Abstract
Purpose
This study aimed to investigate the relationship between magnetic resonance image (MRI) features and the immunohistochemical subtypes of pituitary microadenomas (PMAs) characterized by location and growth pattern.
Materials and methods
A double-center, retrospective review of MRI characteristics was conducted in 57 PMA cases recorded from February 2014 to September 2023, identified based on the 2017 World Health Organization classification of pituitary gland tumors. The geometric center of the tumor was defined, and the possibility of PMA vertical or lateral growth patterns was evaluated according to the ratio of maximum diameter between the X and Y axes.
Results
Among the PMAs, somatotroph adenomas (STAs) significantly frequented the lateral-anteroinferior portion of the pituitary gland (P = 0.036). Lactotroph adenomas (LTAs) showed a significant locational preference for the lateral-posteroinferior portion (P = 0.037), and gonadotroph adenomas (GTAs) were predominantly located in the central-anteroinferior portion (P = 0.022). Furthermore, PMAs in the suprasellar portion exhibited vertical extension with statistical significance (P = 0.0).
Conclusion
In our cohort, micro-STAs were predominantly located in the lateral-anteroinferior portion of the pituitary gland, micro-LTAs in the lateral-posteroinferior portion, and micro-GTAs in the central-anteroinferior portion. The growth pattern of PMAs was highly correlated with their vertical position instead of their immunohistochemical subtypes. Therefore, MRI shows potential in differentiating partial PMA subgroups, especially cases within the silent groups.
Introduction
Pituitary adenoma (PA) is a common intracranial tumor in the sellar region that clinically manifests as hormone dysfunction and is responsible for a series of symptoms (1). The diagnosis of PAs currently depends on clinical characteristics, neuroimaging, and endocrinological and immunohistochemical testing (2). Conventional magnetic resonance imaging (MRI) can assess the typical features of tumors in the pituitary gland (PG), such as size, invasion, and location (3, 4).
MRI scans have described the typical morphological features of different PA subtypes (5, 6, 7). Nevertheless, no morphological MRI criteria have been formulated for the immunohistochemical subtypes of pituitary microadenomas (PMAs). To investigate the potential value of conventional MRI in evaluating the immunohistochemical subtypes of PMAs for therapy strategies, we conducted a retrospective study of PMAs using X–Y–Z data for objective criteria.
Materials and methods
Patients
This institutional review was approved by the local ethics committees of Nanyang Central Hospital and The Second Hospital of Jilin University. Data from 1021 patients who were surgically treated for a PA between February 2014 and September 2023 at our institutions were retrospectively reviewed. Among these, 57 patients with histological confirmation of anterior PA, in accordance with the 2017 World Health Organization (WHO) immunohistochemical classification, were selected (1). These cases involved eight null cell adenomas (NCAs), six somatotroph adenomas (STAs), 18 lactotroph adenomas (LTAs), one thyrotroph adenoma (TTA), seven gonadotroph adenomas (GTAs), one corticotroph adenoma (CTA), and 16 plurihormonal adenomas (PHAs).
Inclusion criteria were as follows: patients with PMA admitted for PA resection to control abnormal hormone secretion or tumor mass effects; and preoperative MRI (T1-weighted sequences, contrast-enhanced T1 sequences, and T2-weighted sequences) data available in our hospital. The data were listed in our institution’s database, including baseline data, clinical symptoms, neuroimaging, and endocrinological and immunohistochemical tests. Fifteen patients with complications from other pituitary lesions (craniopharyngioma, Rathke’s cyst, germinoma, meningioma, and lymphocytic hypophysitis) were excluded. Among the 1021 patients surgically treated for a PA in our hospital over the 10-year study period, 57 patients suffering from PMAs were finally selected and included in this study. All baseline characteristics of these patients are summarized in Table 1.
