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Evaluation of Thyroid Functions, Oxidative Stress and Antioxidants in Egyptian Children with Nephrotic Syndrome



Saad Mohamed, Mohamed Zannoun, Ahmad El-Askary, Mohamed Abdel-aal and Yasser Abdelrahman
 
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ABSTRACT

Background: Nephrotic Syndrome (NS) is characterized by heavy proteinuria that leads to loss of significant amounts of thyroid hormones. Reactive Oxygen Species (ROS) seem to play an important role in the etiopathogenesis of protienuria in nephrotic syndrome. Objective: Evaluation of thyroid functions, oxidative stress and antioxidants in children with nephrotic syndrome. Materials and Methods: The present study was carried out at Al-Azhar University Hospital, Damietta during the period from March, 2015 to February, 2016. The study included 30 Egyptian children with steroid responsive nephrotic syndrome in relapsing phase and remission phase (Cases) and other 30 healthy Egyptian children (Control group). Venous blood was collected for the estimation of SOD activity, MDA, glutathione-S-transferase (GST) and estimation of thyroid hormones FT3, FT4 and TSH. Results: Serum FT3 and FT4 was significantly lower in patients with relapse (2.84±0.74 and 3.14±1.34, respectively) in comparison to remission (8.1±2.64 and 16.75±3.69, respectively) and control group (8.97±1.95 and 18.34±4.68, respectively). However, there was significant increase of TSH in patients with relapse (6.7±2.4) in comparison to remission (2.6±1.8) and control group (2.4±1.2). The SOD and glutathione-S-transferase levels were significantly decreased in patients with relapse (5.24±2.17 and 2.14±1.27, respectively) in comparison to remission (7.14±1.68 and 3.15±0.96, respectively) and control group (7.69±2.43 and 3.54±1.83, respectively). However, there was significant increase in MDA levels in patients with relapse (8.4±2.74) in comparison to remission (2.1±1.22) and control group (1.8±0.86 ). Conclusion: Nephrotic syndrome can loss significant amounts of thyroid hormones along with protein in urine. Increased Reactive Oxygen Species (ROS) as MDA and decreased antioxidants as SOD and GST may be related to the pathogenesis of proteinuria in NS.

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  How to cite this article:

Saad Mohamed, Mohamed Zannoun, Ahmad El-Askary, Mohamed Abdel-aal and Yasser Abdelrahman, 2016. Evaluation of Thyroid Functions, Oxidative Stress and Antioxidants in Egyptian Children with Nephrotic Syndrome. Kidney Research Journal, 6: 9-14.

DOI: 10.3923/krj.2016.9.14

URL: https://scialert.net/abstract/?doi=krj.2016.9.14
 
Received: June 14, 2016; Accepted: July 30, 2016; Published: April 27, 2019



INTRODUCTION

Nephrotic syndrome which is more common in children is characterized by heavy proteinuria, hyperlipidemia, hypoalbuminemia and peripheral edema. Idiopathic Nephrotic Syndrome (INS) is one of the most common renal problems in children1,2.

Nephrotic syndrome results in loss of plasma proteins and various other macromolecules in the urine leading to their deficiencies. Many of the physiologically important molecules which exist in the plasma, bound to plasma proteins are also carried away and lost in urine. The common abnormalities arising as a result of heavy proteinuria include hypothyroidism, vitamin D deficiency and iron deficiency3-5.

Thyroid hormones (THs) are essential for normal metabolic functions of the kidneys. Thyroid dysfunction causes remarkable changes in glomerular and tubular functions, electrolytes and water homeostasis. The decrease in thyroid hormones was often attributed to the urinary loss of Thyroid Binding Globulin (TBG) as a result of proteinuria6,7.

Albumin is a non-enzymatic protein antioxidant that inhibits LDL peroxidation in vitro8. Oxidative damage has been proposed as one of the possible mechanisms involved in the NS9.

Oxidative damage by free radicals has been implicated in a number of clinical disorders including renal injury. Reactive Oxygen Species (ROS) promote cell injury by lipid peroxidation which disrupts the structural integrity of the tubular epithelial cells and increase glomerular permeability to proteins along with alteration of glomerular hemodynamics10,11.

The NS is a consequence of an imbalance between oxidants and antioxidants activity. It was observed that superoxide mediated oxidative injury degrades the glomerular basement membrane and reduces de novo synthesis of proteoglycans that affects the glomerular permeability12.

