Oxidative stress plays a key role in the pathophysiological process of uremia and its complications, particularly in cardiovascular disease. The level of oxidative stress markers is known to increase as chronic kidney disease progresses and correlates signiﬁcantly with the level of renal function. Hemodialysis and peritoneal dialysis are major modes of renal replacement therapy for end-stage renal disease patients, but unfortunately they are also accompanied by increased oxidative stress. Successful kidney transplantation, however, results in near normalization of the antioxidant status and lipid metabolism by eliminating free radicals despite the surge of oxidative stress caused by the surgical procedure and ischemic injury to the organ during the operation. This success is associated with both improved renal function, reduced cardiovascular complications and overall improved morbidity and mortality. Measuring oxidative stress markers such as malondialdehyde is promising in predicting allograft survival and delayed graft function. Key words: antioxidants, chronic kidney disease, end-stage renal disease, kidney transplantation, oxidative stress, renal replacement therapy outgrow the younger population over the next 35 years with an Introduction expected 150% growth rate compared with a growth rate that is The incidence of end-stage renal disease (ESRD) continues to expected to remain almost the same . rise in the USA. By the year 2030, the number of patients with During the past decade, kidney transplantation has increas- ESRD is projected to exceed 2.2 million. This is more than five ingly been recognized as the treatment of choice for medically times the current prevalence . Increasing kidney disease and suitable patients with ESRD . As well as improving quality of subsequent ESRD is related to the aging society and high mor- life, successful transplantation confers major benefits by improv- bidity due to lifestyle diseases such as diabetes, atherosclerosis ing the morbidity and mortality of ESRD patients who receive kid- and hypertension. The world’s elderly population is projected to ney transplant over those who undergo renal replacement Received: May 11, 2017. Editorial decision: July 10, 2017 V C The Author 2017. Published by Oxford University Press on behalf of ERA-EDTA. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Downloaded from https://academic.oup.com/ckj/article-abstract/11/1/130/4083401 by Ed 'DeepDyve' Gillespie user on 16 March 2018 CKD, kidney transplantation and oxidative stress | 131 Fig. 1. Adjusted mortality by treatment modality and Medicare comorbidity among ESRD patients and comorbidity-speciﬁc Medicare populations 65 years of age from 1996 to 2014. Source: United States Renal Data System. 2016 USRDS Annual Data Report: Epidemiology of Kidney Disease in the USA. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2016. therapy (RRT) . Cardiovascular (CV) risk reduction remains the cancer and an overall increased risk of morbidity and mortality leading cause of this improvement, although both modalities pro- . Figure 2 summarizes some of these effects on different vide compatible fluid balance and glomerular filtration rates . tissues. As data from the United States Renal Data System (USRDS) show, mortality improves significantly for ESRD patients who receive renal transplantation as compared with those on RRT. Renal failure and oxidative stress Figure 1 summarizes these finding. In this article, we review kidney transplantation’s role in the Oxidative stress appears to have a key role in the pathophysio- reduction of oxidative stress and its effect of improved morbid- logical process of uremia and its complications . Patients ity and mortality in ESRD patients. with renal insufficiency, and particularly those on hemodialysis Free radicals are unstable chemical species with a highly (HD), exhibit increased activation of oxidative and inflamma- reactive unpaired electron. As it seeks to pair with another tory processes. unpaired electron, it causes a chain reaction of free radical for- Radicals such as superoxide and hydroxyl readily interact mation that is damaging to biological systems. The great major- with the molecular components of a nephron. Radical–molecule ity of these free radicals are oxygen radicals or other reactive interactions, including the oxidation of amino acids resulting in oxygen species (ROS) . the loss of important functional properties, lipid peroxidation of Oxidative stress occurs when ROS overwhelm the antioxi- cell membranes resulting in decreased membrane viability and dant capacity of the organism. ROS are toxic by-products of cleavage and crosslinking of renal DNA resulting in harmful aerobic metabolism, which are disposed of by antioxidants. mutations, promote renal injury through damage to molecular When the antioxidant barrier is unable to fend off the number components of the kidney. The inflammatory processes that of free radicals being generated, there is increased lipid peroxi- exist to repair this radical-mediated damage may be a source