Surgical outcomes using a medial-to-lateral endonasal endoscopic approach to pituitary adenomas invading the cavernous sinus

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Object

This study details the extent of resection and complications associated with endonasal endoscopic surgery for pituitary tumors invading the cavernous sinus (CS) using a moderately aggressive approach to maximize extent of resection through the medial CS wall while minimizing the risk of cranial neuropathy and blood loss. Tumor in the medial CS was aggressively pursued while tumor in the lateral CS was debulked in preparation for radiosurgery.

Methods

A prospective surgical database of consecutive endonasal pituitary surgeries with verified CS invasion on intraoperative visual inspection was reviewed. The extent of resection as a whole and within the CS was assessed by an independent neuroradiologist using pre- and postoperative Knosp-Steiner (KS) categorization and volumetrics of the respective MR images. The extent of resection and clinical outcomes were compared for medial (KS 1–2) and lateral (KS 3–4) lesions.

Results

Thirty-six consecutive patients with pituitary adenomas involving the CS who had surgery via an endonasal endoscopic approach were identified. The extent of resection was 84.6% for KS 1–2 and 66.6% for KS 3–4 (p = 0.04). The rate of gross-total resection was 53.8% for KS 1–2 and 8.7% for KS 3–4 (p = 0.0006). Six patients (16.7%) had preoperative cranial neuropathies, and all 6 had subjective improvement after surgery. Surgical complications included 2 transient postoperative cranial neuropathies (5.6%), 1 postoperative CSF leak (2.8%), 1 reoperation for mucocele (2.8%), and 1 infection (2.8%).

Conclusions

The endoscopic endonasal “medial-to-lateral” approach permits safe debulking of tumors in the medial and lateral CS. Although rates of gross-total resection are moderate, particularly in the lateral CS, the risk of permanent cranial neuropathy is extremely low and there is a high chance of improvement of preexisting deficits. This approach can also facilitate targeting for postoperative radiosurgery.

Abbreviations used in this paper:ACTH = adrenocorticotropic hormone; CCA = cavernous carotid artery; CN = cranial nerve; CS = cavernous sinus; DI = diabetes insipidus; KS = Knosp-Steiner.

Object

This study details the extent of resection and complications associated with endonasal endoscopic surgery for pituitary tumors invading the cavernous sinus (CS) using a moderately aggressive approach to maximize extent of resection through the medial CS wall while minimizing the risk of cranial neuropathy and blood loss. Tumor in the medial CS was aggressively pursued while tumor in the lateral CS was debulked in preparation for radiosurgery.

Methods

A prospective surgical database of consecutive endonasal pituitary surgeries with verified CS invasion on intraoperative visual inspection was reviewed. The extent of resection as a whole and within the CS was assessed by an independent neuroradiologist using pre- and postoperative Knosp-Steiner (KS) categorization and volumetrics of the respective MR images. The extent of resection and clinical outcomes were compared for medial (KS 1–2) and lateral (KS 3–4) lesions.

Results

Thirty-six consecutive patients with pituitary adenomas involving the CS who had surgery via an endonasal endoscopic approach were identified. The extent of resection was 84.6% for KS 1–2 and 66.6% for KS 3–4 (p = 0.04). The rate of gross-total resection was 53.8% for KS 1–2 and 8.7% for KS 3–4 (p = 0.0006). Six patients (16.7%) had preoperative cranial neuropathies, and all 6 had subjective improvement after surgery. Surgical complications included 2 transient postoperative cranial neuropathies (5.6%), 1 postoperative CSF leak (2.8%), 1 reoperation for mucocele (2.8%), and 1 infection (2.8%).

Conclusions

The endoscopic endonasal “medial-to-lateral” approach permits safe debulking of tumors in the medial and lateral CS. Although rates of gross-total resection are moderate, particularly in the lateral CS, the risk of permanent cranial neuropathy is extremely low and there is a high chance of improvement of preexisting deficits. This approach can also facilitate targeting for postoperative radiosurgery.

Lesions involving the cavernous sinus (CS) have proven to be surgically challenging due to the close proximity of critical neurovascular structures and the deep intracranial location. Visualization and dissection of the complex anatomy, including the carotid artery and its branches and numerous cranial nerves, is often hindered by robust blood flow in this space. Although technical advances have increased surgeons' ability to operate within the CS,30 the region remains treacherous even in the hands of experienced surgeons.11

Traditional approaches to the CS have focused on transcranial “lateral-to-medial” routes, where cranial nerves (CNs) III, IV, and VI in the lateral wall significantly obstruct the surgical corridors. Deep to these structures lie the abducens nerve, the carotid artery and its arterial branches to these intracavernous cranial nerves, the dorsal clivus, the tentorium, the pituitary gland, the trigeminal ganglion, and the foramen rotundum.31 While numerous surgical approaches have been described to limit damage to these structures,21,22,40 exposure and visualization, particularly of medially situated lesions, is limited.

Endonasal endoscopic approaches, on the other hand, offer a “medial-to-lateral” route, which places the cranial nerves on the far side of the surgical corridor. We consider this approach a safer corridor when applied to soft tumors that arise medially and push the neurovascular structures laterally, thereby forming a safe passage into the medial, and sometimes even the lateral, CS. Further safety is afforded by angled endoscopes that allow direct visualization of tumor debulking in this area. Since the contents of the lateral CS are further from radiosensitive structures such as the pituitary gland and optic nerves, radical debulking of the medial CS in preparation for radiosurgery is a reasonable surgical goal, assuming it can be achieved safely. Likewise, decompression of the lateral CS can relieve preexisting cranial neuropathies. In this study, we expand on prior studies that have discussed this technique by detailing our series utilizing an endoscopic endonasal “medial-to-lateral” route and evaluate the outcomes of this approach based on the Knosp-Steiner criteria.7,14,25,27,56

Methods

This study and the prospective database were approved for research by the Weill Cornell Medical College institutional review board. We reviewed all endoscopic endonasal pituitary surgeries done by T.H.S. and V.K.A. at Weill Cornell Medical College to identify patients with lesions involving the CS based on MRI. Cases were only included if, at the time of surgery, the surgeon directly visualized the tumor's breach of the medial wall of the CS and recorded that the dissection included this region. All pre- and postoperative images were retrospectively reviewed by an independent neuroradiologist (A.J.T.), who calculated the volume of the tumor, degree of CS invasion (based on the Knosp-Steiner [KS] criteria), and extent of both total resection and resection within each CS. The KS grading system includes 5 categories (Fig. 1):28 Grade 0, no invasion with all of the lesion medial to the cavernous carotid artery (CCA); Grade 1, invasion extending to, but not past, the medial aspect of the CCA; Grade 2, invasion extending to, but not past, the lateral aspect of the CCA; Grade 3, invasion past the lateral aspect of the CCA but not completely filling the CS; and Grade 4, tumor completely filling the CS both medial and lateral to the CCA. Only those cases with intraoperative confirmation of CS invasion were included in the study, regardless of the preoperative KS grade. Based on this grading scheme and the comparison between the pre- and postoperative MRI scans, the extent of resection was categorized by a neuroradiologist using volumetric software as 1) partial resection (< 50% volume removed from the CS), 2) subtotal resection (50%–80% volume removed from the CS), 3) near-total resection (80%–99% volume removed from the CS), and 4) gross-total resection (100% volume removed from the CS). For patients with bilateral involvement, each CS was graded separately with regard to degree of invasion and extent of resection.

