ACUTE SEVERE CUSHING SYNDROME: NOT ALWAYS ECTOPIC ACTH SYNDROME
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1 Case Report ACUTE SEVERE CUSHING SYNDROME: NOT ALWAYS ECTOPIC ACTH SYNDROME Carlos Tavares Bello, MD 1 ; Inês Gil, MD 2 ; Filipa Alves Serra, MD 3 ; João Sequeira Duarte 1 ABSTRACT Objective: Cushing syndrome (CS) is a rare disease that results from prolonged supraphysiologic tissue action of glucocorticoids. Cushing disease is the most frequent cause of endogenous CS and is associated with increased morbidity and mortality. Disease onset and severity reflects the magnitude of cortisol excess, and ectopic adrenocorticotropic hormone (ACTH) syndrome is the most frequent cause of acute, severe CS. Cushing disease tends to have a slower onset with gradual appearance of the typical phenotype and associated metabolic consequences. Methods: Case report and review of the literature. Results: A 62-year-old man was admitted for altered mental status, severe hyperglycemia, and refractory hypokalemia. Despite clinical and biochemical presentation being suggestive of ectopic ACTH secretion, an ACTH-secreting pituitary adenoma was the underlying cause. Endoscopic transsphenoidal tumor excision led to disease remission. Submitted for publication April 9, 2017 Accepted for publication May 9, 2017 From the 1 Department of Endocrinology Hospital de Egas Moniz, Centro Hospitalar de Lisboa Ocidental, Lisboa, Portugal, 2 Department of Neuroradiology, Centro Hospitalar de Lisboa Ocidental, Lisboa, Portugal, and 3 Department of Endocrinology, Hospital das Forças Armadas, Lisboa, Portugal. Address correspondence to Dr. Carlos Tavares Bello, Hospital de Egas Moniz, Centro Hospitalar de Lisboa Ocidental, Rua Da Junqueira 126, , Lisboa, Portugal. bello.carlos04@gmail.com. DOI: /EP CR To purchase reprints of this article, please visit: Conclusion: The case is noteworthy for the atypical clinical presentation, severity of the hypokalemia, and excellent treatment outcome. The biochemical testing has limitations, and these should be kept in mind in the investigation of hypercortisolism. (AACE Clinical Case Rep. 2018;4:e45-e50) Abbreviations: ACTH = adrenocorticotropic hormone; CD = Cushing disease; CS = Cushing syndrome; CT = computed tomography; EAS = ectopic ACTH secretion; MRI = magnetic resonance imaging INTRODUCTION Cushing disease (CD) is the most frequent cause of endogenous Cushing syndrome (CS). It is characterized by an autonomous secretion of cortisol secondary to an underlying pituitary adenoma. Pituitary adenomas are thought to affect 10.6% of the population, mostly undiagnosed and asymptomatic, and among these, up to 13.8% may be adrenocorticotropic hormone (ACTH)-secreting (1,2). CD is more common in female patients and has the highest incidence during the fourth decade of life. Lesions smaller than 1 cm (microadenomas) are more frequent than invasive lesions at the time of diagnosis. Patients with CD often exhibit numerous clinical and laboratory abnormalities. The prolonged supraphysiologic tissue action of glucocorticoids is believed to underlie the majority of the consequences of CS. As glucocorticoids are major contraregulatory hormones in carbohydrate metabolism, glucose intolerance and diabetes mellitus are, as expected, common features, affecting up to 50% of CS patients. Some authors consider this to be an underestimation, as no standardized strategies to screen hyperglycemia AACE CLINICAL CASE REPORTS Vol 4 No. 1 January/February 2018 e45
2 e46 Nonectopic Severe Cushing, AACE Clinical Case Rep. 2018;4(No. 1) in CS have been established (3). Diabetes screening by means of fasting blood glucose levels fails to diagnose a significant portion of patients that have predominant postprandial hyperglycemia. For screening purposes, either the oral glucose tolerance test and/or glycated hemoglobin are considered far more sensitive (4). Furthermore, hypokalemic metabolic alkalosis is not so frequent in CS, being present in up to 15% of cases (5). Although CD remains the most frequent cause of endogenous hypercortisolism, acute, severe clinical presentations are more typical of ectopic ACTH secretion. This presentation may be explained by the fact that disease onset and severity reflect on how high and how fast cortisol levels have risen; in ectopic ACTH secretion, cortisol secretion is far more extreme than in any other CS subtype (6). The authors report on a case of a patient that presented with severe hyperglycemia and refractory hypokalemic metabolic alkalosis that upon investigation was compatible with CD. In the case reports that have described a similar presenting clinical picture, the underlying cause was always ectopic ACTH secretion (7-10). The diagnosis of CD was unexpected; therefore, we believe that this case report is noteworthy. CASE REPORT A 62-year-old man with a past medical history of obesity and hypertension, without any previous medication, was admitted