Comparison of cellulose diacetate and polysulfone membranes in the outcome of acute renal failure. A prospective randomized study
Karine Gastaldello1,
Christian Melot2,
Robert-Jean Kahn2,
Jean-Louis Vanherweghem1,
Jean-Louis Vincent2 and
Christian Tielemans1
1 Department of Nephrology, Dialysis and Transplantation and
2 Department of Intensive Care, Hôpital Erasme, Université Libre de Bruxelles, Belgium
Correspondence and offprint requests to:
Karine Gastaldello, Department of Nephrology, Hôpital Erasme, 808 Route de Lennik, B-1070 Brussels, Belgium.
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Abstract
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Background. Whether the nature of haemodialysis (HD) membranes can influence the outcome of acute renal failure (ARF) remains debatable. Recent studies have suggested that dialysis with bioincompatible unsubstituted cellulosic membranes is associated with a less favourable patient outcome than dialysis with biocompatible synthetic membranes. Since we generally use a modified cellulosic membrane with substantially lower complement- and leukocyte-activating potential than cuprophane, for dialysis of patients with ARF, and because there are no data in the literature regarding the influence of modified cellulosic membranes on the outcome of patients with ARF, we compared the outcome of ARF patients dialysed either with cellulose diacetate or with a synthetic polysulfone membrane. We also investigated the potential role of permeability by comparing membranes with high-flux versus low-flux characteristics.
Methods. This prospective, randomized, single centre study included 159 patients with ARF requiring HD. Patients were stratified according to age, gender, and APACHE II score and then randomized in chronological order to one of three dialysis membranes: low-flux polysulfone, high-flux polysulfone and meltspun cellulose diacetate.
Results. Aetiologies of ARF and the prevalence of oliguria were similarly distributed among the three groups. There was no significant difference between the three groups for survival (multivariate Cox's proportional hazards model, P=0.57), time necessary to recover renal function (P=0.82), and number of dialysis sessions required before recovery (P=0.86). Multivariate analysis showed that survival was significantly influenced only by the severity of the disease state (APACHE III score, P<0.0001), but not by the nature of the dialysis membrane (P=0.57) or the presence of oliguria (P=0.24).
Conclusions. Among patients with ARF requiring HD survival and recovery time are not significantly influenced by the use of either meltspun cellulose diacetate or the more biocompatible high-flux or low-flux polysulfone. Dialysis using modified cellulose membranes is just as effective as dialysis using synthetic polysulfone membranes, but at a lower cost. In addition, the flux of the membrane did not influence patient outcome.
Keywords: acute renal failure; biocompatibility; dialysis membrane; haemodialysis; sepsis; survival
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Introduction
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Despite many technical advances in patient management, the prognosis of acute renal failure (ARF) requiring haemodialysis (HD) has not improved during the last decades, with an overall mortality rate usually ranging between 30 and 80% [1]. This persistently high mortality rate is usually ascribed to changes in the causes of ARF (obstetric causes have declined, while medical causes due to toxicity of therapeutic or diagnostic agents have increased) and increases in the number of associated conditions (such as number of failing organs, coma, hypotension, need for ventilatory support, sepsis, etc.). In addition, clinical and experimental studies using different types of dialysis membranes have suggested that membrane biocompatibility may adversely affect the outcome of patients with acute renal failure requiring HD (review in [2]). Two prospective, randomized clinical trials have indicated that the nature of the dialysis membrane, i.e. flux and/or biocompatibility, may influence the outcome of ARF in intensive care unit (ICU) patients. Hakim et al. [3] showed that the use of the biocompatible (low complement- and leukocyte-activating potential) low-flux polymethylmethacrylate (PMMA) as compared with the bioincompatible low-flux cuprophane, resulted in an improved recovery of renal function in non-oliguric patients. Schiffl et al. [4] reported that patients developing ARF after cardiac or aortic surgery and dialysed with cuprophane membranes had a lower survival rate, required more HD sessions, and had more lethal septic episodes than those treated with the biocompatible high-flux polyacrylonitrile (PAN) membrane. On the contrary, Kurtal et al. [5] comparing cuprophane with polyamide, a biocompatible high-flux membrane, found no differences in the survival rate of ICU patients with ARF or in the number of dialysis sessions required before recovery. Recently, Himmelfarb et al. [6], compared bioincompatible low-flux cuprophane with biocompatible low-flux synthetic membranes in a study which included patients from the Hakim study [3], and demonstrated improved outcomes (survival and recovery of renal function) in patients with ARF dialysed with biocompatible membranes. However these authors [6] underlined that their results may or may not be applicable to substituted cellulosic membranes. We performed a prospective, randomized trial comparing HD membranes with different degrees of biocompatibility (defined by their complement- and leukocyte-activating potential) and different degrees of permeability, i.e. meltspun cellulose diacetate (CDA) and low- or high-flux polysulfone. Outcome parameters included patient survival, recovery of renal function, duration of dialysis treatment, and causes of death.
