J Neurosurg 76:198-206, 1992
The extended frontal approach to tumors of the anterior, middle, and posterior skull base LALIGAM N. SEKnAn, M.D., ANJL NANDA,M.D., CHANDRA N. SEN, M.D., CAnL N. SNVI)EnMAN, M.D., AND IVO P. JANECKA,M.D.
Departments of Neurological Surgery and Ototaryngology, Center for Cranial Base Surgery, University of Piltsburgh School of Medicine, Pittsburgh, Pennsylvania The extended frontal approach is a modification of the transbasal approach of Derome. The addition of a bilateral orhitofrontal or orbitofrontoethmoidal osteotomy improves the exposure of midline lesions of the anterior, middle, and posterior skull base, while minimizing the need for frontal lobe retraction. The authors present a 5-year experience with 49 patients operated on via the extended frontal approach. In seven patients, the extended frontal approach was used alone; in the remaining 42, it was combined with other skull base approaches. Highly malignant tumors were removed en bloc, whereas benign tumors and low-grade malignancies were removed either en bloc or piecemeal. Reconstruction was usually performed using fascia lata, a pericranial flap, and/or autologous fat. A temporalis muscle flap or a distant microvascular free flap was required for some patients. One patient died 1 month postoperatively due to superior mesenteric artery thrombosis. Three patients had postoperative infections, two had cerebrospinal fluid leaks requiring reoperation, and four had brain contusions or hematomas. All but two patients recovered to their preoperative functional level. After an average followup period of 26 months (range 6 to 56 months), 64% of patients with benign lesions, 64% of patients with low-grade malignancies, and 44% of patients with high-grade lesions were alive with no evidence of disease. Kwv WOnDS
9 skull base tumor
y improved understanding of the surgical anatomy of the cranial base ~5 has produced innovations in the operative approaches to extensive skull base neoplasms. Such innovations have permitted the total or near-total excision of extensive tumors with minimal patient morbidity. 9 In this report, we describe a basal approach involving the addition of a bilateral orbitofrontal or orbitofrontoethmoidal osteotomy to a bifrontal craniotomy. This approach allows the surgeon access to midline structures of the anterior, middle, and posterior skull base with less brain retraction and a wider exposure. This approach is an extension of previously described approaches; the concept of performing an ethmoidectomy via the cranial exposure to approach middle and posterior skull base lesions is new.
A
Clinical Material and Methods
Patient Population During the period from April, 1986, to June, 1990, the extended frontal approach was used in a total of 49 patients. The patients ranged in age from 14 to 73 years, with a mean age of 46 years. There were 20 males and 29 females. The lesions for which the approach was used included two cerebrospinal fluid (CSF) fistulae, 198
9 extended frontal approach
surgical approach
nine benign tumors, 22 low-grade malignant tumors, and 16 high-grade malignant tumors (Table 1). Table 2 shows the location of the lesions with respect to the skull base and whether the approach was used alone or in combination with other approaches. Previously, 15 (31%) of these patients had undergone operations, excluding biopsies, 12 (25%) had received radiation therapy, and one had had chemotherapy. Postoperatively, radiation therapy was administered to 17 patients and chemotherapy to 10.
Preoperative Studies All patients underwent computerized tomography (CT) using bone algorithms and magnetic resonance imaging to define the extent of the lesion and the degree of involvement of brain, bone, and vascular structures. Arteriograms were obtained in 14 cases to determine the relationship of the major vessels to the tumor, the source of blood supply to the tumor, and the potential collateral channels available in the event of internal carotid artery (ICA) occlusion. In two cases of vascular tumors, preoperative embolization was performed. In four cases in which the ICA had been displaced and encased by the tumor, a balloon occlusion test of the
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Extended frontal approach to skull base tumors TABLE 1 Tumor diagnosis and patient status Diagnosis
Disease Status* No. of Cases NED AWD DOD DOC
benign lesion meningioma 4 2 (48) 1 (31) fl 1 (36) ossifyingfibroma 2 2 (27) 0 0 13 cranial defect 2 I (30) o o ] (]) chondroblastoma 1 i (45) 0 0 13 fibrous dysplasia 1 0 l (is) 0 13 inverted papilloma 1 I (22) 0 0 0 2 0 2 subtotal 11 7 low-grademalignancy chordoma 7 4 (32) 2(13) 1(29) 0 1 (22) esthesioneuro6 4 (27) I (13) 0 blastoma adenoid cystic 4 3 (31) 0 0 1 (24) carcinoma pituitaryadenoma 3 1 (44) 2 (26) 0 0 chondrosarcoma 2 2 (27) 0 0 0 5 1 2 subtotal 22 14 high-grademalignancy squamous-cell 7 3 (33) 1(23) 3(7) 0 carcinoma undifferentiated 2 0 1(24) 1 (36) 0 carcinoma adenocarcinoma 2 1 (33) 13 1 (12) 0 osteogenicsarcoma 2 2 (36) 0 0 0 melanoma 1 0 1 (43) 0 0 rhabdomyosarcoma 1 0 0 1 (10) 0 malignant fibrous l 1 (16) 13 0 0 histiocytoma subtotal 16 7 3 6 0 total cases 49 28 10 7 4 *Numbers in parentheses denote mean follow-up period in months. NED = no evidenceof disease;AWD = alivewithoutdisease; DOD = died of disease;DOC = died of other causes.
artery was performed with clinical evaluation and cerebral blood flow measurements. 6 Operative
Technique
Anesthesia, Monitoring, and Position A balanced endotracheal anesthetic technique is usually employed, unless there is a need for cranial nerve monitoring. The patient is placed in a supine position with the head fixed with pins. Since the head position may need to be changed during the operation, the head is placed on a horseshoe headrest and the endotracheal tube is secured to the dentition with No. 28 stainlesssteel wire. If temporary occlusion of the ICA is expected during the operation, monitoring of the somatosensory evoked responses and electroencephalography are utilized. If compression of the temporal lobe or the brain stem is possible during the operation, auditory brainstem evoked responses are also monitored. A CSF drain may be used to achieve brain relaxation, or the basal cisterns may be opened to release CSF during subffontal dissection. Intravenous furosemide and/or mannitol are administered when necessary. If
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TABLE 2 Operative approaches in relation to the area ( f the tumor* OperativeApproach
Anterior Anterior& Middle& Base MiddleBase PosteriorBase
extended frontal 6 t3 1 extended frontal & 15 12 (2) 0 transfacial extended frontal & 0 9 (3) 11 subtemporalinfratemporal extended frontal & 0 2 (2) 5 (5) transcavernous extended frontal & 0 0 0 other total cases 21 23 17 * Numbers in parentheses indicatethe number of approaches that overlappedwith other approaches.
excessive blood loss occurs during the operation, the anesthesiologist must maintain the replacement of red cells, coagulation factors, and platelets as needed. Prophylactic intravenous antibiotics and anticonvulsants are administered.
Craniotorny A bicoronal skin incision is made, extending from one zygomatic arch to the other. The incision should cross the vertex at least 15 cm above the lesion to allow for a pericranial flap of adequate length. The pericranium can be divided approximately 3 to 4 cm further posterior to the scalp incision if a longer flap is desired. The skin flap is dissected down to the supraorbital rims and the frontonasal suture. The supraorbital nerves and vessels may occasionally need to be released from their foramina by making cuts in the bone. The temporalis muscles are detached anteriorly and retracted with sutures. The periorbita is dissected from the roof of the orbit about 289 cm posteriorly and extending medially to the anterior ethmoidal artery. A low unilateral frontal craniotomy is performed, extending medially up to the sagittal sinus. The superior sagittal sinus is separated under direct vision, and a contralateral frontal craniotomy flap is then elevated. The next step is an orbitofrontal osteotomy for lesions located in the anterior fossa region or an orbitofrontoethmoidal osteotomy for lesions in the sphenoclival area.
