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NDT Advance Access originally published online on August 25, 2006
Nephrology Dialysis Transplantation 2006 21(12):3532-3538; doi:10.1093/ndt/gfl415
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Effect of dialysis membrane biocompatibility on polymorphonuclear granulocyte activity in dialysis patients*

Giuliana Banche1, Valeria Allizond1, Franca Giacchino2, Narcisa Mandras1, Janira Roana1, Franco Bonello2, Paola Belardi2, Vivian Tullio1, Chiara Merlino1, Nicola Carlone1 and Anna Maria Cuffini1

1Department of Public Health and Microbiology, University of Turin, Turin and 2Department of Internal Medicine, Nephrology and Dialysis Unit, Civil Hospital, Ivrea, Italy

Correspondence and offprint requests to: Prof. Cuffini Anna Maria, Department of Public Health and Microbiology, Microbiology Section, University of Turin, Via Santena 9, 10126 Turin, Italy. Email: annamaria.cuffini{at}unito.it



   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. Among patients with defects of the phagocytic component of the immune system, chronic haemodialysis patients are highly susceptible to microbial infections characterized by high morbidity/mortality, related to an impairment of the phagocytic response. Therefore the potential influence of dialysis membrane biocompatibility on the activity of polymorphonuclear (PMN) granulocytes from dialysis patients was investigated in this study.

Methods. Nineteen patients in haemodialysis were included in the protocol and divided into two groups: a control group (7 patients) and a study group (12 patients). The study group patients were treated for subsequent periods of 1 month with different dialysis membranes: low flux excebrane E membrane (CL-E), low flux polysulfone (PS). The control group patients were treated with a low flux modified cellulose membrane (SMC) for the entire observation period.

The aetiology of end-stage renal disease included glomerulonephritis, nephroangiosclerosis and interstitial nephropathy. Following each period of treatment, clinical and haematological parameters were evaluated; phagocytosis and microbicidal activity of PMNs from uraemic patients against Klebsiella pneumoniae, the pathogen which can pose severe problems in immune depressed patients, were investigated in parallel.

Results. The data evidence that both clinical and haematological parameters remained unchanged during the study period and no differences were found among treatments. On the contrary, the PMN activity varied according to the type of the membrane. In fact, the use of both PS and CL-E, in contrast to SMC, resulted in a PMN functionality similar to that observed in healthy subjects.

Conclusions. These results provide evidence that the depressed PMN activities in dialysis patients may be influenced by membrane biocompatibility in such a way to be totally restored.

Keywords: chronic renal insufficiency; dialysis membrane; human polymorphonuclear cells; intracellular killing; Klebsiella pneumoniae; phagocytosis



   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
Among patients with defects of the phagocytic component of the immune system, chronic haemodialysis patients are highly susceptible to infection characterized by high morbidity and mortality, related to an impairment of the phagocytic response. The depression of the immune response in the uraemic patient is global, and concerns both humoral and cellular sectors. Consequently, the infections are sustained not only by opportunistic microorganisms but also by common bacteria [1]. Since polymorphonuclear granulocytes (PMNs) are the first-time cells of the non-specific defence system, neutrophils' phagocytic functions have been studied extensively in patients with chronic uraemia [1–4]. Immune system dysregulation in uraemic patients may even have been accentuated by dialysis [3]. In fact, during dialysis treatment, cytokines and many other soluble uraemic toxins are not completely eliminated from being responsible for a variety of functional disturbances that contribute to an increased risk of infection by interfering with essential functions of the unspecific immune response such as chemotaxis, phagocytosis and oxidative metabolism [4]. Since the biocompatibility of the membranes might be one of the more fundamental requisites to remedy the problems related to impaired neutrophil functions, the present study was designed to evaluate the potential influence of dialysis membrane biocompatibility on the main functions of PMNs harvested from dialysis patients. The patients included in the study were treated for subsequent periods of 1 month with different dialysis membranes: a low flux modified cellulose membrane (SMC), that represents one approach to an improvement of biocompatibility of cellulose-based materials, compared with either excebrane E membrane (CL-E), a biocompatible material proposed as a novel approach to reduce the accelerated generation of reactive oxygen species that occur during haemodialysis, or a hydrophobic synthetic low flux polysulfone membrane (PS).



