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Left ventricular stiffness in paediatric patients with end-stage kidney disease

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Abstract

Background

We tested the hypothesis that myocardial stiffness is altered in paediatric patients with end-stage kidney disease (ESKD) and explored its association with clinical parameters of chronic kidney disease (CKD).

Methods

Thirty-five patients with ESKD (16 males) aged 17.5 ± 3 years old, 18/35 of whom were receiving dialysis and 17 post kidney transplant, were studied. Left ventricular (LV) myocardial stiffness was determined by measurement of diastolic wall strain (DWS) and stiffness index (SI), while LV diastolic function was interrogated by pulsed-wave and tissue Doppler echocardiography.

Results

Compared with available literature data, both dialysis and transplanted patients had significantly lower DWS and greater SI, reduced transmitral early (E) to late diastolic velocity ratio and septal and lateral mitral annular early (e′) diastolic velocities, and greater septal and lateral E/e′ ratios (all p < 0.05). Multivariate analysis revealed that z score of diastolic blood pressure (β = 0.43, p = 0.004) and the duration of renal replacement therapy (β = 0.55, p < 0.001) were significant determinants of LV SI. Subgroup analysis in post-transplant patients showed z score of diastolic blood pressure (β = 0.54, p = 0.025) remained as a significant determinant of LV SI.

Conclusion

Increased LV myocardial stiffness is evident in paediatric dialysis and transplanted patients with ESKD, and is associated with blood pressure and duration of renal replacement therapy.

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References

  1. Gruppen MP, Groothoff JW, Prins M, van der Wouw P, Offringa M, Bos WJ, Davin JC, Heymans HS (2003) Cardiac disease in young adult patients with end-stage renal disease since childhood: a Dutch cohort study. Kidney Int 63:1058–1065. https://doi.org/10.1046/j.1523-1755.2003.00814.x

    Article  PubMed  Google Scholar 

  2. 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. https://doi.org/10.1161/01.CIR.0000020222.63035.C0

    Article  PubMed  Google Scholar 

  3. Schoenmaker NJ, Kuipers IM, van der Lee JH, Tromp WF, van Dyck M, Gewillig M, Blom NA, Groothoff JW (2014) Diastolic dysfunction measured by tissue Doppler imaging in children with end-stage renal disease: a report of the RICH-Q study. Cardiol Young 24:236–244. https://doi.org/10.1017/S1047951113000188

    Article  PubMed  Google Scholar 

  4. 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. https://doi.org/10.1111/j.1523-1755.2004.00525.x

    Article  PubMed  Google Scholar 

  5. Lindblad YT, Axelsson J, Balzano R, Vavilis G, Chromek M, Celsi G, Bárány P (2013) Left ventricular diastolic dysfunction by tissue Doppler echocardiography in pediatric chronic kidney disease. Pediatr Nephrol 28:2003–2013. https://doi.org/10.1007/s00467-013-2504-x

    Article  PubMed  Google Scholar 

  6. Goren A, Glaser J, Drukker A (1993) Diastolic function in children and adolescents on dialysis and after kidney transplantation: an echocardiographic assessment. Pediatr Nephrol 7:725–728. https://doi.org/10.1007/BF01213334

    Article  PubMed  CAS  Google Scholar 

  7. Chavers BM, Solid CA, Sinaiko A, Daniels FX, Chen SC, Collins AJ, Frankenfield DL, Herzog CA (2011) Diagnosis of cardiac disease in pediatric end-stage renal disease. Nephrol Dial Transplant 26:1640–1645. https://doi.org/10.1093/ndt/gfq591

    Article  PubMed  Google Scholar 

  8. López B, González A, Hermida N, Laviades C, Díez J (2008) Myocardial fibrosis in chronic kidney disease: potential benefits of torasemide. Kidney Int Suppl 74:S19–S23. https://doi.org/10.1038/ki.2008.512

    Article  CAS  Google Scholar 

  9. 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. https://doi.org/10.1093/ejechocard/jep007

    Article  PubMed  Google Scholar 

  10. Takeda Y, Sakata Y, Higashimori M, Mano T, Nishio M, Ohtani T, Hori M, Masuyama T, Kaneko M, Yamamoto K (2009) Noninvasive assessment of wall distensibility with the evaluation of diastolic epicardial movement. J Card Fail 15:68–77. https://doi.org/10.1016/j.cardfail.2008.09.004

