the tumor.
in which manipulation on the inferior plane of the optic chiasm is inevitably performed in a blind fashion with a basal interhemispheric approach (a shortcoming of this approach), as well as in those in which a narrow prechiasmatic space makes tumor resection difficult from the anterior plane of the optic chiasm. A problem with this technique lies in the communication between the sphenoid sinus and the cerebrospinal fluid cavity with the potential to lead to postoperative infection or cerebrospinal fluid leakage. However, these complications were successfully prevented by 1) avoidance of sphenoid sinus mucosa injury at the time of opening the planum sphenoidale, 2) preservation of the dura mater of the planum sphenoidale as far as possible for subsequent utilization at the time of closure, and 3) multilayered reconstruction of the skull base using the galea and fibrin glue. Our present multilayered reconstruction is similar to the endoscopic endonasal transsphenoidal approach (EETSA) for craniopharyngioma resection (4, 13, 14, 16,
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19, 22, 27). Leng et al. (23) reported the development of extended TSAs has been mirrored by the development in skull base closure techniques. Their cerebrospinal fluid leakage rate of 3.8% is comparable to other approaches. Unilateral Basal Interhemispheric Approach Through the Sphenoid Sinus The unilateral basal interhemispheric approach through the sphenoid sinus to under the chiasmatic and intrasellar parts of the craniopharyngioma seems to provide a valid way of removing tumors that have extended from the inferior plane of the optic nerve to the sella turcica by means of expanding the prechiasmatic space. After the recent spread of the use of endoscopes, numerous reports have focused on the effectiveness of tumor removal by the EETSA, and this strategy has been widely adopted. However, there are many cases in which the interhemispheric approach is useful, e.g., those in which the EETSA is difficult when the tumor has extended
The basal interhemispheric approach is a useful surgical approach for craniopharyngiomas located in the median region. When used for removal of a tumor located in the blind angle on the inferior plane of the optic chiasm where operative manipulation is difficult, the manipulations for tumor removal may be facilitated by expansion of the prechiasmatic space, and the tumor inside the sella turcica can also be removed under direct vision if the planum sphenoidale is opened to allow effective utilization of the sphenoid sinus space, although this procedure still has some limitations. Furthermore, utilization of the thus-created space also enables the surgeon to use an endoscope for assessing and manipulating the inferior plane of the optic chiasm. REFERENCES 1. Al-Mefty O, Ayoubi S, Kadri PA: The petrosal approach for the resection of retrochiasmatic craniopharyngiomas. Neurosurgery 62:ONS331ONS335 [discussion ONS335-336], 2008. 2. Al-Mefty O, Ayoubi S, Kadri PA: The petrosal approach for the total removal of giant retrochiasmatic craniopharyngiomas in children. J Neurosurg 106:87-92, 2007. 3. Ali ZS, Lang SS, Kamat AR, Adappa ND, Palmer JN, Storm PB, Lee JY: Suprasellar pediatric craniopharyngioma resection via endonasal endoscopic approach. Childs Nerv Syst 29:2065-2070, 2013. 4. Cavallo LM, Prevedello D, Esposito F, Laws ER Jr, Dusick JR, Messina A, Jane JA Jr, Kelly DF, Cappabianca P: The role of the endoscope in the transsphenoidal management of cystic lesions of the sellar region. Neurosurg Rev 31:55-64 [discussion 64], 2008. 5. Ceylan S, Koc K, Anik I: Extended endoscopic approaches for midline skull-base lesions. Neurosurg Rev 32:309-319 [discussion 318-309], 2009. 6. Ciric IS, Tarkington J: Transsphenoidal microsurgery. Surg Neurol 2:207-212, 1974. 7. Couldwell WT, Weiss MH, Rabb C, Liu JK, Apfelbaum RI, Fukushima T: Variations on the
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18. Kassam AB, Gardner PA, Snyderman CH, Carrau RL, Mintz AH, Prevedello DM: Expanded endonasal approach, a fully endoscopic transnasal approach for the resection of midline suprasellar
28. Patterson RH Jr, Danylevich A: Surgical removal of craniopharyngiomas by the transcranial approach through the lamina terminalis and sphenoid sinus. Neurosurgery 7:111-117, 1980.