This study suggests that nephrotic syndrome patients may benefit from antioxidant therapy along with thyroid hormone supplement13.

Therefore, malondialdehyde (MDA) and nitric oxide indicate the extent of lipid peroxidation caused by reactive oxygen species while, SOD, vitamin E, albumin, uric acid bilirubin and total antioxidant capacity determines antioxidant status of body14,15.

Cellular defense mechanisms against ROS including enzymatic systems such as superoxide dismutase (SOD), catalase, glutathione peroxidase (GPx) and non-enzymatic antioxidant defense system containing albumin, reduced glutathione, uric acid, vitamin C, vitamin E, selenium and zinc16. Antioxidants prevent the production of reactive oxygen substances so, they can play a major role in decreasing the injury in nephrotic syndrome17.

In general, the molecular mechanisms behind acquired NS remain largely unknown. In addition, there is controversy regarding thyroid function among children with nephrotic syndrome and there is lack of studies among Egyptian children. The present study was designed to evaluate the possible role of oxidative stress and its relation to response to treatment and correlation with thyroid function.

MATERIALS AND METHODS

The present study was carried out at Al-Azhar University Hospital, Damietta from March, 2015 to February, 2016. An informed consent from the parents of children had been performed. The study included 30 children with steroid responsive nephrotic syndrome in relapsing phase and remission phase (Cases) and other 30 healthy children (Control group).

All children evaluated for:

Complete clinical examination
Diagnosis of nephrotic syndrome in relapsing phase by proteinuria (24 h urine protein>150 mg) hypoalbunimia (<2.5 mg dL–1) hyperlipidemia and edema and were carried out by auto-analyzer using commercially available kits. Children were said to be in remission phase when there was no proteinuria or trace (24 h urine protein<150 mg dL–1) for 3 consecutive days and no edema
Renal function tests as blood urea and serum creatinine
Thyroid function tests (a) Free tri-iodothyronine (FT3), (b) Free thyroxine (FT4) and (c) Thyroid-stimulating hormone (TSH) using Immulite (REF:030001-04) and laboratory equipment manufactured by Siemens
Estimation of oxidative stress (Malondialdehyde content) the end product of the free radicals initiating lipid peroxidation was measured by using thiobarbituric acid reactivity as described by Uchiyama and Mihara18. Estimation of antioxidants as superoxide dismutase (SOD) was measured by the method of Marklund and Marklund19. Glutathione-S-transferase (GST) activity was measured according to the method defined by Habig et al.20 under standard conditions, the amount of enzyme conjugating 1 μmol of 1-chloro-2,4-dinitrobenzene (CDNB) with glutathione (GSH) in 1 min was defined as 1 unit activity (μmol L‾1). All the parameters of oxidative stress were spectrophotometrically analyzed using the biochemical analyzer manufactured by (ERMA INC. Tokyo, JAPAN, model: AE-600N).

About 10 mL of venous blood was collected of which 4-5 mL was poured into sterile bulb containing heparin for the estimation of SOD activity and GST21. Remaining blood was taken into sterile plain bulb for estimation of MDA22, total protein or albumin23, uric acid and creatinine24, cholesterol and triglycerides25.

Exclusion criteria: Patients with steroid resistant with atypical presentation (Age<2 years and >8 years, hematuria, hypertension and abnormal renal function test), patients with obesity and patients on drugs such as vitamins and minerals that alters the oxidative stress parameters.

Statistical analysis: The numerical (quantitative) collected data were presented as Mean±Standard Deviations (SD). On the other hand, categorical data were presented as relative frequency and percent distributions. Unpaired student (t) test was used for comparison between two means and chi-square (χ2) was used for comparison between two categorical variables. The p-value≤0.05 was considered significant for interpretation of results.

RESULTS

Age and sex distribution of cases and control group were presented in Table 1, there were non-significant difference between cases and control group with regards to the age (p = 0.70 ) and sex (p = 0.77).

Regarding biochemical parameters of cases and control group were presented in Table 2, the levels of serum total protein and albumin were significantly lower in cases with relapse (3.92±0.90 and 2.10±0.42, respectively) in comparison with cases in remission (6.22±0.71 and 4.63±0.54, respectively) and control group (6.75±1.3 and 4.91±0.58, respectively) while, the levels of cholesterol and triglyceride were significantly higher in cases with relapse (489.23±65.24 and 182.39±49.31, respectively) in comparison with cases in remission (204.28±76.54 and 89.28±31.25, respectively ) and control group (158.21±84.46 and 83.14±29.64, respectively). As regarding proteinuria there was significant increase in cases with relapse (3500±1149) in comparison with cases in remission (145±66) and control group (103±29). However, non-significant difference was observed in remission cases and control group regarding total protein, serum albumin, cholesterol, triglyceride and proteinuria. On other hand, non-significant difference was observed between the three groups regarding BUN and creatinine.