   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Acknowledgements
 References
 
Patients
Nineteen patients (12 males and 7 females) undergoing chronic haemodialysis at the Nephrology and Dialysis Unit of the Civil Hospital, Ivrea, Turin, Italy were randomly selected. All patients included in this study gave their informed consent. The mean age was 67 ± 12 years, and the mean time on dialysis was 52.2 ± 41 months, and the causes for renal failure were as follows: glomerulonephritis (3 cases), nephroangiosclerosis (10 cases) and interstitial nephropathy (6 cases). Patients with diabetes and recent infection episode (<6 months) were excluded.

Study design
All patients underwent haemodialysis with a SMC before the beginning of the study. These patients were randomly assigned to two groups: 7 patients to SMC-dialysis group (control group) and 12 patients to the study group. The patients from the study group were switched from the SMC to CL-E for 1 month and then immediately switched back to dialysis with SMC for 1 month. After this period, they were dialysed with low flux PS for 1 month and switched back to dialysis with SMC for 1 month. The patients from the study group were again switched from the SMC to PS for 1 month and then back to dialysis with SMC for 1 month. Then they were dialysed with CL-E for 1 month, switched back to dialysis with SMC for 1 month. This switch back to the SMC was designed to provide evidence that changes during dialysis with CL-E or PS membranes could be membrane-related, at least in variables that can be altered by 1 month of dialysis with SMC. In SMC-dialysis group (control), SMC was continued for the entire observation period.

At the beginning of the study and after each period of 1 month treatment, three groups of data were evaluated in parallel:

  1. haematological data: urea, creatinine, serum albumin, haematocrit, adequate dialysis prescription and nutrition;
  2. clinical well-being data: hypotension, nausea, itching, cramps, restlessness, hunger, sleep, strength, fit for work, thirst, sleeplessness and post-dialysis fatigue;
  3. data regarding the PMN activities: phagocytosis and microbicidal intracellular activity against Klebsiella pneumoniae.

Bacteria
A clinical isolate of K. pneumoniae was cultured on McConkey agar (Oxoid S.p.A., Garbagnate Milanese, Milan, Italy). Young colonies (18–24 h) were picked to approximately 3–4 McFarland standard and inoculated into cryovials containing both cryopreservative fluid and porous beads to allow bacteria to adhere (Microbank, Biomérieux; Rome, Italy). After inoculation, cryovials were kept at –80°C for extended storage.

PMNs
Peripheral venous blood from haemodialysis patients was collected, at the beginning of the last dialysis of the month, into sterile evacuated blood-collecting tubes containing lithium heparin (15 UI LH/ml blood) and settled at room temperature by gravity for 30 min in 2.5% dextran (70 000 molecular weight; Pharmacia S.p.A., Milan, Italy) in normal saline (1:1 ratio). The leucocyte-rich plasma supernatant was carefully layered on Ficoll-Paque (Pharmacia) and centrifuged twice at 1200 g for 15 min; to obtain pure PMNs, residual erythrocytes were lysed by hypotonic shock for 30 s in sterile distilled water and then centrifuged further [5]. After being counted in Bürker cell counting chamber (Marenfield, Germany), the density of PMNs was adjusted to 106 cells/ml in phosphate-buffered saline (PBS) supplied with 1% glucose and 1% human albumin (Sigma, St Louis, MO). The PMNs were placed in sterile plastic tubes treated with RPMI 1640 (Gibco Laboratories, Grand Island, NY), supplemented with 10% fetal calf serum (FCS; Gibco) and incubated at 37°C in a shaking water bath (150 rpm) before the addition of K. pneumoniae. The viability assayed by trypan blue exclusion before and after each experiment was >95%. The time between the collection of blood and the beginning of the experiments did not exceed 3 h. The interval between PMNs harvest and the start of experiments was less than 30 min [5].

Peripheral venous blood was pooled from seven healthy donors, negative for the presence of microbial and viral diseases (A.S.L. San Giovanni Battista Hospital, Turin, Italy), collected and processed, as described earlier, to obtain isolated PMNs.