Fig. 1.
Fig. 1.

Knosp-Steiner classification scheme: Grade 0, no invasion, the lesion does not reach the medial aspect of the CCA; Grade 1, invasion extending to, but not past, the intercarotid line; Grade 2, invasion extending to, but not past, the lateral aspect of the CCA; Grade 3, invasion past the lateral aspect of the CCA but not completely filling the CS; and Grade 4, completely filling the CS both medial and lateral to the CCA. Adapted with permission from Lippincott Williams and Wilkins/Wolters Kluwer Health: Neurosurgery. Knosp et al.: Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33(4):610–618, copyright 1993.

Endonasal endoscopic surgery was performed in a standard fashion as described in previous publications, using a 2-surgeon, binarial technique that enables microdissection with counter-traction.16 Electrophysiological monitoring was not routinely used. Of note, intrathecal fluorescein was used in every case to enable clear visualization of CSF leaks.41 Once a panoramic view of the sphenoid sinus was achieved, CS invasion was addressed in the following manner. First, the bone was removed over the anterior wall of the CS from within the sphenoid sinus using a Kerrison punch, and Doppler ultrasonography was used to identify the exact location of the carotid artery (Fig. 2). For tumors arising within the sella, the dura over the sella was opened as close to the carotid artery as safely possible, and an angled endoscope was used to follow the tumor through the medial wall of the CS behind the carotid siphon, using angled suctions and ring curettes (Fig. 3). All soft tumor tissue that could be easily removed without traumatic dissection was removed in this fashion under direct vision. Since the bone is removed over the anterior wall of the sinus, the carotid artery can be gently pushed laterally to increase visualization. Any breach in the medial CS wall was enlarged bluntly to facilitate further tumor removal. For tumors with a component that pushed the carotid artery medially, the dura was opened lateral to the carotid siphon to remove soft tumor with a ring curette. Lateral visualization was often obtained using a transpterygoid extension of the approach.18 Any firm tumor stuck to neurovascular structures (Fig. 4) was left in place to be addressed with postoperative radiosurgery or observation.

Fig. 2.
Fig. 2.

Exposure of the region of the CCA (A), removal of the overlying bone (B), and location confirmation using micro-Doppler ultrasonography (C). C = carotid artery; Cl = clivus; CS = cavernous sinus; S = sella.

Fig. 3.
Fig. 3.

Angled endoscopes are used to follow the tumor through the medial wall of the CS behind the carotid siphon using angled suction instruments (left) and ring curettes (right). MW = medial wall of CS; P = pituitary gland.

Fig. 4.
Fig. 4.

Preoperative (A) and postoperative (B) coronal Gd-enhanced T1-weighted MR images. The preoperative images demonstrate a large expansive lesion in the right CS. Following endonasal endoscopic surgery the majority of the tumor was removed. Any firm tumor stuck to neurovascular structures was left in place to be addressed with postoperative radiosurgery or observation as indicated by the pathology and the age of the patient. In this case, the small residual from this low-grade lesion was observed.

Clinical outcome and follow-up care were compared based on Knosp-Steiner grade. Cohort summary data were analyzed using mean ± SD, median (interquartile range), and number (%) where appropriate. Categorical data were compared using the chi-square or Fisher exact test where appropriate; parametric data were compared using the Student t-test, and nonparametric data were compared using the Wilcoxon rank-sum test.

Results

Review of a prospective surgical database of over 400 endonasal endoscopic cases identified 36 patients with pituitary tumors with extension into the CS verified on intraoperative visual inspection. The mean patient age was 47.3 years and 22 (61%) of the patients were female. The median duration of follow-up was 13 months (mean 15.5 months, range 1–49 months). The cohort data including presenting symptoms, lesion characteristics, and operative variables, are provided in Table 1.

TABLE 1:

Summary of clinical and demographic characteristics of 36 patients with 49 invasive CS pituitary adenoma lesions undergoing endonasal endoscopic surgery*

VariableValue
mean age in yrs47.3 ± 16.4
female22 (61)
presenting symptoms
 headache9 (25.0)
 vision8 (22.2)
 endocrine16 (44.4)
 cranial neuropathy6 (16.7)
lesion characteristics
 bilateral13 (36.1)
 nonsecretory16 (44.4)
 growth hormone–secreting10 (27.8)
 prolactinoma7 (19.4)
 ACTH-secreting3 (8.3)
 gonadotrophin-secreting2 (5.6)
operative variables
 reoperation3 (8.3)
 approach
  transsellar24 (66.7)
  transsellar transplanum9 (25.0)
  transellar transethmoidal3 (8.3)
 lumbar drain11 (30.6)
 nasoseptal flap18 (50.0)
duration of follow-up (mos)
 median13
 IQR9.5–16.5

Values represent numbers of cases (%) unless otherwise indicated. IQR = interquartile range.

There were 13 patients (36.1%) with bilateral CS involvement. Tumor characteristics included the following: 10 growth hormone–secreting tumors (27.8%), 7 prolactinomas (19.4%), 3 adrenocorticotropic hormone (ACTH)–secreting tumors (8.3%), and 2 gonadotrophin-secreting tumors (5.6%). Three patients had had a previous operation.

The surgical approach was transsellar in 24 cases (66.7%) and either transsellar transplanum or transsellar ethmoidal in 12 (33.3%). The approach to the anterolateral corridor into the CS, including incisions lateral to the carotid artery, was used in 23 cases. In these cases, the bone over the carotid protuberance along the posterior wall of the sphenoid sinus was completely removed to expose the dura lateral to the carotid artery. A vertical incision was then made parallel to the course of the carotid artery. A nasoseptal flap was used to create a multilayered closure of the skull base in 18 patients (50%), and a prophylactic lumbar drain was used in 11 (30.6%) of the cases. An intraoperative CSF leak was visualized in 19 patients (52.8%), aided by intrathecal fluorescein injection at the start of the procedure, as described above. There was only 1 postoperative CSF leak (2.8%), which occurred prior to our use of vascularized mucosal flaps; this leak was successfully managed with a lumbar drain, and the patient did not develop any signs or symptoms of meningitis.

Surgical outcomes are given in Table 2. Based on the preoperative imaging studies, 13 patients (36.1%) had lesions medial to the lateral aspect of the CCA (KS Grade 1–2) and 23 (63.9%) had lesions lateral to the CCA or completely filling the CS (KS Grade 3–4). In evaluating the degree of resection of tumor from within the CS, partial resection was reported in 2 patients (5.6%), subtotal resection in 21 (58.3%), near-total resection in 5 (13.9%), and gross-total resection in 8 (22.2%). Preoperative cranial neuropathies were seen in 6 patients (16.7%); 1 of these neuropathies was due to pituitary apoplexy. Subjective improvement occurred in all 6 cases (100%). New temporary postoperative cranial neuropathy (1 abducens nerve and 1 oculomotor nerve) occurred in 2 patients (5.6%), both of whom had tumor in the lateral CS. The neuropathies resolved after 1 and 3 months. Preoperative visual field defects were seen in 10 patients (27.8%). In 9 cases (90%) they improved postoperatively, and in 1 case (10%) there was no change. Preoperative endocrine defects were found in 15 patients (41.7%). Six of these patients (40.0%) had improvement after surgery, and 9 patients (60.0%) had no change. Of the 6 patients whose condition improved, the hormonal abnormalities were elevated growth hormone level (2), elevated ACTH level (2), elevated prolactin level (1), and decreased follicle-stimulating hormone/luteinizing hormone ratio (1).

