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Published online before print February 1, 2006, 10.1148/radiol.2383042204
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(Radiology 2006;239:223-231.)
© RSNA, 2006

Neuroradiology

Pituitary Macroadenomas: Preoperative Evaluation of Consistency with Diffusion-weighted MR Imaging—Initial Experience1

Alberto Pierallini, MD, Francesca Caramia, MD, Carlo Falcone, MD, Emanuele Tinelli, MD, Amalia Paonessa, MD, Alessia Bernardo Ciddio, MD, Marco Fiorelli, MD, Federico Bianco, MD, Stefania Natalizi, MD, Luigi Ferrante, MD and Luigi Bozzao, MD

1 From the Neuroradiology Section (A. Pierallini, F.C., C.F., E.T., A.B.C., M.F., L.B.) and Neuroradiology Unit, Department of ENS and Neurology (F.B.), Section of Neuropathology (S.N.), Department of Neurological Sciences, University of Rome, "La Sapienza," Viale dell'Università 30, 00185 Rome, Italy; Department of Neuroradiology, I.R.C.C.S. San Raffaele Pisana, Rome, Italy (A. Pierallini, F.C., A. Paonessa); and Section of Neurosurgery, Department of Neurological Sciences, Sant' Andrea Hospital, Rome, Italy (L.F.). Received December 29, 2004; revision requested March 1, 2005; revision received April 29; accepted June 3; final version accepted August 5. Address correspondence to A. Pierallini (e-mail: alberto.pierallini{at}uniroma1.it).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Purpose: To prospectively evaluate use of diffusion-weighted (DW) magnetic resonance (MR) images and apparent diffusion coefficient (ADC) maps for determination of the consistency of macroadenomas.

Materials and Methods: The study protocol was approved by the institutional ethics committee, and informed consent was obtained from all patients. Twenty-two patients with pituitary macroadenoma (10 men, 12 women; mean age, 54 years ± 17.09 [standard deviation]; range, 21–75 years) were examined. All patients underwent MR examination, which included T1-weighted spin-echo and T2-weighted turbo spin-echo DW imaging with ADC mapping and contrast material–enhanced T1-weighted spin-echo imaging. Regions of interest (ROIs) were drawn in the macroadenomas and in normal white matter on DW images, ADC maps, and conventional MR images. Consistency of macroadenomas was evaluated at surgery and was classified as soft, intermediate, or hard. Histologic examination was performed on surgical specimens of macroadenomas. Mean ADC values, signal intensity (SI) ratios of tumor to white matter within ROIs on conventional and DW MR images, and degree of enhancement were compared with tumor consistency and with percentage of collagen content at histologic examination by using analysis of variance for linear trend.

Results: The mean value of ADC in the soft group was (0.663 ± 0.109) x 10–3 mm2/sec; in the intermediate group, (0.842 ± 0.081) x 10–3 mm2/sec; and in the hard group, (1.363 ± 0.259) x 10–3 mm2/sec. Statistical analysis revealed a significant correlation between tumor consistency and ADC values, DW image SI ratios, T2-weighted image SI ratios, and percentage of collagen content (P < .001, analysis of variance). No other statistically significant correlations were found.

Conclusion: Findings in this study suggest that DW MR images with ADC maps can provide information about the consistency of macroadenomas.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
In the past decade, surgical treatment of pituitary tumors was performed by using either the direct endonasal transsphenoidal approach or the traditional sublabial and transseptal transsphenoidal approach. Both techniques required extensive mucosal dissection and led to long-term patient discomfort and rhinologic complications (1–4). Recently, the endoscopic transsphenoidal technique has been applied as a minimally invasive surgical procedure to remove pituitary tumors. An advantage of this technique, compared with the traditional technique, is that postoperative nasal problems may be avoided (5). Not all macroadenomas are amenable to resection with the transsphenoidal endoscopic technique. In cases in which a transnasal approach is contraindicated, such as cases of sphenoid sinusitis or ectatic midline ("kissing") carotid arteries, a transcranial approach may be warranted. Some patients who harbor pituitary macroadenomas with significant lateral suprasellar extension that cannot be adequately removed transsphenoidally may benefit from a transcranial approach (6). Furthermore, the main limitation of the endoscopic transsphenoidal technique, as is the limitation for the traditional transsphenoidal techniques, may be tumor consistency (7–9). Most macroadenomas are soft and easily resectable, whereas about 10% of large pituitary tumors may be fibrous (8,9) and exhibit increased consistency; macroadenomas with hard components cannot be successfully removed with the endoscopic technique and may require a more extensive transsphenoidal approach.

