(Circulation. 2000;102:203.)
© 2000 American Heart Association, Inc.
Clinical Investigation and Reports |
Renal Function, Neurohormonal Activation, and Survival in Patients With Chronic Heart Failure
From the Department of Clinical Pharmacology, State University Groningen, The Netherlands (H.L.H, D.d.Z.); the Department of Intensive Care, University Hospital of Free University, Amsterdam, The Netherlands (A.R.J.G.); the Department of Cardiology/Thoraxcenter, University Hospital Groningen, The Netherlands (P.J.d.K, D.J.v.V.); COEUR/Department of Internal Medicine, University Hospital Dijkzigt, Rotterdam, The Netherlands (F.B.); Nottingham Clinical Trial Data Centre, Nottingham, United Kingdom (A.C.); and Department of Cardiovascular Medicine, Queen’s Medical Centre, Nottingham, United Kingdom (J.R.H.).
Correspondence to Dr D.J. van Veldhuisen, Department of Cardiology/Thoraxcenter, University Hospital Groningen, Hanzeplein 1, PO Box 30.001, 9700 RB Groningen, The Netherlands. E-mail d.j.van.veldhuisen{at}thorax.azg.nl
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Abstract |
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Background—Because renal function is affected by chronic heart failure (CHF) and it relates to both cardiovascular and hemodynamic properties, it should have additional prognostic value. We studied whether renal function is a predictor for mortality in advanced CHF, and we assessed its relative contribution compared with other established risk factors. In addition, we studied the relation between renal function and neurohormonal activation.
Methods and Results—The study population consisted of 1906 patients with CHF who were enrolled in a recent survival trial (Second Prospective Randomized study of Ibopamine on Mortality and Efficacy). In a subgroup of 372 patients, plasma neurohormones were determined. The baseline glomerular filtration rate (GFRc) was calculated using the Cockroft Gault equation. GFRc was the most powerful predictor of mortality; it was followed by New York Heart Association functional class and the use of angiotensin-converting enzyme inhibitors. Patients in the lowest quartile of GFRc values (<44 mL/min) had almost 3 times the risk of mortality (relative risk, 2.85; P<0.001) of patients in the highest quartile (>76 mL/min). Impaired left ventricular ejection fraction (LVEF) was only modestly predictive (P=0.053). GFRc was inversely related with N-terminal atrial natriuretic peptide (ANP; r=-0.53) and, to a lesser extent, with ANP itself (r=-0.35; both P<0.001).
Conclusions—Impaired renal function (GFRc) is a stronger predictor of mortality than impaired cardiac function (LVEF and New York Heart Association class) in advanced CHF, and it is associated with increased levels of N-terminal ANP. Moreover, impaired renal function was not related to LVEF, which suggests that factors other than reduced cardiac output are causally involved.
Key Words: heart failure • prognosis • kidney • hormones
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Introduction |
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Chronic heart failure (CHF) is caused by a loss of ventricular function and by various adaptational responses, including neurohormonal activation, peripheral vasoconstriction, and salt and water retention.1 A large number of clinical, hemodynamic, biochemical, and electrophysiological factors have now been identified that are related to prognosis in patients with CHF.2 In routine clinical practice, left ventricular function (including left ventricular ejection fraction [LVEF]), the clinical severity of the disease (eg, New York Heart Association functional class ([NYHA]), and cause of the disease all carry independent prognostic value. Biochemical markers, including serum sodium, urea, and creatinine, and neurohormones may have additive value.3 4 It has been suggested that the activation of the renin-angiotensin-aldosterone system (RAAS), which occurs when renal perfusion pressure is reduced in CHF, is not primarily a response to preserve circulatory homeostasis, but a renal compensatory reaction to preserve renal function.5 It could thus be postulated that renal function can indirectly be used as an indicator of cardiovascular status in CHF and may, therefore, potentially be a powerful prognostic indicator.
