Surgical Approaches to Central Skull Base and Postsurgical Imaging Mohamad R. Chaaban, MD*, Bradford A. Woodworth, MD†, Surjith Vattoth, MD‡, R. Shane Tubbs, PhD§, and Kristen Owen Riley, MD§ The close proximity to or intricate involvement of critical neurovascular structures in the central skull base region or both present unique surgical challenges. Varied surgical approaches may be used to remove tumors in this region, including open craniotomies and minimally invasive transnasal or transfacial endoscopic approaches. The ideal surgical technique is chosen based on multiple factors including the aggressiveness, histopathology, and location of the tumor with respect to regional neurovascular elements. Postsurgical image analysis of the central skull base requires an intimate understanding of preoperative and expected postoperative appearance in relation to the nature of the excision and surgical materials used. Semin Ultrasound CT MRI 34:476-489 C 2013 Elsevier Inc. All rights reserved.

Introduction

S

urgical resection of central skull base lesions can be extraordinarily challenging owing to the close proximity to or intricate involvement of critical neurovascular structures or both. A number of surgical approaches may be used to excise these tumors including open craniotomies and minimally invasive transnasal or transfacial endoscopic approaches. The ideal surgical technique is chosen based on multiple factors including the aggressiveness, histopathology, and location of the tumor with respect to regional neurovascular elements. Extended or expanded endonasal techniques have become increasingly popular with advancements in optics, powered instrumentation, and expertise from widespread minimally invasive skull base surgical training.1-3 For appropriate indications, the endoscopic approach has several theoretical advantages over open craniotomies including decreased cerebral edema, less risk of cerebrospinal fluid (CSF) leakage,

Project Editor: Suzanne Byan-Parker. Tel.: þ1-205-934-4274; þ1-205-4823229 (mobile). E-mail: [email protected] The author thank medical illustrator David Fisher for providing the conceptual, anatomic illustrations. *Otolaryngology Head and Neck Surgery, Lanier Nasal & Sinus Institute, Valley, AL. †Department of Surgery, Division of Otolaryngology, The University of Alabama at Birmingham, Birmingham, AL. ‡Department of Radiology, Section of Pediatric Neurosurgery, The University of Alabama at Birmingham, Birmingham, AL. §Department of Neurosurgery, Section of Pediatric Neurosurgery, The University of Alabama at Birmingham, Birmingham, AL. Address reprint requests to Mohamad R. Chaaban, MD, Otolaryngology Head and Neck Surgery, Lanier Nasal & Sinus Institute, Valley, AL. E-mail: [email protected]

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0887-2171/$-see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.sult.2013.08.005

and stroke, as well as fewer cosmetic complications that accompany external incisions. Our purpose is to discuss the surgical management of cranial base lesions—focusing on the most common pathologies involving specific subsites of the central skull base.

Pathology of the Central Skull Base Benign Extradural Lesions Benign lesions arising from the posterior nasal cavity and sphenoid are common and include a variety of indolent, but sometimes aggressive processes. Infectious or inflammatory lesions, such as allergic fungal rhinosinusitis with significant skull base erosion, invasive fungal sinusitis, and mucoceles, may result in substantial erosion or invasion of the central skull base, affecting surrounding neurovascular structures. The most common epithelial tumor is an inverted papilloma, which has the potential for malignant degeneration into squamous cell carcinoma. Inverted papillomas often have an area of intense osteitic reaction at the site of origination or attachment and surgical resection is preferred treatment. Fibro-osseous tumors (eg, fibrous dysplasia) may involve the central skull base and can be surgically debulked or resected using an endoscopic transsphenoidal approach when the sphenoid (eg, tuberculum sella and sphenoidal part of the clivus) is affected.4-6 Fibro-osseous lesions involving the orbital apex may lead to compression of the optic nerve and thus surgical decompression should be considered.7 Juvenile

Surgical approaches to central skull base and postsurgical imaging nasopharyngeal angiofibroma (JNA), an unencapsulated tumor found most frequently in adolescent boys, is characterized by extreme vascularity and a high incidence of recurrence.8 JNA originates from the posterolateral roof of the nasal cavity, at the junction of the sphenoidal process of the palatine bone with the vomer. The tumor can grow into the pterygopalatine fossa (PPF), causing bowing of the posterior wall of the maxillary sinus. Further local extension of the tumor may reach the orbit and infratemporal fossa, as well as the middle cranial fossa. Although the aforementioned extradural lesions may be histologically benign, their proximity to critical structures and local aggressiveness with extension through the cranial base can result in significant morbidity and mortality.

