A Rare Case of ACTH-independent Macronodular Adrenal Hyperplasia Associated with Aldosterone-producing Adenoma
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1 CASE REPORT A Rare Case of ACTHindependent Macronodular Adrenal Hyperplasia Associated with Aldosteroneproducing Adenoma Eri Hayakawa 1, Takanobu Yoshimoto 1, Kiichiro Hiraishi 1, Masako Kato 1, Hajime Izumiyama 1, Hironobu Sasano 2 andyukiohirata 1 Abstract A 52yearold man was evaluated for incidentally discovered bilateral adrenal masses. He had drugresistant hypertension but lacked Cushingoid features. Endocrinological tests revealed autonomous secretion of cortisol and aldosterone with suppressed plasma ACTH and renin activity. A selective adrenal venous sampling demonstrated aldosterone hypersecretion from the left adrenal vein. The clinical diagnosis of subclinical Cushing s syndrome due to ACTHindependent macronodular adrenal hyperplasia (AIMAH) associated with primary aldosteronism was made, and he underwent left adrenalectomy; the resected adrenal lesion was consistent with the pathological diagnosis of AIMAH coexistent with aldosteroneproducing adenoma (APA). This is a very rare case of AIMAH with concomitant unilateral APA, whose hypertension improved after surgery. Key words: ACTHindependent macronodular adrenal hyperplasia, primary aldosteronism, adrenal venous sampling, subclinical Cushing s syndrome (Intern Med 50: , 2011) () Introduction Adrenocorticotrophic hormone (ACTH)independent macronodular adrenal hyperplasia (AIMAH) is a rare cause of Cushing s syndrome (CS), accounting for less than 1% of adrenal CS (1). However, it has been recently recognized that AIMAH is found incidentally by abdominal imaging tests, such as ultrasonography, CT and MRI scans. On the other hand, primary aldosteronism (PA) characterized by autonomous aldosterone hypersecretion constitutes mainly two subtypes, aldosteroneproducing adenoma (APA) and bilateral idiopathic hyperaldosteronism (IHA). PA is currently considered to be a more common disease causing secondary hypertension than previously believed; its prevalence among hypertensive patients has been reported to be 515% (2). However, to date only a few cases of PA with CS due to a solitary adenoma cosecreting aldosterone and cortisol have been reported (3). To the best of our knowledge, only a few cases of AIMAH associated with PA have been reported (4, 68). We herein describe a very rare case of AIMAH associated with PA due to unilateral APA, as localized by selective adrenal venous sampling (AVS) and confirmed by the histopathological and immunohistochemical analysis of the resected adrenal specimen. Case Report A 52yearold man was found to have an abnormality of the gallbladder (adenomyomatosis) by abdominal ultrasonography at the complete medical checkup. Subsequent abdominal MRI incidentally revealed bilateral adrenal masses. He was referred to our hospital for further evaluation of bilateral adrenal masses. He had drugresistant hypertension for 8 years. Department of Clinical and Molecular Endocrinology, Tokyo Medical and Dental University Graduate School, Japan and Department of Anatomic Pathology, Tohoku University Graduate School of Medicine, Japan Received for publication August 10, 2010; Accepted for publication October 11, 2010 Correspondence to Dr. Yukio Hirata, yhirata.cme@tmd.ac.jp 227
2 Intern Med 50: , 2011 Table 1. Laboratory and Endocrine Data before and after Surgery Before surgery After surgery (Reference range) Complete blood count White blood cells Neutrophils Lymphocytes Monocytes Eosinophils Basophils Red blood cells Hemoglobin Platelets Biochemistry Blood urea nitrogen Creatinine Sodium Potassium LDLcholesterol Triglyceride Glucose Hemoglobin A1c Insulin HOMAIR Endocrine Data Plasma ACTH Serum cortisol Plasma renin activity Plasma aldosterone concentration ARR Dehydroepiandrosterone sulfate Urinary 17hydroxycorticosteroid Free cortisol Aldosterone (/ L) ( 10 4 / L) (g/dl) ( 10 4 / L) (meq/l) (meq/l) ( U/mL) (pg/ml) ( g/dl) (ng/ml/hr) (pg/ml) (ng/ml) (mg/day) ( g/day) ( g/day) ( ) ( ) ( ) (3.68.5) (0.68.0) (0.01.5) (430554) ( ) ( ) (719) (0.71.1) (138146) (3.75.0) (<139) (26173) (78109) (4.35.8) ( ) (<2.5) (756) ( ) (0.32.9) (30159) (<200) (53342) (1.68.8) ( ) (<10) He was 175 cm tall and weighed kg (body mass index: 39 kg/m 2 ). His blood pressure was 174/86 