Original Article
Sympathetic Overactivity in Patients with Chronic Renal Failure
N Engl J Med 1992; 327:1912-1918December 31, 1992
- Abstract
- Abstract
Background.
Hypertension is a frequent complication of chronic renal failure, but its causes are not fully understood. There is indirect evidence that increased activity of the sympathetic nervous system might contribute to hypertension in patients with end-stage renal disease, but sympathetic-nerve discharge has not been measured directly in patients or animals with chronic renal failure.
Methods.
We recorded the rate of postganglionic sympathetic-nerve discharge to the blood vessels in skeletal muscle by means of microelectrodes inserted into the peroneal nerve in 18 patients with native kidneys who were undergoing long-term treatment with hemodialysis (of whom 14 had hypertension), 5 patients receiving hemodialysis who had undergone bilateral nephrectomy (of whom 1 had hypertension), and 11 normal subjects.
Results.
The mean (±SE) rate of sympathetic-nerve discharge was 2.5 times higher in the patients receiving hemodialysis who had not undergone nephrectomy than in the normal subjects (58±3 vs. 23±3 bursts per minute, P<0.01). In contrast, the rate of sympathetic-nerve discharge was similar in the patients receiving hemodialysis who had undergone bilateral nephrectomy (21±6 bursts per minute) and the normal subjects. The rate of sympathetic-nerve discharge in the patients receiving hemodialysis who had not undergone nephrectomy was also significantly higher (P<0.01) than that in the patients with bilateral nephrectomy, and it was accompanied in the former group by higher values for vascular resistance in the calf (45±4 vs. 22±4 units, P<0.05) and mean arterial pressure (106±4 vs. 76±14 mm Hg, P<0.05). The rate of sympathetic-nerve discharge was not correlated with either plasma norepinephrine concentrations or plasma renin activity.
Conclusions.
Chronic renal failure may be accompanied by reversible sympathetic activation, which appears to be mediated by an afferent signal arising in the failing kidneys. (N Engl J Med 1992;327:1912–8.)
Media in This Article
Figure 1
Recordings of Sympathetic-Nerve Discharge to the Vasculature of the Leg Muscles in a Normal Subject and in Two Patients Receiving Hemodialysis, One with and One without Bilateral Nephrectomy.Figure 2
Mean Arterial Pressure, Vascular Resistance in the Calf, and Sympathetic-Nerve Discharge in the Patients Receiving Hemodialysis Who Had Undergone Bilateral Nephrectomy and in Those Who Had Not Undergone Nephrectomy.Article Activity
- Article
HYPERTENSION occurs in up to 80 percent of patients with chronic renal failure and is a major risk factor for the excessive cardiovascular morbidity and mortality among these patients.1 2 3 However, the underlying causes of this hypertension are not fully understood. There is indirect evidence to suggest that increased activity of the sympathetic nervous system might contribute to hypertension in patients with end-stage renal disease,4 5 6 7 8 9 10 11 12 13 but sympathetic-nerve discharge has not previously been measured directly in patients or animals with chronic renal failure.
Studies in animals have indicated that the kidney is a sensory organ containing mechanically and chemically sensitive afferent nerves that may be involved in the pathogenesis of hypertension by causing reflex activation of the sympathetic nervous system.14 15 16 17 18 Because experimental stimulation of chemosensitive renal afferent nerves by either ischemic metabolites or uremic toxins evokes reflex increases in efferent sympathetic-nerve activity and blood pressure in animals,14 , 15 we hypothesized that in patients treated with hemodialysis, long-term stimulation of these afferent nerves might cause chronic sympathetic overactivity. Because renal afferent denervation can reduce efferent sympathetic overactivity and blood pressure in experimental hypertension,17 , 18 we further hypothesized that in patients with chronic renal failure sympathetic overactivity might be reduced by bilateral nephrectomy, which eliminates renal afferent nerve endings. We therefore used microelectrodes to record postganglionic sympathetic-nerve action potentials in patients undergoing long-term hemodialysis who had had a bilateral nephrectomy and in those who had not.
