EFFECTIVE MEDICAL THERAPY FOR CUSHING DISEASE CAN INCREASE THE SUSCEPTIBILITY TO RELATIVE HYPOCORTISOLISM
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1 Case Report EFFECTIVE MEDICAL THERAPY FOR CUSHING DISEASE CAN INCREASE THE SUSCEPTIBILITY TO RELATIVE HYPOCORTISOLISM Kevin C.J. Yuen, MD, FRCP (UK), FACE; Jennifer U. Mercado, ARNP; Kelley Moloney, ARNP; Frances Broyles, MD ABSTRACT Submitted for publication January 4, 2017 Accepted for publication February 28, 2017 From the Swedish Pituitary Center, Swedish Neuroscience Institute, Seattle, Washington. Address correspondence to Dr. Kevin C.J. Yuen, Swedish Pituitary Center, Swedish Neuroscience Institute, th Avenue, Suite 400, Seattle, WA DOI: /EP CR To purchase reprints of this article, please visit: Objective: Pasireotide is approved for treatment of adults with Cushing disease (CD) with persistent hypercortisolism for whom surgery has failed or is not an option. Effective medical therapy for CD may increase the susceptibility of relative hypocortisolism during acute stress because of a patient s inability to compensate by increasing endogenous adrenocorticotropic hormone (ACTH) and cortisol secretion. We describe a patient with CD on pasireotide therapy for 7 years in whom biochemical eucortisolemia was achieved but subsequently experienced several distinct episodes of relative hypocortisolism during periods of acute illness. Methods: A 67-year-old man with biochemical confirmation of CD exhibited clinical and biochemical features of persistent hypercortisolism after transsphenoidal surgery despite pituitary magnetic resonance imaging showing no residual or recurrent tumor. He was enrolled into a phase 3 study (NCT ) and was initated on twice-daily subcutaneous pasireotide. Results: Long-term pasireotide therapy normalized 24-hour urinary free cortisol, serum cortisol, and ACTH levels. The patient subsequently developed type 2 diabetes mellitus and was managed effectively with oral hypoglycemic agents and insulin therapy. During a routine clinic assessment 79 months after study enrollment, he reported symptoms suggestive of relative hypocortisolism during three distinct substantially acute stressful health events in the preceding 18 months. Conclusion: Successful achievement of eucortisolemia with long-term medical therapy may increase susceptibility to relative hypocortisolism and precipitate symptoms of adrenal insufficiency during periods of acute stress in patients with CD. We recommend that such patients should be counseled on glucocorticoid stress dosing to prevent such events that could lead to adrenal crisis. (AACE Clinical Case Rep. 2018;4:e1-e6) Abbreviations: ACTH = adrenocorticotropic hormone; CD = Cushing disease; FPG = fasting plasma glucose; GH = growth hormone; HbA 1c = hemoglobin A 1c ; T2DM = type 2 diabetes mellitus; TSS = transsphenoidal surgery; UFC = urinary free cortisol INTRODUCTION Cushing disease (CD) is a rare condition caused by an adrenocorticotropic hormone (ACTH)-secreting pituitary adenoma and is associated with increased morbidity and mortality (1,2). Transsphenoidal surgery (TSS) is the firstline therapy for most patients with CD, providing longterm remission rates of 44 to 90% (3). Relapse may occur in up to 46% of cases after long-term follow-up (5 to 10 years) (4), requiring second-line therapeutic intervention such as further surgery, radiotherapy, medical therapy, or bilateral adrenalectomy (5). Pasireotide is a somatostatin analogue with a high binding affinity for somatostatin-receptor subtype 5, which is highly expressed in ACTH-secreting pituitary adenomas, AACE CLINICAL CASE REPORTS Vol 4 No. 1 January/February 2018 e1
