(Circulation. 2000;101:553.)
© 2000 American Heart Association, Inc.
Basic Science Reports |
Antihypertensive Effect of 0.1-Hz Blood Pressure Oscillations to the Kidney
From the Institut für Physiologie (B.N., J.S., E.S., H.W.R., P.B.P.) and the Institut für klinische Chemie (N.R., I.S.) der Humboldt Universität Berlin, Berlin, Germany, and the Department of Medical Physiology, University of Copenhagen Panum Institute, Copenhagen, Denmark (M.H.B.).
Correspondence to Dr Benno Nafz, Physiologisches Institut der Charité, Humboldt Universität Berlin, Tucholskystraße 2, 10117 Berlin, Germany. E-mail b.nafz{at}gmx.de
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Background—Physiological blood pressure (BP) fluctuations with frequencies >0.1 Hz can override renal blood flow autoregulation. The influence of such immediate changes in renal perfusion pressure (RPP) on daily BP regulation, eg, via shear stress–stimulated liberation of renal endothelial NO, however, is unknown. Thus, we studied the effects of such RPP oscillations on renal function and on systemic BP during the onset of renal hypertension.
Methods and Results—Seven beagles (randomly assigned to each of the following protocols) were chronically instrumented for the measurement of systemic BP, RPP, and renal excretory function. An inflatable cuff was used to reduce and to oscillate RPP over 24 hours in the freely moving dog. Reducing RPP to 87±2 mm Hg diminished excretion of sodium and water and doubled plasma renin activity (PRA, n=7, P<0.01) but had no significant effect on urinary nitrate excretion (n=6), a marker of NO generation. Superimposing 0.1-Hz oscillations (±10 mm Hg) onto the reduced RPP blunted hypertension, returned fluid excretion almost to control levels, and doubled renal sodium elimination. Nitrate excretion peaked at 8 hours, only to return to control values shortly thereafter. PRA, conversely, was significantly reduced during the last third of the experimental protocols.
Conclusions—BP fluctuations transiently stimulate NO liberation and induce a reduction in PRA, which enhances 24-hour sodium and water excretion and markedly attenuates the acute development of renovascular hypertension.
Key Words: hemodynamics • hypertension • kidney • Fourier analysis • renin
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The average level of arterial blood pressure (BP) is a major determinant of future cardiovascular complications in hypertension.1 In addition, recent investigations show that the dynamic properties of BP are also of significance for the development of hypertension-related end-organ damage in patients.2 3 4 5 Thus, changes in the dynamic properties of BP, which usually coincide with hypertension,4 6 seem to establish an independent risk factor for cardiovascular complications.
Little is known regarding the influence of such short-term changes in BP on kidney function, a crucial control element for long-term BP regulation.7 8 Conversely, the inability of the renal blood flow (RBF) autoregulation to effectively buffer fast BP fluctuations is well recognized.9 10 It seems likely, therefore, that spontaneous BP oscillations (BPOs), which are not effectively buffered by RBF autoregulation, enhance intrarenal shear stress at the level of the vascular wall. Shear stress, in turn, is known to enhance the liberation of vasoactive substances, eg, endothelium-derived NO, along the renal vascular tree in vitro. Hence, one may expect a profound impact of BPOs on medullary blood flow, on renal excretory function,11 12 and on longer-term BP regulation.13 14
There have been several efforts to determine which systems contribute to modulations in BP levels and BPOs.6 15 16 Nonetheless, the effects of BPOs on regulation of systemic BP remain unknown. We therefore investigated the impact of induced BPOs on the onset of renovascular hypertension, especially with regard to excretory function of the kidney, to urinary nitrate excretion (UNO3), and to renal renin release in the conscious, freely moving dog.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The experiments were carried out on 7 adult, chronically instrumented, purebred female beagles. The general status of the body weight–matched dogs (13.2±0.2 kg) was controlled daily (including body temperature and erythrocyte sedimentation rate). Infections were prevented by a catheter-restricted antibiotic-lock technique.17 Daily intake was controlled with respect to food composition and feeding time. At least 5 days before the first experiment, each animal was fed an individually prepared diet containing 91 mL water, 5.5 mmol Na+, and 3.5 mmol K+ per kg body wt. The last feeding was offered for 30 minutes at 10 PM, ie, 10 hours before an experiment was started the next morning. Any leftovers were fed via a gastric tube, if necessary.