29. Sainte-Rose C, Puget S, Wray A, Zerah M, Grill J, Brauner R, Boddaert N, Pierre-Kahn A: Craniopharyngioma: the pendulum of surgical management. Childs Nerv Syst 21:691-695, 2005. 30. Samii M, Tatagiba M: Surgical management of craniopharyngiomas: a review. Neurol Med Chir (Tokyo) 37:141-149, 1997. 31. Shibuya M, Takayasu M, Suzuki Y, Saito K, Sugita K: Bifrontal basal interhemispheric approach to craniopharyngioma resection with or without division of the anterior communicating artery. J Neurosurg 84:951-956, 1996. 32. Shirane R, Ching-Chan S, Kusaka Y, Jokura H, Yoshimoto T: Surgical outcomes in 31 patients with craniopharyngiomas extending outside the suprasellar cistern: an evaluation of the frontobasal interhemispheric approach. J Neurosurg 96: 704-712, 2002. 33. Suzuki J, Katakura R, Mori T: Interhemispheric approach through the lamina terminalis to tumors of the anterior part of the third ventricle. Surg Neurol 22:157-163, 1984. 34. Suzuki J, Yoshimoto T, Mizoi K: Preservation of the olfactory tract in bifrontal craniotomy for anterior communicating artery aneurysms, and the functional prognosis. J Neurosurg 54:342-345, 1981. 35. Van Effenterre R, Boch AL: Craniopharyngioma in adults and children: a study of 122 surgical cases. J Neurosurg 97:3-11, 2002. 36. Yasargil MG, Curcic M, Kis M, Siegenthaler G, Teddy PJ, Roth P: Total removal of craniopharyngiomas. Approaches and long-term results in 144 patients. J Neurosurg 73:3-11, 1990. 37. Yasui N, Nathal E, Fujiwara H, Suzuki A: The basal interhemispheric approach for acute anterior communicating aneurysms. Acta Neurochir (Wien) 118:91-97, 1992.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 19 September 2013; accepted 8 February 2014 Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.02.005 Journal homepage: www.WORLDNEUROSURGERY.org
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Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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Unilateral Basal Interhemispheric Approach Through the Sphenoid Sinus to Retrochiasmatic and Intrasellar Craniopharyngiomas: Surgical Technique and Results Takayuki Matsuo, Kensaku Kamada, Tsuyoshi Izumo, Izumi Nagata
Key words Craniopharyngioma - Skull base surgery - Transsphenoidal root - Unilateral basal interhemispheric approach -
Abbreviations and Acronyms DI: Diabetes insipidus EETSA: Endoscopic endonasal transsphenoidal approach MRI: Magnetic resonance imaging OT: Open transcranial microscope-based techniques TSA: Transsphenoidal approach Department of Neurosurgery, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan To whom correspondence should be addressed: Takayuki Matsuo, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.02.005 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION The first surgery plays a significant role in treating craniopharyngioma, and whether or not total tumor resection is possible at the initial surgery is closely related to the patient’s outcome (17, 25, 26). Incomplete removal during the first surgery is associated with an increased postoperative recurrence rate (10, 17, 24, 28, 35). Many surgical techniques have been reported, aimed toward complete removal of craniopharyngioma (5, 6, 12, 15, 18, 20, 23, 33, 34, 36, 37). With the basal interhemispheric approach, the tumor is removed via 3 routes (i.e., the prechiasmatic space, the lamina terminalis between the anterior communicating artery and the optic chiasm, and the lamina terminalis superior to the anterior communicating artery), but one of the factors making tumor removal with this approach difficult is narrowing of the prechiasmatic space (28, 35). We report a technique that allows a wide space to be secured for sufficient tumor removal by drilling holes into the planum
- OBJECTIVE:
In the treatment of craniopharyngioma, complete surgical removal offers the best chance of cure and recurrence prevention. The basal interhemispheric approach involves problems with difficulty resecting tumors in the retrochiasmatic space located behind the optic chiasm and inability to resect, under direct view, tumors extending into the sella turcica. We report our approach via the sphenoid sinus devised to resolve these problems.
- METHODS:
A unilateral basal interhemispheric approach is planned for tumor resection. In cases in which the prechiasmatic space is too narrow to be utilized or the tumor has extended into the sella turcica, the prechiasmatic space is expanded by shaving the sphenoid surface and the tuberculum sellae. If the tumor inside the sella turcica needs to be removed, the anterior wall of the sella turcica also is shaved to permit tumor resection.
