FOUR CASES OF HYPOVOLEMIC RENIN-ALDOSTERONE AXIS DEFICIENCY WITHOUT HYPERKALEMIA FOLLOWING UNILATERAL ADRENALECTOMY FOR PRIMARY ALDOSTERONISM

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1 Case Report FOUR CASES OF HYPOVOLEMIC RENIN-ALDOSTERONE AXIS DEFICIENCY WITHOUT HYPERKALEMIA FOLLOWING UNILATERAL ADRENALECTOMY FOR PRIMARY ALDOSTERONISM Marion Vallet, MD 1 *; Alexandre Martin, MD 1 *; Eric Huyghe, MD 2 ; Jacques Amar, MD 3 ; Bernard Chamontin, MD 3 ; Jean Baptiste Kantambadouno 3 ; Ivan Tack, MD 1 ; Béatrice Bouhanick, MD 3 ABSTRACT Objective: Hyperkalemia can occur following unilateral adrenalectomy for primary aldosteronism due to hypoaldosteronism. We hereby report the cases of 4 male patients exhibiting prolonged failure of the renin-aldosterone (RA) axis in association with normal-to-high kalemia or labile blood pressure and, most significantly, a decrease in extracellular fluid volume (ECFV). Methods: Prior to surgery, all patients exhibited hypokalemic hypertension, with documented primary aldosteronism. Within a few weeks of undergoing unilateral adrenalectomy, the patients developed either mild hyperkalemia or labile blood pressure. Complementary investigations revealed a decrease in measured ECFV with inappropriate normal renal sodium excretion, low supine plasma renin activity, and insufficient orthostatic-related aldosterone production. The adrenocorticotropic hormone (ACTH) stimulation test demonstrated no glucocorticoid deficiency, along with responsive aldosterone secretion. Results: The discrepancy between the aldosterone response in the orthostatic position versus the ACTH stimulation test suggested that the aldosterone deficiency Submitted for publication June 17, 2015 Accepted for publication November 24, 2015 From 1 Explorations Fonctionnelles Physiologiques, 2 Département d Urologie, and 3 HTA et THÉRAPEUTIQUE, Hôpital de Rangueil, Toulouse, France. * These authors contributed equally to the work. Address correspondence to Dr. Béatrice Bouhanick, CHU de Rangueil, Service d HTA et THÉRAPEUTIQUE, 1 avenue du Professeur Jean Poulhès - TSA F Toulouse cedex 9, France. duly-bouhanick.b@chu-toulouse.fr. DOI: /EP15874.CR To purchase reprints of this article, please visit: was largely due to RA axis depression. Recovery was confirmed between 3 and 18 months in all but one patient, the latter still requiring mineralocorticoid substitution 23 months later. Conclusion: Following unilateral adrenalectomy for primary aldosteronism, the occurrence of mild hyperkalemia prompted a functional evaluation of the RA system using an orthostatic stimulation test, rather than simply measuring baseline values and evaluating the glucocorticoid axis. In such cases, where RA depression is confirmed to cause latent hypovolemia, all treatments likely to further decrease plasma volume should be avoided, while mineralocorticoid substitution may be required. (AACE Clinical Case Rep. 2016;2:e311-e315) Abbreviations: ACTH = adrenocorticotropic hormone; AVS = adrenal vein sampling; BP = blood pressure; CT = computed tomography; ECFV = extracellular fluid volume; PA = primary aldosteronism; RA = renin-aldosterone INTRODUCTION Primary aldosteronism (PA) is the most common cause of secondary hypertension (1). The current treatment consists of removing the adrenal gland responsible for aldosterone hypersecretion (2). Numerous studies have reported post-unilateral adrenalectomy complications, which can consist of severe hyperkalemia related to adrenal insufficiency (3-9). We hereby report the cases of 4 patients who, despite subnormal kalemia, developed not only temporary aldosterone deficiency, but also prolonged depression of the renin-aldosterone (RA) axis resulting in a decrease in extracellular fluid volume (ECFV) following unilateral adrenalectomy for adenoma or hyperplasia. These observa- AACE CLINICAL CASE REPORTS Vol 2 No. 4 Autumn 2016 e311

2 e312 Renin-Aldosterone Axis Deficiency, AACE Clinical Case Rep. 2016;2(No. 4) tions highlight the value of performing biological followups following surgical PA treatment that include dynamic evaluation of the RA axis. CASE REPORT All but one patient were referred for hypertension to the Department of Internal Medicine and Hypertension of Toulouse University Hospital. All patients exhibited hypokalemia with or without resistant hypertension. PA diagnosis was established according to the ratio of plasma aldosterone concentration (PAC) to active renin, confirmed by either the captopril test (Patients 2 and 3) and/or the intravenous saline infusion test (Patients 3 and 4). Computed tomography (CT) was used to confirm adenoma. Two patients underwent adrenal vein sampling (AVS), and all patients underwent unilateral laparoscopic adrenalectomy. Histological analysis confirmed the presence of an aldosterone-producing adenoma in each patient. We performed postoperative