Anterior Cranial Base Lesions Bilateral Fronto-Orbital Osteotomy. For anterior cranial base lesions, the orbital rims and the anterior two-thirds of the orbital roofs are removed, leaving the ethmoidal bone intact. After removal of CSF via a spinal drain, the subfrontal dura is dissected microsurgieally from the orbital roofs and from the planum sphenoidale. For benign tumors, the crista galli is removed. The dural sleeves of the olfactory groove area are cut on either side and closed primarily with sutures. With malignant tumors, the frontal dura is opened and di199
L. N. S e k h a r , el al. formed. The medial wall of the orbit, anteromedial to the optic nerves, is removed with rongeurs. The otolaryngologist exposes the tumor using a transfacial approach, such as a lateral rhinotomy or a midface degloving approach, and tumor resection is completed. For olfactory groove and planum sphenoidale meningiomas for which this approach is chosen, the anterior and posterior ethmoidal arteries are coagulated bilaterally in the orbit before craniotomy is performed in order to reduce the blood supply to the tumor. After the exposure, osteotomies are made, intradural and extradural tumor resection is performed, taking care to remove all hyperostotic bone and to unroof the optic nerve canals as needed. The anterior clinoid processes are more safely removed intradurally. When a malignant tumor involves the frontal lobe on only one side, partial resection of the frontal lobe may permit total tumor resection. This was done in three of our patients. Middle and Posterior Basal Tumors
FIG. I. Artist's drawings depicting a bilateral fronto-orbital craniotomy and osteotomy for a tumor of the anterior skull base. A: The order of removal of the cranial bones (1, 2, and 3). B: The exposure as seen from above for a malignant tumor after the craniotomy and osteotomy have been completed and some of the orbital roof has been resected. The dura has been preserved over the tumor to provide an additional tumor-free margin. CNI = first cranial nerve.
vided circumferentially around the olfactory groove area and around any tumor-involved dura. The olfactory tracts are divided, the frontal lobes are gently retracted, and the orbitofrontal osteotomies are made. The first orbital roof cuts are made from a superior to an inferior direction, protecting the dura and periorbita with malleable retractor b~ades and using a fine reciprocating saw (Fig. 1). The last cut is made through the nasion from an anterior to a posterior direction, angling the cut slightly upward such that it enters the anterior cranial fossa just in front of the crista galli. This fronto-orbital osteotomy piece is then loosened with an osteotome and removed. Tumor Resection. Further tumor resection will depend upon the biopsy of the tumor. Removal en bloc is attempted for malignant tumors, and benign tumors may be removed in a piecemeal fashion. For tumors of the ethmoid, the planum sphenoidale is penetrated with a high-speed drill, and a wide sphenoidotomy is per200
OrbitofrontoethmoidaI Osteotomy. For midline lesions of the middle and posterior skull base, the upper part of the ethmoidal bone is included in the segment of bone removed from exposure. The frontal dura and the periorbita are separated from the orbital bone as previously described. The coronal cut through the orbital roof is extended through the posterior aspect of the ethmoidal bone (Fig. 2), taking care not to penetrate to a depth of more than 2 or 3 ram. The horizontal osteotomy is then made through the nasal and ethmoidal bones at the level of the ethmoidal foramina, extending posteriorly to the anterior ethmoidal artery. This orbitofrontoethmoidal bone segment is further loosened with an osteotome and removed. The ethmoidal mucosa is quite vascular and will need to be coagulated via bipolar cautery. The anterior and posterior ethmoidal arteries are coagulated as well. For tumors of the clivus, further aggressive removal of the middle and posterior ethmoidal cells is performed. As more of these cells are removed, additional inferior parts of the clivus can be reached with no further brain retraction (Fig. 3). The medial wall of the orbit should also be removed near the orbital apex area to enlarge the exposure. Tumor Resection. Resection of middle and posterior basal tumors is usually performed in a piecemeal fashion. A sphenoidotomy is carried out as previously described. Depending upon the extent of the tumor, one or both of the optic nerves will need to be decompressed, except on the lateral aspect near the anterior clinoid process. The superior and lateral walls of the body of the sphenoid bone are then progressively removed from an anterior to a posterior direction, unroofing the sella. However, the dorsum sellae cannot be removed with this approach if it is very prominent or significantly involved by tumor. The cavernous sinuses and intracavernous ICA are completely unroofed on the medial aspect. The cavernous sinuses are protected Z Neurosurjr / Volume 76 /February, 1992
Extended frontal approach to skull base tumors
FIG. 3. Schematic drawing illustrating the improved exposure by the orbitofrontoethmoidal osteotomy (A) compared with the exposure obtained with the craniotomy alone (B). Note that the osteotomy also reduces brain retraction. Removal of the middle and posterior ethmoidal cells is necessary in order to reach the foramen magnum inferiorly. The dorsum sellae remains a blind spot.
FIG. 2. Artist's drawings depicting an orbitofrontoethmoidal craniotomy and osteolomy for a tumor of the middle or posterior skull base. A: The order of removal of the cranial bones (1, 2, and 3). B: Superior view of the orbitofrontoetbmoidal osteotomy. C: The exposure obtained after the osteotomy and early dissection. Note the removal of the middle and posterior ethmoidal cells. CNII = second cranial nerve.
medially by a thin periosteal layer, but this may be torn during the dissection or may need to be intentionally opened if there is tumor invasion. In such cases, venous bleeding is controlled by packing with rolls of Surgicel. The anterior vertical and posterior vertical segments of the intracavernous ICA can be exposed for about threeJ. Neurosurg. / Volume 76 /February, 1992
quarters of their circumference. The cavernous ICA is followed along the posterior vertical segment to the point where it enters the cavernous sinuses, permitting resection of some of the petrous apex. In this lateral corner, caution must be exercised not to disturb the sixth cranial nerve as it travels extradurally from the dura of the clivus to enter the cavernous sinus through Dorello's canal. The anterior wall of the body of the sphenoid bone can also be resected from this approach, but the surgeon should be careful not to penetrate the wall of the nasopharynx anterior to the bone. The clival tumor and bone are progressivciy removed from a superior to an inferior direction. The clival dura is thick in young and middle-aged individuals, but may be quite thin in older patients or as a result of tumor invasion. In cases where the clival dura is thin, care must be taken not to injure the basilar artery, its branches, or the brain stem. Considerable venous bleeding may occur from the basilar venous plexus, but can be controlled with Surgicel packs. In tumors such as chordomas, the bone resection should extend at least 1 cm beyond radiologically and surgically visible tumor margins, if possible. The lower limit of resection by this approach is the foramen magnum. At the foramen magnum, the resection can be extended laterally up to the hypoglossal canals. Reconstruction Dural defects in the anterior skull base are closed by primary suture or with a graft of fascia lata or parietal 203
L. N. Sekhar, et al. defects following surgery that may have included orbital exenteration and/or maxillectomy, the additional transfer of a temporalis muscle rotational flap or a vascularized free flap is necessary. The purpose of this transfer is to obliterate dead space with vascularized tissues, to prevent CSF leak, to protect an exposed ICA from subsequent infection and rupture, and to facilitate improved cosmesis.~3'23 The orbitofrontal bone segment is replaced after removal of small segments of bone inferiorly to prevent compression of the pericranial flap. It is secured with 2-0 Neurilon sutures or titanium miniplates. Reapproximation of the orbitofrontal osteotomy piece has not resulted in any cosmetic deformities in our series. We found that routine reconstruction of the bone of the ethmoidal and sphenoclival area, as described by Derome, et al., 5 was not necessary unless extensive resection of the medial orbital wall was required during tumor resection. The remainder of the closure follows standard techniques. A subgaleal drain to gravity is left in place for 24 to 48 hours. In cases where the dural closure is tenuous, lumbar spinal drainage is continued for 48 hours postoperatively, draining no more than 50 cc CSF every 8 hours. A CT scan is performed 24 hours after the procedure to detect any asymptomatic complications.
FIG. 4. Artist's drawingsdemonstrating the application of the pericranial flap for reconstruction. CNII = second cranial nerve. Upper:Side view. Note that a fat graft is also placed in the sphenoid and ethmoid sinuses. Lower. View from above.
pericranium. For dural defects of the middle or posterior skull base, a fascia lata graft is used to cover the entire area and is attached with sutures or titanium hemoclips; watertight closure is not possible. The mucosa of the frontal sinus and sphenoid sinus is exenterated. The frontonasal duct and the exposed ethmoidal air cells are packed with small pieces of fat. A long pericranial flap supplied by the supraorbital and supratrochlear vessels is then developed and placed into the tumor resection cavity, reaching the margins of the bone resection. This flap lies between the orbitofrontal bone segment and the ethmoidal sinuses, providing a longer reach, vascularity for the bone segment, and an effective barrier against infection (Fig. 4). Autologous fat is then packed between the fascia lata graft and the pericranial flap or into a pocket of the pericranial flap to occlude the dead space. Overpacking should be avoided since compression of the optic nerve or the brain stem may result. If the patient has previously undergone a bicoronal incision close to the hair line, the length of the pericranial flap is restricted. In such patients, a galeofrontalis flap can be utilized. 2~ In patients with much larger 202
Combination With Other Approaches Patients with highly malignant lesions of the craniofacial area need circumferential exposure of the tumor to permit en bloc resection. While the extended frontal approach provides adequate exposure of the superior aspect of the tumor, the inferior aspect is not exposed. This exposure is usually achieved during the same operation by the otolaryngologist via a transfacial route. A lateral rhinotomy/transethmoidal approach, a midfacial degloving operation, a maxillotomy technique, or a maxillectomy approach is usually selected, depending upon the size and location of the tumor. 4'12If the orbit is involved by a highly malignant tumor, orbital exenteration may also be necessary. For lesions that extend laterally into the petrous bone, the greater wing of the sphenoid, or the infratemporal fossa, the extended frontal approach is combined with an extradural subtemporal-transzygomatic or subtemporal-infratemporal approach. 2~ Resection of the upper part of the dorsum sellae may require an intradural-subtemporal approach. Illustrative Cases Case 1: Anterior and Middle Basal Meningioma
This 70-year-old man had previously undergone three operations and radiation therapy in an attempt to control the growth of a meningioma of the anterior and middle skull base (Fig. 5 upper). He presented with progressive loss of vision and recurrent tumor extending extradurally into the sphenoethmoidal area. The tumor was totally removed via an extended frontal approach (Fig. 5 lower). His vision was unchanged after J. Neurosurg. / Volume 76 / February, 1992
Extended frontal approach to skull base tumors
FIG. 5. Magnetic resonance Trweighted images in Case 1.
