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Perit Dial Int 29(2): 171-177
2009
© 2009 International Society for Peritoneal Dialysis
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Clinical

OXIDATIVE STRESS IN CHILDREN ON PERITONEAL DIALYSIS

Danuta Zwolinska1, Wladyslaw Grzeszczak2, Maria Szczepanska3, Irena Makulska1, Katarzyna Kilis–Pstrusinska1 and Krystyna Szprynger3

Department of Paediatric Nephrology,1 Wroclaw Medical University, Wroclaw; Department of Internal Medicine, Diabetology and Nephrology2 ; Dialysis Division for Children,3 Department and Clinic of Pediatrics, Medical University of Silesia, Zabrze, Poland

Correspondence to: D. Zwolinska, Department of Paediatric Nephrology, Wroclaw Medical University, ul. M. Sklodowskiej-Curie 50/52, 50-369 Wroclaw, Poland. nefped{at}nefped.am.wroc.pl


   ABSTRACT
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 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURE
 REFERENCES
 

{diamondsuit} Objectives: Enhanced oxidative stress has been observed in dialysis and predialysis adult patients with chronic kidney disease (CKD), which resulted in increased mortality and morbidity within this population. Not much attention in the literature has been paid to nonenzymatic antioxidant defense in children with CKD on peritoneal dialysis (PD). The aim of the present study was to describe the plasma, erythrocyte, and dialysate concentrations of oxidized (GSSG) and reduced glutathione (GSH) and vitamins A, E, and C in a pediatric PD population.

{diamondsuit} Patients: 10 children on PD and 27 age-matched healthy subjects were enrolled in the study.

{diamondsuit} Results: Erythrocyte and plasma GSH concentrations were lower in PD patients, erythrocyte concentration of GSSG remained unchanged, and plasma GSSG was significantly higher in children on PD. Children on PD exhibited decreased plasma concentrations of antioxidant vitamins compared to healthy subjects. Moreover, we documented loss of vitamins A, E, and C into ultrafiltrate.

{diamondsuit} Conclusion: Such low plasma levels of vitamins A, E, and C and simultaneously decreased activity of erythrocyte GSH may be responsible for the increased oxidative stress occurring in children with CKD on PD.

KEY WORDS: Chronic kidney disease in children; antioxidant defense; reduced glutathione (GSH); oxidized glutathione (GSSG); vitamins A, E, C.

Patients with chronic kidney disease (CKD), both adults and children, suffer from numerous complications that increase morbidity and mortality within this population. Recent studies emphasized the role of reactive oxygen species and/or decreased activity of enzymatic and nonenzymatic antioxidant systems in the development of cardiovascular and cerebrovascular diseases. Accelerated ageing, atherosclerotic plaque formation, cataracts, β2-microglobulin arthropathy, reduction of erythrocyte wall deformability, and platelet dysfunction also result from increased oxidative stress (1–8). Neutrophils from patients with CKD produce an increased amount of reactive oxygen species that could diffuse and interact with other molecules, for example, membrane lipids and proteins. Various studies have shown that increased oxidative stress may be related to uremia per se and/or, in some aspects, to the influence of materials of the extracorporeal circuit or dialysis solutions, and chronic inflammatory activity of dialyzed patients, both adults and children (6,8–13). Ece et al. concluded that increased oxidative stress and inflammation, together with early cardiovascular alterations, were present in children with CKD, including children on peritoneal dialysis (PD) (7).

Peritoneal dialysis is an effective renal replacement therapy equal to hemodialysis (HD). It is suitable as the first method of renal replacement therapy treatment (14,15). Peritoneal dialysis is the method of choice especially in young infants and children before they will be ready to undergo transplantation. However, PD is not a completely harmless treatment. The study by Noh et al. suggested that reactive oxygen species generated during exposure to high glucose concentration fluids, angiotensin II, or glucose degradation end products may be responsible for membrane hyperpermeability, neoangiogenesis, extracellular matrix accumulation, and, finally, peritoneal fibrosis. They underlined the roles of antioxidants and angiotensin II receptor blockers in better preservation of the structural integrity and function of the peritoneal membrane during long-term PD (16). Gotloib et al. raised critical doubts about icodextrin and high glucose content solutions and their influence on lipid peroxidation contributing to destruction of the peritoneal mesothelial layer. Oxidative injury, they postulated, is linked to lipid components of the mesothelial cell membrane (17).