to the emergency department with altered mental status, polyuria, polydipsia, irritability, easy bruising, and proximal muscle weakness of sudden onset. Complaints were progressive and had begun 1 month prior to hospital admission. On admission, physical examination was remarkable for normal blood pressure, slight dehydration, obesity (body mass index 31.2 kg/m 2 ), moon face, echymoses on the upper limbs, and proximal muscle weakness. There was no peripheral edema, striae, or evidence of congestive heart failure. Neurologically, the patient was disoriented in time and space, and he also had slurred speech. At admission, plasma glucose was 452 mg/dl (25 mmol/l), serum potassium 2.7 mmol/l, arterial ph 7.6, and bicarbonate 50 mmol/l, without evidence of underlying infection (unremarkable complete blood count and C-reactive protein levels). Electrocardiogram revealed no changes typical of hypokalemia. A head computed tomography (CT) showed no evidence of cerebral ischemia or hemorrhage but did reveal an ill-defined sellar mass. The patient was admitted to the medical ward, where intravenous fluids were administered, and a subcutaneous, intensive insulin regimen with glargine and lispro was started. After a transient clinical improvement, the patient developed peripheral edema, orthopnea, and fatigue, along with pulmonary rales, jugular venous distension, arterial hypertension, and an elevated brain natriuretic peptide. Echocardiogram showed left ventricular concentric hypertrophy, diastolic dysfunction, without regional wall motion abnormalities suggestive of ischemia. Acute congestive heart failure was diagnosed, and intravenous diuretics (furosemide 60 mg/day) were administered. Diuretic dose was soon downtitrated due to rapid clinical improvement; however, on the third day of diuretic therapy, laboratory tests documented severe hypokalemia (1.5 mmol/l). Furosemide was stopped, and intravenous potassium supplementation was given. High doses of potassium supplements were needed for correction of the hypokalemia and maintenance of normokalemia. An average maintenance dose of 100 meq/day of potassium chloride was required even after the introduction of spironolactone. When his clinical status stabilized, further investigation revealed ACTH-dependent hypercortisolism and hypercortisolism-induced suppression of thyroid-stimulating hormone, follicle-stimulating hormone, luteinizing hormone, and growth hormone (Table 1). Despite biochemical evidence of ACTH-dependent hypercortisolism and the identification of a sellar mass, the severity of the clinical picture led to further investigations aiming to exclude ectopic ACTH syndrome. A 48-hour, 8-mg dexamethasone suppression test documented a rise in plasma cortisol values (20.3 to 38.3 µg/dl), and inferior petrosal venous sinus sampling revealed baseline and stimulated inferior petrosal sinus to peripheral ACTH ratios of 1.46 and 1.5, respectively. Due to clinical and biochemical suggestion of ectopic ACTH syndrome, Octreoscan followed by CT of the chest, abdomen, and pelvis were performed, both evidencing no relevant changes. Due to the initial CT suggestion of a sellar mass, cranial magnetic resonance imaging (MRI) was performed, revealing a right-sided sellar expansive lesion with suprasellar and right cavernous sinus extension measuring 22 mm maximum diameter. It had a heterogeneous texture with multifocal hypersignaling areas in T1-weighted images (Fig. 1). Despite biochemical evidence suggestive of ectopic ACTH syndrome, the only positive imaging finding was the invasive pituitary adenoma. The patient underwent endoscopic transsphenoidal tumor excision, with pre-operative preparation with metyrapone. Postoperatively, the patient developed transient diabetes insipidus. Intra- and postoperative hormone supplementation with glucocorticoids was prescribed. Potassium supplements were tapered over 7 days after surgery, with rapid potassium level normalization. Hydrocortisone dose was also progressively tapered, and clinical benefits regarding mental status, hyperglycemia, and hypertension were rapidly evident over a 4-week period. Blood and urinary free cortisol and plasma ACTH soon normalized after surgery (postoperative day 7, plasma cortisol 11.1 µg/dl; ACTH, 10.4 pg/ ml) while on oral hydrocortisone replacement therapy. Histology report was a pituitary adenoma without cellular atypia or mitosis. Immunohistochemistry was positive for
