Skip to main content
SpringerLink
Log in

Identification of cardiovascular abnormalities by multiparametric magnetic resonance imaging in end-stage renal disease patients with preserved left ventricular ejection fraction

  • Cardiac
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

Our study aimed to evaluate myocardial strain and tissue characteristics by multiparametric cardiovascular magnetic resonance (CMR) imaging in end-stage renal disease (ESRD) patients on peritoneal dialysis with preserved left ventricular ejection fraction (LVEF).

Methods

ESRD patients on peritoneal dialysis with echocardiographic LVEF > 50% and age- and sex-matched healthy volunteers underwent multiparametric CMR at 3 T. LV function, LV myocardial native T1 and T2, and biventricular strain were measured and compared between the patients and controls. Associations of LV myocardial mass index (LVMI) with tissue characterization and strain were evaluated by multiple linear regression.

Results

A total of 65 subjects (42 healthy volunteers and 23 ESRD patients) were enrolled. ESRD group demonstrated larger LVMI, higher native T1 and T2 (1301.9 ± 30.6 ms, 44.6 ± 2.6 ms) than those of the control group (1255.8 ± 45.2 ms, 40.5 ± 1.6 ms; both p < 0.001). Decreased LV strain and increased right ventricular circumferential strain were observed in the ESRD group. In ESRD patients with normal diastolic function on echocardiography, native T1 and T2 values were higher than those of the control group (p = 0.006, p = 0.001). Increased LVMI was associated with increased native T1 (p = 0.001) and T2 value (p < 0.001) after adjusting for age and sex. Increased myocardial native T1 value was associated with reduced LV strain after adjusting age, sex, and LVMI.

Conclusions

ESRD patients on peritoneal dialysis with preserved LVEF demonstrated higher myocardial mass, higher native T1 and T2 values, decreased LV strain, and increased RVGCS compared with healthy controls. Increased myocardial T1 and T2 were found in ESRD even when no systolic or diastolic dysfunction was detected by routine echocardiography.

Key Points

• Even with preserved LVEF and no known cardiovascular diseases, ESRD patients on peritoneal dialysis demonstrated elevated myocardial T1 and T2 values and decreased left ventricular strain.

• Subclinical changes in myocardial tissue composition may exist in ESRD patients on peritoneal dialysis even when no systolic or diastolic dysfunction was detected by routine echocardiography based on ejection fraction, left atrium size, and tissue Doppler.

• Right ventricular free wall strain could be enhanced in response to subclinical LV systolic dysfunction in ESRD patients on peritoneal dialysis with preserved LVEF at an early stage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

BSA:

Body surface area

CKD:

Chronic kidney disease

CMR:

Cardiovascular magnetic resonance

EDV:

End-diastolic volume

EDVI:

End-diastolic volume index

ESRD:

End-stage renal disease

ESV:

End-systolic volume

ESVI:

End-systolic volume index

LVEF:

Left ventricular ejection fraction

LVGCS:

Left ventricular global circumferential strain

LVGLS:

Left ventricular global longitudinal strain

LVM:

Left ventricular myocardial mass

LVMI:

Left ventricular myocardial mass index

RVGCS:

Right ventricular global circumferential strain

RVGLS:

Right ventricular global longitudinal strain

SV:

Stroke volume

SVI:

Stroke volume index

References

  1. Foley RN, Parfrey PS, Sarnak MJ (1998) Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis 32:S112–S119

    Article  CAS  PubMed  Google Scholar 

  2. Gansevoort RT, Correa-Rotter R, Hemmelgarn BR et al (2013) Chronic kidney disease and cardiovascular risk: epidemiology, mechanisms, and prevention. Lancet 382:339–352

    Article  Google Scholar 

  3. Sosnov J, Lessard D, Goldberg RJ, Yarzebski J, Gore JM (2006) Differential symptoms of acute myocardial infarction in patients with kidney disease: a community-wide perspective. Am J Kidney Dis 47:378–384

    Article  PubMed  Google Scholar 

  4. Panoulas VF, Sulemane S, Konstantinou K et al (2015) Early detection of subclinical left ventricular myocardial dysfunction in patients with chronic kidney disease. Eur Heart J Cardiovasc Imaging 16:539–548

