(0*24+0*01, P < 0.05). development. chloride osmotic diuresis does not exist during maturation in rats.
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1 J. Phyeiol. (1976), 258, pp With 4 text-figuree Printed in Great Britain MATURATION OF THE RENAL RESPONSE TO HYPERTONIC SODIUM CHLORIDE LOADING IN RATS: MICROPUNCTURE AND CLEARANCE STUDIES BY JEFFREY T. BAKER* AD SIDNEY SOLOMON From the Department of Physiology, University of New Mexico School of Medicine, Albuquerque, New Mexico 87131, U.S.A. (Received 16 October 1975) SUMMARY 1. The ability of maturing rats to excrete a sodium load was studied by micropuncture and clearance procedures. 2. During control conditions, no change of glomerular filtration rate or sodium excretion was observed for the time period of the entire procedure (P > 2). During the infusion of hypertonic (4%) sodium chloride, fractional sodium excretion was in rats 21-3 days old and * (P < -1) in adults. However, the depression of proximal tubular water re-absorption was equal in both groups (P > 2). 3. Proximal glomerulotubular balance for water re-absorption was similar in all groups (P > 2). Since end proximal tubular water excretion and depression of fractional water excretion were the same in all animals, differences of urinary sodium excretion during development are probably due to differences of function of segments beyond the proximal tubule during development. 4. Fractional potassium excretion was reduced in young rats (.17 ±.4) during hypertonic sodium chloride infusion, compared to adults (*24+*1, P <.5). 5. Passage time of fast green through cortical segments in seconds is prolonged in young rats during control conditions. Similar decreases of passage time were seen in all groups during hypertonic sodium chloride infusion. No segmental differences of passage time were seen during development. 6. No difference in the relationship between fractional sodium and water excretion was seen during development of the renal response to hypertonic sodium chloride infusion. Thus, altered sensitivity to sodium chloride osmotic diuresis does not exist during maturation in rats. * Present address: Department of Physiology, Eastern Virginia Medical School, P.O. Box 198, Norfolk, Virginia 2351, U.S.A.
2 84 JEFFREY T. BAKER AND SIDNEY SOLOMON INTRODUCTION The less efficient renal response of the neonate to various forms of sodium challenge (Dean & McCance, 1949; McCance & Widdowson, 1957; McCance & Wilkinson, 1947) and extracellular volume expansion (Bengele & Solomon, 1974; Kleinman & Reuter, 1974) is now well established. Early work failed to adequately quantitate by the clearance technique tubular immaturity following oral sodium loads or hypertonic sodium chloride infusion in rats (McCance & Wilkinson, 1947) or piglets (McCance & Widdowson, 1957). Recently, Kleinman (1975) has shown that tubular sodium excretion following extracellular volume expansion is less in puppies than adults. These indirect studies suggest that the distal nephron may be responsible for increased volume re-absorption during extracellular fluid volume expansion in the puppy. Unfortunately, direct analysis using the micropuncture technique has not yet been applied to this question. Of present interest is the renal response to hypertonic sodium chloride. Kamm & Levinsky (1965) suggested that an intrarenal mechanism might control the renal response to hypertonic sodium chloride in dogs. In micropuncture studies of rats, Giebisch, Klose & Windhager (1964) clearly showed that only distal tubular fractional sodium re-absorption was reduced at low rates of infusion. Higher infusion rates appeared to reduce both proximal and distal fractional sodium re-absorption, presumably due to the effects of volume expansion proximally and saturation of the sodium transport mechanism in the distal tubule (Kamm & Levinsky, 1965). It follows that changes of sodium transfer may be simultaneously studied in proximal and distal tubules during hypertonic sodium chloride loading in the rat. The purpose of the present investigation has been to follow the pattern of development of the renal response to large loads of hypertonic sodium chloride in the rat. This method was chosen because reductions of sodium transport in both proximal and distal tubular segments during hypertonic sodium chloride loading in young rats would allow us to determine whether the proximal or distal nephron, or both, is responsible for volume retention in developing animals in which only the proximal tubule is accessible to micropuncture. In addition, variations of fractional sodium excretion might allow for examination of the relationship between urinary sodium and water excretion, as previously described (Baker & Kleinman, 1974), as an indirect reflexion of sensitivity to a sodium osmotic diuresis during maturation of the neonate. The results obtained here were presented in abstract form at the 51st annual meeting of the Federation of American Societies for Experimental Biology in Atlantic City, New Jersey, U.S.A.