In our previous study, increased lipid peroxidation and highly reduced activity of antioxidant enzymes in children on PD was found (5). However, not much attention in the literature has been paid to nonenzymatic antioxidant defense in this group of patients (18,19).

The present study was designed to test the hypothesis that plasma vitamins A, E, and C and erythrocyte glutathione levels might be responsible for the increased oxidative stress occurring in children with CKD on PD. Therefore, we aimed to determine in a pediatric PD population the plasma and erythrocyte concentrations of oxidized (GSSG) and reduced glutathione (GSH); plasma, erythrocyte, and dialysate levels of vitamins A and E; and plasma and dialysate levels of vitamin C. To our best knowledge, this study is the first on the activity of vitamins as part of the antioxidant system in children on PD.


   PATIENTS AND METHODS
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 PATIENTS AND METHODS
RESULTS
 DISCUSSION
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Ten children on PD (PD group) participated in the study. The control group consisted of 27 healthy age-matched children admitted for elective surgery or a routine check-up. None of the patients or controls received drugs having potential oxidant properties. Patients with current infection, vasculitides, or hepatic or respiratory disease were not included. Current infection was defined as clinical acute respiratory disorder, urinary tract infection (the most common acute infection in children) with high leukocytosis, or increased C-reactive protein. Children were excluded from the evaluation if they had such acute disease less than 1 month prior to blood sampling. Vasculitides were excluded by serological examination (the absence of pANCA, cANCA). Clinical and demographic details about the study subjects are provided in Table 1. The causes of CKD in the PD group were chronic glomerulonephritis (n = 3), amyloidosis in the course of juvenile rheumatoid arthritis (n = 2), chronic pyelonephritis (n = 2), polycystic kidney disease (n = 1), cortical necrosis (n = 1), and unknown (n = 1). Informed consent for participation in this study was obtained from the parents of all children. The study protocol was approved by Ethics Committee of Wroclaw Medical University.


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  		TABLE 1 Clinical Characteristics of Study Subjects

 

Blood samples obtained after an overnight fast from the healthy subjects and children on PD were taken from the antecubital vein into heparinized tubes. Dialysis fluid was also examined. Erythrocytes from blood samples were separated from plasma by centrifugation, washed twice with buffered physiological saline solution, and hemolyzed. Plasma and dialysate fluid samples were stored at –80°C until analysis. This study was conducted on the same pediatric population as we previously described for enzymatic antioxidant concentrations in erythrocytes and plasma (5), and the measurements were performed simultaneously. Samples were not refrozen for these additional measurements.

Plasma, dialysate, and erythrocyte vitamin A and E levels were determined by HPLC analysis according to Thurnham et al. (20), which concerns lipid ratios for measurement of vitamin E status. The results in plasma and dialysis fluid are expressed in micromoles per liter, and in erythrocytes as nanograms per milligram protein. Vitamin C was assayed in plasma and dialysis fluid by HPLC analysis according to Leavelle (21) and expressed in micromoles per liter. Oxidized glutathione (glutathione disulfide; GSSG) was measured according to Adams et al. (22) using the modification by Abdalla et al. (23). The method concerns determination of GSSG, which remains unchanged and is not metabolized after the addition of N-ethylmaleimide. The results in plasma and suspended hemolyzed erythrocytes are expressed in micrograms per milliliter. Reduced glutathione (GSH) was assayed according to Ellman et al. (24) using classic spectrophotometry with measurement of absorbance at 240 nm after the addition of DTNB [5,5-dithiobis-(2-nitrobenzoic acid)] solution; the results are expressed in micrograms per milliliter. Serum urea, creatinine, cholesterol, and triglycerides were determined by standard laboratory methods using an AutoAnalyzer (Technicon RA-1000; now Seal Analytical, Burgess Hill, West Sussex, United Kingdom).

STATISTICAL ANALYSIS
Data are expressed as mean ± standard deviation (SD). Nonparametric Mann–Whitney test was used to compare differences between the study groups because of the abnormal distribution of the variables examined. Spearman's correlation was used to analyze correlations between various parameters. A p value < 0.05 was considered significant. The analysis was performed using the statistical package Statistica 6.0 (StatSoft Polska, Kraków, Poland).


