Role of the Sympathetic Nervous System

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1 Role of the Sympathetic Nervos System in the Renal Response to Hemorrhage JOHN R. GCL, JR., and AimED G. T. CASPER From the Endocrinology Branch, National Heart Institte, National Instittes of Health, Bethesda, Maryland 214 A B ST RA CT In 12 stdies, a femoral artery and vein of a donor dog treated with desoxycorticosterone were connected by tbing to a renal artery and vein of a recipient dog treated with desoxycorticosterone, and the kidney with its nerve spply intact was perfsed at femoral arterial pressre. Infsion of normal saline, which contained albmin, from 2.7 to 3.1 g/1 ml, in the donor prodced significant natriresis in a kidney of the donor (from 112 to 532 1Eq/min) and in the perfsed kidney (from 6 to 31 JLEq/min) of the recipient. Increased sodim excretion in the perfsed kidney was associated with an increase in the clearances of inlin and paraaminohipprate (P <.1) and a decrease in hematocrit of perfsing blood (P <.1). Infsion was contined in the donor while recipient was bled 23 ml/kg, with a decrease in mean arterial pressre from 152 to 13 mm Hg. Sodim excretion in perfsed kidney decreased from 31 to 142 Eq/min (P <.1), whereas sodim excretion in donor was nchanged (56 vs. 532 Eq/min; P >.3). Clearance of inlin by perfsed kidney was not significantly affected by bleeding (26 +SE 2 vs. 25 +SE 2; P >.2), bt the clearance of paraaminohipprate was decreased by bleeding (P <.1), so that filtration fraction increased. As the perfsed kidney of the recipient dog contined to receive blood from the natriretic donor dog when the recipient dog was bled, the decrease in sodim excretion that bleeding prodced in the perfsed kidney was presmably mediated by renal nerves. Ths, an increase in nervos stimli to the kidney that is not sfficient to decrease glomerlar filtration rate can increase the tblar reabsorption of sodim and thereby significantly decrease its excretion. This property of the sympathetic nervos system to affect tblar reabsorption of sodim sggests This work was presented in part at the 1st Annal Meeting of the American Society of Nephrology, October 1967, Los Angeles, Calif. Received for pblication 25 October 1968 and in revised form 27 December that an increase in sympathetic activity may constitte an important mechanism for the renal conservation of sodim when intravasclar volme is contracted by hemorrhage or other case. INTRODUCTION Moderate hemorrhage increases sympathetic activity, most likely as a reslt of the effects of a decrease in effective circlating blood volme on baroreceptors (1). The conseqent constriction of arterioles and veins and agmentation of cardiac contraction tend to minimize the decrease in arterial pressre which wold occr were it not for an increase in sympathetic activity (2). If the increase in sympathetic activity does not prevent a decrease in arterial pressre. then a decrease in glomerlar filtration occrs and this decrease correlates well with the decrease in arterial pressre (3). The increase in sympathetic activity also appears to involve the kidneys and to contribte to the decreases in glomerlar filtration rate and renal blood flow. Ths, when Dibenzyline, an alpha adrenergic blocking agent, was injected into a renal artery before bleeding, it partially prevented a decrease in glomerlar filtration rate and renal blood flow ipsilaterally (4). A decrease in arterial pressre and an increase in sympathetic activity together provide a potent stimls to increase the activity of the reninangiotensin system (5), and, in trn, the prodction of aldosterone (6, 7). An interaction of these several factors is the probable case of the decreased renal excretion of sodim that hemorrhage prodces. The present stdies were ndertaken to evalate the effect of the sympathetic nervos system per se on renal fnction in hemorrhage, and to extend the previos observations which sggest that the sympathetic nervos system is part of the mechanism for the renal conservation of sodim (8). In the design of sch an experiment, it is necessary to avoid the effects of a decrease in The Jornal of Clinical Investigation Volme

