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1 AJH 1998;11:8 13 Acute Effects of Intravenous Sodium Chloride Load on Calcium Metabolism and on Parathyroid Function in Patients With Primary Aldosteronism Compared With Subjects With Essential Hypertension Ermanno Rossi, Franco Perazzoli, Aurelio Negro, Carlo Sani, Simona Davoli, Claudio Dotti, Maria Cristina Casoli, and Giuseppe Regolisti To elucidate the mechanisms involved in increased parathyroid function in primary aldosteronism (PA), we evaluated the effects of an intravenous NaCl load on Ca metabolism and plasma level of intact parathyroid hormone (PTH) in patients with PA compared with that in patients with essential hypertension (EH). Sixteen PA patients and 16 EH patients who were well matched for age, gender, body mass index, renal function, and systolic (SBP) and diastolic blood pressure (DBP) were examined. In each subject, after 6 days of a controlled intake of Na, K, and Ca, isotonic saline was infused at a rate of 500 ml/h for 4 h. At baseline, in spite of similar BP values and urinary Na excretion (U Na V), urinary excretion of Ca (U Ca V) and PTH were higher in the PA group than in the EH group. In both groups, the NaCl load caused a decrease of serum ionized Ca (Ca 2 ) and an increase in PTH, U Na V, and U Ca V. However, these changes were significantly greater in the PA group. The increased baseline U Ca V in PA could be due to reduced reabsorption of sodium in aldosterone insensitive tubular sites, as a result of the escape phenomenon. The increased U Ca V may explain the higher basal PTH in PA patients, which is needed for maintaining a normal Ca 2. The greater changes in the Ca 2 /PTH profile elicited by the saline load in PA patients are apparently due to a higher calciuretic response following a more exaggerated natriuresis in PA. Am J Hypertens 1998;11: American Journal of Hypertension, Ltd. KEY WORDS: Intact parathyroid hormone, serum ionized calcium, urinary calcium excretion, primary aldosteronism, essential hypertension. Received July 22, Accepted July 15, From the Fourth Department of Internal Medicine, (ER, FP, AN, CS, SD, MCC, GR), and Laboratory of Endocrinology, S. Maria Nuova Hospital, Reggio Emilia, Italy. Address correspondence and reprint requests to Dr Ermanno Rossi, IV Divisione di Medicina Interna, Ospedale S. Maria Nuova, Padiglione L. Spallanzani, Viale Umberto I, N. 50, Reggio Emilia, Italy by the American Journal of Hypertension, Ltd /98/$19.00 Published by Elsevier Science, Inc. PII S (97)00366-X
2 AJH JANUARY 1998 VOL. 11, NO. 1, PART 1 NaCl, Ca, AND PTH IN PRIMARY ALDOSTERONISM 9 Alterations of calcium metabolism and parathyroid function, namely reduced concentration of serum ionized calcium (Ca 2 ), increased urinary calcium excretion, and elevated circulating level of parathyroid hormone, have been reported in both essential hypertension (EH) 1 3 and primary aldosteronism (PA). 4,5 In a previous study, we observed that in both patients with PA and subjects with EH, Ca 2 is lower than in normotensive controls. However, only in patients with PA intact serum PTH 1 84 (PTH) was higher than in normotensive subjects. Furthermore, in the former group, an increase in Ca 2 and a decrease in PTH were associated with both spironolactone administration and surgical treatment. 5 To elucidate better the mechanisms involved in the altered Ca 2 /PTH profile in PA, we evaluated the acute effects of an intravenous NaCl load on calcium metabolism and PTH in patients with PA compared to patients with EH, all subjects having being submitted to the same intake of Na, K, and Ca in the week preceding the NaCl load. SUBJECTS AND METHODS Sixteen patients with PA, 31 to 71 years of age, and 16 patients with EH, aged 33 to 69 years, were included in the study. The two groups were well matched for age, sex, body mass index (BMI), renal function, systolic (SBP) and diastolic blood pressure (DBP). PA was defined by the presence of each of the following findings: plasma aldosterone (ng/dl)/renin activity (ng/ ml/h) ratio 30 in the sitting position on three consecutive occasions; plasma renin activity (PRA) 1 ng/ml/h in the upright posture for 2 h, after 5 days of a sodium restricted diet; plasma aldosterone 7.5 ng/dl at the end of an intravenous load of 2Lof isotonic saline at an infusion rate of 500 ml/h; and upright plasma aldosterone (ALDO) 5 ng/dl after 5 days of fludrocortisone acetate administration (0.1 mg every 6 hours). Glucocorticoid-suppressible aldosteronism was excluded by a dexamethasone test. Adrenal lesions were assessed by high-resolution thin section computer tomography and dexamethasone suppressed scintigraphy with 131 I-6- -iodomethylnorcholesterol. Unilateral adrenal lesions were diagnosed in nine patients. Adrenocortical adenomas were found in the seven patients so far submitted to unilateral adrenalectomy. Idiopathic aldosteronism