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Oxidative stress and cardiac dysfunction in children with chronic renal failure on regular hemodialysis

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Abstract

Objective

The objective of this study was to evaluate cardiac function in children with end-stage renal disease (ESRD) on regular hemodialysis using speckle tracking echocardiography (STE) and correlate results with plasma glutathione level as a marker of oxidative stress.

Methods

The study involved 30 children with ESRD and 30 healthy controls. The plasma glutathione and C-reactive protein (CRP) levels were measured, and cardiac function was evaluated using conventional echocardiography and STE.

Results

Plasma glutathione levels were significantly lower and CRP significantly higher in patients than in controls. Children with ESRD had significant systolic and diastolic cardiac dysfunctions detected by STE compared with controls. Conventional echocardiography failed to detect these dysfunctions. There was significant increase in left-ventricular relative wall thickness (LV-RWT) in patients, especially those with hypertension, compared with the control group. There was also significant impairment of LV and right-ventricular (RV) global longitudinal strain (GLS) and torsion; however, LV-GLS was significantly better in hypertensive than in normotensive patients. The degree of impairment in GLS and cardiac torsion negatively correlated with plasma glutathione levels.

Conclusion

Significant oxidative stress was present in children with ESRD and was correlated with the degree of cardiac dysfunction detected early using the new cardiac imaging modality, STE.

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References

  1. Foley RN, Parfrey PS, Sarnak MJ (1998) Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis 32(5 Suppl 3):S112–9

    Article  CAS  PubMed  Google Scholar 

  2. Ikizler TA (2002) Epidemiology of vascular disease in renal failure. Blood Purif 20(1):6–10

    Article  PubMed  Google Scholar 

  3. Fellah H, Feki M, Souissi M, Ghorbel H, Ben Abdallah T, Massy Z, Hedhili A, Ben Maiz H, Lacour B, Kaabachi N, Mebazaa A (2006) Oxidative stress in end stage renal disease: evidence and association with cardiovascular events in Tunisian patients. Tunis Med 84(11):724–729

    PubMed  Google Scholar 

  4. Mondillo S, Galderisi M, Mele D, Cameli M, Lomoriello VS, Zacà V, Ballo P, D’Andrea A, Muraru D, Losi M, Agricola E, D’Errico A, Buralli S, Sciomer S, Nistri S, Badano L, Echocardiography Study Group Of The Italian Society Of Cardiology (Rome, Italy) (2011) Speckle-tracking echocardiography: a new technique for assessing myocardial function. J Ultrasound Med 30(1):71–83

    PubMed  Google Scholar 

  5. Geyer H, Caracciolo G, Abe H, Wilansky S, Carerj S, Gentile F, Nesser HJ, Khandheria B, Narula J, Sengupta PP (2010) Assessment of myocardial mechanics using speckle tracking echocardiography: fundamentals and clinical applications. J Am Soc Echocardiogr 23(4):351–69, quiz 453–455

    Article  PubMed  Google Scholar 

  6. Teske AJ, De Boeck BW, Melman PG, Sieswerda GT, Doevendans PA, Cramer MJ (2007) Echocardiographic quantification of myocardial function using tissue deformation imaging, a guide to image acquisition and analysis using tissue Doppler and speckle tracking. Cardiovasc Ultrasound 5:27

    Article  PubMed  PubMed Central  Google Scholar 

  7. Yao Q, Axelsson J, Stenvinkel P, Lindholm B (2004) Chronic systemic inflammation in dialysis patients: an update on causes and consequences. ASAIO J 50(6):13–17

    Article  Google Scholar 

  8. Tbahriti HF, Kaddous A, Bouchenak M, Mekki K (2013) Effect of different stages of chronic kidney disease and renal replacement therapies on oxidant-antioxidant balance in uremic patients. Biochem Res Int 2013:358985

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hsieh CC, Hsieh SC, Chiu JH, Wu YL (2014) Preconditioning somatothermal stimulation on Qimen (LR14) reduces hepatic ischemia/reperfusion injury in rats. BMC Complement Alternat Med 14:18

    Article  Google Scholar 

  10. Guidelines (1996) Update on the 1987 task force report on high blood pressure in children and adolescents: a working group report from the national high blood pressure education program. National high blood pressure education program working group on hypertension control in children and adolescents. Pediatrics 98(4 Pt 1):649–658