During the experiments, the animals moved freely and undisturbed in their 9-m2 kennels. Meanwhile, data recording, control of renal perfusion pressure (RPP), continuous urine sampling, and blood sampling were done via a swivel system from an adjacent room (see Reference 18 for details). For reasons of social well-being, at least 1 more dog (placed in a neighboring kennel) accompanied the dog under investigation in the air-conditioned, sound-protected animal room. A 12-hour dark/light cycle with electronically induced 1/4-hour dawn breaking and dusk falling was used to further standardize environmental conditions.
All experiments and the care of the dogs were supervised by an ethical committee and were approved of and performed in accordance with the German Animal Protection Law.
Surgery
All surgery was performed under aseptic conditions. General
anesthesia was introduced by 8 mg/kg body wt methohexital
IV and maintained under controlled ventilation with 
1% halothane in
combination with a 2:1 mixture of
N2O:O2. Then, 2 catheters
were advanced via the femoral arteries into the abdominal aorta. This
was done in such a way that the tips were placed distally and
proximally to both renal arteries, respectively. An inflatable cuff was
positioned around the aorta, above the origin of the renal arteries and
between the tips of the catheters. Finally, a bladder catheter was
implanted to allow continuous urine collection. All catheters and the
cuff lead were tunnelled subcutaneously to the dog’s neck, where they
were exteriorized. A recovery period of 
3 weeks was allowed between
the surgery and the first experiment.
Protocols and Measurements
BP was measured in the abdominal aorta, above and below the
inflatable cuff, by means of Honeywell micro pressure transducers (type
136PC05G1) and pressure processors (Plugsys bus system, Hugo Sachs
Electronic). Heart rate was derived from the BP signal by a rate meter
(Gould pressure processor). The cuff and the distal catheter were
connected to an electropneumatic pressure control system, a modified
version of a previous device,19 which allowed us to reduce
and to oscillate RPP around a preset level with high precision. After
analog-to-digital conversion (DASH1602, Keithley Instruments), BP and
HR were stored on line on an IBM-compatible PC (sampling rate 20
Hz).
The bladder catheter was used to collect urine continuously into a fraction sampler (1 tube every 20 minutes). Urine flow (UF) was determined by weighing. Blood samples were taken with the proximal arterial catheter into precooled tubes every 4 hours (ie, at 9 AM, 1 PM, 5 PM, 9 PM, 1 AM, and 5 AM) and placed on ice. After centrifugation at 4°C, plasma was separated and stored at -20°C.
All dogs were randomly assigned to the following protocols: protocol 1, Con: A 24-hour time control without external modulations in RPP to determine basal values of BP, HR, UF, sodium excretion (UNaV), potassium excretion (UKV), UNO3, and plasma renin activity (PRA). Protocol 2, P85: During this protocol, BP was elevated by reduction of mean RPP to 85 mm Hg over the 24-hour recording period. All other measurements were performed as during protocol 1. Protocol 3, Osc: To determine the influence of BPOs on renovascular hypertension, RPP was sinusoidally oscillated over 24 hours with a frequency of 0.1 Hz (amplitude, ±10 mm Hg) around the same mean value as used during protocol 2.
Analyses
Sodium and potassium concentrations were determined by flame
photometry (AFM 5052, Eppendorf). A 125I-labeled
radioimmunoassay (Du Pont New England Nuclear) was used to measure PRA.