    Article  PubMed  Google Scholar 

  5. Smiseth OA, Torp H, Opdahl A, Haugaa KH, Urheim S (2015) Myocardial strain imaging: how useful is it in clinical decision making? Eur Heart J 37:1196–1207

    Article  PubMed  PubMed Central  Google Scholar 

  6. Tops LF, Delgado V, Marsan NA, Bax JJ (2017) Myocardial strain to detect subtle left ventricular systolic dysfunction. Eur J Heart Fail 19:307–313

    Article  PubMed  Google Scholar 

  7. 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 120:500–504

    Article  PubMed  Google Scholar 

  8. Claus P, Omar AMS, Pedrizzetti G, Sengupta PP, Nagel E (2015) Tissue tracking technology for assessing cardiac mechanics: principles, normal values, and clinical applications. JACC Cardiovasc Imaging 8:1444–1460

    Article  PubMed  Google Scholar 

  9. Bellenger NG, Burgess MI, Ray SG et al (2000) Comparison of left ventricular ejection fraction and volumes in heart failure by echocardiography, radionuclide ventriculography and cardiovascular magnetic resonance. Are they interchangeable? Eur Heart J 21:1387–1396

    Article  CAS  PubMed  Google Scholar 

  10. Grothues F, Smith GC, Moon JC et al (2002) Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol 90:29–34

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Schietinger BJ, Brammer GM, Wang H et al (2008) Patterns of late gadolinium enhancement in chronic hemodialysis patients. JACC Cardiovasc Imaging 1:450–456

    Article  PubMed  PubMed Central  Google Scholar 

  13. Edwards NC, Moody WE, Yuan M et al (2015) Diffuse interstitial fibrosis and myocardial dysfunction in early chronic kidney disease. Am J Cardiol 115:1311–1317

    Article  PubMed  Google Scholar 

  14. Taylor AJ, Salerno M, Dharmakumar R, Jerosch-Herold M (2016) T1 mapping: basic techniques and clinical applications. JACC Cardiovasc Imaging 9:67–81

    Article  PubMed  Google Scholar 

  15. Rutherford E, Talle MA, Mangion K et al (2016) Defining myocardial tissue abnormalities in end-stage renal failure with cardiac magnetic resonance imaging using native T1 mapping. Kidney Int 90:845–852

    Article  PubMed  PubMed Central  Google Scholar 

  16. Graham-Brown MP, March DS, Churchward DR et al (2016) Novel cardiac nuclear magnetic resonance method for noninvasive assessment of myocardial fibrosis in hemodialysis patients. Kidney Int 90:835–844

    Article  PubMed  Google Scholar 

  17. McAlindon EJ, Pufulete M, Harris JM et al (2014) Measurement of myocardium at risk with cardiovascular MR: comparison of techniques for edema imaging. Radiology 275:61–70

    Article  PubMed  Google Scholar 

  18. Payne AR, Casey M, McClure J et al (2011) Bright-blood T2-weighted MRI has higher diagnostic accuracy than dark-blood short tau inversion recovery MRI for detection of acute myocardial infarction and for assessment of the ischemic area at risk and myocardial salvage. Circ Cardiovasc Imaging 4:210–219

    Article  PubMed  Google Scholar 

  19. Segall L, Covic A (2007) Cardiovascular disease in haemodialysis and peritoneal dialysis: arguments pro haemodialysis. Nephrol Dial Transplant 22:59–63

    Article  PubMed  Google Scholar 

  20. Van Biesen W, Verbeke F, Vanholder R (2007) Cardiovascular disease in haemodialysis and peritoneal dialysis: arguments pro peritoneal dialysis. Nephrol Dial Transplant 22:53–58

    Article  PubMed  Google Scholar 

  21. Burton JO, Jefferies HJ, Selby NM, McIntyre CW (2009) Hemodialysis-induced cardiac injury: determinants and associated outcomes. Clin J Am Soc Nephrol 4:914–920

    Article  PubMed  PubMed Central  Google Scholar 

  22. Nagueh SF, Smiseth OA, Appleton CP 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. Eur J Echocardiogr 17:1321–1360

    Google Scholar 

  23. Tamulenaite E, Zvirblyte R, Ereminiene R, Ziginskiene E, Ereminiene E (2018) Changes of left and right ventricle mechanics and function in patients with end-stage renal disease undergoing haemodialysis. Medicina (Kaunas) 54:87

