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Echocardiographic manifestations in end-stage renal disease

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Abstract

End-stage renal disease (ESRD) is a common but profound clinical condition, and it is associated with extremely increased morbidity and mortality. ESRD can represent four major echocardiographic findings―myocardial hypertrophy, heart failure, valvular calcification, and pericardial effusion. Multiple factors interplay leading to these abnormalities, including pressure/volume overload, oxidative stress, and neurohormonal imbalances. Uremic cardiomyopathy is characterized by left ventricular (LV) hypertrophy and marked diastolic dysfunction. In ESRD patients on hemodialysis, LV geometry is changeable bidirectionally between concentric and eccentric hypertrophy, depending upon changes in corporal fluid volume and arterial pressure, which eventually results in a characteristic of LV systolic dysfunction. Speckle tracking echocardiography enabling to detect subclinical disease might help prevent future advancement to heart failure. Heart valve calcification also is common in ESRD, keeping in mind which progresses faster than expected. In a modern era, pericardial effusion observed in ESRD patients tends to result from volume overload, rather than pericarditis. In this review, we introduce and discuss those four echocardiography-assessed findings of ESRD, with which known and conceivable pathophysiologies for each are incorporated.

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References

  1. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, Parfrey P, Pfeffer M, Raij L, Spinosa DJ, Wilson PW (2003) American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108(17):2154–2169. https://doi.org/10.1161/01.CIR.0000095676.90936.80

  2. Ix JH, Shlipak MG, Liu HH, Schiller NB, Whooley MA (2003) Association between renal insufficiency and inducible ischemia in patients with coronary artery disease: the heart and soul study. J Am Soc Nephrol 14(12):3233–3238. https://doi.org/10.1097/01.asn.0000095642.25603.7a

  3. Law JP, Price AM, Pickup L, Radhakrishnan A, Weston C, Jones AM, McGettrick HM, Chua W, Steeds RP, Fabritz L, Kirchhof P, Pavlovic D, Townend JN, Ferro CJ (2020) Clinical potential of targeting fibroblast growth factor-23 and αKlotho in the treatment of uremia cardiomyopathy. J Am Heart Assoc 9(7):e016041. https://doi.org/10.1161/JAHA.120.016041

    Article  PubMed  PubMed Central  Google Scholar 

  4. De Lima JJG, Macedo TA, Gowdak LHW, David-Neto E, Bortolotto LA (2022) Diastolic and systolic left ventricular dysfunction and mortality in chronic kidney disease patients on haemodialysis. Nephrology (Carlton) 27(1):66–73. https://doi.org/10.1111/nep.13960

  5. Pecoits-Filho R, Barberato SH (2010) Echocardiography in chronic kidney disease: diagnostic and prognostic implications. Nephron Clin Pract 114(4):c242–247. https://doi.org/10.1159/000276575

  6. Taddei S, Nami R, Bruno RM, Quatrini I, Nuti R (2011) Hypertension, left ventricular hypertrophy and chronic kidney disease. Heart Fail Rev 16(6):615–620. https://doi.org/10.1007/s10741-010-9197-z

  7. Mall G, Huther W, Schneider J, Lundin P, Ritz E (1990) Diffuse intermyocardiocytic fibrosis in uraemic patients. Nephrol Dial Transplant 5(1):39–44. https://doi.org/10.1093/ndt/5.1.39

    Article  CAS  PubMed  Google Scholar 

  8. Aoki J, Ikari Y, Nakajima H, Mori M, Sugimoto T, Hatori M, Tanimoto S, Amiya E, Hara K (2005) Clinical and pathologic characteristics of dilated cardiomyopathy in hemodialysis patients. Kidney Int 67(1):333–340. https://doi.org/10.1111/j.1523-1755.2005.00086.x

    Article  PubMed  Google Scholar 

  9. Garikapati K, Goh D, Khanna S, Echampati K (2021) Uraemic cardiomyopathy: a review of current literature. Clin Med Insights Cardiol 15:1179546821998347. https://doi.org/10.1177/1179546821998347

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wang X, Shapiro JI (2019) Evolving concepts in the pathogenesis of uraemic cardiomyopathy. Nat Rev Nephrol 15(3):159–175. https://doi.org/10.1038/s41581-018-0101-8

    Article  PubMed  Google Scholar 

  11. Gansevoort RT, Correa-Rotter R, Hemmelgarn BR, Jafar TH, Heerspink HJ, Mann JF, Matsushita K, Wen CP (2013) Chronic kidney disease and cardiovascular risk: epidemiology, mechanisms, and prevention. Lancet 382(9889):339–352. https://doi.org/10.1016/S0140-6736(13)60595-4

    Article  PubMed  Google Scholar 

  12. Vallianou NG, Mitesh S, Gkogkou A, Geladari E (2019) Chronic kidney disease and cardiovascular disease: is there any relationship? Curr Cardiol Rev 9;15(1):55–63. https://doi.org/10.2174/1573403X14666180711124825

  13. Kakani E, Elyamny M, Ayach T, El-Husseini A (2019) Pathogenesis and management of vascular calcification in CKD and dialysis patients. Semin Dial 32(6):553–561. https://doi.org/10.1111/sdi.12840

    Article  PubMed  Google Scholar 

  14. McIntyre CW, John SG, Jefferies HJ (2008) Advances in the cardiovascular assessment of patients with chronic kidney disease. NDT Plus 1(6):383–391. https://doi.org/10.1093/ndtplus/sfn146

