Magnetic resonance imaging appearance of the medial wall of the cavernous sinus for the assessment of cavernous sinus invasion by pituitary adenomas

doi:10.1016/j.neurad.2013.06.003

Journal of Neuroradiology

Volume 40, Issue 4, October 2013, Pages 245-251

https://doi.org/10.1016/j.neurad.2013.06.003 Get rights and content

Summary

Purpose

The diagnostic criteria for cavernous sinus invasion (CSI) by pituitary adenomas are still unsatisfactory and controversial. For this reason, the study examined the appearance of the medial wall of the cavernous sinus (MWCS) on proton-density-weighted (PDW) magnetic resonance imaging (MRI) to determine its value for preoperative assessment of CSI.

Methods

A 3.0-Tesla MRI scanner was used to obtain preoperative PDW images and conventional MRI sequences of 48 consecutive pituitary adenomas, and the MWCS was examined in PDW images to determine the presence of CSI in comparison to surgical findings and three traditional MRI criteria: Knosp grading system (KGS); percentage of encasement of the internal carotid artery (PEICA); and replacement of cavernous sinus compartments (RCSC) by tumors. The value of the MWCS as seen on MRI was compared with that of the Ki-67 labelling index (Ki-67 LI).

Results

CSI images showed that continuity of the MWCS was interrupted and that tumor tissue had infiltrated the cavernous sinus (CS) compartments through the defects. In 96 CSs from 48 patients, the sensitivity of MRI visualization of the MWCS for detection of CSI was 93.3% with a specificity of 93.8%, which was significantly higher than with KGS, PEICA and RCSC (P = 0.007, P = 0.008 and P = 0.056, respectively). Histopathological results showed no significant differences between MRI visualization of the MWCS and the Ki-67 LI.

Conclusion

PDW imaging permits adequate visualization of the MWCS and is superior to traditional diagnostic criteria for the detection of CSI, providing accurate preoperative images for intraoperative navigation.

Introduction

Pituitary adenomas (PAs) are benign intracranial tumors that, if aggressive, can invade adjacent structures such as the dura, bones, nerves and vessels. Approximately 6–10% of PAs pass though the medial wall of the cavernous sinus (MWCS) to invade the cavernous sinuses (CSs) bilaterally [1], [2]. Because of the high risk of CS bleeding and cranial nerve injury, complete surgical removal of these tumors presents a challenge to neurosurgeons. This means that preoperative assessment, especially using magnetic resonance imaging (MRI), is essential for guiding neurosurgeons in determining the optimal treatment for each patient.

The MWCS is the only barrier separating PAs from the CS, and its appearances on MRI can be a good direct predictor of cavernous sinus invasion (CSI). However, the mean thickness of the medial walls is only around 200 μm in fresh adult cadaver specimens [3], [4], which is too thin to be detected on conventional low-resolution MR images. However, certain studies have claimed that MWCS features are insufficient for early diagnosis of CSI [5], [6], so considerable attention has been given to indirect criteria for CSI on MRI. At least three such criteria — namely, the Knosp grading system (KGS), percentage of encasement of the internal carotid artery (PEICA) and replacement of cavernous sinus compartments (RCSC) by tumors — have so far been proposed [7], [8], [9]. Nevertheless, these three traditional MRI criteria fail to provide detailed information on how the tumors pass through the MWCS and infiltrate CS compartments. Furthermore, no consensus has been achieved on these diagnostic criteria [7], [9], [10]. Wolfsberger et al. [11] successfully devised a rapid acquisition with relaxation enhancement (RARE) sequence to visualize the MWCS, but its diagnostic value was unsatisfactory.

The aim of the present study was to determine the appearances of the MWCS on proton-density-weighted imaging (PDWI) sequences and their value for preoperative assessment of CSI and intraoperative neuronavigation. The diagnostic value of the method was determined by comparing MRI visualization of the MWCS with the three traditional MRI criteria, surgical findings and Ki-67 labelling index (LI).