    Google Scholar 

  11. Abid L, Rekik H, Jarraya F, Kharrat I, Hachicha J, Kammoun S (2014) Acute hemodialysis effects on Doppler echocardiographic indices. Saudi J Kidney Dis Transplant 25(4):756–761

    Article  Google Scholar 

  12. Al-Biltagi M, Serag AR, Hefidah MM, Mabrouk MM (2013) Evaluation of cardiac functions with Doppler echocardiography in children with down syndrome and anatomically normal heart. Cardiol Young 23:174–180

    Article  PubMed  Google Scholar 

  13. Picard MH, Adams D, Bierig SM, Dent JM, Douglas PS, Gillam LD, Keller AM, Malenka DJ, Masoudi FA, McCulloch M, Pellikka PA, Peters PJ, Stainback RF, Strachan GM, Zoghbi WA; American Society of Echocardiography (2011) American society of echocardiography recommendations for quality echocardiography laboratory operations. J Am Soc Echocardiogr 24:1–10

  14. Mitsnefes MM, Kimball TR, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2003) Left ventricular mass and systolic performance in pediatric patients with chronic renal failure. Circulation 107(6):864–868

    Article  PubMed  Google Scholar 

  15. Gidding SS, Carnethon MR, Daniels S, Liu K, Jacobs DR Jr, Sidney S, Gardin J (2010) Low cardiovascular risk is associated with favorable left ventricular mass, left ventricular relative wall thickness, and left atrial size: the CARDIA study. J Am Soc Echocardiogr 123(8):816–822

    Article  Google Scholar 

  16. Tei C, Dujardin KS, Hodge DO, Bailey KR, McGoon MD, Tajik AJ, Seward SB (1996) Doppler echocardiographic index for assessment of global right ventricular function. J Am Soc Echocardiogr 9:838–847

    Article  CAS  PubMed  Google Scholar 

  17. Cao Q, Xie D, Liu J, Zou H, Zhang Y, Zhang H, Zhang Z, Xue H, Zhou J, Chen P (2014) HLA polymorphism and susceptibility to end-stage renal disease in Cantonese patients awaiting kidney transplantation. PLoS One 9(6):e90869

    Article  PubMed  PubMed Central  Google Scholar 

  18. Suffoletto MS, Dohi K, Cannesson M, Saba S, Gorcsan J 3rd (2006) Novel speckle-tracking radial strain from routine black-and-white echocardiographic images to quantify dyssynchrony and predict response to cardiac resynchronization therapy. Circulation 113(7):960–968

    Article  PubMed  Google Scholar 

  19. Takahashi K, Al Naami G, Thompson R, Inage A, Mackie AS, Smallhorn JF (2010) Normal rotational, torsion and untwisting data in children, adolescents and young adults. J Am Soc Echocardiogr 23(3):286–293

    Article  PubMed  Google Scholar 

  20. Al-Biltagi MA, Tolba OA, Mawlana W, Abd El Hamed A, Ghazy M (2015) Resistin and right ventricular function in children with recently diagnosed type-1 diabetes mellitus: a case control study. J Pediatr Endocrinol Metab 28(3–4):299–308

    CAS  PubMed  Google Scholar 

  21. Notomi Y, Lysyansky P, Setser RM, Shiota T, Popović ZB, Martin-Miklovic MG, Weaver JA, Oryszak SJ, Greenberg NL, White RD, Thomas JD (2005) Measurement of ventricular torsion by two-dimensional ultrasound speckle tracking imaging. J Am Coll Cardiol 45(12):2034–2041

    Article  PubMed  Google Scholar 

  22. Haeck ML, Scherptong RW, Marsan NA, Holman ER, Schalij MJ, Bax JJ, Vliegen HW, Delgado V (2012) Prognostic value of right ventricular longitudinal peak systolic strain in patients with pulmonary hypertension. Circ Cardiovasc Imaging 5(5):628–636

    Article  PubMed  Google Scholar 

  23. Motoki H, Borowski AG, Shrestha K, Hu B, Kusunose K, Troughton RW, Tang WH, Klein AL (2014) Right ventricular global longitudinal strain provides prognostic value incremental to left ventricular ejection fraction in patients with heart failure. J Am Soc Echocardiogr 27(7):726–732

