NEWLY DIAGNOSED CARNEY COMPLEX IN 3 YOUNG ADULTS WITH PRIMARY ADRENAL CUSHING SYNDROME A CASE SERIES AND REVIEW OF THE LITERATURE
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1 Case Report NEWLY DIAGNOSED CARNEY COMPLEX IN 3 YOUNG ADULTS WITH PRIMARY ADRENAL CUSHING SYNDROME A CASE SERIES AND REVIEW OF THE LITERATURE Charalampos Lyssikatos, MD 1* ; Praveen V. Pavithran, MD, DM 2* ; Amit Tirosh, MD 1,3 ; Fabio R. Faucz, PhD 1 ; Jayakumar R. Vasukutty, MD, FRCP, DM 2 ; Elena Belyavskaya, MD 1 ; Anish Ahamed, MD, DNB 2 ; Margarita Raygada, PhD, ScM, CGC 1 ; Constantine A. Stratakis, MD, DMSci 1 ABSTRACT Objective: Carney complex (CNC) is a very rare cause of adrenocorticotropic hormone (ACTH)-independent Cushing syndrome (CS). We describe 3 cases of CNC diagnosed through the evaluation of CS, with no other major manifestations of CNC. Methods: We present the relevant history, laboratory, and pathologic data of the current cases, and review relevant documentation from the literature. Results: Among all 3 patients, CS symptomatology was the main clinical characteristic, which was also supported by a diminished diurnal rhythmicity of plasma cortisol and ACTH levels. The paradoxical increase in cortisol after both low and high dose dexamethasone suppression tests (Liddle s test) proved to be the most useful biochemical clue for the diagnosis of primary pigmented nodular adrenocortical disease (PPNAD) in these patients. The absence of bilateral macronodular or unilateral adrenal lesion led to the possible diagnosis of PPNAD/CNC. None of the 3 patients demonstrated any of the other described major manifestations of CNC. Pathologic examination confirmed PPNAD, and genetic testing showed mutations in the protein kinase A regulatory subunit type Iα gene in 2 of the 3 patients. Conclusion: CNC should be suspected among patients with micronodular primary adrenal CS, even in the absence of other major manifestations of this rare disease, as early recognition of CNC is of paramount importance for avoiding the complications from its comorbidities. (AACE Clinical Case Rep. 2017;3:e326-e330) Abbreviations: ACTH = adrenocorticotropic hormone; CNC = Carney complex; CS = Cushing syndrome; IGF-1 = insulinlike growth factor 1; MRI = magnetic resonance imaging; PPNAD = primary pigmented nodular adrenocortical disease; PRKAR1A = protein kinase A regulatory subunit type Iα Submitted for publication August 23, 2016 Accepted for publication December 6, 2016 From the 1 Section on Endocrinology and Genetics, Program on Developmental Endocrinology and Genetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, 2 Department of Endocrinology, Amrita Institute of Medical Sciences, Kochi, Kerala, India, and 3 Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel. *The two first authors contributed equally to this work. Address correspondence to Dr. Charalampos Lyssikatos, National Institutes of Health, NICHD-PDEGEN, 10 Center Drive, Building 10, NIH-Clinical Research Center, Room , MSC1103, Bethesda, MD lyssikatosc@mail.nih.gov DOI: /EP CR To purchase reprints of this article, please visit: AACE makes no claims to U.S. Government works. INTRODUCTION Carney complex (CNC) is a rare multisystem endocrine disorder described in 1985 by Dr. J. Aidan Carney as the combination of myxomas, spotty skin pigmentation, and endocrine overactivity (1). Among the endocrine manifestations of CNC, Cushing syndrome (CS) is the most common, evolving from a distinct type of adrenal hyperplasia primary pigmented nodular adrenocortical disease (PPNAD) (2). In addition, patients with CNC are more prone to pituitary hypersecretion of growth hormone (GH), due to hyperplasia or adenoma. Gonadal neoplasms may also develop as part of CNC, including large cell calcify- e326 AACE CLINICAL CASE REPORTS Vol 3 No. 4 Autumn 2017
2 CNC in young adults with PPNAD, AACE Clinical Case Rep. 2017;3(No. 4) e327 ing Sertoli cell tumors of the testes, and ovarian benign cystadenomas or ovarian cancer (2). Thyroid nodules are observed in three fourths of the cases, with a variable histologic picture ranging from follicular hyperplasia to malignancy. Psammomatous melanotic schwannomas, breast ductal adenomas, and a rare bone tumor, osteochondromyxoma, are additional unusual manifestations (3). The main clinical and laboratory findings in CNC are also used as the diagnostic criteria (4). For CNC diagnosis, a patient must either exhibit 2 major criteria, or 1 major and 1 supplemental criterion. The genetic alteration responsible for most subjects with CNC are inactivating mutations or deletions of the protein kinase A regulatory subunit type Iα (PRKAR1A) gene located at chromosome 17q (5). Previous to the current study, more than 125 different PRKAR1A mutations have been identified. In this article, we present 3 cases of CNC (study codes: CAR , CAR712.03, and CAR713.05) with 2 novel germline PRKAR1A gene mutations (6). The only clinical clue for CNC was a paradoxical increase in cortisol following a dexamethasone suppression test. The final diagnosis of CNC was made after the patients underwent bilateral adrenalectomy for the treatment of CS, with a pathologic diagnosis of PPNAD. CASE REPORT We describe 3 patients that presented to the Department of Endocrinology at the Amrita Institute of Medical Sciences for evaluation of Cushing syndrome. Baseline 24-hour urinary free cortisol (UFC) collections were followed by a morning plasma cortisol measurement after a low dose (0.5 mg dexamethasone every 6 hours for 2 days) and high dose (2 mg dexamethasone every 6 hours for 2 days) dexamethasone suppression (Liddle s test). Morning plasma adrenocorticotropic hormone (ACTH) was measured in order to differentiate between primary adrenal CS and ACTH-secreting tumors, and adrenal computed tomography (CT) scan was performed