    Article  PubMed  PubMed Central  Google Scholar 

  15. Foley RN, Parfrey PS, Harnett JD, Kent GM, Martin CJ, Murray DC, Barre PE (1995) Clinical and echocardiographic disease in patients starting end-stage renal disease therapy. Kidney Int 47(1):186–192. https://doi.org/10.1038/ki.1995.22

    Article  CAS  PubMed  Google Scholar 

  16. London GM, Pannier B, Guerin AP, Blacher J, Marchais SJ, Darne B, Metivier F, Adda H, Safar ME (2001) Alterations of left ventricular hypertrophy and survival of patients receiving hemodialysis: follow-up of an interventional study. J Am Soc Nephrol 12(12):2759–2767. https://doi.org/10.1681/ASN.V12122759

    Article  PubMed  Google Scholar 

  17. Zoccali C, Benedetto FA, Mallamaci F, Tripepi G, Giacone G, Cataliotti A, Seminara G, Stancanelli B, Malatino LS (2004) Prognostic value of echocardiographic indicators of left ventricular systolic function in asymptomatic dialysis patients. J Am Soc Nephrol 15(4):1029–1037. https://doi.org/10.1097/01.asn.0000117977.14912.91

    Article  PubMed  Google Scholar 

  18. McCullough PA, Roberts WC (2016) Influence of chronic renal failure on cardiac structure. J Am Coll Cardiol 67(10):1183–1185. https://doi.org/10.1016/j.jacc.2015.11.065

    Article  PubMed  Google Scholar 

  19. Alhaj E, Alhaj N, Rahman I, Niazi TO, Berkowitz R, Klapholz M (2013) Uremic cardiomyopathy: an underdiagnosed disease. Congest Heart Fail 19(4):E40-45. https://doi.org/10.1111/chf.12030

    Article  PubMed  Google Scholar 

  20. Zoccali C, Moissl U, Chazot C, Mallamaci F, Tripepi G, Arkossy O, Wabel P, Stuard S (2017) Chronic fluid overload and mortality in ESRD. J Am Soc Nephrol 28(8):2491–2497. https://doi.org/10.1681/ASN.2016121341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. London GM (2002) Left ventricular alterations and end-stage renal disease. Nephrol Dial Transplant 17(Suppl 1):29–36. https://doi.org/10.1093/ndt/17.suppl_1.29

    Article  PubMed  Google Scholar 

  22. Lambers Heerspink HJ, de Borst MH, Bakker SJ, Navis GJ (2013) Improving the efficacy of RAAS blockade in patients with chronic kidney disease. Nat Rev Nephrol 9(2):112–121. https://doi.org/10.1038/nrneph.2012.281

    Article  CAS  PubMed  Google Scholar 

  23. Franssen CF, Navis G (2013) Chronic kidney disease: RAAS blockade and diastolic heart failure in chronic kidney disease. Nat Rev Nephrol 9(4):190–192. https://doi.org/10.1038/nrneph.2013.39

    Article  CAS  PubMed  Google Scholar 

  24. Park J (2012) Cardiovascular risk in chronic kidney disease: role of the sympathetic nervous system. Cardiol Res Pract 2012:319432. https://doi.org/10.1155/2012/319432

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schlaich MP, Socratous F, Hennebry S, Eikelis N, Lambert EA, Straznicky N, Esler MD, Lambert GW (2009) Sympathetic activation in chronic renal failure. J Am Soc Nephrol 20(5):933–939. https://doi.org/10.1681/ASN.2008040402

    Article  PubMed  Google Scholar 

  26. Dzau VJ (1993) Tissue renin-angiotensin system in myocardial hypertrophy and failure. Arch Intern Med 153(8):937–942

    Article  CAS  PubMed  Google Scholar 

  27. Xu J, Carretero OA, Liao TD, Peng H, Shesely EG, Xu J, Liu TS, Yang JJ, Reudelhuber TL, Yang XP (2010) Local angiotensin II aggravates cardiac remodeling in hypertension. Am J Physiol Heart Circ Physiol 299(5):H1328-1338. https://doi.org/10.1152/ajpheart.00538.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Barki-Harrington L, Perrino C, Rockman HA (2004) Network integration of the adrenergic system in cardiac hypertrophy. Cardiovasc Res 63(3):391–402. https://doi.org/10.1016/j.cardiores.2004.03.011

    Article  CAS  PubMed  Google Scholar 

  29. Grabner A, Faul C (2016) The role of fibroblast growth factor 23 and Klotho in uremic cardiomyopathy. Curr Opin Nephrol Hypertens 25(4):314–324. https://doi.org/10.1097/MNH.0000000000000231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Quarles LD (2008) Endocrine functions of bone in mineral metabolism regulation. J Clin Invest 118(12):3820–3828. https://doi.org/10.1172/JCI36479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Faul C, Amaral AP, Oskouei B, Hu MC, Sloan A, Isakova T, Gutiérrez OM, Aguillon-Prada R, Lincoln J, Hare JM, Mundel P, Morales A, Scialla J, Fischer M, Soliman EZ, Chen J, Go AS, Rosas SE, Nessel L, Townsend RR, Feldman HI, St John Sutton M, Ojo A, Gadegbeku C, Di Marco GS, Reuter S, Kentrup D, Tiemann K, Brand M, Hill JA, Moe OW, Kuro-O M, Kusek JW, Keane MG, Wolf M (2011) FGF23 induces left ventricular hypertrophy. J Clin Invest 121(11):4393–4408. https://doi.org/10.1172/JCI46122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Mitsnefes MM, Betoko A, Schneider MF, Salusky IB, Wolf MS, Jüppner H, Warady BA, Furth SL, Portale AA (2018) FGF23 and left ventricular hypertrophy in children with CKD. Clin J Am Soc Nephrol 13(1):45–52

