High-resolution magnetic resonance imaging at 3T of pituitary gland: advantages and pitfalls

Introduction

Magnetic resonance imaging (MRI) is an accurate diagnostic tool with a primary indication in several condition both for a diagnostic and interventional intent (1-14). Notably, MRI has been established as dominant modality use in neuroradiological field due to its excellent soft tissue contrast (15-28), which allowed an accurate evaluation of intracranial structures. This characteristic proves to be particularly advantageous in the study of pituitary gland; MRI, indeed, provide a detailed depiction of the pituitary anatomy and its relationship with adjacent structures, helping from the detection of micro alteration of its architecture to the formulation of an adequate treatment planning. In this scenario, computed tomography (CT) take often only a complementary role in the study of pituitary gland, due to its lower soft tissue resolution than MR (11,29-35), useful therefore in identifying the presence of calcification, bony destruction, and surgically relevant bony anatomy (36-41). The purpose of this article is to review the state of the art of high-resolution MRI of the pituitary gland at 3 Tesla (3T), with a particular focus on the main benefits and the possible limitations of higher field imaging.

Anatomy and function of the pituitary gland

The hypophysis or pituitary gland lies in the sella turcica, a cup-shaped depression within the sphenoid bone. The pituitary gland is connected via the pituitary stalk to the hypothalamus which is a thin plate of tissue making up the floor of the anterior part of the 3rd ventricle.

The pituitary gland is formed by two distinct lobes, the anterior one known as adenohypophysis, and a posterior one kwon as neurohypophysis. Each lobe had a distinct embryological origin, considering that the anterior lobe forms from an invagination of the oral ectoderm known as Rathke’s pouch and the posterior lobe develops from a protrusion of the neural ectoderm of the diencephalon.

The adenohypophysis is formed by three parts: pars tuberalis, pars intermedia and pars distalis. Different cell types are involved in hormones production, all involved in specific hormonal circuit which makes the adenohypophysis crucial in central regulation of several bodily function.

The neurohypophysis is divided into three parts: the posterior hypophysial (neural) lobe, the infundibular stem, and the median eminence. The posterior pituitary does not directly synthesize any hormones but instead releases some hormones synthesized in the hypothalamus and then released by exocytosis in the neural lobe. The functional state of the neural lobe is thus highly dependent upon the integrity of the pituitary stalk and hypothalamus (42).

Between the anterior and posterior lobes lies an intermediate lobe which is vestigial and known as the pars intermedia. This is a potential site for small non-functional Rathke’s cyst (43). On both side of pituitary fossa there are the cavernous system, an anatomic compartment through which the internal carotid arteries enter the base, as well as the III, IV, VI cranial nerves, and first and second branches of the V cranial nerve exit the skull.

MRI technique and imaging protocol

MR protocol study requires sagittal and coronal planes, both in thin sections (2 or 3 mm), focused on the pituitary. It is necessary to perform T1-weighted sequences before and after administration of intravenous contrast. Coronal T2-weighted sequences can add some information, but they result less sensitive in the assessing of adenomas. Plans are obtained with specific orientations. The sagittal plane should be oriented parallel to the bi-hemispheric line from a coronal plane. The coronal plane is obtained from a sagittal plane, parallel to the hypophyseal pedicle (Figure 1). It is important to perform post-contrast MR sequences in a dynamic modality (within 40–50 seconds after contrast injection there is a homogenous enhancement of the gland). In this way it is possible to highlight adenomas, as they typically enhance less than the normal pituitary tissue, due to the presence of hypophyseal portal system, and this differential enhancement is sometimes best appreciated within the first arterial phase of the contrast injection. Most of the pituitary adenomas, on the contrary, receive a direct extra portal arterial supply. In the majority of cases, however, lesions are adequately demonstrated on a standard acquisition (non-dynamic) after contrast administration (44).

Figure 1 Sagittal T1 multi echo multiplanar (MEMP) spin-echo (SE), 3 mm slice thickness sequence (A) at 3T showing normal anatomy of the pituitary gland. Coronal 3D T1 fast spoiled gradient echo (FSPGR) 1 mm slice thickness sequence (B) after intravenous administration of gadolinium showing optimal visualization of the pituitary stalk and homogenous parenchymal enhancement.

Microadenomas (diameter <1 cm) can be detected with additional dynamic sagittal plane images to the routine coronal planes (Figure 2) (45). Dynamic contrast MRI also has an equally important role in studying macroadenomas (diameter ≥1 cm) (Figure 3), in cases of possible invasion of the cavernous sinus, and in assessing residual/recurrent tumor from postoperative tissues (46). Some microadenomas exhibit maximum lesion-to-gland contrast on unenhanced scan; however, this image contrast begins to diminish the moment the contrast-enhancing agent arrives in the pituitary gland. It is important to remind that the pituitary gland, pituitary stalk and cavernous sinuses are all vascular structures which enhance after gadolinium injection, the optic chiasm and hypothalamus, on the other hand, do not show enhancement if the blood-brain barrier is intact.

