Pediatric Nephrology

, Volume 32, Issue 8, pp 1401–1410 | Cite as

Longitudinal assessment of myocardial function in childhood chronic kidney disease, during dialysis, and following kidney transplantation

  • Rawan K. Rumman
  • Ronand Ramroop
  • Rahul Chanchlani
  • Mikaeel Ghany
  • Diane Hebert
  • Elizabeth A. Harvey
  • Rulan S. Parekh
  • Luc Mertens
  • Michael Grattan
Original Article

Abstract

Background

Childhood chronic kidney disease (CKD) and dialysis are associated with increased long-term cardiovascular risk. We examined subclinical alterations in myocardial mechanics longitudinally in children with CKD, during dialysis, and following renal transplantation.

Methods

Forty-eight children with CKD (stage III or higher) who received kidney transplants from 2008 to 2014 were included in a retrospective study and compared to 192 age- and sex-matched healthy children. Measurements of cardiac systolic and diastolic function were performed, and global longitudinal strain (GLS) and circumferential strain (GCS) were measured by speckle-tracking echocardiography at CKD, during dialysis, and 1 year following kidney transplantation. Mixed-effects modeling examined changes in GLS and GCS over different disease stages.

Results

Children with CKD had a mean age of 10 ± 5 years and 67% were male. Eighteen children received preemptive transplantation. Children with CKD had increased left ventricular mass, lower GLS, and impaired diastolic function (lower E/A ratio and E′ velocities) than healthy children. Changes in left ventricular diastolic parameters persisted during dialysis and after renal transplantation. Dialysis was associated with reduced GLS compared to CKD (β = 1.6, 95% confidence interval 0.2–3.0); however, this was not significant after adjustment for systolic blood pressure and CKD duration. Post-transplantation GLS levels were similar to those at CKD assessment. GCS was unchanged during dialysis but significantly improved following transplantation.

Conclusions

There are differences in diastolic parameters in childhood CKD that persist during dialysis and after transplantation. Systolic parameters are preserved, with significant improvement in systolic myocardial deformation following transplantation. The impact of persistent diastolic changes on long-term outcomes requires further investigation.

Keywords

Chronic kidney disease Dialysis Kidney transplant Myocardial mechanics Systolic strain Children 

Supplementary material

467_2017_3622_MOESM1_ESM.doc (48 kb)
Supplementary Table 1(DOC 48 kb)
467_2017_3622_MOESM2_ESM.doc (72 kb)
Supplementary Table 2(DOC 71 kb)