    Article  CAS  PubMed  Google Scholar 

  33. Hu MC, Shi M, Cho HJ, Adams-Huet B, Paek J, Hill K, Shelton J, Amaral AP, Faul C, Taniguchi M, Wolf M (1015) Klotho and phosphate are modulators of pathologic uremic cardiac remodeling. J Am Soc Nephrol 26(6):1290–302. https://doi.org/10.1681/ASN.2014050465

  34. Hu MC, Shiizaki K, Kuro-o M, Moe OW (2013) Fibroblast growth factor 23 and Klotho: physiology and pathophysiology of an endocrine network of mineral metabolism. Annu Rev Physiol 75:503–533. https://doi.org/10.1146/annurev-physiol-030212-183727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Schlüter KD, Piper HM (1998) Cardiovascular actions of parathyroid hormone and parathyroid hormone-related peptide. Cardiovasc Res 37(1):34–41. https://doi.org/10.1016/s0008-6363(97)00194-6

    Article  PubMed  Google Scholar 

  36. Schlüter KD, Piper HM (1998) Left ventricular hypertrophy and parathyroid hormone: a causal connection? Cardiovasc Res 39(2):523–524. https://doi.org/10.1016/s0008-6363(98)00097-2

    Article  PubMed  Google Scholar 

  37. Tzikos G, Doundoulakis I, Doutsini S, Adamidou F, Zafeiropoulos S, Koliastasis L, Manani C, Pliakos I, Papavramidis T (2023) Effects of parathyroidectomy on left ventricular mass in patients with hyperparathyroidism. Cureus 15(1):e33429. https://doi.org/10.7759/cureus.33429

    Article  PubMed  PubMed Central  Google Scholar 

  38. Stefenelli T, Abela C, Frank H, Koller-Strametz J, Globits S, Bergler-Klein J, Niederle B (1997) Cardiac abnormalities in patients with primary hyperparathyroidism: implications for follow-up. J Clin Endocrinol Metab 82(1):106–112. https://doi.org/10.1210/jcem.82.1.3666

    Article  CAS  PubMed  Google Scholar 

  39. Tzikos G, Doundoulakis I, Doutsini S, Adamidou F, Zafeiropoulos S, Koliastasis L, Manani C, Pliakos I, Papavramidis T (2023) Effect of parathyroidectomy on left ventricular mass index in patients with primary hyperparathyroidism. Cureus 5(1):e33429. https://doi.org/10.7759/cureus.33429

    Article  Google Scholar 

  40. Nasri H, Baradaran A, Naderi AS (2004) Close association between parathyroid hormone and left ventricular function and structure in end-stage renal failure patients under maintenance hemodialysis. Bratisl Lek Listy 105(10–11):368–373

    CAS  PubMed  Google Scholar 

  41. 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 13(7):1894–1900. https://doi.org/10.1097/01.asn.0000019900.87535.43

    Article  Google Scholar 

  42. Becker B, Kronenberg F, Kielstein JT, Haller H, Morath C, Ritz E, Fliser D (2005) MMKD Study Group. Renal insulin resistance syndrome, adiponectin and cardiovascular events in patients with kidney disease: the mild and moderate kidney disease study. J Am Soc Nephrol 16(4):1091-1098. https://doi.org/10.1681/ASN.2004090742

  43. Nishimura M, Murase M, Hashimoto T, Kobayashi H, Yamazaki S, Imai R, Okino K, Fujita H, Inoue N, Takahashi H, Ono T (2006) Insulin resistance and impaired myocardial fatty acid metabolism in dialysis patients with normal coronary arteries. Kidney Int 69(3):553–559. https://doi.org/10.1038/sj.ki.5000100

  44. Khedr E, El-Sharkawy M, Abdulwahab S, Eldin EN, Ali M, Youssif A, Ahmed B (2009) Effect of recombinant human erythropoietin on insulin resistance in hemodialysis patients. Hemodial Int 13(3):340–346. https://doi.org/10.1111/j.1542-4758.2009.00367.x

    Article  PubMed  Google Scholar 

  45. Levin A, Bakris GL, Molitch M, Smulders M, Tian J, Williams LA, Andress DL (2007) Prevalence of abnormal serum vitamin D, PTH, calcium, and phosphorus in patients with chronic kidney disease: results of the study to evaluate early kidney disease. Kidney Int 71(1):31–38. https://doi.org/10.1038/sj.ki.5002009

    Article  CAS  PubMed  Google Scholar 

  46. Semple D, Smith K, Bhandari S, Seymour AM (2011) Uremic cardiomyopathy and insulin resistance: a critical role for akt? J Am Soc Nephrol 22(2):207–215. https://doi.org/10.1681/ASN.2009090900

    Article  CAS  PubMed  Google Scholar 

  47. Matsui T, Rosenzweig A (2005) Convergent signal transduction pathways controlling cardiomyocyte survival and function: the role of PI 3-kinase and Akt. J Mol Cell Cardiol 38(1):63–71. https://doi.org/10.1016/j.yjmcc.2004.11.005

    Article  CAS  PubMed  Google Scholar 

  48. Sahn DJ, DeMaria A, Kisslo J, Weyman A (1978) Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58(6):1072–1083. https://doi.org/10.1161/01.cir.58.6.1072