Knowledge of the consistency of macroadenomas may help the clinician to plan the proper surgical technique before the procedure; thus, the clinician can avoid conversion from an endoscopic to a full transsphenoidal technique during the procedure. This strategy may prove to be cost effective and psychologically valuable for both the patient and the neurosurgeon.

The role of findings with conventional magnetic resonance (MR) imaging in the prediction of consistency of macroadenomas is controversial. Some authors have reported that macroadenomas that have areas of low signal intensity (SI) on T2-weighted MR images and that enhance more homogeneously are fibrous and contain more collagen (10), whereas others have suggested that there is no particular correlation between MR imaging findings and tumor consistency (9,11,12).

Diffusion-weighted (DW) MR imaging allows the measurement of tissue water diffusion, which is affected by the size and integrity of structures that normally restrict diffusion, in the brain. The apparent diffusion coefficient (ADC) can be increased as a result of pathologic processes that modify tissue integrity, and thus these processes reduce "restricting" barriers (13).

We hypothesized that DW imaging might enable us to characterize tumor components within macroadenomas and to identify tumors with increased fibrosis. Thus, the purpose of our study was to prospectively evaluate DW MR images and ADC maps for the determination of the consistency of macroadenomas.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Patients
For this hypothesis-generated study, we planned to include all consecutive patients with pituitary adenomas who were referred to our center in 1 year. Between April 2002 and May 2003, a total of 22 patients (10 men, 12 women; mean age, 54 years ± 17.09 [standard deviation]; range, 21–75 years) with pituitary macroadenomas were admitted to the Neurosurgery Department at the University of Rome, "La Sapienza," Rome, Italy. All 22 patients were included in our study. The presence of a macroadenoma was suggested by clinical history and physical and neurologic examination findings. Hormonal status was normal in all patients. Our study protocol was approved by the ethics committee at our institution, and informed consent was obtained from all patients.

Imaging and Analysis
All patients underwent bone preoperative coronal computed tomography (CT) (Somatom TM Vision Plus 4 Volume Zoom; Siemens, Munich, Germany) with 2-mm section thickness to show the bone structures and soft tissue of the nasal cavity. The parameters were as follows: field of view, 160 mm; tube current, 100 mA; tube voltage, 130 kV; focal spot, small; and mean total acquisition time, 5 minutes.

All patients underwent MR imaging with a 1.5-T clinical imager (Gyroscan NT Intera Master; Philips, Eindhoven, the Netherlands) and a quadrature head coil. The examination was performed with 3-mm section thickness in coronal planes perpendicular to the sellar floor. MR imaging was performed by using turbo spin-echo T2-weighted (repetition time msec/echo time msec, 3000/110) and spin-echo T1-weighted (400/14) coronal nonenhanced sequences; coronal and sagittal spin-echo T1-weighted sequences were performed after administration of 0.1 mmol per kilogram of body weight gadodiamide (Omniscan; Nycomed Amersham Sorin, Oslo, Norway). Sequences were performed with a 256 x 256-pixel matrix and a 180-mm field of view. Prior to contrast agent administration, DW MR images were acquired in the coronal plane, with diffusion gradients applied along the three principal orthogonal axes, in turn, by using single-shot spin-echo echo-planar sequences (5000/101–108). We used the following parameters: matrix, 224 x 224; field of view, 220 mm; section thickness, 5 mm; intersection gap, 1 mm; maximum gradient strength, 22 mT/m; acquisition time, 32 seconds; and b values, 0 and 1000 sec/mm2. Maps of the ADC also were generated.

