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Minimum Urine Flow Rate During Water Deprivation: Importance of the Nonurea Versus Total Osmolality in the Inner Medulla

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Minimum Urine Flow Rate During Water Deprivation: Importance of the Nonurea Versus Total Osmolality in the Inner Medulla Minimum Urine Flow Rate During Water Deprivation: Importance of the Nonurea versus Total Osmolality in the Inner Medulla STEVEN DEMETRI SOROKA,* SIRITHON CHAYARAKS,* SURINDER CHEEMADHADLI,* JEFFREY ADAM MYERS,* STANLEY RUBIN,t HARALD SONNENBERG,t and MITCHELL LEWIS HALPERIN* *Rena/ Division, St. Michael ‘s Hospital, Toronto, Ontario, canada; tDepartment of Internal Medicine, School of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan; and Department of Physiology, University of Toronto, Toronto, Ontario, Canada. Abstract. Antidiuretic hormone leads to an increase in the mosmol/kg H,O). Nevertheless, they had identical urine flow permeability for water and urea in the inner medullary collect- rates (0.5 ± 0.01 and 0.5 ± 0.02 mI/mm, respectively), and ing duct. Hence, urea may not be an “effective” osmole in the their nonurea osmolality also was similar (587 ± 25 and 475 ± inner medulla during maximal renal water conservation. Ac- 14 mosmollkg H,O, respectively) to the water-deprived normal cordingly, the purpose of this study was to evaluate whether subjects. The composition of their urine differed in that the differences in the rate of urea excretion would influence max- principal nonurea osmoles became NH4 and j3-hydroxybu- imum renal water conservation in humans. tyrate rather than Na and Cl. During water deprivation in In water-deprived rats, the concentration of urea and total normal subjects, the ingestion of urea caused a twofold rise in osmolality were somewhat higher in the urine exiting the inner urine flow rate, a fall in the nonurea osmolality, and a rise in medullary collecting duct than in interstitial fluid obtained the rate of excretion of nonurea osmoles. from the entire papillary tip. Nevertheless, the “nonurea” (total The nonurea osmolality of the urine, and presumably the osmolality minus urea in millimolar terms) osmolality was medullary interstitial fluid as well, was inversely related to the virtually identical in both locations. Chronically fasted human urea excretion rate. In chronic fasting, the nature, but not the subjects that were water-deprived for 1 6 h had a lower rate of quantity, of nonurea osmoles changed. The similar minimum urea excretion (71 ± 7 versus 225 ± 14 p.mollmin) and a urine volume was predictable from an analysis based on nonurea somewhat lower urine osmolality (745 ± 53 versus 918 ± 20 osmole considerations. (J Am Soc Nephrol 8: 880-886, 1997) When water must be conserved, antidiuretic hormone (ADH) be inserted in the IMCD (9). Therefore, it is reasonable to acts on the distal part of the kidney (late distal convoluted suggest that urea in the inner medulla may not have an appre- tubule, cortical collecting duct, and medullary collecting ducts) ciable direct influence on the rate of excretion of water during to increase the permeability for water (reviewed in reference water deprivation if its concentration is similar in the lumen of I ). Because water is likely to achieve diffusion equilibrium in the IMCD and the interstitial fluid of the inner medulla (6-8). this setting, the sum of the solute concentrations in the inner Accordingly, the urine flow rate would be determined by the medullary interstitium and the urine should be equal. The urine number of nonurea osmoles (osmolality - urea concentration flow rate would then be a function of the number of osmoles to in millimolar terms) excreted when ADH acts (10-14) (Equa- be excreted (2-5) (Equation I ). Nevertheless, not all solutes tion 1). Therefore, the question to be addressed is, What is the have the same impact on water distribution. Only particles that influence of variations in the rate of excretion of urea within its achieve a concentration difference across a semipermeable physiologic range on the urine nonurea osmolality and flow membrane obligate water movement here. Urea concentrations rate? are usually similar in the lumen of, and in interstitial fluid surrounding, the inner medullary collecting duct (IMCD) when Volume (L) ADH acts (6-8) because ADH also causes a urea transporter to = Amount of solute (mmol)/Solute concentration (mM) (I) Received January 31, 1996. Accepted December 30. 1996. Correspondence to Dr. Mitchell L. Halperin, Division of Nephrology, St. Michael’s Hospital. 