3 Nonectopic Severe Cushing, AACE Clinical Case Rep. 2018;4(No. 1) e47 Baseline values 1 mg dexamethasone suppression test (DST) Table 1 Patient s Laboratory Investigation Parameter Value Reference range Morning plasma cortisol µg/dl 24-h urinary free cortisol 12, µg/day ACTH 121 <46 pg/ml Renin activity ng/ml/hour Aldosterone <1.1 <22 ng/dl Spot urinary potassium mg/dl Concomitant serum potassium mmol/l TSH µu/l Free T pmol/l Prolactin 9.1 <19 ng/ml FSH < U/L LH < U/L Total testosterone ng/dl IGF ng/ml Cortisol after DST 18.6 <1.8 µg/dl 48-hour 8 mg DST Cortisol: basal post DST 100% a Suggestive of ectopic ACTH syndrome Abbreviations: ACTH = adrenocorticotropic hormone; FSH = follicle-stimulating hormone; IGF-1 = insulin-like growth factor 1; LH = luteinizing hormone; T4 = thyroxine; TSH = thyroidstimulating hormone. a Cortisol levels increased from 18.9 to 38.5 µg/dl after the 48-hour 8 mg DST. Fig. 1. Magnetic resonance imaging presurgery. There is a lesion that expands mainly the right side of the sella turcica with invasion of the posterior region of the right cavernous sinus (red arrow). Fig. 2. Magnetic resonance imaging presurgery showing lesion that expands mainly the right side of sella turcica with invasion of posterior region of right cavernous sinus (red arrow) and spontaneous high signal in T1-weighted images (white arrowheads) demonstrating recent hemorrhagic component.
4 e48 Nonectopic Severe Cushing, AACE Clinical Case Rep. 2018;4(No. 1) ACTH, and the Ki67 index was 1%. Postoperative MRI (6 months) showed a residual lesion of 10 mm that was stable 1 year after the operation (Figs. 3 and 4). Eighteen months after surgery, the patient has no complaints, his Cushingoid phenotype has ameliorated, and he remains on physiologic doses of hydrocortisone (15 mg/day) and metformin monotherapy, with adequate glycemic control. DISCUSSION CS is characterized by a constellation of signs and symptoms that develop due to excessive, prolonged tissue exposure to inappropriate high glucocorticoid levels. The majority of cases are attributable to exogenous corticosteroid use (iatrogenic CS). Endogenous Cushing is far less common, with an estimated incidence of 0.7 to 2.4 per million population. It may be etiologically divided into ACTH-dependent (80 to 85% of cases) and ACTHindependent disease (3). CD accounts for 75 to 80% of ACTH-dependent CS cases, is more prevalent in females, and has the highest incidence in the fourth decade. The source of excessive circulating cortisol is usually an ACTH-secreting pituitary microadenoma (<1 cm). Ectopic ACTH syndrome (EAS) is less common, being responsible for 15 to 20% of endogenous CS cases. It is more frequent in males and occurs later than CD. Excessive ACTH tends to be produced by an extrapituitary tumor such as pulmonary (45% of all EAS cases: bronchial carcinoid, pulmonary small cell or adenocarcinoma), thymic (11%), and gastrointestinal neuroendocrine tumors (5%), islet cell tumors (8%), medullary thyroid carcinomas (6%), and pheochromocytomas (5%). Epithelial neoplasms may also be associated with EAS; however, they are far less frequent (6). Adrenal CS, on the other hand, is the most frequent cause of CS in the pediatric age group. Rare causes of CS include corticotropinreleasing hormone secreting neoplasms and cyclic CS (3). Clinical presentation of CS will vary according to gender, age, underlying cause, duration and severity of hypercortisolism, and the rapidity of biochemical glucocorticoid rise. Men usually present at a younger age with a more severe clinical manifestations, such as violaceous striae, muscle weakness, osteoporosis, and urolithiasis (3). Obesity, hypogonadism, and psychiatric and cognitive dysfunction are highly prevalent in both genders (3). Metabolic complications are also common, namely, hypertension in 70 to 80%, glucose intolerance in 45 to 70%, hypercholesterolemia in 70%, and osteoporosis in 50 to 80%. Hypokalemic metabolic alkalosis affects mostly EAS patients (90% vs. 10 to 15% in CD) (3). According to etiology, circulating cortisol levels are usually higher in patients with EAS, explaining the rapid onset (over 1 month) and severity of the clinical picture in these cases. EAS secondary to more indolent tumors may be clinically indistinguishable from CD, in which the classical clinical and metabolic abnormalities of CS are of gradual onset (over months to years) (9). Diagnosis relies on confirmation of autonomous cortisol secretion with different tests: 1 mg and low-dose dexamethasone suppression * Fig. 3. Magnetic resonance imaging 6 months after surgery. There is lesion reduction, being substituted by multiple cysts with high signal in T2-weighted images (white arrow). The lesion has lobulated borders and peripheral contrast enhancement. The supra-sellar cistern (asterisk) is more permeable due to the reduction of the pituitary adenoma. Left deviation of pituitary stalk (red arrow) persists. These features may correspond to postsurgical changes or presence of residual lesion. Fig. 4. Magnetic resonance imaging 6 months after surgery. There is lesion reduction (9 10 mm), with peripheral enhancement (white arrowheads) in T1-weighted images and lobulated margins. The suprasellar cistern (asterisk) is more permeable due to the reduction of the pituitary adenoma. Left deviation of pituitary stalk (red arrow) persists. These features may correspond to postsurgical changes or presence of residual lesion.