    Article  CAS  PubMed  Google Scholar 

  49. de Simone G (2003) Left ventricular geometry and hypotension in end-stage renal disease: a mechanical perspective. J Am Soc Nephrol 14(10):2421–2427. https://doi.org/10.1097/01.asn.0000088724.66957.fc

    Article  PubMed  Google Scholar 

  50. de Simone G, Devereux RB (2002) Rationale of echocardiographic assessment of left ventricular wall stress and midwall mechanics in hypertensive heart disease. Eur J Echocardiogr 3(3):192–198. https://doi.org/10.1053/euje.2002.0163

    Article  PubMed  Google Scholar 

  51. London GM, Fabiani F, Marchais SJ, de Vernejoul MC, Guerin AP, Safar ME, Metivier F, Llach F (1987) Uremic cardiomyopathy: an inadequate left ventricular hypertrophy. Kidney Int 31(4):973–980. https://doi.org/10.1038/ki.1987.94

    Article  CAS  PubMed  Google Scholar 

  52. Jablonski KL, Fedorova OV, Racine ML, Geolfos CJ, Gates PE, Chonchol M, Fleenor BS, Lakatta EG, Bagrov AY, Seals DR (2013) Dietary sodium restriction and association with urinary marinobufagenin, blood pressure, and aortic stiffness. Clin J Am Soc Nephrol 8(11):1952–1959. https://doi.org/10.2215/CJN.00900113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bolignano D, De Rosa S, Greco M, Presta P, Patella G, Crugliano G, Sabatino J, Strangio A, Romano LR, Comi A, Cianfrone P, Andreucci M, Dragone F, Indolfi C, Foti DP, Coppolino G (2022) Marinobufagenin, left ventricular geometry and cardiac dysfunction in end-stage kidney disease patients. Int Urol Nephrol 54(10):2581–2589. https://doi.org/10.1007/s11255-022-03161-0

    Article  CAS  PubMed  Google Scholar 

  54. Straumann E, Bertel O, Meyer B, Weiss P, Misteli M, Blumberg A, Jenzer H (1998) Symmetric and asymmetric left ventricular hypertrophy in patients with end-stage renal failure on long-term hemodialysis. Clin Cardiol 21(9):672–678. https://doi.org/10.1002/clc.4960210913

    Article  CAS  PubMed  Google Scholar 

  55. Abbasi AS, Slaughter JC, Allen MW (1978) Asymmetric septal hypertrophy in patients on long-term hemodialysis. Chest 74(5):548–551. https://doi.org/10.1378/chest.74.5.548

    Article  CAS  PubMed  Google Scholar 

  56. Bernardi D, Bernini L, Cini G, Ghione S, Bonechi I (1985) Asymmetric septal hypertrophy and sympathetic overactivity in normotensive hemodialyzed patients. Am Heart J 109(3 Pt 1):539–545. https://doi.org/10.1016/0002-8703(85)90560-5

    Article  CAS  PubMed  Google Scholar 

  57. Borrelli S, De Nicola L, Garofalo C, Paoletti E, Lucà S, Chiodini P, Lucà S, Peruzzu N, Netti A, Lembo E, Stanzione G, Conte G, Minutolo R (2022) Prevalence and renal prognosis of left ventricular diastolic dysfunction in non-dialysis chronic kidney disease patients with preserved systolic function. J Hypertens 40(4):723–731. https://doi.org/10.1097/HJH.0000000000003069

    Article  CAS  PubMed  Google Scholar 

  58. Edwards NC, Moody WE, Chue CD, Ferro CJ, Townend JN, Steeds RP (2014) Defining the natural history of uremic cardiomyopathy in chronic kidney disease: the role of cardiovascular magnetic resonance. JACC Cardiovasc Imaging 7(7):703–714. https://doi.org/10.1016/j.jcmg.2013.09.025

    Article  PubMed  Google Scholar 

  59. Zoccali C, Mallamaci F, Parlongo S, Cutrupi S, Benedetto FA, Tripepi G, Bonanno G, Rapisarda F, Fatuzzo P, Seminara G, Cataliotti A, Stancanelli B, Malatino LS (2002) Plasma norepinephrine predicts survival and incident cardiovascular events in patients with end-stage renal disease. Circulation 105(11):1354–1359. https://doi.org/10.1161/hc1102.105261

    Article  CAS  PubMed  Google Scholar 

  60. Pandey A, Shah SJ, Butler J, Kellogg DL Jr, Lewis GD, Forman DE, Mentz RJ, Borlaug BA, Simon MA, Chirinos JA, Fielding RA, Volpi E, Molina AJA, Haykowsky MJ, Sam F, Goodpaster BH, Bertoni AG, Justice JN, White JP, Ding J, Hummel SL, LeBrasseur NK, Taffet GE, Pipinos II, Kitzman D (2021) Exercise intolerance in older adults with heart failure with preserved ejection fraction: JACC state-of-the-art review. J Am Coll Cardiol 78(11):1166–1187. https://doi.org/10.1016/j.jacc.2021.07.014

    Article  PubMed  PubMed Central  Google Scholar 

  61. Paulus WJ, Tschöpe C (2013) A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 62(4):263–271. https://doi.org/10.1016/j.jacc.2013.02.092

    Article  PubMed  Google Scholar 

  62. Adesso S, Popolo A, Bianco G, Sorrentino R, Pinto A, Autore G, Marzocco S (2013) The uremic toxin indoxyl sulphate enhances macrophage response to LPS. PLoS ONE 8(9):e76778. https://doi.org/10.1371/journal.pone.0076778