explorations including ECFV measurement using inulin (10) and based our analysis on normal values ranging from 180 to 210 ml/kg (personal data from 10 healthy subjects). This also enabled us to obtain inulin plasma clearance rates. Patient Characteristics Patient 1 This 49-year-old asymptomatic hypertensive male consulted his physician for poor blood pressure (BP) control. Given his hypokalemia, the physician prescribed spironolactone and amlodipine. Hyperaldosteronism was suspected due to his increased aldosterone values, and CT imaging revealed a small right adrenal nodule (Table 1). Surgery was performed but did not resolve the patient s hypertension and hypokalemia, requiring a course of potassium supplementation and treatment with the combination of amiloride plus amlodipine. On Day 15 postsurgery, the patient presented with diarrhea and vomiting, exhibiting acute kidney injury (plasma creatinine = 294 µmol/l) and hyperkalemia (plasma potassium = 6 mmol/l), requiring hospitalization for rehydration and discontinuation of amiloride. His BP was measured at 130/90 mm Hg without any orthostatic symptoms or salt craving. The hyperkalemia persisted at approximately 5.3 mmol/l. At day 49, without any further treatment, significant hypovolemia (ECFV = 108 ml/kg) with an insufficient basal renin level and low PAC were observed (Table 2). Following orthostatic stimulation, the RA system was found to be deficient, whereas a short adrenocorticotropic hormone (ACTH) test demonstrated a mild response regarding aldosterone secretion. The patient was started on 50 μg fludrocortisone per day. At day 98, investigations revealed persistent hypovolemia (ECFV = 137 ml/kg) under fludrocortisone, still with inadequate renin response (supine: 12.3 mui/l; upright: 9.2 mui/l). The fludrocortisone dosage was then increased to 100 µg per day. On day 265, however, the patient suffered a heart attack due to poor adherence to the amlodipine. On day 686, though the fludrocortisone dosage was reduced to 50 µg per day, the investigation revealed no recovery of the RA axis (Table 2) and persistent hypovolemia (ECFV = 121 ml/kg). The fludrocortisone dosage was increased back up to 100 µg per day, at which point the patient was lost to follow-up. Patient 2 This 67-year-old male presented with poor BP control that gradually worsened despite tritherapy with ramipril, bisoprolol, and amlodipine. Hypokalemia and PA were diagnosed (Table 1). An abdominal CT scan revealed a right adrenal mass. Spironolactone (aldactone) was added preoperatively then discontinued for surgery. In the days following the operation, the patient continued to exhibit hypertension, requiring amlodipine and bisoprolol. A few weeks later, hyperkalemia at 6 mmol/l was detected. The patient remained asymptomatic without asthenia or vertigo and his clinostatic and orthostatic BPs were 130/75 and 130/85 mm Hg, respectively. Glucocorticoid deficiency was suspected and hydrocortisone substitution was initiated, despite the short ACTH stimulation test coming back normal. On day 51 postsurgery, our examinations revealed hypovolemia (ECFV = 165 ml/kg) with low supine renin, inadequate renin response, and low aldosterone (Table 2). Hydrocortisone was progressively phased out. On day 238, his ECFV remained slightly low (163 ml/kg), yet the RA axis had returned to normal, and his BP was efficiently controlled with dual therapy (amlodipine and bisoprolol). Patient 3 This 55-year-old male displayed resistant hypertension despite undergoing a course of 5 antihypertensive drugs: valsartan, hydrochlorothiazide, atenolol, nitrendipine, and urapidil. Hypokalemia was discovered on later tests and PA was diagnosed (Table 1). CT imaging revealed a left adrenal node, while AVS confirmed lateralization of secretion. Spironolactone was added to the treatment course prior to surgery and withdrawn for the operation. No electrolyte disorders requiring medication occurred following surgery, and his BP normalized to around 125/85 mm Hg without requiring any treatment. The patient was completely asymptomatic. On day 61, moderate hypovolemia (ECFV = 166 ml/kg) and an inadequate RA response were observed (Table 2). He was not treated with fludrocortisone, but was advised to avoid diuretics and renin-angiotensin blockers, and was instructed to follow a normal saline diet. The day 527 exploration revealed normovolemia, complete recovery of the RA axis, and normal BP that did not require treatment. Patient 4 This 42-year-old male exhibited hypertension and hypokalemia and was started on verapamil, lercanidip-

