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Factors associated with changes in echocardiographic parameters following kidney transplantation

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Abstract

Background

Chronic kidney disease leads to cardiac remodelling of multifactorial origin known as “uraemic cardiomyopathy”, the reversibility of which after kidney transplantation (KT) remains controversial. Our objectives were to assess, in the modern era, changes in echocardiographic parameters following KT and identify predictive clinical and biological factors associated with echocardiographic changes.

Methods

One hundred six patients (mean age 48 ± 16, 73% male) who underwent KT at the University Hospital of Nancy between 2007 and 2018 were retrospectively investigated. Pre- and post-KT echocardiography findings (8.6 months before and 22 months after KT on average, respectively) were centralised, blind-reviewed and compared.

Results

A majority of patients (60%) had either a left ventricular (LV) ejection fraction < 50%, at least moderately abnormal LV mass index or left atrial (LA) dilatation at pretransplanted echocardiography. After KT, LV remodelling and diastolic doppler indices did not significantly change whereas LA volume index (LAVI) increased (35.9 mL/m2 post-KT vs. 30.9 mL/m2 pre-KT, p = 0.006). Advancing age, cardiac valvular disease, delayed graft function, lower post-KT haemoglobin, and more severe post-KT hypertension were associated with higher LAVI after KT. Higher post-KT serum creatinine, more severe post-KT hypertension and lower pre-KT blood calcium levels were associated with a deterioration in LAVI after KT.

Discussion/Conclusion

Adverse remodelling of the left atrial volume occurred after KT, predominantly in patients with lower pre-KT blood calcium, poorer graft function and post-KT hypertension. These results suggest that a better management of modifiable factors such as pre-KT hyperparathyroidism or post-KT hypertension could limit post-KT cardiac remodelling.

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Data availability

Data are available upon reasonable request to the corresponding author.

Abbreviations

ACEI:

Angiotensin converting enzyme inhibitor

ARB:

Angiotensin II receptor blocker

ATG:

Antithymocyte globulin

AVF:

Arteriovenous fistula

BMI:

Body mass index

CV:

Cardiovascular

DSA:

Donor-specific antibodies

ECD:

Extended criteria donor

EPO:

Erythropoietin

ESRD:

End-stage renal disease

KT:

Kidney transplantation

LAVI:

Left atrial volume index

LDL:

Low density lipoprotein

LVEF:

Left ventricular ejection fraction

LVH:

Left ventricular hypertrophy

LVMI:

Left ventricular mass index

NODAT:

New onset diabetes after transplant

PTH:

Parathyroid hormone

SCD:

Standard criteria donor

TTE:

Transthoracic echocardiography

References

  1. Ahmadmehrabi S, Tang WHW (2018) Hemodialysis-induced cardiovascular disease. Semin Dial 31(3):258–267

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ortiz A, Covic A, Fliser D, Fouque D, Goldsmith D, Kanbay M et al (2014) Epidemiology, contributors to, and clinical trials of mortality risk in chronic kidney failure. Lancet 383(9931):1831–1843

    Article  PubMed  Google Scholar 

  3. Wang X, Shapiro JI (2019) Evolving concepts in the pathogenesis of uraemic cardiomyopathy. Nat Rev Nephrol 15(3):159–175

    Article  PubMed  Google Scholar 

  4. Kaesler N, Babler A, Floege J, Kramann R (2020) Cardiac remodeling in chronic kidney disease. Toxins (Basel) 12(3):161

    Article  CAS  PubMed  Google Scholar 

  5. Mall G, Huther W, Schneider J, Lundin P, Ritz E (1990) Diffuse intermyocardiocytic fibrosis in uraemic patients. Nephrol Dial Transplant 5(1):39–44

    Article  CAS  PubMed  Google Scholar 

  6. Aoki J, Ikari Y, Nakajima H, Mori M, Sugimoto T, Hatori M et al (2005) Clinical and pathologic characteristics of dilated cardiomyopathy in hemodialysis patients. Kidney Int 67(1):333–340