3 Na EXCRETION IN DEVELOPING RATS 85 METHODS Fifty-one male Sprague-Dawley rats (Simonsen strain, Gilroy, California) ranging from 21 to more than 6 days old were studied. All animals were born in our animal quarters and weaned at 2 days of age. All animals were fasted for hr before the experiment, although full access to water was given. Each rat was anaesthetized with Inactin (Promonta), 6-1 mg/kg body weight administered i.p. Polyethylene catheters of appropriate diameter were placed in the left carotid artery for pressure recordings, blood sampling and dye injections. In addition, the left jugular vein was cannulated for [3H]inulin infusion (Amersham-Searle, Arlington Heights, Illinois). The clearance of inulin was equated to the rate of kidney filtration. Finally, the left femoral vein was cannulated for hypertonic (4 %) sodium chloride infusions. [3H]Inulin, 1 or 2 1ac/ml., dissolved in mammalian Ringer-Locke was administered i.v. at a rate of 4 ml./hr per 1 grams body weight as maintenance fluid; rats less than 15 g received the more concentrated inulin solution. Then 3-4 miin after the completion of surgery, the left kidney was exposed by a subcostal incision and gently cleaned of perirenal fat. The ureter was then exposed and cannulated and the kidney placed in a lucite cup. The kidney was bathed in paraffin oil warmed to 37 C. Each animal was allowed 3 min further equilibration before beginning collections. Unless both peritubular capillaries and tubules were uniformly perfused under microscopic examination, the experiment was terminated. Superficial proximal tubules (least mature) were punctured with pipettes of tip diameter jam. The inside of each pipette was coated with Desicote (Beckman Instruments Inc., Fullerton, California). All tubules were blocked with Sudan black stained paraffin oil. The oil column was of sufficient length to prevent retrograde contamination. Tubular re-collections were made slightly proximal to the original site to avoid sample loss (Andreucci, Herrera-Acosta, Rector & Seldin, 1971). Tubular collections for both fractional water excretion (P/TFk) and single nephron glomerular filtration rate analysis varied from 1 to 1 min. All samples containing [3H]inulin were counted in 5 ml. PCS solubilizer (Amersham-Searle) in either a Packard Model 3385 or 331 liquid scintillation counter. Samples were corrected for quenching when necessary. Since very small volumes of tubular samples were usually obtained, especially from young rats, fractional water excretion and single nephron glomerular filtration rates were determined in samples taken from different cortical tubules. To reduce error the entire volume collected for single nephron glomerular filtration rate determination was counted. Samples collected for the determination of fractional water excretion from different tubules were pipetted into calibrated pipettes and the radioactivity determined. FD and C+3 Green was purified according to the method of Parekh, Popa, Galaske, Galaske & Steinhausen (1973) and buffered with Trishydrochloride.Fortyasl. of 1% solution of FD and C+3 Green was injected as a bolus into the carotid artery. The passage time recorded was the time required for dye to pass from the efferent arteriole (diffuse flush) to the end of the proximal convoluted segment (proximal transit time). Proximal transit time plus the passage time through the loop of Henle was recorded as the loop transit time. Passage time from the diffuse flush to the beginning of the ureteral catheter was taken as total nephron passage time. Passage times of proximal tubule and loop of Henle segments were pooled because passage time in all segments could not be measured in the same nephron. Arterial blood samples were usually taken after each tubular collection, immediately centrifuged and stored until the end of the experiment. Urine volumes were determined as the weight of urine collected in a given time. Plasma and urine radioactivity was counted as previously described (Bengele & Solomon, 1974) in
4 86 JEFFREY T. BAKER AND SIDNEY SOLOMON 1 Aal. aliquots. Plasma and urine sodium and potassium concentrations were determined oil an Instrumentation Labs Model 143 internal standard flame photometer the day of the experiment. The Student's t test was used to compare means between experimental groups as well as differences between control and experimental periods. Multiple regression analysis was performed with the computer facilities of the University of New Mexico. Experimental groups Control experiments. Eleven experiments (five adults and six young rats days of age) were conducted to determine the constancy of kidney and tubular function when rats were not given a large sodium chloride load for two sequential collections. Hypertonic sodium chloride loading. In twenty-two animals 21-6 days of age, 4 % sodium chloride was