Division of Neurological Surgery (TCO, OA-M), Department of Physiology (TCO), Department of Otolaryngology--Head and Neck Surgery (JPL), Division of Plastic and Reconstructive Surgery (RI), Loyola University Medical Center, Maywood, Illinois Neurosurgery 31; 1126-1131, 1992 ABSTRACT: THE INVOLVEMENT OF the cavernous sinus by malignant tumors has limited their surgical treatment. We report here a successful en bloc resection of an invasive ethmoid carcinoma involving the cavernous sinus in a 46-year-old man. To prepare for surgery on this patient, a cadaver study was performed to investigate the feasibility of en bloc cavernous sinus resection and reconstruction. The preoperative evaluation, operative approach, and postoperative management are presented. KEY WORDS: Cavernous sinus; En bloc resection; Ethmoid carcinoma; Malignant disease; Skull base Principles of surgical oncology dictate that en bloc resection is mandated for the cure of malignant disease. En bloc resection requires tumor-free margins, which often incorporate normal anatomical structures. Applying these principles to malignant lesions of the anterior skull base often necessitates sacrificing important neurovascular structures. This is especially true for tumors involving or abutting the cavernous sinus. The cavernous sinus previously has been a formidable barrier to en bloc surgical resection. The anterior skull base houses a complex array of anatomical structures composed of soft tissues, bone, nerves, blood vessels, and aerated sinuses, which form the interface between the sequestered intracranial intradural compartment and the external environment. Violating this interface with en bloc resection carries a great risk of creating a neurological defect. The defect created requires reconstruction that is watertight, immunologically competent, structurally supportive, and cosmetically acceptable. We present our experience with en bloc resection of an invasive ethmoid carcinoma in a 46year-old man. To prepare for the case, we simulated the surgical approach in six cadaver heads. This allowed the authors to anticipate possible complications, refine approaches, and develop strategies for both carotid artery transection and transposition. We present the preoperative assessment, surgical technique, and postoperative management, and advocate a multidisciplinary team approach.
Preoperative workup The workup of the primary central nervous system included magnetic resonance imaging (MRI) with and without gadolinium enhancement and CT with and without contrast enhancement. Both revealed an infiltrating mass invading the left orbit and involving the medial wall of the cavernous sinus (Fig. 1). A metastatic workup was performed. Chest and abdominal CT scans and a pan endoscopy revealed no abnormalities, and the bone scan revealed uptake only in the left paranasal sinuses. The nature and location of the lesion led us to consider sacrificing or manipulating the left carotid artery. Cerebral blood flow (CBF), cerebral vascular reactivity, and cerebral vascular reserve (as defined by collateral circulation) were evaluated. Preoperative findings The preoperative xenon CBF studies demonstrated mean f1 (gray matter) flow of 60.2/60.2 (right/left) ml/100 g/min. The carbon dioxide challenge demonstrated normal cerebrovascular reactivity. The four-vessel angiogram with cross-compression studies revealed a large anterior communicating artery with excellent right-to-left cross-filling. No cross-filling was noted on vertebral injections with compression. Transcranial Doppler examination revealed a rapid directional change in the A1 segment of the left anterior communicating artery with left carotid compression. Mean velocities in the left middle cerebral artery were unchanged with carotid compression on the left. No neurological deficits were noted during the occlusion test. The single photon emission CT examination revealed normal symmetrical cerebral perfusion. The preoperative ophthalmological examination demonstrated normal visual acuity and fields in the patient's right eye and only light perception in the left eye. OPERATIVE APPROACH A tracheostomy was performed, and initial proximal control of the patient's left carotid artery was obtained in the neck. The common, external, and internal carotid arteries were isolated with vascular loops. A bicoronal incision was then made from tragus to tragus behind the hairline. The pericranium and the temporalis fascia and muscle were elevated as a single, large, vascularized flap. A modified bifrontal, orbitocranial-pterional craniotomy with sectioning of the zygomatic arch was performed (1,3) (Fig. 2). The bone flap included the left supraorbital ridge, the lateral orbital wall, the
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AUTHOR(S): Origitano, T.C., M.D., Ph.D.; AlMefty, Ossama, M.D.; Leonetti, John P., M.D.; Izquierdo, Ricardo, M.D.
CASE HISTORY The patient, a 46-year-old man, noticed a decrease in the vision of his left eye in December of 1990. Computed tomography (CT) revealed a soft tissue mass extending from the left ethmoid sinus into the left orbit, compressing the optic nerve. Three months later, the patient underwent a transethmoid biopsy, which showed the tumor to be an adenocarcinoma. He was referred to our institution for evaluation and treatment.