2 e2 Hypocortisolism in CD, AACE Clinical Case Rep. 2018;4(No. 1) thereby inhibiting ACTH secretion (6). In a phase 2 study, pasireotide reduced mean 24-hour urinary free cortisol (UFC), serum cortisol, and plasma ACTH in patients with CD (7). Subsequently, a phase 3 study (CSOM230B2305) in CD patients demonstrated that 12 months of pasireotide not only decreased 24-hour UFC, serum and salivary cortisol, and plasma ACTH levels but also improved clinical signs and symptoms (8). In this study, diarrhea (58%), nausea (52%), and hyperglycemia (40%) were the most commonly reported adverse events. Pasireotide is approved in Europe and the United States for the treatment of adult patients with CD with recurrent hypercortisolism after surgery or for whom surgery is contra-indicated (9,10). More recently, phase 3 results of 24 months of pasireotide showed sustained reductions in mean 24-hour UFC and clinical improvements in patients with CD (11). In healthy volunteers, endogenous ACTH stimulates the adrenal glands to synthesize and secrete excess cortisol during physiologically stressful events (12). Conditions such as systemic infections, trauma, surgical interventions, invasive diagnostic tests, or concomitant illnesses in patients with adrenal insufficiency typically require extra dosing of glucocorticoids to avoid symptoms of relative hypocortisolemia (e.g., fatigue, weakness, anorexia, nausea, vomiting, orthostatic dizziness) (13). In patients with adrenal insufficiency, absolute or relative hypocortisolism can lead to frank adrenal crisis, a life-threatening emergency and a major cause of death (13). Because pasireotide effectively suppresses ACTH and secondarily cortisol secretion, patients may be susceptible to developing relative hypocortisolism that may progress to adrenal crisis associated with acute stress due to inadequate, stress-induced increases in endogenous ACTH and cortisol secretion (14). Herein, we report a patient with CD enrolled in a phase 3 study who was effectively treated with pasireotide for 7 years and achieved eucortisolemia but experienced 3 distinct episodes of relative hypocortisolism. This case report highlights the need for patients to be able to recognize potentially dangerous symptoms and for physicians to consider glucocorticoid stress dosing in patients with CD who achieve eucortisolemia while on long-term medical therapy. METHODS Study Design Laboratory findings confirmed hypercortisolism (baseline mean 24-hour UFC 1.5 times upper limit of normal [ULN]) after the patient underwent TSS in August In October 2008, the patient was enrolled in a prospective phase 3 trial (ClinicalTrials.gov identifier, NCT ) (8,11), completed the core study after 1 year, and entered into the extension phase of the study in October 2009, as per protocol. After 5 years (September 2013), the patient entered into a roll-over protocol, allowing access to pasireotide upon completing the initial phase 3 trial (ClinicalTrials.gov identifier, NCT ) (15). Mean 24-hour UFC was calculated using three or four 24-hour urine samples collected within a 14-day period at months 3, 6, and 12 and using 2 consecutive-day samples at other time points (8). Monthly 24-hour UFC was assessed for 6 months and every 3 months thereafter. Hematologic and blood biochemical measurements were performed at 3-month intervals (8,11). Ethical Approval All procedures performed in the phase 3 study, as well as during the patient s follow-up, were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from the individual described in this report. RESULTS Case Presentation The patient was a 67-year-old man with biochemically confirmed CD (Table 1; Fig. 1). After TSS in August 2008, the patient developed secondary hypogonadism, secondary hypothyroidism, and growth hormone (GH) deficiency and was treated with testosterone, levothyroxine, and GH replacement therapies. Hypercortisolemia persisted with 24-hour UFC >2 times ULN on 2 separate assessments (270.2 μg/24 hours and 167 μg/24 hours [reference range, 0 to 50 μg/24 hours]) and a positive dexamethasone corticotropin-releasing hormone test (15-minute cortisol, 2.6 μg/dl [reference range, <1.4 μg/dl]). Postoperative pituitary magnetic resonance imaging did not reveal residual or recurrent tumor that was deemed surgically operable by our dedicated