Abstract
Background
Myocardial dysfunction is common in chronic kidney disease (CKD) and related to poor outcomes. New non-invasive methods to assess cardiac function have been introduced, but comparative studies evaluating their clinical usefulness in pediatric CKD are lacking. We studied left ventricular (LV) function in pediatric CKD and renal transplant patients, comparing conventional pulse-wave Doppler echocardiography (cPWD) with newer tissue Doppler imaging (TDI) and relating the results to known cardiovascular risk factors.
Methods
The study included 34 children/adolescents with CKD stages 2–5, 44 renal transplant patients and 19 patients with a normal renal function. The mean age was 11.4 (range 0.8–18.8) years.
Results
Both patient groups had significantly lower LV diastolic function than those with a normal renal function. The most sensitive determinants were TDI E′/A′ and cPWD E/TDI E′ ratios. In a stepwise linear regression analysis, high blood pressure, young age and the presence of albuminuria all independently predicted LV diastolic function.
Conclusions
Our study confirms the high prevalence of LV diastolic dysfunction in pediatric CKD patients and following renal transplantation, where TDI appears to be more sensitive than cPWD in assessing early myocardial dysfunction. Our results also underline the importance of preventive measures, such as rigorous blood pressure control, in pediatric CKD.
Similar content being viewed by others
References
McDonald SP, Craig JC (2004) Long-term survival of children with end-stage renal disease. N Engl J Med 350:2654–2662
Groothoff J, Gruppen M, de Groot E, Offringa M (2005) Cardiovascular disease as a late complication of end-stage renal disease in children. Perit Dial Int 25[Suppl 3]:S123–S126
Parekh RS, Carroll CE, Wolfe RA, Port FK (2002) Cardiovascular mortality in children and young adults with end-stage kidney disease. J Pediatr 141:191–197
Oh J, Wunsch R, Turzer M, Bahner M, Raggi P, Querfeld U, Mehls O, Schaefer F (2002) Advanced coronary and carotid arteriopathy in young adults with childhood-onset chronic renal failure. Circulation 106:100–105
Johnstone LM, Jones CL, Grigg LE, Wilkinson JL, Walker RG, Powell HR (1996) Left ventricular abnormalities in children, adolescents and young adults with renal disease. Kidney Int 50:998–1006
Matteucci MC, Wuhl E, Picca S, Mastrostefano A, Rinelli G, Romano C, Rizzoni G, Mehls O, de Simone G, Schaefer F (2006) Left ventricular geometry in children with mild to moderate chronic renal insufficiency. J Am Soc Nephrol 17:218–226
Mitsnefes MM, Kimball TR, Border WL, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2004) Impaired left ventricular diastolic function in children with chronic renal failure. Kidney Int 65:1461–1466
Gorcsan J 3rd (2000) Tissue Doppler echocardiography. Curr Opin Cardiol 15:323–329
Hayashi SY, Rohani M, Lindholm B, Brodin LA, Lind B, Barany P, Alvestrand A, Seeberger A (2006) Left ventricular function in patients with chronic kidney disease evaluated by colour tissue Doppler velocity imaging. Nephrol Dial Transplant 21:125–132
Otsuka T, Suzuki M, Yoshikawa H, Sugi K (2009) Left ventricular diastolic dysfunction in the early stage of chronic kidney disease. J Cardiol 54:199–204
Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 10:165–193
Mitsnefes MM, Kimball TR, Kartal J, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2005) Cardiac and vascular adaptation in pediatric patients with chronic kidney disease: role of calcium-phosphorus metabolism. J Am Soc Nephrol 16:2796–2803
Tafreshi RI, Human N, Otukesh H, Nikavar A (2011) Evaluation of combined left ventricular function using the myocardial performance index in children with chronic kidney disease. Echocardiography 28:97–103
Mitsnefes MM, Kimball TR, Border WL, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2004) Abnormal cardiac function in children after renal transplantation. Am J Kidney Dis 43:721–726
Ten Harkel AD, Cransberg K, Van Osch-Gevers M, Nauta J (2009) Diastolic dysfunction in paediatric patients on peritoneal dialysis and after renal transplantation. Nephrol Dial Transplant 24:1987–1991