    Article  PubMed  Google Scholar 

  11. King GJ, Murphy RT, Almuntaser I, Bennett K, Ho E, Brown AS (2008) Alterations in myocardial stiffness in elite athletes assessed by a new Doppler index. Heart 94:1323–1325. https://doi.org/10.1136/hrt.2008.142083

    Article  PubMed  CAS  Google Scholar 

  12. Yu CK, Wong WH, Li VW, Cheung YF (2017) Left ventricular stiffness in adolescents and young adults with repaired tetralogy of fallot. Sci Rep 7:1252. https://doi.org/10.1038/s41598-017-01448-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Ohtani T, Mohammed SF, Yamamoto K, Dunlay SM, Weston SA, Sakata Y, Rodeheffer RJ, Roger VL, Redfield MM (2012) Diastolic stiffness as assessed by diastolic wall strain is associated with adverse remodelling and poor outcomes in heart failure with preserved ejection fraction. Eur Heart J 33:1742–1749. https://doi.org/10.1093/eurheartj/ehs135

    Article  PubMed  PubMed Central  Google Scholar 

  14. Flynn JT, Daniels SR, Hayman LL, Maahs DM, BW MC, Mitsnefes M, Zachariah JP, Urbina EM, American Heart Association Atherosclerosis, Hypertension and Obesity in Youth Committee of the Council on Cardiovascular Disease in the Young (2014) Update: ambulatory blood pressure monitoring in children and adolescents: a scientific statement from the American Heart Association. Hypertension 63:1116–1135. https://doi.org/10.1161/HYP.0000000000000007

    Article  PubMed  CAS  Google Scholar 

  15. Levey AS, Eckardt KU, Tsukamoto Y, Levin A, Coresh J, Rossert J, De Zeeuw D, Hostetter TH, Lameire N, Eknoyan G (2005) Definition and classification of chronic kidney disease: a position statement from kidney disease: improving global outcomes (KDIGO). Kidney Int 67:2089–2100. https://doi.org/10.1111/j.1523-1755.2005.00365.x

    Article  PubMed  Google Scholar 

  16. Lai WW, Geva T, Shirali GS, Frommelt PC, Humes RA, Brook MM, Pignatelli RH, Rychik J, Task Force of the Pediatric Council of the American Society of Echocardiography; Pediatric Council of the American Society of Echocardiography (2006) Guidelines and standards for performance of a pediatric echocardiogram: a report from the Task Force of the Pediatric Council of the American Society of Echocardiography. J Am Soc Echocardiogr 19:1413–1430. https://doi.org/10.1016/j.echo.2006.09.001

    Article  PubMed  Google Scholar 

  17. Mikhail A, Brown C, Williams JA, Mathrani V, Shrivastava R, Evans J, Isaac H, Bhandari S (2017) Renal association clinical practice guideline on anaemia of chronic kidney disease. BMC Nephrol 18:345. https://doi.org/10.1186/s12882-017-0688-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Koshy SM, Geary DF (2008) Anemia in children with chronic kidney disease. Pediatr Nephrol 23:209–219. https://doi.org/10.1007/s00467-006-0381-2

    Article  PubMed  Google Scholar 

  19. Isakova T, Nickolas TL, Denburg M, Yarlagadda S, Weiner DE, Gutiérrez OM, Bansal V, Rosas SE, Nigwekar S, Yee J, Kramer H (2017) KDOQI US commentary on the 2017 KDIGO clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Am J Kidney Dis 70:737–751. https://doi.org/10.1053/j.ajkd.2017.07.019

    Article  PubMed  Google Scholar 

  20. Schmitt CP, Shroff R (2016) Disorders of bone mineral metabolism in chronic kidney disease. In: Geary DF, Schaefer F (eds) Pediatric Kidney Disease. Springer, Berlin Heidelberg, Berlin, pp 1533–1566. https://doi.org/10.1007/978-3-662-52972-0_58

    Chapter  Google Scholar 

  21. Foster BJ, Khoury PR, Kimball TR, Mackie AS, Mitsnefes M (2016) New reference centiles for left ventricular mass relative to lean body mass in children. J Am Soc Echocardiogr 29:441–447. https://doi.org/10.1016/j.echo.2015.12.011

    Article  PubMed  Google Scholar 

  22. Eidem BW, McMahon CJ, Cohen RR, Wu J, Finkelshteyn I, Kovalchin JP, Ayres NA, Bezold LI, O’Brian Smith E, Pignatelli RH (2004) Impact of cardiac growth on Doppler tissue imaging velocities: a study in healthy children. J Am Soc Echocardiogr 17:212–221. https://doi.org/10.1016/j.echo.2003.12.005