Figure 2 Coronal T1 spin-echo (SE) sequence after dynamic contrast enhancement at 3T scanner showing a 3 mm area of delayed enhancement in the left portion of adenohypophysis, consistent with microadenoma.

Figure 3 Sagittal T1 multi echo multiplanar (MEMP) spin-echo (SE) 3 mm slice thickness sequence (A) and coronal T1 MEMP SE 3 mm slice thickness (B) at 3T scanner, both performed after administration of contrast medium, showing inhomogeneous solid mass involving sellar and suprasellar region causing mild displacement of optic chiasm, likely referable to macroadenoma.

Higher resolution pituitary images can be provided by the use of high field strength 3T MR scanners. 3T MRI, thanks to a higher magnetic field than 1.5 Tesla (1.5T) allows to improve image quality and spatial resolution, which are fundamental especially in evaluating subtle differences between normal and abnormal tissue. The superiority of high field scanner at 3T MRI to 1.5T have been demonstrated in several studies.

Kim et al. (47) showed that preoperative localization of pituitary microadenomas in Cushing’s disease is better with 3T MRI compared to 1.5T MRI, although some of these lesions were missed.

They conducted a preliminary study, depicting how 3T MRI can be useful in the evaluation algorithm for Cushing’s disease, amplifying radiographic differences when a subtle imaging abnormality exists. If MRI at 3T plays a central role in the clinical diagnostic field, it revealed to be more accurate than 1.5T also in neurosurgical procedures and gamma knife, stereotactic radiosurgery (SRS) or stereotactic radiotherapy (SRT) planning.

Pinker et al. (48) conducted a study assessing the value of high-field MRI for both diagnosis and surgery of sellar lesions, predicting tumor invasion through the medial cavernous sinus border.

In another study, Fahlbusch and Buchfelder (49) observed that up to 10% of pituitary adenomas infiltrate into parasellar spaces. To assess parasellar spaces invasion is fundamental in surgery planning, as it represents the most common limiting factor in the resection of pituitary adenomas; standard field 1.5T MRI rarely allows to delineate the medial limit of the cavernous sinus and the possible extension into the parasellar spaces. High field 3T MRI scan has been found to be superior to conventional MR units in delineation of parasellar anatomy (Figure 4), defining medial cavernous sinus border. What is more, 3T MRI offers a better depiction of the intracavernous cranial nerves and optic chiasm. Satogami et al. used high resolution MRI at 3T to evaluate the normal pituitary stalk in detail, thereby providing a standard for size of the normal pituitary stalk. It is fundamental starting from the knowledge of the normal imaging appearance of the pituitary stalk in order to make an accurate diagnosis of pituitary infundibular lesions. On high-resolution T2-weighted images, pituitary stalk is characterized by a central hyperintensity and a peripheral rim of isointensity which may represent the infundibular stem and pars tuberalis respectively (50).

Figure 4 Axial T1 fat-suppressed fast spoiled gradient echo (FSPGR) 1 mm slice thickness sequence after administration of contrast medium at 3T scanner, showing pathological enhancement involving right orbital apex and anterior aspect of ipsilateral cavernous sinus, encasing the intracanalicular portion of optic nerve. A case of Tolosa-Hunt syndrome.

Magnetization transfer (MT) imaging is a recent technique that can play a central role in evaluating preoperative and postoperative pituitary adenomas in patients with hyperprolactinemia. In fact, in this imaging modality, the tissue contrast depends mainly on the concentration of macromolecules and quantified by the MT ratio (MTR). Thanks to this modality, it is possible to make difference between prolactin-secreting adenomas and the non-secreting ones. This technique is also important in post-operative assessment and follow-up of patients with pituitary adenomas, as an increased MTR is strongly suggestive of a residual tumor, even if standard MR results negative (51).

Diffusion-weighted imaging (DWI) and apparent diffusion coefficient (ADC) maps result crucial in defining tumor component and consistency. Describing tissue characteristics is important, as a soft microadenoma should be easily removed with a minimally invasive endoscopic trans-sphenoidal access, avoiding invasive surgery; on the other hand, 10% of macroadenomas presenting a high percentage of fibrosis needs a surgical invasive approach. In this scenario it is easily to understand how the definition of macroadenomas consistency plays a central role in planning an adequate surgical technique for resection. Several studies attempted to predict adenoma consistency by using conventional and some novel MRI sequences with controversial results, especially regarding DWI. In fact, this sequence has shown utility in assessing the consistency of adenomas (52-54), but with no convincing data, due to the B₀ related artifacts in the sellar region (55-57). Yiping et al. (58) used the BLADE DWI sequence to acquire ADC values, which reduced artefacts in the sellar region and enhanced the accuracy of signal. BLADE DWI is a turbo spin echo-based diffusion-weighted technique that can oversample the region in the centre on the k-space to correct for heterogeneities prior to combing data. Using this approach they revealed that ADC ratio decreased with increasing collagen content and predicted hard consistency of tumors for ADC <1.077.