Regions of interest (ROIs) for SI and ADC analysis were drawn directly on the images obtained with conventional sequences and on the images with b values of 0 sec/mm2 obtained with the diffusion MR imaging sequence by two authors (A.P. and F.C., each with 15 years of experience with MR imaging of the brain) in consensus. The regions were determined from careful visual comparison of the conventional T2-weighted MR images, the nonenhanced T1-weighted MR images, the contrast material–enhanced MR images, and the baseline MR images with a b value of 0 sec/mm2. All ROIs were of an arbitrarily chosen uniform shape and size (elliptic, 50 mm2) and were drawn by these experienced neuroradiologists (A.P., F.C.) who were blinded to the clinical details. ROIs were identified in the central and solid-appearing portions of the macroadenomas; they were strictly defined anatomically; and cystic, necrotic, or hemorrhagic areas were intentionally excluded. ROIs were also placed in the normal white matter. Partial volume effects were minimized with inspection of the anterior and posterior sections in regard to the ROI to avoid averaging the effects with tissues other than the solid part of macroadenomas (an ROI in the macroadenoma) or with tissues other than normal white matter (an ROI in the white matter). The ROIs placed on the images with a b value of 0 sec/mm2 were transferred onto the ADC maps to obtain the corresponding ADC values.

To avoid scaling problems on conventional MR images, particularly on enhanced T1-weighted images, and on DW images, we decided to calculate SI ratios.

For conventional and DW images, the relative SI of the adenoma was assessed with calculation of the ratio of SI in the tumor to that in the normal white matter in the same patient.

For contrast-enhanced images, degree of enhancement was also calculated by dividing the SI in the ROI drawn in the macroadenoma on the contrast-enhanced T1-weighted images by the SI in the ROI drawn in the macroadenoma on the nonenhanced T1-weighted images.

For ADC values, the absolute values were used for further analysis. ADC values were also calculated in normal white matter, however, for assessment of the validity of our method and for comparison of our findings with the results in previous investigations. Also, for assessment of homogeneity of the magnetic field over time and for measurement of the potential occurrence of a drift in ADC values, before all MR imaging studies were performed, a water phantom maintained at a constant temperature of 22°C was imaged by using the same sequence that was used for DW imaging. The mean ADC value and standard deviation were (2.07 ± 0.06) x 10–3 mm2/sec, and there was no evidence of a substantial drift over time.

Surgery
All patients underwent surgical resection of the macroadenoma performed by one neurosurgeon (L.F., with 30 years of experience in brain surgery). At surgery, tumor consistency was evaluated by the neurosurgeon, who was blinded to the DW MR imaging findings and findings of ADC analysis, and tumors were classified into three groups: tumors with soft consistency (easily removable through suction), tumors with intermediate consistency (removable with difficulty through suction), and tumors with hard consistency (not removable through suction but excised en bloc).

Histologic Examination
Histologic examination was performed in all patients by one pathologist (S.N., with 10 years of experience), who was blinded to clinical and MR imaging data. Immediately after resection of the tumors, the specimens were fixed in 10% buffered formalin and embedded in paraffin. Histologic slices of 4-µm thickness were prepared. Routine specimen processing involved the staining of slides with hematoxylin-eosin and immunohistochemical analysis performed by using antibodies for pituitary hormones. Tumor specimens also were examined histochemically for collagen content by using the Sirius red stain method. A quantitative estimation of fibrous tissue was performed on histologic slices stained with the Sirius red stain method by using an interactive image analysis system (IAS 2000; Delta Sistemi, Rome, Italy), which consisted of a color video–equipped computer that was linked to the microscope by a video camera. All of the measurements were performed by using a microscopic objective magnification of x20. Morphometric analysis was performed in four random regions of each specimen. Each area of collagen and the total tumor area were measured, and the percentage of collagen content (PCC) was calculated by using the following equation: PCC = [{Sigma} (Acoll)/{Sigma} (Atottum–Aart–Abv)] · 100, where Acoll is area of collagen, Atottum is area of total tumor, Aart is the area occupied by the artifactual distortion of tissue architecture, and Abv is the area occupied by blood vessels.

