Endoscopic Surgery - Complications.mg PDF

See the corresponding editorial in this issue, pp 15411543.
J Neurosurg 114:15441568, 2011
Endoscopic endonasal skull base surgery: analysis of complications in the authors initial 800 patients
A review
Amin B. Kassam, M.D.,1,2 Daniel M. Prevedello, M.D.,1 Ricardo L. Carrau, M.D.,1,2 Carl H. Snyderman, M.D.,1,2 Ajith Thomas, M.D.,1 Paul Gardner, M.D.,1 Adam Zanation, M.D., 2 Bulent Duz, M.D., 3 S. Tonya Stefko, M.D.,1,4 Karin Byers, M.D., 5 and Michael B. Horowitz, M.D.1
Departments of 1Neurological Surgery, 2Otolaryngology, 4Ophthalmology, and 5Medicine, Division of Infectious Disease, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania; and 3Department of Neurosurgery, Gulhane Military Medical Academy, Ankara, Turkey
Object. The development of endoscopic endonasal approaches, albeit in the early stages, represents part of the continuous evolution of skull base surgery. During this early period, it is important to determine the safety of these approaches by analyzing surgical complications to identify and eliminate their causes. Methods. The authors reviewed all perioperative complications associated with endoscopic endonasal skull base surgeries performed between July 1998 and June 2007 at the University of Pittsburgh Medical Center. Results. This study includes the data for the authors first 800 patients, comprising 399 male (49.9%) and 401 female (50.1%) patients with a mean age of 49.21 years (range 396 years). Pituitary adenomas (39.1%) and meningiomas (11.8%) were the 2 most common pathologies. A postoperative CSF leak represented the most common complication, occurring in 15.9% of the patients. All patients with a postoperative CSF leak were successfully treated with a lumbar drain and/or another endoscopic approach, except for 1 patient who required a transcranial repair. The incidence of postoperative CSF leaks decreased significantly with the adoption of vascularized tissue for reconstruction of the skull base (< 6%). Transient neurological deficits occurred in 20 patients (2.5%) and permanent neurological deficits in 14 patients (1.8%). Intracranial infection and systemic complications were encountered and successfully treated in 13 (1.6%) and 17 (2.1%) patients, respectively. Seven patients died during the 30-day perioperative period, 6 of systemic illness and 1 of infection (overall mortality 0.9%). Conclusions. Endoscopic endonasal skull base surgery provides a viable median corridor based on anatomical landmarks and is customized according to the specific pathological process. This corridor should be considered as the sole access or may be combined with traditional approaches. With the incremental acquisition of skills and experience, endoscopic endonasal approaches have an acceptable safety profile in select patients presenting with various skull base pathologies. (DOI: 10.3171/2010.10.JNS09406)
minimally invasive approach has been defined as access and visualization through the narrow est practical corridor providing maximum effec tive action at the target with minimal disruption of normal tissues.8,28,45,50 Skull base surgery, like other subspecialties, has evolved to include minimally invasive procedures, such as endoscopic endonasal skull base surgery.2,3, 5,6,15,27,29,30,32,37,42,46 As with other evolutions in surgery, acceptance of a new procedure requires proof of its feasibility, safety, and efficacy.43,47,50 Various reports have described EEAs to the ventral skull base.3,5,23,24,27,29,30,32,52 The origin of these approaches
Key Words endonasal approach endoscopic surgery skull base surgery complication safety
Abbreviations used in this paper: AVM = arteriovenous malformation; BA = basilar artery; CA = carotid artery; CN = cranial nerve; EEA = endoscopic endonasal approach; ICA = internal CA; MPW = medial pterygoid wedge; VA = vertebral artery.
can be traced to EEAs to the sella turcica with the defining work being undertaken by Carrau, Jho, Cappabianca, Frank, and others.3,20,50 This seminal work was then expanded to treat lesions beyond the sella. This required the combined efforts of otolaryngologists and neurosurgeons, who used their respective experiences in endoscopic sinonasal surgery and pituitary surgery to take advantage of the enhanced visualization provided by rod lens endoscopes.6,15 This natural expansion to treat other areas resulted in well-defined anatomy-based modular approaches that access the median ventral skull base (between the ICAs), extending from the crista galli to the odontoid. We refer to this as the sagittal plane.29,30,37 Once these median approaches were defined, the EEAs expanded in a paramedian (that is, lateral to the ICA) direction. We refer to this as the coronal plane.32,40 Understanding the anatomy of the ICA as it courses along the skull base (median
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Complications in endoscopic endonasal approaches

