Evaluation of Inferior Intercavernous Sinus in Patients With Pituitary Microadenoma by Contrast-Enhanced SPACE Imaging : Journal of Computer Assisted Tomography

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Neuroimaging: Head and Neck

Evaluation of Inferior Intercavernous Sinus in Patients With Pituitary Microadenoma by Contrast-Enhanced SPACE Imaging

Zhao, Xianjing MD∗,†; Wu, Yue MD; Rui, Wenting MD; Wang, Jing MD; Wu, Shiman MD; Zhang, Qi MD; Hao, Xiaozhu MD; Tang, Ying MD; Ren, Yan MD; Sun, Huaping MD; Yao, Zhenwei MD, PhD∗,†

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Journal of Computer Assisted Tomography 46(6):p 961-967, 11/12 2022. | DOI: 10.1097/RCT.0000000000001371
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Abstract

Inferior intercavernous sinus (iICS) is a venous channel below the pituitary gland connecting both sides of the cavernous sinus (Fig. 1). The presence of iICS varies from 17% to 100% in macroscopic and microscopic examination of cadaveric specimens.1–3 Because of its specific location and anatomical variation, iICS injury is predisposed to cause venous bleeding during dura incision in transsphenoidal surgery for pituitary adenomas. Intraoperative bleeding may affect operational field of vision, leading to incomplete pituitary tumor resection. In severe cases, it can result in suspension or abortion of surgery.4 Therefore, the presence and morphology of iICS confirmed before surgery may be helpful to avoid bleeding in transsphenoidal surgery.

F1
FIGURE 1:
Inferior intercavernous sinus anatomy. Figure 1 can be viewed online in color at www.jcat.org.

Pituitary magnetic resonance imaging (MRI) is usually performed for preoperative evaluation of pituitary adenomas.5 Contrast-enhanced (CE) sampling perfection with application optimized contrast using different flip angle evolutions (SPACE) sequence is an advanced MRI technique that provides high spatial resolution information of the sellar region and can be reconstructed into any plane without additional acquisitions.6,7 Previous studies demonstrated that CE SPACE sequence not only increased diagnostic confidence for the detection of pituitary microlesions but also provide better contrast of pituitary gland and cavernous sinus.8–10 So far, however, no previous MRI study has investigated the detection rate, size, and shape of iICS in patients with pituitary microadenoma.

Therefore, the aim of this research was to perform a radiological assessment of iICS before pituitary microadenoma resection. Considering the technical features and application of CE SPACE in sellar region, this study used the multiplanar reconstruction images obtained by CE SPACE technique to evaluate iICS in pituitary microadenoma. To our best knowledge, this is the first MRI study to investigate the presence and morphology of iICS before transsphenoidal surgery for pituitary microadenoma and may help neurosurgeons to avoid the iICS during the dura opening or prepare for bleeding if the iICS cannot be avoided.

MATERIALS AND METHODS

Subjects

This was a retrospective study of 156 patients diagnosed with pituitary adenoma from December 2016 to August 2020. Patients who underwent CE SPACE examinations in our hospital within 1 month before endoscopic transsphenoidal surgery were included. The exclusion criteria were (1) pituitary adenoma larger than 10 mm in size and (2) previous history of brain operations. Demographic information, pathologic results, and imaging data were retrospectively collected. Institutional ethical approval was obtained before conducting the study. Individual consent for this retrospective analysis was waived.

Imaging Protocol

Magnetic resonance imaging examinations were performed using a Siemens Magnetom Verio 3.0 T scanner (Siemens, Munich, Germany). Magnetic resonance scanning was conducted in the following order: sagittal and coronal T1-weighted spin-echo imaging; CE coronal, CE 3D-T2 SPACE sequence, and sagittal T1-weighted spin-echo imaging. Contrast-enhanced images were obtained after gadopentetate dimeglumine administration (0.1 mmol/kg). Acquisition parameters are detailed as follows: T1-weighted spin-echo images—repetition time, 600 milliseconds; echo time, 15 milliseconds; flip angle, 90°; field of view, 224 × 230 mm; matrix size, 350 × 512 (coronal), 175 × 256 (sagittal); and slice thickness, 2.5 mm, with no intersection gap; CE 3D-T2 SPACE—repetition time, 2000 milliseconds; echo time, 129 milliseconds; flip angle, 120°; field of view, 180 × 180 mm; matrix size, 316 × 320; and slice thickness, 1 mm, with no intersection gap.

