Important differentiation of factors that predict outcome in peritoneal dialysis patients with different degrees of residual renal function
Angela Yee-Moon Wang1,
Jean Woo2,
Mei Wang1,
Mandy Man-Mei Sea2,
John E. Sanderson1,
Siu-Fai Lui1 and
Philip Kam-Tao Li1
1 Department of Medicine and Therapeutics and 2 Center for Nutritional Studies, Prince of Wales Hospital, Chinese University of Hong Kong, Shatin NT, Hong Kong
Correspondence and offprint requests to: Dr Angela Yee-Moon Wang, Department of Medicine and Therapeutics, Prince of Wales Hospital, Chinese University of Hong Kong, Shatin NT, Hong Kong. Email: awang{at}cuhk.edu.hk
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Abstract
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Background. Residual renal function (RRF) is an important predictor of outcome in peritoneal dialysis (PD) patients. Whether results from survival studies in dialysis patients with RRF can also be extrapolated to anuric patients remains uncertain. In this observational study, we examined the characteristics of PD patients with a residual glomerular filtration rate (GFR)
1 ml/min per 1.73 m2 vs those with complete anuria and differentiated factors that predict outcome in the two groups of patients.
Methods. Two hundred and forty-six continuous ambulatory peritoneal dialysis (CAPD) patients (39% being completely anuric) were recruited from a single regional dialysis centre. Assessments of haemodynamic, echocardiographic, nutritional and biochemical parameters and indices of dialysis adequacy were done at study baseline and were related to outcomes.
Results. During the prospective follow-up of 30.8±13.8 (mean±SD) months, 28.0% of patients with residual GFR
1 ml/min per 1.73 m2 vs 50.5% of anuric patients had died (P = 0.005). The overall 2 year patient survival was 89.7 and 65.0% for patients with GFR
1 ml/min per 1.73 m2 and anuric patients, respectively (P = 0.0012). Compared with patients with GFR
1 ml/min per 1.73 m2, anuric patients were dialysed for longer (P<0.001), were more anaemic (P<0.005), and had higher calciumphosphorus product (P<0.01), higher C-reactive protein (P<0.001), lower serum albumin (P<0.05), greater prevalence of malnutrition according to subjective global assessment (P<0.05) and more severe cardiac hypertrophy (P<0.001) at baseline. Using multivariable Cox regression analysis, serum albumin, left ventricular mass index and residual GFR were significant factors associated with mortality in patients with GFR
1 ml/min per 1.73 m2, while increasing age, atherosclerotic vascular disease and higher C-reactive protein were associated with greater mortality in anuric PD patients.
Conclusions. Our study demonstrates more adverse cardiovascular, inflammatory, nutritional and metabolic profiles as well as higher mortality in anuric PD patients. Furthermore, factors associated with mortality are also not equivalent for PD patients with and without RRF, suggesting that patients with and without RRF are qualitatively different.
Keywords: cardiovascular; inflammation; malnutrition; mortality; peritoneal dialysis
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Introduction
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Residual renal function (RRF) contributes significantly to the total solute clearance in peritoneal dialysis (PD) patients [1] and is well recognized as an important factor influencing mortality [2], nutrition status [3] and quality of life [4] in chronic PD patients. However, an inevitable decline in RRF is observed with time on dialysis, and PD clearance is usually increased to compensate for the loss in RRF. In the recent reanalysis of the CANUSA study, there is clear evidence indicating a much more important contribution of RRF to the clinical outcomes of PD patients than peritoneal clearance [5]. Other studies also share similar observations that residual renal but not peritoneal clearance is directly correlated with patient survival [2,6]. The ADEMEX trial showing no survival advantage for PD patients as a whole and, in the subgroup, analysis of anuric patients by increasing peritoneal clearance [7] is further evidence to indicate that renal and peritoneal clearance cannot be assumed to be equivalent. Anuric patients are likely to be qualitatively different from patients with RRF. Hence, survival data of patients with RRF cannot simply be extrapolated to anuric patients.