    Article  PubMed  Google Scholar 

  24. El-Saeed GS, Fadel F, Elshamaa MF, Galal RE, Elghoroury EA, Nasr SA, Thabet EH, Abdelrahman SM (2015) Advanced glycation end products and soluble receptor as markers of oxidative stress in children on hemodialysis. Ren Fail 37(9):1452–1456

    Article  PubMed  Google Scholar 

  25. Puchades MJ, Saez G, Muñoz MC, Gonzalez M, Torregrosa I, Juan I, Miguel A (2013) Study of oxidative stress in patients with advanced renal disease and undergoing either hemodialysis or peritoneal dialysis. Clin Nephrol 80(3):177–186

    Article  CAS  PubMed  Google Scholar 

  26. Garcia-Bello JA, Gómez-Díaz RA, Contreras-Rodríguez A, Talavera JO, Mondragón-González R, Sanchez-Barbosa L, Diaz-Flores M, Valladares-Salgado A, Gallardo JM, Aguilar-Kitsu A, Lagunas-Munoz J, Wacher NH (2014) Carotid intima media thickness, oxidative stress, and inflammation in children with chronic kidney disease. Pediatr Nephrol 29(2):273–281

  27. Himmelfarb J, McMonagle E, Freedman S, Klenzak J, McMenamin E, Le P, Pupim LB, Ikizler TA, The PICARD Group (2004) Oxidative stress is increased in critically ill patients with acute renal failure. J Am Soc Nephrol 15(9):2449–2456

    Article  CAS  PubMed  Google Scholar 

  28. Annuk M, Soveri I, Zilmer M, Lind L, Hulthe J, Fellström B (2005) Endothelial function, CRP and oxidative stress in chronic kidney disease. J Nephrol 18(6):721–726

    CAS  PubMed  Google Scholar 

  29. Nguyen-Khoa T, Massy ZA, De Bandt JP, Kebede M, Salama L, Lambrey G, Witko-Sarsat V, Drüeke TB, Lacour B, Thévenin M (2001) Oxidative stress and haemodialysis: role of inflammation and duration of dialysis treatment. Nephrol Dial Transplant 16(2):335–340

    Article  CAS  PubMed  Google Scholar 

  30. Mitsnefes MM (2012) Cardiovascular disease in children with chronic kidney disease. J Am Soc Nephrol 23(4):578–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Glassock RJ, Pecoits-Filho R, Barberato SH (2009) Left ventricular mass in chronic kidney disease and ESRD. Clin J Am Soc Nephrol 4(Suppl 1):S79–91

    Article  PubMed  Google Scholar 

  32. Zoccali C, Benedetto FA, Mallamaci F, Tripepi G, Giacone G, Stancanelli B, Cataliotti A, Malatino LS (2004) Left ventricular mass monitoring in the follow-up of dialysis patients: prognostic value of left ventricular hypertrophy progression. Kidney Int 65(4):1492–1498

    Article  PubMed  Google Scholar 

  33. Shamszad P, Slesnick TC, Smith EO, Taylor MD, Feig DI (2012) Association between left ventricular mass index and cardiac function in pediatric dialysis patients. Pediatr Nephrol 27(5):835–841

    Article  PubMed  Google Scholar 

  34. Krishnasamy R, Hawley CM, Stanton T, Pascoe EM, Campbell KL, Rossi M, Petchey W, Tan KS, Beetham KS, Coombes JS, Leano R, Haluska BA, Isbel NM (2015) Left ventricular global longitudinal strain is associated with cardiovascular risk factors and arterial stiffness in chronic kidney disease. BMC Nephrol 16:106

    Article  PubMed  PubMed Central  Google Scholar 

  35. Buckberg G, Hoffman JI, Mahajan A, Saleh S, Coghlan C (2008) Cardiac mechanics revisited: the relationship of cardiac architecture to ventricular function. Circulation 118(24):2571–2587

    Article  PubMed  Google Scholar 

  36. Rüssel IK, Götte MJ, Bronzwaer JG, Knaapen P, Paulus WJ, van Rossum AC (2009) Left ventricular torsion: an expanding role in the analysis of myocardial dysfunction. JACC Cardiovasc Imaging 2(5):648–655