Upper: Preoperative sagittal (left) and coronal (right) images showing a tumor involving the anterior and middle cranial base, There is also an obstruction of the sphenoid sinus with the formation of a mucocele. Lower: Postoperative sagittal (left) and coronal (right) images demonstrating the absence of tumor. Despite some autologous cranial bone reconstruction of the frontal area, there is a slight depression due to extensive bone loss from multiple operations and radiation therapy.
the operation; however, it progressively worsened over a period of 6 months despite the absence of tumor, presumably due to a delayed effect of radiation. He remains independent, active, and free of tumor 4 years later.
Case 2: Middle and Posterior Basal Chordoma This 73-year-old woman had previously undergone partial resection of a sphenoclival chordoma by a transseptal transsphenoidal approach and had received 6000 rad of external beam radiotherapy. However, the tumor continued to grow causing visual deterioration (Fig. 6 upper). An extended frontal approach was utilized for total excision of the tumor, which extended inferiorly to the foramen magnum and laterally to the petrous apices. The clival dura had to be resected (Fig. 6 lower). The patient remains well and disease-free 36 months postoperatively.
Case 3: Extensive Clival Chordoma This 54-year-old woman was referred to us with a clival chordoma involving the entire clivus, both occipital condyles, the fight jugular foramen, the petrous apex region, and the right cavernous sinus area (Fig. 7). Diagnosis had been established by transsphenoethmoidal surgery. The initial tumor resection was performed via an extended frontal approach combined with a subtemporal-infratemporal approach. A fistula extend-
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l:ic. 6. Magnetic resonance TL-weighted images in Case 2.
Upper: Preoperative sagittal (left) and coronal (right) images showing a tumor predominantly involving the upper and middle clivus and the sphenoid bone. Lower: Postoperative sagittal (left) and coronal (right) images showing the absence &tumor and lhe presence of the fat used in the reconstruction along with the pericranial flap.
ing from the pharynx to the middle ear developed due to the inadequacy of the repair and possibly related to the prior transethmoidal operation (Fig. 8). The patient underwent a second operation via an extreme lateral approach to remove additional tumor; reconstruction with a temporali~ muscle flap was performed to close the fistula (Fig. 8). An occiput to C I - 2 fusion was performed at a later date to enable both tumor-involved condyles to be removed. A subsequent intradural transcavernous operation was necessary to resect tumor residue in the cavernous sinuses. The patient is free of tumor 12 months later, and has returned to work. This case is presented as an example of a petroclival tumor that is too large to be removed by a single approach, and to illustrate a potential complication and its management. Results
Follow-Up Resulls The patients in our series were followed for an average of 26 months, ranging from 6 to 56 months. The disease status of patients at follow-up review is shown in Table 1. Seven (64%) of the l 1 patients with benign lesions, 14 (64%) of the 22 patients with low-grade malignancies, and seven (44%) of the 16 patients with high-grade malignancies were alive with no evidence of disease. With the exception of one patient who died and another with an intracerebral contusion and de203
L. N. Sekhar, et al.
FIG. 8. Postoperative studies in Case 3. a: Enhanced computerized tomography scan demonstrating an air-filled communication from the sphenoid and retropharyngeal area from where the tumor was removed to the tympanicondylar area. This failure of reconstruction reflects inadequate vascularity to the area postoperatively, b: Enhanced magnetic resonance image obtained after resection of the remaining tumor and reconstruction of the tumor cavity with a temporalis muscle flap.
FIG. 7. Preoperative magnetic resonance images in Case 3. T2-weighted axial (a) and enhanced sagitlal (b) images and T~-weighted axial (c) and enhanced axial (d) images showing a clival chordoma involving the entire clivus, both occipital condyles, the right jugular foramen, the petrous apex region, and the right cavernous sinus area. The patient's initial operation was an extended frontal approach combined with a subtemporal-infratemperal approach. Because of the extensive nature of the tumor, further operations using different approaches were necessary to achieve complete tumor removal.
layed epidural abscess, the patients had returned to their preoperative functional status within 2 months after surgery.
Complications Postoperative complications are shown in Tables 3 and 4. One patient, who underwent an uncomplicated repair of a spontaneous CSF fistula, was readmitted 3 weeks after discharge and died of superior mesenteric artery thrombosis. This was believed to be unrelated to the operation. Postoperative CSF leaks occurred in two patients with intra- and extradural tumors. In both of these cases, large dural defects were inadequately repaired during the operation and the patients developed postoperative hydrocephalus. Repair was accomplished with a fascia lata and autologous fat graft and insertion of CSF shunts. Three patients developed frontal lobe contusion or edema. In one elderly patient with a large tumor, the dura was badly torn and some bridging veins of the frontal lobe were injured during the craniotomy. A second patient had tumor invasion of the frontal lobe and the third had severe scarring from a previous operation. All three patients were managed with steroid 204
and diuretic agents. A temporal lobe hematoma requiring reoperation occurred in one patient with an extensive adenoid cystic carcinoma that had necessitated the addition of a subtemporal-infratemporal approach in order to remove tumor. Postoperative infection occurred in three patients, all of whom had undergone a transfacial approach in addition to the extended frontal approach. One epidural abscess developed 1 year postoperatively in an elderly woman with a large esthesioneuroblastoma. The reconstruction in this patient had been suboptimal because of her age, the size of tumor, and the thin pericranial flap. She required removal of the frontal bone flap and administration of intravenous antibiotics. A second patient was suspected of having an epidural infection, but cultures of the epidural fluid were sterile. He was treated with antibiotics and did not undergo bone removal. The third patient was Case 3 (reported above), who developed a pharyngotympanic fistula. When epidural infection occurs, we remove the bone flap, but leave the orbitofrontal osteotomy segment. Since this bone is thin and in close contact with vascularized tissue, it appears to vascularize quickly and does not act as a sequestrum. Two patients suffered severe temporary neurological deterioration due to inadvertent excessive lumbar CSF drainage. One elderly patient became severely obtunded, but recovered after the drain was shut off. A middle-aged patient developed uncal herniation, requiting a partial temporal lobectomy and section of the tentorium; recovery was complete. Consequently, we have been very cautious in the use of the lumbar CSF drainage and regulate the drainage by strict volumetric limits. Cranial nerve deterioration or palsy was seen in eight patients, and was temporary in four and permanent in
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Extended frontal approach to skull base tumors TABLE 3 Complications Jblhm ing ~v~tendedfrontal surger)' [br tumor~ ~?/ the skull base No. of No. of Cases LaterOps
Complication
superior mesenteric arteD'thrombosis* 1 0 cerebrospinal fluid leak 2 2 frontal lobe contusion or edema'~ 3 0 temporal lobe hematoma 1 1 epidural abscessor infection 2 2 pharyngotympanicfistula 1 1 neurologicaldeterioratJon:~ 2 1 postoperative seizure 3 0 temporary,weightloss 4 0 * Complication resulted in death of patient. t Complicationresulted in permanent disability for one patient. { Complication was due to excessive lumbar cerebrospinal fluid drainage.