Regarding thyroid hormones levels there was significant increase in TSH level in cases with relapse (6.7±2.4) in comparison with cases in remission (2.6±1.8) and control group (2.4±1.2). While, there was significant decrease in FT3 and FT4 levels in cases with relapse (2.84±0.74 and 3.14±1.34, respectively) in comparison with cases in remission (8.1±2.64 and 16.75±3.69, respectively) and control group (8.97±1.95 and 18.34±4.68, respectively). But, there was non-significant difference between cases in remission and control group regarding TSH, FT3 and FT4 (Table 3).

Regarding parameters of oxidative stress and antioxidant there was significant increase in (MDA) in cases with relapse (8.4±2.74) in comparison with cases in remission (2.1±1.22) and control group (1.8±0.86). On other hand, there was significant decrease in SOD and GST in cases with relapse (5.24±2.17 and 2.14±1.27, respectively) in comparison with cases in remission (7.14±1.68 and 3.15±0.96, respectively) and control group (7.69±2.43 and 3.54±1.83, respectively).

Table 1:Age and sex distribution of cases and control groups
Independent sample t-test was performed at 5% level of significance

Table 2:Biochemical parameters of cases and control groups
ANOVA test was performed at 5% level of significance and *Significant difference from relapsing group

Table 3:Thyroid hormone levels in cases and control groups
ANOVA test was performed at 5% level of significance and *Significant difference from relapsing group

Table 4:Parameters of oxidative stress and antioxidants in cases and control groups
ANOVA test was performed at 5% level of significance and *Significant difference from relapsing group

Table 5:Correlation between thyroid function tests and parameters of oxidative stress
Pearson’s correlation coefficient was performed, MDA: Malondialdehyde, SOD: Superoxide dimutase and GST: Glutathione-S-trandferase

But there was non-significant difference between cases in remission and control group regarding MDA, SOD and GST levels (Table 4).

Table 5 shows MDA levels have significantly negative correlation with FT4 and FT3 but have significantly positive correlation with TSH. On other hand, SOD and GST levels have significantly positive correlation with FT4 and FT3 but have significantly negative correlation with TSH.

DISCUSSION

Nephrotic Syndrome (NS) is a common disorder characterized by alteration of permeability of the glomerular capillary wall, resulting in its inability to restrict the urinary loss of proteins with hypoalbuminemia and hyperlipidemia associated with peripheral edema26,27.

Hypoalbuminemia in NS is due to increased glomerular permeability leading to proteinuria. Infact, this molecule may represent the major circulating antioxidant in plasma known to be exposed to continuous oxidative stress28,29.

The present study was designed to evaluate thyroid function, oxidative stress and antioxidant in children with nephrotic syndrome. The results of the study revealed that the levels of serum total protein and albumin were significantly lower in cases with relapse in comparison with cases in remission and control group while, the levels of cholesterol and triglyceride were significantly higher in cases with relapse in comparison with cases in remission and control group such as regarding proteinuria there was significant increase in cases with relapse in comparison with cases in remission and control group. However, non-significant difference was observed in remission cases and control group regarding serum total protein, albumin, cholesterol, triglyceride and proteinuria. On other hand, non-significant difference was observed between the three groups regarding BUN and creatinine. This was in agreement with study inducted by Kharb14 who shows that cholesterol and triglyceride levels were significantly increase in study group of nephrotic syndrome.

In the present study, the findings of low levels of thyroxin with high levels of TSH in cases with relapsing suggest that a state of primary biochemical hypothyroidism exists in relapsing nephrotic children. This was in agreement with the study conducted by Feinstein et al.30 who showed that the reduced serum levels of FT4 and FT3 in patients with NS may be due to decreased binding to and concentration of serum carrier proteins. The NS in relapse results in loss of plasma proteins and various other macromolecules in the urine leading to their deficiencies.