given I.v. during the second collection period. It has previously been shown in the rat (Giebisch et al. 1964) that both proximal and distal sodium transport is reduced at infusion rates calculated to achieve a plasma sodium concentration of 176 m-equiv/l. To insure these conditions in all rats, we gave infusions greater than those previously reported (Giebisch et al. 1964). All animals were primed with 1-25 ml./1 g body weight over 4 min and received 4 ml./1 g body weight of 4 % sodium chloride per hour for the remainder of the experiment. Animals were infused for half an hr with 4 % sodium chloride before the final re-collections were taken to allow for re-equilibration of sodium chloride and [3H]inulin with body fluid compartments. End proximal collections. End proximal tubular collections were performed in five additional rats 25-3 days old and in four adults. In each animal 3-5 segments were punctured. The segment was identified by injections of fast green as previously described in Methods. These experiments were done in separate groups of animals under control conditions only, since we thought error from leakage of filtrate from small end segments in young rats during re-collection could be significant. Passage time experiments. Passage time through superficial nephron segments was measured in antidiuretic rats and again during 4% sodium chloride loading. Four animals from each of the four age groups (sixteen total) were studied. Passage time through the segments was previously described under Methods. In the text distal tubule refers to the nephron segment between ascending thick limb of Henle and collecting ducts accessible to micropuncture, and distal nephron to all segments beyond that portion of the proximal tubule accessible to micropuncture. RESULTS Table 1 illustrates the results of experiments in which the constancy of water and electrolyte excretion was examined in young and adult rats. Animals were continuously infused with mammalian Ringer-Locke solution, 4 ml./1 g body weight per hour, during the entire procedure. Clearly, no significant change from control occurred in those parameters examined in either young or adult rats during the final portion of the experimental procedure. We noted a tendency for passage times to decrease if prolonged periods, usually greater than 45 min, transpired between timings (J. T. Baker and S. Solomon, unpublished), even though only maintenance infusions were given. Therefore, re-timings were taken within half an hr of the original measurement.
5 Na EXCRETION IN DEVELOPING RATS 87 Large changes of sodium and potassium excretion occurred in rats of all ages when 4%/ sodium chloride was administered (Table 2 C, D, and Fig. 1). There was good correlation between increase of age and increases of fractional sodium excretion (Fig. 1, r = -71, P < -1) during 4% TABLE 1. Re-collection micropuncture and clearance data in young and adult rats. Hypertonic sodium chloride was not given during the final collections. Data are means + 1 S.E. of mean Age (days) Initial single nephron glomerular filtration rate (nl./min) Final single nephron glomerular filtration rate (nl./min) P IP control IF re-collection TF1~ TF1,n Initial glomerular filtration rate (ml./min per gram kidney weight) Final glomerular filtration rate (ml./min per gram kidney weight) Initial fractional excretion of Na+/ Final fractional excretion of Na+ Initial fractional excretion of K+/ Final fractional excretion of K+ P Here n.s. indicates not significant and TF the proximal tubule. TFta > ± 4-8 n.s. -95 ± -4 n.s ± -15 n.s n.s. -93 ± -9 n.s n.s. -95 ± -14 n.s n.s n.s n.s. is the fractional water excretion from sodium chloride infusion. Fractional excretion of sodium in urine increased with age during 4% sodium chloride infusion, although all animals incurred a similar expansion as indicated by plasma sodium (mean range of all animals m-equiv./l. sodium during 4% sodium chloride infusion) and dilution of the hematocrit (Table 2, B). In these same animals, fractional volume excretion by the proximal tubule significantly increased in all age groups during 4 % sodium chloride infusion (Fig. 1 and Table 2, E). However, there was no detectable difference among the groups in fractional volume excretion from the proximal tubule in these rats during 4 % sodium chloride loading (Fig. 1 and Table 2, E). We realized that although the fractional increase of volume excretion in the proximal tubule was the same in rats of all ages, a low end proximal fractional volume re-absorption, and a consequently elevated distal nephron re-absorptive rate, might result in a reduced ability of that fluid excreted from the proximal tubule to saturate transport mechanisms in