pituitary neurosurgeon. Furthermore, the patient declined the possibility of undergoing another pituitary surgery at that time because his wife was suffering from terminal Alzheimer disease and he could not afford to be recuperating from surgery while being her primary caregiver at the same time. Because the patient was willing and eligible to participate in a clinical study, he was enrolled in the phase 3 trial in October 2008 and was randomly assigned to receive twice-daily pasireotide 600 μg injected subcutaneously. After 1 and 6 months, the pasireotide dose was uptitrated to twice-daily 900 μg and 1,200 μg, respectively. Biochemical Control of CD Baseline measurements indicated recurrent CD (mean 24-hour UFC, μg/24 hours; serum cortisol, 20.9 μg/ dl; ACTH, 13.6 pg/ml). At 6 months, mean 24-hour UFC decreased to 5.7 μg/24 hours (Fig. 2 A), whereas serum cortisol (Fig. 2 B) and ACTH levels were comparable to
3 Hypocortisolism in CD, AACE Clinical Case Rep. 2018;4(No. 1) e3 Fig. 1. Timeline of diagnoses of Cushing disease and type 2 diabetes mellitus (T2DM), trial participation, biochemical confirmation of persistent Cushing disease, and events of relative hypocortisolism. MI = myocardial infarction; UTI = urinary tract infection. MRI of the pituitary Clinical parameters Table 1 Clinical and Biochemical Characteristics of the Patient at Baseline 4-mm, right-sided microadenoma Height (m) 1.77 Body weight (kg) 94.3 Body mass index (kg/m 2 ) 30.1 Blood pressure (mm Hg) 142/84 Clinical features Active medical conditions (not inclusive) Biochemical parameters Facial rubeosis, central obesity, supraclavicular fat pad, dorsal fat pad, easy bruising Hypertension, T2DM, chronic fatigue syndrome Morning ACTH (pg/ml) 13.6 (reference range, 6-48) Morning serum cortisol (mg/dl) 20.9 (reference range, ) 24-hour UFC (mg/24 hours) (reference range, 0-50) FPG (mg/dl) 132 (reference range, 60-99) HbA 1c (%) 6.7 (reference range, ) HbA 1c (mmol/mol) 50 (reference range, 29-38) Abbreviations: ACTH = adrenocorticotropic hormone; FPG = fasting plasma glucose; HbA 1c = glycated hemoglobin; MRI = magnetic resonance imaging; T2DM = type 2 diabetes mellitus; UFC = urinary free cortisol. baseline levels (21.1 μg/dl and 13.6 pg/ml, respectively). After 5 years of pasireotide (September 2013), the patient entered the open-label extension phase and maintained normal 24-hour UFC (15.5 μg/24 hours; reference range, 0 to 50 μg/24 hours) (Fig. 2 A). However, serum cortisol and ACTH were marginally increased to 21.7 μg/dl and 18.2 pg/ml, respectively, from baseline. Glycemic Control Nine days after initiating pasireotide, fasting plasma glucose (FPG; 132 mg/dl) increased, consistent with the diagnosis of type 2 diabetes mellitus (T2DM; Table 1) (16). The patient started on oral antidiabetic medications (metformin, glibenclamide, glipizide), but his glycemia continued to worsen after 6 months of pasireotide therapy (FPG, 173 mg/dl; hemoglobin A 1c [HbA 1c ], 10.0% [86 mmol/mol]; Fig. 2 C). Rosiglitazone and sitagliptin were added at 9 months. The patient s T2DM remained poorly controlled (FPG, 185 mg/dl; HbA 1c, 9.9% [85 mmol/ mol]) prior to entering the extension phase, and insulin detemir and glipizide were initiated. At 42 months, HbA 1c levels improved and stabilized but continue to remain uncontrolled, with HbA 1c levels persistently >7.0%; these levels were maintained into the extension study and open-label use. Episodes of Relative Hypocortisolism In May 2015 (79 months after study enrollment), during a routine clinical assessment, the patient reported symptoms suggestive of relative hypocortisolism in the