Gilles et al.5 reported that abnormalities in thyroid function are seen in patients with proteinuria. Specifically, TSH levels were higher in patients with proteinuric renal diseases when compared with controls. These results indicating that nephrotic syndrome increases L-thyroxine requirements because of urinary loss of free and protein-bound thyroid hormones which might leads to clinical hypothyroid state and need for L-thyroxine supplementation. Thus, it is important to monitor clinical symptoms and signs of thyroid dysfunction in children with NS.

Antioxidants may play an important preventive role in nephrotic syndrome and its progression by decreasing the free oxygen radicals. Consequently, hyperlipidemia that increases the lipid oxidation reactions and decreases the antioxidant status may lead to glomerulosclerosis and progression of glomerular damage in nephrotic syndrome31.

In the present study, there was significantly increase in MDA in cases with relapse in comparison with cases in remission and control group which agree with studies of other researchers, where there has been an increase in the concentrations of MDA in nephrotic syndrome8.

There was a significant elevation in the levels of serum MDA in NS. Since, reactive oxygen species can be involved in many degradative processes including lipid peroxidation and increased generation of reactive oxygen species in glomerular basement membrane9.

Lipids are the target molecules for free radicals and this is probably a result of increased consumption of antioxidant components such as erythrocyte-SOD. In the present study, reduction in erythrocyte-SOD activity reflects increased susceptibility of RBC membrane to lipid peroxidation32.

In the present study, there was significant decrease in SOD in cases with relapse in comparison with cases in remission and control group and this was in agreement with the study conducted by Noyan et al.33 who showed that the decreased SOD concentrations have also been observed in nephrotic syndrome.

Zachwieja et al.34 studied the total antioxidant status and mean antioxidant activity in 82 children with nephrotic syndrome of 4-16 years. The study suggested that reduced antioxidant activity in nephrotic syndrome may be related to lipid abnormalities34.

The GSH is a substrate for antioxidant enzymes like glutathione peroxidase (GPx), glutathione-S-transferase (GST) and glutathione reductase (GRx). The decrease in the concentrations may be due to the increased turnover of GSH in preventing oxidative damage in these cases35.

In the present study, there was significant decrease in GST in cases with relapse in comparison in cases in remission and control group, similar studies of lowered GSH concentrations in nephrotic syndrome have been reported earlier36,37 suggesting increased oxidative stress in nephrotic syndrome.

Another study estimated the antioxidant status and reliable factor involved in antioxidant protection in children with nephrotic syndrome. The study suggested an increase in lipid peroxidation and insufficient antioxidant defense in nephrotic syndrome9.

The MDA levels have significantly negative correlation with FT4 and FT3 but have significantly positive correlation with TSH. On other hand, SOD and GST levels have significantly positive correlation with FT4 and FT3 but have significantly negative correlation with TSH and similar study conducted by Sawant et al.38.

The present study confirmed the previous reports regarding the decline of thyroid function in children with NS among Egyptian children. In addition, it highlighted the possible role of oxidative stress and deficiency of antioxidants in the etio-pathogenesis of NS. Furthermore, studies evaluating the effect of antioxidant supplementation is necessary to evaluate the effect on the course and prognosis of NS.

CONCLUSION

Nephrotic patients can loss significant amounts of thyroid hormones along with protein in urine. Increased Reactive Oxygen Species (ROS) and decreased antioxidants defense may be related to the pathogenesis of proteinuria in NS.

The NS is a consequence of an imbalance between oxidants as MDA and antioxidants activity as SOD and GST.

The findings of this study suggests that nephrotic syndrome patients may benefit from antioxidant therapy along with thyroid hormones supplement.

REFERENCES
1:  Tesar, V. and T. Zima, 2008. Recent progress in the pathogenesis of nephrotic proteinuria. Crit. Rev. Clin. Lab. Sci., 45: 139-220.
CrossRef  |  Direct Link  |  

2:  Gipson, D.S., S.F. Massengill, L. Yao, S. Nagaraj and W.E. Smoyer et al., 2009. Management of childhood onset nephrotic syndrome. Pediatrics, 124: 747-757.
Direct Link  |  

3:  Afroz, S., A.H. Khan and D.K. Roy, 2011. Thyroid function in children with nephrotic syndrome. Mymensingh Med. J., 20: 407-411.
PubMed  |  Direct Link  |  

4:  Dagan, A., R. Cleper, I. Krause, D. Blumenthal and M. Davidovits, 2012. Hypothyroidism in children with steroid-resistant nephrotic syndrome. Nephrol. Dial. Transplant., 27: 2171-2175.
CrossRef  |  Direct Link  |  