5 Nonectopic Severe Cushing, AACE Clinical Case Rep. 2018;4(No. 1) e49 test, midnight salivary cortisol, 24-hour urinary free cortisol, and cortisol rhythm. After establishing the diagnosis, establishing the cause is the next step and includes ACTH measurement. If ACTH is elevated, additional tests are needed to distinguish CD from EAS (8 mg dexamethasone suppression test [overnight or 48-hour] and inferior petrosal sinus sampling), and according to the findings, cranial MRI or nuclear imaging (Octreoscan, 68 Ga-DOTATATE), respectively, may be warranted. ACTH levels below 5 pg/ ml warrant adrenal imaging, and if needed, genetic testing (Carney complex, PRKAR1A, ARM5) (10). First-line therapy is almost always surgical. Transsphenoidal surgery in CD is associated with relapse in 20% of patients, while adrenal causes are often curable, with an excellent prognosis in benign disease. EAS, on the other hand, is difficult to manage, since most of the ACTH-secreting neoplasms are already metastasized at the time of diagnosis and may require either medical therapy or bilateral adrenalectomy. Corticosteroid cover is required during and for some time after surgery, since long-term hypercortisolism suppresses both nonadenoma corticotrophes (ACTH-dependent cases) and the healthy adrenal (unilateral ACTH-independent causes). This longterm suppression leads to a temporary adrenal stunning that requires time to full functional recovery. Physiologic glucocorticoid replacement may be required for more than 1 year after surgery. Pituitary radiotherapy may be an option if there is residual tumor after surgery. Its effects are delayed for years and usually require medical therapy until the radiotherapy has an effect. Medical therapy is only indicated as pre-operative preparation in patients with contra-indications to surgery, relapsed and occult disease cases, and as a bridge to the effects of radiotherapy. Pharmacologic options include ketoconazole, metyrapone, mitotane, etomidate, mifepristone, pasireotide, and cabergoline. Most of the agents have a poor side effect profile, and since some are adrenolytic, may warrant concomitant glucocorticoid supplementation (3). The reported case illustrates an acute, severe presentation of CS, which would usually be suggestive of an ectopic ACTH source; however, the absence of an identifiable extrapituitary tumor along with the presence of a pituitary macroadenoma led to a clinical dilemma. On the one hand, the adenoma appeared to be invasive and was the probable cause the hypopituitarism, therefore favoring a surgical indication. On the other hand, incidental pituitary adenomas are present in 10.6% of the population, and the macroadenoma could have been just an incidentaloma, if not for the concomitant hypopituitarism, since the clinical and biochemical picture were both highly suggestive of EAS. From this case, it is clear that pituitary adenomas can also give rise to florid CS presentations. The reason behind the acute presentation is not clear. The large tumor size, along with the low mitotic index, could suggest that the adenoma was not rapidly growing. No typical clinical data of long-term subclinical Cushing suggest a previously undiagnosed CD that suddenly progressed. The tumor was probably an inefficient secreting neoplasm that for unknown reasons suddenly became hormonally active. The authors speculate that beyond tumor mass and mitotic index, other mechanisms might be at play, namely, proopiomelanocortin processing and/or ACTH packaging defects. A few case reports (mostly affecting women before the seventh decade) have described silent macroadenoma progression to florid CS; however, clinical evidence data are still scarce for this seemingly distinct clinical entity (11). After establishing the diagnosis of CS, the etiologic diagnostic strategies also have some limitations. The 8 mg dexamethasone suppression test relies on the principle that pituitary adenoma ACTH secretion is sensitive to prolonged extremely high doses of exogenous glucocorticoids. However, the failure to suppress