3 Renin-Aldosterone Axis Deficiency, AACE Clinical Case Rep. 2016;2(No. 4) e313 Table 1 Preoperative Patient Characteristics Patient 1 Patient 2 Patient 3 Patient 4 Normal values Age (years) Male/Female (M/F) M M M M - Duration of hypertension (years) Office SBP/DBP (mm Hg) 150/90 160/90 135/70 160/ hour ABPM SBP/DBP (mm Hg) MD 143/86 155/95 132/85 - Plasma creatinine (µmol/l) egfr (ml/min/1.73 m 2 ) >90 Plasma sodium (mmol/l) Plasma potassium (mmol/l) Supine/upright plasma renin 1-hour (mui/l) Supine/upright plasma aldosterone 1-hour (ng/l) Supine plasma aldosterone/renin ratio (ng/l per mui/l) MD 2.2 / / / / / MD 206 / / / / MD <23 Histopathology A A + H A A - Abbreviations: A = adenoma; ABPM = ambulatory blood pressure monitoring; DBP = diastolic blood pressure; egfr = estimated glomerular filtration rate using the Chronic Kidney Disease Epidemiology Collaboration formula; H = hyperplasia; MD = missing data; SBP = systolic blood pressure. ine, and amiloride. PA was diagnosed (Table 1) and a CT scan revealed a right adrenal node. Surgery was scheduled following confirmation of aldosterone secretion lateralization by AVS. The patient s BP rapidly improved as a result, requiring only verapamil, and his kalemia normalized. On day 42, he developed alternating episodes of hypotension and hypertension. As a result of what we had learned from Patient 1 s history, this symptom prompted us to measure ECFV. Hypovolemia was discovered (ECFV = 167 ml/ kg), along with an inadequate RA response (Table 2). As with Patient 3, no fludrocortisone was started and the same dietary and medication advice was offered. The day 93 tests revealed regressed hypovolemia (ECFV = 193 ml/kg) and a fully-recovered RA axis (Table 2), with verapamil still required for BP control. DISCUSSION In the context of unilateral adrenalectomy for PA, the discovery of normal to high plasma potassium (4.5 mmol/l) or labile BP could indicate a temporarily insufficient adaptation of the remaining adrenal gland. Such a situation has been reported in previous studies and has been attributed to a transient or prolonged hypoaldosteronism associated with a discrepancy between plasma renin levels and a lack of information concerning volemic status (3-8). We have hereby reported the cases of 4 patients presenting with normal to high kalemia associated with transient (n = 3) or prolonged (n = 1) failure of the RA axis. In these cases, subnormal kalemia and labile BP manifested within a few weeks of surgery, leading us to initiate complementary investigations. Our main findings were as follows: (1) a constant decrease in the ECFV with persistent inappropriate renal excretion of sodium was responsible for reversible impaired renal function in one case, (2) insufficient supine plasma-renin concentration was poorly stimulated in response to the upright position, (3) low baseline plasma aldosterone was unstimulated in an orthostatic test but was responsive to the ACTH stimulation test, and (4) in contrast, normal baseline plasma cortisol levels were found in all but one patient, and were shown to be normally increased by a short ACTH stimulation test. The discrepancy in the aldosterone response, namely pertaining to the orthostatic position versus the ACTH stimulation test, suggests that hypoaldosteronism primarily results from the lack of angiotensin II stimulation as a result of hyporeninism. These findings also indicate that PA can induce prolonged RA axis depression without systematic glucocorticoid deficiency. All 4 patients were male, supporting the belief that this gender is predisposed to such conditions as suggested by Chiang et al (8). The influence of postoperative treatments, such as beta-blockers or fludrocortisone, on the status of the RA axis cannot be ruled out. Nevertheless, the patient receiving fludrocortisone exhibited persistent decreased ECFV along with normal to high kalemia, indicating a persistent mineralocorticoid deficiency as opposed to an excess of fludrocortisone inhibiting the RA axis. Although the risk of postoperative hyperkalemia

4 e314 Renin-Aldosterone Axis Deficiency, AACE Clinical Case Rep. 2016;2(No. 4) Table 2 First and Last Postoperative Explorations Patient 1 Patient 2 Patient 3 Patient 4 Exploration First Last First Last First Last First Last Normal values Days postsurgery egfr (ml/min/1.73m 2 ) >90 mgfr (ml/min/1.73m 2 ) >90 ECFV (ml/kg) Plasma Na (mmol/l) Plasma K (mmol/l) Arterial HCO 3 (mmol/l) MD - Plasma glucose (mmol/l) Urinary Na (mmol/24 h) Urinary K (mmol/24 h) Fasting urinary Na/K ratio Supine/upright plasma renin 1-hour (mui/l) Supine/upright plasma aldosterone 1-hour (ng/l) Plasma aldosterone pre-/ post-acth (ng/l) Plasma cortisol pre-/post- ACTH (µ/100ml) 5.5 / / / MD 17.3 / / / / / / / <11 18 / 26 <10 / / / / / / / / 41 MD <20 / / 107 <20 / 48 MD 19 / / / / / / / / / / Abbreviations: ACTH = adrenocorticotropic hormone; ECFV = extracellular fluid volume; egfr = estimated glomerular filtration rate using the Chronic Kidney Disease Epidemiology Collaboration formula; h = hour; HCO 3 = bicarbonate; K = potassium; MD = missing data; mgfr = measured glomerular filtration rate; Na = sodium.