- RESULTS:
This technique was applied to 7 cases in total (in 3 cases to achieve prechiasmatic space expansion and in 4 cases for intrasellar tumor resection). Gross total removal was achieved in 6 cases and subtotal removal in 1. Of the 6 cases with preoperative visual field defects, 5 showed alleviation of these defects. The 5 patients with partial hypopituitarism developed complete panhypopituitarism postoperatively. All 7 patients have not suffered from postoperative cerebrospinal fluid leakage and meningitis.
- CONCLUSIONS:
This approach allowed a working space to be secured even in cases with a narrow prechiasmatic space, allowing tumor freeing from the lower plane of the optic nerve and safe resection of the intrasellar tumor.
sphenoidale and the tuberculum sellae and making use of the sphenoid sinus space. With this technique, tumor resection under direct vision is made possible, even for tumors that have extended into the sella turcica (such tumors are often left incompletely resected when the basal interhemispheric approach is used), by drilling into the anterior wall of the sella turcica. SURGICAL TECHNIQUE Craniotomy Procedure A coronal skin incision is made within the hairline, and a U-shaped pericranial flap is created so that it can be utilized when the opened frontal sinus is closed. A burr hole is created at 3 sites, with the burr hole closest to the base being created with a high-speed drill for esthetic purposes (Figure 1). The inner table of the frontal
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sinus is sufficiently drilled to secure a working space closer to the frontal skull base and to minimize the dead space formed at the time of cranioplasty. During this step, the frontal sinus mucosa is kept intact, if possible, and coagulation and shrinkage of the natural orifice are induced. Disinfection is performed within the frontal sinus, and the dead cavity is filled with pericranial flap and fibrin glue before closure of the head. To prevent injury of the bilateral frontal lobes, we usually adopt a unilateral approach. With this approach, the mobility of the cerebral falx needs to be secured. For this purpose, the crista galli is sufficiently resected via the epidural route.
INTRADURAL PROCEDURE The bridging vein is preserved as far as possible. The olfactory nerve is abraded up
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Figure 1. Craniotomy and intradural procedure. Burr hole is created at 3 sites.
to a level of the olfactory trigon before applying traction load to the olfactory nerve, allowing sufficient mobility to be secured. Then, this nerve is fixed on the cribriform plate with a combination of Surgicel (Ethicon, North Ryde, New South Wales, Australia) and fibrin glue for the purpose of protection. If the mobility of the cerebral falx is insufficient, greater mobility with a wider range can be achieved with incision of the tip of the cerebral falx. If a sufficient opening can be made, brain retractor use can potentially be minimized. Routes for Tumor Removal Difficulties encountered during tumor removal include preservation of the
UNILATERAL BASAL INTERHEMISPHERIC APPROACH
perforators of the anterior and posterior communicating arteries and abrasion of the optic nerve, hypothalamus, and pituitary stalk from the tumor. With the basal interhemispheric approach, tumor removal is usually achieved via 3 routes, i.e., the prechiasmatic space, the lamina terminalis between the anterior communicating artery and the optic chiasm, and the lamina terminalis superior to the anterior communicating artery (Figures 2A-2C). Because this approach allows sufficient space to be secured in front of the optic chiasms, if the tumor is small, it can be removed without opening the lamina terminalis. If the tumor has extended upward or a sufficient space cannot be secured in front of the optic chiasm, the lamina terminalis needs to be opened. If there is a space enabling an incision of the lamina terminalis to be made from under the anterior communicating artery, this space is to be utilized. However, in cases requiring incision of the lamina terminalis from above the anterior communicating artery, care needs to be taken to preserve the perforators of the hypothalamic and subcallosal arteries, and others, with particular attention given to avoidance of injury to the largest hypothalamic artery (Figure 2C). Which one of these three routes is selected depends on the features of individual cases. If the prechiasmatic space is too narrow to be used for tumor removal from the lower plane of the optic chiasm or if the presence of the tumor within the sella turcica makes direct vision surgery impossible, the area from the planum sphenoidale to the tuberculum sellae and the anterior wall of sella turcica is partially removed with a diamond drill to secure a space in front of the
Figure 2. Routes for tumor removal. (A) The prechiasmatic space. (B) The lamina terminalis between the anterior communicating artery and the optic chiasm. (C) The lamina terminalis superior to the anterior communicating