Baseline data and pituitary microadenoma classifications.
| n (range) | % | |
|---|---|---|
| Number of patients | 57 | |
| Age (year) | 41.8 ± 13.4 (16–72) | |
| Gender | ||
| Female | 37 | 64.9 |
| Male | 20 | 35.1 |
| Size (mm) | 8.7 ± 1.2 (6.3–9.9) | |
| Immunopathological subtype | ||
| Null cell adenoma (NCA) | 8 | 14.0 |
| Somatotroph adenoma (STA) | 6 | 10.5 |
| Lactotroph adenoma (LTA) | 18 | 31.6 |
| Thyrotroph adenoma (TTA) | 1 | 1.8 |
| Gonadotroph adenoma (GTA) | 7 | 12.3 |
| Corticotroph adenoma (CTA) | 1 | 1.8 |
| Plurihormonal adenoma (PHA) | 16 | 28.1 |
| Growth pattern | ||
| Vertical extension | 26 | 45.6 |
| Lateral extension | 31 | 54.4 |
Values are expressed as mean ± s.d., median (interquartile range), or number (%).
MRI morphological data acquisition and analysis
Conventional MR images were acquired using a 3.0 T scanner (Tim Trio; Siemens Medical Solutions, Erlangen, Germany) with the following parameters: T1-weighted image (TR/TE, 400/12) and T2-weighted image (TR/TE, 3000/100) in coronal and sagittal scans; field of view, 200 mm × 200 mm; matrix, 256 mm × 192 mm or larger; and layer thickness, 2 mm or smaller. Gadolinium-DTPA was intravenously delivered at a dose of 0.2 mmol/kg.
All neuroimages were independently evaluated by two trained radiologists blinded to the clinical diagnosis and immunohistochemistry. The maximum diameters of the PAs were measured at the greatest dimension several times on the sagittal and coronal scans.
The location criteria for PMAs were as follows: On MR coronal images, the width of the pituitary gland (PG) was measured as the line parallel to the sellar floor, between the bilateral cavernous segments of the internal carotid arteries (8), and the width was divided into three equal parts (lateral and central) (Fig. 1A and B). The direction in which the PG was squeezed, and the degree of pituitary stalk deviation was used as secondary criteria for evaluation. On the Y axis, the PG was measured as the maximum height, perpendicular to the anterior skull base, using cross-sectional areas on the sagittal scan. On the Z axis, the maximum anteroposterior diameter on the sagittal scan was defined as the pituitary length (9). The height and length were divided into two parts, superior/inferior portions (Fig. 1C and D) and anterior/posterior portions (Fig. 1E and F), respectively. The following illustrative positions are shown in Fig. 2: lateral-anterosuperior (LAS), lateral-posterosuperior (LPS), lateral-anteroinferior (LAI), lateral-posteroinferior (LPI), central-anterosuperior (CAS), central-posterosuperior (CPS), central-anteroinferior (CAI), and central-posteroinferior (CPI). The geometric center of a PMA, where the maximum and minimum diameters intersected, was determined and defined as the position of the tumor core. All data are shown in Table 2.
Location of microadenomas in the X, Y, and Z axis. T1-weighted coronal scan with contrast agent (A, B) and T1-weighted sagittal scan with contrast agent (C–F) showing a microadenoma (asterisk). T1-weighted coronal view (A, B), T1-weighted sagittal view (C) showing a lactotroph microadenoma. On the X axis (A, B), the pituitary gland is divided into three parts along the line parallel to the sellar floor between bilateral cavernous segment carotid arteries (arrow). On the Y axis (B, C), the pituitary gland is divided into superior and inferior portions, perpendicular to the anterior skull base (arrows). On the Z axis (E, F), the pituitary gland is divided into anterior and posterior portions, parallel to the anterior skull base (arrows). The geometric center of the microadenoma where the maximum and minimum diameters intersected was defined (asterisk).
