Skip to main content

Advertisement

SpringerLink
Log in

Multiparametric cardiovascular magnetic resonance characteristics and dynamic changes in asymptomatic heart-transplanted patients

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

A Correction to this article was published on 08 May 2023

This article has been updated

Abstract

Objectives

To describe the dynamic changes in cardiac deformation and tissue characteristics using cardiac magnetic resonance (CMR) in asymptomatic patients during 12 months after heart transplantation (HT).

Methods

From April 2020 to January 2021, 21 consecutive HT patients without clinical symptoms were included in this prospective study. Multiparametric CMR was performed at 3, 6, and 12 months after HT. Twenty-five healthy volunteers served as controls.

Results

During follow-up, a decline in left ventricular (LV) global radial strain (GRS) (p = 0.020) and right ventricular (RV) global longitudinal strain (GLS) (p < 0.001) and an increase in post-contrast T1 (p = 0.024) and T2 (p < 0.001) in asymptomatic HT patients occurred at 3 months, which normalized at 6 months postoperatively, compared with those in healthy controls. A decline in LVGLS (p < 0.001) and LV global circumferential strain (GCS) (p < 0.001) and an increase in native T1 (p < 0.001), T2 (p < 0.001), and extracellular volume (ECV) (p < 0.001) occurred at 3 months. Although most parameters improved gradually, LVGLS, native T1, and ECV remained abnormal compared with those in healthy controls at 12 months; only T2 and LVGCS were normalized at 6 months and 12 months, respectively. ECV was significantly correlated with LVGLS, LVGCS, and LVGRS.

Conclusion

Cardiac deformation and tissue characteristics were abnormal early after HT, although the patients were clinically asymptomatic. The dynamic changes in CMR characteristics demonstrate a gradual recovery of myocardial injury associated with transplantation during the first 12 months after HT.

Key Points

• Multiparametric CMR can detect the dynamic changes of transplantation-associated myocardial injury.

• Post-contrast T1, T2, LVGRS, and RVGLS values are normalized at 6 months after HT.

• Native T1, ECV, and LVGLS values remain abnormal compared with those in healthy controls at 12 months after HT.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

Abbreviations

AR:

Allograft rejection

CAV:

Cardiac allograft vasculopathy

CMR:

Cardiac magnetic resonance

ECV:

Extracellular volume

hsTnT:

High-sensitivity troponin T

HT:

Heart transplantation

LGE:

Late gadolinium enhancement

LV:

Left ventricular

LVEF:

Left ventricular ejection fraction

LVGCS:

Left ventricular global circumferential strain

LVGLS:

Left ventricular global longitudinal strain

LVGRS:

Left ventricular global radial strain

LVmassi:

Left ventricular mass index

NT-proBNP:

N-terminal pro-brain natriuretic peptide

RVGLS:

Right ventricular global longitudinal strain

References

  1. Stehlik J, Kobashigawa J, Hunt SA, Reichenspurner H, Kirklin JK (2018) Honoring 50 years of clinical heart transplantation in circulation: in-depth state-of-the-art review. Circulation 137:71–87

    Article  PubMed  Google Scholar 

  2. Potena L, Zuckermann A, Barberini F, Aliabadi-Zuckermann A (2018) Complications of cardiac transplantation. Curr Cardiol Rep 20:73

    Article  PubMed  Google Scholar 

  3. Kobashigawa J, Zuckermann A, Macdonald P et al (2014) Report from a consensus conference on primary graft dysfunction after cardiac transplantation. J Heart Lung Transplant 33:327–340

    Article  PubMed  Google Scholar 

  4. Romano S, Judd RM, Kim RJ et al (2020) Feature-tracking global longitudinal strain predicts mortality in patients with preserved ejection fraction: a multicenter study. JACC Cardiovasc Imaging 13:940–947

    Article  PubMed  Google Scholar 

  5. Kim MY, Park EA, Lee W, Lee SP (2020) Cardiac magnetic resonance feature tracking in aortic stenosis: exploration of strain parameters and prognostic value in asymptomatic patients with preserved ejection fraction. Korean J Radiol 21:268–279

