Download Physiological Mechanisms for Calcium-Induced

213
Physiological Mechanisms for
Calcium-Induced Changes in Systemic
Arterial Pressure in Stable Dialysis Patients
Susan K. Fellner, Roberto M. Lang, Alex Neumann, Kirk T. Spencer,
David A. Bushinsky, and Kenneth M. Borow
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
The mechanisms by which variations in blood ionized calcium (Ca2+) influence systemic arterial
pressures independent of changes in extracellular fluid volume, pH, and electrolytes are
unknown. To study this issue, we dialyzed eight stable hemodialysis patients on three separate
occasions during 1 week with dialysates differing only in calcium concentration. Ultrafiltration
was adjusted to achieve the patient's estimated dry weight. Postdialysis Ca2+ was measured, as
were arterial blood gases, electrolytes, magnesium, blood urea nitrogen, creatinine, and
hematocrit. Blood pressures and two-dimensional, targeted M-mode echocardiograms were
recorded with the patient in the supine position after 15 minutes of rest. Postdialysis, three
different levels of Ca2+ were achieved. Other measured biochemical variables and body weight
did not differ among the three study periods. Changes in Ca2+ correlated directly with changes
in systolic, diastolk, and mean blood pressures, left ventricular stroke volume, and cardiac
output. In contrast, heart rate, left ventricular end-diastolic dimension, and total systemic
vascular resistance were not altered significantly by changes in Ca 2+ . Thus, alterations in Ca2+
within the physiological range affect systemic blood pressure primarily through changes in left
ventricular output rather than in peripheral vascular tone in stable dialysis patients. {Hypertension 1989;13:213-218)
S
ystemic arterial pressure is determined by the
interaction between blood flow and resistance within the arterial tree. Changes in
serum calcium concentration can theoretically alter
either one or both of these hemodynamic variables.
Prior clinical studies have suggested that hypercalcemia can cause a rise'-7 or no change89 in systemic
arterial pressure, whereas hypocalcemia is reported
to reduce blood pressure.10-12 Studies in patients
undergoing hemodialysis have suggested that raising dialysate calcium concentration diminishes the
typical fall in blood pressure that occurs during
ultrafiltration and hemodialysis.1314 However, the
major methodological problem encountered in these
prior investigations has been the difficulty in varying arterial blood ionized calcium (Ca2+) within the
physiological range in a stable and reproducible
manner. Furthermore, interpretation of these results
has been hampered by simultaneous changes in pH,
plasma volume, and other electrolytes that may
obscure the unique actions of calcium on the cardiovascular system.
In the present study, systemic arterial blood
pressures were measured in unanesthetized, stable
hemodialysis patients immediately after dialysis on
three separate occasions; dialysates differed only in
calcium concentration. In this manner, the hemodynamic effects due to changes in Ca2+ could be
separated from those due to alterations in plasma
volume, pH, magnesium, potassium, hematocrit,
urea, and other nitrogenous compounds.
Patients and Methods
From the sections of Nephrology (S.K.F., D.A.B.) and Cardiology (R.M.L., A.N., K.T.S., K.M.B.), Department of Medicine, University of Chicago, Chicago, Illinois.
Supported in part by Grant AA-06677 from the National
Institutes of Health and by a grant-in-aid from the American
Heart Association, Chicago affiliate.
Address for reprints: Susan K. Fellner, MD, Section of
Nephrology, Box 28, University of Chicago, 5841 South Maryland Avenue, Chicago, IL 60637.
Received April 28, 1988; accepted October 14, 1988.
The study population consisted of eight patients
(four women and four men; mean age, 45±5 years;
range 32-80 years) with stable chronic renal failure
who had been undergoing regular hemodialysis for
34±18 months (range 5-135 months). The cause of
renal failure was focal glomerulosclerosis in two
patients; nephrosclerosis in two patients; and diabetic nephropathy, lupus erythematosus, ureteral
obstruction, and unknown etiology in one patient
214
Hypertension
Vol 13, No 3, March 1989
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
each. None of the study patients had a clinical
history suggestive of ischemic heart disease, chronic
congestive heart failure, or abnormal cardiac rhythm,
nor were left ventricular regional wall motion abnormalities detected by two-dimensional echocardiographic imaging. None of the patients was receiving
antihypertensive medications, nitrates, /3-blockers,
digitalis, or calcitriol. Written informed consent
was obtained in accordance with a protocol approved
by the Clinical Investigation Committee of the University of Chicago Medical Center.