    Article  PubMed  Google Scholar 

  7. Cai QZ, Lu XZ, Lu Y, Wang AY (2014) Longitudinal changes of cardiac structure and function in CKD (CASCADE study). J Am Soc Nephrol 25(7):1599–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hamidi S, Kojuri J, Attar A, Roozbeh J, Moaref A, Nikoo MH (2018) The effect of kidney transplantation on speckled tracking echocardiography findings in patients on hemodialysis. J Cardiovasc Thorac Res 10(2):90–94

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hewing B, Dehn AM, Staeck O, Knebel F, Spethmann S, Stangl K et al (2016) Improved left ventricular structure and function after successful kidney transplantation. Kidney Blood Press Res 41(5):701–709

    Article  CAS  PubMed  Google Scholar 

  10. Hawwa N, Shrestha K, Hammadah M, Yeo PSD, Fatica R, Tang WHW (2015) Reverse remodeling and prognosis following kidney transplantation in contemporary patients with cardiac dysfunction. J Am Coll Cardiol 66(16):1779–1787

    Article  PubMed  PubMed Central  Google Scholar 

  11. Vaidya OU, House JA, Coggins TR, Patil H, Vaidya A, Awad A et al (2012) Effect of renal transplantation for chronic renal disease on left ventricular mass. Am J Cardiol 110(2):254–257

    Article  PubMed  Google Scholar 

  12. Wali RK, Wang GS, Gottlieb SS, Bellumkonda L, Hansalia R, Ramos E et al (2005) Effect of kidney transplantation on left ventricular systolic dysfunction and congestive heart failure in patients with end-stage renal disease. J Am Coll Cardiol 45(7):1051–1060

    Article  PubMed  Google Scholar 

  13. Parfrey PS, Harnett JD, Foley RN, Kent GM, Murray DC, Barre PE et al (1995) Impact of renal transplantation on uremic cardiomyopathy. Transplantation 60(9):908–914

    Article  CAS  PubMed  Google Scholar 

  14. Rigatto C, Foley RN, Kent GM, Guttmann R, Parfrey PS (2000) Long-term changes in left ventricular hypertrophy after renal transplantation. Transplantation 70(4):570–575

    Article  CAS  PubMed  Google Scholar 

  15. du Cailar G, Oudot C, Fesler P, Mimran A, Bonnet B, Pernin V et al (2014) Left ventricular mass changes after renal transplantation: influence of dietary sodium and change in serum uric acid. Transplantation 98(2):202–207

    Article  PubMed  Google Scholar 

  16. Kensinger C, Hernandez A, Bian A, Fairchild M, Chen G, Lipworth L et al (2017) Longitudinal assessment of cardiac morphology and function following kidney transplantation. Clin Transplant 31(1):e12864

    Article  Google Scholar 

  17. Zapolski T, Furmaga J, Wysokinski AP, Wysocka A, Rudzki S, Jaroszynski A (2019) The atrial uremic cardiomyopathy regression in patients after kidney transplantation—the prospective echocardiographic study. BMC Nephrol 20(1):152

    Article  PubMed  PubMed Central  Google Scholar 

  18. McGregor E, Stewart G, Rodger RS, Jardine AG (2000) Early echocardiographic changes and survival following renal transplantation. Nephrol Dial Transplant 15(1):93–98

    Article  CAS  PubMed  Google Scholar 

  19. Patel RK, Mark PB, Johnston N, McGregor E, Dargie HJ, Jardine AG (2008) Renal transplantation is not associated with regression of left ventricular hypertrophy: a magnetic resonance study. Clin J Am Soc Nephrol 3(6):1807–1811

    Article  PubMed  PubMed Central  Google Scholar 

  20. Himelman RB, Landzberg JS, Simonson JS, Amend W, Bouchard A, Merz R et al (1988) Cardiac consequences of renal transplantation: changes in left ventricular morphology and function. J Am Coll Cardiol 12(4):915–923