TABLE 2:

Outcome data for patients undergoing expanded endonasal surgery for invasive pituitary adenomas

VariableNo. of Cases (%)
degree of invasion
 KS Grade 1–213 (36.1)
 KS Grade 3–423 (63.9)
extent of CS resection
 partial (<50%)2 (5.6)
 subtotal (50–80%)21 (58.3)
 near total (80–95%)5 (13.9)
 gross total (>95%)8 (22.2)
postop findings
 visual (n = 10)*
  no change1 (10.0)
  better9 (90.0)
 cranial neuropathy (n = 6)*
  no change0 (0)
  better6 (100)
 endocrine (n = 15)*
  no change9 (60.0)
  better6 (40.0)
follow-up
 radiation therapy11 (30.6)
 medical therapy10 (27.8)
 repeat surgery1 (2.8)
 recurrence2 (5.6)

n = number of patients with preoperative complaints.

There were differences in surgical outcomes between the Knosp-Steiner categories—KS 1–2 (medial CS invasion) and KS 3–4 (lateral CS invasion) (Table 3). The average degree of CS tumor resection (KS 1–2: 84.6% vs KS 3–4: 66.6%, p = 0.04) and percentage of cases with gross-total resection (KS 1–2: 53.8% vs KS 3–4: 8.7%, p = 0.0006) versus subtotal resection (KS 1–2: 15.4% vs KS 3–4: 82.6%, p < 0.0001) of the CS component of the tumor varied significantly by KS category. A significantly higher degree of resection was achieved using the endonasal endoscopic approaches for medial compared with lateral CS lesions. Eleven patients (30.6%) went on to be treated with radiation either in the setting of tumor recurrence or as adjuvant therapy based on the tumor pathology. The remaining patients were followed closely for tumor recurrence or growth of residual tumor. Postoperative radiation therapy was administered to 39.1% of patients with KS 3–4 tumors compared with less than 15.4% of patients with KS 1–2 tumors.

TABLE 3:

Lesion types and outcome data stratified by Knosp-Steiner grade*

VariableKnosp-Steiner Classificationp Value
Grade 1–2 (n = 13) Medial to CCAGrade 3–4 (n = 23) Lateral to CCA
extent of CS resection
 partial (<50%)1 (7.7%)1 (4.3%)0.67
 subtotal (50–80%)2 (15.4%)19 (82.6%)<0.01
 near total (80–95%)3 (23.1%)2 (8.7%)0.23
 gross total (>95%)7 (53.8%)1 (8.7%)<0.01
 average84.6%66.6%0.04
follow-up
 CSF leak0 (0%)0 (0%)NA
 radiation therapy2 (15.4%)9 (39.1%)0.14
 medical therapy2 (15.4%)8 (34.8%)0.21
 repeat surgery0 (0%)1 (4.3%)NA
 recurrence1 (7.7%)1 (4.3%)NA
postop findings
 visual
  no change0 (0.0%)1 (14.3%)0.46
  better3 (83.3%)6 (85.7%)0.84
 cranial neuropathy
  no change0 (0%)0 (0%)NA
  better2 (100%)4 (100%)NA
 endocrine
  no change0 (0.0%)9 (81.8%)<0.01
  better4 (100%)2 (18.2%)0.09

See Fig. 1 for description of Knosp-Steiner grades. Values represent numbers of cases unless otherwise indicated. Boldface type indicates statistical significance. NA = not applicable.

Includes only permanent endocrinopathies.

At the time of last follow-up (median duration 30.7 months), 1 (7.7%) of 13 patients with KS 1–2 lesions had new growth as demonstrated by MRI compared with 1 (4.3%) of 23 patients with KS 3–4 lesions. We divided complications into those that were attributable to CS surgery (for example, cranial neuropathy, infection) and those attributable to pituitary surgery (for example, hypopituitarism, diabetes insipidus [DI], CSF leak, mucocele). Cavernous sinus surgery resulted in an 8.4% transient morbidity (cranial neuropathy in 2 cases and infection in 1 case) and a 0% permanent morbidity rate. Pituitary surgery resulted in 19.2% transient morbidity rate from DI/hypopituitarism (5 cases), CSF leak (1 case), mucocele (1 case), and an 8.3% permanent morbidity rate from DI/hypopituitarism (1 case) and hypopituitarism without DI (2 cases).

Discussion

In this study, we explore the relative merits of a moderately aggressive “medial-to-lateral” approach to pituitary tumors invading the CS. Pituitary tumors arise in the midline and generally push the contents of the CS in a medial-to-lateral direction. For this reason, the carotid artery and cranial nerves are at the lateral aspect of the approach and require minimal manipulation during tumor removal. Notably, there were no carotid artery injuries, only 1 postoperative CSF leak, and 2 temporary cranial neuropathies, both in cases in which tumor was resected from the lateral CS and neither resulting in permanent deficits. As one might expect, we observed that the degree of tumor resection from within the CS varies significantly based on Knosp-Steiner grade, where medially positioned lesions could be more completely removed than laterally positioned tumors.

These results support our overall philosophy, namely that radical debulking of the medial CS can be safely achieved, whereas tumor in the lateral CS, although resectable, results in a higher risk when pursued aggressively, and a strategy of limited debulking may provide a safer and equally effective alternative. This philosophy has been molded by the existence of the stereotactic radiosurgical options available in the current era. Endoscope-assisted surgery has become widely practiced during the last decade. Using certain approaches, visualization during endoscope-assisted surgery can be superior to microsurgery, as the endoscope permits improved visualization from a larger field of view achieved at the end of a narrow corridor since the lens and light source are close to the target. This provides excellent resolution of anatomical and pathological details, particularly with the advent of 3D endoscopes.15,39,43 Moreover, the use of angled endoscopes and instruments enables the surgeon to visualize and remove structures around corners and avoid retraction. Disadvantages can include narrow working spaces causing reduced degrees of freedom with the dissecting instruments and proximity of the lens to debris and blood, mandating frequent scope cleaning. As this technology has evolved, surgeons have explored the use of endonasal endoscopic approaches to remove lesions extending into the CS, particularly using the 2-surgeon, binarial technique, which affords increased precision and safety. This deep, anatomically complex region offers unique challenges, depending on the degree of invasion, consistency of the tumor, and angle of surgical approach.