    Article  PubMed  PubMed Central  Google Scholar 

  6. Yu S, Zhou J, Yang K et al (2021) Correlation of myocardial strain and late gadolinium enhancement by cardiac magnetic resonance after a first anterior st-segment elevation myocardial infarction. Front Cardiovasc Med 8:705487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Coelho-Filho OR, Shah R, Lavagnoli CFR et al (2018) Myocardial tissue remodeling after orthotopic heart transplantation: a pilot cardiac magnetic resonance study. Int J Cardiovasc Imaging 34:15–24

    Article  PubMed  Google Scholar 

  8. Miller CA, Naish JH, Shaw SM et al (2014) Multiparametric cardiovascular magnetic resonance surveillance of acute cardiac allograft rejection and characterisation of transplantation-associated myocardial injury: a pilot study. J Cardiovasc Magn Reson 16:52

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chaikriangkrai K, Abbasi MA, Sarnari R et al (2020) Prognostic value of myocardial extracellular volume fraction and T2-mapping in heart transplant patients. JACC Cardiovasc Imaging 13:1521–1530

    Article  PubMed  PubMed Central  Google Scholar 

  10. Husain N, Watanabe K, Berhane H et al (2021) Multi-parametric cardiovascular magnetic resonance with regadenoson stress perfusion is safe following pediatric heart transplantation and identifies history of rejection and cardiac allograft vasculopathy. J Cardiovasc Magn Reson 23:135

    Article  PubMed  PubMed Central  Google Scholar 

  11. Stewart S, Winters GL, Fishbein MC et al (2005) Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J Heart Lung Transplant 24:1710–1720

    Article  PubMed  Google Scholar 

  12. Butler CR, Savu A, Bakal JA et al (2015) Correlation of cardiovascular magnetic resonance imaging findings and endomyocardial biopsy results in patients undergoing screening for heart transplant rejection. J Heart Lung Transplant 34:643–650

    Article  PubMed  Google Scholar 

  13. Knecht KR, Alexander ML, Swearingen CJ, Frazier EA (2012) NTproBNP as a marker of rejection in pediatric heart transplant recipients. Pediatr Transplant 16:335–339

    Article  CAS  PubMed  Google Scholar 

  14. Beliveau P, Cheriet F, Anderson S et al (2015) Quantitative assessment of myocardial fibrosis in an age-related rat model by ex vivo late gadolinium enhancement magnetic resonance imaging with histopathological correlation. Comput Biol Med 65:103–113

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhou NW, Shu XH, Liu YL et al (2016) A novel method for sensitive determination of subclinical left-ventricular systolic dysfunction in subjects with obstructive sleep apnea. Respir Care 61:366–375

    Article  PubMed  Google Scholar 

  16. Li X, Kou H, Dong Y et al (2020) The value of 2D speckle-tracking strain echocardiography in evaluating the relationship between carotid elasticity and left ventricular systolic function in patients with diabetic nephropathy. Insights Imaging 11:95

    Article  PubMed  PubMed Central  Google Scholar 

  17. Cochera F, Dinca D, Bordejevic DA et al (2018) Nebivolol effect on doxorubicin-induced cardiotoxicity in breast cancer. Cancer Manag Res 10:2071–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cutruzzola A, Irace C, Frazzetto M et al (2020) Functional and morphological cardiovascular alterations associated with neurofibromatosis 1. Sci Rep 10:12070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Chinali M, Esposito C, Grutter G et al (2017) Cardiac dysfunction in children and young adults with heart transplantation: a comprehensive echocardiography study. J Heart Lung Transplant 36:559–566

    Article  PubMed  Google Scholar 

  20. Latus H, Hachmann P, Voges I et al (2019) Reduced biventricular volumes and myocardial dysfunction long-term after pediatric heart transplantation assessed by CMR. Transplantation 103:2682–2691

    Article  PubMed  Google Scholar 

  21. Hu K, Liu D, Herrmann S et al (2013) Clinical implication of mitral annular plane systolic excursion for patients with cardiovascular disease. Eur Heart J Cardiovasc Imaging 14:205–212

    Article  PubMed  Google Scholar 

  22. Chilian WM (1991) Microvascular pressures and resistances in the left ventricular subepicardium and subendocardium. Circ Res 69:561–570

    Article  CAS  PubMed  Google Scholar 

  23. Cikes M, Solomon SD (2016) Beyond ejection fraction: an integrative approach for assessment of cardiac structure and function in heart failure. Eur Heart J 37:1642–1650