Radioactive labelling protocol
A total of 200 µl of the frozen culture was placed into fresh Brain Heart Infusion broth (BHI; Oxoid) containing 150 µCi of 3H-uracil (specific activity, 1165.5 Gbq/mmol; NEN Products, Milan, Italy) at 37°C. The radiolabelled klebsiellae were centrifuged several times with BHI broth and resuspended in fresh medium and adjusted to yield 2 x 107 cfu/ml, as confirmed by colony counts in triplicate.

Phagocytosis assay
In all experiments, the bacterium:PMN ratio was 10:1. Aliquots of 1 ml of klebsiellae in RPMI 1640 with 10% FCS were added to PMNs in sterile plastic tubes (106 cells) and the tubes were then incubated at 37°C in a shaking water bath. After incubation for a period of 30, 60 or 90 min, the tubes were centrifuged at 1200 g for 5 min. The pellet was then resuspended in phosphate saline, and the mixture was centrifuged at 1200 g for 5 min to remove free klebsiellae. The cells were then resuspended in 1 ml of sterile distilled water for 5 min, and 100 µl samples of this suspension were placed in scintillation fluid (Atomlight, NEN) and counted by liquid scintillation spectrophotometry. Radioactivity was expressed as the counts/min/sample. The percentage of phagocytosis at a given sampling time was calculated as follows: phagocytosis (%) = (cpm in PMN pellet/cpm in total bacterial pellet)x100 [6].

Measurement of antimicrobial activity of PMNs
In all the experiments, the bacterium:PMN ratio was 10:1. Aliquots of 1 ml of klebsiellae (2 x 107 cfu) and PMNs in sterile plastic tubes (106 cells) were incubated in RPMI 1640 at 37°C in a shaking water bath for 30 min to allow phagocytosis to proceed. The PMN-bacterium mixtures were centrifuged at 1200 g for 5 min and washed with phosphate saline to remove the free extracellular bacteria. An aliquot of the cells containing bacteria was taken, and was lysed by adding sterile water, and a viable count of intracellular klebsiellae was performed (time zero). The cells were then incubated further, and at intervals (time x), the viable counts of the surviving intracellular bacteria were measured in the same way. The PMN killing values were expressed as the survival index (SI), which was calculated by adding the number of surviving microorganisms at time zero to the number of survivors at time x and dividing by the number of survivors at time zero [6,7]. According to this formula, if bacterial killing was 100% effective, the SI would be 1.

Statistical analysis
Statistical evaluation of the differences between tests and control results were performed by an analysis of variance by Tukey's test.



   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Acknowledgements
 References
 
The haematological data shown in Table 1 indicate that control patients treated with SMC presented similar values to those observed in the patients treated with CL-E and PS. In the same way, the symptoms relative to clinical well-being of the patients did not differ with the varying of the different membranes underlying a depurative equivalence (Table 2). Treatment with SMC membrane used as wash-out period between the treatments resulted in similar data to that observed in the control group.


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  		Table 1. Blood parameters in dialysis patients using dialysers with modified cellulose membrane (SMC), vitamin E-modified (CL-E) and polysulfone (PS)a

 

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  		Table 2. A scoring system (0–10) for subjective health complaints of dialysis patients using dialysers with modified cellulose membrane (SMC), vitamin E-modified (CL-E) and polysulfone (PS)a