To determine nitrate,
[15N]KNO3 (Sigma) was
used as internal standard. The nitrate of the samples was converted to
nitrobenzene by shaking for 30 minutes with a precooled (-80°C)
mixture of trifluoromethanesulfonic acid (120 µL) and
benzene (500 µL, both from Sigma). After separation and
neutralization of the benzene layer, 1 µL of the organic phase was
injected into a temperature program–controlled gas
chromatograph (Varian 3400) equipped with an XTI-5 capillary
column (Resteck Corp). Subsequent selective monitoring with a Varian
Saturn mass spectrometer operating in the positive ion/chemical
ionization mode (with methane as reactant gas) allowed the estimation
of the ratio between endogenous nitrate (m/z 124) and the
15N-labeled internal standard (m/z 125). Although
this method is more costly than the commonly used Griess-Ilosvay
reaction, it is very specific, thereby avoiding interference with many
other compounds that contain
NOx.20
Statistics
Mean values of the hemodynamic data were
obtained by beat-to-beat integration; all other data were averaged by
calculation of arithmetic means. The Student-Newman-Keuls test was used
for statistical comparisons. A probability level of <0.05 was taken to
indicate significance. All data are presented as
mean±SEM.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The 24-hour mean values of HR ranged from 81±8 bpm (P85) to 91±7 bpm (Con) without any significant difference between the protocols (Osc: 86±2 bpm). Figure 1
shows original
recordings of RPP (left) and 1-minute mean values of BP (right)
of a single dog. During control, RPP and mean BP showed a remarkable
variability within seconds (A) and hours (D), thereby ranging between
80 and 140 mm Hg. A reduction in RPP did not exert a major
influence on rapid fluctuations, eg, the
physiological pulsations in RPP, whereas slower
changes in RPP were effectively suppressed in our experiments (B). This
intervention elevated BP to 170 mm Hg at the end of the
24-hour recording period (E). The influence of BP fluctuations
was assessed by superimposing 0.1-Hz oscillations onto the
reduced RPP (C). As depicted in F, the pressure
oscillations markedly attenuated the hypertensive effect of
P85. Because the time course of BP (D through F) revealed a wide
variability and major differences between the protocols, 24-hour mean
values were used for overall comparisons. Thus, 24-hour BP was elevated
from 113±3 mm Hg (Con) to 142±5 mm Hg during P85
(P<0.01 versus Con, RPP=87±2 mm Hg, n=7).
Superimposing RPP oscillations (24-hour mean: 85±2
mm Hg, n=7) significantly attenuated this increase in BP. Thus,
24-hour BP increased only by 8 mm Hg, to 121±7 mm Hg
(P<0.01 versus P85, P=NS versus Con).
|
The respective time courses of UF (same dog as in Figure 1
) are shown in Figure 2 (left),
together with group means of 24-hour electrolyte excretion (right). As
indicated, UF varied spontaneously by a factor of 4 during Con (A)
and Osc (C) but declined after some initial fluctuations to low levels
during P85 (B). In contrast to these short-term changes in UF, which
differed remarkably between the dogs, the 24-hour mean fluid excretion
was stably reduced by P85 to nearly 50% of control (288±33 versus
557±49 mL/24 h, P<0.01, n=7). This effect was nearly
abolished during Osc. Thus, UF increased to 484±48 mL/24 h
(P<0.01 versus P85, P=NS versus Con, n=7) during
this protocol. The changes in UF among the 3 protocols were
paralleled by modulations in UNaV and
UKV: P85 induced a fall in
UNaV (open bars) to 20% of control
(P<0.01, n=7, D and E). Osc (F) doubled
UNaV in comparison to P85 (7.9±1.1 versus
3.3±0.8 mmol/24 h, P<0.05, n=7) but failed to
reestablish normal sodium excretion (P<0.01 versus Con:
17.3±2.1 mmol/24 h). Renal K+ handling was not
so strongly affected by P85 (Con, 22.7±1.4 mmol/24 h; P85,
15.1±2.4 mmol/24 h; P<0.05, n=7) and returned to
normal during Osc (23.4±2.6 mmol/24 h, P=NS versus control,
P<0.05 versus P85, n=7).