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Neurosurgery 1992-98 December 1992, Volume 31, Number 6 1126 En Bloc Resection of an Ethmoid Carcinoma Involving the Orbit and Medial Wall of the Cavernous Sinus Case Report
Transfacial approach Bilateral rhinotomy incisions were made with a transverse incision over the glabella carried inferiorly to the left eye. A series of bone cuts were made at the junction between the nasal and frontal bones bilaterally, mobilizing the nasal dorsum. A soft tissue flap was carried posteriorly by extending the transverse skin incision into the superior aspect of the left brow. The skin of the left eyelid and cheek was reflected anteriorly, and the conjunctiva was oversewn. Care was taken not to enter the orbit, which encapsulated the tumor. The anterior, medial, and posterolateral walls of the maxillary sinus were removed, along with the inferior and middle turbinates. The infraorbital rim and the floor of the orbit were maintained so that they could be taken en bloc with the specimen. Exenteration of the mucosa in the right ethmoid sinus revealed the bone cut from above. This cut was extended by removing the right middle and superior turbinates to the sphenoid sinus. The anterior wall of the sphenoid sinus was removed, and the specimen was delivered en bloc through the facial defect with gentle pressure from above. The specimen included bilateral cribriform plates, the left orbit and its contents, the jugum and left upper quadrant of the sphenoid body, remnants of the left greater and lesser sphenoid without the pterygoid plates, and the medial wall of the left cavernous sinus (Fig. 5). The cranial defect measured 7 cm across, 7 cm front-to-back, and 6 cm in height. Reconstruction The en bloc resection left a large area of dead space (approximately 300 ml, equivalent to a standard 12ounce can) and a potential for leakage of cerebrospinal fluid. Because of this, the patient needed an effective, watertight, cosmetic, immunological barrier adjacent to the oral-nasal sinus. The pericranium was slipped under the brain and tacked to the bone with nylon sutures through wirepasser drill holes in the surrounding bone in such a fashion that a 1.5 cm lip of pericranium could be tucked under the dura. This created a pericranialdural-fascia sandwich (14). Fibrin glue was then placed along the pericranial-dural interface to seal the junction. The bone flap and zygoma were reapproximated with microplates and single-strand 20 stainless steel wire. Before the bone flap was placed, a Jackson-Pratt drain (Heyer-Schulte, Anasco, Puerto Rico) was put into the epidural space and brought out of one of the burr holes. The drain was connected to an air release trap similar to that reported by Arbit and colleagues (5). This drain is constructed with a 100-ml bulb, a 15-ml vacutainer, a spinal needle, and a micropore filter. This system allows trapped air to escape as the brain expands and can be converted to a low-pressure epidural suction drain if fluid collects. We call this system the neurovac.
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sleeve and secured with a small amount of fibrin glue. An antibiotic-soaked pad was then placed over the dura, and the skin flap was turned down.
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pterion, the zygomatic process of the frontal bone, the zygoma, and the bifrontal bone flap. At this point, the procedure continued under microscopic magnification and illumination. The rest of the lateral and superior orbital roof was removed with microkerrisons and a high-speed drill. The left anterior clinoid was removed, and the optic canal was opened. Bone was then removed around the supraorbital foramen and foramen rotundum. The lateral aspect of the greater wing of the sphenoid and sphenoid ridge were removed with a rongeur. With a high speed diamond drill, the petrous carotid artery was exposed from the genu of the vertical segment to the trigeminal ganglion. Attention was then turned to the anterior cranial floor. The dura over the right orbital roof was elevated, while the dura over the cribriform plate and left orbit was left adhering to the bone. A transverse dural opening was made across the anterior frontal lobes, extending from the left lateral orbit to 1 cm beyond the contralateral cribriform plate. The spinal drain was opened, allowing the frontal lobes to gently retract under the influence of gravity. Intradural inspection of the floor of the anterior fossa revealed that the tumor extended through the cribriform plate (Fig. 3). The olfactory tracts were transected proximally. The dural cut was then extended perpendicularly, parallel to the cribriform plate, with a 1-cm margin back to the medial aspect of the optic foramen on the right. The dura over the left sylvian fissure was opened; the fissure itself was split using microsurgical dissection. The optic nerve, supraclinoid carotid artery, and the bifurcation of the carotid were exposed. The left optic nerve was then sharply transected. The dural ring around the carotid artery was opened. This allowed access to the ophthalmic artery, which was suture ligated, cauterized, and transected. The cavernous carotid artery was exposed throughout its cavernous portion to its junction with the mobilized petrous portion at the trigeminal ganglion. No tumor was seen within the cavernous sinus. The medial margin of the en bloc resection was then determined to be the medial wall of the cavernous sinus. The carotid artery was preserved and transposed laterally (Fig. 4). A series of internal skull base cuts were then made. The dura over the left superior orbital fissure was opened, and the third, fourth, fifth, and sixth nerves were transected. Bleeding was controlled with hemostatic packing. The foramen rotundum was then entered, and the second division of the trigeminal nerve transected. The bone cut was brought through the body of the sphenoid across the foramen rotundum and out to meet the cut in the greater wing of the sphenoid. Care was taken to gently retract the left carotid artery while cuts were made. The foramen ovale and its contents were preserved, ensuring motor and sensory function of the mandible. Before beginning the anterior facial approach, the intradural compartment was isolated. A large graft of fascia lata (10 × 15 cm) was harvested and sutured to the dura with 4-0 braided nylon. Where suturing was not possible, the fascia was interposed inside a dural
POSTOPERATIVE COURSE The patient's initial postoperative course was uneventful. On the fifth day after surgery, the patient's mental status changed significantly, and a CT scan revealed mild edema in the left hemisphere. A four-vessel angiogram revealed severe focal spasm of the internal carotid artery from the ophthalmic artery to the carotid bifurcation (Fig. 7). Repeated xenon-CBF studies revealed f1 values of 50.8 on the right and 45.5 on the left, representing a 25% decrease in blood flow in the left hemisphere. Hypertensive hypervolemic hemodilution (triple-H therapy) was begun (15). Systolic blood pressure was augmented to 165 to 170 mm Hg and central venous pressure to 10 to 12 mm Hg. Within 24 hours, the patient's clinical status improved to baseline values. Repeated xenon-CBF studies showed f1 values of 84.2 on the right and 84.1 on the left. Serial cerebral blood flow studies were used to guide the intensity and duration of therapy (Fig. 7). By the 10th postoperative day, repeated Xenon-CBF values were 76.1 on the right and 75.5 on the left. The patient's clinical examination remained stable, and the patient was weaned from Triple-H therapy from Day 14 through Day 18 after surgery. An angiogram done on postoperative Day 18 showed that the vasospasm was resolving.