5:  Gilles, R., M. den Heijer, A.H. Ross, F.C. Sweep, A.R. Hermus and J.F. Wetzels, 2008. Thyroid function in patients with proteinuria. Netherlands J. Med., 66: 483-485.
PubMed  |  Direct Link  |  

6:  Liu, H., W. Yan and G. Xu, 2014. Thyroid hormone replacement for nephrotic syndrome patients with euthyroid sick syndrome: A meta-analysis. Ren. Fail., 36: 1360-1365.
CrossRef  |  Direct Link  |  

7:  Iglesias, P. and J.J. Dies, 2009. Thyroid dysfunction and kidney disease. Eur. J. Endocrinol., 160: 503-515.
CrossRef  |  Direct Link  |  

8:  El-Melegy, N.T., N.A. Mohamed and M.M. Sayed, 2008. Oxidative modification of low-density lipoprotein in relation to dyslipidemia and oxidant status in children with steroid sensitive nephrotic syndrome. Pediatr. Res., 63: 404-409.
CrossRef  |  Direct Link  |  

9:  Bakr, A., S.A. Hassan, M. Shoker, M. Zaki and R. Hassan, 2009. Oxidant stress in primary nephrotic syndrome: Does it modulate the response to corticosteroids? Pediatr. Nephrol., 24: 2375-2380.
CrossRef  |  Direct Link  |  

10:  Kniazewska, M.H., A.K. Obuchowicz, T. Wielkoszynski, J. Zmudzinska-Kitczak, K. Urban and L. Hyla-Klekot, 2009. Evaluation of certain constituents of antioxidant defense in youth treated in the past for steroid-sensitive idiopathic nephrotic syndrome. Pediatr. Nephrol., 24: 2187-2192.
CrossRef  |  Direct Link  |  

11:  Ghodake, S.R., A.N. Suryakar, R.D. Ankush, R.V. Katkam, K. Shaikh and A.V. Katta, 2011. Role of free radicals and antioxidant status in childhood nephrotic syndrome. Indian J. Nephrol., 21: 37-40.
CrossRef  |  Direct Link  |  

12:  Duann, P., P.K. Datta, C. Pan, J.B. Blumberg, M. Sharma and E.A. Lianos, 2006. Superoxide dismutase mimetic preserves the glomerular capillary permeability barrier to protein. J. Pharmacol. Exp. Ther., 316: 1249-1254.
CrossRef  |  Direct Link  |  

13:  Dwivedi, J. and P.D. Sarkar, 2014. The study of lipid profile, LP (a) and electrolytes with oxidative stress, total protein and albumin in nephrotic syndrome. Int. J. Res. Med. Sci., 2: 62-66.
Direct Link  |  

14:  Kharb, S., 2006. Association of serum concentration of total bilirubin and low density lipoprotein cholesterol with myocardial infarction. World J. Med. Sci., 1: 93-94.
Direct Link  |  

15:  Wang, L., G.C. Shearer, M.S. Budamagunta, J.C. Voss, A. Molfino and G.A. Kaysen, 2012. Proteinuria decreases tissue lipoprotein receptor levels resulting in altered lipoprotein structure and increasing lipid levels. Kidney Int., 82: 990-999.
CrossRef  |  PubMed  |  Direct Link  |  

16:  Ozbek, E., 2012. Induction of oxidative stress in kidney. Int. J. Nephrol. 10.1155/2012/465897

17:  Ghodake, S.R., A.N. Suryakar, R.D. Ankush, K. Shaikh and A.V. Katta, 2010. Role of reactive oxygen species in pathogenesis of nephrotic syndrome. Indian J. Clin. Biochem., 25: 82-85.
CrossRef  |  Direct Link  |  

18:  Uchiyama, M. and M. Mihara, 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem., 86: 271-278.
CrossRef  |  Direct Link  |  

19:  Marklund, S. and G. Marklund, 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 47: 469-474.
CrossRef  |  PubMed  |  Direct Link  |  

20:  Habig, W.H., M.J. Pabst and W.B. Jakoby, 1974. Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J. Biol. Chem., 249: 7130-7139.
CrossRef  |  PubMed  |  Direct Link  |  

21:  Das, K., L. Samanta and G.B.N. Chainy, 2000. A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals. Ind. J. Biochem. Biophys., 37: 201-204.
Direct Link  |  

22:  Satoh, K., 1978. Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin. Chim. Acta, 90: 37-43.
CrossRef  |  PubMed  |  Direct Link  |  

23:  Doumas, B.T., 1980. Determination of serum albumin using Bromocresol Green. 5th Edn., Heinemann professional, UK., pp: 553-554.