mmhg with antihypertensive drugs, including amlodipine (5 mg), valsartan (80 mg), doxazosin (1 mg) and spironolactone (50 mg). He had no Cushingoid features, such as central obesity, moon face, skin atrophy, purple striae or buffalo hump. Laboratory examination showed a low normal serum potassium level, elevated fasting immunoreactive insulin levels and LDLcholesterol levels, but normal fasting glucose and glycosylated hemoglobin levels (Table 1). Endocrine tests (Table 2) revealed normal basal cortisol levels, suppressed plasma ACTH level, aldosterone/renin ratio (ARR) of 200 and normal 24 hoururinary excretion of free cortisol, but an increased urinary excretion of 17OHCS and aldosterone. Dynamic endocrine tests showed altered circadian rhythm of cortisol with complete suppression of plasma ACTH, nonsuppressibility of cortisol by highdose (8 mg) dexamethasone suppression test (DST), hyporesponse of ACTH and cortisol to CRH stimulation, and hyperresponse of cortisol and aldosterone to ACTH stimulation (Table 2). These data are consistent with the diagnosis of subclinical CS (SCS) as proposed from the Committee on the Disorders of Adrenal Hormones by the Ministry of Health and Welfare of Japan, 1996 (10). Stimulation with furosemide plus upright posture showed suppressed response of plasma renin activity (PRA), consistent with the diagnosis of PA (Table 2). Computed tomography (CT) scan of the abdomen revealed the presence of bilateral adrenal masses, whose sizes were cm in the left adrenal and cm in the right adrenal, respectively (Fig. 1a). 131 IAdosterol scintigraphy showed an increased uptake of radioactivity by bilateral adrenals, being more predominant in the left side (Fig. 1b). Collectively, these clinical endocrine and imaging findings were consistent with the diagnosis of AIMAH accompanied with PA. A selective AVS was performed to localize the preferential secretion of aldosterone (Fig. 2). The aldosterone level in the left adrenal vein was greater than 14,000 pg/ml after ACTH stimulation (5), the lateralized ratio (LR) of the left to the right side was 4.3, and the contralateral ratio (CR) was 0.7. The results of AVS confirmed aldosterone hypersecretion from the left adrenal vein with comparable cortisol secretion from bilateral adrenal glands. After obtaining informed consent, the patient underwent left adrenalectomy. The resected left adrenal mass was cm in size, consisting of multiple yellow nodules, ranging from a few mm to 40 mm in diameter (Fig. 3). His 228
3 Intern Med 50: , 2011 Table 2. Dynamic Endocrine Tests before and after Surgery Before surgery a) Diural rhythm Clock time 8:00 16:00 23:00 ACTH(pg/mL) Cortisol(μg/dL) b) Dexamethasone suppression test Dexamethasone (mg) ACTH(pg/mL) 26 <5 <5 Cortisol(μg/dL) c) CRH stimulation test Time (min) ACTH(pg/mL) Cortisol(μg/dL) PAC (pg/ml) d) ACTH stimulation test Time (min) Cortisol(μg/dL) PAC (pg/ml) e) Furosemide plus upright test Time (min) PRA (ng/ml/hr) PAC (pg/ml) After surgery f) Diural rhythm Clock time 8:00 23:00 ACTH(pg/mL) 5 5 Cortisol(μg/dL) g) Dexamethasone suppression test Dexamethasone (mg) 1 ACTH(pg/mL) 5 Cortisol(μg/dL) 3.0 h) ACTH stimulation test Time (min) Cortisol(μg/dL) i) Furosemide plus upright test Time (min) PRA (ng/ml/hr) PAC (pg/ml) PRA: plasma renin activity, PAC: plasma aldosterone concentration tologically, these nodules were composed of large clear cells with positive immunostaining for 3βhydroxysteroid dehydrogenase (3βHSD) and small compact cells with positive immunostaining for P450c17, consistent with the pathological diagnosis of AIMAH. In the nonnodular region, a wellencapsulated microadenoma ( 5 mm) composed of large clear cells with positive immunoreactivity for 3βHSD, but negative for P450c17, was present, while zona glomerulosa cells showed negative immunoreactivity for 3βHSD, all compatible with the pathological diagnosis of APA. The postoperative course was uneventful without glucocorticoid replacement. Shortly after operation, his serum potassium level became normalized and blood pressure (120/70 mmhg) was well controlled only with amlodipine (5 mg). Postoperative endocrine data revealed normal PAC with PRA normally responded to furosemide upright posture stimulation (Table 2), whereas suppressed plasma ACTH and normal cortisol levels with its nonsuppressibility to lowdose (1 mg) dexamethasone remained unchanged (Table 2). Discussion It has been reported that concomitant secretion of various biologically inactive steroid metabolites other than cortisol frequently occurs in AIMAH (1). However, to date there have been only a few cases with AIMAH accompanying PA reported (4, 68). In the present case, bilateral adrenal nodular enlargement by CT scan, lack of Cushingoid features, 229