DISCUSSION En bloc resection of malignant lesions of the anterior cranial base is possible only through combined transcranial and facial approaches. Several authors have demonstrated the usefulness of this approach for removing a variety of anterior cranial base lesions with improved outcome (4,8,12,13,17,19,20,21). Involvement of the cavernous sinus and carotid artery has defined the limits of craniofacial resection. Piecemeal removal of malignant disease from the cavernous sinus violates the oncological principles of tumor-free margins and en bloc resection. If sacrifice of the carotid artery is at issue, precise evaluation of the cerebrovascular reserve is mandated before proceeding with en bloc resection. The presence of anatomical collateral circulation should be established with four-vessel angiography incorporating side-to-side and front-to-back crosscompression studies. Once the anatomical collateral has been confirmed, physiological and functional tests of its adequacy can proceed using CBF studies, transcranial Doppler, and balloon occlusion tests. Preoperative sacrifice of the carotid artery is not advised. Intraoperative evaluation of carotid involvement is advocated, and the surgeon should be prepared to reconstruct the vessel (2,18,22). Intraoperative evaluation demonstrated no tumor within the cavernous sinus, and carotid transposition rather than ligation was performed. In our case, the patient developed spasm at the carotid bifurcation. None of the preoperative vascular tests predicted this complication. The use of physiological modulation of cerebral blood flow with Triple-H therapy elevated and maintained CBF through the critical period of vasospasm. The ability to monitor CBF using an inexpensive, reproducible, repeatable method aided significantly in the postoperative recovery of this patient. The Xenon-133 CBF studies correlated with and anticipated clinical changes and guided the intensity and duration of treatment. Reconstruction of the massive defect resulting from this surgery is mandated for a successful outcome (6,7,9,16). The free flap taken from vascularized rectus muscle fat has several novel advantages. The vascularized fat conforms readily to the deep recesses of the defect and can act as a seal against CSF leaks (10,11). The flaps can be tailored to fill large, variously shaped defects. Reversing the flap allows free access to the vascular pedicle and use of the muscle for contouring the superficial portion of the defect. When the graft interfaces directly with the aerodigestive tract, the skin pedicle can produce a secure junction with the epithelial mucosa. This facilitates early oral feedings and prosthetic application. Vascularized reconstruction reestablishes
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PATHOLOGICAL FINDINGS Pathological examination of the en bloc specimen revealed a poorly differentiated adenocarcinoma involving the sphenoid and ethmoid sinuses, with extension through the orbital bone and involvement of the soft tissues of the orbit. The medial, lateral, and inferior margins were free of tumor, as were the cut ends of the olfactory tracts and the optic nerve. At the superior margin, tumor cells were found along the cribriform plate.
The tracheostomy was removed, and the patient was discharged on the 23rd day after surgery. At the time of this report (8 months after surgery), he has completed radiation therapy and returned to work. The patient's cosmetic result is acceptable (Fig. 8). His cosmetic reconstruction will be completed with prosthetic eye replacement and canthoplexy. Downloaded from https://academic.oup.com/neurosurgery/article-abstract/31/6/1126/2752152 by Midwestern University user on 12 January 2019
Vascularized free flap The reconstruction was completed with a reversed, vascularized rectus muscle free flap, which included the overlying vascularized abdominal fat. The facial artery and vein were isolated in the left side of the patient's neck. The muscle flap was sculptured to fit the defect, and the epithelium was removed. The flap was positioned with the vascularized fat against the pericranial flap and skull base. Placing the flap in this reverse fashion positions the vascular pedicle superficially and allows for Doppler monitoring. The pedicle is then tunnelled under the skin to the prepared facial artery and vein. A microvascular anastomosis was performed in end-to-end fashion with interrupted 9-0 single-strand nylon sutures. Total ischemic time for the flap was 2.5 hours, and the muscle flap perfused well once circulation was reestablished. Arterial and venous pulses to the muscle flap were audible by transcutaneous Doppler at closure. The final reconstruction consisted of a fascia lata duraplasty, a pericranial adjacent tissue transfer, and a vascularized free flap constructed from the rectus muscle and abdominal fat (Fig. 6). Total operative time was 22 hours.
ACKNOWLEDGMENTS The authors thank Dr. Douglas Anderson for his contribution to the neurovac, Julie Hipp for editorial assistance, Jill Gordey Wallock for graphics, and Sue Cottrill for illustrations. Received, January 28, 1992. Accepted, July 7, 1992. Reprint requests: T.C. Origitano, M.D., Ph.D., Division of Neurological Surgery, Loyola University Medical Center, 2160 South First Avenue, Maywood, IL 60153.