Citation: Endocrine Connections 13, 12; 10.1530/EC-24-0378
Distribution of the different microadenomas in the pituitary gland. GTAs predominately situate in central-anteroinferior (D) portion of pituitary gland (P = 0.022), somatotroph adenomas (STAs) are often located in lateral-anterosuperior (B) portion (P = 0.036), and lactotroph adenomas (LTAs) show specific location of lateral-posteroinferior (H) portion with significant difference (P = 0.037). Abbreviations: NCAs, null cell adenoma; STAs, somatotroph adenomas; LTAs, lactotroph adenomas; GTAs, gonadotroph adenomas; PHAs, plurihormonal adenomas; LAS, lateral-anterosuperior (A); LAI, lateral-anteroinferior (B); CAS, central-anterosuperior (C); CAI, central-anteroinferior (D); CPS, central-posterosuperior (E); CPI, central-posteroinferior (F); LPS, lateral-posterosuperior (G); LPI, lateral-posteroinferior (H).
Citation: Endocrine Connections 13, 12; 10.1530/EC-24-0378
The location of different microadenoma subtypes.
| Classification | Location | |||||||
|---|---|---|---|---|---|---|---|---|
| LAS | LPS | LAI | LPI | CAS | CPS | CAI | CPI | |
| NCAs | 2 | 1 | 0 | 0 | 0 | 1 | 3 | 1 |
| STAs | 0 | 0 | 4 | 2 | 0 | 0 | 0 | 0 |
| LTAs | 2 | 1 | 3 | 7 | 0 | 0 | 4 | 1 |
| TTAs | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 |
| GTAs | 0 | 0 | 1 | 0 | 1 | 1 | 4 | 1 |
| CTAs | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 |
| PHAs | 1 | 1 | 5 | 3 | 2 | 1 | 0 | 3 |
CAI, central-anteroinferior; CAS, central-anterosuperior; CPI, central-posteroinferior; CPS, central-posterosuperior; CTAs, corticotroph adenomas; GTAs, gonadotroph adenomas; LAI, lateral-anteroinferior; LAS, lateral-anterosuperior; LPS, lateral-posterosuperior; LPI, lateral-posteroinferior; LTAs, lactotroph adenomas; NCAs, null cell adenomas; PHAs, plurihormonal adenomas; STAs, somatotroph adenomas; TTAs, thyrotroph adenomas..
The growth patterns of PMAs were assessed using the following criteria: vertical extension is considered when the PMA presents suprasellar or infrasellar growth (5, 7), and lateral growth is considered when cavernous sinus invasion is observed (5). Given the possibility of multiple growth directions or small volume, the maximum diameter in the X and Y axes of the PMAs was measured to assess growth pattern on the coronal scan (Fig. 3). A ratio greater than 1 indicates that the PMA tends to extend in a lateral direction; otherwise, the growth is vertical.
Criteria for growth pattern of microadenomas. T1-weighted coronal scan with contrast agent (A, B) showing a microadenoma. (A) The lateral growth pattern of the gonadotroph microadenoma is defined due to the ratio of the width (X) to the length (Y) greater than 1. (B) Vertical growth pattern of the null cell microadenoma is defined due to the ratio of X to Y less than 1.
Citation: Endocrine Connections 13, 12; 10.1530/EC-24-0378
Statistical evaluation
Computer-assisted statistical analyses were performed with IBM SPSS Statistics version 20.0. Chi-square tests or Fisher exact tests were used for the descriptive data analysis of PMA immunohistochemical subgroups in relation to tumor location and growth preference. Sensitivity, specificity, and positive and negative predictive values (SE, SP, PPV, and NPV) were calculated. Differences with an error probability of less than 0.05 on univariate analysis were determined as statistically significant.
