THE RENAL HANDLING OF PHOSPHATE IN THYROID DISEASE
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1 THE RENAL HANDLING OF PHOSPHATE IN THYROID DISEASE B. MALAMOS, P. SFIKAKIS and P. PANDOS Department of Clinical Therapeutics of the Athens Medical School, Alexandra Hospital, Athens, Greece (Received 18 March 1969) SUMMARY The fasting serum phosphate level, the tubular maximal (Tm) phosphate reabsorption and the mean renal phosphate threshold were measured in 18 hyper- and six hypothyroid patients in comparison with 11 euthyroid control subjects. A significant increase of serum inorganic phosphate, phosphate Tm and of the mean renal phosphate threshold were found in hyperthyroidism. These findings suggest an increased tubular reabsorption of phosphate in hyperthyroidism. Four main possible mechanisms of such a renal handling of phosphate in thyroid disease are briefly mentioned although their acceptance needs more direct proof. INTRODUCTION Calcium and phosphorus metabolism in thyroid disease have been extensively studied in recent years in an attempt to clarify the pathogenesis of bony lesions, especially in hyperthyroidism. Usually, calcium and phosphorus blood levels are found within normal limits in hyperthyroidism. However, other studies (Aub, Bauer, Heath & Ropes, 1929; Stanley & Fazekas, 1949; Rose & Boles, 1953; Pribek & Meade, 1957 ; Koenig, Scholz & Salassa, 1957 ; Sallin, 1958; Bortz, Eisenberg, Bowers & Pont, 1961 ; Adams, Jowsey, Kelly, Riggs, Kinney & Jones, 1967) have shown that the concentration of blood calcium is sometimes increased in hyperthyroidism, but that it is unlikely that thyroxine has any action on the parathyroids. The ionized portion of plasma calcium may be more frequently increased in hyperthyroidism, even in normocalcaemic cases. This is attributable to the slight hypoproteinaemia often observed in hyperthyroidism (Man, Gildea & Peters, 1940; Buchanan, Koutras, Alexander & Crooks, 1962). The level of blood phosphorus has also been reported to be increased in some cases of hyperthyroidism (Cook, Nassim & Collins, 1959; Par sons & Anderson, 1964; Adams et al. 1967). This paper is concerned with further attempts to study the renal handling of phosphate in hyper-, hypo- and euthyroid subjects, on the basis of the tubular maxi mal phosphate reabsorption (TmP) and the mean renal phosphate threshold deter mination. In addition fasting serum phosphate level was determined in the same subjects. * Present address: First Department of Propedeutic Medicine, King Paul's Hospital, Athens 609, Greece.
2 MATERIAL AND METHODS Eighteen hyperthyroid (7 men, 11 women), six hypothyroid (3 men, 3 women) and eleven euthyroid control subjects (4 men, 7 women) were included in this study. All patients were untreated. In all of them the renal handling of inorganic phosphate was assessed during the intravenous infusion of a 1 % phosphate solution, according to a variation of Anderson's method for estimating the tubular maximal reabsorption of phosphate (Anderson, 1955). None of the individuals studied had clinical and/or laboratory findings indicative of renal, hepatic or cardiac disease and the women were not menstruating. The mean age was comparable in the three groups studied. In all cases the fasting serum phosphate level was determined 1-3 days before the infusion. The renal handling of inorganic phosphate was studied by assessment of the tubular maximal reabsorption of phosphate and the mean renal phosphate threshold. Both were estimated by infusing intravenously 1 % inorganic phosphate solution during water diuresis. The infusion was performed at a precalculated slowly increasing rate. Thus a practically linear increase in the serum phosphate level was obtained. Urine was collected at four 30-min. intervals and blood samples were taken at the mid points of the urine collection periods. The infusion was performed in the morning on fasting subjects because (a) the renal phosphate excretion is minimal and more constant in the morning (Dean & McCance, 1948) and (6) because the postprandial hyperglycaemia decreases the tubu lar reabsorption of inorganic phosphate (Eggleton & Shuster, 1954). In contrast to the method of Anderson (1955), in which the infusion lasts 3 hr., the infusion time in our subjects was limited to 2 hr. for two reasons : (a) after 150 min. from the begin ning of the infusion the TmP starts to decline possibly because parathyroid excretion is inhibited and (6) because the highest