2 arterial pressre, and, in so far as possible, to minimize the effects of changes in circlating angiotensin and aldosterone. To accomplish this objective, a donor dog treated with desoxycorticosterone was sed to perfse a kidney of a desoxycorticosteronetreated recipient dog withot destrction of the nerve spply to the perfsed kidnev. Natriresis was established in the donor dog and in the perfsed kidney to permit better characterization of renal nerve discharge as a stimls to decrease the renal excretion of sodim. The recipient dog was then bled to increase the sympathetic nerve discharge to the perfsed kidney that was protected from the other changes that accompany bleeding. METHODS For each stdy, two mongrel dogs weighing 1728 kg were given a sodim intake of 5 meq/day for 4 days and desoxycorticosterone, 5 mg i.m., the day before and morning of the stdy. After both dogs were anesthetized with Pentothal, hydrated with 48 ml of normal saline, and anticoaglated with heparin, a femoral artery and vein of the donor dog were connected by polyethelene tbing (PE 28 gradated to PE 4) to the left renal artery and vein of the recipient dog, whose kidney was ths perfsed at femoral arterial pressre. Care was taken to preserve the nerve spply to the perfsed kidney, except for for stdies in which the nerve spply to the perfsed kidney was interrpted at the time of cannlation of the renal vessels (experiments 16, 21, 22, and 39). Mean arterial pressre (MAP) was measred in both dogs from catheters in the aorta (9) and rine was collected throgh reteral catheters from both kidneys of the recipient dog and one kidney of the donor. Normal saline containing inlin, paraaminohipprate and pitressin,.2 U/ml, was infsed into both dogs at 1 ml/min by a constant infsion pmp. The experimental design is shown schematically in Fig. 1. Clearance measrements were started approximately 1 hr after the operative procedre; three control periods were obtained, then normal saline, 21 ml, was rapidly infsed into the donor dog, fol MAP URINE DONOR IN REC IPIENT ~~~~~~URINE FIGURE 1 Schematic presentation of the experimental procedre. MAP = mean arterial pressre. 916 J. R. Gill, Jr., and A. G. T. Casper lowed by a continos infsion of normal saline that contained hman albmin, from 2.7 to 3.1 g/1 ml at 15 ml per min, for the remainder of the experiment. The total volme given to the donor dog dring an experiment ranged from 27 to 4 ml. Blood loss in the recipient dog was replaced by normal saline to prevent an increase in sympathetic activity before experimental hemorrhage. After rine flow from the donor dog and from the perfsed kidney of the recipient dog had reached maximal rates, the recipient dog was bled ntil there was an obvios decrease in rine flow from the perfsed innervated kidney. The mean volme of blood shed approximated 2.3% of body weight (mean, 22.7 kg) except in the for experiments in which the perfsed kidney was denervated and in these stdies it was greater and approximated 3.2% of body weight (mean, 22.8 kg). Each stdy consisted of 1116 clearance periods; all clearance periods were 2 min in dration. The clearances of inlin (Ci.) and paraaminohipprate (CPAH) were determined as previosly described (9). The vales presented are the means of from two to for periods: a) immediately before infsion (control), b) dring infsion when sodim excretion by the perfsed kidney was maximal, c) dring and immediately after hemorrhage (seven experiments pls the for experiments in which the perfsed kidney was denervated) and 235 min after completion of hemorrhage (experiments 55, 56, 57, 62, and 64). Standard errors of the mean (SE) are presented for Ci.. The significance of the data was determined by paired analysis. RESULTS Fig. 2 shows the reslts of a stdy in which natriresis in a donor dog was maintained by contined infsion while the recipient dog was bled. In the donor, dring infsion, sodim excretion increased from 248 to 557,Eq/min with an increase in CPAr and G. bt not in MAP. In the recipient dog, sodim excretion in the perfsed kidney increased from 73 to 298 /Eq/min with an increase in CPAH bt