4 Intern Med 50: , 2011 b a L R Figure 1. Diagnostic image tests. (a) Abdominal CT scan, showing bilateral adrenal nodular enlargement (white arrows show adrenal nodules) and (b) adrenal scintigraphy showing bilateral uptake of radioactivity, being more predominant in the left (L) than the right (R) adrenal (arrow). b a c PAC (pg/ml) F (μg/dl) PAC/F a b c Figure 2. Selective adrenal venous sampling (AVS). Plasma aldosterone concentration (PAC), cortisol concentration (F) and the ratios of PAC/F in (a) left adrenal vein, (b) right adrenal vein and (c) inferior vena cava, are shown before and after ( ) ACTH stimulation. normal basal plasma and urinary cortisol levels, nonsuppressibility of cortisol to highdose (8 mg) DST, suppressed ACTH secretion, and hyporesponse to CRH stimulation, caused by AIMAH as confirmed by the histopathological findings of the resected adrenal specimen, are all consistent with the diagnosis of SCS. In addition to poor PRA response after stimulation with furosemideupright posture as a confirmatory test for PA, a unilateral source of aldosterone hypersecretion was confirmed by employing selective AVS with ACTH stimulation. Furthermore, a solitary microadenoma found in the resected left adrenal specimen was immunohistochemically compatible with APA. In fact, the suppressed PRA and increased PAC became normalized after left adrenalectomy. This is the very rare case of AIMAH accompanied with APA as confirmed by the histopathological and immunohistochemical analysis. AVS is currently recognized as the gold standard to determine the lateralization of aldosterone hypersecretion in PA. Recently, clinical practice guidelines for case detection, diagnosis and treatment of PA have been recommended, and several diagnostic criteria by AVS have been proposed (5, 9). Unilateral aldosterone hypersecretion is considered on the basis of the following criteria: 1) LR defined as the gradient of aldosteronecortisol ratio (A/C) in the dominant adrenal vein over that in the nondominant adrenal vein after ACTH stimulation is greater than 4 (9), 2) LR in the absence of ACTH stimulation is greater than 2 (9), 3) A/C from adrenal vein is at least 2.5 times greater than that from the peripheral vein and the A/C in the contralateral adrenal vein (CR) is no higher than peripheral vein (CR<1) (9), and 4) absolute value of PAC in adrenal venous effluent is greater than 14,000 pg/ml (5). In the present case, 3 [1, 3 and 4] out of 4 criteria were fulfilled for lateralization of aldosterone hypersecretion from the left adrenal gland. Since LR by A/C could be affected if the asymmetric cortisol hypersecretion takes place, LR by PAC and/or absolute PAC appears more reliable to determine the source of aldosterone hypersecretion under the excessive cortisol secretion by concomitant cortisolsecreting adenoma and/or AIMAH, such as in the present case. Postoperatively, drugresistant hypertension and hypokalemia in the present case were resolved along with the normalization of PRA and PAC after left adrenalectomy. Therefore, it is strongly suggested that APA plays an important role in the development of hypertension and hypokalemia. However, given the elevated urinary excretion of 17OHCS with a normal urinary excretion of free cortisol, it is possible to speculate that intermediate steroids with weak mineralocorticoid activities, such as deoxycorticosterone and corticosterone, excessively secreted from AIMAH may have been partly involved in the development of hypertension in our 230