Statistical Analysis
Statistical analysis was performed by one author (M.F., with 15 years of experience with statistical analysis) by using statistical software (SPSS, release 11.0.1; SPSS, Chicago, Ill).

We used analysis of variance to test the differences among mean values of several quantitative MR parameters (ADC values, SI ratios on conventional and DW MR images, and degree of enhancement) and the percentage of collagen content across the three tumor consistency groups of adenomas identified at surgery.

The correlation between percentage of collagen content and MR parameters (ADC values, SI ratios on conventional and DW MR images, and degree of enhancement) was tested by using the Spearman correlation test. A difference with a threshold P value of less than .05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Surgical Findings
In one patient in whom the tumor exceeded the boundaries of the pituitary fossa and manifested a hard consistency, the endoscopic endonasal transsphenoidal technique was completed with craniotomy. In the remaining 21 patients, the endoscopic endonasal transsphenoidal technique was used; in three patients in whom the tumor exhibited a hard consistency, a more extensive direct endonasal transsphenoidal technique was used. In 22 patients, the tumor consistency at surgery was classified as soft in 12 (55%) patients, intermediate in six (27%) patients, and hard in four (18%) patients. In two patients, cystic components were evident with conventional MR imaging sequences and were confirmed at surgery.

Findings of Imaging and Analysis
The mean ADC values, the SI ratios on DW MR images and conventional MR images, and the degree of enhancement in the ROI in each group are shown in the Table.


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  		Mean ADC Values, SI Ratios on DW Images and Conventional MR Images, and Percentage of Collagen Content of Macroadenomas

 
Adenomas exhibited heterogeneous values for diffusion and the ADC (mean, [0.839 ± 0.30]x 10–3 mm2/sec; range, [0.485–1.688] x 10–3 mm2/sec). The mean ADC value in normal white matter was (0.784 ± 0.50) x 10–3 mm2/sec, and the range was (0.709–0.884) x 10–3 mm2/sec, and these values were in agreement with values in previous studies (14).

Macroadenomas in the soft group were inhomogeneous and hyperintense or isointense on T2-weighted MR images (Fig 1a) and hypointense on T1-weighted MR images, and they exhibited marked enhancement after administration of contrast agent in all but one patient, in whom little enhancement was found. In patients with macroadenomas in the soft group, tumors were hyperintense on DW MR images, and they exhibited a mean ADC value of (0.663 ± 0.109) x 10–3 mm2/sec (Fig 1b, 1c).


Figure 1
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  		Figure 1a: Macroadenoma with soft consistency in 46-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous isointense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hyperintense mass (arrows) with respect to normal white matter. (c) Coronal ADC map shows mass (arrows) with decreased diffusion coefficient of (0.593 ± 0.126) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with scant fibrous stroma (in red). (Sirius red stain; original magnification, x20.)

 

Figure 1
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  		Figure 1b: Macroadenoma with soft consistency in 46-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous isointense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hyperintense mass (arrows) with respect to normal white matter. (c) Coronal ADC map shows mass (arrows) with decreased diffusion coefficient of (0.593 ± 0.126) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with scant fibrous stroma (in red). (Sirius red stain; original magnification, x20.)

 

Figure 1
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  		Figure 1c: Macroadenoma with soft consistency in 46-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous isointense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hyperintense mass (arrows) with respect to normal white matter. (c) Coronal ADC map shows mass (arrows) with decreased diffusion coefficient of (0.593 ± 0.126) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with scant fibrous stroma (in red). (Sirius red stain; original magnification, x20.)