Numerous anatomical studies have detailed the relevant surgical anatomy for these approaches from both a transcranial and a transnasal perspective. Transcranial studies often describe various corridors between the cranial nerves lying within the lateral wall of the CS. In one of the first landmark studies, Parkinson described surgical corridors to the CCA and detailed the anatomical triangle between CN IV and CN VI, and the tentorium that now carries his name.40 Since then, other groups have advanced these concepts providing anatomical and technical nuances to aid in removing lesions from this area.2,21,22,30–32,46,47,55 Jho and Ha were some of the first to describe transnasal approaches to the CS; they included the paraseptal, middle meatal, and middle turbinectomy corridors and detailed the relationships of key structures to the carotid siphon.23 Numerous other groups have since illustrated the surgical anatomy and techniques important for successful endoscope-assisted access to the CS.3,4,8,17,18,24,25

In the original publication by Knosp and Steiner in 1993 outlining the grading system for lesions invading the CS, they suggested that “the critical area where invasion of the cavernous sinus space becomes very likely and can be proven surgically is located between the intercarotid line and the lateral tangent, which is represented by [the] Grade 2.”28 For this reason, we categorized our cases into Grade 1–2 and Grade 3–4 lesion for the purposes of this study. Our findings corroborate this key anatomical interface at the lateral aspect of the cavernous carotid segments in determining the expected degree of resection and potential recurrence rate for a given lesion. In a later study by Frank and Pasquini, the endonasal endoscopic approach was used to treat 65 patients with pituitary adenomas invading the CS.14 The authors reported gross-total resection in 60% for nonfunctional tumors and hormone remission in 67% of functional tumors. Complications included 3 CSF leaks (5%), 2 patients with pituitary insufficiency (3%), and 1 patient requiring craniotomy for hematoma evacuation. However, the authors did not differentiate these cases based on the relative degree of CS invasion. More recently, Ceylan and colleagues reported on their series of 20 patients undergoing endonasal surgery for pituitary adenomas invading the CS and included Knosp-Steiner designations; in this series, 98% of the tumors were KS Grade 3–4. Gross-total resection was achieved in 65% of cases and subtotal resection in 35%.7 Fifteen (75%) of the tumors were secretory, and hormone remission occurred in 10 (67%) of these 15 cases. Reported complications included DI in 3 cases (15%) and CSF leak in 3 (15%). Although our rates of resection are lower, our complication rates are also lower, indicating that perhaps a more conservative approach, particularly with respect to lateral CS invasion, may reduce complications. Operative time and complications, particularly CSF leaks, are major considerations for these cases. Of note, our low CSF leak rate in this series is the result of a systemic effort to create a multilayer closure construct, which begins with the planning of the bony opening and continues with nasoseptal flap harvesting at the beginning of the surgical procedure in patients with larger (> 2.5 cm) tumors.

Comparisons of the outcomes and complication rates between the transnasal and transcranial approaches are difficult as it is not possible to gauge the important contributions of patient selection bias and surgeon familiarity with these challenging techniques. However, the major publications include varying pathologies and report a 60%–80% degree of resection, transient morbidity in 20%–80% of patients, permanent morbidity in 5%–15%, and recurrence in 10%–25% following transcranial approaches (Table 4). In this series we stratify patients based on CS invasion and offer such radical resection rates only when the medial CS is involved and the tumor can be removed safely. Hence, our extent of resection rate is lower than in other series, as are our morbidity rates, too. Morbidity rates for tumors only positioned within the medial CS are even lower.

TABLE 4:

Summary of studies exploring treatments for invasive CS: transcranial surgery, stereotactic radiosurgery, and endonasal surgery*

Authors & YearNo. of PtsTreatmentPathologyLocationTumor Control/EOR% Morbidity (trans/perm)% RecurrenceMean Follow-Up (mos)
van Lindert et al., 199153TCPACS68% GTR22/63676
Cusimano et al., 1995124TCmixedCS66% GTR80/151029
Dolenc, 1997210TCPACS77% GTR25/10NRNR
Eisenberg et al., 199940TCmixedCS83% GTR35/101548
Kuo et al., 2004139SRSmixedCS41% decr6/2742
Kim et al., 200667SRSPACS72% decr0/2433
Frank & Pasquini, 200665TNPACS60% GTR6/3NR51
Kitano et al., 200836TNPACS72% GTR40/5640
Zhao et al., 2010126TNPACS62% GTR11/6NRNR
Ceylan et al., 201020TNPACS65% GTR30/5NRNR
present study36TNPACS20% GTR8.4/0313

Decr = decrease; EOR = extent of resection; GTR = gross-total resection; NR = not reported; PA = pituitary adenoma; perm = permanent; pts = patients; SRS = stereotactic radiosurgery; TC = transcranial surgery; TN = transnasal surgery; trans = transient.

Gross-total resection rates are based on the total tumor volume. Percentage of decrease rates are based on the CS-specific component of the tumor.

This number includes only morbidity related to surgery in the CS.

While there are no studies directly comparing the clinical outcomes of the transcranial microsurgical approach to the CS with the endonasal endoscopic technique, direct comparisons of the relevant surgical anatomy have been more common, in particular detailing the relative courses of the cavernous cranial nerves.6,19,20 Ultimately, tumors that invade into the medial CS (medial to the lateral carotid tangent) can be approached endonasally with acceptably low morbidity and reasonably high degrees of resection, particularly if the tumor arises in the midline, likely has a soft consistency, and invades in a medial-to-lateral trajectory, pushing the CS contents laterally. Tumors that extend into the lateral CS can be removed at least partially through a medial-to-lateral route, particularly if they are soft. Firmer tumors primarily in the lateral CS, in particular meningiomas, may require a lateral, transcranial approach to achieve a greater degree of resection to effectively decompress neurovascular structures and create space for adjuvant radiation treatment. Consideration of less invasive treatments such as stereotactic radiosurgery or fractionated radiotherapy should be strongly considered depending on the therapeutic goals and the overall treatment plan.

Radiation Therapy

The utility of radiosurgery for lesions in the CS should be carefully considered prior to discussing the goals of surgery: biopsy versus lesion debulking versus gross-total resection. Numerous studies have explored the role of conventional fractionated radiation and stereotactic radiosurgery in the treatment of benign and malignant CS lesions. Rates of tumor control vary from 50% to 100% and rates of tumor reduction from 30% to 70%, depending on the lesion size and histopathology.5,26,29,33–35,37,42,45,48,49 Important in evaluating these studies, the tumor growth rates prior to treatment should be closely considered when determining the tumor control (often set as no new growth) rates following radiation-based therapies. For secretory pituitary adenomas, hormone remission rates have been suggested to be upwards of 40%–50% regardless of the type.26,36,38,44,50,51,53 In addition, the risk of transient and permanent procedure-associated morbidity ranges from 0% to 25% and from 0% to 6%, respectively.26,33,34,42,48 Radiation injury to the optic apparatus and the pituitary gland are particular concerns—with rates reported to be as high as 6% and 35%, respectively.1,50 To enable the use of higher radiation doses and limit this damage, pituitary transposition has been suggested as a useful and effective technique.9,52 The decision to aggressively debulk the medical CS offers an additional measure, like pituitary transposition, to render postoperative radiosurgery safer and increase the radiobiological margin for critical structures.

In this study, we aimed to identify some of the limitations and considerations in designing treatment strategies for patients with pituitary tumors involving the CS. This retrospective analysis provides useful insight into the use of endonasal endoscopic techniques for a medial-to-lateral approach to these lesions. However, our findings cannot account for treatment and patient-selection biases that may play a role in the outcomes reported here. Furthermore, this study does not address the efficacy of our approach for the long-term control of these lesions due to the relatively short follow-up. To limit the interpretation bias associated with the Knosp-Steiner and resection grading, we used an independent, outcome-blinded neuroradiologist to evaluate the pre- and postoperative imaging. Overall, we feel this study offers useful information to guide the clinical decision making for these patients.