   RESULTS
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DISCUSSION
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The details concerning plasma, erythrocyte, and dialysate concentrations of vitamins A, E, and C are shown in Table 2. Plasma levels of vitamins A, E, and C and erythrocyte vitamin E levels were significantly decreased in the PD group compared to controls. Erythrocyte vitamin A levels in children on PD were not different from the levels observed in the healthy children. A significant loss of vitamins E and C and only a minor concentration (< 0.05 µmol/L) of vitamin A in ultrafiltered dialysate were found. The concentration of glucose had no influence on the elimination of vitamins A, E, and C. Erythrocyte and plasma GSH concentrations in children on PD were significantly lower, whereas plasma GSSG level was tenfold higher than in the control group (Table 3). The erythrocyte GSSG/GSH ratio was also increased in the PD group.


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  		TABLE 2 Vitamin A, Vitamin E, and Vitamin C Concentrations in Study Subjects

 

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  		TABLE 3 Plasma and Erythrocyte Concentrations of Reduced (GSH) and Oxidized (GSSG) Glutathione in Study Subjects

 

The significant positive correlations of plasma vitamin E level with erythrocyte vitamin A level, as well as of plasma vitamin C level with erythrocyte GSH level, were recorded (r = 0.6851, p < 0.05 and r = 0.6572, p < 0.05, respectively). The inverse correlations of plasma vitamin E level with erythrocyte and plasma GSSG levels were also significant (r = –0.8049, p < 0.05 and r = –0.6834, p < 0.05, respectively). Plasma BUN showed positive correlations with dialysate vitamin A level (r = 0.7314, p < 0.05) and plasma GSSG level (r = 0.8293, p < 0.05).


   DISCUSSION
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Decreased effectiveness of the intracellular and plasma enzymatic and nonenzymatic antioxidant protection systems contribute to increased oxidative stress (25,26). Superoxide dismutase is the first line of the intracellular antioxidant system (27). Vitamin E, together with the selenium-dependent glutathione peroxidase (GSH-Px) and catalase, creates the second line, which ceases the chain of free radical generation in the stadium of propagation (28). The results of our previous study conducted in the same group of children on PD showed increased levels of lipid peroxidation markers in plasma and erythrocytes compared to healthy controls: mean erythrocyte malondialdehyde (MDA) 11.3 vs 5.9 nmol/mL, plasma MDA 4.6 vs 2.3 nmol/mL, organic hydroperoxide (OHP) 1.75 vs 0.65 µmol/L. The plasma OHP concentrations significantly correlated with serum creatinine concentration (r = 0.6638, p < 0.03) as well as superoxide dismutase (r = 0.8971, p < 0.03) activity in children on PD. We also found a reduction in antioxidant enzymes (superoxide dismutase, GSH-Px, catalase) in the erythrocytes of children on PD (5). Our data are in accordance with Ece et al.'s observation in children on PD: they described significantly increased levels of MDA and decreased concentrations of superoxide dismutase, catalase, and GSH (7). They additionally showed that markers of inflammation (C-reactive protein, proinflammatory cytokines) positively correlated with markers of oxidative stress in follow-up measurements in a pediatric CKD population.

The most active antioxidant of nonenzymatic origin is GSH, which is the scavenger for H2O2, OH– ions, and chlorinated oxidants (28). Reduced glutathione is a low molecular thiol (SH) involved as substrate for GSH-Px, which generally prevents protein SH groups from oxidation and cross-linkage (29). In our study, children on PD showed lower values of erythrocyte and plasma GSH than controls. We noted a simultaneous increase in plasma GSSG. The concentration of GSSG in erythrocytes was higher as well, but was not different compared to control children. The GSSG/GSH ratio is regarded as an excellent index of glutathione stability. This erythrocyte glutathione redox ratio reached a high value in children on PD in comparison to healthy subjects. However, other authors that conducted studies on adult patients on maintenance dialysis had opposite results. Lucchi et al. measured erythrocyte GSH content and showed that transplanted and PD patients had values similar to controls, and significantly lower values compared to HD patients (30). Normal GSH levels were also documented by Chu et al. (31). In the only manuscript regarding children on maintenance HD, by Turi et al., decreased levels of erythrocyte GSH and increased levels of erythrocyte GSSG were also documented, similar to our population on PD, but without any significant difference compared to healthy children (18). Reduced erythrocyte levels of GSH and enhanced GSSG/GSH ratio may be responsible for increased lipid peroxidation. The positive correlation between erythrocyte GSH and plasma vitamin C levels suggests that simultaneous reduction of different antioxidants may contribute to deleterious processes of lipid and protein peroxidation. This could play a role in enhanced endothelial dysfunction due to altered scavenging of two-electron non-radical reactive species (32).