Each patient underwent hemodialysis three times
within a single week with dialysate containing 0.5
mmol/1 (low), 1.75 mmol/1 (medium), or 2.5 mmol/1
(high) calcium chosen in random order. The other
constituents of the dialysate were otherwise identical (mmol/1): sodium 140, potassium 2.5, magnesium
0.75, chloride 111.5, acetate 36, and glucose 138.7.
Dialysis was performed with a Travenol hollow fiber
cuprophane dialyzer (Baxter Travenol Laboratories,
Deerfield, Illinois) for 3.5 to 4 hours on a Gambro
AK 10 machine (Gambro Lundia, Lund, Sweden)
with ultrafiltration adjusted to achieve the patient's
estimated dry weight. The study was blinded, and
only the dialysis technician knew the calcium concentration of the dialysate.
Immediately on completion of each hemodialytic
procedure, blood was obtained from the arterial
dialysis needle for determination of Ca2+, arterial
blood gases, total calcium, electrolytes, creatinine,
blood urea nitrogen (BUN), magnesium, and hematocrit. Ca2+ concentration was measured with an
ion-specific electrode (Nova II, Nova Biomedical
Company, Newton, Massachusetts). Midmolecule
portion of parathyroid hormone was measured with
a radioimmunoassay kit (Incstar, Stillwater, Minnesota) before the institution of the study. All other
blood measurements were made by the blood chemistry laboratory or the pulmonary function laboratory of the University of Chicago Medical Center.
After removal of the dialysis needles, patients
were weighed. They then rested in a recumbent
position for 15 minutes, at which point systolic,
diastolic, and mean blood pressures were measured
in the upper arm by the oscillometric method
(Dinamap 1846 SXP vital signs monitor, Critikon,
Tampa, Florida). The oscillometric method has
been shown previously to give reproducible measurements of systemic arterial pressures independent of cardiac index, systemic vascular resistance,
left ventricular ejection fraction, and body surface
area. 1516 A minimum of 10 blood pressure readings
were recorded during the next 15 to 45 minutes.
Cardiac ultrasound imaging (Hewlett-Packard,
Andover, Massachusetts) was performed with either
a 3.5 or a 5 MHz transducer with the ultrasound
beam directed just off the tip of the anterior leaflet
of the mitral valve. Simultaneous two-dimensional
as well as targeted M-mode echocardiograms of the
left ventricle were recorded in conjunction with
phonocardiograms, electrocardiograms, and sys-
tolic, diastolic, and mean blood pressure measurements. All tracings were obtained at end-expiration.
Left ventricular end-systolic and end-diastolic dimensions were measured from the targeted M-mode
echocardiographic recordings as described previously.1718 Left ventricular end-systolic and enddiastolic volumes were estimated from echocardiographic dimensions by the method of Teichholz et
al.18 This assumes that the visualized portion of the
left ventricle is representative of global left ventricular performance, an assumption shown to be valid
in normally shaped hearts in the absence of left
ventricular asynergy. Cardiac output was calculated as left ventricular stroke volume times heart
rate.19 Total systemic resistance was calculated as
the Dinamap-determined mean arterial pressure
divided by the echocardiographically measured cardiac output, multiplied by 80 to convert to
dynes • sec • cm"3.20 After completion of these measurements, six of the eight study subjects underwent further investigation to determine the effect of
Ca2+ on myocardial contractility. These data are
reported elsewhere.21
Statistical Considerations
Comparisons of the postdialysis hemodynamic
and biochemical data obtained with the low, medium,
and high calcium bath were performed by repeatedmeasures analysis of variance. Isolated differences
between treatment groups were identified with the
Bonferroni / test. A p value of <0.05 was considered to be statistically significant.
Results
Biochemical Changes
When patients were dialyzed with baths differing
only in calcium concentration, three significantly
different levels of Ca2+ were achieved (Table 1).
Arterial Ca2+ concentration was 1.04±0.04 mmol/1
after dialysis with 0.5 mmol/1 (low) calcium bath,
1.40±0.03 mmol/1 after 1.75 mmol/1 (medium) calcium bath, and 1.68±0.08 mmol/1 after 2.5 mmol/1
(high) calcium bath (Table 1). In six of eight patients,
Ca was measured again approximately 2 hours
after completion of each of the dialysis runs; there
were no significant differences between the values
obtained immediately after dialysis and those measured 2 hours later.21 Arterial blood gases, electrolytes, creatinine, BUN, magnesium, and hematocrit, as well as body weight and heart rate did not
differ among the three studies in each patient.