    Article  Google Scholar 

  24. Mangion K, McDowell K, Mark PB, Rutherford E (2018) Characterizing cardiac involvement in chronic kidney disease using CMR-a systematic review. Curr Cardiovasc Imaging Rep 11:2

    Article  PubMed  PubMed Central  Google Scholar 

  25. Aoki J, Ikari Y, Nakajima H et al (2005) Clinical and pathologic characteristics of dilated cardiomyopathy in hemodialysis patients. Kidney Int 67:333–340

    Article  PubMed  Google Scholar 

  26. Messroghli DR, Niendorf T, Schulz-Menger J, Dietz R, Friedrich MG (2003) T1 mapping in patients with acute myocardial infarction. J Cardiovasc Magn Reson 5:353–359

    Article  PubMed  Google Scholar 

  27. Ugander M, Bagi PS, Oki AJ et al (2012) Myocardial edema as detected by pre-contrast T1 and T2 CMR delineates area at risk associated with acute myocardial infarction. JACC Cardiovasc Imaging 5:596–603

    Article  PubMed  PubMed Central  Google Scholar 

  28. Karamitsos TD, Piechnik SK, Banypersad SM et al (2013) Noncontrast T1 mapping for the diagnosis of cardiac amyloidosis. JACC Cardiovasc Imaging 6:488–497

    Article  PubMed  Google Scholar 

  29. Sado DM, Maestrini V, Piechnik SK et al (2015) Noncontrast myocardial T1 mapping using cardiovascular magnetic resonance for iron overload. J Magn Reson Imaging 41:1505–1511

    Article  PubMed  Google Scholar 

  30. Hinojar R, Puntmann VO (2015) Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis a proposed diagnostic algorithm using CMR. JACC Cardiovasc Imaging 8:38–46

    Article  Google Scholar 

  31. Ronco C, Haapio M, House AA, Anavekar N, Bellomo R (2008) Cardiorenal syndrome. J Am Coll Cardiol 52:1527–1539

    Article  PubMed  Google Scholar 

  32. Haberkorn SM, Spieker M, Jacoby C, Flögel U, Kelm M, Bönner F (2018) State of the art in cardiovascular T2 mapping: on the way to a cardiac biomarker? Curr Cardiovasc Imaging Rep 11:15

    Article  Google Scholar 

  33. Wang L, Yuan J, Zhang SJ et al (2016) Myocardial T1 rho mapping of patients with end-stage renal disease and its comparison with T1 mapping and T2 mapping: a feasibility and reproducibility study. J Magn Reson Imaging 44:723–731

    Article  PubMed  Google Scholar 

  34. Liu YW, Su CT, Huang YY et al (2011) Left ventricular systolic strain in chronic kidney disease and hemodialysis patients. Am J Nephrol 33:84–90

    Article  CAS  PubMed  Google Scholar 

  35. Wang H, Liu J, Yao XD et al (2012) Multidirectional myocardial systolic function in hemodialysis patients with preserved left ventricular ejection fraction and different left ventricular geometry. Nephrol Dial Transplant 27:4422–4429

    Article  PubMed  Google Scholar 

  36. Pirat B, Bozbas H, Simsek V et al (2015) Assessment of myocardial mechanics in patients with end-stage renal disease and renal transplant recipients using speckle tracking echocardiography. Exp Clin Transplant 13:235–241

    PubMed  Google Scholar 

  37. Yan P, Li H, Hao C et al (2011) 2D-speckle tracking echocardiography contributes to early identification of impaired left ventricular myocardial function in patients with chronic kidney disease. Nephron Clin Pract 118:c232–c240

    Article  PubMed  Google Scholar 

  38. Odudu A, Eldehni MT, McCann GP, Horsfield MA, Breidthardt T, McIntyre CW (2016) Characterisation of cardiomyopathy by cardiac and aortic magnetic resonance in patients new to hemodialysis. Eur Radiol 26:2749–2761

    Article  PubMed  Google Scholar 

  39. Peng Y, Popovic ZB, Sopko N et al (2009) Speckle tracking echocardiography in the assessment of mouse models of cardiac dysfunction. Am J Physiol Heart Circ Physiol 297:H811–H820