    Article  CAS  PubMed  Google Scholar 

  21. Hernandez D, Lacalzada J, Rufino M, Torres A, Martin N, Barragan A et al (1997) Prediction of left ventricular mass changes after renal transplantation by polymorphism of the angiotensin-converting-enzyme gene. Kidney Int 51(4):1205–1211

    Article  CAS  PubMed  Google Scholar 

  22. Keven K, Calayoglu R, Sengul S, Dincer I, Kutlay S, Erturk S et al (2008) Comparative effects of renal transplantation and maintenance dialysis on arterial stiffness and left ventricular mass index. Clin Transplant 22(3):360–365

    Article  PubMed  Google Scholar 

  23. Sahagun-Sanchez G, Espinola-Zavaleta N, Lafragua-Contreras M, Chavez PY, Gomez-Nunez N, Keirns C et al (2001) The effect of kidney transplant on cardiac function: an echocardiographic perspective. Echocardiography 18(6):457–462

    Article  CAS  PubMed  Google Scholar 

  24. Pickup LC, Law JP, Radhakrishnan A, Price AM, Loutradis C, Smith TO et al (2021) Changes in left ventricular structure and function associated with renal transplantation: a systematic review and meta-analysis. ESC Heart Fail 8(3):2045–2057

    Article  PubMed  PubMed Central  Google Scholar 

  25. De Lima JJ, Abensur H, da Fonseca JA, Krieger EM, Pileggi F (1995) Comparison of echocardiographic changes associated with hemodialysis and renal transplantation. Artif Organs 19(3):245–250

    Article  PubMed  Google Scholar 

  26. Prasad GVR, Yan AT, Nash MM, Kim SJ, Wald R, Lok C et al (2018) Determinants of left ventricular characteristics assessed by cardiac magnetic resonance imaging and cardiovascular biomarkers related to kidney transplantation. Can J Kidney Health Dis 5:2054358118809974

    Article  PubMed  Google Scholar 

  27. Agence de la biomédecine: Rapport médical et scientifique du prélèvement et de la greffe en France (2021) https://rams.agence-biomedecine.fr

  28. Karras A, Boutouyrie P, Briet M, Bozec E, Haymann JP, Legendre C et al (2017) Reversal of arterial stiffness and maladaptative arterial remodeling after kidney transplantation. J Am Heart Assoc 6(9):e006078

    Article  PubMed  PubMed Central  Google Scholar 

  29. Haller MC, Kammer M, Oberbauer R (2019) Dialysis vintage and outcomes in renal transplantation. Nephrol Dial Transplant 34(4):555–560

    Article  PubMed  Google Scholar 

  30. Cheung AK, Chang TI, Cushman WC, Furth SL, Hou FF, Ix JH et al (2021) Executive summary of the KDIGO 2021 clinical practice guideline for the management of blood pressure in chronic kidney disease. Kidney Int 99(3):559–569

    Article  PubMed  Google Scholar 

  31. Kidney Disease: Improving Global Outcomes Diabetes Work G (2022) KDIGO 2022 clinical practice guideline for diabetes management in chronic kidney disease. Kidney Int 102(5S):S1–S127

    Google Scholar 

  32. Wanner C, Tonelli M, Kidney Disease: Improving Global Outcomes Lipid Guideline Development Work Group M (2014) KDIGO Clinical Practice Guideline for Lipid Management in CKD: summary of recommendation statements and clinical approach to the patient. Kidney Int 85(6):1303–1309

    Article  CAS  PubMed  Google Scholar 

  33. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 16(3):233–270

    Article  PubMed  Google Scholar 

  34. Pellicori P, Ferreira JP, Mariottoni B, Brunner-La Rocca HP, Ahmed FZ, Verdonschot J et al (2020) Effects of spironolactone on serum markers of fibrosis in people at high risk of developing heart failure: rationale, design and baseline characteristics of a proof-of-concept, randomised, precision-medicine, prevention trial. The Heart OMics in AGing (HOMAGE) trial. Eur J Heart Fail 22(9):1711–1723