Benign Intradural Lesions Pituitary tumors are the most common benign lesions arising above the central cranial base. Most pituitary neoplasms are histologically benign adenomas and are usually confined to the sella or suprasellar cistern. Extension into the cavernous sinus may make it difficult to distinguish them from other skull base tumors, such as nasopharyngeal carcinomas (NPC), sphenoidal sinus carcinomas, and chordomas.9 The clinical manifestations of functional (secretory) tumors depend on the hormone secreted, whereas large, nonfunctional (nonsecretory) tumors present with compressive symptoms such as visual field deficits or rarely, hydrocephalus. Parasellar extension into the cavernous sinus can occur in up to 40% of macroadenomas.10 Clinically, pituitary adenomas involving the cavernous sinus do not result in cranial nerve deficits unless the patient has hemorrhagic or nonhemorrhagic acute pituitary apoplexy. Conversely, chordomas, chondrosarcomas, and malignant tumors, such as metastases involving the cavernous sinus, typically present with cranial nerve deficits. Management of symptomatic large pituitary tumors, other than prolactinomas, is surgical. Other common lesions involving the sellar and suprasellar locations include craniopharyngiomas, Rathke cleft cysts, meningiomas, and epidermoids. Craniopharyngiomas originate from remnants of the Rathke pouch—the embryologic origin of the anterior pituitary gland.11,12 This tumor has a bimodal age distribution with higher frequency in school age children and adults between the ages of 50 and 60 years.13 Rathke cleft cysts also arise from remnants of the Rathke pouch. They typically occur in the midline and may not enhance with contrast or have thin peripheral enhancement.14 Rathke cleft cysts do not require surgical intervention unless symptomatic, as they have been observed to spontaneously decrease in size.15 Meningiomas can arise anywhere in the skull, but are commonly positioned in a suprasellar location involving the optic nerve sheath.16,17 They occur more frequently in women and present with progressive, painless visual deterioration with a normal appearing optic disc.16 Finally, epidermoid cysts are also located in the suprasellar region. The origin of these lesions is thought to derive from ectopic placement of neuroectoderm during embryologic development.18 Surgery is the treatment of choice for craniopharyngiomas and epidermoid cysts and can

477 be performed endoscopically, if there is only limited infratemporal lobe extension (Fig. 1). In general, management of skull base meningiomas includes observation, surgical debulking or resection, and radiation. Recommendations for an individual patient depend on the size and growth of the meningioma, baseline neurologic status, and resectability. Controversy exists within the neurosurgical community regarding aggressive surgical resection vs radiosurgical treatment of skull base meningiomas.19,20 For epidermoid tumors, surgical removal of all tumor or epithelial cyst lining is difficult, and lesions may require repeated surgeries (sometimes via different approaches) over a patient's lifetime. Cholesterol granulomas are the most common lesions found in the petrous apex. They typically occur in patients with pneumatized petrous apex and history of chronic otitis media. They are fluid filled and are lined with a thick capsule that lacks a true epithelial lining. The fluid is typically brown colored and contains granulation tissue as well as cholesterol crystals. Small lesions may be asymptomatic and are occasionally found incidentally on computed tomography (CT) or magnetic resonance imaging (MRI) scans for unrelated problems. As the lesion enlarges, patients can present with persistent headache, cranial nerve neuropathy, or brainstem dysfunction.

Malignant Extradural Tumors Sinonasal malignancies, such as squamous cell carcinoma, esthesioneuroblastoma, melanoma, adenocarcinoma, and sinonasal-undifferentiated carcinoma, may involve the central skull base. Management usually involves a combination of surgery and radiation or chemotherapy. The most common extracranial neoplasm to invade the central skull base is NPC. It is a unique central skull base region malignancy owing to its association with the Epstein-Barr virus. The highest incidence of NPC is in the southern Chinese population.21 This tumor most commonly originates in the fossa of Rosenmüller and frequently results in eustachian tube malfunction and otitis media.22 NPC can spread through various directions: anterior, posterior, lateral, as well as superior. The anterior, posterior, and superior routes affect the central skull base. Anterior NPC spread can involve the nasal cavity, with possible erosion of the infratemporal wall of the maxillary sinus.23 The tumor can also involve the central skull base and the PPF through the sphenopalatine foramen24,25 intracranial extension is possible via the foramen rotundum.26 NPC can also invade the inferior orbital fissure, orbital apex, superior orbital fissure, and cavernous sinus. Superior spread into the intracranial space can also occur through the foramen ovale.27,28 NPC lesions may cause atrophy of the masticatory muscles by infiltrating the mandibular nerve. Further extension of the tumor can involve the gasserian ganglion, trigeminal nerves, pons, and cavernous sinus.29 Management of nasopharyngeal tumors is with radiation with or without chemotherapy, with surgery reserved for recurrence. Chordomas and chondrosarcomas are similar in their location and radiologic signs, as well as symptoms, but differ

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Figure 1 (A) Coronal, T2-weighted MRI demonstrating a heterogenous-appearing epidermoid in the suprasellar region. The epidermoid appears to be abutting and partially engulfing bilateral ICAs. (B) Wide exposure of the suprasellar region with removal of bone between both optic nerves. Cruciate dural incision (arrow) provides access to the epidermoid cyst. Note the binostril approach with 2-handed technique used for tumor removal. (C) Transnasal endoscopic image demonstrating the 2-handed technique of removal of the intradural intracranial epidermoid. Note the typical white, flaky appearance of the tumor. (D) Endoscopic view capturing the cautious removal of residual epidermoid tumor abutting the right optic nerve close to the chiasm. (E) Remnants of the capsule (arrow) are adherent to the left A2 and anterior communicating artery complex. ICA, internal carotid artery.

in their histology, origin, and outcomes. Chordomas are considered low-grade malignancies, are unique tumors arising from notochordal remnants, and commonly occur at the spheno-occipital synchondrosis or sacrococcygeal region.30 However, chondrosarcomas arise from primitive mesenchymal cells or from embryonic rest of cartilaginous matrix of the cranium. Because of their aggressive nature, these lesions can cause destruction of the clivus and extend intracranially. Patients present with headache, cranial nerve palsies, and

visual disturbances.31 Surgical resection is usually a key part of management along with adjuvant radiation treatment.