TABLE 4 Cranial nerve deterioralion or palsy fidlowing frontal surgery for tumors of the skull base No. of Cases
Cranial Nerve
Temporary 0 0 0 0 2 1 1
2nd 3rd-6th ath 5th 6th 7th 9th, 10th, & 12th
Permanent 1 1 1 1 0 0 0
four (Table 4). Deterioration of the second cranial nerve function occurred postoperatively in one patient with an osseous meningioma that was severely compressing the optic nerve. Deterioration of the second through sixth cranial nerves in one patient with a pituitary adenoma was related to intracavernous tumor removal. One patient suffered trochlear muscle dysfunction, presumably due to the orbitofrontal osteotomy, but compensated without difficulty. The outcome of patients who sustained complications was generally favorable. Except for one patient who died due to superior mesenteric artery thrombosis and another patient who developed a delayed epidural infection and subsequently remained dependent for daily living activities, the patients returned to their previous functional status within 4 to 8 weeks after surgery. Discussion
Historical Perspective
The concept of removal of the orbital rims to improve exposure of the skull base was introduced by Frazier in 1913. 7 Derome, et al., 5 described the transbasal approach to the skull base in 1972. The use of J. Neurosurg. / Volume 76/February, 1992
orbital osteotomies to approach a number of lesions was further developed by Jane, et al., ~ Jackson, et al., ~,") and many recent authors. L2"Sa6'2~ We have expanded these approaches for the treatment of midline cranial base lesions by the addition of ethmoidectomy. A combined transcranial transfacial approach to retinoblastoma was first described by Ray and McLean ~ in 1943. This combined approach was applied to paranasal sinus malignancies in 1954 by Smith, et al., 2: in 1966 by Ketcham, et al., ~4 and in 1968 by Van Buren, et al. 26 The incidence of postoperative infection, CSF leakage, and death was high; however, these series demonstrated the utility of the surgical techniques in producing long-term survivors for tumors previously considered inoperable. Value o f E x t e n d e d Frontal Approach
For anterior skull base lesions, the orbitofrontal osteotomy is not a prerequisite, as shown in recent series. 3,~7,19"22"24However, by removal of basicranial bone close to the surgeon's line of vision and retraction of the orbital tissues, exposure of the tumor is improved and frontal lobe retraction is reduced. When the tumor does not extend inferiorly below the ethmoid sinuses the extended frontal approach is used alone, and the lesion is removed piecemeal. For en bloc resection of highly malignant lesions, this approach needs to be combined with a transfacial approach to obtain circumferential exposure. For middle or posterior skull base lesions, this approach can be used alone when the lesion is in the midline and involves the upper and middle clivus. A clivus lesion located as low as the foramen magnum can be resected if it is an inferior extension of a middle clival tumor. When a midline lesion is predominantly located in the middle or lower clival region, a maxillotomy or a transoral approach will provide adequate exposure. These approaches can also be combined with an extended frontal approach during the same operation. For sphenoclival lesions, the advantage of this approach lies in the excellent exposure of the optic nerve, the sphenoid sinus, and the medial aspect of the cavernous sinuses. Even if the cavernous ICA is injured, the approach is wide and shallow enough to allow direct repair (LN Sekhar, unpublished data). Additionally, the reconstruction described in this paper allows the excision of clival dura with no major risk of CSF leakage. The risk of postoperative infection is also greatly reduced by the vascularized flaps and the elimination of dead space. L i m i t a t i o n s o f E x t e n d e d Frontal Approach
Bilateral olfactory denervation is a necessary sequel to this approach. Although well tolerated by most patients, the sense of smell and flavor of taste may be essential for a patient's occupation. The lateral extension of this approach is limited by the optic nerves, 205
L. N. Sekhar, etal. cavernous sinuses, petrous apices, abducens nerves, and hypoglossal canals, Tumors that extend further laterally require the combination of a Iateral approach such as the subtemporal-infratemporal technique. As noted by Derome, etal. 5 the dorsum sellae is a blind spot behind the sella turcica and cannot be resected by this approach if it is very prominent. The field increases in depth and narrows as the foramen magnum is approached.
Alternative Approaches Alternative approaches available to the surgeon for the resection of sphenoclival lesions include the transethmoidal, the transseptal-transsphenoidal, the unilateral maxillotomy, 2 the facial translocation,~2 the Le Fort I maxillotomy, 25 and the transoral approaches. While some of these approaches provide wide exposure of sphenoclival lesions, exposure of the optic nerves and the cavernous sinus areas is limited or absent. Except for the maxillotomy and facial translocation approaches, vascularized flap reconstruction is not possible. However, the surgeon should be familiar with all of these approaches and should select the best one based on the patient's need and the surgeon's experience. Conclusions Regardless of the approach utilized and the nuances of surgical resection, the most important issues to be considered are postoperative complications and the long-term outcome. Even though the majority of the tumors reported here were large and extensive, the complication rates were acceptable. The follow-up resuits with respect to tumor control are promising, but require further long-term documentation. Acknowledgments The authors thank Tern Pacella for typing the manuscript and assisting in data gathering, Lois Burkhart for assisting with the data collection, and Joan Nilson for providing editorial assistance. References 1. Ala~,~vanM, Sindou M: Fronto-temporal approach with orbito-zygomatic removal. Surgical anatomy. Acta Neuroehir 104:79-83, 1990 2. AI-Mefty O: The supraorbital-pterionai approach to skull base lesions. Neurosurgery 21:474-477, 1987 3. Blacklock JB, Weber RS, Lee YY, etal: Transcranial resection of tumors of the paranasal sinuses and nasal cavity. J Neurosurg 71:10-15, 1989 4. Cocke EW Jr, Robertson JH, Robertson JT, et at: The extended maxillotomy and subtotal maxillectomy for excision of skull base tumors. Arch Otolaryngol Head Neck Surg 116:92-104, 1990 5. Derome P, Akerman M, Anquez L, et al: Les tumeurs spheno-ethmoidales. Possibilit~s d'ex~rNse et de r~paration chirurgicales. Neurochirurgie (Suppl) 18:1-164, 1972 6. Erba SM, Horton JA, Latchaw RE, et al: Balloon test occlusion of the internal carotid artery with stable xenon/ CT cerebral blood flow imaging. AJNR 9:533-538, 1988 7. Frazier CH: An approach to the hypophysis through the anterior cranial fossa. Ann Surg 57:145-150, 1913 906
8. Hakuba A, Liu SS, Nishimura S: The orbitozygomatic infratemporal approach: a new surgical technique. Surg Neurol 26:271-276, 1986 9. Jackson IT: Craniofacial osteotomies to facilitate resection of tumors of the skull base, in Wilkins RH, Rengachary S (eds): Neurosurgery Update I. New York: McGraw-Hill, 1990, pp 277-291 10. Jackson IT, Marsh WR, Hide TA: Treatment of tumors involving the anterior cranial fossa. Head Neck Surg 6: 901-913, 1984 11. Jane JA, Park TS, Pobereskin LH, el al: The supraorbital approach: technical note. Neurosurgery 11:537-542, 1982 12. Janecka IP, Sen CN, Sekhar LN, et al: Facial translocation: a new approach to the cranial base. Otolaryngol Head Neck Surg 103:413-419, 1990 13. Jones NF, Schramm VL, Sekhar LN: Reconstruction of the cranial base following tumour resection. Br J Plast Surg 40:155-162, 1987 14. Ketcham AS, Hoye RC, Van Buren JM, etal: Complications of intracranial facial resection for tumors of the paranasal sinuses. Am J Surg 112:591-596, 1966 15. Lang J: Anterior cranial base anatomy, in Sekhar LN, Schramm VL Jr (eds): Tumors of the Cranial Base. Diagnosis and Treatment. Mt Kisco, NY: Futura, 1987, pp 247-264 16. Lesoin F, Pellerin P, Villette L, etal: IntNr& de la mobilisation du volet orbito-zygomatico-malaire. Neurochirurgie 32:90-93, 1986 17. Persing JA, Jane JA, Levine PA, et at: The versatile frontal sinus approach to the floor of the anterior cranial fossa. Technical note. J Neurosurg 72:513-516, 1990 18. Ray BS, McLean JM: Combined intracranial and orbital operation for retinoblastoma. Arch Ophthalmol 30: 437-445, 1943 19. Schramm VL Jr, Myers EN, Maroon JC: Anterior skull base surgery for benign and malignant disease. Laryngoscope 89:1077-1091, 1979 20. Sekhar LN, Janecka IP, Jones NF: Subtemporal-infratemporal and basal subfrontal approach to extensive cranial base tumours. Acta Neurochir 92:83-92, 1988 21. Sekhar LN, Sen CN, Jho HD, et al: Surgical treatment of intracavernous neoplasms: a four-year experience. Neurosurgery 24:18-30, 1989 22. Smith RR, Kiopp CT, Williams JM: Surgical treatment of cancer of the frontal sinus and adjacent areas. Cancer 7:991-994, 1954 23. Snyderman CH, Janecka IP, Sekhar LN, el al: Anterior cranial base reconstruction: role of galeal and pericranial flaps. Laryngoscope 100:607-614, 1990 24. Sundaresan N, Shah JP: Craniofacial resection for anterior skull base tumors. Head Neck Surg 10:219-224, 1988 25. Uttley D, Moore A, Archer DJ: Surgical management of midline skull-base tumors: a new approach. J Neurosurg 71:705-710, 1989 26. Van Buren JM, Ommaya AK, Ketcham AS: Ten years' experience with radical combined craniofacial resection of malignant tumors of the paranasal sinuses. J Neurosurg 28:341-350, 1968
Manuscript received March 13, 1991. Accepted in final form July 25, 1991. Address for Dr. Nanda: Louisiana State University, Department of Neurosurgery, 1501 Kings Highway, Shreveport, Louisiana. Address reprint requests to: Laligam N. Sekhar, M.D., Department of Neurosurgery, Presbyterian University Hospital, 230 Lothrop Street, Pittsburgh, Pennsylvania 15213.