was presumed on the basis of the absence of a unilateral lesion in both computer tomographic and scintigraphic scanning in the other seven patients. EH was established after exclusion of secondary hypertension on the basis of appropriate clinical and laboratory evaluation. Antihypertensive drugs were discontinued 4 weeks before the beginning of the study. No subject had previously been treated with diuretics, spironolactone, or other potassium sparing drugs. For the purpose of the matching, the individual SBP and DBP were taken as the average of six office measurements in the seated position on three different visits in the 2 weeks before the beginning of the study. In the same period, endogenous creatinine clearance was determined in all subjects. All PA patients had DBP 90 mm Hg, and a DBP 90 mm Hg was used for the selection of patients with essential hypertension. All subjects were placed on a diet containing 110 mmol/day of sodium, 70 mmol/day of potassium, and 650 mg/day of calcium for 6 days. On the seventh day, following an overnight fast, isotonic saline was infused intravenously at a rate of 500 ml/h for 4 h from 8 am to noon. Four-hour urine samples were collected from 4 am to 8 am and from 8 am to noon. Venous blood samples were collected and blood pressures were measured immediately before and at the end of the saline load. Individual blood pressures were considered the mean of six recordings 2 minutes apart. The two urine samples were used to measure urinary output, creatinine, sodium, potassium, and calcium. The two blood samples were used to measure serum sodium, potassium, Ca 2, creatinine, plasma renin activity (PRA), plasma aldosterone (ALDO) and parathyroid hormone (PTH). For each of the two periods creatinine clearance and fractional excretion of sodium (Na clearance/creatinine clearance ratio 100) were calculated. All subjects gave their informed consent; the protocol was approved by the local ethical committee. Blood pressure was measured with a standard mercury sphygmomanometer, using Korotkoff phase V for diastolic blood pressure. Intact serum PTH (PTH 1 84 ) was measured using commercially available radiometric assay kits (Diagnostic Products Corporation, Los Angeles, CA). PRA was evaluated by radioimmunoassay (Sorin Biomedica, Saluggia, Italy) through quantitative determination of angiotensin I. Plasma ALDO was also measured by radioimmunoassay (Diagnostic System Laboratories, Webster, TX). Serum Ca 2 was measured with an ion selective electrode, with values adjusted to ph 7.4. Statistics Statistical analysis was primarily based on two-way analysis of variance (ANOVA) with repeated measures, with group (PA and EH) and time (before and after saline load) as main factors. If ANOVA yielded a significant result, post hoc comparisons were carried out with paired or unpaired Student s t test as appropriate. Percent changes in a given variable after saline load as compared with baseline were compared by unpaired t test. Data are shown as means SEM. A P.05 was considered statistically significant.
3 10 ROSSI ET AL AJH JANUARY 1998 VOL. 11, NO. 1, PART 1 TABLE 1. BLOOD PRESSURE AND LABORATORY VALUES BEFORE (BASELINE) AND AFTER SALINE LOAD Baseline After Saline Load ANOVA Table PA EH PA EH Group Time G T ALDO, ng/ml # F 1, P NS PRA, ng/ml/h # * *# F 1, P Ca 2, mmol/l # F 1, P PTH, pg/ml * F 1, P U Ca V, mg/h # F 1, P U Na V, mmol/h ** F 1, P U K V, mmol/h F 1, P NS.0001 NS FENa, % ** F 1, P V, ml/h F 1, P NS.0001 NS CrC1, ml/min/1.72 m * F 1, P NS.0001 NS SBP, mm Hg F 1, P NS NS NS DBP, mm Hg F 1, P NS NS NS PA, primary aldosteronism; EH, essential hypertension; ALDO, plasma aldosterone; PRA, plasma renin activity; Ca 2, serum ionized calcium; PTH, parathyroid hormone; U Ca V, U Na V, U K V, urinary calcium, sodium, and potassium excretion rate; FENa, fractional excretion of sodium; V, urinary flow rate; CrC1, creatinine clearance; SBP, systolic blood pressure; DBP, diastolic blood pressure. *P.05; P.01; P.001 v baseline by paired t test; ** P.05; #P.01; P.001 v PA by unpaired t test. RESULTS Patients with PA and EH were similar in age ( v years), gender distribution (M/F 8/8 v 8/8), BMI ( v kg/m 2 ), creatinine clearance, SBP, and DBP (Table 1). Serum potassium was lower in the PA group ( v mmol/l, P.05). Hemodynamic and laboratory data recorded before and after saline infusion are summarized in Table 1. In the 4 h baseline period, SBP, DBP, urinary output (V), urinary sodium (U Na V), and potassium (U K V) excretion rates, creatinine clearance (CrC1), fractional excretion of sodium (FENa), and serum Ca 2 did not differ between the two groups. However, at baseline, urinary excretion of calcium and PTH were higher in the PA than in the EH group. The saline load did not affect blood pressures. In both groups creatinine clearance was only slightly though significantly increased, whereas urine output