4 e4 Hypocortisolism in CD, AACE Clinical Case Rep. 2018;4(No. 1) previous 18 months, including nausea, profound fatigue, dizziness, and joint pains that were associated with three substantially stressful health events. These included a myocardial infarction requiring triple coronary stent insertion (January 2014), a urinary tract infection treated with a 10-day course of antibiotics (April 2014), and an episode of renal calculi with acute abdominal pain requiring lithotripsy therapy (October 2014; Fig. 1). Throughout these events, 24-hour UFC was maintained within the reference range. Moreover, the patient did not report these events when they occurred because he was unaware of the possiblity of relative hypocortisolism and therefore did not stressdose with glucocorticoids. The patient was subsequently counseled to be mindful of hypocortisolism symptoms potentially leading to adrenal crisis, to either decrease or temporarily stop pasireotide, to stress-dose with glucocorticoids, and to avoid intensifying his glycemic control to minimize the risk of hypoglycemia A B C Fig. 2. (A) Mean 24-hour urinary free cortisol (UFC); (B) serum cortisol levels over the course of treatment with pasireotide. Dotted line in (A) and (B) indicates the upper limit of the reference range. Values in the diabetic range (glycated hemoglobin [HbA1c] >6.5%) in (C) are indicated in gray above the black line. a Myocardial infarction. b Urinary tract infection. c Abdominal pain due to renal calculi.
5 Hypocortisolism in CD, AACE Clinical Case Rep. 2018;4(No. 1) e5 that may also precipitate another cardiovascular event. A target HbA 1c between 7.0% (53 mmol/mol) and 8.0% (64 mmol/mol) was proposed to the patient. DISCUSSION In patients with CD, successful pituitary surgery and effective medical therapy with adrenal steroidogenesis inhibitors, pituitary-targeted inhibitors of ACTH secretion, and glucocorticoid receptor antagonists may increase the predisposition to glucocorticoid withdrawal symptoms. Pituitary-targeted inhibitors (such as pasireotide) theoretically represent the most physiologic approach to treating CD by suppressing ACTH secretion from the corticotrope adenoma, thereby secondarily normalizing cortisol levels (17). However, the mechanism of medical therapy in inducing eucortisolemia can vary depending on whether therapy targets the corticotrope adenoma, adrenal gland, or peripheral glucocorticoid receptors. Therefore, the dynamics of physiologic cortisol secretion, especially stress-induced increased secretion (18), may not revert to normal physiology with effective medical therapy. Hence, during periods of acute stress, effective medical therapy may increase the susceptibility to relative hypocortisolism with manifestation of symptoms mimicking adrenal insufficiency. Adrenal crisis is caused by insufficient endogenous glucocorticoid production during periods of stress, primarily caused by gastrointestinal infection and fever (45%) (12). Other stressful events, such as major pain, surgery, emotional distress, heat, and pregnancy, could also lead to adrenal crisis (12). Additionally, patients with comorbidities are at higher risk than those without (19). However, adrenal crisis has not been associated with body mass index, glucocorticoid dose, dehydroepiandrosterone treatment, hypogonadism, hypothyroidism, or GH deficiency (12). Adrenal suppression with high-dose glucocorticoid therapy is a form of relative secondary adrenal insufficiency, and stressful incidents are often complicated by hypoglycemia (13). Hence, there is a need for patient education on events triggering glucocorticoid insufficiency (e.g., fever, infections, psychological distress, and neglected glucocorticoid intake) (13). Upon symptom onset, acute glucocorticoid stress dosing can prevent adrenal crisis associated with relative hypocortisolism (13). Due to persistent hypercortisolism after TSS, medical therapy options other than pasireotide that our patient could have been considered for were an adrenal steroidogenesis inhibitor or a glucocorticoid receptor antagonist. Ketoconazole is an adrenal steroidogenesis inhibitor originally developed as an antifungal agent that acts by blocking several steps in adrenal steroid synthesis, but it has an important side effect of hepatotoxicity that requires close monitoring of liver function. Mifepristone, the