 
In all the tests performed with the phagocytes, the viability of granulocytes remained unchanged throughout the experiments. The pattern of phagocytosis and intracellular killing against K.pneumoniae by PMNs harvested from healthy subjects is shown in Tables 3 and 4. PMNs from chronic haemodialysis control patients treated with SMC (Table 3) were able to engulf the bacteria in a range between 10.5 and 8.8% in 90 min of observation, while PMNs harvested from patients dialysed with CL-E showed a greater bacterial ingestion (16.7–9.92%). A higher phagocytic efficiency was observed in the patients after dialysis with PS membrane. In fact, the PMNs engulfed klebsiellae at a rate varying from 18.08 to 15.54% in 90 min of observation (Table 3). A considerable difference was found among the bactericidal abilities of PMNs from haemodialysed patients dialysed with the three membranes (Table 4). PMNs from control patients treated with SMC were able to kill bacteria at a rate varying from 60 to 29% in 90 min of observation, while the use of CL-E produced a significantly higher killing effect reducing the intracellular bacterial load by 88–75%. In the PMNs obtained from patients dialysed with PS, the bactericidal intracellular activity shifted from 58% at 30 min to 61% at 60 min and to 66% at 90 min, indicating a microbicidal activity approximately 2-fold of that observed in SMC control system during the last hour of incubation.


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  		Table 3. Phagocytosis of K. pneumoniae by PMNs from healthy subjects and from dialysis patients using dialysers with modified cellulose membrane (SMC), vitamin E-modified (CL-E) and polysulfone (PS)

 

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  		Table 4. Intracellular killing activity of K. pneumoniae by PMNs from healthy subjects and from dialysis patients using dialysers with modified cellulose membrane (SMC), vitamin E-modified (CL-E) and polysulfone (PS)

 
Treatment with SMC membrane used as wash-out period between the treatments resulted in a PMN functional activity similar to that observed in the control group (Tables 3 and 4).



   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Acknowledgements
 References
 
PMNs play a crucial role in host defence against microbial infections, and there is substantial clinical evidence about profound disturbances in PMN functions in patients on chronic haemodialysis [8]. In fact, impaired chemotaxis, phagocytic capacity, bactericidal activity, and metabolic dysfunction of these cells in dialysed patients have been reported [2,3,9]. Uraemia per se is a cause of some of these derangements, but nowadays blood-membrane interaction during dialysis seems to be responsible for many of these abnormalities. This is particularly true when bio-incompatible cellulose-based membranes are used [10].

Biocompatibility is an important factor that involves the entire haemodialysis treatment playing a major role in the well-being of patients and may have short-and long-term clinical implications [11]. In fact, the contact of blood components with the dialysis membrane can induce a chronic inflammatory state that is thought to adversely affect morbidity and mortality of patients on maintenance haemodialysis [12]. Some in vitro studies indicate that blood components are activated less by synthetic membranes than by membranes derived from cellulose; thus, synthetic membranes are considered to be more biocompatible than those made of cellulose [12]. At the moment there is no evidence on the effect of biocompatibility on the clinical outcome [13]. In this study the influence of membrane biocompatibility upon the functionality of PMNs, collected from hemodialysed patients treated with three different dialysis membranes, was investigated. The first membrane, SMC, is obtained by specific chemical modification, whereby aromatic benzyl groups are covalently introduced into the cellulosic structure by ether bonds, creating hydrophobic domains within the overall hydrophilic cellulose surface, resulting in minimal activation of blood complement, coagulation and cell activation systems [14,15]. The second, CL-E, consists of a multilayer cellulose membrane made by a block polymer, which masks the hydroxyl groups on cellulose, an oleyl alcohol that inhibits platelet aggregation and a vitamin E coating on the blood surface that acts like a powerful scavenger protecting plasma molecules and cell membranes from peroxidative damage [16–19]. Clinically relevant effects of the vitamin E-modified membrane include decreased platelet activation, together with the anti-apoptogenic effect of mononuclear leucocytes and inhibitory function of acute cytokine production during dialysis treatment [19]. The third membrane, PS, has been developed to reduce the ultrafiltration coefficient (Kt) maintaining an adequate permeability to medium-large solutes and a good biocompatibility in terms of minimal activation of complement, blood coagulation and cells (leucocyte, platelet and monocyte), obtained by the total absence of hydroxyl groups on the surface [19–21].