Malignant Intradural Tumors Malignant intradural tumors of the central skull base include lymphomas, pituitary carcinoma, hypothalamic or chiasmatic astrocytomas, as well as metastases.32 Metastatic tumors can occur anywhere along the skull base, but most commonly

Surgical approaches to central skull base and postsurgical imaging present in the parasellar region.33 The most commonly found metastases are from primary sources such as breast, kidney, and thyroid gland tumors.34 The cavernous sinus is a frequent site of metastatic involvement. Patients will often present clinically with cranial nerve deficits and pain. The patient's discomfort and neurologic compromise often seem out of proportion to the size or volume of the tumor and are due to the rapid growth of the malignancy.

Surgical Approaches to the Central Skull Base We discuss surgical corridors with attention to indications and limitations of specific approaches. Outside the scope of this article, but critically important, are the techniques and challenges of skull base repair. For open cranial procedures, vascularized pericranial flaps are often used for skull base reconstruction. Endoscopic approaches frequently use a vascularized nasoseptal flap for repair and prevention of CSF leak. However, if pathology or prior treatment of surgery or radiation prevents the use of a nasoseptal flap, other repair options must be considered.

Sphenoidal Sinus and Sella Turcica Critical structures at risk from compression or invasion or both from sphenoidal sinus, sellar, and suprasellar lesions include the cavernous sinus, dura mater, internal carotid arteries, oculomotor nerves, pituitary gland, optic nerve and chiasm, trochlear nerve, ophthalmic nerve, abducens nerve, maxillary division of the trigeminal nerve, pterygopalatine ganglion, and sphenopalatine artery, as well as the vidian canal and its contents.35 Appropriate imaging is crucial for assistance with diagnosis, evaluation of local invasion or spread, and preoperative planning. The diagnosis and management of sphenoidal and sellar lesions usually involves the multidisciplinary effort of numerous specialties. When surgery is considered, benign and malignant lesions originating ventral or inferior to the internal carotid arteries and optic structures are often better accessed via a transnasal endoscopic approach. However, lesions may involve and even surround neurovascular structures and, thus, decrease the likelihood of complete surgical resection. Over the last decade, surgical removal of sphenoidal and sellar tumors has transitioned from the sublabial transsphenoidal approach36-39 to transnasal endoscopic techniques, now the standard procedure for excision of nongiant pituitary tumors. Craniotomies remain necessary for particularly aggressive tumors. For pituitary tumors, modification of the approach may depend on the waist of the tumor where it passes through the diaphragma sellae. In the transnasal approach, a narrowed waist has been considered a risk factor for visual loss postoperatively as a result of suprasellar bleeding.40 Complete tumor excision in the suprasellar area is also significantly hindered by the presence of an unenlarged sella.41

479 Several surgical techniques involve approaches to the sphenoid and sella. Traditional microsurgical approaches via a transseptal or sublabial incision, or endoscopic approaches may be performed. Endoscopically, both sphenoidal sinuses are opened and the posterior septum removed to allow maximal visualization. Depending upon tumor extent, further advancement toward the sella as well as the planum sphenoidale is then performed. For full exposure to the suprasellar area, the planum sphenoidale is removed and the dura mater is incised. In general, the lateral limitation of the exposure is because of the optic nerves and the internal carotid arteries. Although the primary difference between traditional transsphenoidal approaches and endoscopic technique is the use of the endoscope rather than the microscope, endoscopic approaches to the suprasellar area through the planum sphenoidale create much larger defects in the skull base. In fact, the development of this type of access can replace open craniotomy approaches for select lesions. The transnasal endoscopic technique offers the advantages of avoiding brain retraction, providing better cosmesis, and decreasing postoperative surgical pain, as well as improving ocular outcomes and reducing neurologic complications.42-49 However, the use of the transnasal endoscopic approach is not without hindrances: longer operative times are required, bleeding can obscure endoscopic visualization,44-46 and there is an associative higher likelihood of CSF leak, although it has decreased with the use of vascularized flaps, such as the nasal septal flap.50

Clivus Selection of surgical approaches to clival tumors depends upon patterns of extension through the skull base.51 These tumors can enlarge in all directions. Tumors with anterior spread and those that are restricted to the central skull base are readily removed via an intraoral or midline ventral approach, such as transsphenoidal access (endoscopic or sublabial). Inferior spread of these tumors to the craniovertebral junction may require a combination of more than one skull base approach, such as midface degloving to achieve complete resection.52,53 Tumors extending laterally to the petrous part of the temporal bone, but restricted to an area anterior to the internal acoustic meatus, require an extended middle fossa approach, or an orbitozygomatic infratemporal approach. Further lateral extension of tumors to involve the petroclival region necessitates total petrosectomy for access with further modifications, such as posterior mobilization of the facial nerve.54 Spetzler et al55 divided traditional lateral approaches into retrolabyrinthine, translabyrinthine, and transcochlear approaches. The retrolabyrinthine approach involves petrous resection with hearing preservation. The translabyrinthine approach requires more extensive petrous bone resection with compromise of hearing. The last technique is the transcochlear approach that involves maximal petrous drilling with sacrifice of hearing, as well as transposition of the facial nerve.55 These approaches provide access to the petroclival area with minimal brain retraction.

