CLINICALLY SILENT ACTH CROOKE S CELL ADENOMA PRESENTING AS UNILATERAL EAR PAIN
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1 AACE Clinical Case Reports Rapid Electronic Articles in Press Rapid Electronic Articles in Press are preprinted manuscripts that have been reviewed and accepted for publication, but have yet to be edited, typeset and finalized. This version of the manuscript will be replaced with the final, published version after it has been published in the print edition of the journal. The final, published version may differ from this proof. Case Report ACCR CLINICALLY SILENT ACTH CROOKE S CELL ADENOMA PRESENTING AS UNILATERAL EAR PAIN Krish J. Khatri MD 1 ; Pedram Javanmard MD 2 ; Joshua D. Miller MD, MPH 3 ; Puneet S. Pawha MD 4 Running Title: Clinically Silent ACTH Crooke s Cell Adenoma From: 1 Department of Medicine, Stony Brook University Hospital; 2 Division of Endocrinology Diabetes and Bone Disease, Icahn School of Medicine at Mount Sinai; 3 Department of Endocrinology and Metabolism, Stony Brook University Hospital; 4 Division of Neuroradiology, Icahn School of Medicine at Mount Sinai. Corresponding address: Dr. Krish J. Khatri 460 Old Town Road, Apt 5A, Port Jefferson Station, NY, Krish.khatri@stonybrookmedicine.edu Acknowledgements: 1) Mary Fowkes, MD, PhD, Director of Neuropathology and Autopsy Service with Department of Pathology, Icahn School of Medicine at Mount Sinai for providing images of pathology slides and stains.
2 ABSTRACT BACKGROUND Crooke s cell adenoma is a rare tumor of the anterior pituitary. It is highly aggressive and carries significant morbidity and mortality(1, 2). This report will focus on the presentation of this disease process and review diagnosis and treatment. CASE Patient is a 64-year-old male with a history of resected pituitary adenoma of unknown pathology. He underwent serial MRI surveillance for numerous years without recurrence of tumor, however eventually developed symptoms of worsening left ear pain over three weeks that rapidly evolved to include ptosis. Imaging revealed a new pituitary macroadenoma. Urgent surgical resection revealed histopathological diagnosis of Crooke s Cell Adenoma. DISCUSSION Corticotroph adenomas represent a rare subset of pituitary tumors. Clinically silent pituitary tumors demonstrate relatively higher rates of cavernous sinus invasion(30% vs. 18%) and progression/recurrence(34% vs. 6%) when compared to non-functioning adenomas(5). In Crooke s Cell Adenoma, only 65% of patients have clinical features of Cushing s disease at presentation(1). Twenty-four hour urinary free cortisol is discussed in the literature as a potential tool, where a value four times the upper limit of normal was predictive of higher risk of having Crooke s cell changes(7). With a recurrence rate of up to 60%, multi-modal treatment(surgery and radiation) is preferred.
3 CONCLUSION This case highlights early detection and treatment as keys to preventing significant morbidity and mortality. Currently, there are limited tools for identifying patients who are high risk for developing Crooke s cell changes. Treatment modalities classically include surgery and radiotherapy. Adjuvant and novel chemotherapies are being explored. KEY WORDS 1) Crooke s cell adenoma 2) Pituitary adenomas 3) ACTH tumor 4) Cushing s disease Abbreviations: MRI = Magnetic Resonance Imaging; ACTH = Adrenocorticotropic Hormone; DDAVP = Desmopressin; MIB1 = Mindbomb E3 Ubiquitin Protein Ligase 1; CAM5.2 = Anti-Cytokeratin antibody; MGMT = O-6-methylguanine-DNA methyltransferase Introduction Crooke s cell adenoma is a rare, corticotrophic tumor of the anterior pituitary. It is highly aggressive, with approximately 60% recurrence rate, and carries significant morbidity and mortality[1, 2]. Interestingly, only about 65% of patients have clinical features of Cushing s disease at presentation, with the remainder associated with clinically silent tumors[1]. The wide range of nonspecific symptoms creates a challenging condition to diagnose. Our case pertains to a middle-aged male with chief complaint of ear pain that evolved in a matter of weeks to include
4 ptosis of the left eyelid. After further investigation and surgical resection, the histopathological diagnosis of Crooke s Cell Adenoma was confirmed. This report will focus on the importance of early detection and highlight potential tools to aid in diagnosis. Additionally, we will discuss current treatment modalities that are available. Case Presentation Patient is a 64-year-old male who presented with three weeks of worsening left ear pain, left sided headache, and tinnitus. He had a significant history of a pituitary macroadenoma(unknown pathology or size), status post transsphenoidal resection in early 2000s. The patient reported that the mass at the time was an incidental finding on trauma imaging after a motor vehicle accident. After surgery, the patient developed partial hypopituitarism(diabetes insipidus and hypogonadism-treated with DDAVP and testosterone replacement, respectively). The patient underwent MRI surveillance without recurrence of the tumor. History is also significant for wellcontrolled type two diabetes mellitus, managed with oral agents and insulin therapy. The patient was in his usual state of health until approximately two years after the last surveillance MRI when he developed gradually worsening left ear pain, left sided headache, and tinnitus. The pain was persistent in nature and tinnitus was characterized as intermittent. These symptoms evolved over a three-week period to include ptosis of the left eye. Soon after he was diagnosed with third nerve palsy, he completed urgent brain MRI(Figure 3) which revealed a new 2.6 by 3.2 by 2.1 centimeter pituitary macroadenoma. Radiographic description of the tumor included invasion of the both cavernous sinuses, left greater than right, and growth around bilateral internal carotid arteries(knosp grade 4, bilaterally) without narrowing. However, there