Two previous studies reported the prognostic value of renal function (serum creatinine) in patients with CHF, but whether renal function contributed independently to mortality was not discussed.6 7 Therefore, we examined renal function as a predictor of mortality in advanced CHF. Our secondary aim was to identify the relative contribution of renal function compared with established risk factors to the prognosis of the disease. Finally, we determined whether the relation between renal function and mortality was linked through neurohormonal activation. The study population consisted of patients who were enrolled in a recent survival trial (Second Prospective Randomized study of Ibopamine on Mortality and Efficacy [PRIME-II]).8 In a subgroup of 372 patients, a predefined neurohormonal substudy was conducted.9
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Methods |
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The details of PRIME-II have been described previously.8 Briefly, the study was designed to investigate the effect of the oral dopamine agonist ibopamine on mortality in advanced CHF. The study was conducted in 13 European countries, and 1906 patients were included. PRIME-II was prematurely discontinued in August 1995 when a significantly higher fatality rate was observed in the ibopamine group. Patients, aged 18 to 80 years, were eligible for PRIME-II if they had moderate to severe CHF (NYHA class III to IV) and evidence of left ventricular dysfunction (including LVEF<0.35). In the predefined substudy, which was performed only in the Netherlands, blood for plasma neurohormone detection was collected from 372 patients.9
Renal Function
The glomerular filtration rate (GFR) is the standard
indicator of renal function. Under steady-state conditions, GFR is
estimated from serum creatinine using a formula that
accounts for the influence of age and body weight on
creatinine production (the Cockroft Gault
equation)10 11 : GFRc=[(140-age in
years)x(body weight in kg)]/(72xserum creatinine in
mg/dL). In women, the value is multiplied by 0.85. This formula has
been validated in several studies of CHF and renal dysfunction, and it
showed a correlation >0.90, with accurately measured
GFR.10 11 12 13 14 15
Neurohormonal Measurements
The method of handling, storing, and determining neurohormonal
levels has been previously described in detail.9 10
Plasma norepinephrine, epinephrine, and dopamine
levels were determined by high-performance liquid
chromatography with fluorometric detection. Active
plasma renin concentration was measured by a radioimmunoassay of
generated angiotensin I. To measure
aldosterone, endothelin, atrial natriuretic
peptide (ANP), and plasma N-terminal ANP, commercially available kits
were used.
Statistical Methods
The influence of baseline renal function on survival in the
total study population was studied with Kaplan Meier methods and Cox
regression. To isolate the independent effect of
GFRc on overall mortality, the statistical
analysis included adjustments for several possible risk
factors, including age, sex, blood pressure, heart rate, rhythm, cause
and duration of CHF, and concomitant medication (in particular,
angiotensin-converting enzyme [ACE]
inhibitors, diuretics, digoxin, and antiarrhythmic
drugs). The effects of ibopamine on survival and other baseline
characteristics that were prognostically relevant were also used in
this analysis. A further description of risk factors can be
found elsewhere.8 10
Continuous variables were modelled with indicator variables into quartiles, and relative risks with the lowest risk quartile were calculated for those in the second, third, and fourth quartiles. Test for trends are presented. Only variables with P<0.10 in the univariate Cox regression analysis were used in the multiple Cox regression analysis. Cumulative relative risks were calculated within the subgroups defined by GFRc strata with degree of LVEF and NYHA class. Interaction terms were used to examine effect modification.
To reduce the risk of bias by the empirical use of arbitrary values for missing items of data, we excluded observations with missing values for contributing variables in the multivariate model. Stepwise linear regression analysis was used to determine the relationship between each of the plasma neurohormones with GFRc and LVEF and other relevant, significant baseline variables. Plasma neurohormone values were not normally distributed, and their natural logarithms were incorporated. Pearson or Spearman correlation coefficients were calculated to determine which independent variables had a significant univariate association with serum creatinine. To examine all possible interactions of the effects of various variables, a secondary analysis that included interaction terms was performed. In addition, we performed a separate analysis of the subgroups with and without ibopamine. All reported probability values are 2-tailed, and P<0.05 was considered statistically significant.
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Results |
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Patient Characteristics
Table 1
shows the baseline
characteristics of the total population (n=1906) and the neurohormonal
subgroup (n=372). In 204 of the 1906 patients, values were missing for
1 contributing variable in the multivariate
model; these patients were excluded from the analysis.
Therefore, full analyses of GFRc were
performed on 1702 patients. No significant demographic or clinical
differences were found between the total and actual study
populations.
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Renal Function and Overall Mortality
After a median follow-up of 277 days (range, 0 to 1091 days), 343
patients had died. In unadjusted analyses,
GFRc at baseline was strongly associated with
all-cause mortality, with a clear separation of curves and a marked
stepwise increase in the cumulative incidence of mortality for
successively lower quartiles of GFRc (Figure 1).