only glucocorticoid receptor antagonist currently available in the United States, binds to the glucocorticoid receptor with 18 times the affinity of cortisol (20), resulting in increased ACTH and cortisol levels. Therefore, efficacy and safety monitoring of mifepristone therapy must be based on clinical assessment, not on serum ACTH and cortisol levels. For our patient, pasireotide was the medical therapy of choice because he was eligible and willing to participate in the phase 3 study that was recruiting subjects at that time. Unlike mifepristone, pasireotide allowed us to monitor therapeutic efficacy with 24-hour UFC, serum ACTH, and cortisol levels. However, the major side effect of pasireotide is hyperglycemia, which is induced via inhibition of insulin secretion directly via binding to the sst5 receptor on pancreatic islet cells and indirectly via suppression of incretin hormone production by K and L cells (21). Pasireotideinduced hyperglycemia can be effectively managed with metformin and a dipeptidyl peptidase 4 inhibitor, switching to a glucagon-like peptide 1 receptor agonist and initiating insulin, as required (22,23). After 42 months of pasireotide therapy during the extension and open-label use phase of the study, our patient was treated with stable doses of sitagliptin, glipizide, and insulin detemir that stabilized his glycemia, although his glycemic control was not within the optimal therapeutic target (HbA 1c <7.0%), with HbA 1c levels mostly ranging between 7.0 and 8.0%. During this time, the patient also reported concerns about experiencing neuroglycopenic symptoms; therefore, he proactively avoided allowing his blood glucose levels to drop below 100 mg/dl, thus explaining his suboptimal glycemic control. For T2DM, intensive glucose control is critical to reduce diabetic microvascular complications (24). By contrast, maintaining intensive glycemic control in our patient with coronary artery disease that required triple coronary stent insertion might not be appropriate because this will not only increase the risk of hypoglycemia (25) but would further increase his cardiovascular risk and mortality (26). It has been previously reported that in patients with T2DM who previously underwent coronary artery bypass grafting, and those with HbA 1c levels >9.0% had significantly increased risk of death, whereas those with HbA 1c levels >8.1% had increased risk for combined outcome of death or major adverse cardiovascular event (27). Because patients with CD are at significantly increased risk of cardiovascular disease (28), we recommend maintaining less intensive glycemic targets (HbA 1c between 7.0 and 8.0%) for patients with CD controlled on long-term medical therapy with concurrent T2DM to minimize the risks of hypoglycemic episodes that may precipitate future cardiovascular events. CONCLUSION Our case highlights the importance of patient counseling on symptom recognition and the need for glucocorticoid stress dosing to prevent the development of rela-
6 e6 Hypocortisolism in CD, AACE Clinical Case Rep. 2018;4(No. 1) tive hypocortisolism and potential progression to adrenal crisis. For patients with CD with concurrent T2DM on insulin therapy, avoiding intensive glycemic control is also prudent to reduce the risk of inducing hypoglycemia and potential future adverse cardiovascular events. ACKNOWLEDGMENT This study was supported by Novartis Pharmaceuticals Corporation. Medical editorial assistance was provided by MedThink SciCom (Raleigh, NC) and sponsored by Novartis Pharmaceuticals Corporation. The patient described in this report had been enrolled in a phase 3 study funded by Novartis Pharmaceuticals Corporation. DISCLOSURE K.C.J.Y. has received funding from Novartis Pharmaceuticals Corporation, Cortendo AB, and Corcept Therapeutics to support research at the Swedish Neuroscience Institute and is an ad hoc advisor to Novartis Pharmaceuticals Corporation and Corcept Therapeutics. 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