Section snippets

Patient population

To determine the MRI appearances of the MWCS and its diagnostic value for CSI, 48 consecutive patients (28 men, 20 women; age: 22–74 years, mean: 45.4 ± 1.9 years) with tumors admitted to our hospital were followed from April 2011 to April 2012. All patients gave their informed consent to participate in the study, which was approved by the local Research Ethics Committee. On clinical classification, there were 14 prolactinomas, 29 clinical non-functioning adenomas, two adrenocorticotropic

MRI appearances of the medial wall of the cavernous sinus

The MWCS in healthy subjects and in non-CSI samples was visualized as a continuous hypointense line running between pituitary tissue and the CS on PDWI. The MWCS was significantly thinner than the lateral and superior walls of the CS, and often bulged slightly towards the CS (Fig. 1). However, in images with CSI, continuity of the MWCS was interrupted and tumor tissue could be seen extending into the CS compartments through the defects. In addition, the intact boundary became less curved or

Discussion

The excision of PAs that invade the CS is challenging for neurosurgeons because of the high risk of intraoperative bleeding, the likelihood of residual tumor and high recurrence rate, and thus underscores the importance of preoperative MRI assessment of CSI. Furthermore, because the MWCS is the only dural barrier between the tumor and CS compartments, defects in the MWCS are a direct sign of CSI [15]. However, visualization of the MWCS on MRI is difficult, and neurosurgeons have traditionally

Conclusion

Visualization of the MWCS using PDWI is an excellent preoperative predictor of CSI and may serve as an effective tool for guiding surgeons attempting complete and safe resection of tumors. Direct visualization using MRI enables the detection and localization of defects in the MWCS, which can facilitate the resection of tumors occupying the CS compartments. In addition, visualization by MRI may be of value in avoiding the destruction of any residual normal medial wall.

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.

References (24)

J.O. Vieira et al.
Evaluation of magnetic resonance imaging criteria for cavernous sinus invasion in patients with pituitary adenomas: logistic regression analysis and correlation with surgical findings
Surg Neurol
(2006)
M.I. Dujardin et al.
Quantification of cerebral tumour blood flow and permeability with T1-weighted dynamic contrast enhanced MRI: A feasibility study
J Neuroradiol
(2012)
A. Campero et al.
Surgical anatomy of the dural walls of the cavernous sinus
J Clin Neurosci
(2010)
K. Pinker et al.
The value of high-field MRI (3 T) in the assessment of sellar lesions
Eur J Radio
(2005)
R. Gejman et al.
Role of Ki-67 proliferation index and p53 expression in predicting progression of pituitary adenomas
Hum Pathol
(2008)
J. Ahmadi et al.
Cavernous sinus invasion by pituitary adenomas
Am J Roentgenol
(1986)
K. Thapar et al.
Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody
Neurosurgery
(1996)
Q. Songtao et al.
Membranous layers of the pituitary gland: histological anatomy study and related clinical issues
Neurosurgery
(2009)
A. Yasuda et al.
The medial wall of cavernous sinus: microsurgical anatomy
Neurosurgery
(2004)
J.L. Dietemann et al.
Is there a dural wall between the cavernous sinus and the pituitary fossa? Anatomical and MRI findings
Neuroradiology
(1998)

G. Scotti et al.

MR imaging of cavernous sinus involvement by pituitary adenomas

Am J Roentgenol

(1988)

J.P. Cottier et al.

