VARIABLE THYROID-STIMULATING HORMONE DYNAMICS IN SILENT THYROTROPH ADENOMAS
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1 Case Report VRILE THYROID-STIMULTING HORMONE DYNMICS IN SILENT THYROTROPH DENOMS Nigel Glynn, M 1 ; nne Marie Hannon, M 1 ; Michael Farrell, MD 2 ; Francesca rett, MD 2 ; Mohsen Javadpour, MD 3 ; mar gha, MD 1 STRCT Objective: Pituitary adenomas that produce thyroidstimulating hormone (TSH) are typically accompanied by hyperthyroxinemia and a non-suppressed or elevated TSH at diagnosis. Occasionally, patients with this type of tumor have normal thyroid function test results, a condition termed silent thyrotroph adenomas. This report characterizes TSH dynamics in this rare pituitary tumor subtype. Methods: We report 2 cases of pituitary macroadenoma associated with visual failure and hypopituitarism. The patients had normal thyroid function test results but the adenoma was intensely immunopositive for β-tsh expression. The results of TSH dynamics are reported for both cases. Results: Preoperative assessment did not reveal any clinical or biochemical evidence of pituitary hormone excess save mild, asymptomatic hyperprolactinemia consistent with pituitary stalk compression. In particular, thyroid function test results were within normal ranges. In both cases, each patient s vision recovered following transsphenoidal surgery. Histological analysis confirmed pituitary adenoma with extensive immunopositivity for TSH and the complete absence of immunostaining for all other anterior pituitary hormones. Following surgery, thyroid function test results were again normal. Surveillance Submitted for publication May 26, 2015 ccepted for publication July 7, 2015 From the Departments of 1 Endocrinology, 2 Neuropathology, and 3 Neurosurgery, eaumont Hospital and Royal College Surgeons in Ireland Medical School, Dublin, Ireland. ddress correspondence to Dr. mar gha, Department of Endocrinology, eaumont Hospital, Dublin 9, Ireland. amaragha@beaumont.ie. DOI: /EP15841.CR To purchase reprints of this article, please visit: magnetic resonance imaging performed 6 months postoperatively showed the presence of an intrasellar tumor remnant. postoperative thyrotropin-releasing hormone test yielded a discordant, dynamic TSH response that was normal in one patient but was abnormal and flat in the second patient. Conclusion: TSH dynamics in silent thyrotroph adenomas are variable. It is not known whether the biochemical behavior of the tumor may be indicative of its natural history or response to treatment. (CE Clinical Case Rep. 2016;2:e155-e160) bbreviations: CTH = adrenocorticotrophic hormone; GH = growth hormone; T4 = thyroxine; TRH = thyrotropin-releasing hormone; TSH = thyroid-stimulating hormone INTRODUCTION Thyroid-stimulating hormone (TSH)-secreting pituitary adenomas (thyrotroph adenomas or TSHomas) account for 1 to 2% of all pituitary adenomas (1). Most patients present with pressure effects related to the tumor and they usually exhibit overt or subclinical thyrotoxicosis. iochemical analysis typically reveals hyperthyroxinemia with a non-suppressed or elevated TSH concentration. dynamic TSH response to a variety of stimuli is often useful in differentiating between a TSHoma and other diseases that can produce the same baseline biochemistry. In particular, TSHomas characteristically display blunted TSH stimulation in response to thyrotropin-releasing hormone (TRH). This biochemical phenotype facilitates a preoperative diagnosis in most cases of TSH-secreting pituitary adenoma. Occasionally, patients with this tumor have normal thyroid function test results. This condition is termed a silent thyrotroph adenoma. The natural history and TSH CE CLINICL CSE REPORTS Vol 2 No. 2 Spring 2016 e155
2 e156 Silent TSHoma, CE Clinical Case Rep. 2016;2(No. 2) dynamics in such tumors are not well described. We present 2 cases of a silent thyrotroph macroadenoma that exhibited variable TSH dynamics. CSE 1 31-year-old female reported an 8 month history of visual disturbance and secondary amenorrhoea. visual field assessment confirmed bilateral superior quadrantanopia. Magnetic resonance imaging revealed a partially cystic, suprasellar pituitary tumor (Fig. 1 ). Her serum prolactin concentration was normal and she displayed no clinical features of acromegaly or Cushing s syndrome. She was clinically euthyroid without a goiter. The results of baseline thyroid function tests (performed at another hospital) were normal, with free thyroxine (T4) 1.17 (range, 0.69 to 1.46 ) and TSH 0.65 mu/l (range, 0.35 to 4.94 mu/l) concentrations within normal ranges. Following endoscopic