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Al-Mefty O, Anand VK: Zygomatic approach to skull-base lesions. J Neurosurg 73:668-673, 1990. Al-Mefty O, Khalil N, Elwany MN, Smith RR: Shunt for bypass graft of the cavernous carotid artery. An anatomical and technical study. Neurosurgery 27:721-728, 1990. Al-Mefty O, Smith RR: Tailoring the cranioorbital approach. Keio J Med 39:217-224, 1990. Anand VK, Al-Mefty O: Craniofacial lesions and resection, in Al-Mefty O (ed): Surgery of the Cranial Base. Boston, Kluwer, 1989, pp 167-191. Arbit E, Shah J, Bedford R, Carlon G: Tension pneumocephalus: Treatment with controlled decompression via a closed water-seal drainage system. Case report. J Neurosurg 74:139-142, 1991. Arena S, Fritsch M, Hill EY: Free tissue transfer in head and neck reconstruction. Am J Otolaryngol 10:110-123, 1989. Bridger GP, Baldwin M: Anterior craniofacial resection for ethmoid and nasal cancer with free flap reconstruction. Arch Otolaryngol
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Head Neck Surg 115:308-312, 1989. Cocke EW Jr, Robertson JH, Robertson JT, Crook JP Jr: The extended maxillotomy and subtotal maxillectomy for excision of skull base tumors. Arch Otolaryngol Head Neck Surg 116:92-104, 1990. Fisher J, Jackson IT: Microvascular surgery as an adjunct to craniomaxillofacial reconstruction. Br J Plastic Surg 42:146-154, 1989. House JL, Hitselberger WE, House WF: Wound closure and cerebrospinal fluid leak after translabyrinthine surgery. Am J Otol 4:126-128, 1982. Jones NF, Sekhar LN, Schramm VL: Free rectus abdominis muscle flap reconstruction of the middle and posterior cranial base. Plast Reconstr Surg 78:471-479, 1986. Ketcham AS, Wilkins RH, Van Buren JM, Smith RR: A combined intracranial facial approach to the paranasal sinuses. Am J Surg 106:698-703, 1963. Levine PA, Scher RL, Jane JA, Persing JA, Newman SA, Miller J, Cantrell RW: The craniofacial resection--eleven year experience at the University of Virginia: Problems and solutions. Otolaryngol Head Neck Surg 101:665-669, 1989. Origitano TC, Miller CJ, Izquierdo R, Hubbard T, Morris R: Complex cranial base trauma resulting from recreational fireworks injury. Neurosurgery 30:570-576, 1992. Origitano TC, Wascher TM, Reichman OH, Anderson DE: Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemic hemodilution ("Triple-H" therapy) after subarachnoid hemorrhage. Neurosurgery 27:729- 740, 1990. Schuller DE, Goodman JH, Miller CA: Reconstruction of the skull base. Laryngoscope 94:1359-1364, 1984. Schramm VL Jr, Myers EN, Maroon JC: Anterior skull base surgery for benign and malignant disease. Laryngoscope 89:10771091, 1979. Sekhar LN, Sen CN, Jho HD: Saphenous vein graft bypass of the cavernous internal carotid artery. J Neurosurg 72:35-41, 1990. Sisson GA Sr, Toriumi DM, Atiyah RA: Paranasal sinus malignancy: A comprehensive update. Laryngoscope 99:143-150, 1989. Smith RR, Klopp CT, Williams JM: Surgical treatment of cancer of the frontal sinus and adjacent areas. Cancer 7:991-994, 1954. Snyderman CH, Sekhar LN, Sen CN, Janecka IP: Malignant skull base tumors. Neurosurg Clin North Am 1:243-259, 1990. Spetzler RF, Fukushima T, Martin N, Zabramski JM: Petrous carotid-to-intradural carotid saphenous vein graft for intracavernous giant aneurysm, tumor, and occlusive cerebrovascular disease. J Neurosurg 73:496-501, 1990.
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CONCLUSIONS En bloc resection of malignant lesions of the anterior skull base is possible and is the next logical step in advancing surgical treatment of these lesions. Preoperative evaluation of cerebrovascular collateral circulation is mandated for this resection, and managing the vasculature and its complications is paramount to a successful outcome. Vascular reconstruction should be anticipated. The surgical technique should include saving the superficial temporal artery and preparing the saphenous vein as a graft. A multidisciplinary team is required. Adapting current surgical techniques and creating new approaches are necessary for successful resection and reconstruction. Scientific investigations of patient selection, operative morbidity, and impact on the natural history of the disease processes are needed to test the efficacy of these procedures.
8.
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a competent immunological interface between the intracranial and extracranial compartment. With maturity, the vascularized graft will weather the rigors of adjuvant radiation.
REFERENCES: (1)
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Laligam N. Sekhar Pittsburgh, Pennsylvania
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COMMENTS Dr. Origitano and colleagues have described a very elegant operation for an en bloc resection of a tumor that bordered the cavernous sinus. In this particular case, carotid artery resection was not necessary. We have performed 11 en bloc resections of lesions that involve the cavernous sinus. Many of these cases involved sacrifice of the carotid artery. However, in some cases, the carotid artery could be preserved because there was no actual invasion of the cavernous sinus as in the case demonstrated by the authors (1). We find that the preoperative balloon occlusion test with clinical evaluation and xenon blood flow studies is still the best way of assessing the collateral circulation when planning carotid sacrifice for malignant tumors. However, if there are sacrifices performed, we have also found that they should be performed at the time of the operation by surgical occlusion rather than preoperatively by a balloon followed by surgical excision at a later time. The earlier procedure appeared to be associated with a higher incidence of embolic stroke, presumably because of the hypercoagulable state induced by the preoperative balloon occlusion of the carotid artery. If the carotid artery cannot be sacrificed, then revascularization can be performed. We presently prefer to revascularize using a long saphenous vein graft from the cervical internal or external carotid artery to the M2 or M3 segment of the middle cerebral artery about 2 weeks before the actual operation to resect the tumor. This is preferred to a direct venous saphenous vein graft bypass of the internal carotid artery in cases where there is a possibility of nasopharyngeal contamination and infection in the operative side. This greatly reduces the risk of infection of the graft and a carotid blowout. In the 11 patients with fast growing malignant tumors that had en bloc resection, 50% have survived over a median follow-up of 4 years. The remainder died of local recurrence, regional lymph node metastasis, or systemic metastasis. It is apparent that the adjuvant therapies for these tumors including radiation and chemotherapy have been quite ineffective and have not caught up with the surgical advances. Very careful preoperative patient selection and careful follow-up examination of these patients is necessary. The patient should also be informed preoperatively that such extensive surgical resection is really a treatment of last resort at the present time and is not guaranteed to cure the disease. Of course, many of the patients that we see presently are those for whom other treatment modalities, such as biopsy and radiation therapy and/or chemotherapy, were ineffective. Surgical resection for previously untreated malignancy in suitable cases should be studied prospectively.
Figure 3. Illustration depicting the initial intraoperative findings.
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Figure 2. The skull and orbit after the removal of bone.