Cavernous sinus invasion by pituitary adenoma: MR Imaging

Radiology

(2000)

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On the other hand, two previous studies concluded that PEICA < 25% was useful for exclusion of CSI, as confirmed by the results of this study (PEICA < 28%) [3,15]. Several previous studies have used microscopic reference standards to investigation VCO as a criterion for CSI [3,15,17]. This study supports the findings of previous reports, with respect to the utility of inferolateral and lateral VCO to confirm the diagnosis of CSI [3,15,20].
Cavernous sinus invasion (CSI) by pituitary tumors is associated with subtotal resection and persistent endocrinopathy. The Knosp classification is a magnetic resonance imaging (MRI) tool used to define CSI in the 2017 World Health Organization Classification. However, alternative criteria may have superior diagnostic performance. This study aimed to assess the diagnostic performance of four MRI criteria, using a combination of endoscopy and day 1 MRI as the reference standard for CSI. A cross-sectional study was conducted including patients treated with endoscopic endonasal transsphenoidal surgery for pituitary macroadenomas, recruited from a tertiary pituitary multidisciplinary center in Sydney, Australia between September 2013, and February 2021. The diagnostic performances of four MRI criteria were assessed: the Knosp criteria, percentage encasement of the internal carotid (PEICA), venous compartment obliteration (VCO), and the Fernandez-Miranda classification. Reference CSI was defined using a combination of intraoperative endoscopy and day 1 MRI. A total of 210 cavernous sinuses (105 patients), were analyzed, (51.7 ± 16.3yrs, 43% female), of which 18% had CSI. CSI was best diagnosed by Knosp ≥ 2 (63% sensitivity and 89% specificity), PEICA ≥ 28% (84% sensitivity and 77% specificity) and VCO of ≥ 3 compartments (65% sensitivity and 89% specificity). CSI was unlikely if any of the following signs were present: Knosp < 1, PEICA < 28%, preservation of the medial or superior compartments or sparing of the superior Fernandez-Miranda compartment (negative predictive value 95%, 95%, 94%, 91% and 92% respectively). In conclusion, alternatives to the Knops criteria including PEICA and VCO can aid CSI diagnosis.
First Application of 7-T Magnetic Resonance Imaging in Endoscopic Endonasal Surgery of Skull Base Tumors
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Improved vessel detection may help reduce vascular complications, and it may improve management of nontumor pathologies, such as cerebral aneurysms.44,45 Tumor characteristics such as size, firmness, invasion of CS, and degree of neovascularity are important factors that can significantly impact surgical time, technical difficulty, and extent of resection in sellar and parasellar masses.13,41,46 In pituitry adenomas in particular, MRI allows for both prediction of extent of invasion and delineation of tumor from healthy gland.12,47
Successful endoscopic endonasal surgery for the resection of skull base tumors is reliant on preoperative imaging to delineate pathology from the surrounding anatomy. The increased signal-to-noise ratio afforded by 7-T MRI can be used to increase spatial and contrast resolution, which may lend itself to improved imaging of the skull base. In this study, we apply a 7-T imaging protocol to patients with skull base tumors and compare the images with clinical standard of care.
Images were acquired at 7 T on 11 patients with skull base lesions. Two neuroradiologists evaluated clinical 1.5-, 3-, and 7-T scans for detection of intracavernous cranial nerves and internal carotid artery (ICA) branches. Detection rates were compared. Images were used for surgical planning and uploaded to a neuronavigation platform and used to guide surgery.
Image analysis yielded improved detection rates of cranial nerves and ICA branches at 7 T. The 7-T images were successfully incorporated into preoperative planning and intraoperative neuronavigation.
Our study represents the first application of 7-T MRI to the full neurosurgical workflow for endoscopic endonasal surgery. We detected higher rates of cranial nerves and ICA branches at 7-T MRI compared with 3- and 1.5-T MRI, and found that integration of 7 T into surgical planning and guidance was feasible. These results suggest a potential for 7-T MRI to reduce surgical complications. Future studies comparing standardized 7-, 3-, and 1.5-T MRI protocols in a larger number of patients are warranted to determine the relative benefit of 7-T MRI for endonasal endoscopic surgical efficacy.