serum phosphate level in all our patients was always below 12 mg./100 ml. A phosphate level exceeding 12 mg./100 ml. was avoided because whenever this level is exceeded a portion of phosphate binds with calcium and proteins and becomes non-filtrable through the glomeruli (Walser, 1960). Inorganic phosphate was determined in blood and urine samples according to the method of Fiske & Subbarow (1925) and TmP and the mean phosphate threshold were then calculated. The statistical significance of the differences observed in the three groups studied was assessed by Student's 't' test. RESULTS Figure 1 shows the fasting serum phosphate level which averaged (s.d.) mg./100 ml. in the hyperthyroid patients, mg./100 ml. in the euthyroid patients and mg./100 ml. in the hypothyroid subjects. The differences between the hyper- and hypothyroid groups from the euthyroid controls are statisti cally significant (P < and < 0-05, respectively, Fig. 1). The values for phosphate Tm averaged mg./min. in the hyperthyroid group, mg./min. in the controls and 2-90 ± 0-60 mg./min. in the hypo thyroid subjects (P < and < 0-01, respectively, Fig. 2). The mean renal phosphate threshold (Fig. 3) was 4-51 ± 0-66 mg./100 ml. in the
3 thyrotoxic patients, mg./100 ml. in the controls and 3-10 ± 0-60 mg./ 100 ml. in the hypothyroid group (P < and < 0-025, respectively, Fig. 3). In general, the differences were more significant when the comparison was made between the hyperthyroid patients and the controls than between the hypothyroid patients and the controls. E 6 _ M 5 E, I <0 001 <0 05 Fig. 1 < 0001 <0 01 Fig. 2 o o 3- * : 2- P<0001 P<0025 Fig. 3 Figs Fasting serum phosphate levels (Fig. 1), tubular maximal phosphate résorption (Fig. 2) and mean renal phosphate threshold (Fig. 3). 1 = Hyperthyroid patients ; 2 = euthyroid subjects; 3 = hypothyroid patients.
4 discussion A minor but not negligible aspect of the physiological action of thyroid hormones and their analogues is the handling of water and electrolytes in thyroid disease. Both the cardiac and renal effects of thyroxine deficiency explain the accumulation of subcutaneous fluid in myxoedema which is matched by an early polyuria and dis appearance of oedema during replacement therapy. In addition, thyroxine has been shown to increase glomerular filtration and to diminish the tubular reabsorption of water, probably by interference with the effectiveness of the antidiuretic hormone of the posterior pituitary (Hare, Phillips, Bradshaw, Chambers & Hare, 1944). Further more, a generalized increase in renal function in thyroxine-treated animals shown by increased creatinine clearance, glucose Tm and diodrast Tm, has been found (Eiler, Althausen & Stockholm, 1944). Reports on the influence of thyroid disease on phosphate metabolism are contro versial. An increased serum inorganic phosphate level has been reported recently by Parsons & Anderson (1964) and Adams et al. (1967), while Aub et al. (1929) and Har den, Harrison, Alexander & Nordin (1964) found normal serum phosphate levels in hyperthyroidism. Robertson (1942) found lower phosphate levels in hyperthyroidism. In our study the fasting serum phosphate in hyperthyroidism was increased as compared with euthyroid subjects. In contrast, the serum phosphate level was found to be decreased in hypothyroidism as compared with the controls. These findings agree with the findings of Parsons & Anderson (1964) and Adams et al. (1967). Parsons and Anderson think that the serum level of inorganic phosphate reflects in some way the severity of hyperthyroidism. Both TmP and the mean renal phosphate threshold were significantly increased in hyperthyroidism compared with normal subjects. In hypothyroidism both the TmP values and the mean renal phosphate threshold were decreased as compared with the euthyroid controls. Similar results on the renal handling of phosphate in thyroid disease have been reported previously. Thus, Bijvoet, Jansen, Preñen & Majoor (1964) observed an increased renal phosphate threshold in hyperthyroidism. Parsons & Anderson (1964) found that thyrotoxic subjects had higher values of TmP and the mean renal phos phate threshold which returned to normal when thyrotoxicosis was treated. Using values of % tubular reabsorption of phosphate Bortz et al. (1961) found higher values in hyperthyroidism compared with euthyroid subjects. Harden et al. (1964) found a significantly decreased phosphate excretion index (PEI) (Nordin & Fraser, 1956) in 36 