Results
Patients’ demographics
The study population included 1021 patients who were immunohistochemically diagnosed with a PMA. In our cohort, 57 patients met the admission criteria, with ages ranging from 16 to 72 years (mean age: 42.4 ± 13.6 years). Of these, 37 were female and 20 were male. The following immunohistochemical PA subtypes based on the 2017 WHO classifications, were used for diagnosis: NCAs (n = 8, 14.0%), STAs (n = 6, 10.5%), LTAs (n = 18, 31.6%), CTAs (n = 1, 1.8%), GTAs (n = 7, 12.3%), TTAs (n = 1, 1.8%), and PHAs (n = 16, 28.1%). The size of the PAs ranged from 6.3 mm to 9.9 mm. The overall average maximum diameter was 8.7 ± 1.2 mm (8.9 ± 1.1 mm in NCAs, 9.1 ± 0.7 mm in STAs, 8.9 ± 1.0 mm in LTAs, 9.1 ± 0.9 mm in GTAs, and 8.3 ± 1.3 mm in PHAs).
Comparison of location among PMA subtypes
All data are shown in Table 2. On the X axis, the PMAs often originated from the lateral portion of PG (n = 35, 61.4%), including 3/8 NCAs, 6/6 STAs, 13/18 LTAs, 1/1 TTAs, 1/7 GTAs, 1/1 CTAs, and 10/16 PHAs. Meanwhile, NCAs (n = 5, 62.5%) and GTAs (n = 6, 85.7%) were frequently observed in the central portion of PG. On the Y axis, the PMAs in the inferior portion of PG accounted for 41/57 (71.9%) of all cases, including 4/8 NCAs, 6/6 STAs, 15/18 LTAs, 1/1 TTAs, 4/7 GTAs, and 11/16 PHAs. Meanwhile, 7/16 tumors in the superior portion of the sellar region were NCAs (n = 4) or GTAs (n = 3). On the Z axis, the PMAs were often located in the anterior portion of PG (n = 33, 57.9%), including 5/8 NCAs, 4/6 STAs, 10/18 LTAs, 1/1 TTAs, 5/7 GTAs, and 8/16 PHAs. As shown in Figs. 3 and 4, the tumors in the PG exhibited distinct locational preferences. Among the confirmed NCAs, two were located in the LAS part and three were found in the CAS portion. STAs frequently originated from the LAI portion of PG (n = 4, SE = 66.7%, SP = 80.4%, PPV = 28.6%, NPV = 95.3%, P = 0.036, Fisher’s exact test). LTAs were frequently located in the LPI portion (n = 7, SE = 38.9%, SP = 87.2%, PPV = 58.3%, NPV = 75.6%, P = 0.037, Chi-square test). GTAs significantly dominated the CAS portion compared with the other PMA subtypes (n = 4, SE = 57.1%, SP = 86.0%, PPV = 36.4%, NPV = 93.5%, P = 0.022, Fisher’s exact test). Although the characteristic distribution was observed for PHAs, many of these tumors were found in the LAI portion of PG (n = 5, 31.3%).
Growth pattern and different microadenoma subtypes. This bar chart shows the distribution of growth patterns within different PMA subtypes.
Citation: Endocrine Connections 13, 12; 10.1530/EC-24-0378
Growth pattern of PMA subtypes
Among the 57 cases with PMAs, 31 exhibited a preference for lateral extension. Their growth was significantly correlated with their vertical position in the PG (P = 0.0) (Table 3). The growth patterns for each PMA subtype were as follows (Table 4): NCAs predominantly showed vertical growth with suprasellar extension (n = 7, 87.5%, SE = 26.9%, SP = 96.8%, PPV = 87.5%, NPV = 61.2%, P = 0.018, Chi-square test), STAs often extended laterally (n = 4, 66.7%), LTAs showed a lateral preference (n = 13, 72.2%), GTAs grew horizontally (n = 5, 71.4%), and PHAs had no specific pattern, though vertical extension was common (n = 9, 56%).