Conclusions

The endoscopic endonasal approach provides a useful and safe medial-to-lateral approach to the CS. Radical debulking of the medial CS can be performed safely and may create a suitable distance between radiosensitive structures and the residual tumor. In certain situations, the lateral CS can be debulked as well, but with slightly higher risk to the cranial nerves. One must carefully weigh surgical goals with the risks of surgery and the availability of adjuvant treatment options.

Disclosure

This investigation was supported by grant UL1RR024996 of the Clinical and Translational Science Center at Weill Cornell Medical College (K.S.P.). This grant is funded through the National Institutes of Health and therefore its publication must comply with the NIH Public Access Policy.

Author contributions to the study and manuscript preparation include the following. Conception and design: Schwartz, Woodworth, Burkhardt, Anand. Acquisition of data: Woodworth, Patel, Shin, Tsiouris, McCoul, Anand. Analysis and interpretation of data: Schwartz, Woodworth, Patel, Shin, Burkhardt, Tsiouris, McCoul. Drafting the article: Woodworth, Patel. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Schwartz. Statistical analysis: Schwartz, Woodworth, Patel, Shin, Tsiouris, McCoul. Administrative/technical/material support: Schwartz, Burkhardt, Tsiouris, McCoul, Anand. Study supervision: Schwartz, Anand.

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    • Export Citation
  • 6

    Cavallo LMCappabianca PGalzio RIaconetta Gde Divitiis ETschabitscher M: Endoscopic transnasal approach to the cavernous sinus versus transcranial route: anatomic study. Neurosurgery 56:2 Suppl3793892005

    • Search Google Scholar
    • Export Citation
  • 7

    Ceylan SKoc KAnik I: Endoscopic endonasal transsphenoidal approach for pituitary adenomas invading the cavernous sinus. Clinical article. J Neurosurg 112:991072010

    • Search Google Scholar
    • Export Citation
  • 8

    Ciporen JNMoe KSRamanathan DLopez SLedesma ERostomily R: Multiportal endoscopic approaches to the central skull base: a cadaveric study. World Neurosurg 73:7057122010

    • Search Google Scholar
    • Export Citation
  • 9

    Couldwell WTRosenow JMRovit RLBenzil DL: Hypophysopexy technique for radiosurgical treatment of cavernous sinus pituitary adenoma. Pituitary 5:1691732002

    • Search Google Scholar
    • Export Citation
  • 10

    Cusimano MDSekhar LNSen CNPomonis SWright DCBiglan AW: The results of surgery for benign tumors of the cavernous sinus. Neurosurgery 37:1101995

    • Search Google Scholar
    • Export Citation
  • 11

    DeMonte FSmith HKal-Mefty O: Outcome of aggressive removal of cavernous sinus meningiomas. J Neurosurg 81:2452511994

  • 12

    Dolenc VV: Transcranial epidural approach to pituitary tumors extending beyond the sella. Neurosurgery 41:5425521997

  • 13

    Eisenberg MBAl-Mefty ODeMonte FBurson GT: Benign nonmeningeal tumors of the cavernous sinus. Neurosurgery 44:9499551999

  • 14

    Frank GPasquini E: Endoscopic endonasal cavernous sinus surgery, with special reference to pituitary adenomas. Front Horm Res 34:64822006

    • Search Google Scholar
    • Export Citation
  • 15

    Fraser JFAllen BAnand VKSchwartz TH: Three-dimensional neurostereoendoscopy: subjective and objective comparison to 2D. Minim Invasive Neurosurg 52:25312009

    • Search Google Scholar
    • Export Citation
  • 16

    Fraser JFMass AYBrown SAnand VKSchwartz TH: Transnasal endoscopic resection of a cavernous sinus hemangioma: technical note and review of the literature. Skull Base 18:3093152008

    • Search Google Scholar
    • Export Citation
  • 17

    Higgins TSCourtemanche CKarakla DStrasnick BSingh RVKoen JL: Analysis of transnasal endoscopic versus transseptal microscopic approach for excision of pituitary tumors. Am J Rhinol 22:6496522008

    • Search Google Scholar
    • Export Citation
  • 18

    Hofstetter CPSingh AAnand VKKacker ASchwartz TH: The endoscopic, endonasal, transmaxillary transpterygoid approach to the pterygopalatine fossa, infratemporal fossa, petrous apex, and the Meckel cave. Clinical article. J Neurosurg 113:9679742010

    • Search Google Scholar
    • Export Citation
  • 19

    Iaconetta Gde Notaris MCavallo LMBenet AEnseñat JSamii M: The oculomotor nerve: microanatomical and endoscopic study. Neurosurgery 66:5936012010

    • Search Google Scholar
    • Export Citation
  • 20

    Iaconetta GFusco MCavallo LMCappabianca PSamii MTschabitscher M: The abducens nerve: microanatomic and endoscopic study. Neurosurgery 61:3 Suppl7142007

    • Search Google Scholar
    • Export Citation
  • 21

    Isolan Gde Oliveira EMattos JP: Microsurgical anatomy of the arterial compartment of the cavernous sinus: analysis of 24 cavernous sinus. Arq Neuropsiquiatr 63:2592642005

    • Search Google Scholar
    • Export Citation
  • 22

    Isolan GRKrayenbühl Nde Oliveira EAl-Mefty O: Microsurgical anatomy of the cavernous sinus: measurements of the triangles in and around it. Skull Base 17:3573672007

    • Search Google Scholar
    • Export Citation
  • 23

    Jho HDHa HG: Endoscopic endonasal skull base surgery: Part 2—The cavernous sinus. Minim Invasive Neurosurg 47:9152004

  • 24

    Kassam ABGardner PSnyderman CMintz ACarrau R: Expanded endonasal approach: fully endoscopic, completely transnasal approach to the middle third of the clivus, petrous bone, middle cranial fossa, and infratemporal fossa. Neurosurg Focus 19:1E62005

    • Search Google Scholar
    • Export Citation
  • 25

    Kassam ABPrevedello DMCarrau RLSnyderman CHGardner POsawa S: The front door to Meckel's cave: an anteromedial corridor via expanded endoscopic endonasal approach—technical considerations and clinical series. Neurosurgery 64:3 Supplons71ons832009

    • Search Google Scholar
    • Export Citation
  • 26

    Kim MPaeng SPyo SJeong YLee SJung Y: Gamma Knife surgery for invasive pituitary macroadenoma. J Neurosurg 105:Suppl26302006

    • Search Google Scholar
    • Export Citation
  • 27

    Kitano MTaneda MShimono TNakao Y: Extended transsphenoidal approach for surgical management of pituitary adenomas invading the cavernous sinus. J Neurosurg 108:26362008

    • Search Google Scholar
    • Export Citation
  • 28

    Knosp ESteiner EKitz KMatula C: Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33:6106181993

    • Search Google Scholar
    • Export Citation
  • 29

    Kobayashi TKida YMori Y: Long-term results of stereotactic gamma radiosurgery of meningiomas. Surg Neurol 55:3253312001