J. Neurosurg. / Volume 76/February, 1992
The extended frontal approach to tumors of the anterior, middle, and posterior skull base LALIGAM N. SEKnAn, M.D., ANJL NANDA,M.D., CHANDRA N. SEN, M.D., CAnL N. SNVI)EnMAN, M.D., AND IVO P. JANECKA,M.D.
Departments of Neurological Surgery and Ototaryngology, Center for Cranial Base Surgery, University of Piltsburgh School of Medicine, Pittsburgh, Pennsylvania The extended frontal approach is a modification of the transbasal approach of Derome. The addition of a bilateral orhitofrontal or orbitofrontoethmoidal osteotomy improves the exposure of midline lesions of the anterior, middle, and posterior skull base, while minimizing the need for frontal lobe retraction. The authors present a 5-year experience with 49 patients operated on via the extended frontal approach. In seven patients, the extended frontal approach was used alone; in the remaining 42, it was combined with other skull base approaches. Highly malignant tumors were removed en bloc, whereas benign tumors and low-grade malignancies were removed either en bloc or piecemeal. Reconstruction was usually performed using fascia lata, a pericranial flap, and/or autologous fat. A temporalis muscle flap or a distant microvascular free flap was required for some patients. One patient died 1 month postoperatively due to superior mesenteric artery thrombosis. Three patients had postoperative infections, two had cerebrospinal fluid leaks requiring reoperation, and four had brain contusions or hematomas. All but two patients recovered to their preoperative functional level. After an average followup period of 26 months (range 6 to 56 months), 64% of patients with benign lesions, 64% of patients with low-grade malignancies, and 44% of patients with high-grade lesions were alive with no evidence of disease. Kwv WOnDS
9 skull base tumor
y improved understanding of the surgical anatomy of the cranial base ~5 has produced innovations in the operative approaches to extensive skull base neoplasms. Such innovations have permitted the total or near-total excision of extensive tumors with minimal patient morbidity. 9 In this report, we describe a basal approach involving the addition of a bilateral orbitofrontal or orbitofrontoethmoidal osteotomy to a bifrontal craniotomy. This approach allows the surgeon access to midline structures of the anterior, middle, and posterior skull base with less brain retraction and a wider exposure. This approach is an extension of previously described approaches; the concept of performing an ethmoidectomy via the cranial exposure to approach middle and posterior skull base lesions is new.
A
Clinical Material and Methods
Patient Population During the period from April, 1986, to June, 1990, the extended frontal approach was used in a total of 49 patients. The patients ranged in age from 14 to 73 years, with a mean age of 46 years. There were 20 males and 29 females. The lesions for which the approach was used included two cerebrospinal fluid (CSF) fistulae, 198
9 extended frontal approach
surgical approach
nine benign tumors, 22 low-grade malignant tumors, and 16 high-grade malignant tumors (Table 1). Table 2 shows the location of the lesions with respect to the skull base and whether the approach was used alone or in combination with other approaches. Previously, 15 (31%) of these patients had undergone operations, excluding biopsies, 12 (25%) had received radiation therapy, and one had had chemotherapy. Postoperatively, radiation therapy was administered to 17 patients and chemotherapy to 10.
Preoperative Studies All patients underwent computerized tomography (CT) using bone algorithms and magnetic resonance imaging to define the extent of the lesion and the degree of involvement of brain, bone, and vascular structures. Arteriograms were obtained in 14 cases to determine the relationship of the major vessels to the tumor, the source of blood supply to the tumor, and the potential collateral channels available in the event of internal carotid artery (ICA) occlusion. In two cases of vascular tumors, preoperative embolization was performed. In four cases in which the ICA had been displaced and encased by the tumor, a balloon occlusion test of the
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Extended frontal approach to skull base tumors TABLE 1 Tumor diagnosis and patient status Diagnosis
Disease Status* No. of Cases NED AWD DOD DOC
benign lesion meningioma 4 2 (48) 1 (31) fl 1 (36) ossifyingfibroma 2 2 (27) 0 0 13 cranial defect 2 I (30) o o ] (]) chondroblastoma 1 i (45) 0 0 13 fibrous dysplasia 1 0 l (is) 0 13 inverted papilloma 1 I (22) 0 0 0 2 0 2 subtotal 11 7 low-grademalignancy chordoma 7 4 (32) 2(13) 1(29) 0 1 (22) esthesioneuro6 4 (27) I (13) 0 blastoma adenoid cystic 4 3 (31) 0 0 1 (24) carcinoma pituitaryadenoma 3 1 (44) 2 (26) 0 0 chondrosarcoma 2 2 (27) 0 0 0 5 1 2 subtotal 22 14 high-grademalignancy squamous-cell 7 3 (33) 1(23) 3(7) 0 carcinoma undifferentiated 2 0 1(24) 1 (36) 0 carcinoma adenocarcinoma 2 1 (33) 13 1 (12) 0 osteogenicsarcoma 2 2 (36) 0 0 0 melanoma 1 0 1 (43) 0 0 rhabdomyosarcoma 1 0 0 1 (10) 0 malignant fibrous l 1 (16) 13 0 0 histiocytoma subtotal 16 7 3 6 0 total cases 49 28 10 7 4 *Numbers in parentheses denote mean follow-up period in months. NED = no evidenceof disease;AWD = alivewithoutdisease; DOD = died of disease;DOC = died of other causes.
artery was performed with clinical evaluation and cerebral blood flow measurements. 6 Operative
Technique
Anesthesia, Monitoring, and Position A balanced endotracheal anesthetic technique is usually employed, unless there is a need for cranial nerve monitoring. The patient is placed in a supine position with the head fixed with pins. Since the head position may need to be changed during the operation, the head is placed on a horseshoe headrest and the endotracheal tube is secured to the dentition with No. 28 stainlesssteel wire. If temporary occlusion of the ICA is expected during the operation, monitoring of the somatosensory evoked responses and electroencephalography are utilized. If compression of the temporal lobe or the brain stem is possible during the operation, auditory brainstem evoked responses are also monitored. A CSF drain may be used to achieve brain relaxation, or the basal cisterns may be opened to release CSF during subffontal dissection. Intravenous furosemide and/or mannitol are administered when necessary. If
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TABLE 2 Operative approaches in relation to the area ( f the tumor* OperativeApproach
Anterior Anterior& Middle& Base MiddleBase PosteriorBase
extended frontal 6 t3 1 extended frontal & 15 12 (2) 0 transfacial extended frontal & 0 9 (3) 11 subtemporalinfratemporal extended frontal & 0 2 (2) 5 (5) transcavernous extended frontal & 0 0 0 other total cases 21 23 17 * Numbers in parentheses indicatethe number of approaches that overlappedwith other approaches.
excessive blood loss occurs during the operation, the anesthesiologist must maintain the replacement of red cells, coagulation factors, and platelets as needed. Prophylactic intravenous antibiotics and anticonvulsants are administered.
Craniotorny A bicoronal skin incision is made, extending from one zygomatic arch to the other. The incision should cross the vertex at least 15 cm above the lesion to allow for a pericranial flap of adequate length. The pericranium can be divided approximately 3 to 4 cm further posterior to the scalp incision if a longer flap is desired. The skin flap is dissected down to the supraorbital rims and the frontonasal suture. The supraorbital nerves and vessels may occasionally need to be released from their foramina by making cuts in the bone. The temporalis muscles are detached anteriorly and retracted with sutures. The periorbita is dissected from the roof of the orbit about 289 cm posteriorly and extending medially to the anterior ethmoidal artery. A low unilateral frontal craniotomy is performed, extending medially up to the sagittal sinus. The superior sagittal sinus is separated under direct vision, and a contralateral frontal craniotomy flap is then elevated. The next step is an orbitofrontal osteotomy for lesions located in the anterior fossa region or an orbitofrontoethmoidal osteotomy for lesions in the sphenoclival area.