    Article  CAS  PubMed  Google Scholar 

  35. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 28(1):1-39 e14

    Article  PubMed  Google Scholar 

  36. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T et al (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

    Article  PubMed  Google Scholar 

  37. Khani M, Tara A, Shekarkhar S, Esfahani MA, Bayat F (2020) Effect of kidney transplantation on right ventricular function, assessment by 2- dimensional speckle tracking echocardiography. Cardiovasc Ultrasound 18(1):16

    Article  PubMed  PubMed Central  Google Scholar 

  38. Casas-Aparicio G, Castillo-Martinez L, Orea-Tejeda A, Abasta-Jimenez M, Keirns-Davies C, Rebollar-Gonzalez V (2010) The effect of successful kidney transplantation on ventricular dysfunction and pulmonary hypertension. Transplant Proc 42(9):3524–3528

    Article  CAS  PubMed  Google Scholar 

  39. Meucci MC, Reinders MEJ, Groeneweg KE, Bezstarosti S, Ajmone Marsan N, Bax JJ et al (2021) Cardiovascular effects of autologous bone marrow-derived mesenchymal stromal cell therapy with early tacrolimus withdrawal in renal transplant recipients: an analysis of the randomized TRITON study. J Am Heart Assoc 10(24):e023300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hernandez D, Gonzalez A, Rufino M, Laynez I, de la Rosa A, Porrini E et al (2007) Time-dependent changes in cardiac growth after kidney transplantation: the impact of pre-dialysis ventricular mass. Nephrol Dial Transplant 22(9):2678–2685

    Article  PubMed  Google Scholar 

  41. Huting J (1992) Course of left ventricular hypertrophy and function in end-stage renal disease after renal transplantation. Am J Cardiol 70(18):1481–1484

    Article  CAS  PubMed  Google Scholar 

  42. Thomas L, Muraru D, Popescu BA, Sitges M, Rosca M, Pedrizzetti G et al (2020) Evaluation of left atrial size and function: relevance for clinical practice. J Am Soc Echocardiogr 33(8):934–952

    Article  PubMed  Google Scholar 

  43. Hoit BD (2014) Left atrial size and function: role in prognosis. J Am Coll Cardiol 63(6):493–505

    Article  PubMed  Google Scholar 

  44. Kizer JR, Bella JN, Palmieri V, Liu JE, Best LG, Lee ET et al (2006) Left atrial diameter as an independent predictor of first clinical cardiovascular events in middle-aged and elderly adults: the Strong Heart Study (SHS). Am Heart J 151(2):412–418

    Article  PubMed  Google Scholar 

  45. Kadappu KK, Abhayaratna K, Boyd A, French JK, Xuan W, Abhayaratna W et al (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

    Article  PubMed  Google Scholar 

  46. Tanasa A, Tapoi L, Ureche C, Sascau R, Statescu C, Covic A (2021) Left atrial strain: a novel “biomarker” for chronic kidney disease patients? Echocardiography 38(12):2077–2082

    Article  PubMed  Google Scholar 

  47. Patel RK, Pennington C, Stevens KK, Taylor A, Gillis K, Rutherford E et al (2014) Effect of left atrial and ventricular abnormalities on renal transplant recipient outcome-a single-center study. Transplant Res 3(1):20

    Article  PubMed  PubMed Central  Google Scholar 

  48. Kainz A, Goliasch G, Wiesbauer F, Binder T, Maurer G, Nesser HJ et al (2013) Left atrial diameter and survival among renal allograft recipients. Clin J Am Soc Nephrol 8(12):2100–2105

    Article  PubMed  PubMed Central  Google Scholar 

  49. Regele F, Kainz A, Kammer M, Beer A, Steringer-Mascherbauer R, Binder T et al (2018) Regression of left atrial diameter after kidney transplantation is associated with prolonged survival: an observational study. Transpl Int. https://doi.org/10.1111/tri.13152