Confirmation of this hypothesis comes from the experimental study by Styszynski et al. on rats (33). They supplemented dialysis fluid with L-2-oxothiazolidine-4-carboxylate — a substance with characteristics of a glutathione precursor compound — and found increased GSH-Px activity and preserved peritoneal morphology and function of mesothelial cells during PD (33).

The cause of GSH reduction is multifactorial. Diminished synthesis and/or disturbed regeneration from oxidized compound is the result of pentose cycle disturbances with low levels of NADPH, which are necessary for glutathione reduction. Uremic toxins and enzyme proteins could provoke such disorders. On the other hand, diminished GSH concentration depends on low activity of glucose-6-phosphate dehydrogenase and diffusion of GSSG to plasma through the erythrocyte membrane (34–36).

Vitamins A, E, and C play important roles in the nonenzymatic antioxidant system. Vitamin C also prevents lipid peroxidation and protein and nucleic acid oxidation (37).

Our study showed decreased erythrocyte and plasma levels of vitamin E in the PD patients compared to controls, with a negative correlation with GSSG levels. In our previous study, we showed that erythrocyte vitamin E concentration was also decreased in hemodialyzed children compared to healthy controls (38). Reduced concentration could be the result of this vitamin utilization in processes of free radical generation, which is intensified in uremia. Another cause is continuous loss of vitamin E in ultrafiltrate: we found significant amounts of vitamin E into dialysis fluid.

In an experimental study, Kir et al. documented that parenteral vitamin E administration in rats may partially protect kidney tissue from injury by its action as a free-radical scavenger (39). Several medications have been tested to decrease oxidative stress in patients with CKD. Taccone–Gallucci et al. documented the favorable effect of vitamin E administration to decrease MDA levels in erythrocytes in adult patients with CKD (40). Tam et al. found that combined use of vitamin E and vitamin C in adult patients with systemic lupus erythematosus resulted in a significant decrease in plasma MDA levels (41). Akiyama et al. and Mydlik et al. showed beneficial effects of both vitamin E supplementation and the use of a vitamin E-coated membrane dialyzer on HD-induced oxidative stress (42,43).

Our results showing profound vitamin E deficiency suggest the need for regular oral vitamin E supplementation in pediatric PD patients. Zaniew et al. indicated that successful intervention with antioxidant therapy by administration of vitamin E and N-acetylcysteine orally is also possible in children. After 6 months of such supplementation, they reduced the intracellular oxidative stress measured in peripheral blood lymphocytes in a pilot group of children on PD or HD (19).

In our study, we documented decreased plasma concentration of vitamin C in children on PD. Data obtained in adult patients are in line with this observation (11,44,45). The main cause of reduced plasma vitamin C levels in CKD is inadequate daily intake due to anorexia and dietary restriction with a low potassium diet (46). Loss into dialysis fluid also cannot be neglected, as shown in our study. Supplementation of vitamin C is usually restricted to 60 – 100 mg/day because it is partly metabolized to oxalate, which can accumulate in CKD patients (47,48). However, further studies are needed in children on PD to determine the correct dose for maintaining more efficient erythropoiesis.

We also revealed decreased plasma levels of vitamin A in children on PD, but erythrocyte vitamin A levels in these children were comparable to healthy controls. The causes of reduced plasma vitamin A levels in the examined children could be multifactorial. The lowering of plasma vitamin A levels is probably the result of the shift of this vitamin into erythrocytes. It has been documented that, in healthy children, the concentration of retinol-binding protein is lower by 40% compared to adults, and this results in diminished liver sources of vitamin A. Altered appetite and malabsorption may lead to further reduction in the plasma concentration of this vitamin (49). Moreover, we documented the loss of vitamin A into ultrafiltrate.

In summary, our results show diminished antioxidant nonenzymatic defense in children on maintenance PD. Lower values of erythrocyte and plasma GSH, with an elevated GSSG/GSH ratio, confirm the instability of the glutathione system. Decreased plasma concentrations of antioxidant vitamins have been detected in children on PD. The most profound reduction was observed in plasma levels of vitamin E. Studies evaluating the safety, tolerability, and efficacy of vitamin E supplementation as an antioxidant therapy in children on PD are still needed. Low levels of plasma vitamins A, E, and C, with reduced activity of erythrocyte GSH, might be responsible for increased oxidative stress occurring in children with CKD on PD.


   DISCLOSURE
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 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURE
REFERENCES
 
The authors declare that no financial conflict of interest exists.

Received 12 September 2007; accepted 25 May 2008.


   REFERENCES
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 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
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