markedly rose. The saline load elicited a significant increase in urinary calcium excretion rate in both groups as compared with baseline; however, this increase was proportionally greater in the patients with PA (Figure 1, panel A). Accordingly, serum Ca 2 decreased more and PTH secretion was more actively stimulated after the saline load in patients with PA as compared with those with EH (Figure 1, panels B and C). Urinary sodium excretion rate (Table 1) and FENa (Figure 1, panel D) were also more strongly enhanced in patients with PA, whereas a parallel increase in the urinary excretion of potassium was observed in the two groups. DISCUSSION Our study demonstrates firstly that both baseline urinary excretion of calcium and PTH are higher in primary aldosteronism than in essential hypertension, in the face of equal dietary intakes of calcium and sodium, and similar excretion rates of sodium (Table 1). The higher baseline U Ca V is consistent with the increase of U Ca V observed in both animals 6 and humans 7 after long-term mineralocorticoid administration, as well as with the higher U Ca V reported in patients with PA compared with that in normotensive control subjects. 8 However, this increase in urinary
4 AJH JANUARY 1998 VOL. 11, NO. 1, PART 1 NaCl, Ca, AND PTH IN PRIMARY ALDOSTERONISM 11 FIGURE 1. Percent changes in urinary calcium excretion rate (U Ca V, panel A), serum ionized calcium (Ca 2, panel B), parathyroid hormone (PTH, panel C), and fractional excretion of sodium (FENa, panel D) after the saline load as compared with baseline. EH, essential hypertension; PA, primary aldosteronism. *P.05; **P.01 by unpaired t test. calcium excretion associated with mineralocorticoid excess does not seem due to direct effects of aldosterone. Indeed, the increase of U Ca V requires volume expansion and the consequent escape phenomenon, as neither animals submitted to chronic mineralcorticoid administration 6 nor humans with PA 8 exhibit higher calcium excretion rates when sodium intake is substantially restricted. The increased U Ca V in PA
5 12 ROSSI ET AL AJH JANUARY 1998 VOL. 11, NO. 1, PART 1 could be due to reduced reabsorption of calcium following a reduced reabsorption of sodium in aldosterone-insensitive proximal tubular sites, where sodium handling is closely connected with that of calcium. In this case, the increased calcium excretion would be the result of the escape phenomenon elicited by plasma volume expansion. Some evidence suggests, however, that other possible mechanisms may be involved in mediating the increased calcium excretion. Micropuncture studies in escaped hypertensive saline expanded rats receiving DOCA, compared with hypertensive saline expanded control rats, have indicated a reduced calcium reabsorption in sites beyond the distal late tubule. 9 Moreover, clearance studies in the same animal model have demonstrated that either parathyroidectomy or parathyroid hormone administration following parathyroidectomy fail to alter calcium excretion, suggesting the absence of the anticalciuric effect of parathyroid hormone in the escape phase of mineralcorticoid excess. 9 The inhibition of calcium reabsorption in sites beyond the distal tubule could also follow the inhibition of sodium reabsorption on collecting ducts by atrial natriuretic peptide (ANP). 10 Indeed, the rise in plasma ANP associated with the escape phenomenon in patients with PA is accompanied by an increase in urinary calcium output. 11 Even the lower serum potassium level in PA patients compared to EH patients could contribute to the altered calcium metabolism in PA. In fact, hypokalemia following potassium deprivation in subjects with EH increases both urinary calcium excretion and plasma PTH levels. 12 On the other hand, these effects could be partly secondary to sodium retention and extracellular volume expansion following potassium depletion. Moreover, renal cysts in the collecting ducts and interstitial scarring, reported in PA patients and attributed to chronic hypokalemia, 13 could also adversely affect the tubular reabsorption of calcium. The increased calcium excretion, with the consequent trend towards a decrease of serum Ca 2, may explain the higher basal PTH level in PA patients, needed for restoring and maintaining normal or low normal serum Ca 2. In both PA and EH patients, intravenous saline load caused an increase in serum PTH levels and urinary calcium excretion rate, together with a reduction of serum Ca 2. However, the changes of U Ca V, serum Ca 2 and PTH were greater in PA patients (Figure 1). These changes were associated with a greater increase in sodium excretion in response to the saline load in PA patients, which is consistent with the more exaggerated natriuretic response to an acute volume expansion reported in PA compared with that in EH. 14 Considering the well known dependence of renal calcium reabsorption on