Parathyroid hormone levels were markedly elevated in all but one patient (10.9±3.2 ng/ml, range
1.1-27.5 ng/ml; normal, <1.2 ng/ml).
Hemodynamic Changes
Table 2 summarizes the hemodynamic data
obtained at each level of Ca2+. Heart rate did not
differ among the studies. Systolic and diastolic
blood pressures increased with higher levels of Ca2+
(Figure 1). The correlation coefficients for systolic
Feliner et al
Calcium and Systemic Arterial Pressure
215
TABLE 1. Summary of Biochemical Measurements and Weights
Variables
Low (0.5)
Dialysate calcium (mmol/1)
Medium (1.75)
High (2.5)
Blood
Ca 2+ (mmol/1)
Calcium (mmol/1)
Sodium (mmol/1)
Potassium (mmol/1)
Chloride (mmol/1)
Bicarbonate (mmol/1)
Creatinine (/imol/1)
Blood urea nitrogen (mmol/1 urea)
Magnesium (mmol/1)
Hematocrit (%)
PH
P02 (mm Hg)
Postdialysis weight (kg)
1.04+0.04
8.1±0.6
136±1
4.0±0.2
100±l
27±2
699±177
12.7±1.8
1.16+0.05
27+2
7.44±0.02
%±5
67±7
1.40±0.03*
10.4±0.5*
134±1
3.8+0.2
99±1
26±2
690±177
11.8+1.8
1.18±0.07
29+2
7.44±0.02
92±5
66±7
1.68±0.08*t
11.9±0.8*t
135+1
4.1±0.2
100±l
27±2
684±177
12.1 + 1.8
1.20±0.09
28±2
7.43±0.02
94±7
66±7
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
Values are mean±SEM.
*p<0.01 vs. low dialysis calcium.
tp<0.01 vs. medium dialysis calcium.
and diastolic pressures versus Ca2+ were 0.74
(p<0.001) and 0.46 (p<0.02), respectively. The
relation between Ca2+ and systolic and diastolic
pressures in individual study subjects is depicted in
Figure 2. Higher levels of Ca2+ resulted in augmented left ventricular stroke volume and cardiac
output (Table 2). In contrast, total vascular resistance (a measure of peripheral arteriolar tone) and
left ventricular end-diastolic dimension (a commonly
used measure of ventricular preload) did not change
at the higher levels of Ca2+ (Table 2).
Discussion
We have shown that changes in systemic arterial
pressure that occur with variations in Ca2+ are
largely a function of alterations in left ventricular
output rather than peripheral arteriolar tone in
stable dialysis patients. Evidence for a role of Ca2+
in the modulation of systemic arterial pressure in
humans and experimental animals has been examined by a number of previous investigators.1-710-14
However, our model is the first performed in conscious human subjects that permits assessment of
the effects of variations in Ca2+ within the physiological range on systemic arterial blood pressure at
a time that concomitant changes in blood volume,
urine output, electrolytes, magnesium, pH, BUN or
other nitrogenous molecules, and osmolality are
eliminated as confounding variables. This was
achieved by dialyzing stable hemodialysis patients
three times within the same week with dialysate
differing only in calcium concentration and by adjusting ultrafiltration to achieve the same target weight
with each treatment.
The specific hemodynamic mechanisms by which
changes in Ca2+ alter systemic arterial pressure have
TABLE 2. Summary of Hemodynamic Data Obtained at Three Levels of BkMd Ionized Caldnm
Dialysate calcium (mmol/1)
Variables
Ca2+ (mmol/1)
Heart rate (beats/min)
Systolic blood pressure (mm Hg)
Diastolic blood pressure (mm Hg)
Mean arterial pressure (mm Hg)
End-diastolic dimension (cm)
End-systolic dimension (cm)
Stroke volume (ml/beat)
Cardiac output (1/min)
Systemic vascular resistance
(dynes • sec • cm"3)
Values are mean+SEM.
*p<0.05 vs. low dialysis calcium.
tp<0.05 vs. medium dialysis calcium.
Low (0.5)
1.04±0.04
81±4
113±6
72±5
86±5
4.52+0.19
3.29±0.22
49±5
3.9+0.3
1814±147
Medium (1.75)
High (2.5)
1.40±0.03*
81±5
132+4*
80±4*
97±4*
4.50±0.16
3.09±0.21*
54±5*
4.3+0.4*
1892±153
1.68±0.08*t
79+4
146±5*t
89±5*t
108±4*t
4.53±0.15
2.96±0.22*t
62'±5*t
4.9+0.4*t
1870±185
216
Hypertension
Vol 13, No 3, March 1989
tuu •
o SYSTOUC
• DIASTOUC
o
I
150
E
E
a:
in
100
o
o
o
50
O
°°JA—•""
o 8 ^^~x.