    Article  PubMed  Google Scholar 

  23. 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(Supplement 2):555–576. https://doi.org/10.1161/01.HYP.0000143545.54637.af

    Article  CAS  Google Scholar 

  24. Schaefer F, Doyon A, Azukaitis K, Bayazit A, Canpolat N, Duzova A, Niemirska A, Sözeri B, Thurn D, Anarat A, Ranchin B, Litwin M, Caliskan S, Candan C, Baskin E, Yilmaz E, Mir S, Kirchner M, Sander A, Haffner D, Melk A, Wühl E, Shroff R, Querfeld U, 4C Study Consortium (2017) Cardiovascular phenotypes in children with CKD: the 4C Study. Clin J Am Soc Nephrol 12:19–28. https://doi.org/10.2215/CJN.01090216

    Article  PubMed  Google Scholar 

  25. Brady TM, Schneider MF, Flynn JT, Cox C, Samuels J, Saland J, White CT, Furth S, Warady BA, Mitsnefes M (2012) Carotid intima-media thickness in children with CKD: results from the CKiD Study. Clin J Am Soc Nephrol 7:1930–1937. https://doi.org/10.2215/CJN.03130312

    Article  PubMed  PubMed Central  Google Scholar 

  26. Doyon A, Haas P, Erdem S, Ranchin B, Kassai B, Mencarelli F, Lugani F, Harambat J, Matteucci MC, Chinali M, Habbig S, Zaloszyc A, Testa S, Vidal E, Gimpel C, Azukaitis K, Kovacevic A, Querfeld U, Schaefer F (2019) Impaired systolic and diastolic left ventricular function in children with chronic kidney disease – results from the 4C study. Sci Rep 9:11462. https://doi.org/10.1038/s41598-019-46653-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Schraeger JA, Canby CA, Rongish BJ, Kawai M, Tomanek RJ (1994) Normal left ventricular diastolic compliance after regression of hypertrophy. J Cardiovasc Pharmacol 23:349–357

    PubMed  CAS  Google Scholar 

  28. Narayan S, Janicki JS, Shroff SG, Pick R, Weber KT (1989) Myocardial collagen and mechanics after preventing hypertrophy in hypertensive rats. Am J Hypertens 2:675–682. https://doi.org/10.1093/ajh/2.9.675

    Article  PubMed  CAS  Google Scholar 

  29. Matsubara LS, Matsubara BB, Okoshi MP, Cicogna AC, Janicki JS (2000) Alterations in myocardial collagen content affect rat papillary muscle function. Am J Physiol Heart Circ Physiol 279:H1534–H1539. https://doi.org/10.1152/ajpheart.2000.279.4.H1534

    Article  PubMed  CAS  Google Scholar 

  30. Yamamoto K, Masuyamaaa T, Sakata Y, Nishikawa N, Mano T, Yoshida J, Miwa T, Sugawara M, Yamaguchi Y, Ookawara T, Suzuki K, Hori M (2002) Myocardial stiffness is determined by ventricular fibrosis, but not by compensatory or excessive hypertrophy in hypertensive heart. Cardiovasc Res 55:76–82. https://doi.org/10.1016/S0008-6363(02)00341-3

    Article  PubMed  CAS  Google Scholar 

  31. Martin FL, McKie PM, Cataliotti A, Sangaralingham SJ, Korinek J, Huntley BK, Oehler EA, Harders GE, Ichiki T, Mangiafico S, Nath KA, Redfield MM, Chen HH, Burnett JC Jr (2012) Experimental mild renal insufficiency mediates early cardiac apoptosis, fibrosis, and diastolic dysfunction: a kidney-heart connection. Am J Physiol Regul Integr Comp Physiol 302:R292–R299. https://doi.org/10.1152/ajpregu.00194.2011

    Article  PubMed  CAS  Google Scholar 

  32. Mall G, Huther W, Schneider J, Lundin P, Ritz E (1990) Diffuse intermyocardiocytic fibrosis in uraemic patients. Nephrol Dial Transplant 5:39–44. https://doi.org/10.1093/ndt/5.1.39

    Article  PubMed  CAS  Google Scholar 

  33. Graham-Brown MPM, Patel AS, Stensel DJ, March DS, Marsh A-M, McAdam J, McCann GP, Burton JO (2017) Imaging of myocardial fibrosis in patients with end-stage renal disease: current limitations and future possibilities. Biomed Res Int 2017:5453606. https://doi.org/10.1155/2017/5453606