|
In contrast to BP and fluid and electrolyte excretion, the 8-hour mean
values of UNO3 (Figure 3, A through C) showed a marked transient
increase during Osc (shaded bars). Thus, after a maximum at the first 8
hours of the recording (A), NO3 declined
quickly to control levels (B and C), indicating that NO liberation is
not directly responsible for the prolonged changes in BP and renal
fluid and electrolyte excretion. No significant differences were
observed between Con and P85 (Figure 3, open bars versus solid
bars). Osc reduced 24-hour mean values of PRA by 30% in comparison
with P85 (5.0±0.6 versus 7.5±0.9 ng angiotensin I
· mL-1 · min-1,
P<0.05, P=NS versus Con, n=7), suggesting an
important role of the renin system in the observed antihypertensive
effect. Interestingly, however, the differences in PRA among the
protocols increased slowly (D through F). Thus, no significant increase
in PRA was detected within the first 8 hours of the experiments (D),
and the difference between P85 and Osc gained significance only during
the last 8 hours of the recordings (F). No direct coupling
between the time course of NO3 or PRA and
electrolyte excretion, UF, or BP was observed.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
A vast number of studies over recent years have focused on the description of rapid BP changes and the possibility of using spectral analysis of BP as a tool for quantifying sympathetic and vagal tone.21 22 The importance of BPOs as an individual parameter in BP control, however, remains to be established. The major finding of the present study is that oscillations in RPP alleviate the onset of renal hypertension in the freely moving dog. This antihypertensive effect is probably mediated by the combined action of the following mechanisms: a marked increase in renal fluid and electrolyte excretion, as perhaps achieved by the observed transient increase in NO liberation, and the prevailing attenuation of pressure-dependent renin release.
Hypertension is a major cardiovascular risk factor, thus being in part responsible for the principal cause of death in the industrialized nations.23 It was recognized early, however, that hypertension is commonly accompanied by changes in the dynamic properties of BP.24 Indeed, it seems likely that BPO itself may be intertwined with the regulation of BP. For instance, surgical or pharmacological interruption of the baroreceptor reflex, or the NO system, elevates 24-hour BP and also enhances short-term BPOs in the conscious animal.14 25 26 Conversely, a possible interaction of BPOs with longer-term BP regulation is suggested by the results of 24-hour ambulatory BP recordings, which have shown that enhanced SD of BP coincides with renal end-organ damage in hypertensive subjects.4
Thus, it is conceivable that the kidney does not merely constitute an important control element in the BP regulation network but may also be a target organ for BPOs. The established concepts of BP regulation offer several entry points by which BPOs may interact with longer-term BP.
According to the renal/body-fluid–pressure-control concept, fluid and
electrolyte excretion is crucial for long-term BP regulation (see
Reference 88 for review). In line with this hypothesis, several
investigators reported that an impaired capability of the kidney to
form adequate amounts of urine induces hypertension.7 8 27
Conversely, BP modulates renal fluid and sodium handling, which has
been reported to be closely dependent on renal medullary
hemodynamics.11 Hence, a BP-dependent
increase in medullary blood flow may induce a more or less pronounced
washout of the osmotic gradient within the renal medulla and thereby
attenuates the ability of the kidney to form concentrated
urine.11 12 Therefore, it seems likely that BP-induced
changes in renal hemodynamics can modulate longer-term
BP via a change in renal fluid and sodium excretion. In our
experiments, we used sinusoidal 0.1-Hz RPP oscillations in
the conscious dog to investigate this pathway. Such BPOs are not
effectively buffered by the autoregulation of RBF9 and may
therefore impinge on renal excretory function. Indeed, the induced BPOs
led to an increase in fluid and electrolyte excretion (Figure 2).
It is widely accepted that BPOs can also modulate shear stress at the
vascular wall. Endothelial shear stress stimulates NO
release from arteries, thereby inducing vasodilation and changes in
intrarenal hemodynamics.28 29 Hence, it is
not surprising that recent studies suggest a close coupling between
renal NO liberation and hypertension.14 Unfortunately, the
direct assessment of renal NO liberation is still impossible in the
freely moving animal. Thus, we determined UNO3 as
a measure for NO. To obtain the highest possible accuracy, we performed
all experiments during the postreabsorptive state when influences of
food composition on UNO3 are minimized. In
addition, a very specific mass spectrometric analysis, instead
of the Griess-Ilosvay reaction, was used. This avoids possible
interferences with most physiological
NOx compounds.20 Nonetheless, the
stimulation in NO liberation was detectable only during the first 8
hours of the experiments. Thus, the prolonged antihypertensive effect
of BPOs during renovascular hypertension (Figure 1) cannot be
explained by a direct effect of the enhanced NO release.