5 was no optic chiasm involvement. The patient had no overt Cushingoid changes to suggest hypercortisolism however pre-operative laboratory wok revealed elevated serum ACTH level of 131 picogram/milliliter(reference range 7-69 pg/ml) and elevated AM serum cortisol 40.0 micrograms/deciliter(reference range mcg/dl). Prolactin level was 0.9 nanograms/milliliter(reference range ng/ml). He was started urgently on oral dexamethasone 4 milligrams every six hours given the suspicion for pituitary apoplexy and underwent transsphenoidal resection of the tumor. Intraoperatively, the adenoma was localized and was notable for necrotic features. On histopathology, the tumor was found to be an ACTH positive(70%, Figure 1) Crooke s Cell adenoma with Ki-67/MIB1 labeling index of less than three percent, low p53(1%). The pathology had strong CAM5.2 positivity with ring-like displacement of the granular cytoplasm which is characteristic of Crooke s cell changes(figure 2). Furthermore, there were focal areas of pallor suggesting necrosis, which was consistent with pituitary apoplexy. At the 3-month postoperative visit, follow-up MRI(Figure 4) showed postsurgical changes with residual enhancement in both cavernous sinuses and inferiorly along the posterior sphenoid sinus and clivus. Serum ACTH level at that time was found to be elevated at picograms/milliliter(7am sample, reference range: pg/ml). Concurrent serum cortisol measurement was within normal limits at 9.7 micrograms/deciliter(7am sample, reference range: mcg/dl). He was then referred to radiation oncology for further treatment where he is planned to receive stereotactic radio surgery to the site via intensity modulated radiation therapy in 28 fractions for total of 5040 centigray.
6 Discussion ACTH-secreting adenomas comprise about 10 15% of all pituitary adenomas[4]. Corticotropic adenomas can be classified as functional, nonfunctioning, or silent, with silent defined as clinically and biochemically unapparent adenomas[4]. Patients with silent tumors often do not present with cushingoid features[5]. Incidence varies between 3-19% of the tumors that were classified pre-operatively as non-functioning [4]. Due to the paucity of reported silent tumors, there is limited data and understanding of the disease process. Silent tumors, however, tend to demonstrate relatively higher rates of cavernous sinus invasion(30% versus 18%) and progression/recurrence(34% versus 6%) when compared to non-functioning adenomas[5]. They classically presents in three different histopathological subtypes: densely granulated corticotroph(most common), sparsely granulated corticotroph, and Crooke s cell adenoma[3]. Arthur Crooke, who described the substantial hyalinization of the cytoplasmic granules that occurred in the anterior pituitary cells, first discovered Crooke s cell changes in London in Crooke s cell adenoma remains a rare disease entity with an incidence rate which is incompletely established[2]. Despite being an ACTH positive tumor on staining, Crooke s cell adenoma is only associated with clinically evident Cushing s disease in about 65% of patients, with the remainder accounting for silent tumors[1]. Depending on the growth rate and secretory function of the tumors, the clinical changes from hormone release may or may not be evident at presentation. Our patient had evidence of a functional tumor given the elevated ACTH and cortisol levels pre-operatively, however the clinical changes expected with hypercortisolism were not apparent.
7 Pituitary macroadenomas can present with varying localizing symptoms including: headache(50%), extraocular motor palsies(13%), and visual deficits(61%)[6]. With Crooke s cell adenomas, mass-effect symptoms seem to arise first[1]. Our case demonstrates the aggressive nature of this type of adenoma, as the patient had stable post-operative surveillance of his previous pituitary tumor until the growth exhibited mass effect onto surrounding tissues relatively quickly. One limitation of the report is that we were unable to obtain the records for the original tumor, however given the stability of the surveillance MRIs for over a decade, it was unlikely to be of the same pathological subtype. Rather, this was more likely a transformation of the cell line. The diagnosis of Crooke s cell adenoma is purely histopathological: characteristic accumulation of hyaline material in the cytoplasm is present in more than 50% of cells[3]. Variation in biochemical activity and only moderate association with phenotypic changes expected from hypercortisolism creates a diagnostic dilemma how to identify factors that place patient s at higher risk of developing the tumor. Interestingly, one potential tool is to measure the degree of hypercortisolism[7]. Oldfield et. al. studied 213 patients who underwent resection of pituitary tumor with a pre-operative diagnosis of Cushing s disease. 174 patients had ACTH positive pituitary adenomas by pathology and 81% of those exhibited Crooke s cell changes[7] The study utilized 24 hour urinary free cortisol, where a value four times the upper limit of normal was predictive of higher risk of having Crooke s cell changes.