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Figure 1. Axial MR image demonstrating the invasive lesion within the orbit, ethmoid sinus, and nasal cavity, and involving the medial wall of the cavernous sinus.
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Figure 5. En bloc specimen, frontal view.
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Figure 4. A, the transposed intracavernous carotid artery. B, MR image demonstrating the transposed carotid artery.
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Figure 6. A, illustration of reconstruction consisting of fascia lata duraplasty (cross-hatched area), vascularized pericranial graft (stippled area), and the vascularized rectus muscle-abdominal fat free flap. B, sagittal MR image after surgery, demonstrating the reconstruction.
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Figure 8. The patient shows acceptable cosmetic results 6 months after en bloc resection.
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Figure 7. A, left internal carotid angiogram demonstrating the transposed carotid and spasm distal to the transposition, including the takeoff of the A1 segment. B, xenon-133 cerebral blood flow studies were integral to treating the postoperative vasospasm. Triple-H therapy rapidly restored cerebral blood flow in the face of compromised collateral circulation.
Preoperative workup The workup of the primary central nervous system included magnetic resonance imaging (MRI) with and without gadolinium enhancement and CT with and without contrast enhancement. Both revealed an infiltrating mass invading the left orbit and involving the medial wall of the cavernous sinus (Fig. 1). A metastatic workup was performed. Chest and abdominal CT scans and a pan endoscopy revealed no abnormalities, and the bone scan revealed uptake only in the left paranasal sinuses. The nature and location of the lesion led us to consider sacrificing or manipulating the left carotid artery. Cerebral blood flow (CBF), cerebral vascular reactivity, and cerebral vascular reserve (as defined by collateral circulation) were evaluated. Preoperative findings The preoperative xenon CBF studies demonstrated mean f1 (gray matter) flow of 60.2/60.2 (right/left) ml/100 g/min. The carbon dioxide challenge demonstrated normal cerebrovascular reactivity. The four-vessel angiogram with cross-compression studies revealed a large anterior communicating artery with excellent right-to-left cross-filling. No cross-filling was noted on vertebral injections with compression. Transcranial Doppler examination revealed a rapid directional change in the A1 segment of the left anterior communicating artery with left carotid compression. Mean velocities in the left middle cerebral artery were unchanged with carotid compression on the left. No neurological deficits were noted during the occlusion test. The single photon emission CT examination revealed normal symmetrical cerebral perfusion. The preoperative ophthalmological examination demonstrated normal visual acuity and fields in the patient's right eye and only light perception in the left eye. OPERATIVE APPROACH A tracheostomy was performed, and initial proximal control of the patient's left carotid artery was obtained in the neck. The common, external, and internal carotid arteries were isolated with vascular loops. A bicoronal incision was then made from tragus to tragus behind the hairline. The pericranium and the temporalis fascia and muscle were elevated as a single, large, vascularized flap. A modified bifrontal, orbitocranial-pterional craniotomy with sectioning of the zygomatic arch was performed (1,3) (Fig. 2). The bone flap included the left supraorbital ridge, the lateral orbital wall, the
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AUTHOR(S): Origitano, T.C., M.D., Ph.D.; AlMefty, Ossama, M.D.; Leonetti, John P., M.D.; Izquierdo, Ricardo, M.D.
CASE HISTORY The patient, a 46-year-old man, noticed a decrease in the vision of his left eye in December of 1990. Computed tomography (CT) revealed a soft tissue mass extending from the left ethmoid sinus into the left orbit, compressing the optic nerve. Three months later, the patient underwent a transethmoid biopsy, which showed the tumor to be an adenocarcinoma. He was referred to our institution for evaluation and treatment.
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
Neurosurgery 1992-98 December 1992, Volume 31, Number 6 1126 En Bloc Resection of an Ethmoid Carcinoma Involving the Orbit and Medial Wall of the Cavernous Sinus Case Report
Transfacial approach Bilateral rhinotomy incisions were made with a transverse incision over the glabella carried inferiorly to the left eye. A series of bone cuts were made at the junction between the nasal and frontal bones bilaterally, mobilizing the nasal dorsum. A soft tissue flap was carried posteriorly by extending the transverse skin incision into the superior aspect of the left brow. The skin of the left eyelid and cheek was reflected anteriorly, and the conjunctiva was oversewn. Care was taken not to enter the orbit, which encapsulated the tumor. The anterior, medial, and posterolateral walls of the maxillary sinus were removed, along with the inferior and middle turbinates. The infraorbital rim and the floor of the orbit were maintained so that they could be taken en bloc with the specimen. Exenteration of the mucosa in the right ethmoid sinus revealed the bone cut from above. This cut was extended by removing the right middle and superior turbinates to the sphenoid sinus. The anterior wall of the sphenoid sinus was removed, and the specimen was delivered en bloc through the facial defect with gentle pressure from above. The specimen included bilateral cribriform plates, the left orbit and its contents, the jugum and left upper quadrant of the sphenoid body, remnants of the left greater and lesser sphenoid without the pterygoid plates, and the medial wall of the left cavernous sinus (Fig. 5). The cranial defect measured 7 cm across, 7 cm front-to-back, and 6 cm in height. Reconstruction The en bloc resection left a large area of dead space (approximately 300 ml, equivalent to a standard 12ounce can) and a potential for leakage of cerebrospinal fluid. Because of this, the patient needed an effective, watertight, cosmetic, immunological barrier adjacent to the oral-nasal sinus. The pericranium was slipped under the brain and tacked to the bone with nylon sutures through wirepasser drill holes in the surrounding bone in such a fashion that a 1.5 cm lip of pericranium could be tucked under the dura. This created a pericranialdural-fascia sandwich (14). Fibrin glue was then placed along the pericranial-dural interface to seal the junction. The bone flap and zygoma were reapproximated with microplates and single-strand 20 stainless steel wire. Before the bone flap was placed, a Jackson-Pratt drain (Heyer-Schulte, Anasco, Puerto Rico) was put into the epidural space and brought out of one of the burr holes. The drain was connected to an air release trap similar to that reported by Arbit and colleagues (5). This drain is constructed with a 100-ml bulb, a 15-ml vacutainer, a spinal needle, and a micropore filter. This system allows trapped air to escape as the brain expands and can be converted to a low-pressure epidural suction drain if fluid collects. We call this system the neurovac.