of dation and oxidative stress . These agents are a constant additional free radicals, resulting in further damage to renal tis- threat to living cells by severely damaging DNA, proteins and sue . lipids. Increasing oxidative stress and inflammation may serve to Reactive nitrogen species (RNS) also contribute to increasing promote additional damage to the kidney, as well as initial or oxidative stress. RNS are derived from nitric oxide and superox- additional damage to distal tissues, resulting in the develop- ide produced via the enzymatic activity of inducible nitric oxide ment or progression of concomitant disease. Free radicals, along synthase 2 and nicotinamide adenine dinucleotide phosphate with their constant companion, inflammation, account for (NADPH) oxidase, respectively. Like ROS, RNS play a dual role many of the symptoms of uremic syndrome . Jun et al. since they can be either harmful or beneficial to living systems. showed a benefit from antioxidant therapy in reducing all ROS and RNS play an important role as regulatory mediators in causes of death and the risk of CV disease in people with signaling processes, whereas at moderate or high concentra- chronic kidney disease (CKD) . tions they are harmful for living organisms, inactivating impor- Kaltsatou et al. did a systemic review of the role of oxida- tant cellular molecules . tive stress and uremic myopathy. Muscles continuously pro- Although oxidative response and inflammation constitute duce ROS and RNS at rest and more so during contraction. a major defense against infections and regulate many physio- Moreover, ROS generation can acutely affect contractile func- logical responses in human health, if not properly regulated tion and disturbs the structural transition within the actomyo- they can also lead to several deleterious effects. Oxidative stress sin complex, which is crucial for force generation. Reviewers has a critical role in the pathophysiology of several kidney dis- found that accumulation of these oxidative stress molecules eases and also expose the individual to an increased risk of with progression of CKD is not only directly damaging to muscle hypertension, CV disease, metabolic syndrome, myopathies, cells but also affects their contractility, resulting in muscle Downloaded from https://academic.oup.com/ckj/article-abstract/11/1/130/4083401 by Ed 'DeepDyve' Gillespie user on 16 March 2018 132 | H. Tabriziani et al. Fig. 2. Pathogenic effects of oxidative stress on different organs. weakness, premature fatigue, muscular atrophy and wasting Bacterial infection and sepsis are common complications of and even cardiomyopathy . CKD. Furthermore, Lemesch et al.  showed that the type of Uremic oxidative stress might be the consequence of greater RRT plays a role in mortality. In a cross-sectional observational ROS production based on increases in reduced NADPH oxidase study they compared endotoxemia and neutrophil function, activity and expression reported in patients and models with both of which can be affected by increasing oxidative stress in renal insufficiency even in early CKD . Oxidative stress CKD patients without RRT, CKD patients undergoing HD or PD appears to increase as CKD progresses and correlates signifi- and patients after kidney transplantation. Their results showed cantly with the level of renal function. CKD patients present an a higher endotoxin serum level and a lower neutrophil phago- altered redox status and increased signs of carbonyl stress and cytic capacity compared with all other groups in CKD patients inflammatory activity, which all contribute to increase ROS as undergoing HD, which was associated with a higher mortality kidney function deteriorates . rate. The findings suggest that dialysis modality and not renal Also, progressive loss of renal function is associated with function per se determine the development of neutrophil dys- functional defects in virtually all cell populations of both the function and endotoxemia in CKD patients. HD patients are par- innate and adaptive immune systems, but the lymphoid cell line- ticularly prone to neutrophil dysfunction and endotoxemia, age is more severely affected than the myeloid cell lineage. The whereas neutrophil function seems to improve after kidney ESRD-related changes in the immune system resemble immuno- transplantation . Differences in mortality and improvement logical aging in older healthy individuals, a concept known as of neutrophil phagocytic capacity after kidney transplantation premature immunological aging. Chronic inflammation and oxi- can be partly due to differences in the oxidative stress level in dative stress lead to this epigenetic modification . these groups. In a prospective cohort study by Soleymanian et al.of kidney transplant candidates on HD, they measured total anti- oxidant capacity (TAC), total thiol molecules, lipid peroxidation, RRT and oxidative stress plasma catalase, superoxide dismutase, glutathione peroxidase HD and peritoneal dialysis (PD) are two major modalities of RRT and C-reactive protein as the biomarkers