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Patients and Methods
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All adult patients requiring HD for ARF in the Erasme Hospital (Brussels, Belgium) between November 1993 and April 1997 were eligible for enrolment in this trial. The study was approved by the institutional review board which waived informed consent. Exclusion criteria were: acute glomerulonephritis, renal transplantation, isolated ultrafiltration for fluid overload, and documented prior chronic renal failure (serum creatinine >2.5 mg/dl). No patients were excluded because of the aetiology of ARF, biochemical values, or the presence of concurrent conditions. All decisions regarding initiation, discontinuation of dialysis due to recovery of renal function, and technical conditions of the dialytic treatment were made by the attending clinical nephrologists who were usually not involved in this study. After a decision had been made to initiate HD, the eligible patients were first classified according to three covariables: age (under or over 50 years old), gender, and severity of disease assessed by the APACHE II score at the time of initiation of dialysis (less or more than 20) [7]. The patients were then randomized by minimization to one of the three types of dialysis membranes which were then used for all subsequent dialysis sessions. The clinical staff were not blinded to the membrane assignment. No continuous renal support technique was used during the study.
A total of 162 patients were included, but three patients were later excluded because of an error in the membrane used. All 159 patients were followed until death, discharge from the hospital and off dialysis, or 80 days after initiation of dialysis, whichever came first. In this latter category, if the patient was still requiring dialysis after 80 days of follow-up, it was considered that the patient would not recover renal function. Three types of single-use dialysis membranes were used with different characteristics of biocompatibility and permeability (Table 1
): high-flux polysulfone (HF PS) (Hemoflow F60S, Fresenius, Germany), low-flux polysulfone (LF PS) (Hemoflow F6S, Fresenius, Germany) and cellulose diacetate which is manufactured using the meltspinning technique (CDA, Altra Flux 140, Althin, USA). PS is a synthetic membrane which does not induce complement activation and produces only a slight drop in white blood cell count. These membranes manufactured from synthetic polymers are considered as biocompatible because of their minimal inflammatory-type contact reactions with blood. Meltspun CDA membrane is a synthetically modified cellulose membrane with the same permeability characteristics as PS low-flux but a biocompatibility which is intermediate between the synthetic membranes and the regenerated unmodified cellulose [8]. In fact, CDA membranes induce a moderate complement activation, as well as a substantial drop in white blood cell count but to a lesser degree than cuprophane. All dialytic treatments were performed using monitors equipped with volumetric-control of ultrafiltration. In an attempt to deliver the same dose of dialysis to all patients, we used dialysers having similar hollow fibre configurations, clearance characteristics, and surface area. In addition, the dialysis schedule was adapted to each patient to maintain predialytic urea levels below 200 mg/dl (mainly 3 h daily). Blood flow rate was maintained between 200250 ml/min. Dialysis water was obtained from reverse osmosis. Bicarbonate-based dialysate was used in all cases, and dialysate flow rate was 500 ml/min. Dialysate concentrations of potassium and calcium, ultrafiltration rate, and anticoagulant dose were adapted at each session by the nephrologist according to patient needs. All therapeutic decisions regarding mechanical ventilation, parenteral nutrition, inotropic support, and other specific treatments were made by the attending ICU physician.
Measurements of endotoxin levels
Endotoxin levels in the dialysate were measured routinely using the chromogenic Limulus Amoebocyte specific assay LAL-Coatest® endotoxin (Chromogenix, Mölndal, Sweden). Results are expressed as EU/ml. The sensitivity of the assay is 0.015 EU/ml in the dialysate.