Muscheites J, Meyer AA, Drueckler E, Wigger M, Fischer DC, Kundt G, Kienast W, Haffner D (2008) Assessment of the cardiovascular system in pediatric chronic kidney disease: a pilot study. Pediatr Nephrol 23:2233–2239
Litwin M, Wuhl E, Jourdan C, Trelewicz J, Niemirska A, Fahr K, Jobs K, Grenda R, Wawer ZT, Rajszys P, Troger J, Mehls O, Schaefer F (2005) Altered morphologic properties of large arteries in children with chronic renal failure and after renal transplantation. J Am Soc Nephrol 16:1494–1500
Litwin M, Wuhl E, Jourdan C, Niemirska A, Schenk JP, Jobs K, Grenda R, Wawer ZT, Rajszys P, Mehls O, Schaefer F (2008) Evolution of large-vessel arteriopathy in paediatric patients with chronic kidney disease. Nephrol Dial Transplant 23:2552–2557
Pecoits-Filho R, Barany P, Lindholm B, Heimburger O, Stenvinkel P (2002) Interleukin-6 is an independent predictor of mortality in patients starting dialysis treatment. Nephrol Dial Transplant 17:1684–1688
Shinohara K, Shoji T, Emoto M, Tahara H, Koyama H, Ishimura E, Miki T, Tabata T, Nishizawa Y (2002) Insulin resistance as an independent predictor of cardiovascular mortality in patients with end-stage renal disease. J Am Soc Nephrol 13:1894–1900
Sebekova K, Podracka L, Heidland A, Schinzel R (2001) Enhanced plasma levels of advanced glycation end products (AGE) and pro-inflammatory cytokines in children/adolescents with chronic renal insufficiency and after renal replacement therapy by dialysis and transplantation—are they inter-related. Clin Nephrol 56:S21–S26
Nairn J, Hodge G, Henning P (2005) Changes in leukocyte subsets: clinical implications for children with chronic renal failure. Pediatr Nephrol 20:190–196
Ece A, Gurkan F, Kervancioglu M, Kocamaz H, Gunes A, Atamer Y, Selek S (2006) Oxidative stress, inflammation and early cardiovascular damage in children with chronic renal failure. Pediatr Nephrol 21:545–552
Silverstein DM, Mitchell M, LeBlanc P, Boudreaux JP (2007) Assessment of risk factors for cardiovasuclar disease in pediatric renal transplant patients. Pediatr Transplant 11:721–729
Prokai A, Fekete A, Kis E, Reusz GS, Sallay P, Korner A, Wagner L, Tulassay T, Szabo AJ (2008) Post-transplant diabetes mellitus in children following renal transplantation. Pediatr Transplant 12:643–649
Lindblad YT, Axelsson J, Barany P, Celsi G, Lindholm B, Qureshi AR, Carrea A, Canepa A (2008) Hyperinsulinemia and insulin resistance, early cardiovascular risk factors in children with chronic kidney disease. Blood Purif 26:518–525
Lai HL, Kartal J, Mitsnefes M (2007) Hyperinsulinemia in pediatric patients with chronic kidney disease: the role of tumor necrosis factor-alpha. Pediatr Nephrol 22:1751–1756
Schwartz GJ, Munoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629–637
Brito VN, Batista MC, Borges MF, Latronico AC, Kohek MB, Thirone AC, Jorge BH, Arnhold IJ, Mendonca BB (1999) Diagnostic value of fluorometric assays in the evaluation of precocious puberty. J Clin Endocrinol Metab 84:3539–3544
Elmlinger MW, Kuhnel W, Wormstall H, Doller PC (2005) Reference intervals for testosterone, androstenedione and SHBG levels in healthy females and males from birth until old age. Clin Lab 51:625–632
Norjavaara E, Ankarberg C, Albertsson-Wikland K (1996) Diurnal rhythm of 17 beta-estradiol secretion throughout pubertal development in healthy girls: evaluation by a sensitive radioimmunoassay. J Clin Endocrinol Metab 81:4095–4102
National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576
Wuhl E, Witte K, Soergel M, Mehls O, Schaefer F (2002) Distribution of 24-h ambulatory blood pressure in children: normalized reference values and role of body dimensions. J Hypertens 20:1995–2007
Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C (2005) Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics 115:e500–e503
Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57:450–458
Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise J, Solomon S, Spencer KT, St John Sutton M, Stewart W (2006) Recommendations for chamber quantification. Eur J Echocardiogr 7:79–108