and paramedian planes) is critical to the conception and use of the endonasal endoscopic modules.7,32,57 Once the anatomical basis for any new surgery is defined and its feasibility is established, its safety and efficacy must be documented. Safety is of utmost priority, and efficacy can only be assessed after many years of longitudinal follow-up. In this report, we analyze our experience with major perioperative complications associated with the use of EEAs in our first 800 consecutive patients. We also discuss our surgical evolution based on incremental experience and the development of anatomical modules. This will provide the reader with the necessary perspective to understand the use and limitations of the modular approaches and to sequentially gain experience with EEA techniques while remaining cognizant of their associated complications. riving from the surgical procedure and affecting the patients health, within at least 30 days after the procedure (some complications included in the study occurred after 30 days). Postoperative complications were divided into infectious, systemic, and delayed deficits. Infectious and systemic complications were assessed as a potential cause of death or neurological deficits (permanent or transient). As a special point of interest, the incidence of postoperative CSF leaks was tracked, and the impact of the leak on patients morbidity was determined separately. Delayed deficits were defined as events that, while directly related to the procedure, manifested in a delayed fashion (for example, postoperative hematoma). Delayed complications were similarly assessed to ascertain whether they resulted in permanent or transient neurological deficits.
Defining the Complexity of the Cases
We retrospectively reviewed the clinical data of all patients who underwent EEAs to treat various skull base pathologies at the University of Pittsburgh Medical Center between July 1998 and July 2006 (600 patients) and prospectively collected data between August 2006 and July 2007 (200 patients) (institutional review board #0512017). We used the number of patients as our common denominator; therefore, patients who underwent multistaged procedures or who needed endonasal endoscopic procedures to remedy a perioperative complication were counted only once. However, patients who presented with recurrent disease more than 6 months after their initial surgery were counted as separate events. For investigational purposes, the patients were categorized into 4 age groups as follows: 35 years, > 35 to 50 years, > 50 to 62 years, and > 62 years. The goal of the patient analysis was to identify major complications that led to morbidity and mortality in the series and correlate them with other variables such as patient age and sex, pathology, case complexity, and module of approach. Minor complications such as sinusitis, nasal morbidity, and deep venous thrombosis were not included in the study. Furthermore, data on clinical outcomes (tumor resection, recurrence, vision improvement, endocrine results, and so on) are beyond the scope of this study and are not presented.
Classification of Complications
Methods
Morbidity was classified as neurological and nonneurological. Neurological morbidity was then divided into permanent and transient deficits. To better understand the specific causes of morbidity and mortality, all complications were also categorized as intraoperative or postoperative. Intraoperative complications were defined as those complications that occurred during surgery and were immediately and directly caused by the surgical intervention. These were divided into vascular and neural injuries. Conversely, vascular complications were assessed as a potential cause of death or neurological deficits. All neural injuries were assessed to determine whether they were permanent or transient. A postoperative complication was defined as one de-
In an effort to describe the evolution of our surgical experience, we classified the complexity of the cases into 5 categories or levels, based on key anatomical and pathological conditions. These levels were based on anatomical considerations, potential complications, and the anticipated surgical experience needed to manage these complications. While somewhat arbitrary, they reflect our sequential gain of experience and our own progression in treating patients with pathologies that presented incremental surgical complexity (Table 1). In our classification, Level I procedures correspond to sinonasal surgery for inflammatory disease or for the management of epistaxis. These procedures are considered to have the lowest risk of major complications, because the bony cover of the skull base protects the neurovascular structures. Thus, patients requiring Level I procedures were excluded from the study, as they do not represent endoscopic skull base surgery. However, these represent important experiences in the learning process, because the sinonasal tract delineates the working space/ corridor for all other levels. Level II procedures include endoscopic endonasal repair of CSF leaks and removal of pituitary adenomas with or without suprasellar extension (those that did not require subarachnoid dissection). These procedures often represent the initial experience of the surgical team with endoscopic endonasal transgression of the skull base. Their anticipated major complication rate is greater than that of Level I procedures but less than Level III. We believe that these procedures are critical to develop endoscopic skills. Level III procedures include extrasellar extradural dissections. They require drilling of the skull base to expose but not transgress the dura. An example of a Level III procedure is an odontoid resection for decompression of the brainstem in a patient with pannus due to rheumatoid arthritis. Other examples are sinonasal malignances that do not cross the dura, optic nerve decompressions by extradural drilling of the optic canal, and juvenile angiofibromas. Level III procedures require a thorough understanding of the endoscopic anatomy of the ventral skull base, because critical neurovascular structures are located immediately under the exposed dura.
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TABLE 1: Levels of complexity of endoscopic endonasal skull base procedures Level I II III Corresponding Procedure(s) sinonasal op pituitary op, CSF leak extradural op transcribiform transplanum transclival transodontoid intradural op w/ cortical cuff (IVa) transplanum transcribriform preinfundibular craniopharyngioma w/o cortical cuff (IVb) transplanum transcribriform infundibular craniopharyngioma retroinfundibular craniopharyngioma transclival intradural cerebrovascular op coronal plane aneurysm, AVM
IV
Level IV procedures include those that require intradural surgery; therefore, the frequency and magnitude of complications should theoretically increase. These cases require opening of the dura to access lesions that include purely intradural pathologies and invasive lesions of the skull base that destroy or invade the subdural space and brain parenchyma. Level V procedures represent cerebrovascular surgery and include endoscopic endonasal surgery for the treatment of aneurysms and vascular malformations as well as lesions that require significant manipulation or mobilization of the ICA. From the endonasal standpoint, the ICAs bracket the median skull base as they course from the cervical region to their intracranial position. Any pathological entity that is located lateral or posterior to the ICA requires dissecting, exposing, or even transposing this vessel. Therefore, we consider these procedures as Level V. Although the incidence of complications may not be higher in this group (assuming a conscientious and progressive learning), the complexity of the management and the potential impact of the complications are significantly higher than those associated with the earlier levels. In the series, 3 Level V cases were aneurysms including 1 VA and 2 superior hypophysial artery aneurysms that were clipped endonasally.33,34 One intraosseous clival AVM in a child with Down syndrome was also treated by EEA in the series.39 All other Level V cases were classified as such due to ICA surgical dissection.
Defining the Modules of Approaches and Risks for Complication
Fig. 1. Illustration showing the skull base in an inferior view. Each colored area represents a module of expanded endonasal approach at the skull base. CP-AF = coronal plane anterior fossa; CP-MF = coronal plane middle fossa; CP-PF = coronal plane posterior fossa; TC = trans clival (pink area); TC = transcribriform (white area); TO = transodontoid; TP/T = transplanum/transtuberculum; TS = transsellar.
zone represents the target of a corresponding anatomical corridor, and pair matching is the basis for our modular approaches. Using an augmented nasal corridor, these modules (sequential approaches) may be combined to control multiple areas of the skull base. All cases were classified according to the actual approaches used during surgery. We have grouped these modules into 2 general categories based on their relationship to the ICA. Those oriented in the sagittal plane include the median region between the 2 ICAs as they course along the ventral skull base (Table 2). Conversely, modules in the coronal plane comprise areas (targets) located lateral to the ICA (paramedian, see Table 3). Patients undergo preoperative CT angiography to be used for frameless stereotactic image guidance during the procedure fused with a contrast MR image in selected cases (Stryker-Leibinger Corp.). Following orotracheal intubation, the patient is placed in a 3-pin head holder positioned with the neck slightly extended and slightly turned to the right. The nose is decongested with topical 0.05% oxymetazoline applied using 0.5 3in cottonoids. A povidone solution is applied to the perinasal and periumbilical areas (in the event that an autologous fat free graft is required for reconstruction). Creation of a bilateral nasal (binares) corridor is the
J Neurosurg / Volume 114 / June 2011 General Aspects of the Surgery
To further assess the safety of EEA, the ventral skull base was subdivided into anatomical zones (Fig. 1). Each
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TABLE 2: Median sagittal plane EEAs* Module Corridor Anatomical Boundary SIS to IIS, cavernous to cavernous Cistern subdiaphrag matic & suprasellar Neurovascular Structures carotid siphon; medial cavernous sinus; CNs III, IV, & VI; optic chiasm ant circle of Willis, chiasm, optic nerves, stalk, gyrus rectus, & orbitofron tal gyrus A 2 & orbitofrontal, infe rior sagittal sinus, gyrus rectus, orbito frontal gyrus CN III bilat, pituitary stalk, mammillary bodies, BA, P1 & P2, PCoA, midbrain, pons BA, pst circle of Willis, CN VI, pons CN VI bilat, CN XII bilat, VAs, medulla Key Anatomical Landmark Common Pathology
transsphenoid & pst sellar ethmoid transpla- sphenoid & pst num ethmoid
tuberculum sellae, sellar RCC, pituitary adenoma floor, 4 blues SIS to IIS & cavernous sinuses medial opticocarotid re cess, optic canals meningioma, pituitary adenoma, craniopharyngioma meningioma, esthesio neuroblastoma, ol factory schwannoma meningioma, chordo ma, craniopharyngio ma, pituitary adenoma
pst ethmoidal artery, suprasellar, sella pst, optic can- IHF als, paraclinoid ICA laterally IHF
transcomplete ethmoid, back wall of frontal sicribri- & frontal sinus nus to planum, form Draf III lamina papyracea to lamina papyracea upper sphenoid & naso- dorsum sella, pst 1/3 of pharynx, & pi- clinoid, Dorello clivus tuitary transpo- canal sition
ant & pst ethmoidal arte ries, falx, periorbita
middle 1/3 of clivus lower 1/3 of clivus transodontoid
sphenoid & naso- Dorello canal (sellar pharynx floor) to level of foramen lacerum sphenoid & naso- foramen lacerum level prepontine, pharynx through basion cervicomedullary nasopharynx basion to arch of C-1 cervicomedullary
ant 3rd ventri cle, interpe duncular & prepontine cistern, Liliequist membrane prepontine
parasellar ICA, dorsum sellae, PC, pituitary transposition, & cavern ous sinus
VBJ margin, origin of ab ducens nerve, Dorello canal VBJ margin, origin of ab ducens nerve
meningioma, schwan noma, chordoma, chondrosarcoma meningioma, chordo ma, chondrosarcoma meningioma, chondro sarcoma, chordoma
VAs, CN XII bilat, ETs, odontoid ligaments, medulla, spinal cord, condyles ant spinal arteries
* ant = anterior; bilat = bilaterally; ET = eustachian tube; IHF = interhemispheric fissure; IIS = inferior intercavernous sinus; PC = posterior clinoid; PCoA = posterior communicating artery; pst = posterior; RCC = Rathke cleft cyst; SIS = superior intercavernous sinus; VBJ = vertebrobasilar junction.