38 Shuter Street, Toronto. Ontario. Canada M5B 1A6. Results to be reported indicate that in water-deprived sub- l()46-6673/0806-0880$03.00/0 jects who were fasted for 2 to 3 wk, the rate of excretion of Journal of the American Society of Nephrology urea was much lower than in water-deprived normal subjects. Copyright 0 1997 by the American Society of Nephrology Nevertheless, their urine flow rates were similar because there Control of Urine Flow Rate 881 was no significant difference in the nonurea osmolality of the small volume of water. Urine samples were collected by spontaneous urine; despite this, the composition of the urine was very voiding every hour, and the values reported represent the collections different in these two groups. When the rate of excretion of in which two adjacent samples had similar high rates of urea excretion (samples in the 2 to 4 h after urea ingestion). urea was increased in water-deprived normal subjects, the urine flow rate rose. In this case, both a fall in the urine nonurea osmolality and a rise in the rate of excretion of Analytic Techniques nonurea osmoles could explain their higher urine output. Urine samples were analyzed for Na, K. Cl, urea, creatinine, NH4 , /3-hydroxybutyrate (f3-HB), and osmolality as described previously Materials and Methods (17). Studies in Rats Sprague-Dawley rats (250 to 325 g body wt) were kept without Calculations food and water overnight; they were anesthetized and prepared for Nonurea Osmolality. The nonurea osmolality of the urine is the IMCD microcatheterization as described previously (15). Interstitial measured urine osmolality minus its urea concentration in millimolar fluid was obtained from the exposed papilla by the method of Lee and terms. The rate of excretion of osmoles or nonurea osmoles was equal Williams (16). The inner (white) medulla was excised, blotted, to the product of the urine flow rate and the total osmolality or weighed, and centrifuged twice under oil at 300 and 1500 X g with nonurea osmolality in the urine. fluid obtained during the second centrifugation used for analysis of Statistical Analysis. Values were presented as the mean ± SEM. urea and osmolality. Such fluid is virtually free ofcontamination with Mean values were compared using unpaired values and a I test. IMCD fluid, the contribution of intracellular fluid is minimal, and the composition changes appropriately with dehydration ( 16). Analysis of Results papillary interstitial fluid and urine from the same kidney is provided Studies Rats in Table I. in Fluid obtained from the terminal IMCD had an osmolality and a urea concentration that were somewhat higher than that Studies in Humans in the corresponding interstitial fluid ( 10 16 ± 137 versus The objectives of this study were to examine the effect of variations in the rate of excretion of urea within the physiologic range in 881 ± 150 mosmollkg H,O, and 439 ± 86 versus 296 ± 34 water-deprived subjects on the urine flow rate and to determine mM, respectively, Table 1 ). Nevertheless, there was no differ- whether changes in the urine flow rate correlated with changes in ence in the nonurea osmolality in these fluids (585 ± 50 versus nonurea osmolality. Volunteers (a 37, ages 17 to 58, 26 male and 575 ± 49 mosmollkg H,O, Table I). 1 1 female) followed their usual diet and took no medications. In- formed consent and ethics approval were obtained for all protocols. Studies in Humans Comparison of Overnight Water Deprivation in Controls and Effect of a Low Rate of Urea Excretion on the Compo- Fasted Subjects. All subjects provided a second-voided urine after sition of the Urine During Water Restriction. The compo- I 2 to I 6 h of water deprivation (collection time close to I 0:00 h am.). To study maximal renal water conservation when there was a low rate sition of the urine in subjects who followed their usual diet and of urea excretion, identical studies were also carried out in four were water deprived for 12 to 16 h is shown in Table 2; these markedly obese subjects who had fasted for 2 to 3 wk in a weight values were compared to urine values in obese, fasted subjects reduction program. who had a much lower rate of excretion of urea (7 1 ± 7 versus Effect of a Urea Load on the Urine Composition After Over- 225 ± 14 p.mol/min, P < 0.01, Table 2). In the control night Water Deprivation. The rationale for this protocol was to subjects, approximately half of the urine osmoles were urea. study the effect of raising the rate of excretion of urea within the The urine flow rate after 16 h of water deprivation was similar physiologic range on the urine flow rate and its composition during in both groups (0.5 ± 0.02 and 0.5 ± 0.01 ml/min). The urine antidiuresis. Six subjects followed their regular diet and did not eat or nonurea osmolality was 475 ± 14 mosmollkg H,O in the drink for 1 2 h. A second-voided morning urine sample was obtained, control subjects, and it was slightly higher in the fasted sub- after which each subject ingested 6 mmol urea/kg body wt with a jects (587 ± 25 mosmol/kg H,O, Table 2). When the rate of nonurea osmole excretion was plotted against the rate of urea Table 1. Urea and osmolality in the renal papilla” excretion in the 37 control subjects with and without urea supplements, there was a significant inverse correlation be- Kidney tween these two parameters (Figure 1); the urine flow rate was Papilla Urine now a function of the rate of excretion on nonurea osmoles (Figure 1).
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