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Table 2 summarizes the
univariate and multivariate results of
independent predictors that remained significantly associated (with the
exception of LVEF) with mortality. GFRc was the
most powerful predictor of mortality, as expressed by the Wald
statistics; this was followed by NYHA class and use of ACE
inhibitors. Patients in the lowest quartile of
GFRc values (<44 mL/min) had almost 3 times the
risk of mortality (relative risk, 2.85; P<0.001) of the
patients in the highest quartile (>76 mL/min). LVEF contributed only
modestly to mortality (P=0.053 for trend). The risk of
mortality was almost equal for the first 2 GFRc
quartiles. A similar observation was present for the first 3
quartiles of LVEF (Figure 2). Weak
prognostic values for mortality (relative risks <2.0) were found for
NYHA class, systolic blood pressure, digitalis use, history of
myocardial infarction, sodium level, ß-blocker use, use of
anticoagulants, LVEF, and ibopamine use. The proportional relationship
of GFRc with mortality was also evident in the
Cox-adjusted survival plot (Figure 3).
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When performing secondary analyses, no interaction term was statistically significant in the multivariate analysis, including ibopamine treatment and renal function (P=0.194). In the separate subgroup analyses according to treatment with and without ibopamine, similar highly significant trends in relative risks for successively lower quartiles were observed when compared with the highest quartile of GFRc (relative risks of 1.31, 2.36, and 2.48, respectively, for the ibopamine group [P<0.001] and of 1.35, 1.66, and 3.41, respectively, for the placebo group [P<0.001]).
Additional adjustments for univariate prognostic variables for mortality, such as age, heart rate, body weight, diastolic blood pressure, serum potassium level, urea and creatinine levels, cause of CHF, diabetes mellitus, intraventricular conduction disorders, absence of sinus rhythm, orthopnea, dyspnea, peripheral edema, fatigue, nitrate use, use of direct vasodilators, the administered dose of ACE inhibitors, and furosemide use were nonsignificant in the multivariate model and were not included.
Mortality and the Relationship Between GFRc, LVEF, and
NYHA Class
Cumulative relative risk estimates for the
GFRc categories in combination with NYHA classes
and LVEF are shown in Figures 4 and 5. A stepwise increase in mortality risks
with decreasing GFRc and LVEF was present.
When divided into quartiles, LVEF showed lower risk estimates than
GFRc. No interaction between
GFRc and LVEF was observed, so
GFRc and LVEF had an effect that was additive in
terms of predicting mortality. An identical analysis of
GFRc with NYHA class revealed a similar pattern.
In addition, only weak inverse correlations were observed between
baseline GFRc and NYHA class and between LVEF and
NYHA class (r=-0.062, P=0.002 and
r=-0.030, P=0.142, respectively). There was no
correlation between GFRc and LVEF
(r=-0.013, P=0.422).
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GFRc, LVEF, and Plasma Neurohormones
The neurohormonal subpopulation was largely similar to the general
PRIME-II population (Table 1
). Most neurohormones were elevated
compared with normal values, but epinephrine, dopamine, and
aldosterone levels were within the normal range.
Univariate correlation coefficients for neurohormones with
GFRc and LVEF and the results of the stepwise
multivariate regression analyses are
presented in Table 3. The
majority of plasma neurohormones showed a statistically significant,
but only moderate, relation with GFRc and LVEF.
In general, a more pronounced association was found with
GFRc, and the strongest associations were found
for ANP (r=-0.35) and N-terminal ANP
(r=-0.53).
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Discussion |
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The important new finding in this study is that renal function, as measured by GFRc, is strongly associated with mortality in patients with advanced CHF; it seems to be independent of the impaired LVEF found in these patients. Renal function was more closely associated with mortality in patients with advanced CHF than any other established risk factor, including NYHA class and LVEF. In addition, renal function correlated significantly, and more strongly than LVEF, with plasma neurohormones (in particular, N-terminal ANP).
Renal Function as a Marker of Prognosis and Clinical
Status?