sodium reabsorption, the calciuretic response to the intravenous saline load observed in both groups of patients may be the result of sodium reabsorption inhibition elicited by the acute intravascular volume expansion resulting from the saline load, whereas the greater calciuretic response in PA patients could follow a more exaggerated inhibition of sodium reabsorption in PA. In these patients, an amplification of the same factors responsible for the escape phenomenon and the higher calcium excretion in conditions of steady sodium balance is conceivable; in particular, patients with PA exhibit a greater increase in plasma ANP than patients with EH in response to acute saline load. 14 The combination of increased calcium excretion and hemodilution resulting from the saline infusion seems to explain the reduction of serum Ca 2 in both groups of patients. However, the greater decrease of serum Ca 2 in PA apparently depends exclusively on the higher calcium excretion. Indeed, in PA patients the extracellular volume increase following the saline load seems more attenuated than in EH patients, as indicated by the higher increase in sodium excretion. Finally, the reduction in serum Ca 2 explains the appropriate increase in PTH levels following the saline load in both groups of patients, the higher levels observed in PA being dependent on the lower serum Ca 2. Similar but less pronounced alterations of calcium metabolism have been reported in patients with lowrenin EH as compared with normotensive subjects and patients with normal and high renin EH. 2,3 Even the increase in calcium excretion following an intravenous salt load is greater in patients with NaCl sensitive and low renin EH than in subjects with NaCl resistant EH. 15 Our results in PA patients indirectly support the role of extracellular volume expansion in the altered calcium metabolism reported in low renin or NaCl sensitive EH, as PA represents a prototype of volume dependent hypertension. In conclusion, our results indicate an altered calcium metabolism and enhanced parathyroid function in patients with PA compared with that in patients with EH. These alterations seem to be strictly dependent on the alterations of sodium metabolism and extracellular volume, and could be mediated by the escape phenomenon and by the exaggerated natriuresis in response to an acute saline load. REFERENCES 1. McCarron DA, Pingree PA, Rubin RJ, et al: Enhanced parathyroid function in essential hypertension: a homeostatic response to a urinary calcium leak. Hypertension 1980;2: Resnick LM, Laragh JH, Sealey JE, et al: Divalent cations in essential hypertension: relations between serum ionized calcium, magnesium, and plasma renin activity. N Engl J Med 1983;309:
6 AJH JANUARY 1998 VOL. 11, NO. 1, PART 1 NaCl, Ca, AND PTH IN PRIMARY ALDOSTERONISM Resnick LM, Muller FB, Laragh JH: Calcium regulating hormones in essential hypertension: relation to plasma renin activity and sodium metabolism. Ann Intern Med 1986;105: Resnick LM, Laragh JH: Calcium metabolism and parathyroid function in primary aldosteronism. Am J Med 1985;78: Rossi E, Sani C, Perazzoli F, et al: Alterations of calcium metabolism and of parathyroid function in primary aldosteronism, and their reversal by spironolactone or by surgical removal of aldosterone-producing adenomas. Am J Hypertens 1995;8: Suki WN, Schwettmann RS, Rector FC, et al: Effect of chronic mineralcorticoid administration on calcium excretion in the rat. Am J Physiol 1968;215: Cappuccio FP, Markandu ND, Mac Gregor, GA: Renal handling of calcium and phosphate during mineralcorticoid administration in normal subjects. Nephron 1988;48: Rastegar A, Agus Z, Connor TB, et al: Renal handling of calcium and phosphate during mineralcorticoid escape in man. Kidney Int 1972;2: Gehr MK, Goldberg M: Hypercalciuria of mineralcorticoid escape: clearance and micropuncture studies in the rat. Am J Physiol 1986;251: Zeidel ML: Hormonal regulation of inner medullary collecting duct sodium transport. Am J Physiol 1993; 265:F159 F Nakamura T, Ichikawa S, Sakamaki T, et al: Role of atrial natriuretic peptide in mineralcorticoid escape phenomenon in patients with primary aldosteronism. Proc Exp Biol Med 1987;185: Krishna GC, Kapoor SC: Potassium depletion exacerbates essential hypertension. Ann Intern Med 1991;115: Torres VE, Young WFJ, Offord KP, et al: Association of hypokalemia, aldosteronism and renal cysts. New Engl J Med 1990;322: Kawabe H, Furukawa T, Saito I, et al: Importance of atrial natriuretic hormone in an exaggerated natriuresis during acute sodium load in primary aldosteronism. Acta Endocrinol 1992;126: Galletti F, Ferrara I, Stinga F, et al: Effect of intravenous sodium chloride on renal sodium and calcium handling in hypertensive patients with different sensitivities to sodium chloride. J Hypertens 1993;11(suppl 5):
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