Image Assessments

All magnetic resonance images were transferred to a processing Siemens Syngo workstation (syngo MultiModality Workplace, Siemens Healthineers). Sagittal reformatted images were reconstructed from the coronal CE SPACE sequence. Both coronal and sagittal CE SPACE and CE T1-weighted images were interpreted for the presence, shape, and size of iICS. The iICS was regarded as the vascular channel running on the inferior floor of the sella,11 which has the same signal intensity as cavernous sinus. The shape of iICS on the 2 planes was also noted. To determine the size of iICS, the maximum transverse diameter (width), craniocaudal diameter (height), and anteroposterior diameter (length) were measured using the electronic calipers provided by the workstation. The iICS width was measured from the coronal plane, whereas the iICS height and depth were measured from the sagittal plane. This measuring method of iICS was adapted from that of pituitary from Yadav et al,12 with minor modifications.

Pituitary dimensions were also measured on coronal and sagittal CE SPACE images using the method reported by Ibinaiye et al.13 The pituitary width was measured as the greatest distance to the left and right sides of the pituitary gland on a coronal slice through the pituitary stalk. The pituitary height is measured as the maximum craniocaudal distance and depth as the anteroposterior distance from the midsagittal plane.

All image assessments were performed independently by 2 radiologists, who had 6 and 12 years of experience in neuroimaging, respectively. The inconformity of the visualization and shape of iICS was solved by a discussion or consultation if necessary. The average of the measurements by the 2 radiologists was used in the analyses.

Statistical Analyses

All statistical analyses were carried out using SPSS, version 24. Continuous variables were expressed as the mean ± SD number, and categorical data were presented by number and percentage. Continuous variables for the patients showing iICS or not showing iICS on CE SPACE images were compared using the independent t test, whereas categorical variables were compared by using the χ2 or Fisher exact test, as appropriate. Measurement reliability of 2 radiologists was assessed using the intraclass correlation coefficient (ICC). Specifically, an ICC with 2-way random effects, absolute agreement, and mean of k raters was used. Intraclass correlation coefficient values of <0.5, 0.5 to 0.75, 0.75 to 0.9, and >0.9 are considered to indicate poor, moderate, good, and excellent reliability, respectively. One-way analysis of variance was also used to compare iICS dimensions among different shapes on coronal plane. The size of iICS measured on CE SPACE and CE T1-weighted images were compared using paired t test. A P value of <0.05 was considered significant.

RESULTS

The Characteristics of Patients

The mean ± SD age of the included 156 patients was 37.62 ± 13.65 years, and the majority of them were females (76.92%). The patients included 73 cases (46.79%) of adrenocorticotropic hormone-secreting adenoma, 26 cases (16.67%) of growth hormone adenoma, 30 cases (19.23%) of prolactinoma, 17 cases (10.90%) of nonfunctioning adenoma, and 10 cases (6.41%) of thyroid stimulating hormone-secreting adenoma. In total, 79 microadenomas were located on the left side of pituitary, 62 microadenomas were located on the right side of pituitary, and 15 microadenomas were located on the middle of pituitary. The mean ± SD size of the included pituitary was 5.71 ± 2.06 mm. The mean width, depth, and height of pituitary gland were 13.37 ± 2.25, 11.00 ± 1.00, and 7.16 ± 1.25 mm, respectively. Patients' characteristics are summarized in Table 1.

TABLE 1 - Characteristics of the Patients
iICS Invisible iICS Visible P
No. patients 84 72
Age, y 40.62 ± 14.99 34.13 ± 11.19 0.003
Sex 0.883
 Male 19 17
 Female 65 55
Pituitary dimension
 Width 13.25 ± 2.52 13.52 ± 1.88 0.465
 Depth 11.02 ± 1.23 10.98 ± 0.64 0.805
 Height 7.02 ± 1.22 7.32 ± 1.28 0.131
Histology of adenoma 0.171
 ACTH 35 38
 Growth hormone 17 9
 Prolactin 15 15
 Nonfunctioning 11 6
 TSH 6 4
Adenoma size, mm 6.07 ± 2.31 5.29 ± 1.65 0.017
Adenoma side 0.356
 Left 47 32
 Right 30 32
 Middle 7 8
ACTH indicates adrenocorticotropic hormone; TSH, thyroid stimulating hormone.

In CE SPACE, the iICS was identified in 46.15% of patients with pituitary microadenoma (n = 72). Patients with invisible iICS were older (P = 0.003) and had lager adenoma size (P = 0.017) than patients with visible iICS on CE SPACE images. The sex of patients and pituitary dimensions together with the histology and side of adenoma did not have a statistically significant impact on the detection rate of iICS.