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  63. Sakamoto JI, Shikata T, Ito S, Kimura T, Takamoto K, Manabe E, Asakura M, Ishihara M, Tsujino T (2020) Polypharmacy is associated with accelerated deterioration of renal function in cardiovascular outpatients. Cardiol Res 11(1):15–21. https://doi.org/10.14740/cr991

    Article  PubMed  PubMed Central  Google Scholar 

  64. Tuegel C, Bansal N (2017) Heart failure in patients with kidney disease. Heart 103(23):1848–1853. https://doi.org/10.1136/heartjnl-2016-310794

    Article  CAS  PubMed  Google Scholar 

  65. Rostand SG, Sanders C, Kirk KA, Rutsky EA, Fraser RG (1988) Myocardial calcification and cardiac dysfunction in chronic renal failure. Am J Med 85(5):651–657. https://doi.org/10.1016/s0002-9343(88)80237-7

    Article  CAS  PubMed  Google Scholar 

  66. Adhyapak SM, Iyengar SS (2011) Characteristics of a subset of patients with reversible systolic dysfunction in chronic kidney disease. Congest Heart Fail 17(3):120–126. https://doi.org/10.1111/j.1751-7133.2011.00214.x

    Article  CAS  PubMed  Google Scholar 

  67. De Lima JJG, Macedo TA, Gowdak LHW, David-Neto E, Bortolotto LA (2022) Diastolic and systolic left ventricular dysfunction and mortality in chronic kidney disease patients on haemodialysis. Nephrology (Carlton) 27(1):66–73. https://doi.org/10.1111/nep.13960

    Article  PubMed  Google Scholar 

  68. Pecoits-Filho R, Barberato SH (2010) Echocardiography in chronic kidney disease: diagnostic and prognostic implications. Nephron Clin Pract 114(4):c242–247. https://doi.org/10.1159/000276575

  69. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P, Marino P, Oh JK, Popescu BA, Waggoner AD (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 29(4):277–314. https://doi.org/10.1016/j.echo.2016.01.011

    Article  PubMed  Google Scholar 

  70. Mark PB, Johnston N, Groenning BA, Foster JE, Blyth KG, Martin TN, Steedman T, Dargie HJ, Jardine AG (2006) Redefinition of uremic cardiomyopathy by contrast-enhanced cardiac magnetic resonance imaging. Kidney Int 69(10):1839–1845. https://doi.org/10.1038/sj.ki.5000249

    Article  CAS  PubMed  Google Scholar 

  71. Zhang AH, Guo WK, Yu L, Liu WH (2019) Relationship of serum soluble Klotho levels and echocardiographic parameters in patients on maintenance hemodialysis. Kidney Blood Press Res 44(3):396–404. https://doi.org/10.1159/000499200

    Article  CAS  PubMed  Google Scholar 

  72. Alhaj E, Alhaj N, Rahman I, Niazi TO, Berkowitz R, Klapholz M (2013) Uremic cardiomyopathy: an underdiagnosed disease. Congest Heart Fail. 19(4):E40-45. https://doi.org/10.1111/chf.12030

  73. d’Hervé Q, Girerd N, Bozec E, Lamiral Z, Panisset V, Frimat L, Huttin O (2023) Girerd S (2023) Factors associated with changes in echocardiographic parameters following kidney transplantation. Clin Res Cardiol. https://doi.org/10.1007/s00392-023-02203-6

    Article  PubMed  Google Scholar 

  74. Kadappu KK, Abhayaratna K, Boyd A, French JK, Xuan W, Abhayaratna W, Thomas L (2016) Independent echocardiographic markers of cardiovascular involvement in chronic kidney disease: the value of left atrial function and volume. J Am Soc Echocardiogr 29(4):359–367. https://doi.org/10.1016/j.echo.2015.11.019

    Article  PubMed  Google Scholar 

  75. Tripepi G, Benedetto FA, Mallamaci F, Tripepi R, Malatino L, Zoccali C (2006) Left atrial volume in end-stage renal disease: a prospective cohort study. J Hypertens 24(6):1173–1180. https://doi.org/10.1097/01.hjh.0000226208.11184.bb

  76. Paoletti E, Zoccali C (2014) A look at the upper heart chamber: the left atrium in chronic kidney disease. Nephrol Dial Transplant 29(10):1847–1853. https://doi.org/10.1093/ndt/gft482

    Article  CAS  PubMed  Google Scholar 

  77. Zapolski T, Furmaga J, Wysokiński AP, Wysocka A, Rudzki S, Jaroszyński A (2019) The atrial uremic cardiomyopathy regression in patients after kidney transplantation - the prospective echocardiographic study. BMC Nephrol 20(1):152. https://doi.org/10.1186/s12882-019-1333-y

    Article  PubMed  PubMed Central  Google Scholar 

  78. Malik J, Lachmanova J, Kudlicka J, Rocinova K, Valerianova A, Bartkova M, Tesar V (2016) Left atrial dysfunction in end-stage renal disease patients treated by hemodialysis. Nephron 133(3):169–174. https://doi.org/10.1159/000447500

    Article  CAS  PubMed  Google Scholar 

  79. Hassanin N, Alkemary A (2016) Early detection of subclinical uremic cardiomyopathy using two-dimensional speckle tracking echocardiography. Echocardiography 33(4):527–536. https://doi.org/10.1111/echo.13120