Cavernous Sinus Invasion in Pituitary Adenomas: Systematic Review and Pooled Data Meta-Analysis of Radiologic Criteria and Comparison of Endoscopic and Microscopic Surgery
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KS 1 was defined as lateral tumor extension beyond the medial intercarotid line, KS 2 was extension beyond the median intercarotid line, KS 3 was extension beyond the lateral intercarotid line, and KS 4 was total encasement of the intracavernous internal carotid artery (ICA).25 Interrupted continuity of the medial wall of CS with tumor extending through the defect was considered as defect in medial wall of CS.40 Tumor obliteration of the following venous compartments of CS was also considered: the medial compartment between the ICA and pituitary fossa; the superior compartment above the ICA; the lateral compartment lateral to the ICA; the carotid sulcus compartment between the ICA and the carotid sulcus of the sphenoid bone (CSVCO); and the inferolateral compartment between the carotid sulcus and the inferolateral venous compartment (ILVCO).9
Despite the substantial impact of cavernous sinus invasion (CSI) in pituitary adenoma surgery, its radiologic determination has been inconsistent and variable, and the role of endonasal endoscopic surgery has been unclear. This is a systematic review and pooled data meta-analysis of the literature to ascertain the best radiologic criteria for CSI and verify the efficacy and safety of an endonasal endoscopic approach.
We searched the MEDLINE database (1993–2015) to identify studies on radiologic criteria for CSI and endonasal surgery. Using PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines, the studies included were reviewed for CSI criteria, gross total resection (GTR), endocrine remission, cranial nerve deficits, carotid injury, and other complications.
The prevalence of CSI was 43% radiographically compared with 18% intraoperatively (P < 0.001). The radiologic criteria of inferolateral venous compartment obliteration and Knosp 3–4 had the highest correlation with intraoperative CSI and the lowest correlation with GTR. Microscopy had significantly overestimated intraoperative CSI compared with endoscopy (P < 0.001) for each Knosp grade. Endoscopy had significantly higher GTR than did microscopy particularly for Knosp 3–4 (47% vs. 21%; P = 0.001). Carotid injury and cranial nerve deficits occurred in 0.9% and 5%, respectively, with endoscopy. Among endoscopic series with CSI, GTR% showed significant correlation with number of patients in the series (P ≤ 0.01) but no correlation with complications, indicating the relative safety of endonasal endoscopy in experienced hands for removing tumors with CSI.
Knosp 3–4 remains the best objective indicator of CSI. Microscopy tends to overestimate intraoperative CSI compared with endoscopy. Among pituitary adenomas with CSI, GTR in endoscopic series is higher than microscopy and improves with experience without significant additional morbidity.
The role of FSCN1 in migration and invasion of pituitary adenomas
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The prediction of invasion or malignant behavior in PAs remains challenging. FSCN1, an actin-bundling protein, is associated with increased risk of mortality and metastasis in various cancer types. The objective of the study was to evaluate the expression of FSCN1 in 312 PAs cases, and to analyze its association with clinicopathologic features and invasion of PAs, thus serving as a promoter of cancer invasion. In non-function PAs (NFPA), FSCN1 nuclear-positive cases were 53/97 in the invasive group (IPA), and 21/115 in the noninvasive group (nIPA) (ⅹ² = 30.65, p = 0.004). FSCN1 cytoplasm-positive cases were 36/97 in IPA, and 8/107 in nIPA (ⅹ² = 29.09, p = 0.000). In growth hormone adenomas (GHomas), FSCN1 nuclear-positive were 10/13 in IPA, and 3/37 in nIPA (ⅹ² = 23.67, p = 0.000). FSCN1 cytoplasm-positive were 8/13 in IPA, and 2/37 in nIPA (Table 3 ⅹ² = 18.94, p = 0.000). Overall, a significant difference was found between FSCN1 expression and tumor size (ⅹ² = 46.21, p = 0.000), not age (ⅹ² = 2.09, p = 0.148). In the high FSCN1 expression group, 27/137 cases (19.7%) had tumor recurrence, and 10/175 cases (5.7%) in low FSCN1 level (ⅹ² = 14.40 p = 0.000). Reduction of FSCN1 suppressed the invasion level of GH3 cells through transwells test. In addition, reduction of FSCN1 can obviously down-regulate the level of Notch1 and DLL3. Our data may help in deciding whether FSCN1 can be a predictor for invasion and recurrence of PAs.