in order to define the etiology for adrenal cortisol secretion. Finally, all patients underwent bilateral adrenalectomy to avoid the deleterious effects of hypercortisolemia. Evaluation for Other Manifestations of CNC Screening for functional pituitary tumors included measurement of plasma prolactin and insulin-like growth factor 1 (IGF-1) levels, growth hormone levels before and following an oral glucose tolerance test, and by pituitary magnetic resonance imaging (MRI) scans. No data on IGF-1 are available for case A, and no prolactin levels can be reported for cases A and C. All patients underwent echocardiography for identifying possible cardiac myxomas, and thyroid ultrasound for possible nodules. In addition, dermatologic evaluation for blue nevi and cutaneous myxomas were performed, and male patients underwent testicular ultrasound as a screening for Sertoli cell tumors. Genetic Studies DNA was extracted from peripheral leukocytes and studied for PRKAR1A mutations with polymerase chain reaction followed by bidirectional DNA sequence analysis as previously published (5,7). The Institutional Review Boards of the participating institutions approved these investigations. Written informed consent was obtained from all patients. Results Patient characteristics and test results are detailed in Table 1. All patients were in their late teens or early twenties and had symptoms suggestive of long-standing CS, including high blood pressure, central obesity, hirsutism, and peripheral myopathy. Dermatologic evaluation did not reveal any abnormal findings in any of the patients at presentation; however, patient case B (CAR713.05) had small myxomas of the scalp that were noticed on careful examination. With the exception of one patient (CAR713.05) with a nonfunctional pituitary microadenoma, screening for other manifestations of CNC, including cardiac myxomas, thyroid lesions, and testicular lesions, were all negative (Table 1). Liddle s test showed a paradoxical increase in plasma cortisol levels in all 3 patients. Adrenal CT scans revealed adrenal glands of normal size, with adrenal (diameter <1 cm) forming a bead on a string appearance (Fig. 1). All patients underwent bilateral adrenalectomy. In gross examination, the adrenal glands were within normal size and weight. Characteristic brown pigmented were demonstrated in all 3 cases (Fig. 2 A, B, and C). Finally, none of the first degree relatives had known diagnosis or relevant clinical manifestations of CNC. Sequence analysis and deletion testing of the PRKAR1A gene revealed mutations in 2 of the 3 patients (cases A and C, Table 1). The variant p.e257k (c.769g>a; g g>a; NM_002734) was identified in case A, and the intronic variant g a>g (NM_002734), that is predicted to abolish an acceptor splice site, was identified in case C. Both mutations have been previously associated with CNC (8,9). DISCUSSION In the current series we describe 3 young adults with primary adrenal CS diagnosed with PPNAD and subsequently CNC. Despite negative family history, several clues could suggest the diagnosis, including age at diagnosis, a paradoxical increase in plasma cortisol following administration of dexamethasone, and micronodular appearance of the adrenal glands. The disease was ultimately diagnosed according to histopathology compatible
3 e328 CNC in young adults with PPNAD, AACE Clinical Case Rep. 2017;3(No. 4) Table 1 Patient Characteristics Case A Case B Case C Study code CAR CAR CAR Gender Male Female Male Age at diagnosis (years) Basal plasma cortisol (µg/dl) Criteria for CS LDDST (µg/dl) ACTH (pg/ml; normal range, pg/ml) <1 <1 <1 HDDST Imaging Abdominal CT Pituitary MRI Hormonal reports No abnormalities identified No further testing could be performed Microadenoma IGF-1 and prolactin within normal range No abnormalities identified Normal response to OGTT-GH Genetic testing p.e257k No mutation identified g a>g Abbreviations: ACTH = adrenocorticotropic hormone; CS = Cushing syndrome; CT = computed tomography; HDDST = high dose dexamethasone suppression test; IGF-1 = insulin-like growth factor 1; LDDST = low dose dexamethasone suppression test; MRI = magnetic resonance imaging; OGTT- GH = oral glucose tolerance growth hormone test. with PPNAD among all 3 patients, and mutations in the PRKAR1A gene in 2 of the patients. CNC is a rare endocrine multi-organ syndrome previously diagnosed in ~750 patients (6). A mutation in the PRKAR1A gene has been identified in more than 70% of the cases, including 80% of those with PPNAD (7,10). PRKAR1A is located at the 17q locus and is composed of 11 exons (6). Diagnosis of CNC is based on several criteria, such as PPNAD, and either a mutation in the PRKAR1A gene (patients 1 and 3) or skin myxomas (patient 2). The median age of CNC diagnosis is 20 years, with a similar peak age of diagnosis among those with PPNAD (2,6). The importance of early diagnosis of CNC cannot be A overemphasized. Apart from controlling hypercortisolemia and its deleterious effects, screening for other manifestations of CNC may be lifesaving. These include cardiac myxomas (11) that are responsible for 50% of the mortality from CNC (2,12). In addition, tumors of the gonads, pituitary gland, peripheral nervous system, and other organs may develop and should be followed-up. Several clues in our patients suggested the diagnosis of CNC. First was the earlier age of CS diagnosis in CNC as compared to other primary adrenal etiologies for CS, such as primary bilateral macronodular adrenocortical hyperplasia, which is usually diagnosed later in life between the age of 50 and 60 (13). Second, primary adrenal CS in the absence of bilateral macronodular disease or B Fig. 1. Adrenal computed tomography scan of patient (case A) showing bilateral adrenal in the right (A) and left (B) adrenals (black arrows).