Anterior Cranial Base Lesions Bilateral Fronto-Orbital Osteotomy. For anterior cranial base lesions, the orbital rims and the anterior two-thirds of the orbital roofs are removed, leaving the ethmoidal bone intact. After removal of CSF via a spinal drain, the subfrontal dura is dissected microsurgieally from the orbital roofs and from the planum sphenoidale. For benign tumors, the crista galli is removed. The dural sleeves of the olfactory groove area are cut on either side and closed primarily with sutures. With malignant tumors, the frontal dura is opened and di199
L. N. S e k h a r , el al. formed. The medial wall of the orbit, anteromedial to the optic nerves, is removed with rongeurs. The otolaryngologist exposes the tumor using a transfacial approach, such as a lateral rhinotomy or a midface degloving approach, and tumor resection is completed. For olfactory groove and planum sphenoidale meningiomas for which this approach is chosen, the anterior and posterior ethmoidal arteries are coagulated bilaterally in the orbit before craniotomy is performed in order to reduce the blood supply to the tumor. After the exposure, osteotomies are made, intradural and extradural tumor resection is performed, taking care to remove all hyperostotic bone and to unroof the optic nerve canals as needed. The anterior clinoid processes are more safely removed intradurally. When a malignant tumor involves the frontal lobe on only one side, partial resection of the frontal lobe may permit total tumor resection. This was done in three of our patients. Middle and Posterior Basal Tumors
FIG. I. Artist's drawings depicting a bilateral fronto-orbital craniotomy and osteotomy for a tumor of the anterior skull base. A: The order of removal of the cranial bones (1, 2, and 3). B: The exposure as seen from above for a malignant tumor after the craniotomy and osteotomy have been completed and some of the orbital roof has been resected. The dura has been preserved over the tumor to provide an additional tumor-free margin. CNI = first cranial nerve.
vided circumferentially around the olfactory groove area and around any tumor-involved dura. The olfactory tracts are divided, the frontal lobes are gently retracted, and the orbitofrontal osteotomies are made. The first orbital roof cuts are made from a superior to an inferior direction, protecting the dura and periorbita with malleable retractor b~ades and using a fine reciprocating saw (Fig. 1). The last cut is made through the nasion from an anterior to a posterior direction, angling the cut slightly upward such that it enters the anterior cranial fossa just in front of the crista galli. This fronto-orbital osteotomy piece is then loosened with an osteotome and removed. Tumor Resection. Further tumor resection will depend upon the biopsy of the tumor. Removal en bloc is attempted for malignant tumors, and benign tumors may be removed in a piecemeal fashion. For tumors of the ethmoid, the planum sphenoidale is penetrated with a high-speed drill, and a wide sphenoidotomy is per200
OrbitofrontoethmoidaI Osteotomy. For midline lesions of the middle and posterior skull base, the upper part of the ethmoidal bone is included in the segment of bone removed from exposure. The frontal dura and the periorbita are separated from the orbital bone as previously described. The coronal cut through the orbital roof is extended through the posterior aspect of the ethmoidal bone (Fig. 2), taking care not to penetrate to a depth of more than 2 or 3 ram. The horizontal osteotomy is then made through the nasal and ethmoidal bones at the level of the ethmoidal foramina, extending posteriorly to the anterior ethmoidal artery. This orbitofrontoethmoidal bone segment is further loosened with an osteotome and removed. The ethmoidal mucosa is quite vascular and will need to be coagulated via bipolar cautery. The anterior and posterior ethmoidal arteries are coagulated as well. For tumors of the clivus, further aggressive removal of the middle and posterior ethmoidal cells is performed. As more of these cells are removed, additional inferior parts of the clivus can be reached with no further brain retraction (Fig. 3). The medial wall of the orbit should also be removed near the orbital apex area to enlarge the exposure. Tumor Resection. Resection of middle and posterior basal tumors is usually performed in a piecemeal fashion. A sphenoidotomy is carried out as previously described. Depending upon the extent of the tumor, one or both of the optic nerves will need to be decompressed, except on the lateral aspect near the anterior clinoid process. The superior and lateral walls of the body of the sphenoid bone are then progressively removed from an anterior to a posterior direction, unroofing the sella. However, the dorsum sellae cannot be removed with this approach if it is very prominent or significantly involved by tumor. The cavernous sinuses and intracavernous ICA are completely unroofed on the medial aspect. The cavernous sinuses are protected Z Neurosurjr / Volume 76 /February, 1992
Extended frontal approach to skull base tumors
FIG. 3. Schematic drawing illustrating the improved exposure by the orbitofrontoethmoidal osteotomy (A) compared with the exposure obtained with the craniotomy alone (B). Note that the osteotomy also reduces brain retraction. Removal of the middle and posterior ethmoidal cells is necessary in order to reach the foramen magnum inferiorly. The dorsum sellae remains a blind spot.
FIG. 2. Artist's drawings depicting an orbitofrontoethmoidal craniotomy and osteolomy for a tumor of the middle or posterior skull base. A: The order of removal of the cranial bones (1, 2, and 3). B: Superior view of the orbitofrontoetbmoidal osteotomy. C: The exposure obtained after the osteotomy and early dissection. Note the removal of the middle and posterior ethmoidal cells. CNII = second cranial nerve.
medially by a thin periosteal layer, but this may be torn during the dissection or may need to be intentionally opened if there is tumor invasion. In such cases, venous bleeding is controlled by packing with rolls of Surgicel. The anterior vertical and posterior vertical segments of the intracavernous ICA can be exposed for about threeJ. Neurosurg. / Volume 76 /February, 1992
quarters of their circumference. The cavernous ICA is followed along the posterior vertical segment to the point where it enters the cavernous sinuses, permitting resection of some of the petrous apex. In this lateral corner, caution must be exercised not to disturb the sixth cranial nerve as it travels extradurally from the dura of the clivus to enter the cavernous sinus through Dorello's canal. The anterior wall of the body of the sphenoid bone can also be resected from this approach, but the surgeon should be careful not to penetrate the wall of the nasopharynx anterior to the bone. The clival tumor and bone are progressivciy removed from a superior to an inferior direction. The clival dura is thick in young and middle-aged individuals, but may be quite thin in older patients or as a result of tumor invasion. In cases where the clival dura is thin, care must be taken not to injure the basilar artery, its branches, or the brain stem. Considerable venous bleeding may occur from the basilar venous plexus, but can be controlled with Surgicel packs. In tumors such as chordomas, the bone resection should extend at least 1 cm beyond radiologically and surgically visible tumor margins, if possible. The lower limit of resection by this approach is the foramen magnum. At the foramen magnum, the resection can be extended laterally up to the hypoglossal canals. Reconstruction Dural defects in the anterior skull base are closed by primary suture or with a graft of fascia lata or parietal 203
L. N. Sekhar, et al. defects following surgery that may have included orbital exenteration and/or maxillectomy, the additional transfer of a temporalis muscle rotational flap or a vascularized free flap is necessary. The purpose of this transfer is to obliterate dead space with vascularized tissues, to prevent CSF leak, to protect an exposed ICA from subsequent infection and rupture, and to facilitate improved cosmesis.~3'23 The orbitofrontal bone segment is replaced after removal of small segments of bone inferiorly to prevent compression of the pericranial flap. It is secured with 2-0 Neurilon sutures or titanium miniplates. Reapproximation of the orbitofrontal osteotomy piece has not resulted in any cosmetic deformities in our series. We found that routine reconstruction of the bone of the ethmoidal and sphenoclival area, as described by Derome, et al., 5 was not necessary unless extensive resection of the medial orbital wall was required during tumor resection. The remainder of the closure follows standard techniques. A subgaleal drain to gravity is left in place for 24 to 48 hours. In cases where the dural closure is tenuous, lumbar spinal drainage is continued for 48 hours postoperatively, draining no more than 50 cc CSF every 8 hours. A CT scan is performed 24 hours after the procedure to detect any asymptomatic complications.
FIG. 4. Artist's drawingsdemonstrating the application of the pericranial flap for reconstruction. CNII = second cranial nerve. Upper:Side view. Note that a fat graft is also placed in the sphenoid and ethmoid sinuses. Lower. View from above.
pericranium. For dural defects of the middle or posterior skull base, a fascia lata graft is used to cover the entire area and is attached with sutures or titanium hemoclips; watertight closure is not possible. The mucosa of the frontal sinus and sphenoid sinus is exenterated. The frontonasal duct and the exposed ethmoidal air cells are packed with small pieces of fat. A long pericranial flap supplied by the supraorbital and supratrochlear vessels is then developed and placed into the tumor resection cavity, reaching the margins of the bone resection. This flap lies between the orbitofrontal bone segment and the ethmoidal sinuses, providing a longer reach, vascularity for the bone segment, and an effective barrier against infection (Fig. 4). Autologous fat is then packed between the fascia lata graft and the pericranial flap or into a pocket of the pericranial flap to occlude the dead space. Overpacking should be avoided since compression of the optic nerve or the brain stem may result. If the patient has previously undergone a bicoronal incision close to the hair line, the length of the pericranial flap is restricted. In such patients, a galeofrontalis flap can be utilized. 2~ In patients with much larger 202
Combination With Other Approaches Patients with highly malignant lesions of the craniofacial area need circumferential exposure of the tumor to permit en bloc resection. While the extended frontal approach provides adequate exposure of the superior aspect of the tumor, the inferior aspect is not exposed. This exposure is usually achieved during the same operation by the otolaryngologist via a transfacial route. A lateral rhinotomy/transethmoidal approach, a midfacial degloving operation, a maxillotomy technique, or a maxillectomy approach is usually selected, depending upon the size and location of the tumor. 4'12If the orbit is involved by a highly malignant tumor, orbital exenteration may also be necessary. For lesions that extend laterally into the petrous bone, the greater wing of the sphenoid, or the infratemporal fossa, the extended frontal approach is combined with an extradural subtemporal-transzygomatic or subtemporal-infratemporal approach. 2~ Resection of the upper part of the dorsum sellae may require an intradural-subtemporal approach. Illustrative Cases Case 1: Anterior and Middle Basal Meningioma
This 70-year-old man had previously undergone three operations and radiation therapy in an attempt to control the growth of a meningioma of the anterior and middle skull base (Fig. 5 upper). He presented with progressive loss of vision and recurrent tumor extending extradurally into the sphenoethmoidal area. The tumor was totally removed via an extended frontal approach (Fig. 5 lower). His vision was unchanged after J. Neurosurg. / Volume 76 / February, 1992
Extended frontal approach to skull base tumors
FIG. 5. Magnetic resonance Trweighted images in Case 1.