However, most outcome studies in PD patients are performed in either incident or prevalent cases and included mostly patients with RRF. These studies usually have a median follow-up time of 2 years, but an average of 34 years is required for incident patients to become anuric. Furthermore, the few studies done in anuric patients mainly assessed the importance of peritoneal clearance [8,9]. Other factors that predict outcome of these patients have not been evaluated properly.
With this background, we conducted a single-centre observational study in a large cohort of prevalent continuous ambulatory peritoneal dialysis (CAPD) patients. Our aim was to evaluate whether the causes of death as well as factors that predict mortality differed between prevalent PD patients with and without RRF.
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Subjects and methods
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This observational study was started in the regional dialysis centre in the Prince of Wales Hospital in Hong Kong in September 1999. The research protocol was approved by the Clinical Research and Ethics Committee of the Chinese University of Hong Kong. All patients provided informed consent before study entry.
Altogether, 246 end-stage renal disease (ESRD) patients (128 men and 118 women) who have received CAPD for
3 months were enrolled into the study. All patients were dialysed using conventional glucose-based lactate-buffered PD solutions. Our study cohort represented 91% of the total number of patients on PD treatment at our unit. The remaining 9% of patients excluded from the study included those with underlying malignancy, chronic liver disease, systemic lupus erythematosus, chronic rheumatic heart disease or congenital heart disease, those that received PD for <3 months or those with incomplete data. When there was an acute medical problem such as peritonitis, all the baseline assessments were deferred for at least 1 month after complete resolution of the problem. At study baseline, all patients underwent echocardiography together with assessments of nutrition status, dialysis adequacy and biochemical parameters.
Data collection
Data including age, gender, underlying renal disease, CAPD regimen, smoking history, duration on dialysis before study enrolment, body weight and height, presence of diabetes mellitus and background atherosclerotic vascular disease were obtained at study baseline. Atherosclerotic vascular disease is defined as the presence of ischaemic heart disease and history of angina, previous myocardial infarction, coronary artery bypass surgery or stenting, cerebrovascular event, transient ischaemic attack or peripheral vascular disease with or without amputation. Use of erythropoietin and anti-hypertensives as well as systolic and diastolic blood pressure was recorded at study baseline.
Measurements of dialysis adequacy
Patients were asked to bring back 24 h urine and dialysate at study baseline for measurement of urea and creatinine concentration. Adequacy of dialysis was estimated using standard methods as described elsewhere [3].
Echocardiography
Two-dimensional echocardiography was performed at study baseline with a GE-VingMed System 5 echocardiographic machine (GE-VingMed Sound AB, Horten, Norway) using a 3.3 mHz multiphase array probe in all patients lying in the left decubitus position by a single experienced cardiologist blinded to all clinical details of patients. All echocardiographic data were recorded according to the guidelines of the American Society of Echocardiography [10]. Left ventricular mass was indexed by body surface area.
Biochemical measurements
A 20 ml aliquot of fasting venous blood was collected at study baseline for measurement of C-reactive protein (hs-CRP), serum albumin, calcium and phosphorus, and blood haemoglobin. hs-CRP was measured using the Tina-quant CRP (Latex) highly sensitive assay (Roche Diagnostics GmBH, Mannheim, Germany). Serum albumin was measured by the bromcresol purple method (Roche Diagnostics GmBH). Haemoglobin was measured in the standard haematology laboratory.
Nutrition assessment
A single experienced member of the research staff performed the subjective global assessment (SGA) to determine the overall protein-energy nutritional status [11]. It included assessing patients history of weight loss, presence of anorexia and vomiting, grading of muscle wasting and loss of subcutaneous fat. Oedema is not considered an index of malnutrition [11] but its presence or absence has to be taken into account when assessing changes in body weight. Based on these assessments, each patient was graded a score that reflected the nutrition status, namely 1 = normal nutrition; 2 = mild malnutrition; and 3 = moderate to severe malnutrition [11]. Serum albumin concentration and SGA were taken as markers of nutrition.
Study outcome
All patients were followed-up prospectively after all the baseline assessments. No patient was lost to follow-up. Patients who underwent kidney transplant were censored at the time of transplantation. During the follow-up period, all deaths were recorded accurately, with the exact cause of death provided by the attending physician. In the case of death out of hospital, family members were interviewed by telephone to ascertain the circumstances surrounding death. Cardiovascular death included death associated with a definite myocardial ischaemic event, heart failure, cerebrovascular accident, arrhythmia or peripheral vascular accident, all of which were defined according to standard clinical criteria, and sudden death which was defined as unexpected natural death within 1 h from the symptom onset and without any prior condition that would appear fatal [12]. The clinical outcome evaluated in this study was patient survival.