    Article  PubMed  Google Scholar 

  80. Kramann R, Erpenbeck J, Schneider RK, Röhl AB, Hein M, Brandenburg VM, van Diepen M, Dekker F, Marx N (2014) Speckle tracking echocardiography detects uremic cardiomyopathy early and predicts cardiovascular mortality in ESRD. J Am Soc Nephrol 25(10):2351–2365. https://doi.org/10.1681/ASN.2013070734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Tadic M, Cuspidi C, Marwick TH (2022) Phenotyping the hypertensive heart. Eur Heart J 43(38):3794–3810. https://doi.org/10.1093/eurheartj/ehac393

    Article  PubMed  Google Scholar 

  82. Pagourelias ED, Mirea O, Duchenne J, Unlu S, Van Cleemput J, Papadopoulos CE, Bogaert J, Vassilikos VP, Voigt JU (2020) Speckle tracking deformation imaging to detect regional fibrosis in hypertrophic cardiomyopathy: a comparison between 2D and 3D echo modalities. Eur Heart J Cardiovasc Imaging 21(11):1262–1272. https://doi.org/10.1093/ehjci/jeaa057

    Article  PubMed  Google Scholar 

  83. 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(6):1218–1225. https://doi.org/10.1093/ndt/gfu004

    Article  CAS  PubMed  Google Scholar 

  84. Krishnasamy R, Isbel NM, Hawley CM, Pascoe EM, Burrage M, Leano R, Haluska BA, Marwick TH (2015) Stanton T (2015) Left ventricular global longitudinal strain (GLS) is a superior predictor of all-cause and cardiovascular mortality when compared to ejection fraction in advanced chronic kidney disease. PLoS ONE 10(5):e0127044. https://doi.org/10.1371/journal.pone.0127044.eCollection

    Article  PubMed  PubMed Central  Google Scholar 

  85. Zhang T, Li J, Cao S (2020) Prognostic value of left ventricular global longitudinal strain in chronic kidney disease patients: a systematic review and meta-analysis. Int Urol Nephrol 52(9):1747–1756. https://doi.org/10.1007/s11255-020-02492-0

    Article  PubMed  Google Scholar 

  86. Hensen LCR, Goossens K, Delgado V, Rotmans JI, Jukema JW, Bax JJ (2017) Prognostic implications of left ventricular global longitudinal strain in predialysis and dialysis patients. Am J Cardiol 120(3):500–504. https://doi.org/10.1016/j.amjcard.2017.04.054

    Article  PubMed  Google Scholar 

  87. Lakkas L, Naka KK, Bechlioulis A, Duni A, Moustakli M, Balafa O, Theodorou I, Katsouras CS, Dounousi E, Michalis LK (2023) Coronary microcirculation and left ventricular diastolic function but not myocardial deformation indices are impaired early in patients with chronic kidney disease. Echocardiography 40(7):600–607. https://doi.org/10.1111/echo.15598

    Article  PubMed  Google Scholar 

  88. Nishimura RA, Abel MD, Hatle LK, Tajik AJ (1989) Assessment of diastolic function of the heart: background and current applications of Doppler echocardiography. Part II. Clinical studies. Mayo Clin Proc 64(2):181–204. https://doi.org/10.1016/s0025-6196(12)65673-0

  89. Mandinov L, Eberli FR, Seiler C, Hess OM (2000) Diastolic heart failure. Cardiovasc Res 45(4):813–825. https://doi.org/10.1016/s0008-6363(99)00399-5

    Article  CAS  PubMed  Google Scholar 

  90. Raggi P (2017) Cardiovascular disease: coronary artery calcification predicts risk of CVD in patients with CKD. Nat Rev Nephrol 13(6):324–326. https://doi.org/10.1038/nrneph.2017.61

    Article  CAS  PubMed  Google Scholar 

  91. Schlieper G, Schurgers L, Brandenburg V, Reutelingsperger C, Floege J (2016) Vascular calcification in chronic kidney disease: an update. Nephrol Dial Transplant 31(1):31–39. https://doi.org/10.1093/ndt/gfv111

    Article  CAS  PubMed  Google Scholar 

  92. Ternacle J, Côté N, Krapf L, Nguyen A, Clavel MA, Pibarot P (2019) Chronic kidney disease and the pathophysiology of valvular heart disease. Can J Cardiol 35(9):1195–1207. https://doi.org/10.1016/j.cjca.2019.05.028

    Article  PubMed  Google Scholar 

  93. Brandenburg VM, Schuh A, Kramann R (2019) Valvular calcification in chronic kidney disease. Adv Chronic Kidney Dis 26(6):464–471. https://doi.org/10.1053/j.ackd.2019.10.004

    Article  PubMed  Google Scholar 

  94. Adeney KL, Siscovick DS, Ix JH, Seliger SL, Shlipak MG, Jenny NS, Kestenbaum BR (2009) Association of serum phosphate with vascular and valvular calcification in moderate CKD. J Am Soc Nephrol 20(2):381–387. https://doi.org/10.1681/ASN.2008040349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Matsuo H, Dohi K, Machida H, Takeuchi H, Aoki T, Nishimura H, Yasutomi M, Senga M, Ichikawa T, Kakuta K, Mizutani Y, Tanoue A, Isaka N, Oosugi K, Koyabu S, Sakurai M, Fukui Y, Kakimoto H, Sugimoto T, Ohnishi T, Murata T, Ishikawa E, Okamoto R, Yamada T, Ogura T, Nishimura Y, Tanigawa T, Nomura S, Nishikawa M, Ito M (2018) Echocardiographic assessment of cardiac structural and functional abnormalities in patients with end-stage renal disease receiving chronic hemodialysis. Circ J 82(2):586–595. https://doi.org/10.1253/circj.CJ-17-0393