6 88 JEFFREY T. BAKER AND SIDNEY SOLOMON more distal sites. This might result in net volume retention in young animals. As seen in Table 2 G, no difference in end proximal fractional water re-absorption between five rats 2-3 days old and four adult rats was observed under control conditions. Furthermore, no difference of final urinary water re-absorption was seen between these same two groups of animals during control conditions (Table 2). Therefore, the data suggest A S C C.15 i zlw. U -1 x S C *O. L. *5 C * bo L. C U L x * B 'Us Lw. L.O Age (days) Fig. 1. A, relationship between age and fractional excretion of sodium in P /P urine, control T- experimental; and B, between age and fractional excretion of water by the proximal tubule during infusion of 4 % sodium chloride solution. In A, y = 12x+ 5 (r = -71, P < 1); and in B, y = 1x+O-67 (r = 11, not significant). that the proximal and distal nephron segments re-absorb similar fractions of the filtered volume even in the least mature superficial cortical nephrons of the rat. In addition, since both fractional depression of volume re-absorption (Table 2, E) and end proximal volume re-absorption (Table 2, G) were similar in all age groups during antidiuretic and diuretic
7 S Na EXCRETION IN DE VELOPING RA TS OQ, C.)._ c CC to A 1o ~~~ mp ' N _o o CO" '4 q r 1 = N O c +1 +1, t:- +1 COC cq 1 m -. +l +l.) 6 A 1.4 Sz 89 ce fe o e + c. o*; e :Ye,;o C. 4 in rn r O i- c~ GP OO co O CO+ +I c cl -q o N 8 : z6g 6 :> CO Ns cq C4, I +I +1-1 C4.) 6 A 1._ Ci) ; x 14. * 1 4.4> C o e - U.)e 1Q. o S o e 1.4 _th O Cs + d e Ca oa;c. Ca m wo - ce 1.4 -S to Ca > C " w, = _- ;_4 ;.4 E o ;- C -4') w.. -Z, : o-~ o v C) >. C)
8 9 JEFFREY T. BAKER AND SIDNEY SOLOMON conditions, distal nephron segments probably receive similar fractions of the filtered load in all groups examined. It may be worth noting that in rats in which end proximal segments were identified by repeated injections of purified fast green, no diuresis was noted as seen by fractional urinary water excretion (Table 2, H). Following 4% sodium chloride infusion, increases of whole kidney glomerular filtration rate were consistent but of borderline significance (.5 < P <.1) for all animals studied (Fig. 2). The increase of superficial cortical single nephron glomerular filtration rate was considerably greater, however, in the same animals of every age group compared to the.c 6 -T 2-4 so 5-2 Fig. 2. Comarson o sigl nehrn gomrulr iltaton ats (pec E E ~~~~~~~~~~~~~~~~~ T-1-2~ vc.9 2 -T-.8 E a 1 W'W ~~~~~~~~~~~~~~~~ --4 (U Age (days) Fig. 2. Comparisons of single nephron glomerular filtration rates (open columns) and whole kidney glomerular filtration rates (hatched columns) before, C, and after 4% sodium chloride infusion, E. Animals were arbitrarilydividedinto 1-dayage groups. All data arethe mean +1.E. of mean. elevation of whole kidney filtration rate (P < 1). Consistent with previous work in this laboratory for rats (Solomon & Capek, 1972) and with others (Horster & Valtin, 1971; Spitzer & Brandeis, 1974), nephron filtration rate increased continuously during maturation under control conditions. Since single nephron glomerular filtration rate increased considerably more than whole kidney filtration rate, a relative redistribution of glomerular filtrate to the outer cortex probably occurred during development in the control animals as described for rats (S. Solomon and H. H. Bengele, unpublished) and guinea-pigs (Spitzer & Brandeis, 1974) and in all groups during hypertonic sodium chloride loading (Table 2). Similar changes were observed during acute infusions of 4% sodium chloride (Table 2, F). As can be seen here, a clear trend toward a relatively large increase in superficial vs. whole kidney glomerular filtration rate occurred. Thus, the least mature nephrons received a large increase in -
9 Na EXCRETION IN DEVELOPING RATS 91 glomerular flow during the experimental procedure compared to more mature inner cortical nephrons. Fig. 3 gives the results of the relationship between the change of fractional sodium and fractional potassium excretion during 4% sodium chloride infusion. Animals are arbitrarily divided into two groups above and below 4 days of age. The curve is calculated from polynomial regression and was selected since it gave better correlation between the variables than did linear regression. Clearly, younger animals showed both a lower fractional potassium excretion and sodium excretion (Table 2, C, D, and Fig. 3). We have felt it valid to pool data for fractional sodium and potassium excretion to better gain understanding of this relationship.2 vi 16 - C.2.12 V,~~~~~ X 4-2 * Changes in fractional excretion of K+ in urine Fig. 3. Relationship between changes of fractional sodium and fractional potassium excretion in young rats, less than 4 days old () and adult rats, older than 4 days (@), during the infusion of 4% sodium chloride. This curve is described by the equation y = x--*18 x 2 (r = -78, P <.1). during maturation. Previous results from this laboratory (Solomon, 1974a) suggest that young rats establish similar sodium and potassium gradients across the proximal tubule during mannitol loading. Since end proximal fractional volume re-absorption is unchanged during development, fractional sodium and potassium delivery to the distal segments is probably similar. Therefore, changes of potassium excretion might be a result of reduced potassium secretion from the distal segments during 4% sodium chloride infusions. Comparative dependence of fractional water excretion (V/GFR) on fractional sodium excretion was examined in an attempt to determine whether an altered response to sodium chloride osmotic diuresis exists in