    Article  PubMed  Google Scholar 

  50. Reinders MEJ, Groeneweg KE, Hendriks SH, Bank JR, Dreyer GJ, de Vries APJ et al (2021) Autologous bone marrow-derived mesenchymal stromal cell therapy with early tacrolimus withdrawal: The randomized prospective, single-center, open-label TRITON study. Am J Transplant 21(9):3055–3065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Meucci MC, Reinders MEJ, Groeneweg KE, Bezstarosti S, Marsan NA, Bax JJ et al (2023) Left atrial structural and functional response in kidney transplant recipients treated with mesenchymal stromal cell therapy and early tacrolimus withdrawal. J Am Soc Echocardiogr 36(2):172–179

    Article  PubMed  Google Scholar 

  52. Lee SL, Daimon M, Nakao T, Singer DE, Shinozaki T, Kawata T et al (2016) Factors influencing left atrial volume in a population with preserved ejection fraction: left ventricular diastolic dysfunction or clinical factors? J Cardiol 68(4):275–281

    Article  PubMed  Google Scholar 

  53. Dereli S, Bayramoglu A, Ozer N, Cersit S, Kaya A, Ozbilen M (2019) Evaluation of left atrial volume and function by real time three-dimensional echocardiography in anemic patients without overt heart disease before and after anemia correction. Int J Cardiovasc Imaging 35(9):1619–1626

    Article  PubMed  Google Scholar 

  54. Beysel S, Caliskan M, Kizilgul M, Apaydin M, Kan S, Ozbek M et al (2019) Parathyroidectomy improves cardiovascular risk factors in normocalcemic and hypercalcemic primary hyperparathyroidism. BMC Cardiovasc Disord 19(1):106

    Article  PubMed  PubMed Central  Google Scholar 

  55. Andersson P, Rydberg E, Willenheimer R (2004) Primary hyperparathyroidism and heart disease–a review. Eur Heart J 25(20):1776–1787

    Article  CAS  PubMed  Google Scholar 

  56. Purra S, Lone AA, Bhat MH, Misgar RA, Wani AI, Bashir MI et al (2022) Cardiac structural and functional abnormalities in primary hyperparathyroidism. J Endocrinol Invest 45(2):327–335

    Article  CAS  PubMed  Google Scholar 

  57. Kepez A, Yasar M, Sunbul M, Ileri C, Deyneli O, Mutlu B et al (2017) Evaluation of left ventricular functions in patients with primary hyperparathyroidism: is there any effect of parathyroidectomy? Wien Klin Wochenschr 129(9–10):329–336

    Article  PubMed  Google Scholar 

  58. Isakov O, Ghinea R, Beckerman P, Mor E, Riella LV, Hod T (2020) Early persistent hyperparathyroidism post-renal transplantation as a predictor of worse graft function and mortality after transplantation. Clin Transplant 34(11):e14085

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Tristan GIGANT (F-CRIN INI-CRCT) for his help in preparing the visual abstract.

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Authors and Affiliations

  1. Nephrology Department, University Hospital of Nancy, Vandoeuvre-lès-Nancy, France

    Q. d’Hervé, V. Panisset, L. Frimat & S. Girerd

  2. Université de Lorraine, Inserm, Centre d’Investigations Cliniques-1433, and Inserm U1116, University Hospital of Nancy, F-CRIN INI-CRCT, Vandoeuvre-lès-Nancy, France

    N. Girerd, E. Bozec, Z. Lamiral, O. Huttin & S. Girerd

  3. Cardiology Department, University Hospital of Nancy, Vandoeuvre-lès-Nancy, France

    O. Huttin

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  1. Q. d’Hervé
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Correspondence to S. Girerd.

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Pr GIRERD received personal fees from Novartis, Pfizer, Astra Zeneca, Boehringer, Vifor, Bayer and Lilly. All other authors declared no competing interest.

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d’Hervé, Q., Girerd, N., Bozec, E. et al. Factors associated with changes in echocardiographic parameters following kidney transplantation. Clin Res Cardiol 113, 412–424 (2024). https://doi.org/10.1007/s00392-023-02203-6

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