    Article  PubMed  Google Scholar 

  37. Stefani L, Pedrizzetti G, De Luca A, Mercuri R, Innocenti G, Galanti G (2009) Real-time evaluation of longitudinal peak systolic strain (speckle tracking measurement) in left and right ventricles of athletes. Cardiovasc Ultrasound 7:17

    Article  PubMed  PubMed Central  Google Scholar 

  38. Murata T, Dohi K, Onishi K, Sugiura E, Fujimoto N, Ichikawa K, Ishikawa E, Nakamura M, Nomura S, Takeuchi H, Nobori T, Ito M (2011) Role of haemodialytic therapy on left ventricular mechanical dyssynchrony in patients with end-stage renal disease quantified by speckle-tracking strain imaging. Nephrol Dial Transplant 26(5):1655–1661

    Article  PubMed  Google Scholar 

  39. Sgambat K, Frank L, Ellini A, Sable C, Moudgil A (2012) Carnitine supplementation improves cardiac strain rate in children on chronic hemodialysis. Pediatr Nephrol 27(8):1381–1387

    Article  PubMed  Google Scholar 

  40. Yingchoncharoen T, Agarwal S, Popović ZB, Marwick TH (2013) Normal ranges of left ventricular strain: a meta-analysis. J Am Soc Echocardiogr 26(2):185–191

    Article  PubMed  Google Scholar 

  41. Shizukuda Y, Bolan CD, Tripodi DJ, Sachdev V, Nguyen TT, Botello G, Yau YY, Sidenko S, Inez E, Ali MI, Waclawiw MA, Leitman SF, Rosing DR (2009) Does oxidative stress modulate left ventricular diastolic function in asymptomatic subjects with hereditary hemochromatosis? Echocardiography 26(10):1153–1158

    Article  PubMed  PubMed Central  Google Scholar 

  42. Loch T, Vakhrusheva O, Piotrowska I, Ziolkowski W, Ebelt H, Braun T, Bober E (2009) Different extent of cardiac malfunction and resistance to oxidative stress in heterozygous and homozygous manganese-dependent superoxide dismutase-mutant mice. Cardiovasc Res 82(3):448–457

    Article  CAS  PubMed  Google Scholar 

  43. McIntyre CW, Burton JO, Selby NM, Leccisotti L, Korsheed S, Baker CS, Camici PG (2008) Hemodialysis-induced cardiac dysfunction is associated with an acute reduction in global and segmental myocardial blood flow. Clin J Am Soc Nephrol 3(1):19–26

    Article  PubMed  PubMed Central  Google Scholar 

  44. Sood MM, Pauly RP, Rigatto C, Komenda P (2008) Left ventricular dysfunction in the haemodialysis population. NDT Plus 1(4):199–205

    PubMed  PubMed Central  Google Scholar 

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Author information

Authors and Affiliations

  1. Pediatric Department, Tanta University, Tanta, Al Gharbia, Egypt

    Mohammed Al-Biltagi, Osama A. Tolba, Maher Ahmed Abd ElHafez, Ahmed Abd ElBasset Abo-Elezz & Eman Kamel EL Kady

  2. Clinical Pathology Department, Faculty of Medicine, Tanta University, Tanta, Egypt

    Sahar Mohey El-din Hazza

Authors
  1. Mohammed Al-Biltagi
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  2. Osama A. Tolba
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  3. Maher Ahmed Abd ElHafez
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  4. Ahmed Abd ElBasset Abo-Elezz
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  5. Eman Kamel EL Kady
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  6. Sahar Mohey El-din Hazza
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Corresponding author

Correspondence to Mohammed Al-Biltagi.

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Ethical approval

The study was approved by the Ethics Committee of the Tanta Faculty of Medicine and conducted in accordance with the Declaration of Helsinki. Written informed consent was obtained from each child’s guardian, with assurance of patient privacy.

Conflict of interest

There were no financial or ethical conflicts of interest.

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Cite this article

Al-Biltagi, M., Tolba, O.A., ElHafez, M.A.A. et al. Oxidative stress and cardiac dysfunction in children with chronic renal failure on regular hemodialysis. Pediatr Nephrol 31, 1329–1339 (2016). https://doi.org/10.1007/s00467-016-3314-8

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  • DOI: https://doi.org/10.1007/s00467-016-3314-8

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