Upper: Preoperative sagittal (left) and coronal (right) images showing a tumor involving the anterior and middle cranial base, There is also an obstruction of the sphenoid sinus with the formation of a mucocele. Lower: Postoperative sagittal (left) and coronal (right) images demonstrating the absence of tumor. Despite some autologous cranial bone reconstruction of the frontal area, there is a slight depression due to extensive bone loss from multiple operations and radiation therapy.
the operation; however, it progressively worsened over a period of 6 months despite the absence of tumor, presumably due to a delayed effect of radiation. He remains independent, active, and free of tumor 4 years later.
Case 2: Middle and Posterior Basal Chordoma This 73-year-old woman had previously undergone partial resection of a sphenoclival chordoma by a transseptal transsphenoidal approach and had received 6000 rad of external beam radiotherapy. However, the tumor continued to grow causing visual deterioration (Fig. 6 upper). An extended frontal approach was utilized for total excision of the tumor, which extended inferiorly to the foramen magnum and laterally to the petrous apices. The clival dura had to be resected (Fig. 6 lower). The patient remains well and disease-free 36 months postoperatively.
Case 3: Extensive Clival Chordoma This 54-year-old woman was referred to us with a clival chordoma involving the entire clivus, both occipital condyles, the fight jugular foramen, the petrous apex region, and the right cavernous sinus area (Fig. 7). Diagnosis had been established by transsphenoethmoidal surgery. The initial tumor resection was performed via an extended frontal approach combined with a subtemporal-infratemporal approach. A fistula extend-
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l:ic. 6. Magnetic resonance TL-weighted images in Case 2.
Upper: Preoperative sagittal (left) and coronal (right) images showing a tumor predominantly involving the upper and middle clivus and the sphenoid bone. Lower: Postoperative sagittal (left) and coronal (right) images showing the absence &tumor and lhe presence of the fat used in the reconstruction along with the pericranial flap.
ing from the pharynx to the middle ear developed due to the inadequacy of the repair and possibly related to the prior transethmoidal operation (Fig. 8). The patient underwent a second operation via an extreme lateral approach to remove additional tumor; reconstruction with a temporali~ muscle flap was performed to close the fistula (Fig. 8). An occiput to C I - 2 fusion was performed at a later date to enable both tumor-involved condyles to be removed. A subsequent intradural transcavernous operation was necessary to resect tumor residue in the cavernous sinuses. The patient is free of tumor 12 months later, and has returned to work. This case is presented as an example of a petroclival tumor that is too large to be removed by a single approach, and to illustrate a potential complication and its management. Results
Follow-Up Resulls The patients in our series were followed for an average of 26 months, ranging from 6 to 56 months. The disease status of patients at follow-up review is shown in Table 1. Seven (64%) of the l 1 patients with benign lesions, 14 (64%) of the 22 patients with low-grade malignancies, and seven (44%) of the 16 patients with high-grade malignancies were alive with no evidence of disease. With the exception of one patient who died and another with an intracerebral contusion and de203
L. N. Sekhar, et al.
FIG. 8. Postoperative studies in Case 3. a: Enhanced computerized tomography scan demonstrating an air-filled communication from the sphenoid and retropharyngeal area from where the tumor was removed to the tympanicondylar area. This failure of reconstruction reflects inadequate vascularity to the area postoperatively, b: Enhanced magnetic resonance image obtained after resection of the remaining tumor and reconstruction of the tumor cavity with a temporalis muscle flap.
FIG. 7. Preoperative magnetic resonance images in Case 3. T2-weighted axial (a) and enhanced sagitlal (b) images and T~-weighted axial (c) and enhanced axial (d) images showing a clival chordoma involving the entire clivus, both occipital condyles, the right jugular foramen, the petrous apex region, and the right cavernous sinus area. The patient's initial operation was an extended frontal approach combined with a subtemporal-infratemperal approach. Because of the extensive nature of the tumor, further operations using different approaches were necessary to achieve complete tumor removal.
layed epidural abscess, the patients had returned to their preoperative functional status within 2 months after surgery.
Complications Postoperative complications are shown in Tables 3 and 4. One patient, who underwent an uncomplicated repair of a spontaneous CSF fistula, was readmitted 3 weeks after discharge and died of superior mesenteric artery thrombosis. This was believed to be unrelated to the operation. Postoperative CSF leaks occurred in two patients with intra- and extradural tumors. In both of these cases, large dural defects were inadequately repaired during the operation and the patients developed postoperative hydrocephalus. Repair was accomplished with a fascia lata and autologous fat graft and insertion of CSF shunts. Three patients developed frontal lobe contusion or edema. In one elderly patient with a large tumor, the dura was badly torn and some bridging veins of the frontal lobe were injured during the craniotomy. A second patient had tumor invasion of the frontal lobe and the third had severe scarring from a previous operation. All three patients were managed with steroid 204
and diuretic agents. A temporal lobe hematoma requiring reoperation occurred in one patient with an extensive adenoid cystic carcinoma that had necessitated the addition of a subtemporal-infratemporal approach in order to remove tumor. Postoperative infection occurred in three patients, all of whom had undergone a transfacial approach in addition to the extended frontal approach. One epidural abscess developed 1 year postoperatively in an elderly woman with a large esthesioneuroblastoma. The reconstruction in this patient had been suboptimal because of her age, the size of tumor, and the thin pericranial flap. She required removal of the frontal bone flap and administration of intravenous antibiotics. A second patient was suspected of having an epidural infection, but cultures of the epidural fluid were sterile. He was treated with antibiotics and did not undergo bone removal. The third patient was Case 3 (reported above), who developed a pharyngotympanic fistula. When epidural infection occurs, we remove the bone flap, but leave the orbitofrontal osteotomy segment. Since this bone is thin and in close contact with vascularized tissue, it appears to vascularize quickly and does not act as a sequestrum. Two patients suffered severe temporary neurological deterioration due to inadvertent excessive lumbar CSF drainage. One elderly patient became severely obtunded, but recovered after the drain was shut off. A middle-aged patient developed uncal herniation, requiting a partial temporal lobectomy and section of the tentorium; recovery was complete. Consequently, we have been very cautious in the use of the lumbar CSF drainage and regulate the drainage by strict volumetric limits. Cranial nerve deterioration or palsy was seen in eight patients, and was temporary in four and permanent in
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Extended frontal approach to skull base tumors TABLE 3 Complications Jblhm ing ~v~tendedfrontal surger)' [br tumor~ ~?/ the skull base No. of No. of Cases LaterOps
Complication
superior mesenteric arteD'thrombosis* 1 0 cerebrospinal fluid leak 2 2 frontal lobe contusion or edema'~ 3 0 temporal lobe hematoma 1 1 epidural abscessor infection 2 2 pharyngotympanicfistula 1 1 neurologicaldeterioratJon:~ 2 1 postoperative seizure 3 0 temporary,weightloss 4 0 * Complication resulted in death of patient. t Complicationresulted in permanent disability for one patient. { Complication was due to excessive lumbar cerebrospinal fluid drainage.