Methods
Subjects
We studied 18 patients undergoing long-term maintenance hemodialysis whose kidneys had not been removed, 5 patients undergoing long-term maintenance hemodialysis who had undergone bilateral nephrectomy, and 11 normal subjects (Table 1Table 1
Characteristics of the Three Groups of Subjects.*). The patients who had not undergone nephrectomy had been treated by hemodialysis for 5 to 120 months (mean, 29). The patients who had undergone nephrectomy had been operated on 11 to 96 months (mean, 35) earlier. The causes of the chronic renal failure in the two groups of patients were chronic glomerulonephritis (six patients), obstructive uropathy (five patients), hypertension (four patients), renal failure related to treatment with analgesic drugs (two patients), interstitial nephritis (one patient), Alport's syndrome (one patient), and unknown (four patients). In the anephric patients, the indications for bilateral nephrectomy were chronic reflux in four patients and uncontrolled hypertension in one patient. Patients with diabetes mellitus, congestive heart failure, alcohol abuse, cardiac arrhythmias, evidence of peripheral or autonomic neuropathy, or other serious systemic illnesses were excluded. Nine patients were taking antihypertensive medications, and these were discontinued in five patients 48 hours before the study began and continued in four patients, in whom it was deemed unsafe to discontinue treatment.The subjects were studied in the human neurophysiology laboratories of the University of Texas Southwestern Medical Center, Dallas, and the Cleveland Clinic Foundation, Cleveland. The protocol was approved by the institutional review boards of both institutions, and all subjects provided written informed consent before participation.
General Procedures
All studies were performed with the subject in the supine position. Heart rate (measured by electrocardiography), blood pressure (measured with a Dinamap sphygmomanometer; Critikon, Tampa, Fla.), and efferent sympathetic-nerve discharge to the vasculature of the leg muscles were recorded continuously, and blood flow in the calf (measured by plethysmography) was recorded once every 15 seconds. All data were stored on a TEAC R-71 tape recorder (Tokyo, Japan) and transcribed onto paper with a Gould ES1000 electrostatic recorder (Oxnard, Calif.).
Recording of Sympathetic-Nerve Discharge
Multiunit recordings of postganglionic sympathetic-nerve discharge were obtained with unipolar tungsten microelectrodes inserted selectively into the fascicles of the peroneal nerve that innervate blood vessels in the distal leg muscles.19 The neural signals were amplified 20,000 to 50,000 times, filtered (bandwidth, 700 to 2000 Hz), rectified, and integrated (time constant, 0.1 second) to obtain a mean-voltage neurogram, with each multiunit discharge of sympathetic activity being displayed as a narrow peak, or "burst" (Fig. 1Figure 1
Recordings of Sympathetic-Nerve Discharge to the Vasculature of the Leg Muscles in a Normal Subject and in Two Patients Receiving Hemodialysis, One with and One without Bilateral Nephrectomy.). A recording of sympathetic discharge was considered acceptable when the neurograms revealed spontaneous bursts of neural activity, with the largest bursts showing a minimal signal-to-noise ratio of 3:1. At the beginning of each experiment, we confirmed that the impaled nerve fiber innervated skeletal muscle rather than skin by demonstrating that electrical stimulation through the microelectrode elicited muscle twitches rather than paresthesias. We also confirmed that the spontaneous activity recorded was efferent discharge in sympathetic-nerve fibers (which innervate vascular smooth muscle) rather than motor or sensory activity by demonstrating that this activity was under baroreceptor-reflex regulation, as evidenced by cardiac rhythmicity (i.e., the minimal interburst interval equaled the length of the cardiac cycle) and a characteristic biphasic response to the Valsalva maneuver.20 This response consists of sympathetic activation during phases II and III (responding to a decrease in blood pressure) followed by sympathetic inhibition during phase IV (responding to an increase in blood pressure on release); the response during phase IV is used to define the noise level.Sympathetic bursts were detected by inspecting the filtered and mean-voltage neurograms. A deflection on the mean-voltage display was counted as a burst if it had a minimal signal-to-noise ratio of 2:1 and if the interval between bursts was equal to or a multiple of the RR interval on the electrocardiogram. The interobserver and intraobserver variations in identifying bursts were less than 10 percent and less than 5 percent, respectively.21 Inadvertent contraction of the leg muscle adjacent to the recording electrode produced electrical artifacts that were easily distinguished from sympathetic bursts; neurograms that revealed such artifacts were excluded from the analysis. The rate of sympathetic-nerve discharge was expressed as the number of bursts of sympathetic activity per minute; this rate normally varies by less than 15 percent when an individual subject is studied on repeated occasions.20 No attempt was made to measure the amplitude of sympathetic bursts, since this measurement depends on the position of the recording electrode in the nerve fascicle. All nerve recordings were analyzed by an investigator who was unaware of the group assignment of the subjects.