References

  1. 1.
    Wilson AC, Mitsnefes MM (2009) Cardiovascular disease in CKD in children: update on risk factors, risk assessment, and management. Am J Kidney Dis 54:345–360CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Mitsnefes MM (2012) Cardiovascular disease in children with chronic kidney disease. J Am Soc Nephrol 23:578–585CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Lal AK, de Biasi AR, Alexander S, Rosenthal DN, Sutherland SM (2012) End-stage renal disease and cardiomyopathy in children: cardiac effects of renal transplantation. Transplantation 93:182–187CrossRefPubMedGoogle Scholar
  4. 4.
    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 43:721–726CrossRefPubMedGoogle Scholar
  5. 5.
    Kim GB, Kwon BS, Kang HG, Ha JW, Ha IS, Noh CI, Choi JY, Kim SJ, Yun YS, Bae EJ (2009) Cardiac dysfunction after renal transplantation; incomplete resolution in pediatric population. Transplantation 87:1737–1743CrossRefPubMedGoogle Scholar
  6. 6.
    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 27:835–841CrossRefPubMedGoogle Scholar
  7. 7.
    Bozbas H, Altin C, Karacaglar E, Kanyilmaz S, Yildirir A, Muderrisoglu H, Haberal M (2013) The prevalence and types of cardiovascular disease in patients with end-stage renal disease undergoing renal transplantation. Transplant Proc 45:3478–3480CrossRefPubMedGoogle Scholar
  8. 8.
    Dounousi E, Mitsis M, Naka KK, Pappas C, Lakkas L, Harisis C, Pappas K, Koutlas V, Tzalavra I, Spanos G, Michalis LK, Siamopoulos KC (2014) Differences in cardiac structure assessed by echocardiography between renal transplant recipients and chronic kidney disease patients. Transplant Proc 46:3194–3198CrossRefPubMedGoogle Scholar
  9. 9.
    Gu H, Sinha MD, Li Y, Simpson J, Chowienczyk PJ (2015) Elevated ejection-phase myocardial wall stress in children with chronic kidney disease. Hypertension. 66(4):823–829Google Scholar
  10. 10.
    Malatesta-Muncher R, Wansapura J, Taylor M, Lindquist D, Hor K, Mitsnefes M (2012) Early cardiac dysfunction in pediatric patients on maintenance dialysis and post kidney transplant. Pediatr Nephrol 27:1157–1164CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    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 16:106CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Krishnasamy R, Isbel NM, Hawley CM, Pascoe EM, Leano R, Haluska BA, Stanton T (2014) The association between left ventricular global longitudinal strain, renal impairment and all-cause mortality. Nephrol Dial Transplant 29:1218–1225CrossRefPubMedGoogle Scholar
  13. 13.
    Kramann R, Erpenbeck J, Schneider RK, Rohl AB, Hein M, Brandenburg VM, van Diepen M, Dekker F, Marx N, Floege J, Becker M, Schlieper G (2014) Speckle tracking echocardiography detects uremic cardiomyopathy early and predicts cardiovascular mortality in ESRD. J Am Soc Nephrol 25:2351–2365CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kovacs A, Tapolyai M, Celeng C, Gara E, Faludi M, Berta K, Apor A, Nagy A, Tisler A, Merkely B (2014) Impact of hemodialysis, left ventricular mass and FGF-23 on myocardial mechanics in end-stage renal disease: a three-dimensional speckle tracking study. Int J Cardiovasc Imaging 30:1331–1337CrossRefPubMedGoogle Scholar
  15. 15.
    Fukushima K, Javadi MS, Higuchi T, Bravo PE, Chien D, Lautamaki R, Merrill J, Nekolla SG, Bengel FM (2012) Impaired global myocardial flow dynamics despite normal left ventricular function and regional perfusion in chronic kidney disease: a quantitative analysis of clinical 82Rb PET/CT studies. J Nucl Med 53:887–893CrossRefPubMedGoogle Scholar
  16. 16.
    Edwards NC, Hirth A, Ferro CJ, Townend JN, Steeds RP (2008) Subclinical abnormalities of left ventricular myocardial deformation in early-stage chronic kidney disease: the precursor of uremic cardiomyopathy? J Am Soc Echocardiogr 21:1293–1298CrossRefPubMedGoogle Scholar
  17. 17.
    Panoulas VF, Sulemane S, Konstantinou K, Bratsas A, Elliott SJ, Dawson D, Frankel AH, Nihoyannopoulos P (2015) Early detection of subclinical left ventricular myocardial dysfunction in patients with chronic kidney disease. Eur Heart J Cardiovasc Imaging 16:539–548CrossRefPubMedGoogle Scholar
  18. 18.
    Florescu M, Benea DC, Rimbas RC, Cerin G, Diena M, Lanzzillo G, Enescu OA, Cinteza M, Vinereanu D (2012) Myocardial systolic velocities and deformation assessed by speckle tracking for early detection of left ventricular dysfunction in asymptomatic patients with severe primary mitral regurgitation. Echocardiography 29:326–333CrossRefPubMedGoogle Scholar
  19. 19.
    Friedberg MK, Mertens L (2012) Deformation imaging in selected congenital heart disease: is it evolving to clinical use? J Am Soc Echocardiogr 25:919–931CrossRefPubMedGoogle Scholar
  20. 20.
    Mignot A, Donal E, Zaroui A, Reant P, Salem A, Hamon C, Monzy S, Roudaut R, Habib G, Lafitte S (2010) Global longitudinal strain as a major predictor of cardiac events in patients with depressed left ventricular function: a multicenter study. J Am Soc Echocardiogr 23:1019–1024CrossRefPubMedGoogle Scholar
  21. 21.
    Chinali M, Matteucci MC, Franceschini A, Doyon A, Pongiglione G, Rinelli G, Schaefer F (2015) Advanced parameters of cardiac mechanics in children with CKD: the 4C study. Clin J Am Soc Nephrol 10:1357–1363Google Scholar
  22. 22.
    Chinali M, de Simone G, Matteucci MC, Picca S, Mastrostefano A, Anarat A, Caliskan S, Jeck N, Neuhaus TJ, Peco-Antic A, Peruzzi L, Testa S, Mehls O, Wuhl E, Schaefer F (2007) Reduced systolic myocardial function in children with chronic renal insufficiency. J Am Soc Nephrol 18:593–598CrossRefPubMedGoogle Scholar
  23. 23.
    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 20:629–637CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Grattan MJ, Mertens L (2014) Echocardiographic assessment of ventricular function in pediatric patients: a comprehensive guide. Future Cardiol 10:511–523CrossRefPubMedGoogle Scholar
  25. 25.
    Koopman LP, McCrindle BW, Slorach C, Chahal N, Hui W, Sarkola T, Manlhiot C, Jaeggi ET, Bradley TJ, Mertens L (2012) Interaction between myocardial and vascular changes in obese children: a pilot study. J Am Soc Echocardiogr 25:401–410CrossRefPubMedGoogle Scholar
  26. 26.
    Foster BJ, Mackie AS, Mitsnefes M, Ali H, Mamber S, Colan SD (2008) A novel method of expressing left ventricular mass relative to body size in children. Circulation 117:2769–2775CrossRefPubMedGoogle Scholar
  27. 27.
    Falkner B, Daniels SR (2004) Summary of the fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Hypertension 44:387–388CrossRefPubMedGoogle Scholar
  28. 28.
    Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL (2002) 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11:1–190Google Scholar
  29. 29.
    Simpson JM, Rawlins D, Mathur S, Chubb H, Sinha MD (2013) Systolic and diastolic ventricular function assessed by tissue Doppler imaging in children with chronic kidney disease. Echocardiography 30:331–337CrossRefPubMedGoogle Scholar
  30. 30.
    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 8:203–210CrossRefPubMedGoogle Scholar
  31. 31.
    Chen R, Wu X, Shen LJ, Wang B, Ma MM, Yang Y, Zhao BW (2014) Left ventricular myocardial function in hemodialysis and nondialysis uremia patients: a three-dimensional speckle-tracking echocardiography study. PLoS ONE 9:e100265CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Asp AM, Wallquist C, Rickenlund A, Hylander B, Jacobson SH, Caidahl K, Eriksson MJ (2015) Cardiac remodelling and functional alterations in mild-to-moderate renal dysfunction: comparison with healthy subjects. Clin Physiol Funct Imaging 35:223–230CrossRefPubMedGoogle Scholar
  33. 33.
    Mencarelli F, Fabi M, Corazzi V, Doyon A, Masetti R, Bonetti S, Castiglioni L, Pession A, Montini G (2014) Left ventricular mass and cardiac function in a population of children with chronic kidney disease. Pediatr Nephrol 29:893–900CrossRefPubMedGoogle Scholar
  34. 34.
    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 21:125–132CrossRefPubMedGoogle Scholar
  35. 35.
    Lindblad YT, Axelsson J, Balzano R, Vavilis G, Chromek M, Celsi G, Barany P (2013) Left ventricular diastolic dysfunction by tissue Doppler echocardiography in pediatric chronic kidney disease. Pediatr Nephrol 28:2003–2013Google Scholar