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Edwards NC, Moody WE, Yuan M, Hayer MK, Ferro CJ, Townend JN, Steeds RP (2015) Diffuse interstitial fibrosis and myocardial dysfunction in early chronic kidney disease. Am J Cardiol 115:1311–1317. https://doi.org/10.1016/j.amjcard.2015.02.015

    Article  PubMed  Google Scholar 

  35. 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–S91. https://doi.org/10.2215/CJN.04860709

    Article  PubMed  Google Scholar 

  36. Naito Y, Tsujino T, Matsumoto M, Sakoda T, Ohyanagi M, Masuyama T (2009) Adaptive response of the heart to long-term anemia induced by iron deficiency. Am J Physiol Heart Circ Physiol 296:H585–H593. https://doi.org/10.1152/ajpheart.00463.2008

    Article  PubMed  CAS  Google Scholar 

  37. Malik J (2018) Heart disease in chronic kidney disease - review of the mechanisms and the role of dialysis access. J Vasc Access 19:3–11. https://doi.org/10.5301/jva.5000815

    Article  PubMed  Google Scholar 

  38. Lijnen P, Petrov V (1999) Renin-angiotensin system, hypertrophy and gene expression in cardiac myocytes. J Mol Cell Cardiol 31:949–970. https://doi.org/10.1006/jmcc.1999.0934

    Article  PubMed  CAS  Google Scholar 

  39. Amann K, Ritz E, Wiest G, Klaus G, Mall G (1994) A role of parathyroid hormone for the activation of cardiac fibroblasts in uremia. J Am Soc Nephrol 4:1814–1819

    PubMed  CAS  Google Scholar 

  40. Saleh FN, Schirmer H, Sundsfjord J, Jorde R (2003) Parathyroid hormone and left ventricular hypertrophy. Eur Heart J 24:2054–2060. https://doi.org/10.1016/j.ehj.2003.09.010

    Article  PubMed  CAS  Google Scholar 

  41. Charnaya O, Moudgil A (2017) Hypertension in the pediatric kidney transplant recipient. Front Pediatr 5:86. https://doi.org/10.3389/fped.2017.00086

    Article  PubMed  PubMed Central  Google Scholar 

  42. Mitsnefes MM (2004) Hypertension and end-organ damage in pediatric renal transplantation. Pediatr Transplant 8:394–399. https://doi.org/10.1111/j.1399-3046.2004.00111.x

    Article  PubMed  Google Scholar 

  43. Galutira PJ, Del Rio M (2012) Understanding renal posttransplantation anemia in the pediatric population. Pediatr Nephrol 27:1079–1085. https://doi.org/10.1007/s00467-011-2036-1

    Article  PubMed  Google Scholar 

  44. Litwin M, Niemirska A (2014) Metabolic syndrome in children with chronic kidney disease and after renal transplantation. Pediatr Nephrol 29:203–216. https://doi.org/10.1007/s00467-013-2500-1

    Article  PubMed  Google Scholar 

  45. Guzzo I, Di Zazzo G, Laurenzi C, Ravà L, Giannone G, Picca S, Dello Strologo L (2011) Parathyroid hormone levels in long-term renal transplant children and adolescents. Pediatr Nephrol 26:2051–2057. https://doi.org/10.1007/s00467-011-1896-8

    Article  PubMed  Google Scholar 

  46. Rozenfeld MN, Podberesky DJ (2018) Gadolinium-based contrast agents in children. Pediatr Radiol 48:1188–1196. https://doi.org/10.1007/s00247-018-4165-1

    Article  PubMed  Google Scholar 

  47. Rutherford E, Talle MA, Mangion K, Bell E, Rauhalammi SM, Roditi G, McComb C, Radjenovic A, Welsh P, Woodward R, Struthers AD, Jardine AG, Patel RK, Berry C, Mark PB (2016) Defining myocardial tissue abnormalities in end-stage renal failure with cardiac magnetic resonance imaging using native T1 mapping. Kidney Int 90:845–852. https://doi.org/10.1016/j.kint.2016.06.014

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Yiu-fai Cheung.

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The study was approved by the Institutional Review Board of the Hospital Authority, Kowloon West Cluster, Hong Kong, China, and the study protocol conformed to approved guidelines and regulations.

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Choi, A.Wm., Fong, Nc., Li, V.Wy. et al. Left ventricular stiffness in paediatric patients with end-stage kidney disease. Pediatr Nephrol 35, 1051–1060 (2020). https://doi.org/10.1007/s00467-020-04484-9

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