Growth tendency and location of microadenoma.
| Growth tendency | P | ||
|---|---|---|---|
| Vertical | Horizontal | ||
| X axis | |||
| Lateral | 15 (42.9%) | 20 (57.1%) | 0.598 |
| Central | 11 (50.0%) | 11 (50.0%) | |
| Y axis | |||
| Superior | 14 (87.5%) | 2 (12.5%) | 0.0 |
| Inferior | 12 (29.3%) | 29 (70.7%) | |
| Z axis | |||
| Anterior | 14 (42.4%) | 19 (57.6%) | 0.571 |
| Posterior | 12 (50.0%) | 12 (50.0%) | |
Comparison growth pattern among different microadenoma subtypes.
| Classification | Growth tendency | P | |
|---|---|---|---|
| Vertical | Horizontal | ||
| NCAs | 7 (87.5%) | 1 (12.5%) | 0.018 |
| STAs | 2 (33.3%) | 4 (66.7%) | 0.678 |
| LTAs | 5 (27.8%) | 13 (72.2%) | 0.089 |
| TTAs | 0 (0.0%) | 1 (100.0%) | –a |
| GTAs | 2 (28.6%) | 5 (71.4%) | 0.436 |
| CTAs | 1 (100.0%) | 0 (0.0%) | –a |
| PHAs | 9 (56.3%) | 7 (43.7%) | 0.382 |
aStatistical evaluation cannot be available due to too small a number of TTAs and CTAs.
CTAs, corticotroph adenomas; GTAs, gonadotroph adenomas; LTAs, lactotroph adenomas; NCAs, null cell adenomas; PHAs, plurihormonal adenomas; STAs, somatotroph adenomas; TTAs, thyrotroph adenomas.
Discussion
PA, a type of neuroendocrine neoplasm with a series of abnormal hormonal syndromes, is classified based on distinct cell types (10). According to the 2017 WHO classification, five types of cell subtypes in the anterior PG (LTAs, STAs, CTAs, GTAs, and TTAs) (11) are routinely used for PA classifications. MRI can display the characteristic features of different PA subtypes (3, 5, 6, 7, 8, 12); however, a definitive and specific consensus on the MRI criteria for differentiation remains lacking. Bette et al. retrospectively analyzed data from 198 patients with PAs and identified some MRI features for diverse PAs as follows (13): i) STAs exhibited characteristic MRI features, such as intra-/infrasellar extension; and ii) CTAs demonstrated distinct MRI characteristics, such as intrasellar location, small size, and no enlargement of the sellar region. Macroadenomas and giant adenomas, which obscure the delineation of the PG and complicate the locational analysis, were also considered in the study. In another cohort of 54 cases validated as functional PAs, the following correlations were observed between the location and subtype of PAs (5): i) LTAs were frequently located in the lateral part of PG, ii) ATCH-secreting PAs were typically clustered in the medial part of the PG, and iii) STAs were predominantly found in the lower part of the sellar region. These studies summarized the common locations and growth patterns linked to the PA subtypes, providing valuable information for predicting PA types and managing these tumors. However, most studies combined data on both micro- and macroadenomas. In addition, a consensus for PMAs is lacking. Therefore, the classification of PAs based on MRI remains a challenge. Additional assessments with valuable data are needed for accurate diagnosis. The criteria for locational assessment vary across studies, contributing to ambiguity. Building on previous findings, we analyzed the MRI features of different PMA subtypes and identified key morphological characteristics using X–Y–Z axis data. The findings will assist radiologists in more objectively and precisely detecting and diagnosing PMAs and will support potential databases for artificial intelligence.