trans-sphenoidal debulking, histological analysis confirmed pituitary adenoma with extensive cytoplasmic immunopositivity for the β subunit of TSH (β-tsh): 100% of cells stained positive for β-tsh in some parts of the adenoma, with an average immunoreactivity rate of 50% in the tumor overall. There was a complete absence of immunostaining for all other anterior pituitary hormones (Fig. 2). Postoperative assessment revealed partial growth hormone (GH) and adrenocorticotrophic hormone (CTH) deficiency. The peak GH concentration and cortisol response to insulin-induced hypoglycemia were mu/l (3.77 µg/l) and µg/dl, respectively (normal response >15 mu/l [5 µg/l] and >18.1 µg/dl, respectively). Her menses resumed and thyroid function test results were again normal, with normal concentrations of TSH (1.64 mu/l, normal range 0.5 to 4.2 mu/l), free T4 (0.85, normal range 0.54 to 1.24 ), and total T3 (114, normal range 65 to 195 ). Surveillance magnetic resonance imaging performed 6 months postoperatively showed an intrasellar tumor remnant invading the cavernous sinus (Fig. 1 ). TRH test performed at this time yielded a normal dynamic TSH response, with a rise in TSH at 20 minutes followed by a fall at 60 minutes (Table 1). The a subunit/tsh molar ratio was within normal limits at 2.6 (pre-menopausal range, 0.4 to 5.5). surveillance magnetic resonance imaging scan performed 18 months postoperatively showed no evidence of recurrence. CSE 2 78-year-old female complaining of long-standing fatigue was found to have euvolemic hyponatremia, with a serum sodium concentration of 122 mmol/l, urea 16.8 mg/ Fig. 1., Preoperative coronal magnetic resonance image of a suprasellar pituitary tumor compressing the optic chiasm., Postoperative coronal magnetic resonance image showing the intrasellar tumor remnant with deviation of the pituitary stalk and the decompressed optic chiasm.
3 Silent TSHoma, CE Clinical Case Rep. 2016;2(No. 2) e157 Fig. 2., Pituitary tumor tissue showing a densely cellular neoplasm composed of cells with eosinophilic granular cytoplasm and small central nuclei (hematoxylin and eosin stain)., Most tumor cells (>80%) were immunoreactive for β-thyroid-stimulating hormone expression. Tumor cells did not show any immunopositivity for other anterior pituitary hormones. bbreviations: CTH = adrenocorticotrophic hormone; FSH = follicle-stimulating hormone; HGH = human growth hormone; LH = luteinizing hormone; PRO = prolactin Postoperative minute TSH mu/l Table 1 Thyrotropin-Releasing Hormone Test Case 1 Case 2 ft4 TT3 SU µg/l TSH mu/l ft4 TT SU µg/l bbreviations: SU = alpha subunit; ft4 = free thyroxine; TSH = thyroid-stimulating hormone; TT3 = total triiodothyronine. Reference ranges: SU, adult (male and female) <1 µg/l; menopause and mid-cycle <3 µg/l; TSH, 0.5 to 4.2 mu/l; ft4, 0.54 to 1.24 ; TT3, 65 to 195. dl, and creatinine 0.69 mg/dl. Subsequent investigations confirmed CTH deficiency, with an early morning cortisol concentration of 3.84 µg/dl and non-elevated CTH. Magnetic resonance imaging demonstrated a pituitary macroadenoma that was distorting the optic chiasm (Fig. 3 ). Her serum prolactin concentration was modestly elevated (49.9 ng/ml), gonadotrophins were low, and insulin-like growth factor-1 was at the lower end of the reference range at 43 μg/l (range, 39 to 168 µg/l). She did not have a goiter and her thyroid function test results were normal: free T (range, 0.54 to 1.24 ) and TSH 1.73 mu/l (range, 0.5 to 4.2 mu/l). Her hyponatremia resolved with physiological glucocorticoid replacement. n examination revealed a bitemporal superior quadrantanopia. However, her vision recovered following endoscopic transsphenoidal tumor resection. Histological analysis confirmed the lesion was a pituitary adenoma with intense immunostaining for β-tsh (Fig. 4). The tumor showed no immunopositivity for any other pituitary hormones. postoperative glucagon test confirmed persistent CTH deficiency, with basal and peak cortisol concentrations of 6.56 μg/dl and 12.7 μg/dl, respectively (peak
4 e158 Silent TSHoma, CE Clinical Case Rep. 2016;2(No. 2) Fig. 3., Preoperative, non-contrast coronal magnetic resonance image showing a pituitary macroadenoma displacing the optic chiasm., Postoperative magnetic resonance image showing decompression of the optic chiasm but residual tumor present in the sella turcica. Fig. 4., Pituitary tumor tissue showing a cellular neoplasm composed of cells with small central nuclei (hematoxylin and eosin stain)., Immunostaining for β-thyroid-stimulating hormone was positive in most (>80%) tumor cells. Immunoreactivity for other pituitary hormones was not evident.