Nishimura RA, Tajik AJ (1997) Evaluation of diastolic filling of left ventricle in health and disease: Doppler echocardiography is the clinician’s Rosetta Stone. J Am Coll Cardiol 30:8–18
Frommelt PC (2006) Echocardiographic measures of diastolic function in pediatric heart disease. Curr Opin Cardiol 21:194–199
Balzano R, Lindblad YT, Vavilis G, Jogestrand T, Berg UB, Krmar RT (2011) Use of annual ABPM, and repeated carotid scan and echocardiography to monitor cardiovascular health over nine yr in pediatric and young adult renal transplant recipients. Pediatr Transplant 15:635–641
Wikland KA, Luo ZC, Niklasson A, Karlberg J (2002) Swedish population-based longitudinal reference values from birth to 18 years of age for height, weight and head circumference. Acta Paediatr 91:739–754
Rolland-Cachera MF, Sempe M, Guilloud-Bataille M, Patois E, Pequignot-Guggenbuhl F, Fautrad V (1982) Adiposity indices in children. Am J Clin Nutr 36:178–184
Mitsnefes MM, Kimball TR, Kartal J, Witt SA, Glascock BJ, Khoury PR, Daniels SR (2006) Progression of left ventricular hypertrophy in children with early chronic kidney disease: 2-year follow-up study. J Pediatr 149:671–675
El-Husseini AA, Sheashaa HA, Hassan NA, El-Demerdash FM, Sobh MA, Ghoneim MA (2004) Echocardiographic changes and risk factors for left ventricular hypertrophy in children and adolescents after renal transplantation. Pediatr Transplant 8:249–254
Matteucci MC, Chinali M, Rinelli G, Wuhl E, Zurowska A, Charbit M, Pongiglione G, Schaefer F (2013) Change in cardiac geometry and function in CKD children during strict bp control: a randomized study. Clin J Am Soc Nephrol 8:203–210
Matsushita K, van der Velde M, Astor BC, Woodward M, Levey AS, de Jong PE, Coresh J, Gansevoort RT (2010) Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet 375:2073–2081
Edfeldt K, Agerberth B, Rottenberg ME, Gudmundsson GH, Wang XB, Mandal K, Xu Q, Yan ZQ (2006) Involvement of the antimicrobial peptide LL-37 in human atherosclerosis. Arterioscler Thromb Vasc Biol 26:1551–1557
Kanbay M, Ikizek M, Solak Y, Selcoki Y, Uysal S, Armutcu F, Eryonucu B, Covic A, Johnson RJ (2011) Uric acid and pentraxin-3 levels are independently associated with coronary artery disease risk in patients with stage 2 and 3 kidney disease. Am J Nephrol 33:325–331
Tong M, Carrero JJ, Qureshi AR, Anderstam B, Heimburger O, Barany P, Axelsson J, Alvestrand A, Stenvinkel P, Lindholm B, Suliman ME (2007) Plasma pentraxin 3 in patients with chronic kidney disease: associations with renal function, protein-energy wasting, cardiovascular disease, and mortality. Clin J Am Soc Nephrol 2:889–897
Kirkpantur A, Kahraman S, Genctoy G, Altun B, Abali G, Arici M, Turgan C (2008) The interleukin-10 promoter genotype predicts diastolic dysfunction in maintenance hemodialysis patients. Hemodial Int 12:352–361
Canpolat N, Caliskan S, Sever L, Guzeltas A, Kantarci F, Candan C, Civilibal M, Kasapcopur O, Arisoy N (2012) Glucose intolerance: is it a risk factor for cardiovascular disease in children with chronic kidney disease? Pediatr Nephrol 27:627–635
Acknowledgments
Ylva Tranæus Lindblad was partly supported by grants from the Swedish Kidney Foundation, as well as those from the Jerring-, Freemason-, Swärd/Ekelund-, Samaritan- and Signe Olof Wallenius- Foundations. Financial support was also provided by the Society of child-welfare and through the regional agreement on medical training and clinical research (ALF) between Stockholm county council and the Karolinska Institute. The authors also wish to thank the nurses and staff at the Pediatric Nephrology Department at Astrid Lindgren Pediatric Hospital Huddinge, as well as the staff at the renal research lab. Special thanks is given to Abdul Rashid Qureshi who checked and reanalyzed the multiple regression statistical analyses.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lindblad, Y.T., Axelsson, J., Balzano, R. et al. Left ventricular diastolic dysfunction by tissue Doppler echocardiography in pediatric chronic kidney disease. Pediatr Nephrol 28, 2003–2013 (2013). https://doi.org/10.1007/s00467-013-2504-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00467-013-2504-x