hyperthyroid patients. Their findings were confirmed by Adams et al. (1967). However, normal values of PEI were reported in hyperthyroidism in the earlier studies of Nordin & Fraser (1960). Our findings suggest that the renal excretion of inorganic phosphate is decreased in hyperthyroidism. This change may be attributed to increased tubular reabsorption of phosphate resulting in an increase of serum phosphate levels in hyperthyroidism. The changes in the renal handling of phosphate could be related to the pathogenesis of the thyroid osteopathy, especially in hyperthyroidism. So far, four main mechanisms could be postulated for the explanation of the renal handling of phos phate in hyperthyroidism. (1) A direct renal effect of thyroxine and tri-iodothyronine on the proximal tubule resulting in an increase of the rate of phosphate reabsorption ;
5 (2) relative inactivity of the parathyroids; (3) thyrocalcitonin deficiency and (4) possibly, an increase in growth hormone secretion. These mechanisms are not fully substantiated by experimental evidence. However, mechanisms 2 and 3 seem at present the most likely explanation of the abnormal renal handling of phosphate in hyperthyroidism. REFERENCES Adams, P. H., Jowsey, J., Kelly, P. J., Riggs, B. L., Kinney, V. R. & Jones, J. D. (1967). Effects of hyperthyroidism on bone and mineral metabolism in man. Q. Jl Med. 36, Anderson, J. (1955). A method for estimating Tm for phosphate in man. J. Physiol., Lond. 130, Aub, J. C, Bauer, W., Heath, C. & Ropes, M. (1929). Studies on calcium and phosphorus metabolism. III. The effects of the thyroid hormone and thyroid disease. J. clin. Invest. 7, Bijvoet, O. L. M., Jansen, A. P., Preñen, H. & Majoor, C. L. H. (1964). The renal phosphate threshold: its evaluation and application in different clinical conditions. In Water and electrolyte metabolism II, p West-European Symposia on Clinical Chemistry, vol. in. Eds. J. de Graeff and B. Leijnse. Amsterdam: Elsevier. Bortz, W., Eisenberg, E., Bowers, C. Y. & Pont, M. (1961). Differentiation between thyroid and para thyroid causes of hypercalcaemia. Ann. intern. Med. 54, Buchanan, W. W., Koutras, D.., Alexander, W. D. & Crooks, J. (1962). Serum proteins in thyroid disease. Br. med. J. i, Cook, P. B., Nassim, J. R. & Collins, J. (1959). The effects of thyrotoxicosis upon the metabolism of calcium, phosphorus and nitrogen. Q. Jl Med. 28, Dean, R. F. A. & McCance, R. A. (1948). Phosphate clearances in infants and adults. J. Physiol., Lond. 107, Eggleton, M. G. & Shuster, S. (1954). Glucose and phosphate excretion in the cat. J. Physiol., Lond. 124, Eiler, J. J., Althausen, T. L. & Stockholm, M. (1944). The effect of thyroxin on the maximum rate of transfer of glucose and diodrast by the renal tubules. Am. J. Physiol. 140, Fiske, C. H. & Subbarow, Y. (1925). The colorimetrie determination of phosphorus. J. biol. Chem. 66, Harden, R. McG., Harrison, M. T., Alexander, W. D. & Nordin, B. E. C. (1964). Phosphate excretion and parathyroid function in thyrotoxicosis. J. Endocr. 28, Hare, K., Phillips, D. M., Bradshaw, J., Chambers, G. & Hare, R. (1944). Diuretic action of thyroid in diabetes insipidus. Am. J. Physiol. 141, Koenig, M. P., Scholz, D. A.& Salassa, R. M. (1957). Hypercalcaemia in hyperthyroidism. Minn. Med. 40, Man, E. B., Gildea, E. F. & Peters, J. P. (1940). Serum lipoids and proteins in hyperthyroidism. J. clin. Invest. 19, Nordin, B. E. C. & Fraser, R. (1956). Ciba Foundation Symposium on bone structure and metabolism. Eds. G. E. W. Wolstenholme and G. M. O'Connor. London: Churchill. Nordin, B. E. C. & Fraser, R. (1960). Assessment of urinary phosphate excretion. Lancet i, Parsons, V. & Anderson, J. (1964). The maximum renal tubular reabsorptive rate for inorganic phosphate in thyrotoxicosis. Clin. Sci. 27, Pribek, R. A. & Meade, R. C. (1957). Thyrotoxicosis simulating hyperparathyroidism. Archs intern. Med. 100, Robertson, J. D. (1942). Calcium and phosphorus excretion in thyrotoxicosis and myxoedema. Lancet i, Rose, E. & Boles, R. S., Jun. (1953). Hypercalcaemia in thyrotoxicosis. Med. Clins..Am. 37, Sallin, O. (1958). Hypercalcaemic nephropathy in thyrotoxicosis. ^4cto endocr., Copenh. 29, Stanley, M. M. & Fazekas, J. (1949). Thyrotoxicosis simulating hyperparathyroidism. Am. J. Med. 7, Walser, M. (1960). Protein binding of inorganic phosphate in plasma of normal subjects and patients with renal disease. J. clin. Invest. 39,
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