not in G.. Sodim excretion in the contralateral kidney was not affected. When the recipient dog was bled, MAP decreased slightly from 145 to 14 mm Hg, and sodim excretion decreased from 143,Eq/min to 87 /AEq/min, bt CPAH and G. were nchanged. Sodim excretion in the perfsed kidney decreased from 298 to 174 /AEq/min withot a change in CPAH and GIn. In the donor dog sodim excretion, MAP, and GIn were essentially nchanged, whereas CPAH increased from 141 to 153 ml/min. The reslts of 12 sch stdies are presented in Table I. Infsion in the donor dog increased sodim excretion from a mean vale of 112 JEq/min to 532,Eq/min with an increase in mean CPAH from 91 ml/min to 125 ml/min (P <.1), an increase in mean CG from 33, +SE 3 to 37 ±SE 3 (P <.5), and an increase in mean MAP from 154 mm Hg to 169 mm Hg (P <.2). Mean hematocrit in the donor dog decreased from 46% to 29% (P <.1). In the recipient dog, sodim excretion in the perfsed kidney increased in response to infsion in' the donor dog from a mean vale of 6 /AEq/min to 31 Eq/min

3 E 71 DONOR DOG RECIPIENT DOG Infsion D MAP mm Hg CPAH ml/min CIN ml/min UnaV IAEq /min O Ml NUTES FIGURE 2 Effect of infsion in donor dog (D) and of infsion in donor dog together with bleeding of recipient dog (R) on MAP (mean arterial pressre), CPAH (clearance of paraaminohipprate), CIn (clearance of inlin) and UNaV (sodim excretion) in the donor dog and in the recipient dog. The solid dots nder recipient dog denote the perfsed kidney. Note that bleeding the recipient dog decreased sodim excretion bt did not affect Ci. in the perfsed kidney, and did not change UN.V in donor dog. (P <.1), with an increase in mean CPAH from 66 ml/ min to 91 ml/min (P <.1) and in mean Cin from 23 +SE2 to 26 +SE2 (P <.1). The recipient dog was then bled 23 ml/kg. The reslts of observations made dring and immediately after hemorrhage were similar to the reslts obtained after a wait of 235 min from the end of hemorrhage (experiments 5557, 62, 64). Mean MAP in the recipient dog decreased with bleeding from 152 to 13 mm Hg (P <.1). Mean CPAH decreased from 8 ml/min to 69 ml/ min (P <.5), mean Cin decreased from 35 ±SE 3 ml/ min to 28 +SE 4 ml/min (P <.1) and mean sodim excretion decreased from 133 /AEq/min to 46 Eq/min (P <.1). In the perfsed kidney, mean sodim excretion decreased from 31 /AEq/min to 142 /AEq/min (P <.1) with a decrease in mean CPAH from 91 ml/min to 81 ml/min (P <.1), bt withot a change in mean Cin (26 +SE 2 vs. 25 +SE 2 ml/min) (P >.2). In the donor dog, mean sodim excretion wvas sstained (532 vs. 56,Eq/min) as mean CPAH, mean 7MAP. and mean hematocrit decreased (the latter two variables, significantly, P <.1), and, CIn increased (P <.1). The reslts of for stdies in which the perfsed kidney lacked a normal nerve spply are presented in Table II. Infsion in the donor dog increased sodim excretion in the donor dog from a mean vale of 22 Eq/min to 461,mEq/min and in the perfsed kidney of the recipient dog from a mean vale of 9 /Eq/min to 258 /AEq/ min. The recipient dog was then bled 32 ml/kg. MNean MAP in the recipient dog decreased with bleeding from 156 to 91 mm Hg. In the two stdies in which they were determined, mean CPAH decreased from 7 ml/min to 28 ml/min and mean Cnx decreased from 34 ml/min to 13 ml/min. Mean sodim excretion decreased from 61 Eq/ min to 16,tEq/min. In the perfsed kidney. mean sodim Renal Nerves and the Renal Response to Hemorrhage 917

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6 TABLE I I Effect of Denervation of Perfsed Kidney Donor dog Recipient dog Right kidney Perfsed kidney Contralateral kidney Experiment Regimen UNN Cmn CPAH MAP Hct UNav CIn CPAH UNaV Crn CPAH MAP peq/min ml/min mm Hg % peq/min ml/min IAEq/min ml/min mm Hg 16 C* ID HR C ID HR C ID HR C ID HR Mean C ID HR Specimens were lost before determination of Ci. and CPAH for experiments 21 and 22. * C = control t ID = infsion of normal saline which contained albmin, from 2.7 to 3.1 g/1 ml in the donor dog. HR = bleeding of recipient dog pls infsion in donor dog. CI,, = mean clearance of inlin; CPAH = mean clearance of Paminohipprate; MAP = mean arterial pressre; Hct = hematocrit: UNAV = sodim excretion. excretion, mean Cin and mean CPAH showed little change (258 vs. 268 Eq/min, 38 vs. 34 ml/min, and 64 vs. 64 ml/min, respectively). In the donor dog mean sodim excretion, mean CIn mean CPAH, and mean MAP were sstained (461 vs. 435 Eq/min, 26 vs. 28 ml/min, 6 vs. 58 ml/min, and 158 vs. 156 mm Hg, respectively). DISCUSSION In 12 stdies in which a kidney of a recipient dog with its nerve spply intact was perfsed by blood from a donor dog at femoral arterial pressre, the recipient dog showed a significantly lower CPAH (P <.2) and CI. (P <.2) in the perfsed kidney than in the contralateral kidney dring the control observations (Table I). Operative maniplation of a kidney can prodce as great a decrease in CPAH and G. as that observed in the present stdies, and is very likely the reason for the diminished fnction of the perfsed kidney (4). The effect of maniplation on CPAH and Gn can be abolished by an injection of Dibenzyline, an alpha adrenergic blocking agent, into the renal artery (4). When the nerve spply to the perfsed kidney was interrpted, mean CPAH and Gn in the perfsed kidney were comparable to those in the contralateral kidney (Table II). Renal denervation at the time of maniplation also appears to prevent alterations in the pattern of renal blood flow that accompany maniplation of the kidney (1). The effects of maniplation therefore probably reslt from increased renal nerve discharge with vasoconstriction. Infsion of normal saline, which contained albmin, from 2.7 to 3.1 g/1 ml, in the donor dog prodced a natriresis in the donor dog (532 Eq/min) and in the perfsed (31,Eq/min) bt not in the contralateral kidney of the recipient dog (Table I). The natriresis was accompanied by significant increases in MAP, CPAH, and Cln, and a significant decrease in hematocrit in the donor dog, and by significant increases in both CPAH and Cln in the perfsed kidney. Recent stdies sggest that physical factors (increase in mean arterial pressre, decrease in hematocrit, and increase in renal blood flow) (11) and release of a "natriretic sbstance" (12) are the principal determinants of the decrease in tblar reabsorption of sodim (13) and of the increased excretion of sodim that occrs in response to expansion of the intravasclar vol 92 J. R. Gill, Jr., and A. G. T. Casper

7 me with saline or plasma. All of these factors, as well as an increase in glomerlar filtration rate, cold have mediated the natriretic response of the donor dog and of the perfsed kidney of the recipient dog. While the infsion was contined in the donor dog, the recipient dog was bled ntil there was an appreciable decrease in rine flow from the perfsed kidney. The reslt was a 5% decrease in sodim excretion by the perfsed kidney from 31 to 142 /xeq/min (P <.1), withot a significant change in sodim excretion by the donor dog (532 vs. 56,Eq/min (P >.3) (Fig. 2, Table I). The decrease in sodim excretion ths occrred despite contined exposre of the perfsed kidney to natriretic stimli sch as hemodiltion (14) and, possibly, a circlating "natriretic sbstance" (12), which wold tend to oppose sch a decrease. Presmably, the sympathetic nerves of the recipient dog which spplied the perfsed kidney mediated its response to a blood loss of 23 ml/kg with a decrease in MAP of 14% in the recipient dog. A blood loss of from 1 to 12 ml/kg is sfficient to increase renal resistance and, ths, is probably a sfficient stimls to increase the rate of discharge of the renal nerves (15). When the sympathetic nerve spply from the recipient dog to the perfsed kidney had been interrpted, however, the perfsed kidney was naffected by a blood loss of 32 ml/ kg with a decrease in MAP of 42% in the recipient dog. Whereas the effect of hemorrhage on blood flow was comparable in the innervated perfsed and contralateral kidneys (a decrease of 1 ml/min, or 11%, and 11 ml/ min, or 14%, respectively), the effect on glomerlar filtration rate was considerably greater in the contralateral kidney (a decrease of 7 ml/min, or 2%, as opposed to 1 ml per min) (Table I). Previos stdies on the renal response to hemorrhage indicate that the degree of decrease in