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optic chiasm via the sphenoid sinus (Figures 3A-3C). If necessary, the falciform fold is incised. Utilization of the thus-created space allows the tumor to be removed from the sella turcica under direct vision. In cases in which the prechiasmatic space has expanded or narrowed, this route also allows tumor removal from the inferior plane of the optic nerve (Figures 3D and 3E). In cases in which the sphenoid sinus has developed, a particularly wide space can be secured with this route, facilitating utilization of an endoscope through this space to identify the inferior plane of the optic nerve and to free the tumor from this plane. However, if this route is selected, the sphenoid sinus needs to be opened, thus requiring postoperative reconstruction of the sphenoid sinus. To prepare for such postoperative reconstruction, it is essential 1) to preserve the dura mater of the sphenoid surface as far as possible so that it can later be used for closure of the communication between the opened sphenoid sinus and the intracranial cavity, and 2) to avoid damaging the sphenoid sinus mucosa at the time of drilling. Upon completion of tumor removal, the opened portion of the planum sphenoidale needs to be closed from within the skull using galea, fibrin glue, and the preserved dura mater from the opened planum sphenoidale (Figures 4A and 4B). Freeing from the Surrounding Tissue When a tumor is surrounded by important structures and the space for manipulation or the surgeon’s visual field is restricted, sufficient tumor decompression is the first surgical procedure for tumor removal or
artery. OC, optic chiasm; T, tumor; Acom, anterior communicating artery; HTA, hypothalamic artery.
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Figure 3. Transsphenoidal root. (A, B, C) The planum sphenoidale to the tuberculum sellae and the anterior wall of sella turcica is drilled with a diamond drill to secure a space in front of the optic chiasm via the sphenoid sinus. Arrow head, drilling line; arrow, dural incision line; star, dural flap. (D, E) The space thus created allows the tumor to be removed from the sella turcica under direct vision. OC, optic chiasm; T, tumor; PS, planum sphenoidale; SS, sphenoid sinus; S, sella turcica.
for securing sufficient space for tumor dissection from the surrounding tissue. If the tumor is located above the third ventricle, adhesion is often mild. In such cases, easy orientation for dissection of the upper tumor plane is possible if manipulation is advanced backward from the upper median plane of the tumor, which has undergone internal decompression, toward the midbrain aqueduct while checking cerebrospinal fluid outflow. Adequate care must be taken when the tumor is freed from the hypothalamus located lateral to the tumor. The manipulation for freeing the tumor from the hypothalamus involves gently pulling the tumor free, rather than
manipulating the brain so as to free it from the tumor. Using a spatula, these maneuvers are cautiously carried out to ensure that the gliosis layer is left as intact as possible on the freed brain surface. When the tumor is free from the optic nerve, care needs to be taken to avoid injury of the blood vessels around the optic nerve, and the manipulations used to free this nerve should be made with meticulous attention to the subarachnoid membrane. The pituitary stalk can easily be identified on the basis of the longitudinally arranged blood vessels. Whether or not the pituitary stalk should be preserved is determined based on the features of individual cases, but it is resected in
Figure 4. (A, B) After tumor removal, the opened sphenoid sinus needs to be closed from within the skull using galea, fibrin glue, and the preserved dura mater. G, galea.
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cases in which removal of the entire tumor is judged to be feasible. Even if the tumor has extended toward the prepontine cistern, the Lilienquist membrane often serves as a partition between the basilar artery and its perforators if the patient has not previously undergone surgery. Under such circumstances, the tumor in that area is not directly nourished by these vessels. Thus, there is little risk of injuring these vessels if the tumor is resected paying close attention to the subarachnoid membrane. CLINICAL MATERIAL Seven patients with craniopharyngiomas underwent surgery via this approach. In 3 patients, the objective was enlargement of the prechiasmatic space. In the other 4 patients, the objective was removal of the tumor from inside the sella turcica. The clinical features are detailed in Table 1. The degree of resection was determined using the results of follow-up enhanced magnetic resonance imaging (MRI) within 48 hours after surgery. A gross total excision was achieved in 6 patients, whereas only subtotal removal was possible in 1. All 7 patients have not suffered from postoperative cerebrospinal fluid leakage or meningitis. Partial anterior pituitary dysfunction and diabetes insipidus (DI)
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Table 1. Summary of 7 Patients Who Underwent a Basal Interhemispheric Approach With Transsphenoidal Root Case Number
Sex
Age
M
15
1
Maximum Diameter (mm)/Type
Tumor Location
31.4 Multicystic
Initial Hormonal Insufficiency
SS
APHY, DI
Visual
Other
BLH
2
F
4
32.1 Solid and cyst
SS þ S
DI
BLH
3
F
45
40.2 Solid and cyst
SS þ S
ACTHY, TSHY, DI
BLH
4
M
12
45.1 Multicystic
SS þ S
APH, DI
Left LH
5
M
58
38.2 Solid
SS
ACTHY, TSHY, DI
BLH
6
M
32
34.5 Cystic
SS
ACTHY, DI
Right BLH
7
M
47
36.6 Solid and cyst
SS þ S
ACTHY, TSHY, DI
Normal
Hydrocephalus/dementia
M, male; F, female; SS, suprasellar; S, sellar; APH, anterior panhypopituitarism; DI, Diabetes insipidus; BLH, bilateral hemianopsia; ACTH, adrenocorticotropic hormone; TSH, thyroid stimulating hormone; LH, lateral hemianopsia.