5 Silent TSHoma, CE Clinical Case Rep. 2016;2(No. 2) e159 cortisol threshold 16 μg/dl) (2). Her prolactin concentration declined to 29.6 ng/ml, but her gonadotrophin concentrations remained low, with follicle-stimulating hormone at 6.7 U/L, luteinizing hormone at 2.5 U/L. The patient continued on physiological hydrocortisone replacement. Her thyroid function test results were again normal at TSH 2.04 mu/l, free T4 0.96, total triiodothyronine 97.4, and free triiodothyronine 214 pg/dl (range, 168 to 402 pg/dl). Serum a subunit was not elevated at 2.05 μg/l (reference range, <3 μg/l) and her a subunit/ TSH molar ratio was within normal limits at 8.96 (postmenopausal range, 1.7 to 29.1). Surveillance magnetic resonance imaging performed 6 months postoperatively showed an intrasellar tumor remnant (Fig. 3 ). subsequent, postoperative TRH test yielded an abnormal, flat response (Table 1). The tumor remnant remained stable on a subsequent scan performed 1 year later. DISCUSSION We report 2 cases of pituitary macroadenomas with strong immunopositivity for β-tsh but no clinical or biochemical evidence of excess TSH secretion preoperatively. oth patients had associated visual compromise. However, their vision recovered following endoscopic trans-sphenoidal tumor debulking. Despite a persistent postoperative tumor remnant, their thyroid functions remained normal and both patients were clinically euthyroid. However, a TRH test revealed discordant TSH dynamics, with a normal response in 1 patient but a flat abnormal response in the other. recent European epidemiological study estimated that the annual incidence of functioning TSHomas was 0.15 per million inhabitants (3). These tumors have traditionally been regarded as aggressive, with a requirement for multimodality therapy. This perception is supported by Malchiodi et al., who retrospectively reviewed the experience of 2 institutions that treated TSHomas over a 30 year period (4). Data collected from 70 patients showed that 70% of cases were macroadenomas, with 75% of this group showing suprasellar extension, and all patients had abnormal TSH dynamics. Surgery was the mainstay of treatment for most patients, but medical therapy was used in over half of patients and 27% of patients required external beam radiotherapy. Irrespective of thyroid function, immunopositivity for β-tsh may be found in up to 13% of pituitary adenoma specimens (5). However, in most cases only a small number of tumor cells (<20%) stain positive for TSH. Circumstances where more than 50% of cells express TSH are typically in the context of plurihormonal immunoreactivity for other glycoprotein hormones and GH (5). It is estimated that approximately 16% of tumors have clinical and/or biochemical evidence of GH co-secretion and 10% of tumors secrete a mixture of TSH and prolactin (1). Normal thyroid function tests are rarely reported in the presence of intense tumor immunopositivity for β-tsh alone. Furthermore, TSH dynamics are deranged in the presence of this tumor: over 90% of secretory macro TSHomas exhibit a less than 1.5-fold rise in serum TSH in response to TRH stimulation (1). Tritos et al. reported a consecutive series of 166 patients with pituitary adenomas whose tumors demonstrated β-tsh immunoreactivity (5). Surprisingly, only 26% of patients with >20% tumor cells immunoreactive for β-tsh had biochemical evidence of thyrotropin-dependent hyperthyroidism. However, approximately 90% were also immunoreactive for β-follicle-stimulating hormone and/or β-luteinizing hormone. In addition, 20% of these patients had acromegaly, with their tumors predominantly regarded as somatotroph adenomas. TSH dynamics were not evaluated in this series. In a recent series of 32 patients with pituitary tumors expressing TSH treated at a single ritish institution, the patients were divided into those