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
sleeve and secured with a small amount of fibrin glue. An antibiotic-soaked pad was then placed over the dura, and the skin flap was turned down.
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pterion, the zygomatic process of the frontal bone, the zygoma, and the bifrontal bone flap. At this point, the procedure continued under microscopic magnification and illumination. The rest of the lateral and superior orbital roof was removed with microkerrisons and a high-speed drill. The left anterior clinoid was removed, and the optic canal was opened. Bone was then removed around the supraorbital foramen and foramen rotundum. The lateral aspect of the greater wing of the sphenoid and sphenoid ridge were removed with a rongeur. With a high speed diamond drill, the petrous carotid artery was exposed from the genu of the vertical segment to the trigeminal ganglion. Attention was then turned to the anterior cranial floor. The dura over the right orbital roof was elevated, while the dura over the cribriform plate and left orbit was left adhering to the bone. A transverse dural opening was made across the anterior frontal lobes, extending from the left lateral orbit to 1 cm beyond the contralateral cribriform plate. The spinal drain was opened, allowing the frontal lobes to gently retract under the influence of gravity. Intradural inspection of the floor of the anterior fossa revealed that the tumor extended through the cribriform plate (Fig. 3). The olfactory tracts were transected proximally. The dural cut was then extended perpendicularly, parallel to the cribriform plate, with a 1-cm margin back to the medial aspect of the optic foramen on the right. The dura over the left sylvian fissure was opened; the fissure itself was split using microsurgical dissection. The optic nerve, supraclinoid carotid artery, and the bifurcation of the carotid were exposed. The left optic nerve was then sharply transected. The dural ring around the carotid artery was opened. This allowed access to the ophthalmic artery, which was suture ligated, cauterized, and transected. The cavernous carotid artery was exposed throughout its cavernous portion to its junction with the mobilized petrous portion at the trigeminal ganglion. No tumor was seen within the cavernous sinus. The medial margin of the en bloc resection was then determined to be the medial wall of the cavernous sinus. The carotid artery was preserved and transposed laterally (Fig. 4). A series of internal skull base cuts were then made. The dura over the left superior orbital fissure was opened, and the third, fourth, fifth, and sixth nerves were transected. Bleeding was controlled with hemostatic packing. The foramen rotundum was then entered, and the second division of the trigeminal nerve transected. The bone cut was brought through the body of the sphenoid across the foramen rotundum and out to meet the cut in the greater wing of the sphenoid. Care was taken to gently retract the left carotid artery while cuts were made. The foramen ovale and its contents were preserved, ensuring motor and sensory function of the mandible. Before beginning the anterior facial approach, the intradural compartment was isolated. A large graft of fascia lata (10 × 15 cm) was harvested and sutured to the dura with 4-0 braided nylon. Where suturing was not possible, the fascia was interposed inside a dural
POSTOPERATIVE COURSE The patient's initial postoperative course was uneventful. On the fifth day after surgery, the patient's mental status changed significantly, and a CT scan revealed mild edema in the left hemisphere. A four-vessel angiogram revealed severe focal spasm of the internal carotid artery from the ophthalmic artery to the carotid bifurcation (Fig. 7). Repeated xenon-CBF studies revealed f1 values of 50.8 on the right and 45.5 on the left, representing a 25% decrease in blood flow in the left hemisphere. Hypertensive hypervolemic hemodilution (triple-H therapy) was begun (15). Systolic blood pressure was augmented to 165 to 170 mm Hg and central venous pressure to 10 to 12 mm Hg. Within 24 hours, the patient's clinical status improved to baseline values. Repeated xenon-CBF studies showed f1 values of 84.2 on the right and 84.1 on the left. Serial cerebral blood flow studies were used to guide the intensity and duration of therapy (Fig. 7). By the 10th postoperative day, repeated Xenon-CBF values were 76.1 on the right and 75.5 on the left. The patient's clinical examination remained stable, and the patient was weaned from Triple-H therapy from Day 14 through Day 18 after surgery. An angiogram done on postoperative Day 18 showed that the vasospasm was resolving.