initial step of all the modules with rare exceptions. This is the prerequisite of all EEAs and consists of resecting or lateralizing the right middle turbinate and lateralizing the left middle turbinate. The key element to the binares approach is a posterior septectomy that allows unencumbered bimanual maneuverability of the instruments while avoiding contamination of the endoscope, thereby optimizing visualization. Over the past decade we have strongly advocated this bimanual approach as the foundation of all expanded endoscopic approaches.29,30,50 Rare exceptions for binostril approaches are situations in which noncomplex diseases involve only 1 of the nasal cavities and/or anterior skull base extradurally (that is, unilateral CSF leak from the anterior fossa, unilateral orbit and optic nerve decompression, and so on). Other unusual circumstances include children, particularly those younger than 3 years of age with exceptionally small nostrils to pass instruments and in whom a sublabial incision is required to enter the piriform aperture. The exposure is initiated using a 0 rod lens endoscope (Karl Storz). We use an irrigating system, either an endoscopic sheath or manual irrigation with a 60-ml
syringe, to clean the lens of the endoscope and maintain visualization. Lateralization of the inferior turbinates increases the space for the insertion and manipulation of the instruments. A right middle turbinectomy is usually performed, particularly in expanded approaches. Hemostasis of the posterior attachment of the middle turbinate, containing a branch of the sphenopalatine artery, is achieved with a suction electrocautery. The contralateral middle turbinate is preserved and outfractured, allowing a wider corridor. At this point, we harvest a nasoseptal flap pedicled on the posterior septal arteries of the contralateral side. This flap is used for reconstruction of the skull base defect at the end of the procedure, but its elevation precedes the posterior septectomy, as otherwise the septectomy would destroy its blood supply. The flap is stored either in the nasopharynx or in the ipsilateral maxillary sinus to protect it during the dissection and to facilitate visualization. A posterior nasal septectomy in addition to wide bilateral sphenoidotomies and posterior ethmoidectomies complete the nasal corridor. The floor of the sphenoid sinus is then drilled using a 3- or 4-mm hybrid cutting/
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TABLE 3: Paramedian plane approaches* Module transorbital Corridor endonasal, trans ethmoid complete endonasal, maxil lary antrostomy, pterygoid process endonasal, transsphenoidal Anatomical Boundary from ant skull base to maxillary sinus, lamina papyracea Cistern ant fossa Neurovascular Structures optic nerve; CNs III, IV, & VI; ophthalmic nerve; ophthalmic ar tery; ethmoidal arteries V1V3, IMA & branches, vidian nerve & artery Key Anatomical Landmark Pathology
optic canal, superi - schwannoma, hem or orbital fissure, angioma, menin lamina papygioma racea schwannoma, angio fibroma chondrosarcoma, cholesterol granu loma, cholestea toma, chordoma chondrosarcoma, cholesterol granu loma, cholestea toma, chordoma schwannoma, men ingioma chondro sarcoma, chor doma, CSF leak hemangioma, menin gioma, pituitary adenoma, schwannoma schwannoma, menin gioma, angiofibro ma, CSF leak schwannoma, menin gioma, paraganglioma paraganglioma, me ningioma, schwannoma
transpterygoid
Zone 1 (pe trous apex) Zone 2 (infrapetrous)
from medial to lat middle fossa pterygoid plates, from V2 to maxillary floor level medial & pst to parapst fossa, clival ICA middle fossa inferior to petrous ICA, pst fossa, lat to vidian nerve cerebellopontine cistern quadrangular space: middle fossa, superior to petrous Meckel ICA, lat to paraclival cave ICA, inferior to CN VI, medial to V2 lat to cavernous ICA middle fossa (siphon), superior to quadrangular space lat to lat pterygoid plate, medial to mandible lat to inferior 1/3 of clivus, medial to ascending parapha ryngeal ICA lat to parapharyngeal ICA middle fossa
endonasal, trans pterygoid, medi al maxilla, fossa of Rosenmller Zone 3 (supra- endonasal, medial petrous) maxilla, transpterygoid Zone 4 (cavernous sinus) Zone 5 (temporal-infratemporal fossa) Zone 6 (condyle) endonasal transpterygoid
pterygoid wedge, pst wall of max illary sinus, pterygoid plates CN VI, ICA, vidian nerve vidian nerve, CN VI at Dorello canal, carotid protuberance vidian nerve & artery, V2 vidian nerve, ET, & V3, petrous ICA, petroclival syn CNs VII & VIII chondrosis CN VI, V1V3, petrous & paraclival ICA, vidian nerve CNs III, IV, & VI; V1V3; cavernous ICA; meningohypophysial trunk; inferolateral trunk IMA, V2 & V3, temporal lobe, parapharyngeal ICA vidian nerve, ca rotid protuber ance, foramen rotundum, V2, ET sella, parasellar carotid (cavern ous ICA), optic canal
endonasal trans pterygoid, Denker endonasal transpterygoid
Zone 7 (jugular endonasal, transforamen) pterygoid, Denker * IMA = internal maxillary artery.
pst fossa, cerebellomedul lary cistern pst fossa, jug- CNs IXXII, parapharyn ular fora geal ICA, jugular vein men
lat pterygoid plate, foramen rotun dum, V2 & V3, ET parapharyngeal ICA, CN ET, foramen mag XII, VA num, occipital condyle ET, occipital con dyle, parapha ryngeal ICA
diamond bur until it is reduced to be in the same plane as the clival recess. From this point, the approach can vary depending on the pathology or module used.
Modular Approaches in the Sagittal Plane
Approaches in the sagittal plane were divided into transsellar, transplanum, transcribriform, transclival, and transodontoid approaches. Multiple cases required more than 1 module to approach a complex lesion. To facilitate statistical analysis, we created the category combined median approach for those cases in which more than 1 median module was required.
Transsellar Approach. The working corridor for this module includes a posterior septectomy, wide bilateral
sphenoidotomies, partial posterior ethmoidectomies, and a sellotomy (Fig. 2). During this module, we drill the anterior wall of the sella, exposing the superior and inferior intercavernous sinuses and the cavernous sinuses bilaterally. This relatively wide exposure, coupled with an incision of the dura, allows an unencumbered intrasellar dissection. The most common indications for this approach are pituitary adenomas, intrasellar craniopharyngiomas, and Rathke cleft cysts. The most important anatomical structures related to this module are the 4 blues, which comprise the superior and inferior intercavernous sinus rostrocaudally and the cavernous sinuses laterally. The transsellar approach may be combined with a transplanum and/or a transclival (upper third) approach to access extrasellar (intradural) disease.29
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Fig. 2. Transsellar approach. A and B: Coronal (A) and sagittal (B) contrast-enhanced MR images showing preoperative images of a hemorrhagic macroadenoma with suprasellar extension. C and D: Postoperative coronal (C) and sagittal (D) MR images demonstrating complete resection of the lesion and preservation of the pituitary gland at the right side of the sella.E: Intraoperative photograph obtained after resection of the lesion through an endoscopic endonasal transsellar approach. Note the diaphragmatic herniation toward the sphenoid sinus passing the level of the sellar dura.
Fig. 3. Transplanum approach. A and B: Preoperative, contrast-enhanced T1-weighted coronal (A) and sagittal (B) MR images of a tuberculum sellae meningioma. C and D: Corresponding postoperative coronal (C) and sagittal (D) MR images demonstrating complete resection of the lesion. The arrow in D indicates the reconstruction of the skull base with a vascularized enhanced nasoseptal flap. E: Intraoperative endoscopic view of the suprasellar region after complete extirpation of a tuberculum sellae meningioma, showing the optic chiasm, the pituitary stalk, the ICA on the right side, and the anterior communicating artery (Acom). The pituitary gland is shown in the sella protected by intact dura. The superior hypophysial arteries (SHa) were preserved and are seen bilaterally.
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Transplanum/Transtuberculum Approach. The working corridor for this module includes a posterior septectomy, wide bilateral sphenoidotomies, posterior ethmoidectomies, and removal of the planum sphenoidale with or without a sellotomy (Fig. 3). Therefore, this module is defined by the removal of the planum sphenoidale and tuberculum sellae. The optic canals mark the lateral limits, whereas the posterior ethmoidal arteries mark the anterior limit of the bony resection. Resection of the skull base anterior to these arteries risks injury to the olfactory fibers and epithelium. Lesions involving the posterior aspect of the anterior skull base (intra- or extradural) and the suprasellar region, such as meningiomas and extrasellar pituitary adenomas, are common indications for this approach. The contents of the suprasellar cistern, including the optic nerves/chiasm, ICAs, and the anterior cerebral arteries (A1 segment, artery of Huebner, anterior communicating artery, and perforating arteries), are important landmarks for this module. The most critical anatomical landmark in this module is the medial opticcarotid recess.29,31
frontal sinus anteriorly, and the posterior ethmoidal arteries posteriorly. A frontal sinusotomy allows a more direct access to the anterior aspect of most pathological entities in this location. In addition, it improves the access for resection and reconstruction. Pathological entities that require a transcribriform approach include meningiomas, esthesioneuroblastomas, and other sinonasal malignancies that invade the anterior skull base. A transcribriform approach is frequently combined with a transplanum approach to complete the resection of these lesions. A trans cribriform approach sacrifices olfaction; however, this is often a moot point as lesions in this area often produce anosmia. The most important structures related to this module are the anterior and posterior ethmoidal arteries, the medial orbits, and the contents of the interhemispheric fissure, that is, the anterior cerebral arteries (A2) and their branches (frontoorbital and frontopolar).29
Transclival Approach. The working corridor for this module is the posterior septectomy, bilateral removal of the rostrum and floor of the sphenoid sinuses, and a posterior and superior nasopharyngectomy (Fig. 5). This approach facilitates a partial (upper, middle, or lower third) or complete removal of the clivus (panclivectomy). The upper third is anatomically related to the dorsum sellae (median) and the posterior clinoids (paramedian). The latter can be removed intradurally via a transsellar approach, or extradurally via a subsellar corridor, both of which require a superior pituitary transposition.36 This transdorsal/posterior clinoid approach provides direct
Transcribriform Approach. The working corridor for this approach is an extended posterior septectomy, complete anterior and posterior ethmoidectomies, and a bilateral frontal sinusotomy (Draf III or endoscopic Lothrop sinusotomy) (Fig. 4). Removal of the cribriform plate defines this module. This module exposes the area between the posterior ethmoidal arteries and the crista galli. Its boundaries include the lamina papyracea laterally, the
Fig. 4. Transcribriform approach. A and B: Preoperative axial (A) and coronal (B) T1-weighted, contrast-enhanced MR images of an olfactory groove meningioma. C and D: Postoperative axial (C) and coronal (D) T1-weighted, contrast-enhanced MR images demonstrating complete resection of the lesion. The arrow in D indicates the skull base reconstruction using a vascularized nasoseptal flap. E: Intraoperative photograph of a transcribriform view during sharp dissection of the tumor (meningioma). The interface between the meningioma and the left frontal lobe is visible. The frontopolar artery (art.) is shown over the left gyrus rectus.
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Fig. 5. Transclival approach. A and B: Preoperative axial (A) and sagittal (B) contrast-enhanced, T1-weighted MR images showing a neurenteric cyst. Note the arrows indicating the neurenteric cyst delineated by the yellow dotted lines. C and D: Postoperative axial (C) and sagittal (D) contrast-enhanced, T1-weighted MR images demonstrating complete resection of the lesion. E: Intraoperative oblique, 45 endoscopic view of the prepontine cistern showing the brainstem at the level of the pons, CN V (V), CN VI (VI), and the complex of CNs VII and VIII (VII and VIII).