of oxidative stress and in ESRD. Unfortunately, both methods are accompanied by inflammation. They compared the level of these markers before increased oxidative stress. The composition of the dialysis solu- and 3 months after kidney transplantation. They concluded that tion, the characteristics of the HD membranes, loss of anti- oxidative stress and inflammation are elevated in HD patients oxidants and activation of leukocytes increase the formation of and could be improved significantly by restoration of kidney ROS and promote an overall pro-inflammatory state . function after kidney transplantation . Downloaded from https://academic.oup.com/ckj/article-abstract/11/1/130/4083401 by Ed 'DeepDyve' Gillespie user on 16 March 2018 CKD, kidney transplantation and oxidative stress | 133 It is well known that HD patients experience increased oxi- findings indicate that kidney transplantation seems to restore a dative stress. In a systemic review by Poulianiti et al. , the nearly normal level of glycoxidative stress markers and an authors concluded that HD therapy per se seems to exert a neg- increase of TAC, but complete remission is only possible when ative influence on systemic redox status. Retention of water the renal function is normal . and salt in kidney disease patients results in increased water- It is very important to keep in mind that TAC is a compre- soluble toxins. In contrast, because of an abnormal balance of hensive index of antioxidant capacity and simplifying that nor- protein-bound blood components in the patients with CKD, malization of kidney function is the only factor contributing to there is retention of protein-bound toxins. As Gao et al.  this drastic improvement of TAC after kidney transplantation reported, this increase in oxidation may alter high-density lipo- is not realistic. Decreasing ROS after successful kidney trans- protein (HDL) function not only by chemically modifying pro- plantation results in breaking the vicious cycle of cell damage, teins and lipids but also by altering the rate of HDL remodeling inflammation and distal organ damage. This means recovery and/or shifting the population distribution among HDL sub- from many uremic syndrome sequelae, such as myopathy, car- classes. Mild oxidation in vivo may enhance HDL functions in diomyopathy and a decrease in appetite. Clinically, this reverse cholesterol transport, but extensive oxidation would improvement translates to more effective cardiac output, bet- inhibit protein distribution and lipoprotein remodeling, which ter nutrition and more muscle mass, which can all contribute would impair reverse cholesterol transport and increase oxida- to better metabolism and less production of oxidative stress tive stress in these patients . and improvement in TAC after successful kidney transplantation. CKD patients present an altered redox status and increased Kidney transplant and oxidative stress signs of carbonyl stress and inflammatory activity as kidney function deteriorates, which was partially but significantly Unfortunately, the nature of the surgery and organ transfer improved after renal transplantation . In the study con- from a donor to recipient causes inevitable renal ischemia. This ducted by Vostalova et al. , the restoration of kidney function renal ischemia reperfusion (RIR) injury during transplantation after kidney transplantation led to a reduction in metabolic is the major cause of renal transplant dysfunction. It causes an abnormalities and elimination of oxidative stress. Time- oxidative burst that triggers inflammation and tubular cell dependent changes in oxidative stress–related markers and kid- injury. In a recent study, Tennankore et al.  showed a corre- ney function and metabolic parameters were evaluated for 3 lation between prolonged warm ischemia and mortality and months in patients before and after kidney transplantation. In graft failure. Evidences suggests that NADPH oxidase is acti- particular, TAC, AOPPs, lipid peroxidation as thiobarbituric vated during RIR injury and may play a potential role in the acid–reactive substances (TBARS) and reduced glutathione pathogenesis of progressive renal damage in this setting. (GSH); activities of glutathione peroxidase, catalase and super- Nicholson et al.  performed a double-blind randomized clini- oxide dismutase and kidney function markers were measured. cal trial (RCT) regarding remote ischemic conditioning and were AOPPs, TAC and TBARS were significantly decreased, whereas unable to show an improvement in renal function at 1 and GSH was significantly increased after kidney transplantation. 