MR imaging of cavernous sinus lesions: Pictorial review
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Recent studies suggested that 3T MRI can potentially increase the sensitivity and specificity of CS invasion compared to 1.5T MRI [18]. Proton density-weighted images have high sensitivity and specificity (about 93%) in detection of CS invasion by demonstrating interruption of the medial wall of the CS [19]. Craniopharyngiomas arise from remnants of Rathke's craniopharyngeal pouch [20].
The main purpose of this pictorial review is to highlight the important MR imaging findings of various conditions involving the cavernous sinus in addition to brief description of normal anatomy. The pathological conditions that can involve the cavernous sinus can be categorized into infective, inflammatory, granulomatous, vascular and neoplastic causes. Imaging, especially with MRI, plays an important role not only in detection but also in definition of disease extent and in characterization of the pathology. Currently, high-resolution MR images clearly show various components of cavernous sinus which help in making a proper diagnosis and thus appropriate further management.
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To accomplish these tasks, we redefined the walls of the CS using sectioned images and three-dimensional (3D) models. For analyzing the shape of the CS, related articles published since 1976 were searched in the U.S. National Library of Medicine and National Institutes of Health (http://www.ncbi.nlm.nih.gov/pubmed/) (1, 2, 4, 5, 7, 17, 20, 22). After the analysis (Table 1), the inferred shape of the CS was drawn into a schematic figure employing Adobe Illustrator (Adobe Systems, Inc., San Jose, California, USA) (Figure 1).
For the diagnosis and surgical treatment of diseases around the cavernous sinus (CS), radiologists should achieve complete mastery of the sectional anatomy of the CS, and neurosurgeons need to understand the stereoscopic orientation of the CS and circumjacent structures. However, despite the complicated structure of the CS, the current educational resources for its sectional and stereoscopic anatomy are insufficient. Another problem is that the definition of CS walls varies for each researcher. The purpose of this study is to redefine the walls of the CS and to provide related educational materials.
Previous studies on the shape of the CS were analyzed. Sectioned images of a cadaver were prepared at 0.1-mm intervals to be made into three-dimensional (3D) models of the CS and neighboring structures.
Based on other studies, the shape of the CS was redefined as a hexahedron, consisting of 6 walls, and was illustrated as a schematic figure. Scientific exactitude of the hexahedron was proven through matching the points with the actual structures on the sectioned images and 3D models that were made in this study.
The combination of the hexahedron theory, the sectioned images, and the 3D models in this study will enhance the efficiency of studying CS anatomy. The educational resources of this study can be obtained free of charge by medical students, radiologists, and neurosurgeons requiring knowledge of CS anatomy.

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Original articleMagnetic resonance imaging appearance of the medial wall of the cavernous sinus for the assessment of cavernous sinus invasion by pituitary adenomas

Summary

Purpose

Methods

Results

Conclusion

Introduction

Section snippets

Patient population

MRI appearances of the medial wall of the cavernous sinus

Discussion

Conclusion

Disclosure of interest

Surg Neurol

J Neuroradiol

J Clin Neurosci

Eur J Radio

Hum Pathol

Cavernous sinus invasion by pituitary adenomas

Am J Roentgenol

Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody

Neurosurgery

Membranous layers of the pituitary gland: histological anatomy study and related clinical issues

Neurosurgery

The medial wall of cavernous sinus: microsurgical anatomy

Neurosurgery

Is there a dural wall between the cavernous sinus and the pituitary fossa? Anatomical and MRI findings

Neuroradiology

MR imaging of cavernous sinus involvement by pituitary adenomas

Am J Roentgenol

Cavernous sinus invasion by pituitary adenoma: MR Imaging

Radiology

Original article
Magnetic resonance imaging appearance of the medial wall of the cavernous sinus for the assessment of cavernous sinus invasion by pituitary adenomas