was present in all cases on admission (Table 1). Complete panhypopituitarism developed postoperatively in the 5 patients with partial hypopituitarism (Table 2). Visual field defects were seen in 6 patients preoperatively, and 5 of them showed alleviation of these defects.
ILLUSTRATIVE CASES
a sufficient prechiasmatic space, followed by opening of the lamina terminalis and removal of the tumor via the space above and under the optic chiasm. Postoperative MRI showed no residual tumor (Figures 5C and 5D). Anterior panhypopituitarism and DI persisted after surgery, but the visual field defects resolved and there was no cerebrospinal fluid leakage postoperatively.
the entire tumor, including the solid lesion inside the sella turcica. Postoperative MRI showed no residual tumor (Figures 6C and 6D). Postoperatively the patient developed complete panhypopituitarism, but the visual field defects resolved after surgery and there was no cerebrospinal fluid leakage postoperatively.
DISCUSSION Case 1 The patient was a 15-year-old adolescent boy. His initial clinical manifestations were visual field defects, DI, and anterior panhypopituitarism. MRI revealed a multicystic lesion compressing the optic nerve in the suprasellar region (Figures 5A and 5B). The tumor was removed with a right unilateral basal interhemispheric approach. Because the prechiasmatic space was narrow, the sphenoid surface was shaved to open the sphenoid sinus and thereby secure
Case 2 The patient was a 4-year-old girl. Her initial manifestations were DI and visual field defects. The sphenoid sinus was poorly developed. A cystic lesion, part of which was accompanied by a solid lesion, was seen on MRI in the area from the sella turcica to the suprasellar region (Figures 6A and 6B). With a right unilateral interhemispheric approach, we drilled into the bone in the area from the sphenoid surface to the tuberculum sellae, followed by removal of
Table 2. Surgical Outcomes and Complications Case Number
Surgical Result
Follow-Up Visual (years) Improvement
CSF Leakage/ Meningitis
Hormonal Outcome
Adjuvant Therapy
1
GTR
1.5
Yes
e
APH, DI
No
2
GTR
7
Yes
e
APH, DI
No
3
GTR
1
Yes
e
APH, DI
No
4
GTR
2
Yes
e
APH, DI
No
5
GTR
3
No change
e
ACTHY, TSHY, DI
No
6
STR
8
Yes
e
APH, DI
SRS
7
GTR
8
Yes
e
APH, DI
No
GTR, gross total removal; STR, subtotal removal; APH, anterior panhypopituitarism; TSH, thyroid stimulating hormone; SRS, stereotactic radiosurgery.
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In the treatment of craniopharyngioma, whether or not gross total removal can be achieved with the first surgery determines the outcomes of patients (10, 24, 26, 28, 35). Cases with little lateral extension of a tumor located below the Monro foramen have a good indication for the anteromedian surgical approach. With the anterior approach, the optic chiasm is located in front of the tumor. To avoid this obstacle, the tumor needs to be removed via the prechiasmatic space. If this space is narrow, the lamina terminalis is opened to allow the manipulations necessary for removal of the tumor from the inferior plane of the optic chiasm, but the manipulations on the reverse side of the optic chiasm are inevitably performed in a blind fashion when an anterior approach is applied. Techniques reported to resolve this problem include the posterior petrosal approach (1, 2, 15) and the endoscopic endonasal extended transsphenoidal approach (TSA) (3, 7, 11, 13). Comparison of the Basal Interhemispheric Approach and the Other Transcranial Approach The unilateral or bilateral subfrontal approach [Samii et al. (30), Yasargil et al.