DISCUSSION En bloc resection of malignant lesions of the anterior cranial base is possible only through combined transcranial and facial approaches. Several authors have demonstrated the usefulness of this approach for removing a variety of anterior cranial base lesions with improved outcome (4,8,12,13,17,19,20,21). Involvement of the cavernous sinus and carotid artery has defined the limits of craniofacial resection. Piecemeal removal of malignant disease from the cavernous sinus violates the oncological principles of tumor-free margins and en bloc resection. If sacrifice of the carotid artery is at issue, precise evaluation of the cerebrovascular reserve is mandated before proceeding with en bloc resection. The presence of anatomical collateral circulation should be established with four-vessel angiography incorporating side-to-side and front-to-back crosscompression studies. Once the anatomical collateral has been confirmed, physiological and functional tests of its adequacy can proceed using CBF studies, transcranial Doppler, and balloon occlusion tests. Preoperative sacrifice of the carotid artery is not advised. Intraoperative evaluation of carotid involvement is advocated, and the surgeon should be prepared to reconstruct the vessel (2,18,22). Intraoperative evaluation demonstrated no tumor within the cavernous sinus, and carotid transposition rather than ligation was performed. In our case, the patient developed spasm at the carotid bifurcation. None of the preoperative vascular tests predicted this complication. The use of physiological modulation of cerebral blood flow with Triple-H therapy elevated and maintained CBF through the critical period of vasospasm. The ability to monitor CBF using an inexpensive, reproducible, repeatable method aided significantly in the postoperative recovery of this patient. The Xenon-133 CBF studies correlated with and anticipated clinical changes and guided the intensity and duration of treatment. Reconstruction of the massive defect resulting from this surgery is mandated for a successful outcome (6,7,9,16). The free flap taken from vascularized rectus muscle fat has several novel advantages. The vascularized fat conforms readily to the deep recesses of the defect and can act as a seal against CSF leaks (10,11). The flaps can be tailored to fill large, variously shaped defects. Reversing the flap allows free access to the vascular pedicle and use of the muscle for contouring the superficial portion of the defect. When the graft interfaces directly with the aerodigestive tract, the skin pedicle can produce a secure junction with the epithelial mucosa. This facilitates early oral feedings and prosthetic application. Vascularized reconstruction reestablishes
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PATHOLOGICAL FINDINGS Pathological examination of the en bloc specimen revealed a poorly differentiated adenocarcinoma involving the sphenoid and ethmoid sinuses, with extension through the orbital bone and involvement of the soft tissues of the orbit. The medial, lateral, and inferior margins were free of tumor, as were the cut ends of the olfactory tracts and the optic nerve. At the superior margin, tumor cells were found along the cribriform plate.
The tracheostomy was removed, and the patient was discharged on the 23rd day after surgery. At the time of this report (8 months after surgery), he has completed radiation therapy and returned to work. The patient's cosmetic result is acceptable (Fig. 8). His cosmetic reconstruction will be completed with prosthetic eye replacement and canthoplexy. Downloaded from https://academic.oup.com/neurosurgery/article-abstract/31/6/1126/2752152 by Midwestern University user on 12 January 2019
Vascularized free flap The reconstruction was completed with a reversed, vascularized rectus muscle free flap, which included the overlying vascularized abdominal fat. The facial artery and vein were isolated in the left side of the patient's neck. The muscle flap was sculptured to fit the defect, and the epithelium was removed. The flap was positioned with the vascularized fat against the pericranial flap and skull base. Placing the flap in this reverse fashion positions the vascular pedicle superficially and allows for Doppler monitoring. The pedicle is then tunnelled under the skin to the prepared facial artery and vein. A microvascular anastomosis was performed in end-to-end fashion with interrupted 9-0 single-strand nylon sutures. Total ischemic time for the flap was 2.5 hours, and the muscle flap perfused well once circulation was reestablished. Arterial and venous pulses to the muscle flap were audible by transcutaneous Doppler at closure. The final reconstruction consisted of a fascia lata duraplasty, a pericranial adjacent tissue transfer, and a vascularized free flap constructed from the rectus muscle and abdominal fat (Fig. 6). Total operative time was 22 hours.
ACKNOWLEDGMENTS The authors thank Dr. Douglas Anderson for his contribution to the neurovac, Julie Hipp for editorial assistance, Jill Gordey Wallock for graphics, and Sue Cottrill for illustrations. Received, January 28, 1992. Accepted, July 7, 1992. Reprint requests: T.C. Origitano, M.D., Ph.D., Division of Neurological Surgery, Loyola University Medical Center, 2160 South First Avenue, Maywood, IL 60153.
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Al-Mefty O, Anand VK: Zygomatic approach to skull-base lesions. J Neurosurg 73:668-673, 1990. Al-Mefty O, Khalil N, Elwany MN, Smith RR: Shunt for bypass graft of the cavernous carotid artery. An anatomical and technical study. Neurosurgery 27:721-728, 1990. Al-Mefty O, Smith RR: Tailoring the cranioorbital approach. Keio J Med 39:217-224, 1990. Anand VK, Al-Mefty O: Craniofacial lesions and resection, in Al-Mefty O (ed): Surgery of the Cranial Base. Boston, Kluwer, 1989, pp 167-191. Arbit E, Shah J, Bedford R, Carlon G: Tension pneumocephalus: Treatment with controlled decompression via a closed water-seal drainage system. Case report. J Neurosurg 74:139-142, 1991. Arena S, Fritsch M, Hill EY: Free tissue transfer in head and neck reconstruction. Am J Otolaryngol 10:110-123, 1989. Bridger GP, Baldwin M: Anterior craniofacial resection for ethmoid and nasal cancer with free flap reconstruction. Arch Otolaryngol
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Head Neck Surg 115:308-312, 1989. Cocke EW Jr, Robertson JH, Robertson JT, Crook JP Jr: The extended maxillotomy and subtotal maxillectomy for excision of skull base tumors. Arch Otolaryngol Head Neck Surg 116:92-104, 1990. Fisher J, Jackson IT: Microvascular surgery as an adjunct to craniomaxillofacial reconstruction. Br J Plastic Surg 42:146-154, 1989. House JL, Hitselberger WE, House WF: Wound closure and cerebrospinal fluid leak after translabyrinthine surgery. Am J Otol 4:126-128, 1982. Jones NF, Sekhar LN, Schramm VL: Free rectus abdominis muscle flap reconstruction of the middle and posterior cranial base. Plast Reconstr Surg 78:471-479, 1986. Ketcham AS, Wilkins RH, Van Buren JM, Smith RR: A combined intracranial facial approach to the paranasal sinuses. Am J Surg 106:698-703, 1963. Levine PA, Scher RL, Jane JA, Persing JA, Newman SA, Miller J, Cantrell RW: The craniofacial resection--eleven year experience at the University of Virginia: Problems and solutions. Otolaryngol Head Neck Surg 101:665-669, 1989. Origitano TC, Miller CJ, Izquierdo R, Hubbard T, Morris R: Complex cranial base trauma resulting from recreational fireworks injury. Neurosurgery 30:570-576, 1992. Origitano TC, Wascher TM, Reichman OH, Anderson DE: Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemic hemodilution ("Triple-H" therapy) after subarachnoid hemorrhage. Neurosurgery 27:729- 740, 1990. Schuller DE, Goodman JH, Miller CA: Reconstruction of the skull base. Laryngoscope 94:1359-1364, 1984. Schramm VL Jr, Myers EN, Maroon JC: Anterior skull base surgery for benign and malignant disease. Laryngoscope 89:10771091, 1979. Sekhar LN, Sen CN, Jho HD: Saphenous vein graft bypass of the cavernous internal carotid artery. J Neurosurg 72:35-41, 1990. Sisson GA Sr, Toriumi DM, Atiyah RA: Paranasal sinus malignancy: A comprehensive update. Laryngoscope 99:143-150, 1989. Smith RR, Klopp CT, Williams JM: Surgical treatment of cancer of the frontal sinus and adjacent areas. Cancer 7:991-994, 1954. Snyderman CH, Sekhar LN, Sen CN, Janecka IP: Malignant skull base tumors. Neurosurg Clin North Am 1:243-259, 1990. Spetzler RF, Fukushima T, Martin N, Zabramski JM: Petrous carotid-to-intradural carotid saphenous vein graft for intracavernous giant aneurysm, tumor, and occlusive cerebrovascular disease. J Neurosurg 73:496-501, 1990.