glomerlar filtration rate correlates well with the degree of decrease in arterial pressre (3). Therefore, one wold expect the decrease in mean arterial pressre of 22 to 13 mm Hg in the recipient dog to have a greater effect on glomerlar filtration rate than the decrease of 1 to 159 mm Hg in the donor dog (Table I). Normally, changes in mean arterial pressre of this magnitde have very little effect on renal blood flow or glomerlar filtration rate when vasclar tone is normal (16). Ths, the increased renal vasclar tone associated with increased sympathetic activity probably acconts for the loss of the normal stability of glomerlar filtration rate and its greater dependence pon arterial pressre following hemorrhage. The decrease in sodim excretion in the perfsed innervated kidney when the recipient dog was bled was associated with a significant decrease in mean CPAII (P <.1), bt not in mean Cim (P >.2) in the perfsed kidney. These findings sggest that the change in sodim excretion in the perfsed kidney which accompanied hemorrhage in the recipient dog reslted from a change in the tblar reabsorption of sodim. As sggested above, an increase in nervos stimli to the perfsed kidney best explains an increase in sodim reabsorption when it occrs in response to hemorrhage in a dog connected by renal nerves bt not by blood spply to that kidney. In this case, 'the blood was spplied by a donor dog with stable sodim excretion. An increase in sympathetic nerve discharge cold increase the tblar reabsorption of sodim in several ways: first, a decrease in the volme of interstitial flid arond the proximal tbles as a reslt of an increase in oncotic pressre of the blood in the peritblar capillaries cold indirectly lead to an increase in the tblar reabsorption of sodim (17). When the recipient dog was bled, filtration fraction increased from.29 to.31 in the perfsed kidney and this change is compatible with an increase in peritblar capillary oncotic pressre. If, in addition, hemorrhage decreased peritblar capillary hydrostatic pressre, then this change wold also tend to decrease the volme of interstitial flid and to agment the effect of increased capillary oncotic pressre. Second, an increase in the proportion of total renal glomerlar filtrate that traverses jxtamedllary nephrons with long loops and, presmably, with a greater capacity for sodim reabsorption cold lead to an increase in the tblar reabsorption of sodim (18). This hypothesis is based on the reports that hemorrhagic hypotension decreased blood flow throgh the sperficial cortex bt had little effect on blood flow throgh the jxtamedllary area (19, 2). More recent stdies, however, indicate that hemorrhagic hypotension decreases cortical and medllary blood flow to the same extent and ths do not spport the concept of a selective resistance of the jxtamedllary circlation to hemorrhage (21). Conceivably, glomerlar filtration rate cold increase in the jxtamedllary area relative to the sperficial cortical area in response to hemorrhage despite a comparable decrease in blood flow in the two areas. It has recently been sggested that a decrease in the intake of sodim leads to a decrease in glomerlar filtration rate in sperficial cortical nephrons bt an increase in glomerlar filtration rate in the jxtamedllary nephrons (22). Third, an increase in sodim reabsorption cold reslt from a direct effect of the renal nerves or catechols on tblar transport processes. The extent to which any or all of these three mechanisms are operative remains to be established. Ths, in the present stdy, a decrease in the volme of extracelllar flid prodced by hemorrhage prodced a sizable decrease in the renal excretion of sodim with Renal Nerves and the Renal Response to Hemorrhage 921