    Article  CAS  PubMed  Google Scholar 

  96. Rufino M, García S, Jiménez A, Alvarez A, Miquel R, Delgado P, Marrero D, Torres A, Hernández D, Lorenzo V (2003) Heart valve calcification and calcium x phosphorus product in hemodialysis patients: analysis of optimum values for its prevention. Kidney Int Suppl S115–118. https://doi.org/10.1046/j.1523-1755.63.s85.27.x

  97. Zoppellaro G, Faggin E, Puato M, Pauletto P, Rattazzi M (2012) Fibroblast growth factor 23 and the bone-vascular axis: lessons learned from animal studies. Am J Kidney Dis 59(1):135–144. https://doi.org/10.1053/j.ajkd.2011.07.027

    Article  CAS  PubMed  Google Scholar 

  98. Gutiérrez OM, Mannstadt M, Isakova T, Rauh-Hain JA, Tamez H, Shah A, Smith K, Lee H, Thadhani R, Jüppner H, Wolf M (2008) Fibroblast growth factor 23 and mortality among patients undergoing hemodialysis. N Engl J Med 359(6):584–592. https://doi.org/10.1056/NEJMoa0706130

    Article  PubMed  PubMed Central  Google Scholar 

  99. Kirkpantur A, Balci M, Gurbuz OA, Afsar B, Canbakan B, Akdemir R, Ayli MD (2011) Serum fibroblast growth factor-23 (FGF-23) levels are independently associated with left ventricular mass and myocardial performance index in maintenance haemodialysis patients. Nephrol Dial Transplant 26(4):1346–1354. https://doi.org/10.1093/ndt/gfq539

    Article  CAS  PubMed  Google Scholar 

  100. Di Lullo L, Gorini A, Bellasi A, Morrone LF, Rivera R, Russo L, Santoboni A, Russo D (2015) Fibroblast growth factor 23 and parathyroid hormone predict extent of aortic valve calcifications in patients with mild to moderate chronic kidney disease. Clin Kidney J 8(6):732–736. https://doi.org/10.1093/ckj/sfv073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Fox CS, Larson MG, Vasan RS, Guo CY, Parise H, Levy D, Leip EP, O’donnell CJ, D’Agostino RB Sr, Benjamin EJ, (2006) Cross-sectional association of kidney function with valvular and annular calcification: the Framingham heart study. J Am Soc Nephrol 17(2):521–527. https://doi.org/10.1681/ASN.2005060627

    Article  PubMed  Google Scholar 

  102. Braun J, Oldendorf M, Moshage W, Heidler R, Zeitler E, Luft FC (1996) Electron beam computed tomography in the evaluation of cardiac calcification in chronic dialysis patients. Am J Kidney Dis 27(3):394–401. https://doi.org/10.1016/s0272-6386(96)90363-7

    Article  CAS  PubMed  Google Scholar 

  103. Perkovic V, Hunt D, Griffin SV, du Plessis M, Becker GJ (2003) Accelerated progression of calcific aortic stenosis in dialysis patients. Nephron Clin Pract 94(2):c40-45. https://doi.org/10.1159/000071280

    Article  PubMed  Google Scholar 

  104. Mohty D, Magne J, Deltreuil M, Aboyans V, Echahidi N, Cassat C, Pibarot P, Laskar M, Virot P (2013) Outcome and impact of surgery in paradoxical low-flow, low-gradient severe aortic stenosis and preserved left ventricular ejection fraction: a cardiac catheterization study. Circulation 128(11 Suppl 1):S235-242. https://doi.org/10.1161/CIRCULATIONAHA.112.000031

    Article  PubMed  Google Scholar 

  105. Clavel MA, Dumesnil JG, Capoulade R, Mathieu P, Sénéchal M, Pibarot P (2012) Outcome of patients with aortic stenosis, small valve area, and low-flow, low-gradient despite preserved left ventricular ejection fraction. J Am Coll Cardiol 60(14):1259–1267. https://doi.org/10.1016/j.jacc.2011.12.054

    Article  PubMed  Google Scholar 

  106. Nestico PF, Depace NL, Morganroth J, Kotler MN, Ross J (1984) Mitral annular calcification: clinical, pathophysiology, and echocardiographic review. Am Heart J 107(5 Pt 1):989–996. https://doi.org/10.1016/0002-8703(84)90840-8

    Article  CAS  PubMed  Google Scholar 

  107. Silbiger JJ (2012) Anatomy, mechanics, and pathophysiology of the mitral annulus. Am Heart J 164(2):163–176. https://doi.org/10.1016/j.ahj.2012.05.014

  108. Movahed MR, Saito Y, Ahmadi-Kashani M, Ebrahimi R (2007) Mitral annulus calcification is associated with valvular and cardiac structural abnormalities. Cardiovasc Ultrasound 5:14. https://doi.org/10.1186/1476-7120-5-14

    Article  PubMed  PubMed Central  Google Scholar 

  109. Muddassir SM, Pressman GS (2007) Mitral annular calcification as a cause of mitral valve gradients. Int J Cardiol 123(1):58–62. https://doi.org/10.1016/j.ijcard.2006.11.142

    Article  PubMed  Google Scholar 

  110. Alpert MA, Ravenscraft MD (2003) Pericardial involvement in end-stage renal disease. Am J Med Sci 325(4):228–236. https://doi.org/10.1097/00000441-200304000-00009

    Article  PubMed  Google Scholar 

  111. Langendorf R, Pirani CL (1947) The heart in uremia; an electrocardiographic and pathologic study. Am Heart J 33(3):282–307. https://doi.org/10.1016/0002-8703(47)90657-1