Proton magnetic resonance spectroscopy (1H-MRS) is a MR-based technique able to measure concentrations of different metabolites in the cerebral parenchima, widely used for differentiating neoplastic from non-neoplastic pathology. In fact this method allows to define tumor type, grade, proliferation and to predict therapeutic sensitivity and prognosis in different central nervous system pathologies (59). The application of 1H-MRS in the sellar region is found as a diagnostic tool in the evaluation of sellar and parasellar neoplasms. It has been shown that hypothalamic gliomas, for example, are defined by increased choline and decreased N-acetyl aspartate peaks, while pituitary adenomas may show only an increase of choline peak or no metabolites if there is an intramural haemorrhage, as iron ions of hemosiderin lead to worsened homogeneity of the magnetic field (60). Hypothalamic hamartomas show decreased N-acetyl aspartate and increased myo-inositol compared to grey matter (61). Craniopharyngiomas and germinomas are defined by a dominant lipid peak (62,63). Hu et al. enhanced the capability of 1H-MRS in predicting the pathological subtype and somatostatin receptor 2 (SSTR2) expression of growth hormone-secreting pituitary adenomas (GH-PAs). In fact, the best medical treatment of acromegaly after surgery is somatostatin analogs (SSAs); however, one-third of patients show some degree of resistance to SSA treatment. In this scenario, it is crucial to identify factors that could be related to resistance to SSA therapy. 1H-MRS may be a useful, non-invasive method to predict tumor subtype and SSTR2 expression. One of the best predictors, among the several parameters of MRS, is considered to be the choline/creatine (Ch/Cr) ratio. This value has revealed to be consistent with others reported predictors of SSA response, such as T2 signal intensity and the Ki-67 value. MRS could have also a role in predicting subtype in cases of isointense T2 signals. In this way, MRS could represent a potentially novel and non-invasive method to predict the response to SSAs in patients with GH pituitary macroadenomas (64).

Another field in which 3T MRI scan showed to be fundamental is the intraoperative navigation.

Wolfsberger et al. (65) decided to do intraoperative navigation guided combining 3T MR images with CT scans; in this case, CT scans plays a role during trans-sphenoidal approach to depict the nasal bone structures, while 3T MRI scans result particularly useful to explore parasellar tumor extension during microsurgical and/or endoscopic resection. Nakazawa et al. (66) determined how 3T is superior to 1.5T for sellar lesions with small pituitary tumors; 3T is better than 1.5T to differentiate tumor and normal tissue in SRS and SRT planning of pituitary tumors. What is more, they showed that for both field strengths, three dimensional-fast spoiled gradients recalled acquisition in the steady state (3D-FSPGR) enabled the high-resolution acquisition, and two-dimensional spin-echo (SE) T1-weighted (2D-T1W1) and 2D-fluid-attenuated inversion recovery (FLAIR) were able to well enhance tissue contrast (66).

Pitfalls

Although the cited benefits, the high magnetic field of 3T scanner is related to some limits which is mandatory to take into account for a comprehensive evaluation of 3T pituitary study.

It is well known, indeed, that susceptibility effects increase with higher B₀, as well as artifacts related to vascular flow and patient movement are more pronounced and sometimes may outweigh the benefits, even 3T shows an increased capability in the detection of microbleeds in vascular encephalopathy.

Besides, problems with specific absorption ratio (SAR) limitations are correlated with an increase in field strength. Although even small reductions of the flip angle lead to significant SAR decreases, flip angle reductions may cause a reduction in signal intensity, limiting the gain from higher fields. The use of gradient echo sequences is a valuable alternative, even if these sequences are prone to susceptibility artifacts which limit their use (67).

Lastly, grey-to-white matter contrast is reduced in SE T1 imaging at 3T when compared to 1.5T, since T1 times of grey and white matter lengthen and converge at higher fields. Inversion recovery sequences provide a superior grey-to-white matter contrast but, on the other hand, enhancing lesions may not be visible. Therefore, these sequences are not quite useful for comparative pre- and postcontrast imaging, regardless of B₀ (68).

Conclusions

MRI represent the mainstay imaging modality nowadays in the evaluation of both pituitary gland and sellar and parasellar structures thanks to its excellent contrast resolution and the possibility to obtain a dynamic evaluation of contrast enhancement within the pituitary tissue, which represents a critical factor in the detection of pituitary adenomas.

High field 3T-MRI, despite some limitations, mainly regarding increased SAR exposure, changes in T1 relaxation times and susceptibility effects, can provide several advantages over 1.5T scanners, ranging from a higher spatial resolution to the possibility of acquiring dedicated MRI sequences (e.g., BLADE DWI sequences). Also, 3T-MRI enables a more accurate evaluation of important parameters of pituitary adenomas such as composition and consistency and provides crucial elements helping in the differential diagnosis of a wide range of neoplasms which may affect sellar and parasellar region thanks to MRS applications.

Acknowledgments

None.

Footnote

Conflicts of Interest: The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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