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needed to achieve sufficient lateral development comparable to that possible with the bifrontal basal interhemispheric approach reported by Shibuya et al. (31). We also cut the anterior communicating artery in 1 of our 7 cases. Furthermore, if the area from the planum sphenoidale to the tuberculum sellae is drilled to open the sphenoid sinus, a sufficient working space can be secured not only in the lateral direction but also in the anterior direction, thereby expanding the operative field.
Figure 5. Case 1. Preoperative coronal (A) and sagittal (B) T1-weighted post-Gd magnetic resonance imaging studies showing retrochiasmatic multicystic craniopharyngioma. Postoperative coronal (C) and sagittal (D) T1-weighted post-Gd (gadolinium enhanced) magnetic resonance imaging studies showing gross total resection of the tumor.
(36)] is simple, does not require opening of the interhemispheric fissure, and has been used extensively. However, as compared to the interhemispheric approach, this strategy has several disadvantages, including the relatively narrow operative field, difficulty in opening the entire lamina terminalis, and the intense retraction of the frontal lobe, which is required (31-34). Shibuya et al. (31) compared the bifrontal basal interhemispheric approach (32) with unilateral approaches such as the pterional one used in surgery for large craniopharyngiomas, reporting that the basal interhemispheric approach was superior to other approaches in terms of preservation of the perforator and pituitary stalk and avoidance of bilateral hypothalamus injuries. They also highlighted the importance of visualizing the lateral aspect of the tumor via the interhemispheric approach (33), stating that favorable outcomes were
obtained by lateral expansion, achieved by cutting the anterior communicating artery in cases in which this artery was an obstacle to lateral expansion. Yasui et al. (37) reported a unilateral basal interhemispheric approach. According to their report, this approach is advantageous in that there is less injury of the bridging vein, and the opening of the interhemispheric fissure is small, allowing the operative time to be shortened and less brain damage to occur. Furthermore, they reported that their approach allows the upper part of the tumor extending into the third ventricle to be checked from a lower angle. Basically, we adopt the unilateral basal interhemispheric approach, involving incision of the unilateral dura mater, an approach similar to that reported by Yasui et al. (37). However, we have modified this approach by sufficiently resecting the crista galli and cutting the falx tip as
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Comparison of the Basal Interhemispheric Approach and the TSA Another possible strategy for accessing a craniopharyngioma from the inferior plane of the optic nerve is the TSA. Comparison of the TSA and basal interhemispheric approach reveals the former to be superior in terms of the manipulation for freeing the area from the inferior to the posterior plane of optic chiasm. This approach is advantageous in that the risk of perforator injury (from the posterior communicating artery, P1, etc.) or postoperative cranial nerve palsy is lower than with the posterior petrosal approach and other lateral or posterior approaches aimed at viewing the optic chiasm from its inferior plane. Komotar et al. (21) reviewed 88 reports involving 3470 cases and made comparisons among the endoscopic endonasal transsphenoidal, transsphenoidal purely microscope-based, and open transcranial microscope-based (OT) techniques. They concluded that the endoscopic endonasal transsphenoidal technique was safer and more effective for craniopharyngioma surgery than the other approaches. Consideration must, however, be given as the pterional approach was used for many of the OT group cases. Incomplete tumor removal due to poor sellar visualization was listed as one of the reasons for the low gross total resection rate in the OT group. If the transsphenoidal route we propose is adopted, a tumor located inside the sella turcica can be removed under direct vision. This supports the likelihood of improving the gross total resection rate with the OT technique. Reconstruction of Skull Base The technique presented herein, i.e., securing the space for manipulations by opening the planum sphenoidale and utilizing the sphenoid sinus, is expected to provide a valid operative procedure in cases
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beyond the dorsum sellae, adhesions with surrounding tissues developed after previous surgery, etc., and blood vessels have become incorporated into the tumor (8, 9, 29). Our approach is promising as a technique that is both safe and effective for treating craniopharyngiomas extending into the sella turcica and for resection of craniopharyngiomas affecting the inferior plane of the optic nerve where a sufficient prechiasmatic space cannot be secured. CONCLUSIONS
Figure 6. Case 2. Preoperative coronal (A) and sagittal (B) T1-weighted post-Gd (gadolinium enhanced) magnetic resonance imaging studies showing a cystic craniopharyngioma, part of which was accompanied by a solid lesion in the area from the sella turcica to the suprasellar region. Postoperative coronal (C) and sagittal (D) T1-weighted post-Gd magnetic resonance imaging studies showing gross total resection of the tumor.