Measurement of Blood Flow in the Calf
While recording sympathetic outflow to the calf muscles in one leg, we simultaneously measured blood flow in the calf of the contralateral leg using venous-occlusion plethysmography.22 The calf was elevated above the level of the right atrium to collapse the veins. The circulation to the foot was arrested during the determinations of blood flow, which were performed at 15-second intervals. Vascular resistance in the calf was calculated as the mean arterial pressure (one third of the pulse pressure plus the diastolic pressure), expressed in millimeters of mercury, divided by blood flow in the calf, expressed in milliliters per minute per 100 ml of tissue.
Experimental Protocol
To ensure that the base-line values were stable, all subjects rested quietly for 30 minutes after the plethysmographic cuff had been applied and the microelectrode inserted. Heart rate, blood pressure, nerve activity, and blood flow at rest were recorded continuously for 60 minutes. The values for these variables represent the mean for this period. In the patients receiving hemodialysis, the study was performed in the dialysis unit immediately before the start of hemodialysis. In four of the patients who had not undergone nephrectomy, the same measurements were repeated on two consecutive days (i.e., 24 hours before and 1 hour before hemodialysis) to determine whether sympathetic-nerve discharge is affected by changes in plasma-volume status during the period between dialysis treatments.
Measurements of Plasma Renin Activity, Norepinephrine, and Angiotensin II
In the patients receiving hemodialysis, blood samples were drawn from the dialysis access to the forearm fistula just before the start of hemodialysis. In the normal subjects, blood samples were drawn from an indwelling catheter in a forearm vein. The samples were collected in prechilled tubes treated with heparin for the measurement of plasma norepinephrine, in tubes treated with EDTA for the determination of plasma renin activity, and in tubes treated with a protease inhibitor for the measurement of plasma angiotensin II; all tubes were promptly centrifuged at 4°C. Plasma norepinephrine was measured by a radioenzymatic assay with a sensitivity of 15 pg per milliliter (0.09 nmol per liter).23 Plasma renin activity was measured by a radioimmunoassay with a sensitivity of 0.005 ng per milliliter per hour (0.002 ng per liter · second).24 Plasma angiotensin II was measured after plasma extraction by a radioimmunoassay with a sensitivity of 1.0 pg per milliliter (0.95 pmol per liter).25 The assays for plasma norepinephrine, plasma renin activity, and angiotensin II were performed at the Cleveland Clinic Foundation.
Statistical Analysis
The mean differences between the three groups were compared by analysis of variance, with Dunnett's test for comparisons between pairs of treatment groups. Unpaired t-tests were used for the analysis of plasma biochemical values between the two groups of patients receiving hemodialysis. Correlation coefficients were calculated according to the method of least squares. A P value of less than 0.05 was considered to indicate significance.
Results
The characteristics of the study groups are shown in Tables 1 and 2Table 2
Predialysis Laboratory Values in the Patients Receiving Hemodialysis Who Had Not Undergone Nephrectomy and in Those Who Had Undergone Bilateral Nephrectomy.*, and representative recordings of sympathetic-nerve discharge in each group are shown in Figure 1. In the patients receiving hemodialysis who had not undergone nephrectomy, the sympathetic-nerve discharge retained its normal cardiac rhythmicity (i.e., the minimal interval between bursts equaled the length of the cardiac cycle), but the rate of discharge was 2.5 times higher than that in the normal subjects (mean [±SE], 58±3 vs. 23±3 sympathetic bursts per minute; P<0.01). Although the two groups of patients receiving hemodialysis were comparable with respect to plasma electrolyte and serum creatinine concentrations, arterial blood gas values, and body weight (Table 2), the sympathetic-discharge rate in the patients who had not undergone nephrectomy was 2.8 times higher than in the patients who had undergone nephrectomy (P<0.01); the value in the latter group was indistinguishable from that in normal subjects (21±6 vs. 23±3 bursts per minute) (Fig. 1 and 2Figure 2Mean Arterial Pressure, Vascular Resistance in the Calf, and Sympathetic-Nerve Discharge in the Patients Receiving Hemodialysis Who Had Undergone Bilateral Nephrectomy and in Those Who Had Not Undergone Nephrectomy.). The sympathetic nerves fired during 82±4 percent of the cardiac cycles in the patients receiving hemodialysis who had not undergone nephrectomy, but only during 25±6 percent of the cardiac cycles in the patients with nephrectomy (P<0.01) and during 37±5 percent of the cardiac cycles in the normal subjects (P not significant). The lower levels of sympathetic-nerve discharge in the patients with nephrectomy as compared with those without nephrectomy were accompanied by lower levels of regional vascular resistance (22±4 vs. 45±4 units, P<0.05) and mean arterial pressure (76±14 vs. 106±4 mm Hg, P<0.05) (Fig. 2).In the patients receiving hemodialysis who had not undergone nephrectomy, sympathetic-nerve discharge was increased comparably in the five patients whose antihypertensive medications were discontinued before the study, the four who continued to take these medications, and the nine who had never received antihypertensive medications (63±1, 56±9, and 57±4 bursts per minute, respectively). The rate of sympathetic-nerve discharge was equivalent in the nine patients receiving erythropoietin and the nine who were not (60±3 vs. 57±4 bursts per minute). In four patients who were studied on two consecutive days during the interval between dialysis treatments, body weight increased from 70.7±6.1 kg to 73.8±6.1 kg but the rate of sympathetic-nerve discharge was stable (60±2 vs. 58±4 bursts per minute).