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Fig. 1. KaplanMeier survival curves of peritoneal dialysis patients with RRF (defined as those with residual GFR 1 ml/min per 1.73 m2) vs those with complete anuria or no RRF.
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Statistical analysis
Statistical analysis was performed using SPSS software, version 10.0 (SPSS, Inc., Chicago, IL). Continuous data were reported as mean±SD. Skewed distributions were reported as median (interquartile range; IQR). Categorical data were reported as percentages. The different parameters of patients with and without RRF were compared using the unpaired t-test, MannWhitney test or
2 test where appropriate. In the analysis of patient survival, the event was death. Transplantation was counted as censored observations. A patient's death while on CAPD or after conversion to haemodialysis was counted as an event. Factors predictive of mortality in patients with residual GFR
1 ml/min per 1.73 m2 and completely anuric patients were first determined using univariate Cox regression analysis. Variables significant at a P-value <0.25 on univariate analysis were presented further to the multivariable Cox regression models together with dialysis duration. A backward stepwise elimination procedure was applied and only variables that remained significant at a P-value <0.05 were kept in the model. Survival curves were generated according to the KaplanMeier method. Differences in the survival between patients with residual GFR
1 ml/min per 1.73 m2 and anuric patients were compared by the Mantel log-rank test. A P-value of <0.05 was considered statistically significant.
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Results
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Our study cohort had a mean±SD age of 55±12 years and were on CAPD treatment for a median duration of 27 (range 4151) months before study enrolment. The underlying renal diagnosis included chronic glomerulonephritis in 77 patients (31%), diabetic nephropathy in 60 patients (24%), hypertensive nephrosclerosis in 34 patients (14%) and other miscellaneous causes in 75 patients (31%). Among the 246 patients, 75 patients (31%) had diabetes mellitus and 56 patients (23%) had clinical atherosclerotic vascular disease. Ninety-five patients were completely anuric, 58 patients had GFR between 0 and 1 ml/min per 1.73 m2, and 93 patients had GFR
1 ml/min per 1.73 m2. Forty percent of our patients were prescribed erythropoietin. The daily PD exchanges performed were 4.5 l in four patients (1.6%), 5 l in one patient (0.4%), 6 l in 175 patients (71.1%), 8 l in 57 patients (23.2%) and 10 l in nine patients (3.7%). The average weekly total and PD Kt/V of our study patients was 1.81±0.45 and 1.52±0.36, respectively. The mean weekly total creatinine clearance (CCr) was 57±22 l/week per 1.73 m2, and residual GFR was 1.25 (range 08.24) ml/min per 1.73 m2. Correlations of the different factors with dialysis duration are shown in Table 1.
We compared the characteristics of patients with residual GFR
1 ml/min per 1.73 m2 (n = 93) vs those with complete anuria (n = 95) in Tables 2 and 3. Seventy-six percent of patients with GFR
1 ml/min per 1.73 m2 vs 46% of anuric patients had a weekly total Kt/V of
1.7 (P<0.001). Seventy percent of patients with GFR
1 ml/min per 1.73 m2 vs 1% of anuric patients had a weekly total CCr of
60 l/week per 1.73 m2. Background atherosclerotic vascular disease was present in 37% of anuric men vs 17% of anuric women (P = 0.028). Among patients with GFR
1 ml/min per 1.73 m2, men (20%) and women (19%) did not differ in the prevalence of atherosclerotic vascular disease (P = 0.931).