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480 Reports that are more recent have emerged on the use of endoscopic approaches for lateral extension of clival chordomas and chondrosarcomas. The endoscopic approach has significant advantages over the lateral skull base approach as it avoids sigmoid sinus ligation, facial nerve transposition with resultant paresis, sacrifice of the inner ear, and elevation of the internal carotid artery from the carotid canal.56 These procedures increase the operating time as well as operative risk. An endoscopic approach can expose a wide area between the temporomandibular joints transversely and an area from the sellar floor to the foramen magnum vertically.57,58 Laterally, exposure can also be obtained up to the foramina ovale and rotundum and is not limited by the internal carotid artery. Reassurance regarding the location of anatomical and vital structures can be checked with an intraoperative navigation system. Complete tumor removal is an important goal in the management of clival chordomas and chondrosarcomas. Transsphenoidal approaches to clival lesions have been the preferred approach; however, traditionally these have been performed with the microscope.4,59 Endoscopic techniques have demonstrated success with surgical resection in recent reports.5,60,61 In addition to being minimally invasive, advantages of this approach are that it provides the best anatomical trajectory of the lesions with elimination of the lateral skull base approach. This approach is an excellent choice for biopsy as well. It should be noted that safe performance of endoscopic techniques relies on appropriate case selection, as well as surgeon experience and training.

Orbital Apex Benign and malignant lesions of the orbital apex are difficult to treat effectively without compromising visual or oculomotor function. Malignant orbital apex lesions tend to occur more frequently in individuals older than 60 years.2 Although these tumors are typically benign, the proximity of critical structures may lead to significant morbidity as well as mortality.62 Approaches to the orbital apex include open cranial and transnasal endoscopic approaches. Selection of the approach largely depends on the characteristics of the tumor and the availability of the otolaryngologist and neurosurgeon, as well as the ophthalmologist, as deemed necessary for certain tumors. Smaller lesions located laterally or on the base of the orbit can be approached through a lateral orbitotomy or a transconjunctival approach. Lesions located dorsolaterally may be approached through a supraorbital route. Larger tumors require transcranial approaches, such as the pterional approach with resections that extend to the optic nerve medially. Not all tumors can be approached endoscopically. A multidisciplinary team consisting of the neurosurgeon, otolaryngologist, neuroradiologist, and an endocrinologist is recommended when deciding on the method of treatment. In addition to tumor histology, certain features of tumors can determine which approach would be best suited for removal. Contraindications to endoscopic endonasal removal include extension of the tumor to involve a

significant portion of the optic canal laterally as well as an extension lateral to the major neurovascular structures. In addition, an open approach is preferred if complete resection is required for these tumors, the tumor encases the internal carotid or anterior communicating arteries, or larger tumors are present (44 cm) with significant swelling around the tumor.45-47,63

Nasopharynx Nasopharyngectomy is indicated for recurrent NPC. There are several different approaches to this tumor, depending largely on the size, as well as the extent of tumor spread. Small mucosal recurrences can be approached through a transnasal endoscopic approach.64 However, this approach is contraindicated with parapharyngeal spread or bony skull base extension.65 Other approaches to the nasopharynx include the transpalatal approach, which is the most direct approach; however, it has limited superior exposure and carries the risk of oronasal fistula. Mandibulotomy is usually able to provide superior exposure and can reach and expose the vertical segment of the internal carotid artery, but not the petrous horizontal portion. Other approaches include the maxillary swing or midface degloving approach66 but these have limited superior exposure when invasion of the tumor is through the pterygoid plate or foramen ovale. In such a case, neurosurgical approaches are indicated,65,67-69 including the subfrontal approach, which exposes the cribriform plate, the fovea ethmoidalis, and planum sphenoidale.67 Tumors with extensive involvement can be approached best with the facial translocation technique, which is considered one of the best surgical approaches to the anterior and middle regions of the skull base.70 This option offers the most direct access to the central skull base for optimal exposure and preservation of critical structures.70 The approach can be combined with elective craniofacial osteotomies and subfrontal or subtemporal approaches to expose the entire central skull base.70,71 Access to nasopharyngeal tumors should be adapted according to the extension of the tumor. In its full extent, unilateral facial translocation can offer exposure from the contralateral fossa of Rosenmüller to the ipsilateral glenoid fossa. Combined with a subfrontal approach, extension to the ethmoid and cribriform plate can also be removed. If there is extension to the foramen ovale and lesser wing of the sphenoid, then the addition of a subtemporal approach would be needed for resection.

Petrous Apex Lesions in the petrous apex area of the skull base present a challenge to the neurosurgeon. Lesions in this area may reach a considerable size before becoming symptomatic and are in close relation to the major structures including the internal carotid artery, basilar and vertebral arteries, brainstem, as well as the cranial nerves. Similar to the other areas discussed, there are several skull base approaches to this

Surgical approaches to central skull base and postsurgical imaging region including transnasal endoscopic as well as open approaches Traditional, open techniques have been lateral, through the mastoid or ear, which typically require favorable anatomy to minimize morbidity. The ultimate decision on which approach to take depends on multiple factors including the pathology of the tumor, favorable anatomy of the patient, as well as the skill and experience of the surgeon.