Transodontoid Approach. The working corridor for this module is similar to that of the lower clivus with a J Neurosurg / Volume 114 / June 2011
midline access to the cistern space behind the Liliequist membrane, specifically, the contents of the infundibular recess, third ventricle, and interpeduncular cistern. The middle clivus can be directly accessed at the posterior aspect of the sphenoid sinus. Its resection is limited laterally by the ascending paraclival ICAs, which are guarded anteriorly by the MPW. We define the MPW as the most medial projection of the base of the pterygoid plate as it meets the floor of sphenoid sinus.40 The lower third of the clivus, containing the foramen magnum, basion, and medial occipital condyles, is limited laterally by the parapharyngeal ICA that is guarded anteriorly by the eustachian tube. A panclivectomy extends from the dorsum sellae and posterior clinoids to the basion at the foramen magnum. The middle and lower clivectomies, respectively, provide access to the contents of the prepontine and premedullary cisterns. The most critical neurovascular structures therein are the brainstem, CNs IIXII, and the entire posterior circulation (BAs and VAs, superior cerebellar arteries, posterior cerebral arteries, and respective perforating vessels). Critical extradural landmarks include the MPW and eustachian tubes that mark the paraclival and parapharyngeal ICA segments and intradurally the vertebrobasilar junction that marks the origin of the abducens nerve. Commonly treated pathological conditions include chordomas, petroclival meningiomas, and craniopharyngiomas.
caudal extension of the nasopharyngectomy (Fig. 6). This module is defined by the removal of the odontoid process of the axis (second vertebra). The lower third of the clivus and anterior arch of C-1 are removed after dissection of the nasopharyngeal mucosa and the longus capitis muscles. The arch of C-1 is removed, and the odontoid process is exposed and drilled. This approach is used extradurally for resection of the odontoid process in patients with degenerative/inflammatory diseases or intradurally to expose the ventral medulla and cervicomedullary junction. In some specific cases, the clivus can be preserved and only the anterior arch of C-1 and odontoid process are removed. There is no need for manipulation or splitting of the soft palate since the entire dissection is performed above the Passavant ridge. The most important neurovascular landmarks for this module are contained in the premedullary and prepontine cisterns, that is, the caudal neurovascular structures discussed above and the anterior spinal arteries.30
Combined Median Approach. We coined the term combined median approach to apply in patients who required more than 1 module (to approach a complex lesion). Therefore, this term was used for analytical purposes when more than 1 midline module was required.
Modular Approaches in the Coronal Plane
Approaches in the coronal plane must be considered in 3 different depths as we advance from an anterior to posterior direction. The anterior coronal plane relates to the anterior fossa and orbits, the middle coronal plane
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Fig. 6. Transodontoid approach. A and B: Preoperative axial (A) and sagittal (B) CT angiograms showing a foramen magnum meningioma. C and D: Postoperative axial (C) and sagittal (D) CT angiograms demonstrating resection of the bone and lesion. E: Intraoperative view of the cervicomedullary junction during resection of a foramen magnum meningioma (Tu). The anterior spinal artery (ASa) is seen ventral to the spinal cord. The inferior rootlet of the hypoglossal nerve is seen on the left side (XII). Note the C-1 ventral root (C1) and the dentate ligament (DL). Bilateral VAs are identified (RVa and LVa).
Anterior Coronal Plane (Anterior Fossa). Tumors located in this plane are reached using a transorbital approach. This approach is defined by the removal of the lamina papyracea and the medial aspect of the optic nerve canals and can be extraconal or intraconal (Fig. 7). It requires anterior and posterior ethmoidectomies to expose the lateral wall of the nasal cavity. Sinonasal lesions that invade the medial wall of the orbit and intraconal lesions, such as schwannomas, hemangiomas, and meningiomas are common indications. Important anatomical structures related to this module include the optic nerves, the anterior and posterior ethmoidal arteries, and the ophthalmic artery with its branch. The optic nerves and ophthalmic artery with the central retina artery constitute the lateral limits; specifically, the ophthalmic artery and optic nerve cannot be mobilized and represent the lateral limit of the resection via EEA. Middle Coronal and Posterior Coronal Planes. The anatomy-based modules to access middle and posterior paramedian planes are defined by 7 zones based on the location of the lesion relative to the ICA. The vidian canals are key landmarks for all paramedian approaches, as the vidian nerve and vidian artery lead to the lacerum segment (petrous segment) of the ICA specifically marking the genu.40 All modules in the middle (Fig. 8) and posterior (Fig. 9) coronal planes with the exception of a Zone 1 module start with a transpterygoid approach using the maxillary
to the middle fossa and temporal lobe, and the posterior coronal plane to the posterior fossa.
sinus as the working corridor. Initially a maxillary antrostomy is performed, exposing the posterior wall of the maxillary sinus. The sphenopalatine and posterior nasal arteries are identified, and their branches are coagulated and ligated. The posterior wall of the maxillary sinus is removed, and the soft tissues of the sphenopalatine fossa are mobilized laterally. The vidian foramen and foramen rotundum are identified in the rostral sphenoid bone.40 The lateral sphenoid recess is opened, and the base of the sphenoid plates is drilled. This exposure allows direct access to the medial infratemporal fossa. Zone 1 corresponds to the petrous apex, and its approach is basically a lateral extension of a midclival approach.32 The working corridor for this target is the lateral recess of the sphenoid sinus. Cholesterol granulomas and chondrosarcomas are typical pathologies found at this location. The most relevant structures are the paraclival ICA and CN VI at the Dorello canal. Zone 2 corresponds to the petroclival junction.32 Its working corridor comprises the lateral sphenoid recess, medial maxilla, and the fossa of Rosenmller. The dura of the posterior fossa and its venous plexus is exposed after removing the overlying bone, which corresponds to that under the petrous ICA. Therefore, the middle cranial fossa represents the superolateral boundary. Chondrosarcomas are the most common pathology in this region. Anatomical structures related to this module are CNs VII and VIII laterally, the petrous ICA superiorly, and CN XII inferolaterally. Zone 3 is also known as the quadrangular space or the front door to Meckels Cave.32 The working corridor
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Fig. 7. Coronal plane, anterior fossa approach (transorbital). A and B: Preoperative axial noncontrast-enhanced (A) and coronal contrast-enhanced (B) T1-weighted MR images showing an expansive intraconal lesion in the right orbit (arrows) that proved to be a hemangioma. C and D: Postoperative axial noncontrast-enhanced (C) and coronal contrast-enhanced (D) T1-weighted MR images demonstrating total resection of the lesion. (The decompressed right optic nerve can be seen in C.) The yellow arrow indicates the enhancing nasoseptal flap that was used for reconstruction. E: Intraoperative view of the right orbit (RO) from a 45 endoscope, in which the sphenoid sinus (SS) is seen posteriorly. The window used for dissection was between the middle rectus muscle (MRM) and the inferior rectus muscle (IRM). The hemangioma (Tu) is visualized during resection.
Fig. 8. Coronal plane, middle fossa approach. A and B: Preoperative axial (A) and coronal (B) contrast-enhanced T1weighted MR images showing an expansive, homogeneously enhancing lesion in the right mesial temporal fossa, which proved to be a trigeminal schwannoma. C and D: Postoperative axial (C) and coronal (D) contrast-enhanced MR images demonstrating complete resection of the lesion through an endonasal route. The yellow arrow indicates the nasoseptal flap that was used for reconstruction. E: Intraoperative view of the Meckel cave (MC) after the trigeminal schwannoma was removed using a 0 endoscope. Note the preserved V1 branch of the trigeminal nerve preserved superiorly in the field at the level of the superior orbital fissure (SOF). The sella is seen posteriorly as well as the clival recess (CR). The right ICA was skeletonized and kept covered by the periosteum of the carotid canal.
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Fig. 9. Coronal plane, posterior fossa approach. A and B: Preoperative axial (A) and coronal (B) T1-weighted contrastenhanced MR images showing a right jugular foramen enhancing lesion, which proved to be a chondrosarcoma. Note the ICA is pushed laterally by the tumor, creating an endonasal corridor for resection (A). C and D: Postoperative axial (C) and coronal (D) contrast-enhanced MR images demonstrating complete resection of the lesion through an endonasal route. The yellow arrow indicates the nasoseptal flap that was used for reconstruction. E: Intraoperative endoscopic view after resection of a posterior fossa lesion using an EEA. Note the right internal auditory canal (IAC) with CNs VII and VIII. Inferiorly, the area of the jugular foramen (JF) is seen with CNs IX and X.
includes the removal of the medial maxilla and complete removal of the back wall of the antrum. This module is used to access lesions located in the anteromedial segment of the Meckel cave.35 This space is outlined by the petrous ICA inferiorly, the ascending paraclival ICA medially, CN VI superiorly in the cavernous sinus, and the maxillary division of the trigeminal nerve (V2) laterally. Pathologies commonly encountered in this region include invasive adenoid cystic carcinomas, meningiomas, schwannomas, and invasive pituitary adenomas. The important structures related to this module are those that comprise its boundaries discussed above. Zone 4 corresponds to the cavernous sinus, which is defined as the area lateral to the sella turcica, containing the cavernous ICA and CNs III, IV, and VI as well as the ophthalmic division of the trigeminal nerve.32 The working corridor is primarily the posterior ethmoids and sphenoid sinuses. We rarely use this approach, because its indication is limited to patients presenting with CN III, IV, and VI deficits such as those who have an apoplectic pituitary adenoma causing a cavernous sinus syndrome. Structures at risk for this approach are CNs III, IV, V, and VI, and the ICA with its sympathetic fibers. Zone 5 corresponds to the infratemporal fossa. Its corridor requires a medial maxillectomy-transmaxillary approach often expanded by an endoscopic Denker approach.32 The internal maxillary artery and its branches are systematically isolated and ligated within the ptery1554
gopalatine fossa. The dissection continues laterally to expose and often remove the lateral pterygoid plate until it is flush with the middle cranial fossa and foramen ovale. This requires control and mobilization of the structures of the pterygomaxillary fissure. The foramen rotundum and the lacerum segment of the ICA are identified medially. Pathologies encountered in this region include invasive carcinomas, schwannomas, and meningiomas. The relevant structures in this region are the internal maxillary artery, the ICA (pharyngeal and petrous segments), and the maxillary and mandibular nerves. Zone 6 is the region directly behind (posterior) the eustachian tube and medial to the parapharyngeal ICA. It contains the fossa of Rosenmller, occipital condyle, and hypoglossal canal. Its working corridor is the inferior portion of the medial maxilla and nasopharynx. The eustachian tube is an important landmark to safely determine the position ascending the parapharyngeal segment of the ICA. The medial aspect of the occipital condyle is lateral to the foramen magnum, and the hypoglossal canal is rostrolateral to the condyle (located at the 10 and 2 oclock positions).32,34 The critical structures in this module are the parapharyngeal ICA and CN XII. Zone 7 is the region posterior and lateral to Zone 6 and the parapharyngeal ICA. This area contains the jugular foramen and lateral mass of C-1. Its working corridor is the posterior and lateral maxillary sinus (use of endoscopic Denker approach) and lateral nasopharynx. The