    Article  CAS  PubMed  Google Scholar 

  40. Kramann R, Erpenbeck J, Schneider RK et al (2014) Speckle tracking echocardiography detects uremic cardiomyopathy early and predicts cardiovascular mortality in ESRD. J Am Soc Nephrol 25:2351–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Amann K, Neimeier KA, Schwarz U et al (1997) Rats with moderate renal failure show capillary deficit in heart but not skeletal muscle. Am J Kidney Dis 30:382–388

    Article  CAS  PubMed  Google Scholar 

  42. Parnham S, Gleadle JM, Bangalore S et al (2015) Impaired myocardial oxygenation response to stress in patients with chronic kidney disease. J Am Heart Assoc 4:e002249

    Article  PubMed  PubMed Central  Google Scholar 

  43. Graham-Brown MP, Rutherford E, Levelt E et al (2017) Native T1 mapping: inter-study, inter-observer and inter-center reproducibility in hemodialysis patients. J Cardiovasc Magn Reson 19:21

    Article  PubMed  PubMed Central  Google Scholar 

  44. London GM (2003) Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin Dial 16:85–94

    Article  PubMed  Google Scholar 

  45. Unger ED, Dubin RF, Deo R et al (2016) Association of chronic kidney disease with abnormal cardiac mechanics and adverse outcomes in patients with heart failure and preserved ejection fraction. Eur J Heart Fail 18:103–112

    Article  PubMed  Google Scholar 

  46. Bove AA, Santamore WP (1981) Ventricular interdependence. Prog Cardiovasc Dis 23:365–388

    Article  CAS  PubMed  Google Scholar 

  47. Buckberg GD, Group R (2006) The ventricular septum: the lion of right ventricular function, and its impact on right ventricular restoration. Eur J Cardiothorac Surg 29(Suppl 1):S272–S278

    Article  PubMed  Google Scholar 

  48. Becker M, Humpel C, Ocklenburg C et al (2010) The right ventricular response to high afterload: comparison between healthy persons and patients with transposition of the great arteries: a 2D strain study. Echocardiography 27:1256–1262

    Article  PubMed  Google Scholar 

  49. Pettersen E, Helle-Valle T, Edvardsen T et al (2007) Contraction pattern of the systemic right ventricle shift from longitudinal to circumferential shortening and absent global ventricular torsion. J Am Coll Cardiol 49:2450–2456

    Article  PubMed  Google Scholar 

  50. Paneni F, Gregori M, Ciavarella GM et al (2010) Right ventricular dysfunction in patients with end-stage renal disease. Am J Nephrol 32:432–438

    Article  PubMed  Google Scholar 

  51. Dorairajan S, Chockalingam A, Misra M (2010) Myocardial stunning in hemodialysis: what is the overall message? Hemodial Int 14:447–450

    Article  PubMed  Google Scholar 

Download references

Funding

This study was funded by the Guangdong Science and Technology Department (2013B021800136). The work of the first author (LL) was funded in part by China Scholarship Council (CSC201807720065).

Author information

Authors and Affiliations

  1. Department of Radiology, Leiden University Medical Center, Albinusdreef 2, 2333 ZA, Leiden, The Netherlands

    Ling Lin, Ilona A. Dekkers, Qian Tao & Hildo J. Lamb

  2. Department of Radiology, The Eighth Affiliated Hospital of Sun Yat-sen University, Shennan Middle Road 3025, Shenzhen, China

    Qiuxia Xie & Xuhui Zhou

  3. Department of Ultrasonography, Guangzhou Women and Children’s Medical Center, Jinsui Road 9, Guangzhou, China

    Mei Zheng

Authors
  1. Ling Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiuxia Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mei Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xuhui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ilona A. Dekkers
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qian Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hildo J. Lamb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xuhui Zhou.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Xu-Hui Zhou.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects in this study.

Ethical approval

This study was approved by the institutional review board of the First Affiliated Hospital of Sun Yat-sen University (reference number: [2018]068).

Methodology

• prospective

• observational

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, L., Xie, Q., Zheng, M. et al. Identification of cardiovascular abnormalities by multiparametric magnetic resonance imaging in end-stage renal disease patients with preserved left ventricular ejection fraction. Eur Radiol 31, 7098–7109 (2021). https://doi.org/10.1007/s00330-021-07752-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-021-07752-w

Keywords

Search

Navigation