Scoring of severity of illness
Severity of illness was determined at initiation of dialysis treatment using both the APACHE II and APACHE III scores [7,9,10]. These scores represent the sum of values evaluating current physiologic condition, age, and previous chronic conditions. Since the APACHE II score is a major determinant of hospital mortality in ARF patients [11,12]: (provided it is recorded on dialysis initiation and not on ICU admission [7,11]) we used APACHE II scores for the stratification of patients. For probability analysis of survival (see statistical section), we preferred to use the APACHE III score in the multivariate regression analysis. We also recorded the existence of comorbid conditions (presence of hypertension, congestive heart failure, ischaemic cardiomyopathy, cerebral vascular disease, peripheral vascular disease, liver failure, respiratory insufficiency, neoplasm, immunocompromised status, diabetes), the presence of oliguria (as defined by urine output <400 ml/min), the type of admission (medical, elective surgery, emergency surgery), the need for inotropic support or mechanical ventilation, and the aetiology of ARF (hypotension, sepsis, toxic, rhabdomyolysis, or other). Most patients had an ARF of multifactorial origin. Sepsis was defined as clinical evidence of infection plus at least two of the following conditions: temperature >38°C or <36°C, heart rate >90 beats/min, white blood cell count >12000/mm3 or <4000/mm3, and respiratory rate >20/min.
Outcome measurements
Differences in the survival rate between the three groups were examined by multivariate analysis (Cox proportional hazards method). Outcome measures included survival, cause of death, recovery of renal function (defined as discontinuation of dialysis because it was no longer required as measured by a spontaneous fall in serum creatinine without dialytic intervention), number of HD sessions up to 80 days. We also recorded in each patient confounding factors that may influence the outcome of ARF such as: administration of radiocontrast material, nephrotoxic drugs given after the initiation of dialysis, and the number of HD sessions with hypotension. Hypotension was defined as a decrease in mean arterial pressure of at least 20 mmHg requiring the discontinuation of ultrafiltration, the administration of fluid or the infusion, or increase in dosage, of vasopressive agents.
Statistical analysis
Differences between groups were evaluated using the
2 test for discrete variables and analysis of variance (ANOVA) for continuous data. Probability of survival was analysed using a multivariate Cox's proportional hazards model stratified by the type of dialysis membrane and adjusted for the following covariables: patient characteristics (age, gender), severity of illness (APACHE III score), oliguria, aetiology of ARF (hypotension, sepsis, toxic origin, rhabdomyolysis, chronic renal failure, other causes), comorbidities (hypertension, coronary artery disease, congestive heart failure, peripheral vascular disease, cerebral vascular disease, hepatic insufficiency, respiratory insufficiency, neoplasm, immuno-compromised status, diabetes), organ support (inotropic agents, mechanical ventilation), and type of admission (non postoperative patient, elective postoperative patient, or emergency postoperative patient). P values <0.05 were considered significant except for survival analyses for which we considered a P<0.01 as significant, thus taking into account the two interim analyses. We separately analysed survival in the subgroup of non-oliguric patients using the multivariate Cox's proportional hazards model stratified by the type of dialysis membrane and adjusted for the same covariables as for the whole group except oliguria.
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Results
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The characteristics of the three types of HD membranes used are presented in Table 1
. The study included 159 patients, 53 in each HD membrane group. The patient characteristics at initiation of dialysis are detailed in Tables 2 and 3
. There were no significant differences between groups in demographic data, underlying diseases, severity of illness (APACHE II and III scores), prevalence of oliguria, type of admission, need for organ support, and causes of ARF. Ninety-three per cent of enrolled patients were in the ICU at the time of the first dialytic treatment. The number of patients with an APACHE II score <20 was similar in the three groups (CDA, 16; LF PS, 11; HF PS, 15).
The endotoxin concentrations of the dialysate were assessed throughout the study and were less than 1 EU/ml in all cases.