5 Renin-Aldosterone Axis Deficiency, AACE Clinical Case Rep. 2016;2(No. 4) e315 has been clearly related to the duration of hypertension and pre- or postoperative impaired renal function (6,8,9) as reported in Patient 1, we found that the RA axis can be deficient, even in patients with normal renal function and in the absence of hyperkalemia. The 4 patients reported herein represent 15% of the patients that underwent surgery for PA in our department during the study period. However, since ECFV measurement and postoperative RA axis explorations were not performed systematically, we cannot exclude the possibility that the prevalence of temporary RA axis deficiency was underestimated, as progressive and moderate decreases in ECFV are almost undetectable by clinical examination (11). We believe it possible that ACTH-stimulated aldosterone secretion could play a role in these cases, as the ACTH stimulation test was slightly responsive in these patients. However, the concomitant lack of aldosterone response during the orthostatic tests suggests that ACTH was probably not recruited in our patients when in the upright position. Such a discrepancy could result from an inadequate orthosympathetic response, as described in other studies of diabetic patients with hyporeninemic hypoaldosteronism (12,13). In conclusion, RA system depression can occur following unilateral adrenalectomy and should be investigated not only in hyperkalemic patients, but also in those with normal to high kalemia ( 4.5 mmol/l). As a result, actions with the potential to further decrease plasma volume (i.e., diuretic therapy or sodium-restricted diets) must be avoided so as to prevent symptomatic hypovolemia and functional renal insufficiency. We propose that, rather than an ACTH test, the RA axis should be functionally challenged by means of an orthostatic stimulation test. ACKNOWLEDGMENT The manuscript was written by M.V., A.M., I.T., and B.B., with all coauthors approving the final version. E.H. performed the surgeries. J.B.K., J.A., and B.C. recruited the patients. DISCLOSURE REFERENCES 1. Ganguly A. Primary aldosteronism. N Engl J Med. 1998;339: 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. 2008;93: Taniguchi R, Koshiyama H, Yamauchi M, et al. A case of aldosterone-producing adenoma with severe postoperative hyperkalemia. Tohoku J Exp Med. 1998;186: Huang WT, Chau T, Wu ST, Lin SH. Prolonged hyperkalemia following unilateral adrenalectomy for primary hyperaldosteronism. Clin Nephrol. 2010;73: Gadallah MF, Kayyas Y, Boules F. Reversible suppression of the renin-aldosterone axis after unilateral adrenalectomy for adrenal adenoma. Am J Kidney Dis. 1998;32: Fischer E, Hanslik G, Pallauf A, et al. Prolonged zona glomerulosa insufficiency causing hyperkalemia in primary aldosteronism after adrenalectomy. J Clin Endocrinol Metab. 2012;97: Hibi Y, Hayakawa N, Hasegawa M, et al. Unmasked renal impairment and prolonged hyperkalemia after unilateral adrenalectomy for primary aldosteronism coexisting with primary hyperparathyroidism: report of a case. Surg Today. 2015;45: Chiang WF, Cheng CJ, Wu ST, et al. Incidence and factors of post-adrenalectomy hyperkalemia in patients with aldosterone producing adenoma. Clin Chim Acta. 2013;424: Park KS, Kim JH, Ku EJ, et al. Clinical risk factors of postoperative hyperkalemia after adrenalectomy in patients with aldosterone-producing adenoma. Eur J Endocrinol. 2015;172: Bröchner-Mortensen J, Giese J, Rossing N. Renal inulin clearance versus total plasma clearance of 51Cr-EDTA. Scand J Clin Lab Invest. 1969;23: Chung HM, Kluge R, Schrier RW, Anderson RJ. Clinical assessment of extracellular fluid volume in hyponatremia. Am J Med. 1987;83: Kuhlmann U, Vetter W, Fischer E, Siegenthaler W. Control of plasma aldosterone in diabetic patients with hyporeninemic hypoaldosteronism. Klin Wochenschr. 1978;56: Elisaf MS, Tomos PP, Milionis HJ, Siamopoulos KC. Prerenal azotemia in a diabetic patient with hyporeninemic hypoaldosteronism and autonomic neuropathy. Diabetes Metab. 1999;25: The authors have no multiplicity of interest to disclose.

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