The Shape of iICS

The characteristics of iICS are shown in Table 2. The iICS may be seen as 3 different types of filiform shapes on coronal CE SPACE images. Among the 72 patients with visible iICS on CE SPACE images, the iICS connected both sides of the cavernous sinus in a large majority of patients (n = 58 [80.56%], type 1). In 8 cases, the iICS arose at the left cavernous sinus but did not reach the right cavernous sinus (type 2). In 6 cases, the iICS arose at the right cavernous sinus but did not reach the left cavernous sinus (type 3). On sagittal images, all of the visible iICS were appeared as a crescent shaped hyperintense structure below the pituitary gland Representative examples of each type are presented in Figures 2, 3, and 4.

TABLE 2 - Characteristics of the iICS on CE Spaces Images
Shape on the Coronary Plane Type 1 Type 2 Type 3 P
Number (%) 58 (80.56) 8 (11.11) 6 (8.33)
Width, mm 12.38 ± 2.42 5.45 ± 1.98 6.93 ± 2.65 <0.001
Depth, mm 5.40 ± 1.24 5.22 ± 1.06 4.30 ± 1.20 0.121
Height, mm 1.41 ± 0.19 1.37 ± 0.30 1.41 ± 0.10 0.914
Type 1, the iICS connects both sides of the cavernous sinus; type 2, the iICS arises at the left cavernous sinus but does not reach the right cavernous sinus; type 3, the iICS arises at the right cavernous sinus but does not reach the left cavernous sinus.

F2
FIGURE 2:
A 38-year-old woman with pathologically proven thyroid stimulating hormone-secreting adenoma on the left side of the pituitary. A, T1-weighted image displays subtle low signal intensity of this mass. B, C, Coronal and sagittal enhanced T1-weighted images shows a rounded region of hypoenhancement compared with the rest of the gland. D, E. Coronal and sagittal CE SPACE images demonstrate high signal intensity lesion on the left side of the pituitary. The iICS appears to be plexiform shaped and connects both sides of the cavernous sinus on coronal CE SPACE images. The iICS appears as a crescent-shaped hyperintense structure below the pituitary gland. PM, pituitary microadenoma.
F3
FIGURE 3:
A 31-year-old man with pathologically proven adrenocorticotropic hormone-secreting adenoma on the right side of the pituitary. A, T1-weighted image displays mixed hyperintense and hypointense signal intensity of this mass. B, C, Coronal and sagittal enhanced T1-weighted images shows a rounded region of hypoenhancement compared with the rest of the gland. D, E, Coronal and sagittal CE SPACE images demonstrate high signal intensity lesion on the left side of the pituitary. The iICS arises at the left cavernous sinus but does not reach the right cavernous sinus on coronal CE SPACE images. The iICS appears as a crescent shaped hyperintense structure below the pituitary gland. PM, pituitary microadenoma.
F4
FIGURE 4:
A 42-year-old man with pathologically proven prolactinoma on the left side of the pituitary. A, T1-weighted image displays subtle low signal intensity of this mass. B, C, Coronal and sagittal enhanced T1-weighted images shows heterogeneous enhancement. D, E, Coronal and sagittal CE SPACE images demonstrate high signal intensity lesion on the left side of the pituitary. The iICS arises at the right cavernous sinus but does not reach the left cavernous sinus on coronal CE SPACE images. The iICS appears as a crescent-shaped hyperintense structure below the pituitary gland on coronal CE SPACE images. The iICS appears as a crescent-shaped hyperintense structure below the pituitary gland. PM, pituitary microadenoma.

Fifty-two patients had visible iICS on both CE SPACE and CE T1-weighted images. The iICS also had 3 different types of filiform shapes on coronal CE T1-weighted images: type 1 in 73.1% (n = 38), type 2 in 11.5% (n = 6), and type 3 in 15.4% (n = 8) of cases. On sagittal CE T1-weighted images, all of the visible iICS were appeared as a crescent-shaped hyperintense structure below the pituitary gland.