24:  Folin, O. and W. Denis, 1913. A new (colorimetric) method for the determination of uric acid in blood. J. Biol. Chem., 13: 469-475.
Direct Link  |  

25:  Allain, C.C., L.S. Poon, C.S.G. Chan, W. Richmond and P.C. Fu, 1974. Enzymatic determination of total serum cholesterol. Clin. Chem., 20: 470-475.
CrossRef  |  PubMed  |  Direct Link  |  

26:  Siddall, E.C. and J. Radhakrishnan, 2012. The pathophysiology of edema formation in the nephrotic syndrome. Kidney Int., 82: 635-642.
CrossRef  |  PubMed  |  Direct Link  |  

27:  Doucet A, G. Favre and G. Descenes, 2007. Molecular mechanism of edema formation in nephrotic syndrome: Therapeutic implications. Pediatr. Nephrol., 22: 1983-1990.
CrossRef  |  Direct Link  |  

28:  Kaneko, K., T. Kimata, S. Tsuji, T. Shimo, M. Takahashi and S. Tanaka, 2012. Serum albumin level accurately reflects antioxidant potentials in idiopathic nephrotic syndrome. Clin. Exp. Nephrol., 16: 411-414.
CrossRef  |  Direct Link  |  

29:  Roche, M., P. Rondeau, N.R. Singh, E. Tarnus and E. Bourdon, 2008. The antioxidant properties of serum albumin. FEBS Lett., 582: 1783-1787.
CrossRef  |  PubMed  |  Direct Link  |  

30:  Feinstein, E.I., E.M. Kaptein, J.T. Nicoloff and S.G. Massry, 1982. Thyroid function in patients with nephrotic syndrome and normal renal function. Am. J. Nephrol., 2: 70-76.
CrossRef  |  Direct Link  |  

31:  Li, H.Q., J. Wu, D.M. Niu, Y.H. Shi, C.N. Zhang and J.J. Wang, 2012. The level of native and oxidized lipoprotein (a) in children with nephrotic syndrome. Clin. Biochem., 45: 101-105.
CrossRef  |  Direct Link  |  

32:  Pawlak, K., D. Pawlak and M. Mysliwiec, 2005. Cu/Zn superoxide dismutase plasma levels as a new useful clinical biomarker of oxidative stress in patients with end-stage renal disease. Clin. Biochem., 8: 700-705.
CrossRef  |  Direct Link  |  

33:  Noyan, A., N. Dikmen and A. Anarat, 1996. Superoxide dismutase as a prognostic criterion in nephrotic syndrome. Nephron, 74: 477-477.
CrossRef  |  Direct Link  |  

34:  Zachwieja, J., W. Bobkowski, A. Dobrowolska-Zachwieja, M. Zaniew and J. Maciejewski, 2003. Decreased antioxidant activity in hypercholesterolemic children with nephrotic syndrome. Med. Sci. Monit., 9: 235-239.
Direct Link  |  

35:  Ece, A., Y. Atamer, F. Gurkan, M. Davutoglu, Y. Kocyigit and M. Tutanc, 2005. Paraoxonase, total antioxidant response and peroxide levels in children with steroid-sensitive nephrotic syndrome. Pediatr. Nephrol., 20: 1279-1284.
CrossRef  |  Direct Link  |  

36:  Hamed, E.A., T.B. El-Abaseri, A.O. Mohamed, A.R. Ahmed and T.H. El-Metwally, 2012. Hypoxia and oxidative stress markers in pediatric patients undergoing hemodialysis: Cross section study. BMC Nephrol., Vol. 13. 10.1186/1471-2369-13-136

37:  Tkaczyk, M., A. Czupryniak, M. Nowicki M, G. Chwatko and E. Bald, 2009. [Homocysteine and glutathione metabolism in steroid-treated relapse of idiopathic nephrotic syndrome]. Pol. Merkur. Lekarski: Organ Polskiego Towarzystwa Lekarskiego, 26: 294-297.
PubMed  |  Direct Link  |  

38:  Sawant, S.U., S. Chandran, A.F. Almeida and M.G.R. Rajan, 2011. Correlation between oxidative stress and thyroid function in patients with nephrotic syndrome. Int. J. Nephrol. 10.4061/2011/256420

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