Patients with renal dysfunction had a significantly poorer
prognosis compared with patients with relatively preserved renal
function, despite a similar NYHA functional class and LVEF. A number of
studies focusing on specific groups such as hypertensive individuals,
the elderly, patients with recent stroke, survivors of myocardial
infarction, and patients after open heart surgery indicated that
elevated serum creatinine may be an independent predictor
of all-cause and of cardiovascular disease
mortality.16 17 18 19 Two previous studies have reported the
prognostic value of renal function in patients with CHF; both used
serum creatinine as a measure for renal
function.6 7 However, the patient characteristics of those
populations were limited and, remarkably, the impact of this
observation was not discussed in either article. In another study, it
was speculated that renal function might carry prognostic information,
but this study mainly dealt with changes in serum
creatinine.20
In several studies, LVEF has been shown to correlate directly with survival in patients with CHF. Although LVEF is an indicator of left ventricular dysfunction, it does not have a strong relationship with clinical symptoms.4 21 Renal function includes both cardiovascular and hemodynamic properties and, thus, its prognostic value in CHF could be expected. It may be postulated that because renal function is measured on a continuous scale, it is more likely to be a more powerful predictor of the clinical status of the patient than, for example, NYHA class. However, the present study shows that LVEF, GFRc, and NYHA class are prognostically important and that they act in part independently and show only weak correlations with each other. This is demonstrated by the relatively large number of patients with severely impaired renal function who do not have severely impaired cardiac function and vice versa. Further, it supports the hypothesis that cardiac function, clinical status, and renal function represent, in part, different prognostic entities of CHF.
Treatment with ibopamine was a unique aspect of this study. Ibopamine is an oral dopamine analogue with vasodilatory, positive inotropic, and diuretic effects.22 In the PRIME-II study, ibopamine increased the risk of death among patients with advanced CHF, but the reasons for this increase are not clear. In a post hoc subgroup analysis, antiarrhythmic treatment was a significant predictor of increased mortality in ibopamine-treated patients.8 The possibility that ibopamine may have contributed to the relationship between GFRc and mortality was investigated by interaction analysis in the total population and in a separate analysis of the subgroups. Although in this exploratory analysis ibopamine did not seem to modify this effect, a confounding influence still may have been present. The present findings must, therefore, be viewed cautiously.
Relation Between Renal and Cardiac Dysfunction and
Neurohormonal Activation
In the early stages of CHF, GFR is well maintained by compensatory
increases in filtration fraction; in patients with more severe CHF, GFR
becomes more dependent on afferent arteriolar flow and the stimulation
of hemodynamic and hormonal pathways.20 23
Furthermore, the fall in effective renal blood flow is relatively more
pronounced and therefore disproportional to the reduction in cardiac
output.23 24 Nevertheless, it was recently demonstrated
that renal hemodynamic reserve is already impaired in
patients with asymptomatic left ventricular
dysfunction.25 Traditionally, the contribution of the
kidneys to CHF has been considered an adaptive response mechanism
evoking a series of compensatory neurohormonal changes, in particular,
increased adrenergic drive and activation of the RAAS to maintain
perfusion to vital organs and to expand the inadequate
arterial blood volume.20 23 24 25 26 27 28 29 30 31 With respect
to the kidneys, however, activation of the RAAS is not only a response
to preserve systemic circulatory volume; indeed, it is primarily a
response to preserve GFR as renal blood flow decreases and renal
perfusion pressure declines.5 Therefore, it could be
postulated that the association between renal function and prognosis is
linked by neurohormonal activation.
In our study, renal function correlated significantly, and more strongly than LVEF, with neurohormonal activation (in particular, with N-terminal ANP). N-terminal ANP is a powerful predictor of cardiovascular mortality.32 The majority of the other vasoactive neurohormones, including those related to the RAAS, however, were only weakly associated with renal function. A direct relationship between the kidney and natriuretic peptides has never been demonstrated, but the main counteracting mechanism available to the circulation to break through the vicious circle of salt and water retention induced by the failing kidneys is the production of ANP. In the present study, a relation between renal function and ANP and N-ANP was indeed observed. Renal responsiveness to natriuretic peptides, however, seems to decrease as CHF worsens, even in the presence of rising plasma concentrations of these peptides.33
Limitations of the Study
This study is limited by its observational nature. GFR was
calculated using the Cockroft Gault equation. Thus, GFR in patients
with severe CHF could potentially be overestimated because serum
creatinine is dependent on muscle mass, which may be
lowered in patients with CHF, particularly in those with cachexia.
However, if one takes that into account, the results would be even more
convincing. Also, this study constitutes cross-sectional observational
data and, thus, can only be used to generate new hypotheses. In this
respect, it must be noted that half of the patients were treated with
ibopamine, which showed an increased risk for mortality in the original
study. Further, although medication was in general similar, not all
patients were using the same drugs or doses of drugs. Although we
corrected for these differences, their true influence may not have been
adequately represented by the multivariate
analysis.