 

Figure 1
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  		Figure 1d: Macroadenoma with soft consistency in 46-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous isointense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hyperintense mass (arrows) with respect to normal white matter. (c) Coronal ADC map shows mass (arrows) with decreased diffusion coefficient of (0.593 ± 0.126) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with scant fibrous stroma (in red). (Sirius red stain; original magnification, x20.)

 
Macroadenomas in the intermediate group appeared inhomogeneous and hyperintense on T2-weighted MR images (Fig 2a) and iso- or hypointense on T1-weighted MR images, and they exhibited marked and, in some cases, inhomogeneous enhancement after administration of gadodiamide. In one patient, a cystic component was observed. In patients with macroadenomas in the intermediate group, tumors appeared hyperintense on DW MR images, and the mean ADC value was (0.842 ± 0.081) x 10–3 mm2/sec (Fig 2b, 2c).


Figure 2
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  		Figure 2a: Macroadenoma with intermediate consistency in 57-year-old man. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous slightly hyperintense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows slightly hyperintense lesion (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with diffusion coefficient similar to that of normal parenchyma, (0.842 ± 0.103) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with relatively conspicuous stromal fibrosis (in red). (Sirius red stain; original magnification, x20.)

 

Figure 2
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  		Figure 2b: Macroadenoma with intermediate consistency in 57-year-old man. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous slightly hyperintense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows slightly hyperintense lesion (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with diffusion coefficient similar to that of normal parenchyma, (0.842 ± 0.103) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with relatively conspicuous stromal fibrosis (in red). (Sirius red stain; original magnification, x20.)

 

Figure 2
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  		Figure 2c: Macroadenoma with intermediate consistency in 57-year-old man. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous slightly hyperintense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows slightly hyperintense lesion (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with diffusion coefficient similar to that of normal parenchyma, (0.842 ± 0.103) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with relatively conspicuous stromal fibrosis (in red). (Sirius red stain; original magnification, x20.)

 

Figure 2
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  		Figure 2d: Macroadenoma with intermediate consistency in 57-year-old man. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous slightly hyperintense pituitary mass (arrows). (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows slightly hyperintense lesion (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with diffusion coefficient similar to that of normal parenchyma, (0.842 ± 0.103) x 10–3 mm2/sec. (d) Specimen of mass at histologic examination shows small cells (in blue) with relatively conspicuous stromal fibrosis (in red). (Sirius red stain; original magnification, x20.)

 
Adenomas in the hard group were inhomogeneous and hyperintense on T2-weighted MR images (Fig 3a) and hypointense on T1-weighted MR images, and they exhibited marked enhancement after intravenous administration of gadopentetate dimeglumine. In one patient in this group, a cystic component that was not included in the ROI analysis was observed. In patients with macroadenomas in the hard group, the tumors were hypointense on DW MR images, and the mean ADC value was (1.363 ± 0.259) x 10–3 mm2/sec (Fig 3b, 3c).


Figure 3
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  		Figure 3a: Macroadenoma with hard consistency in 32-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous hyper- and isointense mass (arrows) with respect to white matter. (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hypointense mass (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with marked increase of diffusion coefficient as compared with that of brain parenchyma, (1.349 ± 0.099) x 10–3 mm2/sec. (d) Specimen at histologic examination shows mass characterized by areas with moderate cellularity (in blue) and little fibrosis (in red) as shown at bottom and areas with abundant fibrous stroma and low cellularity as seen at top. (Sirius red stain; original magnification, x20.)

 

Figure 3
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  		Figure 3b: Macroadenoma with hard consistency in 32-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous hyper- and isointense mass (arrows) with respect to white matter. (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hypointense mass (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with marked increase of diffusion coefficient as compared with that of brain parenchyma, (1.349 ± 0.099) x 10–3 mm2/sec. (d) Specimen at histologic examination shows mass characterized by areas with moderate cellularity (in blue) and little fibrosis (in red) as shown at bottom and areas with abundant fibrous stroma and low cellularity as seen at top. (Sirius red stain; original magnification, x20.)