10 92 JEFFREY T. BAKER AND SIDNEY SOLOMON young rats. As shown in Fig. 4, no such difference was seen. Points from animals were arbitrarily divided into two groups (21-4 and greater than 4-day-old rats) and plotted on the same regression line which relates fractional water to sodium excretion. Although less sodium was excreted in young animals during 4% sodium chloride loading, neither elevated nor reduced fractional water excretion occurred at any level of sodium excretion _- C *Z -1 1 ro..- -8,, -6 v x 1 -, -4 C U. 2 O Fractional excretion of Nag in urine Fig. 4. Correlation between fractional sodium and fractional water excretion (VIGFR) in urine of young rats, less than 4 days old (a), and adult rats, older than 4 days (O), during 4% sodium chloride infusion. This line is described by the equation y = -667x--8 (r = 95; P < -1). TABLEo 3. Passage times through cortical nephron segments in developing rats during control and hypertonic sodium chloride loading periods. All values are means + 1 S.E. of mean Age (days) Proximal tubulk Loop of Henle Final urine Proximal tubuk Loop of Henle Final urine Passage time during control (sec) ± ± ± Passage time during sodium chloride loading (see) * * * 5 5 ± 68* * * * 65-3 ± 15.* * * Significant at the 5 level. > ± ± ± * 49* * 5 +.6*
11 Na EXCRETION IN DEVELOPING RATS 93 Since previous work (Gertz, Mangos, Braun & Pagel, 1965) suggests that fractional re-absorption increases as passage time in the nephron is prolonged, we have also attempted to determine whether a relative change in passage time of any nephron segment(s) might account for differences of volume retention in tubular segments following a change from antidiuretic to diuretic conditions. In order to avoid potential artifacts due to diuretic effects of fast green, micropuncture was not performed in these experiments. Table 3 shows prolonged passage time in all nephron segments during antidiuresis in rats 2-4 days old. There were similar fractional increases of passage time in all rats following a 4 % sodium chloride load although proximal passage times in rats 2-4 days old remained slightly prolonged (Table 3). Passage times in see through proximal tubule plus loop of Henle were very similar in all rats during 4% sodium chloride infusion although times were prolonged during control in rats less than 4 days of age. Some functional nephron heterogeneity (Baker & Kleinman, 1973; Edelmann, Barnett & Stark, 1967; Fetterman, Shuplock, Phillipp & Gregg, 1965) no doubt exists in neonates still undergoing nephrogenesis. We were, therefore, unable to determine directly the passage time through the cortical collecting ducts during hypertonic sodium chloride loading, since the final urine is an admixture of flows from inner and outer cortical nephrons. DISCUSSION It was evident that since nephron heterogeneity is known to exist in certain new-born animals (Baker & Kleinman, 1973; Edelmann et al. 1967; Fetterman et al. 1965), certain methods of tubular collections might not give true representations of actual changes following an experimental manipulation. Increased variability of the measured fractional re-absorption could give a false estimate of the fractional depression of fluid reabsorption in a limited series of samples if punctures of end proximal tubules with low fractional water excretion inulin ratios were followed by punctures of different end proximal tubules with higher fractional water excretion inulin ratios. We therefore thought that the same tubules should be studied by re-collection. Since the end segment is often revealed as a cortical point separating two subcortical sections (nearby upstream recollection not feasible) near a vascular 'welling-point' in young rats, the possibility of leakage during re-collection of this small section was considered great. We therefore chose random re-collections from elongated sections of proximal segments to avoid this potential artifact. Knowing that fractional depression was similar in all groups during the experimental manipulation, a second group of experiments was therefore initiated in which the end segment was identified and punctured during control only.