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CONCLUSIONS En bloc resection of malignant lesions of the anterior skull base is possible and is the next logical step in advancing surgical treatment of these lesions. Preoperative evaluation of cerebrovascular collateral circulation is mandated for this resection, and managing the vasculature and its complications is paramount to a successful outcome. Vascular reconstruction should be anticipated. The surgical technique should include saving the superficial temporal artery and preparing the saphenous vein as a graft. A multidisciplinary team is required. Adapting current surgical techniques and creating new approaches are necessary for successful resection and reconstruction. Scientific investigations of patient selection, operative morbidity, and impact on the natural history of the disease processes are needed to test the efficacy of these procedures.
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a competent immunological interface between the intracranial and extracranial compartment. With maturity, the vascularized graft will weather the rigors of adjuvant radiation.
REFERENCES: (1)
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Laligam N. Sekhar Pittsburgh, Pennsylvania
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COMMENTS Dr. Origitano and colleagues have described a very elegant operation for an en bloc resection of a tumor that bordered the cavernous sinus. In this particular case, carotid artery resection was not necessary. We have performed 11 en bloc resections of lesions that involve the cavernous sinus. Many of these cases involved sacrifice of the carotid artery. However, in some cases, the carotid artery could be preserved because there was no actual invasion of the cavernous sinus as in the case demonstrated by the authors (1). We find that the preoperative balloon occlusion test with clinical evaluation and xenon blood flow studies is still the best way of assessing the collateral circulation when planning carotid sacrifice for malignant tumors. However, if there are sacrifices performed, we have also found that they should be performed at the time of the operation by surgical occlusion rather than preoperatively by a balloon followed by surgical excision at a later time. The earlier procedure appeared to be associated with a higher incidence of embolic stroke, presumably because of the hypercoagulable state induced by the preoperative balloon occlusion of the carotid artery. If the carotid artery cannot be sacrificed, then revascularization can be performed. We presently prefer to revascularize using a long saphenous vein graft from the cervical internal or external carotid artery to the M2 or M3 segment of the middle cerebral artery about 2 weeks before the actual operation to resect the tumor. This is preferred to a direct venous saphenous vein graft bypass of the internal carotid artery in cases where there is a possibility of nasopharyngeal contamination and infection in the operative side. This greatly reduces the risk of infection of the graft and a carotid blowout. In the 11 patients with fast growing malignant tumors that had en bloc resection, 50% have survived over a median follow-up of 4 years. The remainder died of local recurrence, regional lymph node metastasis, or systemic metastasis. It is apparent that the adjuvant therapies for these tumors including radiation and chemotherapy have been quite ineffective and have not caught up with the surgical advances. Very careful preoperative patient selection and careful follow-up examination of these patients is necessary. The patient should also be informed preoperatively that such extensive surgical resection is really a treatment of last resort at the present time and is not guaranteed to cure the disease. Of course, many of the patients that we see presently are those for whom other treatment modalities, such as biopsy and radiation therapy and/or chemotherapy, were ineffective. Surgical resection for previously untreated malignancy in suitable cases should be studied prospectively.
Figure 3. Illustration depicting the initial intraoperative findings.
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Figure 2. The skull and orbit after the removal of bone.
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Figure 1. Axial MR image demonstrating the invasive lesion within the orbit, ethmoid sinus, and nasal cavity, and involving the medial wall of the cavernous sinus.
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Figure 5. En bloc specimen, frontal view.
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Figure 4. A, the transposed intracavernous carotid artery. B, MR image demonstrating the transposed carotid artery.
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Figure 6. A, illustration of reconstruction consisting of fascia lata duraplasty (cross-hatched area), vascularized pericranial graft (stippled area), and the vascularized rectus muscle-abdominal fat free flap. B, sagittal MR image after surgery, demonstrating the reconstruction.
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Figure 8. The patient shows acceptable cosmetic results 6 months after en bloc resection.
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Figure 7. A, left internal carotid angiogram demonstrating the transposed carotid and spasm distal to the transposition, including the takeoff of the A1 segment. B, xenon-133 cerebral blood flow studies were integral to treating the postoperative vasospasm. Triple-H therapy rapidly restored cerebral blood flow in the face of compromised collateral circulation.