The Size of iICS

The mean ± SD width and depth of iICS were 11.15 ± 3.47 mm and 5.29 ± 1.24 mm, whereas the mean ± SD height of iICS was 1.41 ± 0.19 mm. The mean ± SD width, depth, and height of iICS type 1 were 12.38 ± 2.42 mm, 5.40 ± 1.24 mm, and 1.41 ± 0.19 mm, respectively. The corresponding values for iICS type 2 were 5.45 ± 1.98 mm, 5.22 ± 1.06 mm, and 1.37 ± 0.30 mm, respectively. As for iICS type 3, the mean ± SD width was 6.93 ± 2.65 mm, the mean ± SD depth was 4.30 ± 1.20 mm, and the mean ± SD height was 1.41 ± 0.10 mm. There was a statistically significant difference between the width of 3 types (<0.001). The depth and height of the 3 types of iICS were not statistically significant.

Table 3 summarizes the comparison of the iICS size measured on CE SPACE and CE T1-weighted images. There were no significant differences between the width, depth, and height of iICS measured on CE SPACE and CE T1-weighted images.

TABLE 3 - Comparison of the iICS Measured on CE SPACE and CE T1-Weighted Images
CE SPACE CE T1-Weighted P
Type 1
 Width, mm 12.62 ± 2.30 12.70 ± 2.27 0.436
 Depth, mm 5.51 ± 1.32 5.50 ± 1.35 0.395
 Height, mm 1.41 ± 0.18 1.40 ± 0.20 0.499
Type 2
 Width, mm 6.93 ± 2.65 6.95 ± 2.65 0.755
 Depth, mm 4.30 ± 1.20 4.30 ± 1.18 0.967
 Height, mm 1.41 ± 0.10 1.35 ± 0.11 0.161
Type 3
 Width, mm 10.93 ± 3.70 5.52 ± 1.84 0.345
 Depth, mm 5.23 ± 1.30 5.18 ± 1.06 0.345
 Height, mm 1.40 ± 0.21 1.39 ± 0.19 0.394
Type 1, the iICS connects both sides of the cavernous sinus; type 2, the iICS arises at the left cavernous sinus but does not reach the right cavernous sinus; type 3, the iICS arises at the right cavernous sinus but does not reach the left cavernous sinus.

In assessing interobserver reliability for measuring iICS on CE SPACE images, the ICC was 0.922 for iICS width, 0.933 for iICS depth, and 0.783 for iICS height; the ICC of ICS width, depth, and height measured on CE T1-weighted images were 0.957, 0.979, and 0.761, respectively. These results indicated that the measuring method had good to excellent reproducibility.

DISCUSSION

In this study, we reported the first use of CE SPACE sequence to evaluate iICS for the patients with pituitary microadenoma. SPACE is a 3-dimensional fast spin-echo MRI sequence with extremely long echo train lengths and ultrashort echo spacing. This technique can provide many useful image contrasts and are less sensitive to susceptibility artifacts. In addition, it can produce high-resolution isotropic images that can be retrospectively reformatted for viewing in freely selectable directions,14,15 thus facilitating the assessment of complex anatomical structures related to many clinical applications, including the sellar region. It has been shown that CE SPACE has great ability in identification of cavernous sinus invasion by pituitary macroadenoma.7 In the present study, we enrolled 156 patients with pituitary microadenoma. We demonstrated the detection rate of iICS on CE SPACE images was 46.15%. Our study also found the location, shape, and size of iICS can be clearly displayed on CE SPACE images in patients with pituitary microadenoma. These findings suggest that CE SPACE may be used as a promising modality in evaluating iICS before surgery for pituitary microadenoma.

Most of the prior studies focused on the assessment of ICSs using cadaveric specimens. In these anatomical studies, the presence of iICS was variable, ranging from 17% to 100% (Table 4). The detection rate of iICS was both more than 94% in 2 studies on serial microscopic sections.3,18 Other researchers, however, who performed macroscopic evaluation on cadaveric specimens, found the presence of iICS varied from 17% to 100%.1,2,16,17,19,20 With regard to the shape of iICS, plexiform was the most frequent in these researches. Deng and coworkers17 demonstrated what was mostly presented as a crescent or oval shape in the midsagittal section of the cadavers, which are similar to our results. Through evaluating the presence and morphology of iICS before transsphenoidal surgery for pituitary microadenoma, neurosurgeons could try to avoid the iICS during the dura opening or prepare for bleeding if the iICS cannot be avoided (Fig. 5).