Petrous Apex: Lateral Approaches Traditional approaches to the petrous apex include the temporal transpetrosal, transcochlear, translabyrinthine, extended middle fossa, transpalatal, transpharyngeal, as well as combined infratentorial and supratentorial approaches.72-87 Depending on the location and extent of the tumor, other approaches can be used including retromastoid and subtemporal approaches with lower reported complications than the standard skull base approaches.88 In a series using the retrosigmoid or pterional approach for the removal of skull base chondrosarcomas, the complication rate of CSF leak was reported as 10.3% and was managed with lumbar drain.89 The retrosigmoid approach was used in another series of patients with petrous apex meningiomas, with no reported complications82 However, neurologic deficits have been found to be fairly similar with the standard skull base approaches to the petrous apex, reporting rates of cranial nerve palsies between 33.5% and 40%.80,89,90 In patients with cholesterol granuloma, which are the most common lesions,91 drainage of the cyst is the only requirement,92 whereas in meningiomas and neurinomas, complete removal is preferred, given the increased rate of recurrence and improved survival. Biopsy only with subsequent chemotherapy or radiotherapy or both may be a better choice for tumors, such as metastases as well as malignant bone tumors.93 Radiosurgery may need to be discussed as a potential offering to the patient when extensive skull base approaches are contemplated for surgical removal of these tumors.84,94,95 The extended middle fossa transpetrosal-transtentorial route is the approach of choice for petroclival meningiomas.96 The complications of this approach, if not combined with other surgical approaches, appear to be less than the traditional open approaches.75,77 In patients who already have hearing loss secondary to the tumor, the translabyrinthine or transcochlear approaches can be used.79,97 An alternative to this procedure is the partial labyrinthectomy petrous apicectomy in which 2 of the semicircular canals are scarified with subsequent lower incidence of hearing loss.98,99 Additional complications for these procedures include CSF leak, occlusion of the vein of Labbé, flap hematoma, and wound dehiscence.76,98 The combined supra and infratentorial retrolabyrinthine approaches provide another lateral access to the petrous apex usually preserve hearing, but have complications including CSF leak and meningitis, which is around 13%-20%.100-102 The middle fossa approach preserves hearing, but requires brain retraction during surgery with possible subsequent brain injury. The open transsphenoidal approach to the petrous apex

481 was initially described by Montgomery103 and preserves inner ear function. In addition to tumor pathology and extent, individual patient anatomy must be considered when selecting the surgical approach. The degree of temporal bone pneumatization is important to consider when thinking about the lateral approaches,104 whereas the ideal candidates for the transnasal endoscopic approach is a patient with a wellpneumatized sphenoid sinus that allows access to the petrous apex behind the internal carotid artery. One study comparing both the lateral approach, as well as the transnasal endoscopic technique, found that the most important determinant factor in choosing the operation is position of vital structures, more so than pneumatization of the sphenoid or temporal bone.105 In the same study, authors found that easy surgical access through one technique does not predict the ease of access through the other. For this reason, patients should technically be considered for both operations. Ultimately, choice of surgical technique depends on many factors including mastoid and sphenoid pneumatization, location of vital structures, hearing or inner ear status, and more importantly, the pathology of the lesion.

Endoscopic Approach Endoscopic, skull base surgical advancements and imageguidance technology have led to the increased use of this technique for cholesterol granulomas. Approaches to lesions of the petrous apex can be performed through a unilateral sphenoidotomy; however, bilateral approaches are favored. This allows for a bimanual, 4-handed technique with the expertise of both neurosurgeons and otolaryngologists.106 The team approach is crucial when there is a risk of manipulation of the internal carotid artery106 and provides an improved angle for visualization and instrumentation.107-109 Endoscopic surgical access to the petrous apex includes the following: (1) the medial approach, (2) medial approach with internal carotid artery lateralization, and (3) a transpterygoid infrapetrous approach (below the petrous internal carotid artery). The choice of approach depends on relation to the carotid artery (medial or inferior), medial expansion of the tumor, as well as the pathology. An endoscopic transsphenoidal approach to the petrous apex may be contraindicated when there is no expansion of the petrous apex lesion into the sphenoid sinus or in the presence of a narrow corridor between the brainstem and the vertical segment of the internal carotid.110,111 This, however, is not an absolute contraindication as it has been demonstrated that removal can be assisted with image guidance.87 The infrapetrous approach has advantages over the medial technique because it provides exposure of the petrous lesion under the internal carotid artery. The medial approach provides access to the petrous apex with limitation laterally from the internal carotid artery. Complications may arise with endoscopic surgery, including arterial injury to the internal carotid artery as well as the basilar artery during removal of the clivus. Other morbidity

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Figure 2 (A) Unenhanced coronal T1-weighted image 3 months after pituitary macroadenoma resection shows hyperintense area of fat-packing material in the left anterior sellar resection bed (arrow). (B) Postcontrast coronal fatsuppressed T1-weighted image at the corresponding level shows hypointensity in the region due to suppression of fat signal (arrow), and there is no contrast enhancement. (C) Unenhanced coronal T1-weighted image 16 months after pituitary macroadenoma resection shows near resolution of the hyperintense fat-packing material (arrow). There are tiny foci of residual T1-hyperintense fat, which may remain for many years. (D) Postcontrast fat-suppressed MRI after 16 months shows mild enhancement of the resorbed fat-packing material (arrow).

includes injuries to neural structures including cranial nerve V (second or third divisions), dry eyes from vidian nerve dissection, or injuries to the sixth nerve while drilling the clivus. Venous oozing may also develop following removal of the clivus with bleeding primarily from the basilar venous plexus.