""""^ o
——•
0
0.5
1
1
1
2.5
1.0
1.5
2.0
BLOOD IONIZED CALCIUM ( mmol / L )
FIGURE 1. Relation between systolic and diastolic blood
pressures and blood ionized calcium (Ca2*). r=0.74,
p<0.001 for systolic blood pressure vs. Ca2+; r=0.46,
p<0.02 for diastolic blood pressure vs. Ca2*.
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
been controversial. Depending on the experimental
model employed, previous investigators have found
a reduction,9-22 no change,6 or an increase 1 - 3723 in
systemic vascular resistance with hypercalcemia.
However, interpretation of many of these studies
has been difficult because Ca2+ was not measured,
pharmacological rather than physiological doses of
calcium were used, or various anesthetic agents
altered cardiovascular hemodynamics. In addition,
hypercalcemia causes an immediate diuresis and
natriuresis24-26 that leads to a reduction of plasma
volume, a decrease in venous return to the heart,
and subsequently, an adrenergically mediated rise
in systemic vascular resistance. These renalinduced alterations were not an issue in the current
study because all patients were functionally
anephric.
The rise in systemic arterial pressures noted with
increasing Ca2+ in our patients was due to increases
in left ventricular stroke volume (A=10%, low vs.
medium; A=27%, low vs. high) without associated
changes in heart rate, ventricular preload (as measured by end-diastolic dimension), or total vascular
resistance. However, the expected response to an
isolated increase in left ventricular output is arterial
baroreceptor stimulation, possibly accompanied by
activation of the smooth muscle stress-relaxation
phenomenon leading to peripheral vasodilation and
a fall in vascular resistance.2728 The fact that our
patients did not respond in this way may be
explained by several factors. First, raising Ca2+
could have resulted in peripheral vasoconstriction,
which masked the normal vasodilator response.
This would be in accordance with the previously
reported smooth muscle constrictor effect of hypercalcemia seen in isolated myofibrils2930 and rat
femoral arteries.31 Second is the possibility that our
patients with chronic renal failure had abnormalities
in arterial baroreceptor function (affector limb) or
autonomic nervous system dysfunction (effector
limb).3233 The presence of either of these abnormalities would lead to the conclusion that increases in
Ca2+ had little direct effect on vascular smooth
O = SYSTOLIC
•
= DIASTOLIC
too
E
B
LU
OJ
1.0
1J
tO
2J
OJ
1.0
U
10
13
OJ
1.0
1.5
10
IS
OJ
1.0
U
10
IS
OJ
1.0
U
10
13
OJ
IX
U
10
2J
OJ
1.0
U
10
2J
OJ
1J)
1J
10
13
(0
111
oc
Q.
Q
o
o
BLOOD IONIZED CALCIUM (mmol/L)
FIGURE 2. Relation between systolic and diastolic blood pressures and blood ionized calcium (Ca*+) in each of eight patients.
Fellner et al
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
muscle tone. Finally, it is possible that the peripheral vasculature in our patients was intrinsically
abnormal and thus unable to undergo vasodilation
in response to increased pressure and flow. Since
total vascular resistance was at most only mildly
elevated in our study population, and since we have
previously shown that peripheral vasodilation can
be easily obtained with nitroprusside in these
patients,21 this explanation seems unlikely.
Several methodological issues should be addressed
regarding the current study. First, serum catecholamines were not measured. However, Marone et al2
have previously shown that raising serum calcium
does not change norepinephrine levels, although
small increases in epinephrine do occur that nonetheless remain within the normal range. Whether
the changes in Ca2+ in the current study influenced
the release or action of other vasoactive hormones
or autocoids is unknown. Second, parathyroid hormone was substantially elevated in all but one of
our patients. Although infusion of parathyroid hormone in experimental animals has been shown to
produce vasodilation,34 it is unlikely that the relatively small variations in parathyroid hormone that
might occur in response to changes in Ca2+ during
hemodialysis in patients with pre-existing secondary hyperparathyroidism (and parathyroid levels 10
times normal) could account for the magnitude of
the changes in blood pressure observed in this
study. Finally, use of total systemic resistance
neglects the contribution of mean right atrial pressure to the resistance calculation. Since each patient
was ultrafiltered to his or her estimated dry body
weight with each dialysis, it was assumed that no
significant interstudy differences in ventricular and
atrial filling characteristics occurred. This was corroborated by the consistent measurements obtained
for left ventricular end-diastolic dimension.