8 Recurrence rates can be in excess of 60%,[1, 2] thus a multi-modal treatment approach is usually preferred. The first step involves surgical intervention, usually with transsphenoidal resection followed by external radiation usually via stereotactic radiosurgery[4]. Close post-therapy monitoring for new or worsening hypopituitarism is warranted. In our patient, although his symptoms related to mass-effects had resolved after surgery, the presence of residual tumor is concerning. Thus, stereotactic radiosurgery was the next step in his treatment. Adjunctive chemotherapy has also been investigated. Temozolomide was trialed as a chemotherapy agent for tumors with low or absent MGMT immunostaining[4]. Asimakopoulou, et al reviewed Temozolomide therapy and correlation with long term remission rates[8]. The report included individual patients in which the agent was used as adjuvant treatment for refractory cases of Crooke s cell adenoma which had suboptimal response to surgery and radiation. Two of the three patients achieved sustained response to Temozolomide, with one patient in complete remission at eighteen months. Given that only a handful of patients have been trialed on Temozolomide with mixed results, data for its utility and efficacy in Crooke s is overall limited[8]. Conclusion Crooke s cell adenoma remains a rare, yet highly clinically significant disease process with limited data on outcomes and prognosis. The case described above is one of few with this pathophysiology and testify to the importance of early detection, treatment, and close follow-up as keys to preventing significant morbidity and mortality. Currently, there are limited tools for identifying patients who are high risk for developing Crooke s cell changes. Treatment modalities classically include surgery and radiotherapy however adjuvant and novel chemotherapies are being explored.
9 References 1. George DH, Scheithauer BW, Kovacs K, et al. Crooke's cell adenoma of the pituitary: an aggressive variant of corticotroph adenoma. Am J Surg Pathol. 2003;27: Kovacs K, Diep CC, Horvath E, et al. Prognostic indicators in an aggressive pituitary Crooke's cell adenoma. Can J Neurol Sci. 2005;32: Cooper O. Silent corticotroph adenomas. Pituitary. 2015;18: Jahangiri A, Wagner JR, Pekmezci M, et al. A comprehensive long-term retrospective analysis of silent corticotrophic adenomas vs hormone-negative adenomas. Neurosurgery. 2013;73:8-17; discussion Syro LV, Rotondo F, Ramirez A, et al. Progress in the Diagnosis and Classification of Pituitary Adenomas. Front Endocrinol (Lausanne). 2015;6: Scheithauer BW, Jaap AJ, Horvath E, et al. Clinically silent corticotroph tumors of the pituitary gland. Neurosurgery. 2000;47:723-9; discussion E 7. Oldfield EH, Vance ML, Louis RG, Pledger CL, Jane JA, Jr., Lopes MB. Crooke's Changes In Cushing's Syndrome Depends on Degree of Hypercortisolism and Individual Susceptibility. J Clin Endocrinol Metab. 2015;100: Asimakopoulou A, Tzanela M, Koletti A, Kontogeorgos G, Tsagarakis S. Long-term remission in an aggressive Crooke cell adenoma of the pituitary, 18 months after discontinuation of treatment with temozolomide. Clin Case Rep. 2014;2:1-3.
10 FIGURES Figure 1: ACTH stain with brown signifying positivity(20x Magnification) Figure 2: Hematoxylin and eosin stain showing hyperproliferative neoplastic cells with abundant pink cytoplasm consistent with Crooke s cell changes(40x Magnification) Figure 3: Pre-op images. Pre-contrast (a) and post-contrast (b) sagittal T1-weighted images demonstrate a large expansile enhancing sellar mass eroding inferiorly into the clivus and sphenoid sinus. Coronal (c) postcontrast T1-weighted images and coronal T2-weighted image (d) demonstrate encasement of the cavernous internal carotid arteries (Knosp grade 4 bilaterally), more pronounced on the left where is prominent lateral bulging of the cavernous sinus. Note the ICA flow voids are not narrowed. Rightward deviation of the infundibulum is present (c). Note the growth is predominantly inferior and lateral, without significant suprasellar extension. Figure 4: 3 month post-op images. Coronal T2-weighted image(a) shows partial resection of the tumor, with residual noted inferiorly and also laterally within the cavernous sinuses. Sagittal non-contrast T1-weighted image(b) demonstrates T1 hyperintense fat packing in the sellar region, and T1 hypointense residual tumor inferiorly involving the sphenoid sinus and eroding the clivus.
11 Fig 1 Fig 2
12 Fig 3 Fig 4
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