The activity of the renin-angiotensin system was lower
during Osc than during P85 (Figure 3). In light of the
well-established stimulus-response curve of pressure-dependent renin
release, an attenuated renin release is a surprise. Under short-term
steady-state conditions (stepwise pressure reduction), a pronounced
influence of RPP on renin release has been detected only below
90 mm Hg.30 Thus, the minima of the RPP
oscillations should lead to a pressure-dependent
stimulation in renin release, whereas maxima in RPP should not reduce
renin release to the same degree. Therefore, if one assumes that
possible hysteresis effects can be neglected, one would expect higher
PRA during Osc than during P85. In addition, the 24-hour mean value of
RPP was slightly but not significantly lower during Osc than during P85
(85±2 versus 87±2 mm Hg), which may also have contributed to an
elevated PRA. Thus, the influence of BPOs on a reduction in renin
release is probably underestimated in our experiments. Obviously, the
BPOs used exert a major influence on renin release in the freely moving
dog. The renin-angiotensin system interacts with BP
regulation via the direct vasoconstrictory effects of
angiotensin II and via the influence on renal fluid and
sodium handling. This suggests that the sustained antihypertensive
effect of Osc on renovascular hypertension is mediated mainly by
lowered PRA. In contrast to the prolonged effect on PRA, the
stimulation of NO generation seems to be important only during the
first 8 hours of our experiments.
It must be kept in mind, however, that further influences of BPOs on the intrarenal microcirculation may participate in the observed antihypertensive effect: BPO-induced changes in local blood flow probably modulate physical forces along the nephron. Likewise, it is plausible that BPOs interfere with the local release of many vasoactive substances (eg, prostaglandins and kinins), thereby changing local hemodynamics and kidney function.
With respect to the wide spectrum of spontaneous BP fluctuations that have been observed in hypertensive subjects, it is emphasized that our approach covers only a specific BPO and therefore cannot simply be extended to other BPOs that have also been observed during hypertension.
Nonetheless, the data demonstrate the importance of BP dynamics for
kidney function and provide evidence that the investigated BPOs can
attenuate RPP (P85)-induced changes in PRA, volume, and electrolyte
homeostasis and thereby alleviate renal hypertension in our
experiments. Interestingly, 0.1-Hz oscillations in
muscle sympathetic nerve activity and RR interval have been reported to
be markedly attenuated during heart failure and blunted during severe
heart failure in humans.31 Given that the patterns of
muscle sympathetic nerve activity and RR interval are mirrored by
corresponding BPOs, one may hypothesize that BPOs facilitate excretion
of fluid and electrolytes and reduce PRA, thereby improving the
prognosis of these patients.
Conclusions
Using a new approach to chronically oscillate RPP around a reduced
RPP in conscious dogs, we demonstrate that BP changes in the range of
several seconds enhance daily sodium and fluid excretion and attenuate
the BP elevation during the onset of renal hypertension. The RPP
oscillations also induce a transient increase in NO
liberation and lead to a sustained reduction in renin activity, which
have been shown to be major factors in long-term BP control. These
results may be a first step in understanding the importance of
short-term BP fluctuations for the development of hypertension.
|
Acknowledgments |
|---|
We thank K. Dannenberg, D. Bayerl, A. Gerhardt, and S. Molling for technical assistance and the employees of the Forschungseinrichtung Experimentelle Medizin for perfect animal caretaking.
Received May 30, 1999; revision received July 18, 1999; accepted August 11, 1999.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
-
Sytkowski PA, Kannel WB, D’Agostino RB. Changes
in risk factors and the decline in mortality from
cardiovascular disease: the Framingham Heart Study.
N Engl J Med. 1990;23:1635–1641.
-
Frattola A, Parati G, Cuspidi C, Albini F, Mancia G.
Prognostic value of 24-hour blood pressure variability. J
Hypertens. 1993;11:1133–1137.[Medline]
[Order article via Infotrieve]
-
Mancia G, Frattola A, Parati G, Santucciu C, Ulian L.
Blood pressure variability and end organ damage. J
Cardiovasc Pharmacol. 1994;24:S6–S11.