There was no difference between the three membrane groups in survival or number of HD sessions (Table 4
and Figure 1
). The rate of recovery of renal function was also not significantly different between the three groups of patients (CDA, 45.3%; LF PS, 45.3%; HF PS, 52.8%). The distribution of confounding factors such as the number of HD sessions complicated by hypotension, and exposure to nephrotoxics after inclusion, was similar between the three groups. The main cause of death was sepsis and this was equally distributed in the three groups (Table 4
). Also, there were no differences in any of these parameters when low-flux membranes were pooled (CDA+LF PS) and compared to the high-flux polysulfone membrane (P=0.73) or when synthetic membranes were pooled (HF PS+LF PS) and compared to cellulosic membrane CDA (P=0.49) (data not shown).

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Fig. 1. Multivariate Cox's proportional hazards survival curves (%) according to time of follow up for the three different haemodialysis membranes. CDA: meltspun cellulose diacetate; HF PS and LF PS: respectively high- and low-flux polysulfone.
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Although there was no significant difference between the three groups at baseline, there was a trend towards a lower APACHE III score, less oliguria, and sepsis in the CDA group (Table 2
), which could be a slight bias in favour of the CDA membrane. Therefore, we performed the survival analysis using a stratified multivariate Cox's proportional hazards model to adjust for these variables, which showed that survival between strata was not influenced by the nature of the dialysis membrane (P=0.57), the presence of oliguria (P=0.18), the toxic cause of ARF (P=0.87) or the presence of sepsis (P=0.38). On the contrary, survival was significantly related to the APACHE III score (P<0.0001) as expected.
Finally, in the subgroup of the 69 patients without oliguria, survival was similar with the three membranes (P=0.88, data not shown) and the rate of recovery of renal function was similar for the three groups (CDA, 55%; LF PS, 57%; HF PS, 57%).
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Discussion
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Several groups of investigators have proposed that HD per se may adversely affect the course and the outcome of ARF. Solez et al. [13] have described fresh areas of acute tubular necrosis that could not be explained by the initial renal insult, but rather to further administration of nephrotoxic agents or to exposure of the kidneys (which had lost their capacity of blood flow autoregulation) to repeated hypotensive episodes. Alternatively, it has been hypothesized [14,15] that complement activation and products of leukocyte activation (e.g. reactive oxygen species, leukotrienes, proinflammatory cytokines, proteases), resulting from the interaction of blood with the HD membrane [16], may exacerbate the renal injury and prolong the course of ARF. However, experimental and clinical studies investigating this issue have yielded contradictory results. Using isolated perfused rat kidneys submitted to a mild ischaemic stress, Linas et al. [14] demonstrated the role of activated neutrophils in causing ARF via neutrophil oxidant and/or protease mediated mechanisms. In a model of ischaemic ARF in rats, Schulman et al. [15] found that transfusion of the animals with blood incubated with cuprophane as opposed to PAN resulted in delayed recovery. However, using the same model, Kränzlin et al. [17] found no difference in the outcome of ARF between rats haemodialysed on cuprophane or PAN membrane.
The present prospective, randomized study investigated the role of the HD membrane in the outcome of ARF in 159 patients stratified according to age, gender, and the APACHE II score, and then randomly allocated to three different dialyses. To investigate the respective roles of permeability and biocompatibility of the HD membrane, we compared synthetic membranes with either high- or low-flux characteristics to a low-flux modified cellulosic membrane which was also less biocompatible.
As expected, survival was well predicted by the APACHE III score. Conversely, the nature of the membranes used had no significant influence on survival, on the required number of HD sessions, or on the recovery time. In particular, the outcome of ARF was not better with PS than with the less biocompatible CDA membrane. Patient outcome was independent of membrane permeability, since the outcome was similar when we compared HF PS with LF PS and when we compared pooled low-flux membranes (CDA and LF PS) to HF PS membrane.
To adjust for the severity of the disease underlying ARF, we used the APACHE II score for patient stratification. To confirm that stratification was successful, we also recorded the APACHE III score, which confirmed that severity of illness was equally distributed among the three groups. We are aware of the limitations of these scores but recent data have suggested that the APACHE II and III scores are representative indicators of the severity of disease of patients with ARF [10,11,20].