8 ot a decrease in glomerlar filtration rate, presmably as a reslt of an increase in the tblar reabsorption of sodim mediated by an increase in sympathetic nervos system activity. In a previos stdy, a decrease in the volme of extracelllar flid prodced by restriction of dietary sodim did not decrease the renal excretion of sodim in a normal fashion despite a decrease in glomerlar filtration rate and mean arterial pressre, when sympathetic nervos system activity was blocked, presmably as a reslt of the inability of the sympathetic nervos system to increase the tblar reabsorption of sodim (8). Together, these two stdies provide evidence that the sympathetic nervos system may play an important role in the normal renal conservation of sodim throgh its ability to increase the tblar reabsorption of sodim. ACKNOWLEDGMENT We are gratefl for the invalable technical assistance of John Tate, James Cox, Belle Rskin, and Harvey J. McDonald. REFERENCES 1. Chien, S Role of the sympathetic nervos system in hemorrhage. Physiol. Rev. 47: Wagner, H. N The inflence of atonomic vasoreglatory reflexes on the rate of sodim and water excretion in man. J. Clin. Invest. 36: Coelho, J. B., and S. E. Bradley Fnction of the nephron poplation dring hemorrhagic hypotension in the dog, with special reference to the effects of osmotic diresis. J. CGin. Invest. 43: Handley, C. A., and J. H. Moyer Unilateral renal adrenergic blockade and the renal response to vasopressor agents and to hemorrhage. J. Pharmacol. Exp. Ther. 112: Vander, A. J Control of renin release. Physiol. Rev. 47: Carpenter, C. C. J., J.. Davis, and C. R. Ayers Relation of renin, angiotensin II, and experimental renal hypertension to aldosterone secretion. J. Clin. Invest. 4: Slater, J. D. H., B. H. Barbor, H. H. Henderson, A. G. T. Casper, and F. C. Bartter Inflence of the pititary and the reninangiotensin system on the secretion of aldosterone, cortisol and corticosterone. J. Clin. Invest. 42: Gill, J. R. Jr., and F. C. Bartter Adrenergic nervos system in sodim metabolism. II. Effects of ganethidine on the renal response to sodim deprivation in nor, mal man. N. Engl. J. Med. 275: Gill, J. R. Jr., A. A. Carr, L. E. Fleischman, A. G. T. Casper, and F. C. Bartter Effects of pentolinim on sodim excretion in dogs with constriction of the vena cava. Amer. J. Physiol. 212: Rosen, S. M., B. P. Trniger, H. R. Kriek, J. E. Mrray, and J. P. Merrill Intrarenal distribtion of blood flow in the transplanted dog kidney: effect of denervation and rejection. J., Clin. Invest. 46: Martino, J. A., and L. E. Earley Demonstration of a role of physical factors as determinants of the natriretic response to volme expansion. J. Clin. Invest. 46: Rector, F. C. Jr., M. MartinezMaldonado, N. A. Krtzman, J. C. Sellman, F. Oerther, and D. W. Seldin Demonstration of a hormonal inhibitor of proximal tblar reabsorption dring expansion of extracelllar volme with isotonic saline. J. Clin. Invest. 47: Dirks, J. H., W. J. Cirksena, and R. W. Berliner The effect of saline infsion on sodim reabsorption by the proximal tble of the dog. J. Clin. Invest. 44: Craig, G. M., I. H. Mills, G. W. Osbeldiston, and B. L. Wise The effect of change in perfsion pressre and haematocrit in the perfsed isolated kidney of the dog. J. Physiol. (London). 186: 113 P. 15. Abel, F. L., and Q. R. Mrphy Mesenteric, renal and iliac vasclar resistance in dogs after hemorrhage. Amer. J. Physiol. 22: Thra, K., and K. Kramer Weitere nterschngen zr myogen Natr der Atoreglation des Nierenkreislafes, Afhebng der Atoreglation drch msklotrope Sbstanzen and drckpassives Verhalten des Glomerlsfiltrates. Pfleger Arch. Ges. Physiol. 269: Lewy, J. E., and E. E. Windhager Peritblar control of proximal tblar flid reabsorption in the rat kidney. Amer. J. Physiol. 214: Barger, A. C Renal hemodynamic factors in congestive heart failre. Ann. N. Y. Acad. Sci. 139: Selkrt, E. E., and M. J. Elpers Inflence of hemorrhagic shock on renal hemodynamics and osmolar clearance in the dog. Amer. J. Physiol. 25: Carriere, S., G. D. Thorbrn, C. C. C. O'Morcloe, and A. C. Barger Intrarenal distribtion of blood flow in dogs dring hemorrhagic hypotension. Circ. Res. 19: Akland, K., and M. Wolgast Effect of hemorrhage and retransfsion on intrarenal distribtion of blood flow in dogs, J. Clin. Invest. 47: Horster, M., and K. Thra Micropnctre stdies on the filtration rate of single sperficial and jxtamedllary glomerli in the rat kidney. Pfleger Arch. Ges. Physiol. 31: J. R. Gill, Jr., and A. G. T. Casper

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