The study cohort was followed for a mean duration of 30.8 months (range 1.848.7). During this period, 22 patients were transferred to long-term haemodialysis and 23 patients underwent kidney transplantation. Altogether, 74 patients (39.4%) died, six of which occurred after transferral to haemodialysis (two patients with GFR
1 ml/min per 1.73 m2 and four anuric patients). Causes of death were classified as cardiovascular in 44 patients. Slightly more anuric men (58%) than women (44%) died during follow-up (P = 0.308). Among patients with GFR
1 ml/min per 1.73 m2, men (27%) and women (30%) showed no significant difference in mortality (P = 0.948). The clinical outcomes of patients with GFR
1 ml/min per 1.73 m2 and anuric patients are detailed in Table 4. During the follow-up period, 28.0% of patients with GFR
1 ml/min per 1.73 m2 vs 50.5% of anuric patients died (P = 0.005). According to the KaplanMeier analysis, the overall patient survival at 12, 24 and 36 months was 95.6, 89.7 and 79.5% for patients with GFR
1 ml/min per 1.73 m2 vs 81.7, 65.0 and 51.2%, respectively, for anuric patients (P = 0.0012). Anuric patients were at 2.17-fold higher risk (95% confidence interval, 1.34 3.50; P = 0.002) for mortality than those with residual GFR
1 ml/min per 1.73 m2.
The results of the univariate Cox regression analysis for mortality in patients with residual GFR
1 ml/min per 1.73 m2 and anuric patients are summarized in Table 5. In multivariable Cox regression analysis, serum albumin, left ventricular mass index and residual GFR were associated with mortality in patients with GFR
1 ml/min per 1.73 m2. Among anuric patients, backward elimination resulted in a model with age, hs-CRP and atherosclerotic vascular disease (Table 6). PD Kt/V was not significant in the multivariable model for mortality in anuric patients.
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Table 5. Univariate Cox regression analysis of baseline variables in relation to mortality in patients with and without residual renal function
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Table 6. Multivariable Cox regression analysis showing factors independently associated with mortality in patients with and without residual renal function
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Discussion
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In this prospective study, we observed a significantly higher mortality, from both cardiovascular and non-cardiovascular causes, in anuric patients than in those with RRF. This is in keeping with the majority of studies including our own showing an important contribution of RRF to the overall solute clearance [1], nutrition status [3] and mortality [2,5] in PD patients. Although Chinese PD patients generally have better survival despite a lower overall solute clearance [13], our results showed that the 2 year survival of anuric Chinese PD patients was only 65.0% compared with 89.7% for those with GFR
1 ml/min per 1.73 m2 and 78% for the Caucasian PD patients of the CANUSA study [14], indicating that the survival benefit of Chinese PD patients is largely maintained in the presence of RRF. Our results are comparable with those of a previous study from our centre reporting a 2 year survival of 68% in a different cohort of anuric PD patients [8]. The higher mortality in anuric patients probably represents the lead-time bias as anuric patients were dialysed for a median of 30 months more than those with GFR
1 ml/min per 1.73 m2.
Compared with patients with preserved RRF, anuric patients showed a more adverse metabolic and cardiovascular profile at study baseline as evidenced by the greater anaemia with more erythropoietin resistance, higher calciumphosphorus product (Ca x P), more inflammation and malnutrition, more hypertension, greater cardiac hypertrophy as well as higher overall and cardiovascular mortality. Indeed, a decline in residual GFR with greater CRP, higher Ca x P and left ventricular mass index as well as greater PD Kt/V were observed with increasing duration on dialysis. In this study, the PD Kt/V of anuric patients was only modestly higher than that of those with RRF, and the resulting total Kt/V remained marginally below the recommended total Kt/V of at least 1.7 for Chinese PD patients [15]. Hence, a prospective study is needed to evaluate whether increasing PD clearance will modify these other risk factors in anuric patients. According to the ADEMEX study, increasing PD Kt/V within the range studied (from 1.62 to 2.13) had neutral effects on patient survival and a number of secondary parameters including blood pressure, anaemia and the appearance of protein nitrogen [7]. No assessments were made, however, with respect to cardiovascular and inflammatory parameters in the ADEMEX study.