jugular foramen and its contents (jugular vein and lower CNs IX, X, and XI) and CN XII as it exits the hypoglossal canal medially are the most relevant structures for this module.32 Common pathologies in this area include schwannomas, chordomas, and jugular foramen tumors. Zones 6 and 7 can be extended inferiorly to the level of the medial occipital condyles to the C-1 joint (O-1 joint). In our experience, the medial condyle can be drilled as long as the synovium of the O-1 joint is preserved and stability is maintained. We have used this approach for lesions that require proximal VA control such as aneurysms and foramen magnum meningiomas.32,34
TABLE 4: Age distribution among 800 patients who underwent EEAs Age Group (yrs) 35 >35 to 50 >50 to 62 >62 No. of Patients (%) 181 (22.6) 194 (24.2) 217 (27.1) 203 (25.3)
Combined Coronal Approach. All paramedian approaches share 1 major characteristic, their proximity to the ICA. In most paramedian approaches, multiple zones were required to control the lesion and adjacent neurovascular structures. Therefore, for the purpose of statistical analyses, we included them in a single group that we named combined coronal approach. However, these approaches were classified as a combined coronal approach only if the predominant location or epicenter of the pathology in question was paramedian. Statistical Analysis
Outcomes were examined for the weighted effects of age, level of complexity of the procedure, anatomy-based module, and year that the surgery was performed. The latter was included to assess the impact of incremental experience. Frequency distributions for age groups, surgical approaches, levels of complexity, and year of surgery were generated. Associations of outcomes with these variables were determined by chi-square exact tests with Yates correction. Logistic regression with stepwise selection was applied to identify factors that were significantly associated with various complications. Analyses were performed using SAS version 9.1 (SAS Institute). We established statistical significance as a p value < 0.05.
from our facility. Specifically, the CSF leaks in this cohort were not those that resulted from an EEA, but they represent traumatic and spontaneous cases referred to our institution for repair. A CSF leak was associated with an encephalocele in 23 (36.5%) of 63 patients. Primary sinonasal malignancies were grouped together, representing 8.5% of the cases. Metastases to the skull base were categorized separately (1.5%). Patients with benign sinonasal lesions that presented with destruction or invasion of the skull base, such as hemangiomas, osteomyelitis, fungus balls, mucoceles, and osteomas, were grouped together (4.0%). Angiofibromas (1.9%) and invasive inverted papillomas (0.9%) were categorized separately since they have unique characteristics. Optic nerve decompressions for traumatic neuropathy were grouped in the miscellaneous category. This category also included a diverse array of pathologies (AVM, granular cell tumor, enterogenous cyst, cholesteatoma, and others), each representing no more than 0.3% of the total.
Surgical Approaches
Table 6 summarizes the frequency of use of the different endonasal approaches to the skull base. Our most common approach was the transsellar module (41.9%) followed by the transcribriform one (16%). The collective group of paramedian approaches was the third most common module, encompassing 13.1% of the cases. Table 7 illustrates the distribution of the incremental surgical levels of complexity for our 800 procedures. Surgeries with a Level II complexity were most common (48.4%), followed by those with a Level IV complexity (22.3%). A total of 127 patients (15.9%) developed a postoperative CSF leak, our most common complication. Thirty patients (23.6%) were treated with a lumbar drain only early in the series. Fifty-three patients (41.7%) were treated endoscopically, and a lumbar drain was installed. Forty-four patients (34.6%) were treated with endoscopic repair only. Thus, endoscopic repair (with or without a lumbar drain) was performed in 97 patients (76.4%). The endoscopic endonasal reconstruction failed in only 1 patient; this patient had undergone prior concurrent radioand chemotherapy. Transient neurological deficits occurred in 20 patients (2.5%) and permanent neurological deficits in 14 patients (1.8%). There were 38 additional patients (4.8%)
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Results
Patient Population
Levels of Complexity
We identified 800 patients who underwent endonasal approaches to the skull base at the University of Pittsburgh Medical Center between July 1998 and July 2007. Three-hundred ninety-nine patients were male (49.9%) and 401 were female (50.1%). Their age distribution is shown in Table 4. Nine patients were counted twice and 2 patients were counted 3 times due to recurrent disease (beyond 6 months after the first procedure). The remaining 776 patients were considered only once. Table 5 provides a summary of pathological entities encountered during the study period. The most common benign pathologies were pituitary adenomas in 313 cases (39.1%), of which 34 (10.9%) required an expanded extrasellar approach for resection. Pituitary adenomas were followed by meningiomas (11.8%) and CSF leaks (7.9%). We did not include patients with a postoperative CSF leak
Complications
Pathological Entities
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TABLE 5: Pathology encountered in 800 patients who underwent EEAs Pathology pituitary adenoma meningioma malignant sinonasal lesion CSF leak benign sinonasal lesion RCC craniopharyngioma chordoma esthesioneuroblastoma angiofibroma metastasis chondrosarcoma fibrous dysplasia odontoid disease schwannoma cholesterol granuloma inverted papilloma lymphoma/plasma cell optic decompression dermoid/epidermoid arachnoid cyst glioma/glioblastoma multiforme hemangiopericytoma paraganglioma aneurysm germinoma miscellaneous total No. of Patients (%) 313 (39.1) 94 (11.8) 68 (8.5) 63 (7.9) 32 (4.0) 25 (3.1) 29 (3.6) 20 (2.5) 17 (2.1) 15 (1.9) 12 (1.5) 11 (1.4) 11 (1.4) 11 (1.4) 8 (1.0) 8 (1.0) 7 (0.9) 7 (0.9) 7 (0.9) 5 (0.6) 5 (0.6) 4 (0.5) 3 (0.4) 3 (0.4) 3 (0.4) 3 (0.4) 16 (2.0) 800 (100) TABLE 7: Distribution of 800 patients who underwent EEA regarding the level of complexity of the case Level II III IV V No. of Patients (%) 387 (48.4) 161 (20.1) 178 (22.3) 74 (9.3)
mortality (7 patients) was 2.6%. Tables 10 and 11 provide a summary of our complications; however, we will discuss each complication category separately.
Intraoperative Complications
who experienced a procedure-related complication, such as seizure, infection (for example, meningitis), or systemic complication (for example, pulmonary embolism) with no neurological sequelae. Seven patients died (0.9%); 6 died of systemic complications (for example, pulmonary embolism) and 1 of meningitis (Tables 8 and 9). Therefore, the overall permanent morbidity (14 patients) and
TABLE 6: Endonasal skull base approaches in 800 patients Approach transsellar transcribriform combined coronal transplanum transclival transorbital combined midline transodontoid total No. of Patients (%) 335 (41.9) 128 (16.0) 105 (13.1) 96 (12.0) 51 (6.4) 39 (4.9) 34 (4.3) 12 (1.5) 800 (100)
Vascular Injury. We encountered 7 major vascular complications (0.9%). One patient suffered an avulsion of a P1 perforator during the resection of a craniopharyngioma. This vessel was controlled using a topical hemostatic agent (Syvek NT patch, Marine Polymer Technologies; this is an off-label indication), but the patient suffered a severe transient dysphasia. Two patients suffered an ICA injury, and 1 suffered an avulsion of the ophthalmic artery. All 3 injuries were controlled intraoperatively before transferring the patients to the endovascular suite for additional control or sacrifice of the vessel. One of the ICA injuries and the ophthalmic artery injury were controlled with direct bipolar coagulation and soft-tissue welding with intraoperative vessel sacrifice. The second ICA injury was controlled by proximal and distal endonasal ICA clipping at the paraclival segment with intraoperative vessel sacrifice. None of these 4 patients developed a new permanent clinical deficit. Three patients developed postoperative permanent
TABLE 8: Intraoperative complications after expanded endonasal surgeries in 800 patients Category Consequence Type of Lesion &/or Deficit
These are defined as neurological complications that resulted directly from surgery and during surgery. Table 8 illustrates our intraoperative complications.
vascular injury death (0%) none (0.9%) transient deficit (0.1%) P1 perforator permanent deficit (0.4%) pontine bleed (quadri plegic), IMA laceration (hemiparesis), fronto polar avulsion (rt lower limb paresis) no deficit (0.4%) 1 ophthalmic (already blind), 2 ICA lacerations neural injury permanent deficit (0.5%) CNs IX, X, & XII (1 case), (1.8%) CNs IX & X (1 case), CN VI (2 cases) transient deficit (1.3%) CN III (2 cases), V3 motor (1 case), CN VI (3 cas es), hemiparesis (4 cases)
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TABLE 9: Postoperative complications after expanded endonasal surgeries in 800 patients* Category infection (1.9%) Consequence Type of Complication
death (0.1%) meningitis & status epilepticus (1 case) successfully treated (1.6%) intradural abscess (1 case), extradural abscess (1 case), meningitis (11 cases) deficit (0.1%) intradural abscessincapacitated (1 case) systemic (2.9%) death (0.7%) PE <30 days (2 cases), PE >30 days (2 cases), pneumonia & MI <30 days (1 case), multiorgan failure >30 days (1 case) successfully treated (2.1%) acute renal failure transfusion (1 case), respiratory failure (7 cases), PE <30 days (5 cases), MI (3 cases), immediate postop asystole (1 case) delayed deficit (1.9%) permanent deficit (0.6%) visual deficit (perfusion [2 cases]; late hypotension, hematoma [1 case each]); hemiplegia (postop apoplexy [1 case]); ataxia (OG tube passed clivectomy [1 case]) transient deficit (1.3%) visual deficit (encephalocele [1 case], hematoma [4 cases], nasal balloon [2 cases]); CN III (hematoma [1 case]); proptosis (retrobulbar hemato ma [1 case]) * MI = myocardial infarction; OG = orogastric; PE = pulmonary embolism. There were 5 patients who presented with seizures during the postoperative period with no sequelae.
neurological deficits (0.4%). One of these 3 patients suffered an avulsion of a frontopolar artery (A2) during the resection of an olfactory groove meningioma. The patient developed permanent right hemiparesis and cognition deficits after rupture of an A2 pseudoaneurysm, hematoma evacuation, and endovascular treatment. Another patient suffered a postoperative pontine hemorrhage after an episode of hypertension following the resection of a clival chordoma with brainstem involvement. This led to permanent quadriplegia. The third patient suffered an injury of the internal maxillary artery during the dissection of an infratemporal fossa encephalocele. Blood tracked up through the skull base defect, developing into an acute subdural hematoma that required multiple craniotomies. This patient developed a permanent weakness (4/5) of the left upper limb.
Neural Injury. Fourteen patients (1.8%) suffered a neurological injury, of which 4 (0.5%) were permanent and 6 (0.8%) were transient cranial neuropathies, and 4 (0.5%) were transient hemiparesis, as shown in Table 8.
Postoperative Complications
Table 9 illustrates our postoperative complications. Twenty-three patients (2.9%) suffered major postoperative systemic complications. Seventeen patients were successfully treated with no sequelae, and 6 died as a result of the complications (0.7%). Fifteen patients suffered intracranial infections with confirmed bacterial growth in cultures (1.9%). Thirteen of these patients were successfully treated and suffered no sequelae (11 bacterial meningitis, 1 intradural abscess, and 1 extradural abscess). Two of the 15 patients suffered sequelae: one patient died of meningitis and secondary status epilepticus, and the other developed a suprasellar abscess and became incapacitated from secondary stroke. Fifteen patients developed delayed postoperative deficits (1.9%), 6 (0.6%) of which were permanent. All these patients were examined after surgery and did not present with the deficit that was later encountered. Four patients had vision deterioration on a severe preoperative visual loss. The fifth patient developed permanent hemiparesis after an apoplectic event in the residual pituitary
TABLE 10: Analysis of complications in 800 patients who underwent EEA* Complication systemic infection vascular neural injury Frequency 23/800 (2.9%) 15/800 (1.9%) 7/800 (0.9%) 14/800 (1.8%) Relevant Factor age >60 yrs Level IV Level IV Level V combined coronal approach Levels IV & V Factor Impact 16/23 (69.6%) 12/23 (52.2%) 12/15 (80%) 4/7 (57.1%) 4/7 (57.1%) 11/14 (78.6%) OR (95% CI) 6.05 (2.4315.06) 4.59 (1.6912.44) 13.92 (3.0862.87) 22.06 (2.43200.27) IV: 5.24 (1.3420.51), V: 7.31 (1.6033.39) p Value <0.0001 0.01 <0.0001 0.001 0.0048 0.001
* There was no factor related to complications classified as delayed deficits. Compared with patients younger than 60 years of age. Compared with Level II.
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TABLE 11: Categorized complications after EEA in 800 patients in relation to the complexity level of the procedure No. of Patients (%) Level II (387 patients) III (161 patients) IV (178 patients) V (74 patients) total p value Vascular 1 (0.3) 0 2 (1.1) 4 (5.4)* 7 (0.9) 0.001* Neural Injury 3 (0.8) 0 7 (3.9)* 4 (5.4)* 14 (1.8) 0.001* Delayed Deficit 6 (1.6) 2 (1.2) 5 (2.8) 2 (2.7) 15 (1.9) 0.13 Systemic 6 (1.6) 4 (2.5) 12 (6.7)* 1 (1.4) 23 (2.9) 0.001* Infection 2 (0.5) 1 (0.6) 12 (6.7)* 0 15 (1.9) 0.004* Total 18 (4.7) 7 (4.3) 35 (19.7)* 11 (14.9)* 71 (9.3) <0.0001*
* Statistically significant. Three patients who underwent a Level IV procedure had more than 1 modality of complication. Five additional patients developed seizures during the postoperative period.