    Article  PubMed  Google Scholar 

  24. Kraigher-Krainer E, Shah AM, Gupta DK et al (2014) Impaired systolic function by strain imaging in heart failure with preserved ejection fraction. J Am Coll Cardiol 63:447–456

    Article  PubMed  Google Scholar 

  25. Cikes M, Sutherland GR, Anderson LJ, Bijnens BH (2010) The role of echocardiographic deformation imaging in hypertrophic myopathies. Nat Rev Cardiol 7:384–396

    Article  CAS  PubMed  Google Scholar 

  26. Saleh HK, Villarraga HR, Kane GC et al (2011) Normal left ventricular mechanical function and synchrony values by speckle-tracking echocardiography in the transplanted heart with normal ejection fraction. J Heart Lung Transplant 30:652–658

    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. Anthony C, Imran M, Pouliopoulos J et al (2022) Cardiovascular magnetic resonance for rejection surveillance after cardiac transplantation. Circulation 145:1811–1824

    Article  CAS  PubMed  Google Scholar 

  29. Kfoury AG, Hammond ME, Snow GL et al (2009) Cardiovascular mortality among heart transplant recipients with asymptomatic antibody-mediated or stable mixed cellular and antibody-mediated rejection. J Heart Lung Transplant 28:781–784

    Article  PubMed  Google Scholar 

  30. Quarles E, Basisty N, Chiao YA et al (2020) Rapamycin persistently improves cardiac function in aged, male and female mice, even following cessation of treatment. Aging Cell 19:e13086

    Article  CAS  PubMed  Google Scholar 

  31. Johnsson C, Gerdin B, Tufveson G (2004) Effects of commonly used immunosuppressants on graft-derived fibroblasts. Clin Exp Immunol 136:405–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 81974262 and 81970288); the Natural Science Foundation of Guangdong Province (Grant No. 2020A1515010650); the Guangdong Cardiovascular Institute Project (Grant No.2020XXG009); and the Guangdong Provincial Key Laboratory of Artificial Intelligence in Medical Image Analysis and Application (Grant No. 2022B1212010011).

Author information

Author notes

  1. Yuelong Yang and Tingyu Li contributed equally to this study as co-first authors.

  2. Hui Liu and Min Wu contributed equally to this study as co-corresponding authors.

Authors and Affiliations

  1. The Second School of Clinical Medicine, Southern Medical University, Guangzhou, 510515, China

    Yuelong Yang

  2. Department of Radiology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, 510080, China

    Yuelong Yang, Zekun Tan, Rui Chen, Xiaodan Li, Wei Luo, Huanwen Xu, Weitao Ye & Hui Liu

  3. Department of Medical Imaging Center, Nanfang Hospital, Southern Medical University, Guangzhou, 510515, China

    Tingyu Li

  4. Department of Radiology, The Fifth Affiliated Hospital of Sun Yat-sen University, Zhuhai, 519000, China

    Xiaobing Zhou

  5. Department of Pathology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, 510080, China

    Zebin Xiao

  6. WeiLun PET Center, Department of Nuclear Medicine, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, 510080, China

    Entao Liu

  7. Philips Healthcare China, Shenzhen, 518000, China

    Zhigang Wu

  8. Guangdong Cardiovascular Institute, Guangdong Provincial Key Laboratory of South China Structural Heart Disease, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, 510080, China

    Min Wu

  9. Guangdong Provincial Key Laboratory of Artificial Intelligence in Medical Image Analysis and Application, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, 510080, China

    Hui Liu

Authors
  1. Yuelong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tingyu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaobing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zekun Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zebin Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaodan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wei Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huanwen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Weitao Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Entao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zhigang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Min Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Min Wu or Hui Liu.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Hui Liu.

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

One of the authors has significant statistical expertise. No complex statistical methods were necessary for this paper.

Informed consent

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

Ethical approval

Institutional review board approval was obtained.

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.

The original online version of this article was revised: only the affiliations 2 & 9 should be assigned to the author Hui Liu.

Supplementary Information

ESM 1

(DOCX 541 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Li, T., Zhou, X. et al. Multiparametric cardiovascular magnetic resonance characteristics and dynamic changes in asymptomatic heart-transplanted patients. Eur Radiol 33, 4600–4610 (2023). https://doi.org/10.1007/s00330-022-09358-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-022-09358-2

Keywords

Search

Navigation