3 months posttransplant . Kumar et al. , through in vitro Antioxidant enzyme activities were not significantly changed studies on immortalized human renal proximal tubular epithe- during the monitored period. Kidney function markers and glo- lial cells, suggested the role of antioxidants such as N-acetylcys- merular filtration rate significantly increased and the creatinine teine (NAC) in decreasing RIR and thus improving mortality. level significantly decreased after transplantation. They also Also, most of the currently accepted immunosuppressive found that after transplantation there is a trend toward medication, such as corticosteroids, calcineurin inhibitors increased HDL cholesterol. These results show that successful (CNIs) and mammalian target of rapamycin inhibitors, which kidney transplantation contributes to normalization of antioxi- are the mainstay of posttransplant antirejection medications, dant status and lipid metabolism that is associated with both are all known to increase the risks of developing new-onset dia- improved renal function and reduced CV complications . betes after transplant (NODAT) as well as metabolic syndrome, Sulfatide is a major component of glycosphingolipids in lipo- which by itself can translate to increased oxidative stress. proteins. Wang et al.  reported that a low serum level of sul- In contrast, kidney transplantation restores, at least parti- fatide in HD patients might be related to the high incidence of ally, the fundamental processes of glomerular filtration, which CV disease. The recovery of serum sulfatide derives from the eliminates toxic solutes, including from oxidative stress. To attenuation of systemic oxidative stress. The normal level of determine the net effect of the oxidative stress level after suc- serum sulfatide in kidney transplant recipients affects platelet cessful kidney transplantation, Antolini et al.  did a cross- function and contributes to a reduction in the incidence of CV sectional study to determine the levels of several different gly- disease . coxidative stress-related parameters after kidney transplanta- Malondialdehyde (MDA) and serum sulfatide are two tion. They measured glycoxidative stress markers such as markers of oxidative stress, which were investigated by Kamijo albumin-bound and free pentosidine, low molecular weight et al.  in post–kidney transplant patients . The high level advanced glycation end products (LMW-AGEs), advanced oxida- of MDA in the kidney transplant recipients decreased dramati- tion protein products (AOPPs) and low molecular weight carbon- cally, but was still high, 1 year after kidney transplant. MDA lev- yls (LMW-Cs). TAC was monitored by measuring both the ferric els decreased further and reached near normal levels in about reducing/antioxidant power (FRAP) and oxygen radical absorb- 3 years. ance capacity (ORAC). Antolini et al. showed that transplant To determine the effect of immunosuppression choices in patients with normal kidney function had levels of these com- this drastic reduction of oxidative stress after kidney transplant, pounds that were comparable to normal controls, except for the Vostalova et al.  followed 70 patients after kidney transplant. LMW-AGEs, which were higher. Levels of LMW-AGEs, pentosi- The patients were divided into two groups: those receiving dine, LMW-Cs and AOPPs were inversely correlated with creati- cyclosporine and those receiving tacrolimus. Oxidative stress– nine clearance. The TAC was paradoxically higher in transplant related markers such as TAC, AOPPs and lipid peroxidation patients than in controls, regardless of kidney function. These Downloaded from https://academic.oup.com/ckj/article-abstract/11/1/130/4083401 by Ed 'DeepDyve' Gillespie user on 16 March 2018 134 | H. Tabriziani et al. products all decreased. There was no significant difference Kidney transplantation has shown promise in decreasing between these two CNIs in any of the measured parameters. oxidative stress. By alleviating oxidative stress, modifying the Improved renal function after kidney transplant is linked to a immunologic response, improving endothelial function, sup- reduction in oxidative stress, but independent of immunosup- pressing platelet aggregation and decreasing arterial stiffness, pressive therapy. kidney transplantation leads to a decrease in CV morbidity and Interestingly, the reduction in oxidative stress markers can mortality. be used as a prognostic factor after kidney transplantation. But it is very important not to forget that although oxidative Increased MDA levels on the first day after kidney transplant stress is a major risk factor in CV disease, the increased risk of might be an early prognostic indicator of delayed graft function CV disease after kidney transplant can be also related to a high (DGF), and levels on Day 7 might represent a useful predictor of prevalence and accumulation of other atherogenic risk factors. 