PPF Other than JNAs, tumors of the PPF primarily arise elsewhere and extend into this region. Multiple approaches to JNA surgical resection have been described in the literature. These include the traditional open techniques: transpalatal, transzygomatic, transmandibular, transhyoid, transantral as well the midface degloving or lateral rhinotomy and craniotomy.112 The endoscopic approach to the excision of these lesions was first described by Kamel.113 It has been reported that this technique is most useful for tumors that are limited to the nose, with no extension to the orbit, middle cranial fossa, or

infratemporal fossae.114 With more recent advances in endoscopic skills, these tumors can be removed endoscopically, unless there is gross intracranial extension. The additional advantage of intranasal removal is the ability to pull the tumor into the nasal cavity with only minimal dissection because it is not densely attached to the surrounding structures. Preoperative embolization has been controversial, but it has been shown to decrease intraoperative blood loss by approximately 60%.115 In addition to its morbidity, preoperative embolization may deal with the ipsilateral arterial system, but the tumor may receive blood supply from the contralateral side. Decreased recurrence rates have been reported in patients who were embolized before their surgery.116 The transnasal endoscopic approach is adequate for tumors with maximum stage II C (Sessions classifications).117 These tumors can extend to the ethmoid, maxillary, sphenoid, nasopharynx, or PPF and limited infratemporal fossa. A combined intracranial as well as extracranial approach is better suited for tumors that involve the middle cranial fossa.

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Figure 3 (A) Postcontrast coronal T1-weighted image show a moderate-sized pituitary macroadenoma-filling majority of the sella (vertical arrow). The compressed normal pituitary gland is seen displaced toward the right side of sella (in between horizontal arrows). (B) Unenhanced coronal T1-weighted image after complete transsphenoidal resection of macroadenoma shows hyperintense fat graft in the sella (arrow). (C) Postcontrast coronal fat-suppressed T1-weighted image show that the enhancing normal pituitary gland has re-expanded and now surrounds the hypointense suppressed fat graft (arrows).

Postoperative Imaging of Endoscopic Endonasal Surgery with Special Emphasis on Sellar Region Evaluation of the postsurgical sella requires a thorough understanding of the type and extent of surgical excision, packing material used, original preoperative appearance of the adenoma, and the evolution of expected postoperative MRI finding. Early postoperative imaging is critical following any brain tumor surgery as inflammatory changes beyond 24-48 hours after surgery may produce altered contrast enhancement. Additionally, time-sensitive degradation of blood and hemostatic synthetic materials like Surgicel and Gelfoam begins. These processes result in increased precontrast T1 signal (hyperintensity) that makes evaluation of contrast enhancement difficult in the subacute stage. In 2001, Kilic et al118 evaluated the postsurgical sella at 24 hours; at 3, 6, and 9 months; and at 1 year or more following pituitary adenoma surgery and found that early imaging at 24

hours postsurgery provides reliable information. The size and anatomical appearance of the postsurgical sella resembles its preoperative studies. Tumor region is now occupied by postsurgical material and the beginnings of deoxyhemoglobin or oxyhemoglobin blood accumulation. Confounding factors like inflammatory changes and T1-hyperintense methemoglobin blood-product accumulation have not yet begun. Identification of residual tumor at this early stage has a very high positive predictive value. In the same year, Yoon et al119 studied enhancement patterns suggestive of residual pituitary adenoma in early postoperative MRI and found that nodular or combined nodular or peripheral enhancement in the region of the resected adenoma suggested residual tumor. Absence of enhancement or only peripheral enhancement in the region usually excludes tumor. The peripheral enhancement represents compressed pituitary tissue or pseudocapsule if only fat graft is used,119 or granulation tissue, in case of gelatin-foam implant.120 It can be difficult in some situations to determine whether peripheral enhancement represents residual tumor, tumor

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Figure 4 Unenhanced coronal T1. (A) Postcontrast coronal, (B) postcontrast sagittal, and (C) T1-weighted images show the isointense C-shaped nasoseptal flap (arrows), enhancing on postcontrast images sealing the large bilateral anterior sellar floor and planum sphenoidale region skull base defect.

capsule, or pituitary gland. Ultimately, MRI surveillance studies can resolve this dilemma if the tissue stabilizes and conforms to a normal pituitary size and shape within the sella.121 A hypointense mass with peripheral enhancement may also be due to necrotic areas within the tumor, partial voluming from suprasellar cistern extension into the surgical defect, fibrous tissue with surrounding granulation, or nontumorous causes that do not progress on follow-up imaging.