Figure 3Figure 3
Relation between Sympathetic-Nerve Discharge to the Vasculature of the Leg Muscles and Plasma Norepinephrine Concentrations in 11 Patients Receiving Hemodialysis Who Had Not Undergone Nephrectomy (Solid Circles), 4 Patients Receiving Hemodialysis Who Had Undergone Bilateral Nephrectomy (Open Circles), and 8 Normal Subjects (Triangles). shows the relation between the rate of sympathetic-nerve discharge and venous plasma norepinephrine concentrations in the three groups. Plasma norepinephrine concentrations were significantly higher in the patients receiving hemodialysis who had undergone nephrectomy and in those who had not undergone nephrectomy than in the normal subjects (534±177 and 495±87 vs. 175±23 pg per milliliter [3.2±1.0 and 2.9±0.5 vs. 1.0±0.1 nmol per liter], P<0.05). However, there was considerable overlap between the groups, and there was no correlation between plasma norepinephrine concentrations and the rate of sympathetic-nerve discharge.Figure 4Figure 4
Relation between Sympathetic-Nerve Discharge to the Vasculature of the Leg Muscles and Plasma Renin Activity in 12 Patients Receiving Hemodialysis Who Had Not Undergone Nephrectomy. shows the relation between sympathetic-nerve discharge and plasma renin activity in patients receiving hemodialysis who had not undergone nephrectomy. Plasma renin activity was markedly elevated in the four patients who were receiving an angiotensin-converting—enzyme inhibitor, as compared with the values in the patients who were receiving no medications at the time of study (14.7±3.0 vs. 3.5±0.6 ng per milliliter per hour [4.1±0.8 vs. 1.0±0.2 ng per liter · second], P<0.01); values in the latter group of patients were within normal limits. Sympathetic-nerve activity was elevated comparably in these two subgroups (55±3 vs. 55±5 bursts per minute), however, and was not correlated with plasma renin activity. Plasma angiotensin II concentrations were within normal limits in patients receiving an angiotensin-converting—enzyme inhibitor and in those who were not receiving such a drug (10.6±3.1 vs. 16.1±2.4 pg per milliliter [10.1±2.9 vs. 15.3±2.3 pmol per liter]).Discussion
We found that the sympathetic vasoconstrictor discharge to the skeletal-muscle circulation was markedly elevated in patients with native kidneys who were receiving long-term treatment with hemodialysis but normal in patients receiving hemodialysis who had undergone bilateral nephrectomy. These results suggest that chronic uremia may be accompanied by reversible sympathetic overactivity, which appears to be mediated by an afferent signal arising in the failing kidneys.
Previous attempts to study the effect of chronic renal failure on the sympathetic nervous system were based mainly on plasma norepinephrine concentrations, which ranged from very low26 27 28 29 to very high.5 , 7 , 10 , 11 Plasma norepinephrine concentrations varied markedly in both our patient groups, and there was no correlation between plasma norepinephrine concentrations and the rate of sympathetic-nerve discharge. This lack of correlation is probably related to the confounding effects of uremia on prejunctional modulation of norepinephrine release and on plasma catecholamine clearance.30 31 32
In contrast to the findings for plasma norepinephrine, an increased rate of sympathetic-nerve discharge was a robust finding in our patients receiving hemodialysis who had not undergone nephrectomy. In these patients, the rate of sympathetic-nerve discharge did not vary as a function of the patients' age or antihypertensive medications. In addition, the increased sympathetic-nerve discharge was unrelated to treatment with erythropoietin, which can exacerbate hypertension in patients with chronic renal failure,33 and was not a nonspecific effect of hypertension, since sympathetic-nerve discharge to the skeletal-muscle circulation previously has been shown to be normal, not elevated, in patients with essential hypertension and normal renal function.34 35 36
The increased sympathetic-nerve discharge in the patients receiving hemodialysis was remarkably constant throughout the interval between dialysis treatments despite the fact that there were large increases in total body water. This finding was unexpected, because in normal humans sympathetic-nerve discharge decreases over time with increases in total body water, a decrease presumably mediated by baroreceptor reflexes.37 , 38 Thus, the reproducibility of increased sympathetic-nerve discharge at different points during the period between dialysis treatments might be interpreted to suggest that uremia activates some excitatory neural influence that overrides the inhibitory baroreceptor reflex—mediated influence of an expanded plasma volume.