1-year graft function . DNA fragmentation is one of the typi- Hypertension, NODAT and hyperlipidemia are well-recognized cal features of apoptosis, frequently induced by oxidative stress. risk factors for the development of CV events after renal trans- Low levels of oxidation and apoptosis at 6 months after trans- plantation and are strongly associated with immunosuppres- plantation correlate with a better recovery of renal function in sive therapy. The elevated risk may also be caused by kidney allografts . nontraditional risk factors such as anemia, adhesion molecules, hyperhomocysteinemia, a microinflammatory state and abnor- mal coagulation . Moreover, the contribution of some CV risk factors to renal allograft dysfunction has been well demon- CV disease after kidney transplant strated. This relation causes a vicious cycle, since progressive renal dysfunction may also influence the risk of CV complica- CV disease is the leading cause of death in patients with renal tions after renal transplantation. failure. Although improved, the morbidity and mortality rates are still higher after kidney transplantation than in the general population and many renal transplant recipients die with func- tional grafts. With the advent of improved immunosuppression Conclusion and surgical technique, deaths resulting from CV disease have become an increasingly important cause of graft loss, particu- Oxidative stress has a key role in the pathophysiological process larly after the first posttransplantation year. of uremia and its complications, including CV disease. The level One of the major factors in the pathogenesis of CV complica- of these markers correlates with the severity of CKD and the tions is the imbalance between the formation and clearance of level of renal function. Unfortunately, both modalities of RRT ROS by the antioxidative system. This disparity can cause endo- (HD and PD) increase the level of oxidative stress. thelial dysfunction and impairment of the regulatory functions Although the surgical procedure of transplantation and of endothelium for vasodilatation. It is also the foundation of ischemic injury to the organ during the procurement and trans- smooth muscle cell proliferation and fibrinolysis, which play a plantation can also cause increases oxidative stress, it seems pivotal role in the pathogenesis of CV events. Also, as men- that successful kidney transplant results in near normalization tioned above, this can lead to disturbances in contractility, and of the antioxidant status and lipid metabolism by eliminating resulting in cardiomyopathy . free radicals and decreasing oxidative stress. Achieving any In a recent study, Hornum et al.  investigated the effect of level of kidney function after successful kidney transplantation kidney transplantation on vascular hemodynamics by measur- will decrease the oxidative stress level. This success is con- ing arterial function at baseline and 12 months after kidney nected with both improved renal function and reduced CV com- transplantation. Arterial function was estimated by the pulse plications and eventually improving morbidity and mortality in wave velocity of the carotid–femoral pulse wave, aortic aug- these patients. It is important to remember that the degree of mentation index and flow-mediated (endothelium-dependent) renal function after transplantation is one of the key factors of and nitroglycerin-induced vasodilatation (endothelium inde- eliminating these radicals. pendent) of the brachial artery. They found that arterial func- Measuring oxidative stress markers such as MDA is also tion improved 1 year after kidney transplantation and was also promising in predicting allograft survival and the possibility of associated with a decline in blood pressure. These seemingly DGF. Unfortunately, most of the studies in this regard have beneficial changes in arterial hemodynamics had occurred been very limited. They all have small sample size and are despite increased insulin resistance and unchanged high levels mainly observational or cohort studies. There are many unre- of cholesterol and triglyceride . This shows the importance solved issues regarding the role of oxidative stress and the net of a healthy endothelium, which can be achieved by reducing balance of these toxins after kidney transplantation that need ROS after successful kidney transplantation. to be further studied. In another study by Yilmaz et al. , they measured plasma It is the hope of the authors that this review has identified asymmetric dimethyl arginine (ADMA) levels before transplan- the key literature surrounding this important discussion and tation and on Days 1, 3, 7, 14 and 28. We know that ADMA is an that it may be used as a step for further research in this arena. endogenous modulator of endothelial function and oxidative stress and increased levels of this molecule have been reported in metabolic disorders and CV diseases. In this study, they Conflict of interest statement measured brachial artery flow-mediated dilatation as a marker of endothelium function before transplantation and on Day 28. None declared. Their finding indicates that ADMA is associated with flow- mediated dilatation in CKD, both before and after kidney trans- References plantation. Endothelial functions improve at the very beginning of the posttransplantation period with an accompanying reduc- 1. Collins AJ, Foley RN, Chavers B et al. US Renal Data System tion in ADMA levels. 2013 Annual Data Report. 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Clinical Kidney Journal – Oxford University Press
Published: Feb 1, 2018
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