-
Mancia G, Ulian L, Santucciu C, Parati G. Ambulatory
blood pressure in hypertension with particular reference to the kidney.
J Nephrol. 1997;10:198–202.[Medline]
[Order article via Infotrieve]
-
Parati G, Ulian L, Santucciu C, Tortorici E, Villani
A, Di Rienzo M, Mancia G. Clinical value of blood pressure variability.
Blood Press Suppl. 1997;2:91–96.[Medline]
[Order article via Infotrieve]
-
Holstein-Rathlou NH, He J, Wagner AJ, Marsh DJ.
Patterns of blood pressure variability in normotensive and hypertensive
rats. Am J Physiol. 1995;269:R1230–R1239.
[Abstract/Free Full Text]
-
Guyton AC. Blood pressure control: special role of the
kidney and body fluids. Science. 1991;252:1813–1816.
[Abstract/Free Full Text]
-
Cowley AW Jr. Long-term control of
arterial blood pressure. Physiol Rev. 1992;72:231–300.
[Abstract/Free Full Text]
-
Wittmann U, Nafz B, Ehmke H, Kirchheim HR, Persson PB.
Frequency domain of renal autoregulation in the conscious dog.
Am J Physiol. 1995;269:F317–F322.
[Abstract/Free Full Text]
-
Holstein-Rathlou NH, Marsh DJ. Renal blood flow
regulation and arterial pressure fluctuations: a case study
in nonlinear dynamics. Physiol Rev. 1994;74:637–681.
[Abstract/Free Full Text]
-
Cowley AW Jr, Mattson DL, Lu S, Roman RJ. The renal
medulla and hypertension. Hypertension. 1995;25:663–673.
[Abstract/Free Full Text]
-
Franchini KG, Mattson DL, Cowley AW Jr. Vasopressin
modulation of medullary blood flow and pressure
natriuresis-diuresis in the decerebrated rat. Am J
Physiol. 1997;272:R1472–R1479.
[Abstract/Free Full Text]
-
Schricker K, Potzl B, Hamann M, Kurtz A. Coordinate
changes of renin and brain-type nitric-oxide-synthase (bNOS) mRNA
levels in rat kidneys. Pflugers Arch. 1996;432:394–400.[Medline]
[Order article via Infotrieve]
-
Mattson DL, Maeda CY, Bachman TD, Cowley AW Jr.
Inducible nitric oxide synthase and blood pressure.
Hypertension. 1998;31:15–20.
[Abstract/Free Full Text]
-
Fornage M, Amos CI, Kardia S, Sing CF, Turner ST,
Boerwinkle E. Variation in the region of the
angiotensin-converting enzyme gene influences
interindividual differences in blood pressure levels in young white
males. Circulation. 1998;97:1773–1779.
[Abstract/Free Full Text]
-
Letienne R, Barres C, Cerutti C, Julien C. Short-term
haemodynamic variability in the conscious areflexic rat. J
Physiol (Lond). 1998;506:263–274.
[Abstract/Free Full Text]
-
Palm Ü, Boemke W, Bayerl D, Schnoy N, Juhr NC,
Reinhardt HW. Prevention of catheter-related infections by a new,
catheter-restricted antibiotic filling technique. Lab Anim. 1991;25:142–152.
[Abstract/Free Full Text]
-
Reinhardt HW, Palm Ü, Mohnhaupt R, Dannenberg K,
Boemke W. Computer-assisted long-term measurements of urinary output
and other biological data. Am J Physiol. 1990;258:R274–R280.
[Abstract/Free Full Text]
-
Nafz B, Persson PB, Ehmke H, Kirchheim HR. A servo
control system for open- and closed-loop blood pressure regulation.
Am J Physiol. 1992;262:F320–F325.
[Abstract/Free Full Text]
-
Tracey WR, Linden J, Peach MJ, Johns RA. Comparison of
spectrophotometric and biological assays for nitric oxide (NO) and
endothelium-derived relaxing factor (EDRF):
nonspecificity of the diazotization reaction for NO and failure to
detect EDRF. J Pharmacol Exp Ther. 1990;252:922–928.
[Abstract/Free Full Text]
-
Eckberg DL. Sympathovagal balance: a critical
appraisal. Circulation. 1997;96:3224–3232.