 

Figure 3
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  		Figure 3c: Macroadenoma with hard consistency in 32-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous hyper- and isointense mass (arrows) with respect to white matter. (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hypointense mass (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with marked increase of diffusion coefficient as compared with that of brain parenchyma, (1.349 ± 0.099) x 10–3 mm2/sec. (d) Specimen at histologic examination shows mass characterized by areas with moderate cellularity (in blue) and little fibrosis (in red) as shown at bottom and areas with abundant fibrous stroma and low cellularity as seen at top. (Sirius red stain; original magnification, x20.)

 

Figure 3
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  		Figure 3d: Macroadenoma with hard consistency in 32-year-old woman. (a) Coronal spin-echo T2-weighted MR image (3000/110) shows large inhomogeneous hyper- and isointense mass (arrows) with respect to white matter. (b) Coronal DW single-shot spin-echo echo-planar MR image (5000/101) with diffusion gradient in three principal orthogonal axes and b values of 0 and 1000 sec/mm2 shows hypointense mass (arrows) with respect to normal white matter. (c) ADC map shows mass (arrows) with marked increase of diffusion coefficient as compared with that of brain parenchyma, (1.349 ± 0.099) x 10–3 mm2/sec. (d) Specimen at histologic examination shows mass characterized by areas with moderate cellularity (in blue) and little fibrosis (in red) as shown at bottom and areas with abundant fibrous stroma and low cellularity as seen at top. (Sirius red stain; original magnification, x20.)

 
Histologic Findings
At histologic examination, all tumors were confirmed to be hormone-negative pituitary adenomas. They exhibited a wide variation in architecture: Some tumors were trabecular or papillary, and others were composed of solid sheets. The cells were mostly polyhedral with spherical euchromatic nuclei. Cytoplasm was abundant and often granulated.

At histologic examination, macroadenomas in the soft group displayed homogeneous morphometric characteristics within and between samples. They exhibited high cellularity and scant fibrous stroma in all cases (Fig 1d). The mean percentage of collagen content in this group was 1.34% ± 1.21.

Histologically, tumors of the intermediate group displayed areas with high cellularity and little or no fibrosis and areas with a relatively conspicuous stromal fibrosis and low cellularity (Fig 2d). The mean percentage of collagen content in this group was 6.89% ± 1.91.

Histologically, the four adenomas in the hard group displayed areas with moderate cellularity and little fibrosis and areas with abundant fibrous stroma and low cellularity (Fig 3d). The mean percentage of collagen content was 7.23% ± 4.80.

Findings at Statistical Analysis
Findings at statistical analysis indicated that the three groups of adenomas, classified according to their consistency at surgery, differed significantly in terms of absolute and relative ADC values (P < .001, Fig 4a) and relative SI on DW MR images (P < .001, Fig 4b) and on T2-weighted MR images (P < .035, Fig 4c). Results of the test of linearity also were significant and showed that the three groups of adenomas, classified according to tumor consistency at surgery, displayed progressively greater absolute and relative ADC values and percentage of collagen content and progressively decreased SI ratios on DW MR images. Results of the test for linearity did not reveal any significant linear relationship between the degree of consistency and SI ratios on T2-weighted MR images. No significant differences were found between mean SI values for macroadenomas on all other conventional MR images across the three tumor consistency groups. As expected, a significant correlation was observed between tumor consistency and the percentage of collagen content (P < .001). A significant correlation also was observed between the percentage of collagen content and both absolute and relative ADC values. Analysis of all other MR parameters did not reveal a significant correlation between them and the percentage of collagen content.


Figure 4
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  		Figure 4a: Box plots show (a) median, interquartile range, and extreme cases of absolute ADC values; (b) SI ratio on DW images; and (c) SI ratio on T2-weighted images in three groups of macroadenomas according to consistency. Significant associations between tumor consistency and ADC values, SI ratio on DW images, and SI ratio on T2-weighted images were observed (P < .05, analysis of variance). A horizontal reference line is drawn at ADC value of 1 mm2/sec, which could be used as a cutoff value to differentiate tumors amenable to aspiration, because of small overlap between ADC values of tumors in the hard versus the soft or intermediate group. ADC values are expressed in squared millimeters per second.