Inflammation is a well-known predictor of mortality in PD patients [16] and is associated with atherosclerosis. In this study, CRP shows a differential effect on survival in that it predicts mortality in anuric patients but not in patients with RRF. The exact explanation for this difference is not clear, but the higher CRP in anuric patients in contrast to the lower CRP and less variability in CRP among those with RRF suggests that our study may not be sufficiently powered to detect an association between CRP and mortality among those with RRF. It also raises the possibility that CRP or inflammation may be more of a problem and has greater impact in anuric PD patients. As shown in a recent study, CRP and pro-inflammatory mediators are inversely related to RRF [17]. Renal insufficiency may increase inflammatory mediators via increased oxidative stress that further lead to monocyte activation and cytokine production [18], or it may impair clearance of inflammatory mediators as in nephrectomized rats [19]. This is in good agreement with the higher CRP observed among our anuric PD patients. In anuric patients, PD is usually increased to compensate for the loss in RRF. However, PD may not completely replace all the functions of the failing native kidneys especially clearance of middle and large molecular weight uraemic toxins, acute-phase reactants such as CRP as well as pro-inflammatory cytokines. Furthermore, PD may enhance inflammation as a result of bio-incompatibility of dialysis solutions and advanced glycation end-product formation [20]. The qualitative differences between renal and peritoneal clearance may potentially explain why PD patients with and without RRF are qualitatively different and thus cannot be assumed to be equivalent.
Volume expansion is increasingly recognized as an important predictor of mortality in PD patients [21]. While blood pressure is better controlled with PD in the initial years, a long-term study showed that blood pressure tends to increase over time with declining RRF [22] and explains the greater cardiac hypertrophy observed with increasing time on dialysis. Another study also identified declining RRF as one of the important predictors of hypertension in PD patients [23], indicating that euvolaemia may be more difficult to achieve in anuric patients. Indeed, even though PD is suggested to allow better fluid control and preserve RRF better in patients with RRF [24], a study showed that long-term, anuric CAPD patients are generally more volume expanded and have more left ventricular hypertrophy than long-term haemodialysis patients [25]. In our study, the greater use of anti-hypertensives and greater left ventricular hypertrophy in anuric patients compared with those with RRF suggests that anuric patients are indeed more volume expanded and have greater difficulty in maintaining fluid balance.
In this study, PD Kt/V showed no significant association with mortality in anuric patients. This finding is similar to a number of other studies also showing no impact of PD Kt/V on survival in anuric patients [2,5,9] but differs from an earlier study from our centre showing an independent effect of PD Kt/V on the survival of anuric PD patients [8]. The explanation for this discrepancy is not clear, but it may be explained by differences in the covariates being adjusted. In the previous study from our centre [8], CRP and left ventricular hypertrophy, both being well known predictors for mortality, were not considered at all in the analysis. At first sight, our results may appear counter-intuitive as it is obvious that without PD, anuric ESRD patients will inevitably die. We cautioned that our results should not be interpreted as though PD clearance is not important in anuric patients. Rather, the lack of significance may relate to the narrow range of PD Kt/V and also other factors such as CRP and atherosclerotic vascular disease being more significant in predicting outcome of anuric patients.
In this study, prevalent but not incident cases were examined and may result in an over-representation of anuric patients, hence leading to either an under- or over-estimation of the true risk associated with anuria. A single time point measurement of each parameter at study baseline was used to predict subsequent outcome and may not reflect changes over time. Furthermore, our study is of cross-sectional design and it remains undetermined whether the risk factors of anuric patients are inherent to them and also predispose them to more rapid loss of RRF. Nevertheless, our study demonstrates important qualitative differences between patients with and without RRF and also that factors affecting outcome are also not equivalent in these patients. Apart from increasing dialysis clearance to compensate for the loss in RRF, our results indicate that more emphasis should be placed on maintaining fluid balance and nutrition status, targeting inflammation, and reducing calcium phosphorus load and anaemia and atherosclerotic vascular diseases, all of which have important influence on the outcome of PD patients.
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Acknowledgments
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This study was supported by the Hong Kong Health Service Research Fund and the Bristol Myers Squibb Unrestricted Nutrition Grant Program.
Conflict of interest statement. None declared.
[See related article by Davies (this issue, pp. 270272)].
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Received for publication: 27. 2.04
Accepted in revised form: 30. 4.04
Related articles in NDT:
- Are PD patients with or without residual renal function qualitatively differentor are they simply at different stages of the continuum of progressive uraemia?
- Simon Davies
NDT 2005 20: 270-272.
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