with and without clinical evidence of hyperthyroidism at presentation (6). However, although it is evident that many patients in the clinically euthyroid group had biochemical hyperthyroxinemia, it is not clear if any of them had normal thyroid function tests. Wang et al. reported 9 silent thyrotroph adenomas from 2 institutions over 26 years (7). However, the series only included 1 patient in whose tumor >50% of the cells were immunopositive for β-tsh alone. ll other cases had moderate-to-weak TSH immunostaining or showed plurihormonal staining. When compared with 20 concurrent secretory TSHomas from the same institutions, the silent tumor was larger than the functioning adenomas. Cellular structure, analyzed by electron microscopy, was consistent with thyrotroph cells, regardless of secretory status. TSH dynamics were not reported in either series. In silent thyrotroph adenomas, the tumor cells may not be manufacturing the α subunit and therefore are unable to form the intact glycoprotein dimers required for TSH biological activity. lternatively, the tumor cells may not possess the intracellular machinery required to bring about degranulation of TSH secretory vesicles. Silent corticotroph adenomas are more common than thyrotroph adenomas and have been shown to exhibit a variety of defects in pituitary hormone processing, including incomplete cleavage of the prohormone (8). Furthermore, secretion of insufficient or biologically inactive forms of CTH has been described in clinically silent corticotroph adenomas (8). Defects at different stages of hormone processing, secretion, and immunological activity may explain the divergent response to TRH seen in both of the cases described here. Immunopositivity for other anterior pituitary hormones such as CTH and GH in clinically and biochemically nonfunctional pituitary tumors may be associated with a higher risk of recurrence and a need for multimodal treatment.
6 e160 Silent TSHoma, CE Clinical Case Rep. 2016;2(No. 2) However, it is not known whether the strong β-tsh immunoreactivity in clinically silent adenomas confers a similarly poor prognosis. lso, it remains to be seen whether the abnormal TSH dynamics of silent thyrotroph adenomas are predictive of a higher risk of recurrence or responsiveness to medical treatments such as somatostatin analogues. DISCLOSURE This project received no funding and the authors have no conflict of interest to declare. REFERENCES 1. eck-peccoz P, Persani L, Mannavola D, Campi I. Pituitary tumours: TSH-secreting adenomas. est Pract Res Clin Endocrinol Metab. 2009;23: gha, Rogers, Sherlock M, et al. nterior pituitary dysfunction in survivors of traumatic brain injury. J Clin Endocrinol Metab. 2004;89: Ónnestam L, erinder K, urman P, et al. National incidence and prevalence of TSH-secreting pituitary adenomas in Sweden. J Clin Endocrinol Metab. 2013;98: Malchiodi E, Profka E, Ferrante E, et al. Thyrotropinsecreting pituitary adenomas: outcome of pituitary surgery and irradiation. J Clin Endocrinol Metab. 2014;99: Tritos N, Eppakayala S, Swearingen, et al. Pathologic and clinical features of pituitary adenomas showing TSH immunoreactivity. Pituitary. 2013;16: Kirkman M, Jaunmuktane Z, randner S, Khan, Powell M, aldeweg SE. ctive and Silent Thyroid- Stimulating Hormone-Expressing Pituitary denomas: Presenting Symptoms, Treatment, Outcomes, and Recurrence. World Neurosurg. 2014;82: Wang EL, Qian ZR, Yamada S, et al. Clinicopathological characterization of TSH-producing adenomas: special reference to TSH-immunoreactive but clinically non-functioning adenomas. Endocr Pathol. 2009;20: Kojima Y, Suzuki S, Yamamura K, Ohhashi G, Yamamoto I. Comparison of CTH secretion in Cushing s adenoma and clinically silent corticotroph adenoma by cell immunoblot assay. Endocr J. 2002;49:
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