in which manipulation on the inferior plane of the optic chiasm is inevitably performed in a blind fashion with a basal interhemispheric approach (a shortcoming of this approach), as well as in those in which a narrow prechiasmatic space makes tumor resection difficult from the anterior plane of the optic chiasm. A problem with this technique lies in the communication between the sphenoid sinus and the cerebrospinal fluid cavity with the potential to lead to postoperative infection or cerebrospinal fluid leakage. However, these complications were successfully prevented by 1) avoidance of sphenoid sinus mucosa injury at the time of opening the planum sphenoidale, 2) preservation of the dura mater of the planum sphenoidale as far as possible for subsequent utilization at the time of closure, and 3) multilayered reconstruction of the skull base using the galea and fibrin glue. Our present multilayered reconstruction is similar to the endoscopic endonasal transsphenoidal approach (EETSA) for craniopharyngioma resection (4, 13, 14, 16,
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19, 22, 27). Leng et al. (23) reported the development of extended TSAs has been mirrored by the development in skull base closure techniques. Their cerebrospinal fluid leakage rate of 3.8% is comparable to other approaches. Unilateral Basal Interhemispheric Approach Through the Sphenoid Sinus The unilateral basal interhemispheric approach through the sphenoid sinus to under the chiasmatic and intrasellar parts of the craniopharyngioma seems to provide a valid way of removing tumors that have extended from the inferior plane of the optic nerve to the sella turcica by means of expanding the prechiasmatic space. After the recent spread of the use of endoscopes, numerous reports have focused on the effectiveness of tumor removal by the EETSA, and this strategy has been widely adopted. However, there are many cases in which the interhemispheric approach is useful, e.g., those in which the EETSA is difficult when the tumor has extended
The basal interhemispheric approach is a useful surgical approach for craniopharyngiomas located in the median region. When used for removal of a tumor located in the blind angle on the inferior plane of the optic chiasm where operative manipulation is difficult, the manipulations for tumor removal may be facilitated by expansion of the prechiasmatic space, and the tumor inside the sella turcica can also be removed under direct vision if the planum sphenoidale is opened to allow effective utilization of the sphenoid sinus space, although this procedure still has some limitations. Furthermore, utilization of the thus-created space also enables the surgeon to use an endoscope for assessing and manipulating the inferior plane of the optic chiasm. REFERENCES 1. Al-Mefty O, Ayoubi S, Kadri PA: The petrosal approach for the resection of retrochiasmatic craniopharyngiomas. Neurosurgery 62:ONS331ONS335 [discussion ONS335-336], 2008. 2. Al-Mefty O, Ayoubi S, Kadri PA: The petrosal approach for the total removal of giant retrochiasmatic craniopharyngiomas in children. J Neurosurg 106:87-92, 2007. 3. Ali ZS, Lang SS, Kamat AR, Adappa ND, Palmer JN, Storm PB, Lee JY: Suprasellar pediatric craniopharyngioma resection via endonasal endoscopic approach. Childs Nerv Syst 29:2065-2070, 2013. 4. Cavallo LM, Prevedello D, Esposito F, Laws ER Jr, Dusick JR, Messina A, Jane JA Jr, Kelly DF, Cappabianca P: The role of the endoscope in the transsphenoidal management of cystic lesions of the sellar region. Neurosurg Rev 31:55-64 [discussion 64], 2008. 5. Ceylan S, Koc K, Anik I: Extended endoscopic approaches for midline skull-base lesions. Neurosurg Rev 32:309-319 [discussion 318-309], 2009. 6. Ciric IS, Tarkington J: Transsphenoidal microsurgery. Surg Neurol 2:207-212, 1974. 7. Couldwell WT, Weiss MH, Rabb C, Liu JK, Apfelbaum RI, Fukushima T: Variations on the
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 19 September 2013; accepted 8 February 2014 Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.02.005 Journal homepage: www.WORLDNEUROSURGERY.org
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