5 Intern Med 50: , 2011 a. c. HE f. HE d. 3ßHSD g. 3ßHSD b. 3ßHSD ZG ZF e. P450c17 h. P450c17 Figure 3. Histopathological and immunohistochemical analysis of the resected left adrenal specimen. (a) A gross appearance of left adrenal showing multiple nodular lesions, (b) hyperplastic zona glomerulosa cells of nonnodular lesion with negative immunostaining for 3βHSD, (c) macronodules composed of large clear cells and small compact cells with positive immunostaining for (d) 3βHSD and (e) P450c17, and (f) a microadenoma composed of large clear cells with positive immunostaining for (g) 3βHSD, but negative for (h) P450c17 (Magnification 100). case, although we did not study steroid mapping. Although the clinical significance of surgical treatment in patients with AIMAH by either unilateral or bilateral adrenalectomy remains controversial, unilateral adrenalectomy for the removal of APA and hemiside AIMAH was considered reasonable in our case. It has been shown that aberrant and/or exaggerated expression of multiple G proteincoupled receptors, including receptor for gastric inhibitory peptide (GIP), βadrenergic agonist, vasopressin, serotonin, and luteinizing hormone/human chronic gonadotropin (LH/hCG), are involved in the pathogenesis of AIMAH with abnormal proliferation of zona fasciculata cells and with dysregulation of steroidgenesis (1). Recently, it has been shown that the receptors for GIP, LH, thyrotropinreleasing hormone and gonadotropinreleasing hormone aberrantly expressed are functionally related to the abnormal aldosterone secretion in certain APAs (11, 12). It is therefore intriguing to speculate that the expression of common aberrant receptor(s) yetunspecified might be involved in the concurrent development of AIMAH and APA in our case, although further study is needed to prove such assumption. In summary, this is a rare case of AIMAH associated with PA due to unilateral APA, which was localized by a selective AVS and confirmed by the histopathological and immunohistochemical analysis of the resected adrenal specimen, in whom hypokalemia and drugresistant hypertension were resolved after the removal of the affected unilateral adrenal lesion. The authors state that they have no Conflict of Interest(COI). Acknowledgement This study was supported in part by the Grantinaid from the Ministry of Education, Science, Sports and Culture, and the Ministry of Health, Welfare and Labor of Japan. References 1. Lacroix A. ACTHindependent macronodular adrenal hyperplasia. Best Pract Res Clin Endocrinol Metab 23: , Young WF Jr. Minireview:primary aldosteronismchanging concepts in diagnosis and treatment. Endocrinology 144: , Willenberg HS, Spath M, MaserGluth C, et al. Sporadic solitary aldosterone and cortisolcosecreting adenomas: endocrine, histological and genetic findings in a subtype of primary aldosteronism. Hypertens Res 33: , Abe T, Sasaki K, Sugata Y, et al. A case of initial AIMAH leision with multiple aldosteroneproducing nodules. Nippon Naibunpi 231
6 Intern Med 50: , 2011 Gakkai Zasshi (Folia Endocrinol Jpn) 86: 164, 2010 (in Japanese, Abstract). 5. Omura M, Saito J, Yamaguchi K, Kakuta Y, Nishikawa T. Prospective study on the prevalence of secondary hypertension among hypertensive patients visiting a general outpatient clinic in Japan. Hypertens Res 27: , Suzuki H, Okazawa M, Uno T, et al. A case of AIMAH associated with APA. Nippon Naibunpi Gakkai Zasshi (Folia Endocrinol Jpn) 99 (Suppl): 229, 2010 (in Japanese, Abstract). 7. Hayashi Y, Takeda Y, Kaneko K, et al. A case of Cushing s syndrome due to ACTHindependent bilateral macronodular hyperplasia associated with excessive secretion of mineralocorticoids. Endocr J 45: , Yamada Y, Sakaguchi K, Inoue T, et al. Preclinical Cushing s syndrome due to adrenocorticotropinindependent bilateral adrenocortical macronodular hyperplasia with concurrent excess of glucoand mineralocorticoids. Intern Med 36: , Funder JW, Carey RM, Fardella C, et al. Case detection, diagnosis, and treatment of patients with primary aldosteronism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 93: , Nawata H, Demura H, Suda T, Takayanagi R. Adrenal preclinical Cushing s syndrome. In: Annual Report of the Ministry of Health and Welfare [Disorders of Adrenal Hormones]. Research Committee, Japan, 1996: (in Japanese). 11. Zwermann O, Suttmann Y, Bidlingmaier M, Beuschlein F, Reincke M. Screening for membrane hormone receptor expression in primary aldosteronism. Eur J Endocrinol 160: , Lampron A, Bourdeau I, Oble S, et al. Regulation of aldosterone secretion by several aberrant receptors including for glucosedependent insulinotropic peptide in a patient with an aldosteronoma. J Clin Endocrinol Metab 94: , The Japanese Society of Internal Medicine 232
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