macroadenoma. The sixth patient with permanent deficit had a transclival resection of a foramen magnum meningioma and developed a postoperative CSF leak. During the preparation for the CSF leak repair, an enteral tube was inadvertently passed through the clival defect reaching the cerebellum, causing permanent mild ataxia. Seven additional patients suffered delayed visual deterioration that recovered once the causative agent was addressed. One patient had hydrocephalus treated by a ventriculoperitoneal shunt. Four patients developed a postoperative intrasellar hematoma and underwent reoperation. Two additional patients had a compressive effect of the nasal balloon packing, which was deflated. One child developed proptosis due to a retrobulbar hematoma after the resection of a juvenile nasopharyngeal angiofibroma. An immediate orbital decompression resolved the problem and avoided any permanent sequelae. Five patients (0.6%) suffered postoperative seizures.
Impact of Age
Twelve of 15 patients with infection had surgeries classified as Level IV, of which 1 led to a permanent sequela and 1 led to death. Compared with Level II procedures, Level IV procedures are 13.92 (OR 13.92, 95% CI 3.08 62.87) times more likely to have an infection complication. Levels IV and V procedures were also associated with more neural complications (11 patients [4.4%]), of which 2 (0.8%) proved to be permanent, than Levels II and III (3 patients [0.5%]) (p < 0.0001). Systemic complications were more commonly en
TABLE 12: Logistic regression to determine factors related to complications after EEAs in 800 patients* Logistic Regression Variable age 60 vs <60 yrs Level III IV V approach combined coronal combined midline transclival transcribriform transodontoid transorbital transplanum CSF leak OR (95% CI) 2.49 (1.444.30) 0.66 (0.152.87) 7.44 (2.1825.44) 3.32 (0.6816.31) 1.24 (0.265.82) 0.58 (0.122.84) 1.80 (0.427.70) 0.61 (0.172.20) 4.75 (0.5640.52) 1.98 (0.2814.26) 0.26 (0.061.11) 2.92 (1.595.35) p Value 0.001
Systemic complications occurred most commonly in patients older than 60 years of age (p < 0.0001). Only 2 systemic complications occurred in patients younger than 50 years of age (acute respiratory distress syndrome and aspirative pneumonia). All 6 deaths due to systemic complications occurred in patients older than 50 years of age (79, 96, 56, 87, 79, and 70 years old; Table 9). Table 11 provides a summary of the correlation between the complications and the procedures level of complexity. Patient age, surgical complexity (Level IV or Level V), and the development of a postoperative CSF leak were associated with a higher incidence of complications in general (Table 12). Four of 7 vascular complications occurred during procedures classified as Level V. Therefore, vascular complications occurred more often in Level V procedures than in any other level of complexity (p = 0.001). Of the 4 events, 1 led to a permanent deficit. Compared with Level II procedures, Level V procedures are 22.06 (OR 22.06, 95% CI 2.43200.27) times more likely to have a vascular complication. Level IV procedures were more frequently associated with infection than other procedures (p = 0.0001).
0.0001
Impact of Levels of Case Complexity
0.030 0.001
* This model selects variables that are significantly associated with any complication (71 patients). Variables considered in the model included sex, age, level, approach, and CSF leak. Among these variables, age, level, complication, and CSF leak are found to be associated with any complication. The model indicated that those who are older, have higher level of complexity, and have a CSF leak are more likely to have a complication. Also, when compared with the patients who underwent the transsellar approach, those who underwent the transplanum, trans cribriform, and combined midline approaches were less likely to have complications. Stepwise selection was used. Level II is used as the reference level. The transsellar approach is used as the reference approach.
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countered in patients undergoing Level IV surgeries (6.7%) than in those undergoing surgeries of other complexity levels (p = 0.01). Patient age and a Level IV complexity were independently associated with systemic complications (Table 12). Patients older than 60 years of age were 6.05 times more likely to have systemic complications, and surgeries with a Level IV complexity were 4.4 times more likely to be associated with a systemic complication compared with those with Levels II, III, or V surgery (Table 13). Thirty-nine of 178 patients who underwent a procedure with a Level IV complexity developed at least 1 complication. Nevertheless, 28 (71.8%) of these 39 patients underwent successful treatment of the condition with no sequelae. Four patients died after systemic or infectious complications (2.2%), and 7 patients (3.9%) suffered permanent deficits. Therefore, the combined mortality/morbidity rate for Level IV procedures was 6.1%. To have a better understanding of the complication risk associated with extrasellar expanded approaches, we analyzed our data excluding the Level II procedures. This analysis is provided in Table 14.
Impact of Type of Approach
Combined coronal approaches are associated with a vascular complication rate of 3.8% (4 of 105 cases). When compared with other approaches, the difference was statistically significant (p = 0.0048). The odds ratios for the risk of any complication for all approaches when compared with that of transsellar approaches are shown in Table 10.
Endoscopic endonasal surgery of the skull base is an emerging field and, consequently, there is a lack of published data addressing its associated complications.50 Although several studies have attempted to document complications, no study has systematically examined this issue in a large series. Admittedly, reviewing and comparing complication rates is difficult given the heterogeneity of the pathology treated, and, given this, we believe that a controlled comparison with conventional approaches is difficult. However, we do believe that it is important to report and discuss complications and to analyze them in the
TABLE 13: Logistic regression to determine factors related to systemic complications after EEAs in 800 patients* Logistic Regression Variable age 60 vs <60 yrs Level IV OR (95% CI) 6.05 (2.4315.06) 4.41 (1.8810.34) p Value 0.0001 0.0007
Discussion
context of the rates that have been reported for conventional approaches, while trying to take into consideration an equivalent level of complexity (Table 15). It is important to understand some key limitations of the study. Obviously the lack of controlled prospective data is foremost. Retrospective biases factor into all aspects of the study, from data collection to interpretation. We have made efforts to mitigate this influence, collecting data prospectively after the first 600 cases. For that reason, the study focused only on major complications, which were reliably encountered retrospectively. Thus, our study lacks data on minor complications such as sinusitis, nasal morbidity, and others, which would require an appropriate prospective study for analysis. As stated, another important limitation of this study is the heterogeneity of pathologies and surgical procedures. Specifically the grouping of heterogeneous data may dilute or concentrate the complication rates according to which pathologies constitute the predominant group. It may be argued that pituitary adenomas should be analyzed separately. While this may have some merit, subsets of pituitary tumors are invasive and expansive, increasing the complexity and consequent potential complications (Fig. 10). These are often managed using conventional skull base approaches. Similarly, when managing these tumors with significant extrasellar extension using EEA, we often need multiple modules. Thus, rather than excluding any specific lesion or site of origin, we have provided an additional analysis considering the pathologies as sellar and extrasellar cohorts. Other limitations are related to patient selection bias that occurred particularly in the beginning of the series. At that time, the surgeons were building the experience and naturally avoided performing complex endonasal skull base cases. Progressive skills and knowledge acquisition allowed the development of Levels IV and V of complexity, which occurred only later in the series, after 56 years of experience. We also have to remember that there is a possibility, although sporadic, that patients had a complication but preferred to go to a different center for care and were lost to follow-up and are therefore not considered in the database. The CSF leak rate after transsphenoidal surgery has been reported to vary from 2%18,55 to 13%59 in the literature. Pure endoscopic approaches to pituitary adenomas have shown equivalent results with rates of 2%4 to 3.5%.12 Reported rates of postoperative CSF leaks after conventional approaches to skull base pathology are significant. Deschler et al.13 and Feiz-Erfan et al.19 reported CSF leakage rates after open approaches to the anterior skull base of 13% and 29%, respectively. Sekhar et al.54 encountered a postoperative CSF leak in 20.3% of patients undergoing traditional skull base approaches for chordomas and chondrosarcomas. Our overall postoperative CSF leakage rate was 15.9%. However, several important considerations, which also affect the outcomes of conventional approaches, need to be discussed.13,19,54 Cerebrospinal fluid leakage rates were higher for extrasellar (19.4%) than for
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* The above model shows that age and level are independently associated with systemic complications (23 patients). Patients at least 60 years of age are 6.05 times more likely to have a systemic complication, and those with Level IV surgery are 4.41 times more likely to have a systemic complication compared with those with Level II, III, or V surgery. Levels II, III, and V are the reference levels.
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TABLE 14: Statistical analysis comparing extrasellar approaches (Levels IIIV) to the sellar approach (Level II) in relation to the likelihood of complications No. of Patients (%) Complication CSF leak no yes any complication no yes delayed* no yes infection no yes neurological no yes systemic no yes vascular no yes Level II 340 (87.86) 47 (12.14) 369 (95.35) 18 (4.65) 381 (98.45) 6 (1.55) 385 (99.48) 2 (0.52) 384 (99.22) 3 (0.78) 381 (98.45) 6 (1.55) 386 (99.74) 1 (0.26) Levels IIIV 333 (80.63) 80 (19.37) <0.0001 356 (86.2) 57 (13.8) 0.096 399 (96.61) 14 (3.39) 0.006 400 (96.85) 13 (3.15) 0.042 402 (97.34) 11 (2.66) 0.030 396 (95.88) 17 (4.12) 0.125 407 (98.55) 6 (1.45) 5.69 (0.6847.48) 2.73 (1.066.99) 3.50 (0.9712.65) 6.26 (1.4027.91) 2.23 (0.855.86) 3.28 (1.895.69) p Value 0.005 OR (95% CI) 1.74 (1.182.57)
* Five patients with seizures were included in this analysis as delayed complication.
Level II (12.1%) pathology, which includes the treatment for CSF leaks. When considering only the pituitary adenomas that required a transsellar approach for resection, the CSF leak rate was 10% (28 of 279). Endonasal repair of postoperative CSF leaks was effective for all but 1 patient in the entire series. This patient had received preoperative chemo- and radiotherapy for an advanced sinonasal undifferentiated carcinoma. Focal channels due to incomplete healing or migration of the free tissue grafts were a universal finding in patients with postoperative CSF leaks. Despite multiple techniques, we failed to decrease the postoperative CSF leaks to levels that we would consider satisfactory; therefore, we strived to develop reconstructive techniques that included the use of vascularized tissues. The nasoseptal mucosal flap provides a more robust layer of tissue and faster healing than any free tissue graft. Its use substantially reduced our overall postoperative CSF leakage rate (5.4%).25,38 Reconstruction using multilayer free tissue grafting still has a role; however, our data show that defects associated with EEAs are more reliably repaired using a pedicled vascularized flap. This is best demonstrated when analyzing the complications in our series of craniopharyngiomas where we found a CSF leakage rate of 58% prior to the adoption of the nasoseptal flap.23 This complication was reduced to 5.56% (1 of 18) once the flap was consistently used.52 High levels of CSF leaks were also seen in other series of expanded endonasal approaches for craniopharyngiomas before reconstruction with vascular1560
ized tissue. De Divitiis et al.10 had a 20% leakage rate and Frank et al.21 had a 30% CSF leakage rate after EEA for craniopharyngiomas. The same scenario was also seen after treatment of tuberculum sellae meningiomas with the expanded endoscopic technique by de Divitiis et al.,11 with a CSF leak rate of 33%. The nasal morbidity related to the nasoseptal flap elevation must be studied prospectively. However, it is our experience that once the flap covers the sphenoid sinus drilled bone, it does not generate deep crusting. On the other hand, the denuded septum can generate crusting for 3 months. At that point, a granulation tissue forms and the septum re-mucosalizes. Crusting of the anterior septum is easily cleaned during an otolaryngology office visit, whereas crusting of a deep sphenoid sinus, avoided by the flap, is usually not. Another significant aspect, which is frequently missed in the analyses, is the indirect morbidity of postoperative CSF leaks, or the incidence of secondary complications. These issues will be discussed in the next section.
Infectious Complications
Infectious complications such as meningitis and intracranial abscesses are well-recognized complications of skull base approaches. Postoperative meningitis occurs in 0.3%5.5% of patients undergoing microsurgical transsphenoidal surgery.18,55,59 Cappabianca et al.4 presented a rate of 0.7% of meningitis after pure endoscopic approaches for pituitary adenomas, a low rate that was