TABLE 4 - Summary of the Cadaveric Studies on iICS
Study No. Cases Method Presence Shape
Aquini et al, 1994 3 32 Serial microscopic sections 97% Plexuslike, venous lake, and mixed
Banks et al, 2020 16 15 Macroscopic evaluation 66% NM
Chenin et al, 2020 1 17 Macroscopic evaluation 100% Plexiform, filiform, or punctiform
Deng et al, 2015 17 18 Macroscopic evaluation 61% Crescent or oval
Green, 1957 18 18 Serial microscopic sections 94% Oval
Lu et al, 2006 19 10 Macroscopic evaluation 50% NM
Tubbs et al, 2014 2 35 Macroscopic evaluation 17% NM
Wahl et al, 2020 20 50 Macroscopic evaluation 26% Plexiform
NM indicates not mentioned.

F5
FIGURE 5:
Transsphenoidal surgery for pituitary microadenoma. Neurosurgeons should try to avoid the iICS during the dura opening. Figure 5 can be viewed online in color at www.jcat.org.

In terms of radiological studies on iICS, both computed tomography and MRI techniques were used to evaluate iICS in patients with different diseases (Table 5). The detection rates of iICS were both 29% in patients with normal parasellar and sellar anatomy, although using different imaging method.11,17 Researchers also have found dilated iICS in patients with intracranial hypotension.21,22 Alcaide-Leon et al21 determined that a crescent iICS was the most common shape in patients with craniospinal hypotension, followed by an oval or rounded shape; the triangular shape was the least common shape among those patients on sagittal T1-weighted images. Regarding studies on patients with sellar lesions, Mizutani and colleagues23 included patients with pituitary adenoma and tuberculum sellae meningioma in their research, and they did not detect ICS when the volume of pituitary adenoma was greater than 5 mL. This result was similar with our finding that iICS was more able to be detected in patients with smaller pituitary microadenoma. We also found that iICS was more able to be detected in younger patients, whereas Mizutani et al23 found no significant difference between the younger than 50 years and older than 51 years groups. This discordance is likely a result of differences in the study subjects. This result should be researched further.

TABLE 5 - Summary of the Radiological Studies on iICS
Citation No. Cases Disease Method Presence Shape
Alcaide-Leon et al, 2016 21 26 Craniospinal hypotension NC-T1W, CE-T1W, MRV 50% Crescent, oval, rounded or triangular
Bonneville et al, 2011 22 12 Craniospinal hypotension MRI 92% NM
Deng et al, 2015 17 24 Suspected as intracranial lesion or lacunar cerebral infarction CE-MRV 29% NM
Mizutani et al, 2016 23 52 Pituitary adenoma CT-DSV 5.8% NM
Mizutani et al, 2016 23 13 Tuberculum sellae meningioma CT-DSV 23.1% NM
Mizutani et al, 2015 11 97 Unruptured cerebral aneurysm CT-DSV 29% NM
CE-MRV indicates contrast-enhanced magnetic resonance venography; CE-T1W, contrast-enhanced T1-weighted imaging; CT-DSV, computed tomography digital subtraction venography; MRV, magnetic resonance venography; NC-T1W, noncontrast T1-weighted imaging; NM, not mentioned.

The iICS in our study was presented as filiform shapes on coronal CE SPACE images. The iICS usually demonstrated as hyperintense line below the pituitary gland on coronal T1-weighted magnetic resonance images (Fig. 6). Whether coronal CE SPACE images can assist in differentiating between iICS and pituitary lesion needs further investigation. In addition, we found that the iICS arose at the left cavernous sinus but did not reach the right cavernous sinus in 8 cases. This finding was also detected by Chenin et al.1 One possible explanation may account for this is that the iICS may be partially compressed and obliterated by pituitary adenoma.

F6
FIGURE 6:
A 24-year-old woman with pathologically proven prolactinoma on the left side of the pituitary. A, T1-weighted image displays high signal intensity of iICS (white arrow). B, Coronal CE SPACE images demonstrate high signal intensity of iICS (white arrow) and high signal intensity pituitary microadenoma (black arrow).

Limitations of the current study included small sample size and retrospective design. Although CE SPACE sequence was introduced to our institute for 4 years, the number of patients underwent surgery for pituitary microadenoma who received CE SPACE examinations was limited. Further prospective studies with larger sample sizes are needed to clarify our findings and to elucidate their potential clinical value, for example, to compare the preoperative imaging with operative view of iICS in each patient.

CONCLUSIONS

In conclusion, CE SPACE may serve as a promising technique in evaluating iICS and individualized preoperative planning before transsphenoidal surgery for pituitary microadenoma.

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Keywords:

intercavernous sinus; pituitary neoplasms; magnetic resonance imaging; transsphenoidal surgery

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