cortisol secretion after high-dose dexamethasone (to less than 50% of baseline cortisol concentration) has been shown to have poor accuracy, sensitivity, and specificity (76.5, 79.3, and 66.7%, respectively) in the differentiation between CD and EAS. Furthermore, pituitary ACTH-secreting macroadenomas, compared with microadenomas, are often less suppressible in dynamic testing, possibly explaining some of the unexpected biochemical results (12). Inferior petrosal sinus sampling also has limitations, most of which are of technical character. This approach requires the expertise of a high-volume center, as the imprecise placement of the central catheters may be a significant source of error (13). In the reported case, the clinical and biochemical response to pituitary surgery are highly suggestive of underlying CD. If clinical or biochemical evidence of relapse CS is documented, repeated full diagnostic approach should be done. The case is noteworthy for the severe and rapidly progressive clinical course of CS, that despite biochemically being compatible with ectopic ACTH secretion, the underlying cause was an ACTH-secreting pituitary macroadenoma. Not all acute CS cases are due to ectopic ACTH, and even well-recognized diagnostic strategies have caveats, as was the case here. CONCLUSION CD often presents with the gradual onset of a constellation of signs and symptoms of prolonged supraphysiologic cortisol levels. Sudden and dramatic onset of CS often suggests an ectopic ACTH-secreting tumor. These cases are more frequently accompanied by altered mental status, hyperglycemic emergencies, and hypokalemia. The described case illustrates an atypical presentation of a severe case of CD with new, marked hyperglycemia and severe refractory hypokalemia. It is noteworthy to emphasize the importance in the suspicion of a secondary cause of diabetes mellitus in the presence of hyperglycemia
6 e50 Nonectopic Severe Cushing, AACE Clinical Case Rep. 2018;4(No. 1) emergencies. Furthermore, the biochemical investigation of ACTH-dependent CS is complex and subject to inaccuracy, justifying a holistic approach and goal-oriented therapy in all cases. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Molitch ME. Nonfunctioning pituitary tumors and pituitary incidentalomas. Endocrinol Metab Clin North Am. 2008;37: Buurman H, Saeger W. Subclinical adenomas in postmortem pituitaries: classification and correlations to clinical data. Eur J Endocrinol. 2006;154: Sharma ST, Nieman LK, Feelders RA. Cushing s syndrome: epidemiology and developments in disease management. Clin Epidemiol. 2015;7: Pivonello R, De Leo M, Vitale P, et al. Pathophysiology of diabetes mellitus in Cushing s syndrome. Neuroendocrinology. 2010;92(suppl 1): Howlett TA, Drury PL, Perry L, Doniach I, Rees LH, Besser GM. Diagnosis and management of ACTH-dependent Cushing s syndrome: comparison of the features in ectopic and pituitary ACTH production. Clin Endocrinol (Oxf). 1986;24: Isidori AM, Lenzi A. Ectopic ACTH syndrome. Arq Bras Endocrinol Metabol. 2007;51: Fernández-Rodríguez E, Villar-Taibo R, Pinal-Osorio I, et al. Severe hypertension and hypokalemia as first clinical manifestations in ectopic Cushing s syndrome. Arq Bras Endocrinol Metabol. 2008;52: Torpy DJ, Mullen N, Ilias I, Nieman LK. Association of hypertension and hypokalemia with Cushing s syndrome caused by ectopic ACTH secretion: a series of 58 cases. Ann N Y Acad Sci. 2002;970: Stewart P. The adrenal cortex. In: Williams Textbook of Endocrinology. 13th ed. 2016: Lacroix A, Feelders RA, Stratakis CA, Nieman LK. Cushing s syndrome. Lancet. 2015;386: Tan EU, Ho MS, Rajasoorya CR. Metamorphosis of a nonfunctioning pituitary adenoma to Cushing s disease. Pituitary. 2000;3: Katznelson L, Bogan JS, Trob JR, et al. Biochemical assessment of Cushing s disease in patients with corticotroph macroadenomas. J Clin Endocrinol Metab. 1998;83: Findling JW, Raff H. Cushing s syndrome: important issues in diagnosis and management. J Clin Endocrinol Metab. 2006;91:
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