Clinical Implications
Our findings have several clinical implications; the most
important is that renal function may serve as one of the most important
determinants of prognosis in advanced CHF and that it seems to be more
powerful than cardiac parameters (such as LVEF) in
discriminating patients at risk. Moreover, in a substantial number of
patients, the compromised renal function is probably not caused by
cardiac disease. We speculate that nephrosclerosis,
which seems to run in parallel with systemic
atherosclerosis, accounts for the impaired renal
function.34 A strong, direct relationship between renal
function and activation of the RAAS could not be established, but a
significant correlation between plasma levels of N-terminal ANP and
GFRc was found. Therefore, determination of renal
function may serve to identify CHF patients at risk, which may have
therapeutic implications. This hypothesis will require further
prospective studies. It must be emphasised, however, that a population
with severe CHF was studied, and the results cannot be automatically
extrapolated to patients with less severe CHF.
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Acknowledgments |
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Dr van Veldhuisen is a Clinical Established Investigator of the Netherlands Heart Foundation.
Received September 21, 1999; revision received January 28, 2000; accepted February 11, 2000.
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R. P.E. van Dokkum, W. B.A. Eijkelkamp, A. C.A. Kluppel, R. H. Henning, H. van Goor, M. Citgez, W. A.K.M. Windt, D. J. van Veldhuisen, P. A. de Graeff, and D. de Zeeuw Myocardial Infarction Enhances Progressive Renal Damage in an Experimental Model for Cardio-Renal Interaction J. Am. Soc. Nephrol., December 1, 2004; 15(12): 3103 - 3110. [Abstract] [Full Text] [PDF]
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J. Ezekowitz, F. A. McAlister, K. H. Humphries, C. M. Norris, M. Tonelli, W. A. Ghali, M. L. Knudtson, and APPROACH Investigators The association among renal insufficiency, pharmacotherapy, and outcomes in 6,427 patients with heart failure and coronary artery disease J. Am. Coll. Cardiol., October 19, 2004; 44(8): 1587 - 1592. [Abstract] [Full Text] [PDF]
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K. Bibbins-Domingo, F. Lin, E. Vittinghoff, E. Barrett-Connor, D. Grady, and M. G. Shlipak Renal insufficiency as an independent predictor of mortality among women with heart failure J. Am. Coll. Cardiol., October 19, 2004; 44(8): 1593 - 1600. [Abstract] [Full Text] [PDF]
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M. G. Shlipak and B. M. Massie The Clinical Challenge of Cardiorenal Syndrome Circulation, September 21, 2004; 110(12): 1514 - 1517. [Full Text] [PDF]
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G.M. Felker, K. F. Adams Jr, W. A. Gattis, and C. M. O'Connor Anemia as a risk factor and therapeutic target in heart failure J. Am. Coll. Cardiol., September 1, 2004; 44(5): 959 - 966. [Abstract] [Full Text] [PDF]
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M. G. Shlipak, G. L. Smith, S. S. Rathore, B. M. Massie, and H. M. Krumholz Renal Function, Digoxin Therapy, and Heart Failure Outcomes: Evidence from the Digoxin Intervention Group Trial J. Am. Soc. Nephrol., August 1, 2004; 15(8): 2195 - 2203. [Abstract] [Full Text] [PDF]
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P. van der Meer, A. A. Voors, E. Lipsic, T. D. J. Smilde, W. H. van Gilst, and D. J. van Veldhuisen Prognostic value of plasma erythropoietin on mortality in patients with chronic heart failure J. Am. Coll. Cardiol., July 7, 2004; 44(1): 63 - 67. [Abstract] [Full Text] [PDF]
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A. Cataliotti, G. Boerrigter, L. C. Costello-Boerrigter, J. A. Schirger, T. Tsuruda, D. M. Heublein, H. H. Chen, L. S. Malatino, and J. C. Burnett Jr Brain Natriuretic Peptide Enhances Renal Actions of Furosemide and Suppresses Furosemide-Induced Aldosterone Activation in Experimental Heart Failure Circulation, April 6, 2004; 109(13): 1680 - 1685. [Abstract] [Full Text] [PDF]
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F. A. McAlister, J. Ezekowitz, M. Tonelli, and P. W. Armstrong Renal Insufficiency and Heart Failure: Prognostic and Therapeutic Implications From a Prospective Cohort Study Circulation, March 2, 2004; 109(8): 1004 - 1009. [Abstract] [Full Text] [PDF]
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E. Ritz and W. M. McClellan Overview: Increased Cardiovascular Risk in Patients with Minor Renal Dysfunction: An Emerging Issue with Far-Reaching Consequences J. Am. Soc. Nephrol., March 1, 2004; 15(3): 513 - 516. [Abstract] [Full Text] [PDF]
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