TABLE 15: Comparison of complications of multiple series divided according to the equivalent level of complexity* Authors & Year Laws, 1999 Fatemi et al., 2008 Feiz-Erfan et al., 2005 Sekhar et al., 2001 Cappabianca et al., 2002 Dehdashti et al., 2008 de Divitiis et al., 2007 Frank et al., 200622 present study Sudhakar et al., 2004 Semple & Laws, 1999 Fatemi et al., 2008 Deschler et al., 1996 Feiz-Erfan et al., 2005 Sekhar et al., 2001 Cappabianca et al., 2002 Dehdashti et al., 2008 Frank & Pasquini, 2002 de Divitiis et al., 2007 de Divitiis et al., 2008 present study Semple & Laws, 1999 Sudhakar et al., 2004 Fatemi et al., 2008 Feiz-Erfan et al., 2005 Sen & Triana, 2001 Cappabianca et al., 2002 Dehdashti et al., 2008 Frank et al., 200621 Frank et al., 200622 present study Ciric et al., 1997 Sudhakar et al., 2004 Barrow & Tindall, 1990 Fatemi et al., 2008 Fahlbusch & Schott, 2002 Pamir et al., 2005 Schick & Hassler, 2005 Sekhar et al., 2001 Frank et al., 200621 Frank et al., 200622 de Divitiis et al., 2007 de Divitiis et al., 2008 present study Approach TSR TSR craniotomy craniotomy EEA EEA EEA craniopharyngioma EEA chordoma, chondrosarcoma EEA TSR TSR TSR craniotomy craniotomy craniotomy EEA EEA EEA craniopharyngioma EEA craniopharyngioma EEA tuberculum sellae meningioma EEA TSR TSR TSR craniotomy craniotomy EEA EEA EEA craniopharyngioma EEA chordoma, chondrosarcoma EEA TSR TSR TSR TSR craniotomy craniotomy craniotomy craniotomy EEA craniopharyngioma EEA chordoma, chondrosarcoma EEA craniopharyngioma EEA tuberculum sellae meningioma EEA Level II Vascular Complications 0.58% 0.4% 0.68% 0% 0.3% CSF Leak 13% 1.9% 2% 2% 3.5% 10% (pituitary adenoma only), 12.4% Meningitis & Abscesses 0.8%2% 5.5% 0.3% 0.68% 1% 0.5% Neural Injury (transient & permanent) 0.6%2.6% 0.6%2.6% 0.6%2.6% 0.3% permanent 0.8% 9.1% 0% 13% 29% 0% 30% 20% 33% 19.37% 2% 30.7% 10% 0% 6.7% 2% permanent 10%29% 10%29% 10%29% 10% transient 0% 0% 33% transient 3.9% 10% 9% 1.1% 6% 2% 12%14% 5.4% 20.3% Level III Level IV Level V
0.6% 0%
17.2% 0% 33%41% 5.4% (continued)
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TABLE 15: Comparison of complications of multiple series divided according to the equivalent level of complexity (continued)* Authors & Year Laws, 1999 Sudhakar et al., 2004 Fatemi et al., 2008 Origitano et al., 2006 Frank et al., 200621 de Divitiis et al., 2007 de Divitiis et al., 2008 present study Fahlbusch et al., 1986 Sen & Triana, 2001 Hentschel et al., 2004 Dias et al., 1999 present study Approach TSR TSR TSR craniotomy EEA craniopharyngioma EEA craniopharyngioma EEA tuberculum sellae meningioma EEA TSR craniotomy craniotomy craniotomy EEA Level II Level III Level IV Level V
Delayed Deficits (transient & permanent) 0.14% 0.8% 0.7% 1% 7.4% 20% 10% 17%** 1.6% 1.2% 2.8% 2.7% Systemic Complications 6% (Cushing) 6.9% 11%32% (>70 yrs) 10% (>60 yrs) 1.6% 2.5% 6.7% 1.4% 6.7% (>60 yrs)
* TSR = transsphenoidal resection; = either the authors did not treat patients at the level stated, or the data were reported for more than 1 level as indicated. This rate applies to complications for all patients undergoing Level III and IV procedures. This rate applies to complications for all patients undergoing Level IIIV procedures. This rate applies to complications for all patients undergoing Level II and III procedures. Subdural hematoma. ** Intraventricular hematoma. This rate applies to complications for all patients undergoing Level IIV procedures.
recently reinforced by Gentilis series in the report by Deh dashti et al.,12 showing 1% of meningitis in 200 cases. Frank et al.21 encountered a rate of 10% of meningitis after EEA for craniopharyngiomas and none after EEA for chordomas and chondrosarcomas.22 Sen and Triana56 showed a 17.2% rate of major infectious complications, such as meningitis and intracranial abscesses, in patients who underwent traditional skull base surgery for the treatment of chordomas. Feiz-Erfan et al.19 encountered infectious complications, such as meningitis and intracranial abscesses, in 30.7% of patients undergoing a transbasal midline approach for either benign or malignant disease. In our series, we encountered a 1.8% incidence of bacterial meningitis or abscesses. Intracranial infection was most commonly associated with intradural surgeries (Level IV complexity), affecting 6.7% of patients who required such an approach. The incidence of intracranial infection in the subgroup with extrasellar pathology was 2.4%. One patient died of complications arising from Escherichia coli meningitis that evolved into status epilepticus. We encountered long-term sequelae related to infection in only 1 patient. In our experience, despite the initial high rate of CSF leakage (prior to the advent of the nasoseptal flap), the permanent morbidity associated with infectious complications proved to be relatively low at 0.25% (1 death and 1 sequela). However, it is not our intention to understate the impact of postoperative CSF leaks. Additional effects need to be considered, such as the impact of immobiliza1562
tion potentially affecting the rate of systemic complications (see Systemic Complications below), and effects of a second anesthesia and surgical repair.
Vascular Complications
Level II: Pituitary and CSF Leaks. Fatemi et al.18 reported 0.4% of CA injury during more than 700 cases of transsphenoidal surgery for pituitary adenomas. Laws44 reported 18 cases of major vascular injuries in 3061 patients (0.58%) who underwent transsphenoidal surgery for the resection of various intrasellar pathologies. Pituitary adenomas comprised 87% of his series; thus, these cases are comparable to our Level II cases. Cappabianca et al.4 had a rate of 0.68% of CA injury in pure endoscopic endonasal surgery for pituitary adenomas. Dehdashti et al.12 did not have a single case in 200 patients who underwent the same approach. Similarly, in our series, we did not encounter a single vascular injury during pituitary surgery (Level II). However, we did encounter a hemorrhage from an internal maxillary artery injury during repair of a spontaneous CSF leak related to a large infratemporal
Vascular injuries are the most feared complications in traditional skull base surgery because they represent a major cause of morbidity and mortality.41 One would anticipate their risk to be directly proportional to the level of complexity of the procedure and the underlying pathology. Therefore, we will discuss these based on our levels of surgical complexity and anatomical module.
Fig. 10. Contrast-enhanced MR images of a giant pituitary adenoma. A and B: Preoperative coronal (A) and sagittal (B) images. C and D: Postoperative coronal (C) and sagittal (D) images demonstrating an extensive resection of the tumor with preservation of the pituitary gland.
encephalocele. Therefore, our overall incidence of a vascular injury during Level II procedures was 0.3%. This occurred early in our experience and prior to the development of appropriate endoscopic bipolar coagulators. We believe that this resulted from the use of monopolar suction electrocautery along the perimeter of the encephalocele, injuring the internal maxillary artery. Subsequent to this event, we modified our technique to avoid the use of monopolar cauterization within any sinus for fear of heat dispersion and inadvertent injury.
Level III/IV: Extra-/Intradural Median Approaches. Fatemi et al.18 encountered a 2% rate of CA injury during extended transsphenoidal approaches. De Divitiis et al.10 had a 10% rate of vascular complication represented by a case of brainstem hemorrhage after EEA for craniopharyngiomas. Feiz-Erfan et al.19 reported a 9.1% rate of cerebrovascular injury associated with the resection of benign and malignant lesions of the anterior skull base using a transbasal approach. These cases are comparable J Neurosurg / Volume 114 / June 2011
to our Level III (extradural) and Level IV (intradural) procedures. Our incidence of vascular compromise in Level III and IV procedures was 0% and 1.1%, respectively. It is important to note that the hemorrhage accompanying these events was successfully controlled intraoperatively. Although the incidence of a vascular event during intradural surgery (Level IV) is relatively low (1.1%), the ability to manage this endoscopically at the time of surgery is critical and cannot be overemphasized. Furthermore, despite control of the bleeding, both of the vascular events associated with Level IV approaches resulted in neurological deficits; one was permanent (frontopolar artery compromise) and the other transient, albeit protracted (P1 perforator compromise). The P1 perforator avulsion occurred during the dissection of a retroinfundibular craniopharyngioma using a pure transplanum module. This was a milestone complication that spearheaded the genesis of the pituitary transposition technique.36 This technique facilitates sharp extracapsular dissection pro1563
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viding direct control of the posterior circulation.36 Based on this single event, we no longer use a transplanum module alone to access retrodorsal (dorsum sellae) lesions behind the membrane of Liliequist. We have modified our technique to include the transposition with a transdorsum sellae approach to deal with these lesions.36 carry a significant potential for permanent neurological compromise. Specifically, in this study, injury to small vessels proved to be of greater consequence to the patients. Based on this premise, we subdivided intradural Level IV surgery into IVa (cortical cuff of intervening brain separating the tumor from microcirculation) and IVb (absence of any protective cortical cuff with direct apposition of the cerebral vasculature to the tumor capsule) (Table 1). In summary, although we are appropriately concerned, we believe that the incidence or the need to manage vascular injuries is not an absolute contraindication for EEA (overall incidence of 0.9%). As with conventional cranial base surgery, the risk of vascular injury, and the ability to treat it effectively, are related to the experience of the operating team. A neurosurgeon who has cerebrovascular expertise is a valuable addition to the skull base surgery team and may be a critical component for the management of cases with complexity Levels IV and V. Regardless, the surgical team should acquire experience incrementally with surgeries of lower levels of complexity prior to undertaking procedures with complexity Levels IV and V. Our data demonstrate an increase in the incidence of vascular events that is directly proportional to the increase in the level of surgical complexity. Figure 11 demonstrates that we did not systematically pursue Levels IV (intradural) and V (paramedian) approaches until the 4th and 5th years of our endoscopic experience, respectively. Microscopic transsphenoidal surgery for tumors, equivalent to a procedure with a Level II complexity, such as that required for pituitary adenomas is associated with a rate of visual deterioration that varies from 0.3% to 2.6%.1,9,18,59 Visual deterioration in patients who undergo a transcranial resection of tuberculum sellae meningiomas, which are cases equivalent to EEA with a Level IV complexity, occur in 10%29%.17,49,51,53 Fatemi et al.18 had a 2% rate of new neurological deficits after extended transsphenoidal approaches. Sekhar et al.54 reported that 33% of the patients undergoing a traditional skull base procedure for resection of chordomas suffered a new CN deficit. Similarly, chondrosarcomas were associated with an incidence of new postoperative deficits of 41%. Frank et al.21 had 10% of transient neural deficit after EEA for craniopharyngiomas. On the other hand, Frank et al.22 did not have a single case of new neurological deficits after surgery for chordomas and chondrosarcomas. De Divitiis et al.10,11 encountered a 33% rate of transient neurological deficit after endoscopic endonasal surgery for tuberculum sellae meningiomas and no new deficit after performing the same approach for craniopharyngiomas. Our incidence of neural injury was 0.8% for Level II, none for Level III, 3.9% for Level IV, and 5.4% for Level V cases. The incidence of neural injury in the entire extrasellar subgroup was 2.4%. It should be noted that 11 patients (1.4% overall) suffered a delayed visual deficit after an early postoperative evaluation in which they demonstrated no new deficits. When only considering the extrasellar group, the rate was
J Neurosurg / Volume 114 / June 2011 Intraoperative Neural Injury
Level V: Paramedian/Coronal Plane. Conventional cranial base approaches for excising chordomas and chondrosarcomas are associated with an incidence of vascular complications of 12% and 14%, respectively.54 The risk of injuring a major vessel during traditional skull base surgery for recurrent disease is significantly higher, occurring in almost 1 (24%) of every 4 patients.54 These rates cannot be directly compared with those of endoscopic approaches, as heterogeneity and multiple other variables must be considered to create a comparable series. However, these cases are similar to those that we primarily classified as Level V (paramedian approaches). In our series, vascular complications occurred in 5.4% of Level V procedures. Frank et al.22 encountered a 9% rate of CA injury during expanded endoscopic endonasal procedures for resections of chordomas and chondrosarcomas of the skull base. Vascular injuries were more often associated with the treatment of paramedian lesions (lateral to the ICA), likely because of the need to dissect along the course of the ICAs. Specifically, vascular injuries were most commonly associated with the combined coronal approaches, which most commonly comprise procedures with levels of complexity that vary from Level III to Level V. When considering only injuries to the CA during a Level V procedure, our incidence was 2.7% (2 of 74 cases with complexity Level V). Our incidence of CA injury was 0 of 11 during chondrosarcoma surgery and 1 (5%) of 20 during chordoma surgery.58 It is important to emphasize that, despite their rarity, an appropriate concern in endoscopic skull base surgery has been the ability to effectively and endoscopically manage injuries to major vessels. This has been a fundamental factor when considering EEA as an option to manage these lesions, especially in paramedian and intradural locations. In our series, all cases of ICA injury were effectively controlled endoscopically and did not result in a new deficit. We believe that this may be partly a reflection of multiple factors, such as acquiring adequate endoscopic experience and skills before exposure to these events, preoperative planning, and a multidisciplinary team approach. We consider a balloon test occlusion of the ICA and external CA branch coiling for select patients who require a Level V approach, especially in the setting of previous radiation therapy or surgery. There were 3 additional injuries to major branches of the CA (internal maxillary artery, frontopolar artery, and ophthalmic artery), all of which were also effectively managed using a combination of endoscopic techniques and endovascular therapy. The first 2 of these resulted in a permanent deficit (discussed previously). Our data suggest that although large vessel injuries can lead to catastrophic bleeding, injuries of small vessels that are in direct contact with the brain or brainstem also 1564