12 94 JEFFREY T. BAKER AND SIDNEY SOLOMON Since no change of end proximal fractional water excretion inulin ratios during control occurred during development and since fractional depression of volume re-absorption was the same during 4% sodium chloride infusion in all groups, the fraction of filtrate entering the distal nephron must have been the same in all groups during 4% sodium chloride infusion. The results of the present investigation lend further support to the results of Giebisch et al. (1964). These authors found a depression of fractional volume re-absorption in the rat proximal tubule following large infusions of 4% sodium chloride (fractional excretion of sodium > 12 %). Fractional excretion of sodium in adult rats of the present study are greater than 12 %, since our infusion rates were calculated to provide this. We have extended the findings of these authors since we have noted both an increase and a relative preponderance of outer cortical glomerular filtration in adult and developing rats during 4% sodium chloride infusions. We have primarily concerned ourselves with direct localization of the site(s) of increased sodium retention in young animals. Kleinman (1975) noted equivalent fractional sodium excretion in new-born and adult dogs when extracellular fluid volume expansion was given during distal blockade of sodium re-absorption, suggesting that the proximal tubule behaved similarly in both groups. Micropuncture results during hypertonic sodium chloride loading in rats of the present investigation give direct support to this hypothesis. No difference in the fractional depression of proximal volume re-absorption during 4% sodium chloride infusion was noted in developing rats. Moreover, when compared to adults, the glomerulotubular balance for volume re-absorption is maintained during development in rats (Solomon, 1974b) as it is for maturing guinea-pigs (Spitzer & Brandeis, 1974) and dogs (Horster & Valtin, 1971) as evidenced by equal end proximal tubular fra tional water excretion inulin ratios in rats 2-3 days old and in adults. We have assumed that if proximal tubular fractional water excretion inulin ratios are equal in the two most divergent groups, they are probably equal in those age groups between. These findings for the rat are consistent with previous work for the guinea-pig (Spitzer & Brandeis, 1974) and dog (Horster & Valtin, 1971). Since both fractional depression of volume re-absorption and end proximal fractional water excretion inulin ratios are equal in all age groups, sodium retention in young animals occurs beyond this site. Unfortunately, direct micropuncture of segments beyond the proximal tubule has not been found feasible by current methods. Nevertheless, it may be worthy of note that based on these observations, diuretics acting primarily in the distal segments ought to be more effective than proximal acting diuretics in the stimulation of sodium excretion in the new-born.
13 Na EXCRETION IN DEVELOPING RATS 95 Because of the difficulty in micropuncture of distal segments in young rats, we have used analysis of potassium excretion during 4% sodium chloride infusion to provide insight into the specific distal site of sodium retention in young animals. Work by Goldstein (197) suggests that by 15 days of age (even younger than animals studied in the present investigation), the ability of rats to acidify urine is mature. Therefore, differences of potassium excretion between young and adult rats during 4% sodium chloride infusion may be due to differences in distal tubular potassium secretion independent of H+ secretion. Malnic, Klose & Giebisch (1966) have shown that 4% sodium chloride infusion alters the distal tubular electrochemical potential gradient which stimulates passive potassium secretion. The increment of potassium excretion observed by Malnic et al. (1966) is very similar to that of the adults of this study. Although the reasons for reduced potassium excretion in young rats following 4% sodium chloride infusion remain unknown, certain explanations do exist. Some authors have emphasized the role of flow rate through the distal tubule as a determinant of potassium excretion (Kunau, Webb & Burman, 1974; Malnic et al. 1966). Animals with low flow would be expected to have a low output of potassium, a situation which might exist with the youngest rats. Another possibility which might co-exist is that of an absence at least in part of a distal secretary mechanism, as suggested previously (Braunlich & Puschmann, 1972; S. Solomon and H. H. Bengele, unpublished). Previous work from this laboratory suggested that at about 4 days of age, rats begin a response similar to the adult in the 'escape response' to DOC (deoxycorticosterone acetate) administration by an increase in potassium excretion. Data ofthe present investigation support this in part, since animals 4-5 days of age show a larger increase of potassium excretion than younger animals following 4% sodium chloride infusion. Passage time of dye through the proximal segment in young rats has been described in preliminary form elsewhere (Capek, Dlouha, Fernandez & Popp, 1968) for the Wistar rat. Our data extend this analysis to the remaining segments of the nephron for both control and hypertonic sodium chloride loading, although proximal times are not in complete agreement with Gapek et al. (1968). In rats 2-4 days of age, the passage time of filtrate through proximal and distal nephron segments was prolonged compared to older animals during antidiuresis. Following hypertonic sodium chloride loading, passage time in see decreased in all animals to an equivalent extent in all segments. This is partly to be expected since the rise in filtration and the fractional depression of proximal re-absorption were equivalent. Compared to adults, however, passage time per unit nephron length remained prolonged in younger rats in all segments during hypertonic sodium chloride loading. Comparisons of passage time analysis 4 PHY 258
14 96 JEFFREY T. BAKER AND SIDNEY SOLOMON in sec is of little meaning in animals with different nephron lengths, unless relative changes between control and experimental periods can be made. There was no tendency for contact time to remain prolonged in distal segments of young rats re-absorbing large fractions of the filtered volume. We therefore doubt that contact time per se plays a significant role in the volume retention of young animals. Single nephron glomerular filtration rate increased with age in the present experiments and averaged 43 nl./min in adults. In a recent review by Wright & Giebisch (1972) a large variability of single nephron glomerular filtration rate was reported from different laboratories. It was pointed out by the authors that sampling technique, strain differences, weight and age may be responsible for the differences reported. Our work gives clear support to the notion that age (and therefore size) is associated with higher values of single nephron glomerular filtration rate in the rat. Gertz et al. (1965) have shown that the intrinsic rate of proximal reabsorption can be predicted from knowledge of passage times and fractional volume re-absorptions. Relative tubular lengths and perfusion rates clearly affect these interpretations. Prolonged passage times are expected in young animals since the single nephron glomerular filtration rate is less; in the present experiments, we found it increased from 5-7 to 43- nl./min, i.e. a seven-and-a-half fold increase. In observations of Sprague-Dawley rats from this laboratory (Solomon, 1974b), a fourfold increase of proximal tubular length was observed in rats of comparable size to those examined here. Therefore, perfusion/mm proximal tubule is lower in young rats. Since fractional re-absorption by the end of this segment is the same during antidiuresis in all rats, intrinsic volume re-absorptive capacity of this segment must increase during development, a finding different from that of the guinea-pig (Spitzer & Brandeis, 1974). Since neither collections from distal segments nor micropuncture of these areas has yet been performed in maturing rats, we are unable to state whether intrinsic reabsorptive capacity is less in these areas. A reduced intrinsic re-absorptive capacity in distal segments, however, would be paradoxical in view of the increased re-absorption which appears to occur there. The relationship between fractional sodium and water excretion in rats during sodium osmotic diuresis is different from that seen in puppies and adult dogs during glucose diuresis (Baker & Kleinman, 1974). Unlike the puppy, the relationship between fractional sodium and water excretion remained unchanged during maturation of the renal response to hypertonic sodium diuresis. Therefore, maximum ADH effects were probably achieved. In support of this, Dlouha, Krecek, Kraus & Pliska (1965) have observed that plasma ADH levels reach adult values by 2 days of age. The similarity of the relationship between fractional sodium and water