4 CNC in young adults with PPNAD, AACE Clinical Case Rep. 2017;3(No. 4) e329 A B C Fig. 2. Histopathologic specimens (hematoxylin and eosin stained) of patient case C (CAR712.03) with findings typical of PPNAD: well circumcised adrenocortical (A: black arrows, 4) composed of eosinophilic cells with uniform nuclei and brown pigment (B and C; 10 and 40, respectively). unilateral adrenal lesion might indicate the diagnosis of PPNAD. Third, the paradoxical increase in plasma cortisol and urinary free cortisol excretion following dexamethasone administration is another feature that differentiates CS due to PPNAD from other adrenocortical disorders (14). Groussin et al (15,16) reported 2 groups of patients with isolated PPNAD and a mutation in the PRKAR1A gene. In one series (n = 5) (15), 5 distinct mutations were reported, whereas in the second series (n = 12) (16), all patients shared a 6 base pair deletion in the exon 7 splice acceptor site. In our report, a PRKAR1A mutation was identified in 2 of 3 patients, in intron 1 and exon 8, respectively, different from any of the previously described mutations. This is the first report of genetically proven CNC presenting with PPNAD from the Indian subcontinent. In the presented patients, the diagnoses were made only on pathologic evaluation despite the clinical clues during the clinical evaluation: the paradoxical increase in cortisol levels following dexamethasone administration and the typical adrenal appearance on imaging. This characteristic response to dexamethasone has been seen in most CNC patients and is a valuable laboratory test pointing towards the diagnosis (14). The absence of any skin manifestations is not surprising, as the characteristic lentigines may not always be an overt finding. However, a thorough physical and dermatologic examination is essential, as missing such findings may delay the diagnosis for many years as was evident in our cases. Establishing the diagnosis of CNC might be lifesaving, given the risk of developing cardiac myxomas in the absence of the recommended screening. CNC is an important and frequently missed cause of ACTH-independent CS, especially when the cutaneous findings are not pronounced. Screening tests in patients with CNC includes cardiac ultrasound, every 6 months in those with a medical history of cardiac myxoma and annually for patients without a history of cardiac myxoma, to avoid heart failure, stroke, and sudden death due to embolism (2). Also recommended annually are MRI of the pituitary gland for the detection of pituitary adenomas (accompanied by serum GH, IGF-1, and prolactin levels), MRIs for the early detection of schwannomas, thyroid ultrasound, ultrasound of the testicles for men and of the ovaries for women, and measurement of 24-hour and diurnal cortisol followed by Liddle s test for confirmation of PPNAD in patients that have not undergone bilateral adrenalectomy. CONCLUSION In conclusion, we identified 2 PRKAR1A gene mutations in 3 sporadic CNC cases. CNC should be suspected among patients with micronodular primary adrenal CS, even in the absence of major clinical manifestations of this rare disease. Early recognition of CNC signs is of paramount importance for avoiding the complications from comorbidities including hypertension, osteoporosis, gigantism/acromegaly, embolic strokes from cardiac myxomas, and the possibility of other tumors or cancer. After the CNC diagnosis, meticulous physical examination, laboratory work, and imaging studies during annual follow-up are indicated. ACKNOWLEDGMENTS This research was supported in part by the Intramural Research Program of the National Institutes of Health (NIH), Eunice Kennedy Shriver National Institute of Child Health and Human Development, protocol 1995-CH-0059 (ClinicalTrials.gov Identifier: NCT ), Bethesda, MD, 20892, USA. We would like also to acknowledge the Department of Pathology, Amrita Institute of Medical Sciences, particularly Dr. Annie Jojo for arranging the pathology slide pictures. DISCLOSURE The authors have no multiplicity of interest to disclose.
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