    Article  CAS  PubMed  Google Scholar 

  112. Wacker W, Merrill JP (1954) Uremic pericarditis in acute and chronic renal failure. J Am Med Assoc 156(8):764–765. https://doi.org/10.1001/jama.1954.02950080012005

    Article  CAS  PubMed  Google Scholar 

  113. Cochran M, Lawton S, Rowlands LM (1979) Fibrinous pericarditis and fibrinolysis in chronic dialysis patients. Clin Nephrol 11(1):23–25

    CAS  PubMed  Google Scholar 

  114. Ravi V, Iskander F, Saini A, Brecklin C, Doukky R (2018) Clinical predictors and outcomes of patients with pericardial effusion in chronic kidney disease. Clin Cardiol 41(5):660–665. https://doi.org/10.1002/clc.22946

    Article  PubMed  PubMed Central  Google Scholar 

  115. Rehman KA, Betancor J, Xu B, Kumar A, Rivas CG, Sato K, Wong LP, Asher CR, Klein AL (2017) Uremic pericarditis, pericardial effusion, and constrictive pericarditis in end-stage renal disease: insights and pathophysiology. Clin Cardiol 40(10):839–846. https://doi.org/10.1002/clc.22770

    Article  PubMed  PubMed Central  Google Scholar 

  116. Aghsaeifard Z, Firouzi R, Alizadeh R (2022) Predisposing factors and uremic pericardial effusion among ESRD patients undergoing dialysis. Ann Med Surg (Lond) 77:103579. https://doi.org/10.1016/j.amsu.2022.103579

    Article  PubMed  Google Scholar 

  117. Yoshida K, Shiina A, Asano Y, Hosoda S (1980) Uremic pericardial effusion: detection and evaluation of uremic pericardial effusion by echocardiography. Clin Nephrol 13(6):260–268

    CAS  PubMed  Google Scholar 

  118. Frommer JP, Young JB, Ayus JC (1985) Asymptomatic pericardial effusion in uremic patients: effect of long-term dialysis. Nephron 39(4):296–301. https://doi.org/10.1159/000183393

    Article  CAS  PubMed  Google Scholar 

  119. Rostand SG, Rutsky EA (1990) Pericarditis in end-stage renal disease. Cardiol Clin 8(4):701–707

    Article  CAS  PubMed  Google Scholar 

  120. Tonelli M, Pfeffer MA (2007) Kidney disease and cardiovascular risk. Annu Rev Med 58:123–139. https://doi.org/10.1146/annurev.med.58.071105.111123

    Article  CAS  PubMed  Google Scholar 

  121. Kleynberg RL, Kleynberg VM, Kleynberg LM, Farahmandian D (2011) Chronic constrictive pericarditis in association with end-stage renal disease. Int J Nephrol 469602. https://doi.org/10.1016/j.ahj.2012.05.014

  122. Marcu CB, Caracciolo E, Donohue T (2005) Rapid progression of pericardial calcification in a patient with end-stage renal disease. Catheter Cardiovasc Interv 65(1):43–46. https://doi.org/10.1002/ccd.20361

    Article  PubMed  Google Scholar 

  123. Hateboer N, McGonigle RJ, Lewis CT (1995) Pericardiectomy after two decades of constrictive pericarditis in a patient with chronic renal failure. Nephrol Dial Transplant 10(10):1935–1937

    CAS  PubMed  Google Scholar 

  124. Kleiman JH, Motta J, London E, Pennell JP, Popp RL (1978) Pericardial effusions in patients with end-stage renal disease. Br Heart J 40(2):190–193. https://doi.org/10.1136/hrt.40.2.190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Dad T, Sarnak MJ (2016) Pericarditis and pericardial effusions in end-stage renal disease. Semin Dial 29(5):366–373. https://doi.org/10.1111/sdi.12517

    Article  PubMed  Google Scholar 

  126. Ashraf H, Lee H, Tran KH, Agasthi P, Keddis MT, Unzek S, Narayanasamy H, Wilansky S (2020) Prevalence and outcomes of pericardial effusion in kidney transplant candidates. Am J Cardiol 132:140–146. https://doi.org/10.1016/j.amjcard.2020.07.009

    Article  PubMed  Google Scholar 

  127. Klein AL, Abbara S, Agler DA, Appleton CP, Asher CR, Hoit B, Hung J, Garcia MJ, Kronzon I, Oh JK, Rodriguez ER, Schaff HV, Schoenhagen P, Tan CD, White RD (2013) American Society of Echocardiography clinical recommendations for multimodality cardiovascular imaging of patients with pericardial disease: endorsed by the Society for Cardiovascular Magnetic Resonance and Society of Cardiovascular Computed Tomography. J Am Soc Echocardiogr 26(9):965-1012.e15. https://doi.org/10.1016/j.echo.2013.06.023

    Article  PubMed  Google Scholar 

  128. Martin RP, Bowden R, Filly K, Popp RL (1980) Intrapericardial abnormalities in patients with pericardial effusion. Findings by two-dimensional echocardiography Circulation 61(3):568–572. https://doi.org/10.1161/01.cir.61.3.568

    Article  CAS  PubMed  Google Scholar 

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    Takahide Ito & Kanako Akamatsu

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Ito, T., Akamatsu, K. Echocardiographic manifestations in end-stage renal disease. Heart Fail Rev 29, 465–478 (2024). https://doi.org/10.1007/s10741-023-10376-5

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