15 Na EXCRETION IN DEVELOPING RATS 97 excretion in our two animal groups therefore is to be expected and furthermore suggests a similar sensitivity to osmotic stimulation of ADH release in the rats of the present study. This work was partially supported by grants from the National Science Foundation (BMS ) and the National Institutes of Health (HL 5633). REFERENCES ANwDRzucci, V. E., HERREBA-AcOsTA, J., RECTOR, F. C. & SELDIN, D. W. (1971). Measurement of single nephron glomerular filtration rate by micropuncture: analysis of error. Am. J. Phyeiol. 221, BAKER, J. T. & KIErnuLN, L. I. (1973). Glucose reabsorption in the newborn dog kidney. Proc. Soc. exp. Biol. Med. 142, BArn, J. T. & KCLEiNaN, L. 1. (1974). Relationship between glucose and sodium excretion in the new-born dog kidney. J. Phy8"i. 243, BENGELE, H. H. & SOLOMON, S. (1974). Development of renal response to blood volume expansion in the rat. Am. J. Physiol. 227, BRXuNucH, H. & PuscmuNt, R. (1972). Die Entwicklung der renalen Aussheidung von natrium und kaliuim in der postnatalen Periode bieder Ratte. Acta biol. med. Germ. 28, CAPEr, K., DLOuIHA, H., FERNANDEZ, J. & Popp, M. (1968). Regulation of proximal tubular reabsorption in the early postnatal period of infant rats. Int. physiol. cong. 7, 74 (abstract). DEAN, R. F. A. & MCOANcE, R. A. (1949). The renal responses of infants and adults to the administration of hypertonic solutions of sodium chloride and urea. J. Physiol. 19, DLOUHA, H., KRECEK, J., KRAus, M. & PLisKs, V. (1965). Sensitivity of rats to vasopressin in the weanling period. Physiologia. bohemoslov. 14, EDELMANN, C. M., BARNETT, H. L. & STARK, H. (1967). Renal bicarbonate reabsorption and hydrogen ion secretion in normal infants. J. din.'invest. 46, FETTERMAN, G. H., SHUPLOCK, N. A., PmLLIPP, F. J. & GIEXG, H. S. (1965). Growth and maturation of human glomeruli and proximal convolutions from term to adulthood: Studies by microdissection. Pediatrics, Springfiedk 35, GERTZ, K. H., MANGOS, J. A., BRAUN, G. & PAGEL, H. D. (1965). The glomerular tubular balance in the rat kidney. Pflugers Arch. ges. Physiol. 285, GIEBISCH, G., KLosE, R. M. & WINDHAGER, E. E. (1964). Micropuncture study of hypertonic sodium chloride loading in the rat. Am. J. Physiol. 26, GoLsTEIN, L. (197). Renal ammonia and acid excretion in infant rats. Am. J. Physiol. 218, HORsTER, M. & VALTiN, H. (1971). Postnatal development of renal function: micropuncture and clearance studies in the dog. J. din. Invest. 5, KeAIm, D. E. & LEVINSKY, N. G. (1965). Inhibition of renal tubular sodium reabsorption by hypernatremia. J. clin. Invest. 44, KTINrAN, L. I. (1975). Renal sodium reabsorption during saline loading and distal blockade in newborn dogs. Am. J. Physiol. 228, KLEIAN, L. I. & REUTER, J. H. (1974). Renal response of the new-born dog to a saline load: the role of the intrarenal blood flow distribution. J. Physiol. 239,
16 98 JEFFREY T. BAKER AND SIDNEY SOLOMON KuNAU, R. T., WEBB, H. L. & BuuM"., S. C. (1974). Characteristics of the relationship between the flow rate of tubular fluid and potassium transport in the distal tubule of the rat. J. cdin. Invest. 54, MALNIc, G., KLOSE, R. M. & GIEBISCH, G. (1966). Micropuncture study of distal tubular potassium and sodium transport in rat nephron. Am. J. Physiol. 211, McCANcE, R. A. & WIDDOWSON, E. M. (1957). Hypertonic expansion of the extracellular fluids. Acta paediat., Stockh. 46, McCANcE, R. A. & WILXXNsON, E. (1947). The response of adult and suckling rats to the administration of water and of hypertonic solutions of urea and salt. J. Physiol. 16, PARIC, N., POPA, G., GAT-AsX, R., GAL.sxz, W. & STEINHAUSEN, M. (1973). Renal test dyes. I. Physical and chemical properties of some dyes suitable for renal passage time measurements. Pfluiger8 Arch. ge8. Physiol. 343, 1-9. SOLOMON, S. (1974a). Maximal gradients of Na and K across proximal tubules of kidneys of immature rats. Biologia neonat. 25, SOLOMON, S. (1974b). Absolute rates of sodium and potassium reabsorption by proximal tubule of immature rats. Biologia neonat. 25, SOLOMON, S. & CAPER, K. (1972). Regulation of superficial single nephron glomerular filtration rates in infant rats. Proc. Soc. exp. Biol. Med. 139, SPITZER, A. & BRANDEis, M. (1974). Functional and morphologic maturation of the superficial nephrons: relationship to total kidney function. J. dlin. Invest. 53, WRGHT, F. S. & GIEBISCH, G. (1972). Glomerular filtration in single nephrons. Kid. Int. 1,
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