In summary, our findings demonstrate that the
changes in blood pressure associated with controlled alterations in Ca2+ concentrations occur primarily from preload-independent variations in aortic blood flow rather than from changes in peripheral
arteriolar tone in dialysis patients. This is particularly interesting when considering recent work from
our institution21 that was performed with use of
load-independent indexes of left ventricular contractility, which confirmed the hypothesis that myocardial contractility in humans varies directly with
Ca2+. Thus, changes in systemic arterial pressures
that occur with variations in Ca2+ within the physiological range are largely the consequence of alterations in left ventricular output in these patients.
Acknowledgments
We gratefully acknowledge the expert assistance
of Christina M. Foster and Glenn Hallam.
References
1. Mori K: The effects of infusion of calcium and magnesium on
the cardiovascular system in man. Jpn Heart J 1978;
19:226-235
Calcium and Systemic Arterial Pressure
217
2. Marone C, Beretta-Piccoli C, Weidmann P: Acute hypercalcemic hypertension in man: Role of hemodynamics, catecholamines, and renin. Kidney Int 1980,20:92-96
3. Drop LJ, Scheidegger D: Plasma ionized calcium concentration: Important determinant of the hemodynamic response
to calcium infusion. J Thorac Cardiovasc Surg 1980;
79:425-431
4. Sica DA, Harford AM, Zawada ET: Hypercalcemic hypertension in hemodialysis. Clin Nephrol 1984;22:102-104
5. Weidmann P, Massry SG, Cobum JW, Maxwell MH, Atelson
J, Kleeman CR: Blood pressure effects of acute hypercalcemia:
Studies in patients with chronic renal failure. Ann Intern
Med 1972;76:741-745
6. Eriksen C, Sorensen B, Bflle-Brahe NE, Lunding M: Haemodynamic effects of calcium chloride administered intravenously
to patients with and without cardiac disease during neurolept
anaesthesia. Ada Anaesthesiol Scand 1983^7:13-17
7. Berl T, Levi M, Ellis M, Chaimovitz C: Mechanism of acute
hypercalcemic hypertension in conscious rat. Hypertension
1985;7:923-930
8. Kramer W, Wizemann V, Thormann J, Bechtold A, Schutterll G, Lasch HG: Mechanism of altered myocardial contractility during hemodialysis: Importance of changes in the
ionized calcium to plasma potassium ratio. Klin Wochenschr
1985;63:272-278
9. Delinger JK, Kaplan JA, Lecky JH, Wollman H: Cardiovascular responses to calcium administered intravenously to man
during halothane anesthesia. AnesthesMogy 1975;42:390-397
10. Llach F, Weidmann P, Reinhart R, Maxwell MH, Cobum
JW, Massry SG: Effect of acute and long standing hypocalcemia on blood pressure and plasma renin activity in man. J
Clin Endocrinol Metab 1974;38:841-847
11. Haddy FJ, Scott JB, Emerson TE, Overbeck HW, Daugherty RM Jn Effects of generalized changes in plasma electrolyte concentration and osmolality on blood pressure in the
anesthetized dog. Ore Res 1969; 14:1-59-1-74.
12. Shackney J, Hasson J: Precipitous fall in serum calcium,
hypotension and acute renal failure after intravenous phosphate therapy for hypercalcemia. Ann Intern Med 1967;
66:906-916
13. Maynard JC, Cruz C, Kleerekoper M, Levin NW: Blood
pressure response to changes in serum ionized calcium
during hemodialysis. Ann Intern Med 1986;104:358-361
14. Sherman RA, Bialy GB, Gazinski B, Bemholc AS, Eisinger
RP: The effect of dialysate calcium levels on blood pressure
during dialysis. Am J Kidney Dis 1986;8:244-247
15. Ramsey M III: Noninvasive automatic determination of
mean arterial pressure. MedBiolEng Comput 1979;17:11-18
16. Silas JH, Barker AT, Ramsay LE: Clinical evaluation of
Dinamap 845 automated blood pressure recorder. Br Heart J
1980;43:202-205
17. Borow KM, Neumann A, Lang RM: Milrinone versus dobutamine: Contribution of altered myocardial mechanics and
augmented inotropic state to improved left ventricular performance. Circulation 1986;73(suppl III):III-153—III-161
18. Teichholz LE, Kreulin T, Herman MV, Gorlin R: Problems in
echocardiographic volume determinations: Echocardiographicangiographic correlations in the presence or absence of
asynergy. Am J Cardiol 1976;37:7-11
19. Kronik G, Slany J, Mosslacher H: Comparative value of
eight M-mode echocardiographic formulas for determining
left ventricular stroke volume. Circulation 1979;60:1308-1316
20. Stefadouros MA, Dougherty MI, Grossman W, Craige E:
Determination of systemic vascular resistance by noninvasive technique. Circulation 1973;47:101-107
21. Lang RM, Fellner SK, Neumann A, Bushinsky DA, Borow
KM: Left ventricular contractility varies directly with blood
ionized calcium. Ann Intern Med 1988; 108:524-529
22. Stanley TH, Isem-Amaral J, Liu W-S, Lunn JK, Gentry S:
Peripheral vascular versus direct cardiac effects of calcium.