[Free Full Text]
-
Persson PB. Spectrum analysis of
cardiovascular time series. Am J
Physiol. 1997;273:R1201–R1210.
[Abstract/Free Full Text]
-
Whelton PK. Epidemiology of
hypertension. Lancet. 1994;344:101–106.[Medline]
[Order article via Infotrieve]
-
Pickering TG. Strategies for the evaluation and
treatment of hypertension and some implications of blood pressure
variability. Circulation. 1987;76(suppl I):I-77–I-82.
-
Nafz B, Wagner CD, Persson PB. Endogenous
nitric oxide buffers blood pressure variability between 0.2 and 0.6 Hz
in the conscious rat. Am J Physiol. 1997;272:H632–H637.
[Abstract/Free Full Text]
-
Just A, Wittmann U, Nafz B, Wagner CD, Ehmke H,
Kirchheim HR, Persson PB. The blood pressure buffering capacity of
nitric oxide by comparison to the baroreceptor reflex. Am J
Physiol. 1994;267:H521–H527.
[Abstract/Free Full Text]
-
DiBona GF, Kopp UC. Neural control of renal function.
Physiol Rev. 1997;77:75–197.
[Abstract/Free Full Text]
-
Rubanyi GM, Romero JC, Vanhoutte PM. Flow-induced
release of endothelium-derived relaxing factor.
Am J Physiol. 1986;250:H1145–H1149.
[Abstract/Free Full Text]
-
Lamontagne D, Pohl U, Busse R. Mechanical deformation
of vessel wall and shear stress determine the basal release of
endothelium-derived relaxing factor in the intact
rabbit coronary vascular bed. Circ Res. 1992;70:123–130.
[Abstract/Free Full Text]
-
Gross R, Kirchheim HR, Ruffmann K. Effect of carotid
occlusion and of perfusion pressure on renal function in conscious
dogs. Circ Res. 1981;48:777–784.
[Abstract/Free Full Text]
-
van de Borne P, Montano N, Pagani M, Oren R, Somers VK.
Absence of low-frequency variability of sympathetic nerve activity in
severe heart failure. Circulation. 1997;95:1449–1454.
[Abstract/Free Full Text]
This article has been cited by other articles:
 |
|
 |
|
  C. Julien The enigma of Mayer waves: Facts and models Cardiovasc Res, April 1, 2006; 70(1): 12 - 21. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. A. Lanfranchi and V. K Somers Arterial baroreflex function and cardiovascular variability: interactions and implications Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2002; 283(4): R815 - R826. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. FLEMMING, N. ARENZ, E. SEELIGER, T. WRONSKI, K. STEER, and P. B. PERSSON Time-Dependent Autoregulation of Renal Blood Flow in Conscious Rats J. Am. Soc. Nephrol., November 1, 2001; 12(11): 2253 - 2262. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L.S. Pires, C. Barres, J. Sassard, and C. Julien Renal Blood Flow Dynamics and Arterial Pressure Lability in the Conscious Rat Hypertension, July 1, 2001; 38(1): 147 - 152. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. NAFZ and P. B. PERSSON Renal Arterial Pressure Variability: A Role in Blood Pressure Control? Ann. N.Y. Acad. Sci., June 1, 2001; 940(1): 407 - 415. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Butkevich, R. A. Phillips, B. Nafz, J. Stegemann, E. Seeliger, H. W. Reinhardt, P. B. Persson, M. H. Bestle, N. Richter, and I. Schimke Blood Pressure Oscillations: Is There an Independent Antihypertensive Effect? Response Circulation, January 30, 2001; 103 (4): e21 - e21. [Full Text] [PDF]
|
|
|
|
 |
|
 H. M. Stauss and P. B. Persson Role of Nitric Oxide in Buffering Short-Term Blood Pressure Fluctuations Physiology, October 1, 2000; 15(5): 229 - 233. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. J. A. Janssen, E. V. Lukoshkova, and G. A. Head Sympathetic modulation of renal blood flow by rilmenidine and captopril: central vs. peripheral effects Am J Physiol Renal Physiol, January 1, 2002; 282(1): F113 - F123. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||