  • 30

    Krayenbühl NHafez AHernesniemi JAKrisht AF: Taming the cavernous sinus: technique of hemostasis using fibrin glue. Neurosurgery 61:3 SupplE522007

    • Search Google Scholar
    • Export Citation
  • 31

    Krisht ABarnett DWBarrow DLBonner G: The blood supply of the intracavernous cranial nerves: an anatomic study. Neurosurgery 34:2752791994

    • Search Google Scholar
    • Export Citation
  • 32

    Krisht AF: Transcavernous approach to diseases of the anterior upper third of the posterior fossa. Neurosurg Focus 19:2E22005

  • 33

    Kuo JSChen JCYu CZelman VGiannotta SLPetrovich Z: Gamma knife radiosurgery for benign cavernous sinus tumors: quantitative analysis of treatment outcomes. Neurosurgery 54:138513942004

    • Search Google Scholar
    • Export Citation
  • 34

    Lee JYNiranjan AMcInerney JKondziolka DFlickinger JCLunsford LD: Stereotactic radiosurgery providing long-term tumor control of cavernous sinus meningiomas. J Neurosurg 97:65722002

    • Search Google Scholar
    • Export Citation
  • 35

    Litré CFColin PNoudel RPeruzzi PBazin ASherpereel B: Fractionated stereotactic radiotherapy treatment of cavernous sinus meningiomas: a study of 100 cases. Int J Radiat Oncol Biol Phys 74:101210172009

    • Search Google Scholar
    • Export Citation
  • 36

    Losa MPicozzi PRedaelli MGLaurenzi AMortini P: Pituitary radiotherapy for Cushing's disease. Neuroendocrinology 92:Suppl 11071102010

    • Search Google Scholar
    • Export Citation
  • 37

    Milker-Zabel SZabel-du Bois AHuber PSchlegel WDebus J: Fractionated stereotactic radiation therapy in the management of benign cavernous sinus meningiomas: long-term experience and review of the literature. Strahlenther Onkol 182:6356402006

    • Search Google Scholar
    • Export Citation
  • 38

    Minniti GGilbert DCBrada M: Modern techniques for pituitary radiotherapy. Rev Endocr Metab Disord 10:1351442009

  • 39

    Moral AIKunkel METingelhoff KRilk MWagner IEichhorn KG: 3D endoscopic approach for endonasal sinus surgery. Conf Proc IEEE Eng Med Biol Soc 2007:468346862007

    • Search Google Scholar
    • Export Citation
  • 40

    Parkinson D: A surgical approach to the cavernous portion of the carotid artery. Anatomical studies and case report. J Neurosurg 23:4744831965

    • Search Google Scholar
    • Export Citation
  • 41

    Placantonakis DGTabaee AAnand VKHiltzik DSchwartz TH: Safety of low-dose intrathecal fluorescein in endoscopic cranial base surgery. Neurosurgery 61:3 Suppl1611662007

    • Search Google Scholar
    • Export Citation
  • 42

    Roche PHRégis JDufour HFournier HDDelsanti CPellet W: Gamma knife radiosurgery in the management of cavernous sinus meningiomas. J Neurosurg 93:Suppl 368732000

    • Search Google Scholar
    • Export Citation
  • 43

    Roth JFraser JFSingh ABernardo AAnand VKSchwartz TH: Surgical approaches to the orbital apex: comparison of endoscopic endonasal and transcranial approaches using a novel 3D endoscope. Orbit 30:43482011

    • Search Google Scholar
    • Export Citation
  • 44

    Rowland NCAghi MK: Radiation treatment strategies for acromegaly. Neurosurg Focus 29:4E122010

  • 45

    Selch MTAhn ELaskari ALee SPAgazaryan NSolberg TD: Stereotactic radiotherapy for treatment of cavernous sinus meningiomas. Int J Radiat Oncol Biol Phys 59:1011112004

    • Search Google Scholar
    • Export Citation
  • 46

    Seoane ERhoton AL Jrde Oliveira E: Microsurgical anatomy of the dural collar (carotid collar) and rings around the clinoid segment of the internal carotid artery. Neurosurgery 42:8698861998

    • Search Google Scholar
    • Export Citation
  • 47

    Seoane ETedeschi Hde Oliveira EWen HTRhoton AL Jr: The pretemporal transcavernous approach to the interpeduncular and prepontine cisterns: microsurgical anatomy and technique application. Neurosurgery 46:8918992000

    • Search Google Scholar
    • Export Citation
  • 48

    Shin MKurita HSasaki TKawamoto STago MKawahara N: Analysis of treatment outcome after stereotactic radiosurgery for cavernous sinus meningiomas. J Neurosurg 95:4354392001

    • Search Google Scholar
    • Export Citation
  • 49

    Shin MKurita HSasaki TTago MMorita AUeki K: Stereotactic radiosurgery for pituitary adenoma invading the cavernous sinus. J Neurosurg 93:Suppl 3252000

    • Search Google Scholar
    • Export Citation
  • 50

    Snead FEAmdur RJMorris CGMendenhall WM: Long-term outcomes of radiotherapy for pituitary adenomas. Int J Radiat Oncol Biol Phys 71:9949982008

    • Search Google Scholar
    • Export Citation
  • 51

    Stapleton CJLiu CYWeiss MH: The role of stereotactic radiosurgery in the multimodal management of growth hormone-secreting pituitary adenomas. Neurosurg Focus 29:4E112010

    • Search Google Scholar
    • Export Citation
  • 52

    Taussky PKalra RCoppens JMohebali JJensen RCouldwell WT: Endocrinological outcome after pituitary transposition (hypophysopexy) and adjuvant radiotherapy for tumors involving the cavernous sinus. Clinical article. J Neurosurg 115:55622011

    • Search Google Scholar
    • Export Citation
  • 53

    Tinnel BAHenderson MAWitt TCFakiris AJWorth RMDes Rosiers PM: Endocrine response after gamma knife-based stereotactic radiosurgery for secretory pituitary adenoma. Stereotact Funct Neurosurg 86:2922962008

    • Search Google Scholar
    • Export Citation
  • 54

    van Lindert EJGrotenhuis JAMeijer E: Results of follow-up after removal of non-functioning pituitary adenomas by transcranial surgery. Br J Neurosurg 5:1291331991

    • Search Google Scholar
    • Export Citation
  • 55

    Yasuda ACampero AMartins CRhoton AL Jrde Oliveira ERibas GC: Microsurgical anatomy and approaches to the cavernous sinus. Neurosurgery 56:1 Suppl4272005

    • Search Google Scholar
    • Export Citation
  • 56

    Zhao BWei YKLi GLLi YNYao YKang J: Extended transsphenoidal approach for pituitary adenomas invading the anterior cranial base, cavernous sinus, and clivus: a single-center experience with 126 consecutive cases. Clinical article. J Neurosurg 112:1081172010

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

Address correspondence to: Theodore H. Schwartz, M.D., Departments of Neurological Surgery, Otolaryngology, Neurology and Neuroscience, Brain and Spine Center, Weill Cornell Medical College, NewYork-Presbyterian Hospital, 525 E. 68th St., Box #99, New York, NY 10065. email: schwarh@med.cornell.edu.