 

Figure 4
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  		Figure 4b: Box plots show (a) median, interquartile range, and extreme cases of absolute ADC values; (b) SI ratio on DW images; and (c) SI ratio on T2-weighted images in three groups of macroadenomas according to consistency. Significant associations between tumor consistency and ADC values, SI ratio on DW images, and SI ratio on T2-weighted images were observed (P < .05, analysis of variance). A horizontal reference line is drawn at ADC value of 1 mm2/sec, which could be used as a cutoff value to differentiate tumors amenable to aspiration, because of small overlap between ADC values of tumors in the hard versus the soft or intermediate group. ADC values are expressed in squared millimeters per second.

 

Figure 4
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  		Figure 4c: Box plots show (a) median, interquartile range, and extreme cases of absolute ADC values; (b) SI ratio on DW images; and (c) SI ratio on T2-weighted images in three groups of macroadenomas according to consistency. Significant associations between tumor consistency and ADC values, SI ratio on DW images, and SI ratio on T2-weighted images were observed (P < .05, analysis of variance). A horizontal reference line is drawn at ADC value of 1 mm2/sec, which could be used as a cutoff value to differentiate tumors amenable to aspiration, because of small overlap between ADC values of tumors in the hard versus the soft or intermediate group. ADC values are expressed in squared millimeters per second.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCE IN KNOWLEDGE
 References
 
Our results suggest that DW MR imaging with generation of ADC maps is a useful imaging method for prediction of consistency of pituitary macroadenomas with respect to tumor resectability with an endoscopic technique.

In this study, we tested both conventional MR imaging and DW imaging for the prediction of consistency of macroadenomas. MR imaging typically depicts a mass arising from the pituitary fossa that is hypointense on T1-weighted MR images and often heterogeneous or hyperintense on T2-weighted MR images (15). We found a correlation between tumor consistency and SI on T2-weighted MR images, and soft tumors displayed a lower SI than did intermediate and hard tumors. Researchers in a previous report described an inverse correlation between SI on T2-weighted MR images and the percentage of collagen content in macroadenomas (10). Although a greater percentage of collagen should account for lower SI on T2-weighted images, this correlation has not been consistently demonstrated. Findings in some reports have indicated no relationship between tumor consistency and SI on conventional MR images (9,11,12). Fibrous tissue in macroadenomas is not the only source of SI on T2-weighted MR images. The discrepancy among findings in previous reports may be explained by the contribution of different tissue components of adenomas to SI on T2-weighted MR images: Fibrous tissue and high cellularity with a low nucleus-to-cytoplasm ratio produce a decrease in SI, whereas extracellular space may cause a large increase in SI on T2-weighted MR images because of an increase in free water (16). These phenomena can contribute differently to SI on T2-weighted MR images and may therefore limit the diagnostic utility of these images for evaluation of fibrous adenomas. We did not find a statistically significant correlation between SI on other conventional MR images or contrast enhancement and tumor consistency (no correlation between SI on T1-weighted images and tumor consistency, SI on T2-weighted images and tumor consistency, and contrast enhancement and tumor consistency). Our results are in agreement with those in previous studies that have suggested that there is no relationship between tumor consistency and SI on T1-weighted MR images and contrast enhancement (9,11,12).

On the other hand, conventional MR images can easily depict cysts and hemorrhages that may be incidentally found in macroadenomas (15). Such macroscopic MR imaging findings may be related to the consistency of macroadenomas: Decreased enhancement after intravenous injection of gadopentetate dimeglumine (observed in one patient in our study) can be considered predictive of a soft consistency of the tumor, most likely because of the presence of colliquation phenomena. In our case study, we found cystic components that were macroscopically visible only in two of 22 patients. Such components were seen on the DW MR images in every case and were easily differentiated from the solid tissue of the adenoma. Therefore, they were eliminated from the ROI, and they did not contribute to SI on the DW MR images.