We did not measure the dose of delivered dialysis, since at the time this study started, there was no data suggesting that the dose of dialysis could affect patient outcome in ARF. However, to minimize the differences between groups, we tried to maintain the same level of uraemia in all patients and we used dialysers with the same hollow fibre configuration and surface area.
Clinical studies investigating the impact of the HD membrane on patient survival are summarized in Table 5
. Only three studies have been published as full papers and were prospective and randomized for the membrane. These studies have given conflicting results. The first study by Hakim et al. [3] found no difference between cuprophane and low-flux PMMA in the whole group of patients, but a better survival and recovery of renal function in a subgroup of non-oliguric patients. It must be emphasized that this subgroup was constructed a posteriori and that the distribution of the patients' characteristics between the membranes within this subgroup was not reported. The second study by Schiffl et al. [4] found a marginally higher death rate, especially from sepsis, in patients dialysed on cuprophane as compared to AN69. However, PAN membranes differ from bioincompatible membranes not only in terms of biocompatibility but also in terms of permeability and adsorptive properties, so that the improved outcome may be due to a combination of the aforementioned factors. This study also presented several limitations which raised criticisms [19,21,22]. The third study by Kurtal et al. [5] found no difference between cuprophane and polyamide but causes of ARF were somewhat heterogeneously distributed in the two groups. Recently, a prospective multi-centre study by Himmelfarb et al. [6], which included patients from the Hakim study [3], shed some light on the role of the HD membrane in the outcome of patients with ARF requiring HD. This study, comparing bioincompatible unsubstituted cellulosic membranes with biocompatible synthetic membranes, demonstrated that biocompatibility is important in determining patient survival and recovery of renal function, particularly in patients who were non-oliguric at the time of initiation of dialysis. It should be noted that modified cellulosic membranes can exhibit more biocompatible patterns than unsubstituted cellulose so that conclusions drawn from the previously cited studies may not be applicable to all cellulosic membranes. Indeed, evidence suggests that modifications of cellulosic membranes reducing their complement activating potential may result in a patient survival rate comparable to synthetic biocompatible membranes. Hakim et al. [28] compared the relative risk of mortality of end-stage renal disease patients dialysed with synthetic, modified cellulosic or unsubstituted cellulosic membranes, and demonstrated that patient survival was greater with either synthetic or modified cellulosic membranes than with unsubstituted cellulosic membranes. Neveu et al. [18] reported similar results, i.e. a better survival rate in patients dialysed with synthetic or modified cellulosic membranes than in those dialysed with unsubstituted bioincompatible cellulosic membranes, although their study was not randomized for membrane allocation. Analysis of the other studies is impossible because substituted cellulosic membranes are sometimes regarded as the bioincompatible membrane [25] or, on the contrary, mixed with synthetic membranes [18,24].
Manufacturing conditions can also influence the performance and the biocompatibility of the membranes [29]. Hollow-fibre can be manufactured either by solution spinning or by solution meltspinning. Solution spinning processes involve synthetic polymers, solvents, pore formers, wetting agents and coagulation steps leading to toxic residuals. During the meltspinning process, heat is used to melt the polymer blend, nitrogen core gas is used to keep the lumen open during extrusion, and air cooling is employed to accomplish thermal phase inversion; the hollow fibres are further processed in hot water and glycerin baths into a semi-permeable membrane. In this study, we used meltspun CDA membranes, and the results may have been different with a cellulosic membrane prepared through another process.
In conclusion, many studies have shown that the biocompatibility of the dialysis membrane plays an important role in the outcome of patients with ARF, but, no study has thus far investigated the possible role of modified cellulosic membrane in this issue. The present controlled, randomized study demonstrated that the modified cellulosic membrane, CDA (which has less complement-activating potential), is just as effective as synthetic PS membranes in the HD of patients with ARF, and at a lower cost.
We also investigated the possible role of membrane permeability on the outcome of patients with ARF, since a previous study by Schiffl et al. [4] suggested that the difference in survival rate between patients dialysed with biocompatible or bioincompatible membranes may result from additive benefits of the permeability and the biocompatibility. We found there was no significant difference between high-flux and low-flux PS in patient outcome.
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Acknowledgments
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The study was partially supported by the Fondation Erasme.
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Received for publication: 8. 3.99
Accepted in revised form: 28. 9.99