In clinical practice, identifying which tumors in the silent group are positive for immunoreactive hormone and which among the NCAs are immunonegative for hormonal markers is difficult without immunohistochemistry (14). In our cohort, micro-GTAs exhibited a significant locational preference for the CAI portion. Meanwhile, the NCAs showed a significant tendency for vertical growth extension compared to the other PMA subtypes. This result could serve as a criterion for differentiating silent GTAs from other nonfunctional or asymptomatic silent PAs and NCAs. Furthermore, micro-STAs significantly originated from the LAI portion, which is consistent with findings from another study (7). Although LTAs were distributed throughout the PG (15, 16), many micro-LTAs were found predominantly in the LPI part with statistical significance. This result aligns with previous research indicating that LTAs were more frequently located in the lateral portion of the sellar region compared to the other subtypes (5). Given the small number of cases, especially CTAs and TTAs with only one case of each, the sensitivity and specificity are insufficient, making it difficult to draw firm conclusions about PMA classification based on these MRI features. However, some preliminary and relatively clear conclusions can still be drawn from this study. Despite the limitations, these findings provide valuable assistance to radiologists in identifying difficult-to-detect PMAs and offer potential insights for the radiological diagnosis of PMA subtypes.
Most studies assessed the growth direction according to the descriptive features of the suprasellar or infrasellar extension (6, 7, 10); however, this criterion is not ideal for PMAs, as their small size makes it difficult to identify their predominant intrasellar extension. Due to different growth rates, the abundance of PAs varies across different directions (17). Here, we defined the extension preference based on the basis of the width/height ratio of PMAs on the coronal scans, which provides an objective and quantifiable parameter. The PMA in the superior part of the PG demonstrated a tendency for vertical growth, accompanied by the local hump of the diaphragma sellae over a period of time. Micro-NCAs in the superior portion showed a statistically significant preference for vertical extension. Therefore, the growth pattern was highly correlated with the position of PMAs and slightly related to the histology of cell types. This finding contrasts with previous reports (5, 6). Tumor extension is influenced by adjacent structures, including the sellar floor or diaphragma sellae (18). Invasive growth is observed with the progression of pituitary tumor development (19, 20, 21, 22). We hypothesized that cases located in the superior portion warrant special attention due to their preference for vertical extension, which could potentially compress the optic chiasm at an early stage. Additionally, visual field examinations should be conducted in patients with PMAs in the superior part of the PG, particularly during pregnancy, when adenomas may enlarge in response to physiological changes (23).
Our study has several limitations. One limitation is its retrospective design. Medical treatment is the first-line strategy to control abnormal hormonal symptoms as a result of PMA in clinical practice. Instead of random selection, we selected patients who underwent resection to preserve pituitary tissue and control abnormal hormones for our cohort. All cases were recorded from a double center, and the number of certain types of PAs, such as TTAs and CTAs, was extremely small to provide informative value. Additionally, our focus was on PMAs, and cavernous sinus invasion could not be assessed due to the small size of the PAs.
Conclusion
In conclusion, associations were observed between the imaging characteristics and subtypes of PMAs. In our cohort, micro-STAs were predominantly located in the LAI portion of the PG, micro-LTAs in the LPI portion, and micro-GTAs in the CAI portion. The growth pattern of PMAs was highly correlated with their vertical position instead of their immunohistochemical cell types. Owing to the low sensitivity and specificity of PMA morphological characteristics, MRI should be used for differential diagnosis rather than for confirming tumor subtypes.
Declaration of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.
Funding
The present study was funded by 2019 Nanyang City Science and Technology Research Projects (Grant no. KJGG154) and Henan Province Science and Technology Research Projects (Grant no. 242102311136).
Data availability statement
All data generated or analyzed during this study are included in this published article.
Author contributions statement
Guarantor of integrity of entire study: PX; HW. Study concepts: LZ, HW. Study design: SY; HW. Literature research: HL. Clinical studies: SX; HL; YL. Data acquisition: YW; HW. Statistical analysis: LZ; SX; YL. Manuscript preparation: LZ; SY; SX. All authors contributed to the article and approved the submitted version.
Acknowledgements
We did not receive any third-party support in conducting this research, analyzing the data, or preparing the manuscript for submission. We thank Dr Jia-yin Li and Dr Zong-ao Yu from the Radiology department of Nanyang Central Hospital for their contributions to imaging diagnosis and recognition.
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