Copyright information

© IPNA 2017

Authors and Affiliations

  • Rawan K. Rumman
    • 1
    • 2
  • Ronand Ramroop
    • 3
  • Rahul Chanchlani
    • 2
    • 4
    • 5
  • Mikaeel Ghany
    • 2
  • Diane Hebert
    • 6
  • Elizabeth A. Harvey
    • 6
  • Rulan S. Parekh
    • 6
    • 7
  • Luc Mertens
    • 3
    • 7
  • Michael Grattan
    • 3
    • 8
  1. 1.Institute of Medical Science, and the Cardiovascular Sciences Collaborative ProgramUniversity of TorontoTorontoCanada
  2. 2.Child Health Evaluative Sciences, Research InstituteThe Hospital for Sick ChildrenTorontoCanada
  3. 3.Division of Cardiology, Labatt Family Heart CenterThe Hospital for Sick ChildrenTorontoCanada
  4. 4.Division of Nephrology, Department of PediatricsMcMaster Children’s Hospital–McMaster UniversityHamiltonCanada
  5. 5.Institute of Health Policy, Management and EvaluationUniversity of TorontoTorontoCanada
  6. 6.Division of NephrologyThe Hospital for Sick Children–University of TorontoTorontoCanada
  7. 7.Department of Pediatrics, Hospital for Sick Children and MedicineUniversity Health Network–University of TorontoTorontoCanada
  8. 8.Department of Pediatrics, Children’s Hospital, London Health Sciences Centre University of Western OntarioLondonCanada

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