Implant Materials and Packing: Influences on Postsurgical Imaging A variety of packing material is used for hemostatic control and to ensure closure of the central skull base defect. Knowledge of the MRI appearance of these materials is important. Early on, oxidized hemostatic cellulose materials such as Surgicel or Oxycel, demonstrate T1-hypointense signal and can show marked signal voids related to air bubbles embedded within the material. Days later, the material demonstrates minimal peripheral enhancement. Gelfoam, within the postsurgical sella, usually disappears in 3-6 months, shows signal characteristics of blood and fluid in the early 24-hour postoperative MRI, is isointense to gray matter in signal, and does not

enhance. Evaluation of both T1- and T2-weighted images is essential to identify this. Later, contrast-enhancing granulation tissue develops as the Gelfoam degrades and could mimic recurrent tumor. A fat graft, in contrast, usually disappears more slowly over 6-12 months and does not produce much contrast enhancement as it resolves. However, in our experience, mild contrast enhancement is sometimes seen and small foci of fat signal may remain for many years (Fig. 2). As expected the appearance of fat packing is dependent on the volume placed, and larger fat grafts will persist longer. The anticipated imaging appearance in some situations may guide the decision to place a fat graft or not. If the surgical excision is incomplete, as with cavernous sinus invasion, it might be better to use fat graft instead of Gelfoam to avoid confusing enhancing granulation tissue from Gelfoam degradation for tumor extent, especially if image-guided radiosurgery is contemplated.118,122 As explained earlier, the postsurgical pituitary mass constituted by the remaining normal gland and postsurgical changes with packing material and hemorrhage, with or without residual tumor, in the immediate postoperative MRI has the same dimensions as the combined volume of

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Figure 5 A 62-year-old man in whom nasoseptal flap could not be used during pituitary adenoma surgery owing to prior septal perforation. (A) Postcontrast sagittal T1-weighted MRI shows an enhancing graft extending from the lateral aspect of the nasal cavity inferiorly to seal the sellar floor defect up to the point of planum sphenoidale (arrows). Also, note the suprasellar residual tumor (vertical arrow). (B) Coronal postcontrast T1-weighted image through the anterior nasal cavity shows that the flap originates from the right inferior turbinate (arrow).

presurgical gland and tumor. Later the normal gland reexpands and the total bulk of the pituitary mass reduces owing to degradation of the blood and implanted material (Fig. 3). As expected, re-expansion of the normal pituitary is less prominent in microadenoma cases because of the smaller original pituitary mass.119 Dynamic pituitary MR imaging can help to differentiate the normal enhancement of the residual pituitary gland from granulation tissue or tumor-enhancement pattern. Implanted muscle with fascia is seen as round, T1 hypointensity in the sphenoid sinus with slight peripheral enhancement. In T2-weighted images, the denervated muscle shows increased signal, whereas a line of low signal intensity represents the fascia. There will be decreasing intensity of contrast enhancement on follow-up study. Bladowska et al122 reported no significant change in the T2 signal intensity within the implanted muscle and fascia in follow-up MRI up to 31 months. In addition, there was no decrease in the volume of the implanted muscle and fascia, unlike the fat implants, which demonstrated progressive resorption. However, they did note that small foci of fat could be seen for as long as 10 years yet, hemostatic material disappeared approximately 1 month after surgery, in contrast to the observation by Kilic et al118 that Gelfoam degrades by 3-6 months.

Reconstructive Grafts Knowledge of the various avascular and vascular graft options for skull base reconstruction is essential to evaluate postsurgical MRI scans. Smaller skull base defects from endoscopic endonasal transsphenoidal pituitary tumor resection could be effectively sealed with fat or inlay-onlay using Alloderm or fascia lata. Larger defects of the anterior skull base from expanded endonasal surgeries are best reconstructed with a vascular pedicle nasoseptal mucoperiosteal flap based on the nasoseptal artery (Hadad-Bassagasteguy flap). The nasoseptal

flap could be used to seal any skull base defect, does not require an inlay bony buttress, and is especially useful if the defect extends to optic nerve and internal carotid artery bony margins. The graft should also cover any soft tissue or bony defect on the nasal side to avoid CSF leak. The most important predictor of postoperative CSF leak is the need to open the CSF cisterns widely during the surgery, producing high-flow intraoperative leak.123 There is no need for intranasal reconstruction for endoscopic pituitary surgery if there is no intraoperative CSF leak or exposure as per Sonnenburg et al.124 A multilayer reconstruction is used with an inlay subdural graft over which the nasoseptal flap can be applied directly to the dura. Alternatively, it could be placed on an onlay graft of fat or fascia. The flap is fixed with a glue and nasal sponge packing or 14-F Foley balloon-catheter helps to hold it in place. On performing an MRI, the flap is seen as a C-shaped, isointense structure underlying the surgical defect in precontrast T1- and T2-weighted images and shows contrast enhancement in postgadolinium T1-weighted images. The multilayer inlay and onlay graft material is seen as a linear hypointense, nonenhancing structure deep to the flap on precontrast and postcontrast T1-weighted images and shows slight T2 hyperintensity. Postoperative debris and fluid is seen as T2 hyperintense material superficial to the flap in early postsurgical MRI, which resolve in later follow-up studies (Fig. 4). Foley catheter-balloon holding the flap in place is seen in early studies, and is usually removed by third to fifth postoperative day.125 Kang et al125 noted variation in enhancement patterns including thinner enhancement of the flaps in follow-up MRI studies after a few months compared with the immediate postoperative study in 60%, which correlated with the general follow-up endoscopic findings of contraction in the flaps. There was thicker enhancement in 30% (3 of 10), which was attributed to the operative bed granulation tissue found at later