Please include this information when citing this paper: published online February 14, 2014; DOI: 10.3171/2014.1.JNS131228.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Knosp-Steiner classification scheme: Grade 0, no invasion, the lesion does not reach the medial aspect of the CCA; Grade 1, invasion extending to, but not past, the intercarotid line; Grade 2, invasion extending to, but not past, the lateral aspect of the CCA; Grade 3, invasion past the lateral aspect of the CCA but not completely filling the CS; and Grade 4, completely filling the CS both medial and lateral to the CCA. Adapted with permission from Lippincott Williams and Wilkins/Wolters Kluwer Health: Neurosurgery. Knosp et al.: Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33(4):610–618, copyright 1993.

  • View in gallery

    Exposure of the region of the CCA (A), removal of the overlying bone (B), and location confirmation using micro-Doppler ultrasonography (C). C = carotid artery; Cl = clivus; CS = cavernous sinus; S = sella.

  • View in gallery

    Angled endoscopes are used to follow the tumor through the medial wall of the CS behind the carotid siphon using angled suction instruments (left) and ring curettes (right). MW = medial wall of CS; P = pituitary gland.

  • View in gallery

    Preoperative (A) and postoperative (B) coronal Gd-enhanced T1-weighted MR images. The preoperative images demonstrate a large expansive lesion in the right CS. Following endonasal endoscopic surgery the majority of the tumor was removed. Any firm tumor stuck to neurovascular structures was left in place to be addressed with postoperative radiosurgery or observation as indicated by the pathology and the age of the patient. In this case, the small residual from this low-grade lesion was observed.

References

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    Arbolay OLGonzález JGGonzález RHGálvez YH: Extended endoscopic endonasal approach to the skull base. Minim Invasive Neurosurg 52:1141182009

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    • Export Citation
  • 5

    Brell MVillà STeixidor PLucas AFerrán EMarín S: Fractionated stereotactic radiotherapy in the treatment of exclusive cavernous sinus meningioma: functional outcome, local control, and tolerance. Surg Neurol 65:28342006

    • Search Google Scholar
    • Export Citation
  • 6

    Cavallo LMCappabianca PGalzio RIaconetta Gde Divitiis ETschabitscher M: Endoscopic transnasal approach to the cavernous sinus versus transcranial route: anatomic study. Neurosurgery 56:2 Suppl3793892005

    • Search Google Scholar
    • Export Citation
  • 7

    Ceylan SKoc KAnik I: Endoscopic endonasal transsphenoidal approach for pituitary adenomas invading the cavernous sinus. Clinical article. J Neurosurg 112:991072010

    • Search Google Scholar
    • Export Citation
  • 8

    Ciporen JNMoe KSRamanathan DLopez SLedesma ERostomily R: Multiportal endoscopic approaches to the central skull base: a cadaveric study. World Neurosurg 73:7057122010

    • Search Google Scholar
    • Export Citation
  • 9

    Couldwell WTRosenow JMRovit RLBenzil DL: Hypophysopexy technique for radiosurgical treatment of cavernous sinus pituitary adenoma. Pituitary 5:1691732002

    • Search Google Scholar
    • Export Citation
  • 10

    Cusimano MDSekhar LNSen CNPomonis SWright DCBiglan AW: The results of surgery for benign tumors of the cavernous sinus. Neurosurgery 37:1101995

    • Search Google Scholar
    • Export Citation
  • 11

    DeMonte FSmith HKal-Mefty O: Outcome of aggressive removal of cavernous sinus meningiomas. J Neurosurg 81:2452511994

  • 12

    Dolenc VV: Transcranial epidural approach to pituitary tumors extending beyond the sella. Neurosurgery 41:5425521997

  • 13

    Eisenberg MBAl-Mefty ODeMonte FBurson GT: Benign nonmeningeal tumors of the cavernous sinus. Neurosurgery 44:9499551999

  • 14

    Frank GPasquini E: Endoscopic endonasal cavernous sinus surgery, with special reference to pituitary adenomas. Front Horm Res 34:64822006

    • Search Google Scholar
    • Export Citation
  • 15

    Fraser JFAllen BAnand VKSchwartz TH: Three-dimensional neurostereoendoscopy: subjective and objective comparison to 2D. Minim Invasive Neurosurg 52:25312009

    • Search Google Scholar
    • Export Citation
  • 16

    Fraser JFMass AYBrown SAnand VKSchwartz TH: Transnasal endoscopic resection of a cavernous sinus hemangioma: technical note and review of the literature. Skull Base 18:3093152008

    • Search Google Scholar
    • Export Citation
  • 17

    Higgins TSCourtemanche CKarakla DStrasnick BSingh RVKoen JL: Analysis of transnasal endoscopic versus transseptal microscopic approach for excision of pituitary tumors. Am J Rhinol 22:6496522008

    • Search Google Scholar
    • Export Citation
  • 18

    Hofstetter CPSingh AAnand VKKacker ASchwartz TH: The endoscopic, endonasal, transmaxillary transpterygoid approach to the pterygopalatine fossa, infratemporal fossa, petrous apex, and the Meckel cave. Clinical article. J Neurosurg 113:9679742010

    • Search Google Scholar
    • Export Citation
  • 19

    Iaconetta Gde Notaris MCavallo LMBenet AEnseñat JSamii M: The oculomotor nerve: microanatomical and endoscopic study. Neurosurgery 66:5936012010

    • Search Google Scholar
    • Export Citation
  • 20

    Iaconetta GFusco MCavallo LMCappabianca PSamii MTschabitscher M: The abducens nerve: microanatomic and endoscopic study. Neurosurgery 61:3 Suppl7142007

    • Search Google Scholar
    • Export Citation
  • 21

    Isolan Gde Oliveira EMattos JP: Microsurgical anatomy of the arterial compartment of the cavernous sinus: analysis of 24 cavernous sinus. Arq Neuropsiquiatr 63:2592642005

    • Search Google Scholar
    • Export Citation
  • 22

    Isolan GRKrayenbühl Nde Oliveira EAl-Mefty O: Microsurgical anatomy of the cavernous sinus: measurements of the triangles in and around it. Skull Base 17:3573672007

    • Search Google Scholar
    • Export Citation
  • 23

    Jho HDHa HG: Endoscopic endonasal skull base surgery: Part 2—The cavernous sinus. Minim Invasive Neurosurg 47:9152004

  • 24

    Kassam ABGardner PSnyderman CMintz ACarrau R: Expanded endonasal approach: fully endoscopic, completely transnasal approach to the middle third of the clivus, petrous bone, middle cranial fossa, and infratemporal fossa. Neurosurg Focus 19:1E62005

    • Search Google Scholar
    • Export Citation
  • 25

    Kassam ABPrevedello DMCarrau RLSnyderman CHGardner POsawa S: The front door to Meckel's cave: an anteromedial corridor via expanded endoscopic endonasal approach—technical considerations and clinical series. Neurosurgery 64:3 Supplons71ons832009

    • Search Google Scholar
    • Export Citation
  • 26

    Kim MPaeng SPyo SJeong YLee SJung Y: Gamma Knife surgery for invasive pituitary macroadenoma. J Neurosurg 105:Suppl26302006

    • Search Google Scholar
    • Export Citation
  • 27

    Kitano MTaneda MShimono TNakao Y: Extended transsphenoidal approach for surgical management of pituitary adenomas invading the cavernous sinus. J Neurosurg 108:26362008