Anesthesiology 1976;45:46-58
23. Overbeck HW, Pamnani MB, Derifield RS: Similar vasoconstrictive responses to calcium in normotensive and essential
hypertensive men. Proc Soc Exp Biol Med 1975;149:519-525
218
Hypertension
Vol 13, No 3, March 1989
24. Suki WN, Eknoyan G, Rector FC, Seldin DW: The renal
diluting and concentrating mechanisms in hypercalcemia.
Nephron 1969;6:50-61
25. Beck N, Singh H, Reed SW, Murdaugh HV, Davis BB:
Pathogenic role of cyclic'AMP in the impairment of urinary
concentrating ability in acute hypercalcemia. J Clin Invest
1974 ;54:1049-1055
26. DiBona G: Effect of hypercalcemia on renal tubular sodium
handling in the rat. Am J Physiol 1971 £20:49-53
27. Guyton AC: Arterial pressure regulation—rapid pressure
control by nervous reflexes and other mechanisms, in:
Textbook of.Medical Physiology, ed 7. Philadelphia, W.B.
Saunders and Co, 1986, chap 21, pp 244-256
28. Kaplan NM: Systemic hypertension—mechanisms and diagnosis, in Braunwald E (ed): Heart Disease—A Textbook of
Cardiovascular Medicine, ed 2. Philadelphia, W.B. Saunders and Co, 1984, pp 861-862
. 29. Yue DT: Intracellular [Ca2+] related to rate of force development in twitch contraction of heart. Am J Physiol 1987;
252:H760-H770
30. Morgan JP, Morgan KG: Calcium and cardiovascular function: Intracellular calcium levels during contraction and
relaxation of mammalian cardiac and vascular smooth muscle as detected with aequorin. Am J Med 1984;77:33-46
31. Soltis EE, Field FP: Extracellular calcium and altered vascular responsiveness in the deoxycorticosterone acetate-salt
rat. Hypertension 1986;8:526-532
32. Daul AE, Wang XL, Michel MC, Brodde O-E: Arterial
hypotension in chronic hemodialyzed patients. Kidney Int
1987;32:728-735
33. Nakashima Y, Fouad FM, Nakamoto S, Textor SC, Bravo
EL, Tarazi RC: Localization of autonomic nervous system
dysfunction in dialysis patients. AmJ Nephrol 1987;7:375-381
34. Pang PKT, Tenner TE Jr, Yee JA, Yang M, Janssen HF:
Hypotensive action of parathyroid hormone preparations on
rats and dogs. Proc Natl Acad Sci USA 1980;77:675-678 .
KEY WORDS
calcium
systemic arterial pressure • blood pressure
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
Physiological mechanisms for calcium-induced changes in systemic arterial pressure in
stable dialysis patients.
S K Fellner, R M Lang, A Neumann, K T Spencer, D A Bushinsky and K M Borow
Downloaded from http://hyper.ahajournals.org/ by guest on April 30, 2017
Hypertension. 1989;13:213-218
doi: 10.1161/01.HYP.13.3.213
Hypertension is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1989 American Heart Association, Inc. All rights reserved.
Print ISSN: 0194-911X. Online ISSN: 1524-4563
The online version of this article, along with updated information and services, is located on the
World Wide Web at:
http://hyper.ahajournals.org/content/13/3/213
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published
in Hypertension can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial
Office. Once the online version of the published article for which permission is being requested is located,
click Request Permissions in the middle column of the Web page under Services. Further information about
this process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Hypertension is online at:
http://hyper.ahajournals.org//subscriptions/