That the rate of sympathetic-nerve discharge was normal in patients receiving hemodialysis who had undergone bilateral nephrectomy suggests that sympathetic overactivity in patients with native kidneys who are undergoing long-term treatment with hemodialysis is not caused by the hemodialysis procedure itself, by stimulation of arterial chemoreceptors (since the two groups of patients receiving hemodialysis were comparable with respect to arterial blood gases and hematocrit values), or by permanent alterations in the sympathetic nervous system. In contrast, it appears that bilateral nephrectomy removes some afferent signal arising in the failing kidneys.
Although the precise nature of this signal is not known, at least two possibilities might be considered. First, the failing kidney releases humoral substances, such as renin, that might lead to central activation of sympathetic outflow. Angiotensin II increases central sympathetic outflow experimentally in animals,39 , 40 but in our patients this mechanism is an unlikely explanation for sympathetic overactivity, because it was dissociated from both plasma renin activity and plasma angiotensin II concentrations and appeared to be unaffected by angiotensin-converting—enzyme inhibition. A second and more likely possibility is that intrarenal accumulation of uremic toxins or of other chemical substances present in the uremic milieu might stimulate renal afferent nerves that, in turn, lead to reflex activation of efferent sympathetic-nerve discharge. Experimental stimulation of renal afferent nerves with intrarenal administration of uremic toxins (e.g., urea) or ischémie metabolites (e.g., adenosine) in animals reflexly increases efferent sympathetic-nerve discharge and blood pressure,14 , 15 and renal afferent denervation can reduce sympathetic overactivity and blood pressure in experimental hypertension.17 , 18
In patients undergoing long-term treatment with hemodialysis, the cause of hypertension is undoubtedly multifactorial.3 However, reduced sympathetic-nerve discharge may be one important mechanism by which bilateral nephrectomy lowers blood pressure in patients with chronic renal failure.
Supported by funding from the Extramural Grant Program of the Renal Division of the Baxter Healthcare Corporation, by a National Institutes of Health Career Development Grant (5-T32-HL07360–13), and by grants from the Danish Heart Foundation, the Danish Research Academy, the S&W Foundation, Leo's Kemiske Fabriks Research Foundation, and the National Heart, Lung, and Blood Institute (R0–1 HL44010). Dr. Jacobsen is the recipient of a Fogarty International Research Fellowship (National Institutes of Health, 1-F05-TW04494–01), and Dr. Victor is an Established Investigator of the American Heart Association.
We are indebted to Ms. Patricia Powell for assistance in the preparation of the manuscript; to Mr. Troy Obregon, Mr. Rich Cooley, Ms. Christine Bennett, and Mr. Jay Cology for research assistance; to Drs. R. Sanders Williams, Jere H. Mitchell, Robert Graham, Donald W. Seldin, and Lee Henderson and the members of the Medical Advisory Board of the Extramural Grant Program, Baxter Healthcare Corporation (Renal Division), for their continued support and critical review of this work; to Drs. Magnus O. Magnusson, Robert J. Heyka, Emil P. Paganini, and Karl Brinker for allowing us to study their patients; to Drs. Urs Sherrer and Patricia Painter for their work on the pilot studies; to Dr. Carlos M. Ferrario for performing the assay for angiotensin II; and to Dr. Emanuel L. Bravo for performing the assays for norepinephrine and plasma renin activity.
Source Information
From the Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas (R.L.C., T.N.J., R.D.T., C.M.T.J., R.G.V.), and the Research Institute of the Cleveland Clinic Foundation, Cleveland (F.C., F.F.-T.). Address reprint requests to Dr. Victor at the Cardiology Division, Department of Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235–9034.
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