TABLE 4 Cranial nerve deterioralion or palsy fidlowing frontal surgery for tumors of the skull base No. of Cases
Cranial Nerve
Temporary 0 0 0 0 2 1 1
2nd 3rd-6th ath 5th 6th 7th 9th, 10th, & 12th
Permanent 1 1 1 1 0 0 0
four (Table 4). Deterioration of the second cranial nerve function occurred postoperatively in one patient with an osseous meningioma that was severely compressing the optic nerve. Deterioration of the second through sixth cranial nerves in one patient with a pituitary adenoma was related to intracavernous tumor removal. One patient suffered trochlear muscle dysfunction, presumably due to the orbitofrontal osteotomy, but compensated without difficulty. The outcome of patients who sustained complications was generally favorable. Except for one patient who died due to superior mesenteric artery thrombosis and another patient who developed a delayed epidural infection and subsequently remained dependent for daily living activities, the patients returned to their previous functional status within 4 to 8 weeks after surgery. Discussion
Historical Perspective
The concept of removal of the orbital rims to improve exposure of the skull base was introduced by Frazier in 1913. 7 Derome, et al., 5 described the transbasal approach to the skull base in 1972. The use of J. Neurosurg. / Volume 76/February, 1992
orbital osteotomies to approach a number of lesions was further developed by Jane, et al., ~ Jackson, et al., ~,") and many recent authors. L2"Sa6'2~ We have expanded these approaches for the treatment of midline cranial base lesions by the addition of ethmoidectomy. A combined transcranial transfacial approach to retinoblastoma was first described by Ray and McLean ~ in 1943. This combined approach was applied to paranasal sinus malignancies in 1954 by Smith, et al., 2: in 1966 by Ketcham, et al., ~4 and in 1968 by Van Buren, et al. 26 The incidence of postoperative infection, CSF leakage, and death was high; however, these series demonstrated the utility of the surgical techniques in producing long-term survivors for tumors previously considered inoperable. Value o f E x t e n d e d Frontal Approach
For anterior skull base lesions, the orbitofrontal osteotomy is not a prerequisite, as shown in recent series. 3,~7,19"22"24However, by removal of basicranial bone close to the surgeon's line of vision and retraction of the orbital tissues, exposure of the tumor is improved and frontal lobe retraction is reduced. When the tumor does not extend inferiorly below the ethmoid sinuses the extended frontal approach is used alone, and the lesion is removed piecemeal. For en bloc resection of highly malignant lesions, this approach needs to be combined with a transfacial approach to obtain circumferential exposure. For middle or posterior skull base lesions, this approach can be used alone when the lesion is in the midline and involves the upper and middle clivus. A clivus lesion located as low as the foramen magnum can be resected if it is an inferior extension of a middle clival tumor. When a midline lesion is predominantly located in the middle or lower clival region, a maxillotomy or a transoral approach will provide adequate exposure. These approaches can also be combined with an extended frontal approach during the same operation. For sphenoclival lesions, the advantage of this approach lies in the excellent exposure of the optic nerve, the sphenoid sinus, and the medial aspect of the cavernous sinuses. Even if the cavernous ICA is injured, the approach is wide and shallow enough to allow direct repair (LN Sekhar, unpublished data). Additionally, the reconstruction described in this paper allows the excision of clival dura with no major risk of CSF leakage. The risk of postoperative infection is also greatly reduced by the vascularized flaps and the elimination of dead space. L i m i t a t i o n s o f E x t e n d e d Frontal Approach
Bilateral olfactory denervation is a necessary sequel to this approach. Although well tolerated by most patients, the sense of smell and flavor of taste may be essential for a patient's occupation. The lateral extension of this approach is limited by the optic nerves, 205
L. N. Sekhar, etal. cavernous sinuses, petrous apices, abducens nerves, and hypoglossal canals, Tumors that extend further laterally require the combination of a Iateral approach such as the subtemporal-infratemporal technique. As noted by Derome, etal. 5 the dorsum sellae is a blind spot behind the sella turcica and cannot be resected by this approach if it is very prominent. The field increases in depth and narrows as the foramen magnum is approached.
Alternative Approaches Alternative approaches available to the surgeon for the resection of sphenoclival lesions include the transethmoidal, the transseptal-transsphenoidal, the unilateral maxillotomy, 2 the facial translocation,~2 the Le Fort I maxillotomy, 25 and the transoral approaches. While some of these approaches provide wide exposure of sphenoclival lesions, exposure of the optic nerves and the cavernous sinus areas is limited or absent. Except for the maxillotomy and facial translocation approaches, vascularized flap reconstruction is not possible. However, the surgeon should be familiar with all of these approaches and should select the best one based on the patient's need and the surgeon's experience. Conclusions Regardless of the approach utilized and the nuances of surgical resection, the most important issues to be considered are postoperative complications and the long-term outcome. Even though the majority of the tumors reported here were large and extensive, the complication rates were acceptable. The follow-up resuits with respect to tumor control are promising, but require further long-term documentation. Acknowledgments The authors thank Tern Pacella for typing the manuscript and assisting in data gathering, Lois Burkhart for assisting with the data collection, and Joan Nilson for providing editorial assistance. References 1. Ala~,~vanM, Sindou M: Fronto-temporal approach with orbito-zygomatic removal. Surgical anatomy. Acta Neuroehir 104:79-83, 1990 2. AI-Mefty O: The supraorbital-pterionai approach to skull base lesions. Neurosurgery 21:474-477, 1987 3. Blacklock JB, Weber RS, Lee YY, etal: Transcranial resection of tumors of the paranasal sinuses and nasal cavity. J Neurosurg 71:10-15, 1989 4. Cocke EW Jr, Robertson JH, Robertson JT, et at: The extended maxillotomy and subtotal maxillectomy for excision of skull base tumors. Arch Otolaryngol Head Neck Surg 116:92-104, 1990 5. Derome P, Akerman M, Anquez L, et al: Les tumeurs spheno-ethmoidales. Possibilit~s d'ex~rNse et de r~paration chirurgicales. Neurochirurgie (Suppl) 18:1-164, 1972 6. Erba SM, Horton JA, Latchaw RE, et al: Balloon test occlusion of the internal carotid artery with stable xenon/ CT cerebral blood flow imaging. AJNR 9:533-538, 1988 7. Frazier CH: An approach to the hypophysis through the anterior cranial fossa. Ann Surg 57:145-150, 1913 906
8. Hakuba A, Liu SS, Nishimura S: The orbitozygomatic infratemporal approach: a new surgical technique. Surg Neurol 26:271-276, 1986 9. Jackson IT: Craniofacial osteotomies to facilitate resection of tumors of the skull base, in Wilkins RH, Rengachary S (eds): Neurosurgery Update I. New York: McGraw-Hill, 1990, pp 277-291 10. Jackson IT, Marsh WR, Hide TA: Treatment of tumors involving the anterior cranial fossa. Head Neck Surg 6: 901-913, 1984 11. Jane JA, Park TS, Pobereskin LH, el al: The supraorbital approach: technical note. Neurosurgery 11:537-542, 1982 12. Janecka IP, Sen CN, Sekhar LN, et al: Facial translocation: a new approach to the cranial base. Otolaryngol Head Neck Surg 103:413-419, 1990 13. Jones NF, Schramm VL, Sekhar LN: Reconstruction of the cranial base following tumour resection. Br J Plast Surg 40:155-162, 1987 14. Ketcham AS, Hoye RC, Van Buren JM, etal: Complications of intracranial facial resection for tumors of the paranasal sinuses. Am J Surg 112:591-596, 1966 15. Lang J: Anterior cranial base anatomy, in Sekhar LN, Schramm VL Jr (eds): Tumors of the Cranial Base. Diagnosis and Treatment. Mt Kisco, NY: Futura, 1987, pp 247-264 16. Lesoin F, Pellerin P, Villette L, etal: IntNr& de la mobilisation du volet orbito-zygomatico-malaire. Neurochirurgie 32:90-93, 1986 17. Persing JA, Jane JA, Levine PA, et at: The versatile frontal sinus approach to the floor of the anterior cranial fossa. Technical note. J Neurosurg 72:513-516, 1990 18. Ray BS, McLean JM: Combined intracranial and orbital operation for retinoblastoma. Arch Ophthalmol 30: 437-445, 1943 19. Schramm VL Jr, Myers EN, Maroon JC: Anterior skull base surgery for benign and malignant disease. Laryngoscope 89:1077-1091, 1979 20. Sekhar LN, Janecka IP, Jones NF: Subtemporal-infratemporal and basal subfrontal approach to extensive cranial base tumours. Acta Neurochir 92:83-92, 1988 21. Sekhar LN, Sen CN, Jho HD, et al: Surgical treatment of intracavernous neoplasms: a four-year experience. Neurosurgery 24:18-30, 1989 22. Smith RR, Kiopp CT, Williams JM: Surgical treatment of cancer of the frontal sinus and adjacent areas. Cancer 7:991-994, 1954 23. Snyderman CH, Janecka IP, Sekhar LN, el al: Anterior cranial base reconstruction: role of galeal and pericranial flaps. Laryngoscope 100:607-614, 1990 24. Sundaresan N, Shah JP: Craniofacial resection for anterior skull base tumors. Head Neck Surg 10:219-224, 1988 25. Uttley D, Moore A, Archer DJ: Surgical management of midline skull-base tumors: a new approach. J Neurosurg 71:705-710, 1989 26. Van Buren JM, Ommaya AK, Ketcham AS: Ten years' experience with radical combined craniofacial resection of malignant tumors of the paranasal sinuses. J Neurosurg 28:341-350, 1968
Manuscript received March 13, 1991. Accepted in final form July 25, 1991. Address for Dr. Nanda: Louisiana State University, Department of Neurosurgery, 1501 Kings Highway, Shreveport, Louisiana. Address reprint requests to: Laligam N. Sekhar, M.D., Department of Neurosurgery, Presbyterian University Hospital, 230 Lothrop Street, Pittsburgh, Pennsylvania 15213.
J. Neurosurg. / Volume 76/February, 1992