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Figure 6 A 50-year-old woman with complex history of large invasive macroadenoma treated by endoscopic resection followed by radiation to the skull base. She subsequently developed right-sided CSF rhinorrhea. (A) Precontrast T1-weighted sagittal image show postoperative appearance of deformed sella and residual tissue at the skull base. (B) Axial T1-weighted image show nonspecific abnormal signal extending inferiorly and anteriorly into the posterior ethmoid region. (C) CT cisternogram does not clearly demonstrate contrast within the region of abnormality in posterior ethmoid (arrow). (D) MRI with intrathecal gadolinium done at the same setting appears to be more sensitive and shows opacification of the sellar region as well as subtle contrast layering within the posterior ethmoid component (arrow). The CSF leak was successfully repaired surgically.

endoscopy or increased flap mucosalization. Twenty percent of their patients (2 of 10) did not show flap enhancement in the early study but enhanced on follow-up. Ten percent (1 of 10 patients) did not show enhancement in the follow-up study, but had shown enhancement in the immediate postoperative MRI. They postulated that nonenhancement may be the result of vascular compromise from injury or compression and could be a predictor of flap failure or CSF leak in larger skull base defect repair However, none of their patients with nonenhancing flaps had a CSF leak. In 2012, Adappa et al126 retrospectively studied 19 patients with immediate postoperative MRI scans to determine if nonenhancement of the nasoseptal flap is predictive of CSF leak development. In their study, 3 patients who developed CSF leaks had enhancing flaps, yet there was no CSF leak in another 3 patients whose vascular nasoseptal flaps did not enhance. They concluded that CSF leak in patients with

nasoseptal flaps were associated more with posterior fossa lesions and that nasoseptal flap enhancement was associated with younger age. The nasoseptal flap can desiccate and contract if its mucoperichondrial surface is not opposed to the denuded sinonasal cavity, with the higher risk for flap displacement or migration being along the superior margin of the surgical defect. Care should be taken that fat (hyperintense on non–fat suppressed T1), bone wax, or surgical clips (may not be clearly visualized in MRI scan) placed deep to the flap does not interpose between the denuded sinonasal cavity margins and the flap, to avoid flap displacement and CSF leak. Flaps that are rotated with the mucosal surface—facing the defect instead of the sinonasal cavity—will not heal and is another cause of flap failure. MRI cannot differentiate the mucosal and mucoperichondrial surfaces and will show normal flap enhancement and miss this cause of failure.

Surgical approaches to central skull base and postsurgical imaging A pericranial flap can be used as an alternative to repair sellar or anterior skull base defects, when nasoseptal flaps are unavailable. However, it will be difficult for the vascular pedicle of endoscopically harvested pericranial flaps to reach the posterior skull. The inferior turbinate flap can be used for small clival defect repair, but defects larger than 1 cm may require an additional fat bolster. This flap cannot reach the anterior cranial fossa or suprasellar region owing to the vascular pedicle-length constraints. Inferior turbinate flap from the anterior aspect could, however, be used for sellar floor repair (Fig. 5). Temporoparietal fascial flaps could efficiently seal parasellar and clival defects; however, these cannot be used adequately for anterior skull base repair, owing to limitations in the arc of rotation needed to tunnel the pedicle through the PPF. The less commonly used flaps include middle turbinate flaps, which aid in repairing small sphenoid and anterior cranial fossa defects. Theoretically, the pedicled palatal flap can be used for any skull base region reconstruction, as it has a longer pedicle. But dissection of palatine canals is difficult, and there is a chance for complications in the oral cavity donor site, and is not commonly used.123 CSF leaks can be evaluated using CT cisternograms after intrathecal administration of iodinated contrast material, which show the skull base defect, and the leakage of contrast-opacified CSF. Alternatively, noninvasive methods, such as T2-weighted MR cisternograms, whose heavily T2-weighted sequences show fluid-signal CSF leak, can be effectively used in correlation with the plain, high-resolution CT scan showing a bony defect in the same location. Recently we could demonstrate a CSF leak into the posterior ethmoid sinus (complicating endoscopic pituitary adenoma resection) using the highly sensitive T1 MR cisternogram acquired after injection of 0.4-mL ProHance gadolinium contrast intrathecally (Bracco Diagnostics Inc, Princeton, NJ). Interestingly, the leak was not demonstrated in a CT cisternogram done in the same setting; however, the leak was confirmed surgically and repaired successfully (Fig. 6).

Conclusions Surgical management of central skull base lesions can be challenging, given the close proximity to critical neurovascular structures. The ideal surgery is selected based on a multidisciplinary team that may consist of neurosurgeons, otolaryngologists, ophthalmologists, neuroendocrinologists, neuroradiologists, as well as neuropathologists. The pathology, extent of tumor growth and behavior, anatomy, as well as surgeon's experience are critical factors that determine surgical technique. A detailed understanding of the type and extent of surgical excision, packing materials and flaps used, original preoperative appearance of the lesions and expected chronologic postsurgical MR appearance is essential to evaluate adequately the postoperative scan.

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Surgical approaches to central skull base and postsurgical imaging.

The close proximity to or intricate involvement of critical neurovascular structures in the central skull base region or both present unique surgical ...
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