ated with delayed complications in the literature. Frank et al.21 encountered a 20% rate of subdural hematomas, and de Divitiis et al.10 had the same complication in 10% of their cases. De Divitiis et al.11 encountered a 17% rate of postoperative intraventricular hemorrhage after EEA for tuberculum sellae meningiomas, which unfortunately was associated with death. Delayed complications occurred in 2.4% of our 800 patients. Interestingly, they did not correlate with any particular approach or surgical level of complexity. In our series, 0.8% (6 of 800) of patients suffered a permanent deficit from a delayed complication. When only the extrasellar group was considered, the incidence of delayed complication was 2.9%; 1.2% (5 of 413) of delayed complications were permanent. Of note, 4 of these patients with delayed deficits developed permanent visual loss. All of these patients presented with poor vision preoperatively, had stable vision checked immediately after surgery, and developed visual loss over the initial 48 hours thereafter. We suspect this was spasm of perforators in the setting of a severely ischemic optic apparatus. An additional important observation was that 2 patients whose medial optic canal had been drilled out developed visual deterioration 24 hours postoperatively. A Foley balloon had been used to buttress the reconstruction and its deflation resulted in recovery of vision. The case of hydrocephalus following resection of a large meningioma that was treated with ventriculoperitoneal shunting is another good example that these delayed complications are not unique to EEA. Although the rates compare favorably with those of conventional cranial surgery, we have learned critical lessons and have modified our technique accordingly. Patients presenting with severely compromised vision are now managed in the ICU postoperatively for a minimum of 72 hours, preserving their mean arterial pressure around 85 mm Hg. In addition, intracisternal papaverine is now often injected when we face a situation with a potential risk for vasospasm. There have been no such events since the adoption of these modifications. Balloon packing is avoided if the optic nerves have been exposed during the surgery (optic canal decompression). Deflation of the balloon is mandated when patients who have balloon packing develop any evidence of visual deterioration (or if the patient cannot be examined adequately). Systemic complications have been reported in association with transsphenoidal surgery for the resection of pituitary adenomas. Cushing disease is commonly associated with systemic complications.55 Fahlbusch et al.16 reported a 4% rate of deep venous thrombosis followed by pulmonary embolism and a 2% mortality related to postoperative pneumonia. Sen and Triana56 reported a systemic complication rate of 6.9% in patients who underwent skull base surgery for the treatment of chordomas. Hentschel et al.26 encountered a 32% rate of major systemic complications after standard skull base procedures in patients older than 70 years of age. Systemic complica1565 Systemic Complications
Fig. 11. Graph showing the distribution of expanded endoscopic endonasal skull base surgeries during the 1st 9 years of development at University of Pittsburgh Medical Center, divided into levels of complexity (IIV). Cases from 2007 were not included in this graph to avoid confusion since it is represented by a half year in this series. Note that we did not systematically pursue Level IV (intradural) and Level V (paramedian) approaches until the 4th and 5th years of our endoscopic experience, respectively.
2.4% (10 of 413). Only 4 (1%) of these patients had a permanent deficit. Data from these cases are listed in Table 9 and are discussed in Delayed Neurological Deficits (below). As expected, the incidence of neural injury correlated significantly with complexity Levels IV and V (3.9% and 5.4%, respectively). When examining these deficits, the incidence of a permanent deficit for Level IV and V procedures was 0.6% and 1.4%, respectively. The most common cranial neuropathy for Level IV and V procedures was a CN VI palsy, all cases of which were transient. These injuries were likely to occur during dissection near the Dorello canal. The 2 permanent CN VI palsies in the series developed during Level II procedures. Both occurred in acromegalic patients with tumor invading the cavernous sinus. These data suggest that the rates reported in this series (1% of permanent CN deficits) are at least comparable and may be favorable to those of conventional approaches.14,17,44,48,49,54,59 It should be noted, however, that there is an inherent selection bias because only cases suitable for a ventral corridor were considered for EEA, whereas in the previously reported literature all cases were included. Laws44 encountered 4 cases (0.14%) of postoperative hemorrhage in 3061 patients who underwent microscopic transsphenoidal surgery. Sudhakar et al.59 reported a personal rate of postoperative hematoma after transsphenoidal surgery of 0.8%. In addition, in a review of the literature, he found incidences of up to 3%.44 Fatemi et al.18 reported a 0.7% rate of postoperative hematomas after transsphenoidal surgery, which increased to 1% in cases of extended transsphenoidal procedures. Feiz-Erfan et al.19 reported a 2.3% rate of brain compression due to the use of a graft used for reconstruction after a transbasal approach for anterior skull base lesions. Origitano et al.48 reported a 7.4% incidence of delayed deficits caused by postoperative hematoma or by problems with the reconstructive flap after skull base surgery for malignancies. An EEA for craniopharyngiomas has been associJ Neurosurg / Volume 114 / June 2011 Delayed Neurological Deficits
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tions were significantly more frequent in the elderly than in the younger group (11%). Dias et al.14 reported a 10% rate of systemic complication when studying patients with a mean age of 60 years who were undergoing traditional skull base surgery. It is not possible to provide a meaningful comparison of systemic complications, as this would require collection of anesthesia risk scales and considerations of pathology and surgical complexity. However, as an overall perspective, in our series we encountered a rate of systemic complications of 2.9%. Similar to the previously discussed reports, these were associated with patient age. Patients older than 60 years were predisposed to systemic complications (p < 0.0001). The specific incidence of a systemic complication in a patient older than 60 years in our series was 6.7%. Of note, the highest rate of systemic complications in our series was associated with a Level IV procedure (6.7%). This is likely a consequence of higher rates of CSF leakage during the postoperative period in patients who underwent Level IV procedures, resulting in longer hospitalization and less patient mobilization than for those who underwent Level II, III, and V procedures. With the recent advent of the vascularized nasoseptal flap and the concomitant significant reduction in CSF leak, it will be important to observe if this rate is substantially reduced over time.38 Despite these factors, our rate of systemic complications after expanded endonasal approaches still compares favorably to conventional approaches. Dias et al.14 reported an overall complication rate of 48.6% in 104 patients who underwent a craniofacial resection for benign and malignant lesions. Feiz-Erfan et al.19 reported an overall complication rate of 59% in 44 patients who underwent a transbasal approach for benign and malignant lesions of the anterior skull base. Mortality associated with traditional approaches for the treatment of skull base malignancies varies from 2% to 7%. Most commonly, death is caused by vascular events or infectious complications, particularly meningitis.19,41 Our data compare favorably with those offered by these reports, as the overall rate of complications (transient or permanent), including intraoperative, postoperative, as well as systemic, was 9.5% (including the postoperative seizures). A 15.9% incidence of CSF leak was noted. However, when assessing the long-term impact of these complications, the incidence of permanent morbidity and mortality was 2.6% (permanent deficits 1.8% and death 0.9%).
Final Analysis Overall Morbidity and Mortality
sual loss, and 4.1% incidence of systemic complications. This yields an overall permanent morbidity of 2.2% (9 of 413) and mortality of 1.2% (5 of 413) (yielding a combined morbidity/mortality rate of 3.4%). We believe that these rates are favorable when compared with conventional approaches; however, they should be further improved with the evolution of vascularized reconstruction techniques. We further believe that the rate of postoperative CSF leakage will be substantially reduced beyond that demonstrated in this study. This is analogous to the evolution in open skull base surgery with the development of the pericranial flap. Our report covers a time span of 9 years; therefore, it reflects our progressive experience with the use of these approaches and the evolution of their technical nuances. Intuitively, one would expect a reduction in the overall complication rates over time. However, slight increments were noted, albeit not statistically significant (p = 0.2). This may be due to the fact that incremental experience leads to the management of cases with increasing levels of complexity. A trend is apparent toward the reduction of specific complications, such as that described for postoperative CSF leaks. The overall complication rates following EEA in appropriately selected cases seem to be very encouraging as reflected in the overall permanent morbidity and mortality rates of 1.8% and 0.9%, respectively (combined morbidity/mortality rate of 2.6%).
In summary, the incidence of complications in the entire cohort was as follows: 15.9% CSF leak (5.4% after the advent of the flap), 1.9% infectious complication, 0.9% vascular injury, 1.8% neural injury, 1.9% delayed neurological deficit, 0.5% permanent visual loss, and 2.9% incidence of systemic complications. When only considering extrasellar skull base pathology, the incidence of complications was as follows: 19.4% CSF leak, 3.2% infectious complication, 1.5% vascular injury, 2.7% neural injury, 3.4% of delayed neurological deficit, 1% permanent vi-
The 2 main sources of morbidity in skull base surgery are injury to the vasculature and/or the CNs. Complications associated with cerebrovasculature can be mitigated by a thorough understanding of the surgical relationships of the ICA, VAs, and the circle of Willis. In our opinion, cerebrovascular surgery forms the underpinning of all skull base surgery, be it conventional or endonasal. Accordingly, cerebrovascular surgery is an integral part of our training program and fellowship. Moreover, in our practice the same surgeons who perform EEA undertake our vascular procedures (aneurysms, AVMs, and so on). With respect to CN-related morbidity, we believe that it is related to the poor tolerance of these nerves to manipulation. Consequently, when selecting the appropriate corridor, be it lateral (conventional) or anterior (ventral) EEA, we try to maintain the general principle of not crossing the plane of CNs. Specifically, the nerves are kept at the perimeter of the lesion to avoid manipulation and secondary deficits. On occasion, this may require a multicorridor strategy combining lateral approaches with EEA. It is our perspective that if endoscopic skull base surgery (beyond the sella) is the goal, the skill sets and rhinology and pituitary training should be augmented and combined with those of conventional skull base surgery and cerebrovascular surgery to truly offer comprehensive care. As in other specialties, endoscopic techniques in skull base surgery represent progress. They allow us to potentially expand our surgical capabilities and minimize our patients morbidity. They are not, however, the solution to every surgical problem. Endoscopic approaches are not
Conclusions
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a substitute but a complement to traditional transcranial and microscopic approaches; therefore, it is critical that skull base surgeons be versed in all techniques to be able to offer the best alternative to their patients. Establishment of the longevity of the procedure will require a longer period of follow-up. Nevertheless, efficacy data are increasing in the literature, suggesting that expanded endonasal endoscopic approaches have become part of the skull base surgeons armamentarium. It should be recognized that the endoscope is a tool, and outcomes are determined by the judgment with which it is selected and the technique with which it is applied.
Disclosure Dr. Kassam is a paid consultant for Karl Storz Endoscopy and Stryker Navigation and holds equity stake in NICO Corp. Dr. Carrau is a paid consultant for Karl Storz Endoscopy and received an honorarium and travel expenses from that company to serve as faculty at a workshop in Europe. The following authors received travel expenses only from Karl Storz Endoscopy to serve as faculty at 1 or more workshops in Europe and/or the Middle East: Gardner, Prevedello. The following authors received travel expenses only from OmniGuide for a research and development meeting in the US: Gardner, Snyderman. Dr. Snyderman also received travel expenses only from Alcatel Lucent for a research and development meeting in the US. The authors have no personal financial or institutional interest in any of the drugs, materials, and devices described in this article. Author contributions to the study and manuscript preparation include the following. Conception and design: Kassam, Carrau, Hor o witz. Acquisition of data: Duz, Prevedello, Thomas, Zanation. Draft ing the article: Prevedello, Kassam. Critically revising the article: Kassam, Carrau, Stefko, Byers, Horowitz. Administrative/ technical/material support: Snyderman, Gardner. Study supervision: Prevedello, Kassam. Acknowledgment The authors thank Yue-Fang Chang for performing all the statistical analysis of the manuscript. References 1. Barrow DL, Tindall GT: Loss of vision after transsphenoidal surgery. Neurosurgery 27:6068, 1990 2. Bragg K, Vanbalen N, Cook N: Future trends in minimally invasive surgery. AORN J 82:10061014, 10161018, 2005 3. Cappabianca P, Alfieri A, de Divitiis E: Endoscopic endonasal transsphenoidal approach to the sella: towards functional endoscopic pituitary surgery (FEPS). Minim Invasive Neurosurg 41:6673, 1998 4. Cappabianca P, Cavallo LM, Colao A, de Divitiis E: Surgical complications associated with the endoscopic endonasal transsphenoidal approach for pituitary adenomas. 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J Neurosurg 109:35, 2008 53.Schick U, Hassler W: Surgical management of tuberculum sellae meningiomas: involvement of the optic canal and visual outcome. J Neurol Neurosurg Psychiatry 76:977983, 2005 54. Sekhar LN, Pranatartiharan R, Chanda A, Wright DC: Chordomas and chondrosarcomas of the skull base: results and complications of surgical management. Neurosurg Focus 10(3):E2, 2001 55. Semple PL, Laws ER Jr: Complications in a contemporary series of patients who underwent transsphenoidal surgery for Cushings disease. J Neurosurg 91:175179, 1999 56. Sen C, Triana A: Cranial chordomas: results of radical excision. Neurosurg Focus 10(3):E3, 2001 57. Solari D, Magro F, Cappabianca P, Cavallo LM, Samii A, Esposito F, et al: Anatomical study of the pterygopalatine fossa using an endoscopic endonasal approach: spatial relations and distances between surgical landmarks. J Neurosurg 106:157 163, 2007 58. Stippler M, Gardner PA, Snyderman CH, Carrau RL, Prevedello DM, Kassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:268278, 2009 59. Sudhakar N, Ray A, Vafidis JA: Complications after transsphenoidal surgery: our experience and a review of the literature. Br J Neurosurg 18:507512, 2004 Manuscript submitted March 13, 2009. Accepted October 13, 2010. Current affiliation for Dr. Kassam: University of Ottawa, On tario, Canada. Current affiliation for Dr. Prevedello: The Ohio State Uni versity, Columbus, Ohio. Current affiliation for Dr. Carrau: Institute at Saint Johns Hos pital, Santa Monica, California. Current affiliation for Dr. Thomas: Beth Israel Deaconness Med ical Center, Boston, Massachusetts. Current institution for Dr. Zanation: University of North Caro lina, Chapel Hill, North Carolina. Please include this information when citing this paper: published online December 17, 2010; DOI: 10.3171/2010.10.JNS09406. Address correspondence to: Daniel M. Prevedello, M.D., De partment of Neurological Surgery, The Ohio State University, N-1011 Doan Hall, 410 West 10th Avenue, Columbus, Ohio, 43210. email: daniel.prevedello@osumc.edu.
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See the corresponding editorial in this issue, pp 15411543.

J Neurosurg 114:15441568, 2011

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

ant & pst ethmoidal arte ries, falx, periorbita

middle 1/3 of clivus lower 1/3 of clivus transodontoid

Zone 1 (pe trous apex) Zone 2 (infrapetrous)

endonasal trans pterygoid, Denker endonasal transpterygoid

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

Modular Approaches in the Coronal Plane

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

Impact of Levels of Case Complexity

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

17.2% 0% 33%41% 5.4% (continued)

J Neurosurg / Volume 114 / June 2011

J Neurosurg / Volume 114 / June 2011

Complications in endoscopic endonasal approaches

Complications in endoscopic endonasal approaches

Complications in endoscopic endonasal approaches

J Neurosurg / Volume 114 / June 2011

J Neurosurg / Volume 114 / June 2011

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