In our patients, we encountered heterogeneous SI values on DW MR images and ADC maps. During surgery, the majority (>50%) of pituitary macroadenomas were characterized by a soft consistency that allowed complete removal through suction. In this large group of patients, we encountered relatively low ADC values. In the group of patients in whom the neurosurgeons indicated that tumors were of intermediate consistency, we encountered ADC values that were slightly higher with respect to those of the soft group, with some overlapping between the two groups. In these patients, the endoscopic removal of the tumors by using suction was also possible. In the group of four patients who had tumors with a hard consistency, the solid tumors could not be aspirated and therefore were fragmented and excised en bloc; in this group, we encountered ADC values that were significantly higher than those encountered in the other two groups of patients.

The small number of hard tumors in our series did not allow a formal estimation of the most accurate cutoff value for the ADC. In consideration of the correlation between tumor consistency and ADC values and of the small overlap between ADC values for the hard and soft or intermediate groups, however, a cutoff value of 1 mm2/sec could be considered for differentiation of tumors amenable to aspiration. More experience will be needed in this regard.

The capability of diffusion MR imaging to help differentiate SI produced by stationary water molecules from that produced by moving water molecules renders it highly sensitive and specific in the diagnosis of central nervous system diseases, and these diseases include central nervous system tumors (16–28). According to findings in a study (16) on lymphomas and high-grade cerebral tumors and those in other previous studies (13,19–22,25–28), hyperintensity on DW images was correlated with increased cellularity. To our knowledge, no published data concerning consistency of macroadenomas evaluated with DW MR imaging are available. The only report about DW MR imaging for macroadenomas describes two cases of pituitary apoplexy, in which normal DW MR images and ADC maps were obtained in patients with histologically confirmed noninfarcted macroadenomas (29).

One may hypothesize that several mechanisms could explain the differences in ADC values among the three groups of macroadenomas. The phenomena that may favor an increase in ADC values are a reduction in cellularity and an increase in extracellular space, as seen in fibrous adenomas. Phenomena that may have contributed to a reduction in ADC values are an increase in cellularity, a reduction in extracellular space, and a cytoplasmic content with a higher nucleus-to-cytoplasm ratio (16), as seen in soft adenomas.

Support for these hypotheses comes from the results of histologic examinations: Adenomas characterized by a hard consistency at surgery and higher ADC values at MR imaging were more fibrous with smaller cells, whereas adenomas with a soft consistency and lower ADC values had higher cellularity and scant fibrous stroma.

A limitation of our study was the lack of a quantitative analysis of extracellular space and of nucleus-to-cytoplasm ratio; however, tumor removal with suction made it difficult to preserve an intact tissue architecture. Also, because the study sample was small, further studies should include a larger number of patients to validate the potential definition of a threshold value for ADC for tumor resectability by using aspiration.

Our study results indicate that DW MR images can provide information about the consistency of macroadenomas that cannot be reliably obtained with conventional MR techniques. Because addition of DW MR imaging to the examination does not change the examination time substantially, we suggest that it should become part of the routine preoperative examination of patients with macroadenomas. In particular, tumor characterization with DW MR images and ADC maps has a direct relationship with tumor resectability with minimally invasive surgical techniques. Preoperative detection of hard and highly fibrous tumors is important for the planning of the surgical approach and for avoidance of multistage surgical procedures.


   ADVANCE IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
References
 


   FOOTNOTES
 

Abbreviations: ADC = apparent diffusion coefficient • DW = diffusion weighted • ROI = region of interest • SI = signal intensity

Author contributions: Guarantor of integrity of entire study, A. Pierallini; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, A. Pierallini, F.C., C.F., E.T., A. Paonessa, A.B.C., F.B.; clinical studies, all authors; experimental studies, F.B.; statistical analysis, M.F., F.B., S.N., L.F., L.B.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 

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