As shown by the results reported in Tables 1 and 2, the haematological data and the symptoms relative to clinical well-being of the patients did not differ at all with the varying of the three involved membranes underlying a great depurative equivalence among SMC, CL-E and PS. The phagocyte investigation shows a different picture, indicating that the PMN phagocytic activity varies according to the type of membrane used in dialysis treatment (Table 3). In fact, by using a synthetically modified cellulose membrane (SMC-dialysis control group), a diminished in vitro phagocytosis was noted compared with that seen in PMNs in patients treated with both CL-E and PS membranes. These data are in agreement with those by Vanholder et al. [22]: the authors pointed out a defect of phagocytosis in uraemic patients before dialysis, a defect that even increased during the dialysis treatment in relation to the membranes used. The influence of dialysis on phagocytosis seems to be particularly strong if complement-activating membranes are used [23]. Conflicting results have been produced recently by Anding et al. [23] who showed that dialysis does not have a significant influence on the phagocytic activity of neutrophils, confirming what was previously stated by other authors [1,24,25]: no impairment of phagocytic activity by uraemia compared with that observed in healthy subjects [23].

Since a functional impairment of PMN functions in uraemia is believed to increase the susceptibility to infections, the most interesting result of our investigation is represented by the data obtained with the synthetic membrane, polysulfone. PS induces a great enhancement of the phagocytic response in PMNs from uraemic patients that results in a totally restored functionality with a pattern similar to that observed in PMNs from healthy subjects (Table 3). These results are probably correlated with both high biocompatibility and flux properties of this dialysis membrane that allow the removal of a great number of uraemic toxins from plasma.

Some literature studies [23] report that uraemic patients have a significantly lower antimicrobial killing activity compared with that of healthy subjects while, after the dialytic treatment, they show a slightly improved intracellular killing (10–15%), supporting the hypothesis that factors altering the microbial killing can be partially removed by dialysis [4,8]. According to Anding et al. [23], our results demonstrate that dialysis with PS membrane enhances the microbicidal activity of phagocytes resulting in killing values that are significantly greater than those observed either from control patients treated with SMC or from the healthy subjects (Table 4), confirming the PS capability of removing from the plasma some of the uraemic toxins responsible for the functional defects of phagocytes like GIP I and GIP II [4,8,26].

Moreover, a beneficial effect of dialysis vitamin-E coated membrane has been detected by our study (Table 4): this membrane is able to completely restore the functionality of the granulocytes that kill the bacteria in a percentage even greater (88–75%) than that observed in healthy controls (64–41%; Table 4). Such enhancement is probably related to the anti-oxidant properties of vitamin E that preserve the PMN capacity to produce oxygen radicals, confirming the literature data [27–29]. On the contrary, in control patients treated with SMC, we did not observe any increase in bacterial killing, probably related to SMC inability to remove solutes with high molecular weight like the proteins that inhibit granulocyte functionality. Moreover, the treatment with SMC membrane, used as wash-out period between the treatments, resulted in a PMN functional activity similar to that observed in the control SMC-dialysis group (Tables 3 and 4), providing strong evidence that changes during dialysis with CL-E or PS membranes were membrane-related.

In conclusion, this study demonstrates that switching from a cellulose dialysis membrane to the one made of PS or the one modified with vitamin E during the treatment of chronic haemodialysis patients leads to a great improvement of phagocytic functionality. These results provide evidence that the depressed PMN activities in dialysis patients may be influenced by membrane biocompatibility in such a way to be totally restored. To confirm the benefit of the therapy based on biocompatible dialysis membranes, further experiments including either a greater sample size or a long-term CL-E and PS dialysis treatment period are actually ongoing.



   Acknowledgements
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
References
 
The authors are grateful to the participants in the study and to the staff of Nephrology and Dialysis Unit. Supported by grants from the Italian MURST (Ministero dell’Università e della Ricerca Scientifica) and the Regione Piemonte, Ricerca Scientifica Applicata 2004.

Conflict of interest statement. None declared.



   Notes
 
* This study was presented in part at the ASN meeting, October 27–November 1 2004, St Louis, MO, USA. Back



   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 

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  2. Marewska E, Baj Z, Sulowska Z, et al. (2003) Effects of uraemia and haemodialysis on neutrophil apoptosis and expression of apoptosis-related proteins. Nephrol Dial Transplant 18:2582–2588.[Abstract/Free Full Text]
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Received for publication: 12. 4.06
Accepted in revised form: 13. 6.06


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