    • Search Google Scholar
    • Export Citation
  • 28

    Knosp ESteiner EKitz KMatula C: Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33:6106181993

    • Search Google Scholar
    • Export Citation
  • 29

    Kobayashi TKida YMori Y: Long-term results of stereotactic gamma radiosurgery of meningiomas. Surg Neurol 55:3253312001

  • 30

    Krayenbühl NHafez AHernesniemi JAKrisht AF: Taming the cavernous sinus: technique of hemostasis using fibrin glue. Neurosurgery 61:3 SupplE522007

    • Search Google Scholar
    • Export Citation
  • 31

    Krisht ABarnett DWBarrow DLBonner G: The blood supply of the intracavernous cranial nerves: an anatomic study. Neurosurgery 34:2752791994

    • Search Google Scholar
    • Export Citation
  • 32

    Krisht AF: Transcavernous approach to diseases of the anterior upper third of the posterior fossa. Neurosurg Focus 19:2E22005

  • 33

    Kuo JSChen JCYu CZelman VGiannotta SLPetrovich Z: Gamma knife radiosurgery for benign cavernous sinus tumors: quantitative analysis of treatment outcomes. Neurosurgery 54:138513942004

    • Search Google Scholar
    • Export Citation
  • 34

    Lee JYNiranjan AMcInerney JKondziolka DFlickinger JCLunsford LD: Stereotactic radiosurgery providing long-term tumor control of cavernous sinus meningiomas. J Neurosurg 97:65722002

    • Search Google Scholar
    • Export Citation
  • 35

    Litré CFColin PNoudel RPeruzzi PBazin ASherpereel B: Fractionated stereotactic radiotherapy treatment of cavernous sinus meningiomas: a study of 100 cases. Int J Radiat Oncol Biol Phys 74:101210172009

    • Search Google Scholar
    • Export Citation
  • 36

    Losa MPicozzi PRedaelli MGLaurenzi AMortini P: Pituitary radiotherapy for Cushing's disease. Neuroendocrinology 92:Suppl 11071102010

    • Search Google Scholar
    • Export Citation
  • 37

    Milker-Zabel SZabel-du Bois AHuber PSchlegel WDebus J: Fractionated stereotactic radiation therapy in the management of benign cavernous sinus meningiomas: long-term experience and review of the literature. Strahlenther Onkol 182:6356402006

    • Search Google Scholar
    • Export Citation
  • 38

    Minniti GGilbert DCBrada M: Modern techniques for pituitary radiotherapy. Rev Endocr Metab Disord 10:1351442009

  • 39

    Moral AIKunkel METingelhoff KRilk MWagner IEichhorn KG: 3D endoscopic approach for endonasal sinus surgery. Conf Proc IEEE Eng Med Biol Soc 2007:468346862007

    • Search Google Scholar
    • Export Citation
  • 40

    Parkinson D: A surgical approach to the cavernous portion of the carotid artery. Anatomical studies and case report. J Neurosurg 23:4744831965

    • Search Google Scholar
    • Export Citation
  • 41

    Placantonakis DGTabaee AAnand VKHiltzik DSchwartz TH: Safety of low-dose intrathecal fluorescein in endoscopic cranial base surgery. Neurosurgery 61:3 Suppl1611662007

    • Search Google Scholar
    • Export Citation
  • 42

    Roche PHRégis JDufour HFournier HDDelsanti CPellet W: Gamma knife radiosurgery in the management of cavernous sinus meningiomas. J Neurosurg 93:Suppl 368732000

    • Search Google Scholar
    • Export Citation
  • 43

    Roth JFraser JFSingh ABernardo AAnand VKSchwartz TH: Surgical approaches to the orbital apex: comparison of endoscopic endonasal and transcranial approaches using a novel 3D endoscope. Orbit 30:43482011

    • Search Google Scholar
    • Export Citation
  • 44

    Rowland NCAghi MK: Radiation treatment strategies for acromegaly. Neurosurg Focus 29:4E122010

  • 45

    Selch MTAhn ELaskari ALee SPAgazaryan NSolberg TD: Stereotactic radiotherapy for treatment of cavernous sinus meningiomas. Int J Radiat Oncol Biol Phys 59:1011112004

    • Search Google Scholar
    • Export Citation
  • 46

    Seoane ERhoton AL Jrde Oliveira E: Microsurgical anatomy of the dural collar (carotid collar) and rings around the clinoid segment of the internal carotid artery. Neurosurgery 42:8698861998

    • Search Google Scholar
    • Export Citation
  • 47

    Seoane ETedeschi Hde Oliveira EWen HTRhoton AL Jr: The pretemporal transcavernous approach to the interpeduncular and prepontine cisterns: microsurgical anatomy and technique application. Neurosurgery 46:8918992000

    • Search Google Scholar
    • Export Citation
  • 48

    Shin MKurita HSasaki TKawamoto STago MKawahara N: Analysis of treatment outcome after stereotactic radiosurgery for cavernous sinus meningiomas. J Neurosurg 95:4354392001

    • Search Google Scholar
    • Export Citation
  • 49

    Shin MKurita HSasaki TTago MMorita AUeki K: Stereotactic radiosurgery for pituitary adenoma invading the cavernous sinus. J Neurosurg 93:Suppl 3252000

    • Search Google Scholar
    • Export Citation
  • 50

    Snead FEAmdur RJMorris CGMendenhall WM: Long-term outcomes of radiotherapy for pituitary adenomas. Int J Radiat Oncol Biol Phys 71:9949982008

    • Search Google Scholar
    • Export Citation
  • 51

    Stapleton CJLiu CYWeiss MH: The role of stereotactic radiosurgery in the multimodal management of growth hormone-secreting pituitary adenomas. Neurosurg Focus 29:4E112010

    • Search Google Scholar
    • Export Citation
  • 52

    Taussky PKalra RCoppens JMohebali JJensen RCouldwell WT: Endocrinological outcome after pituitary transposition (hypophysopexy) and adjuvant radiotherapy for tumors involving the cavernous sinus. Clinical article. J Neurosurg 115:55622011

    • Search Google Scholar
    • Export Citation
  • 53

    Tinnel BAHenderson MAWitt TCFakiris AJWorth RMDes Rosiers PM: Endocrine response after gamma knife-based stereotactic radiosurgery for secretory pituitary adenoma. Stereotact Funct Neurosurg 86:2922962008

    • Search Google Scholar
    • Export Citation
  • 54

    van Lindert EJGrotenhuis JAMeijer E: Results of follow-up after removal of non-functioning pituitary adenomas by transcranial surgery. Br J Neurosurg 5:1291331991

    • Search Google Scholar
    • Export Citation
  • 55

    Yasuda ACampero AMartins CRhoton AL Jrde Oliveira ERibas GC: Microsurgical anatomy and approaches to the cavernous sinus. Neurosurgery 56:1 Suppl4272005

    • Search Google Scholar
    • Export Citation
  • 56

    Zhao BWei YKLi GLLi YNYao YKang J: Extended transsphenoidal approach for pituitary adenomas invading the anterior cranial base, cavernous sinus, and clivus: a single-center experience with 126 consecutive cases. Clinical article. J Neurosurg 112:1081172010

    • Search Google Scholar
    • Export Citation

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