Skip to main content
Log in

Diastolic strain imaging: a new non-invasive tool to detect subclinical myocardial dysfunction in early cardiac allograft rejection

  • Original Article
  • Published:
The International Journal of Cardiovascular Imaging Aims and scope Submit manuscript

Abstract

Acute cellular rejection (ACR) remains a significant contributor to increased morbidity and mortality in heart transplant recipients. Early detection of ACR by non-invasive imaging is of potential clinical benefit. This study sought to investigate the use of non-invasive early global diastolic strain rate (GDSRe) and global longitudinal strain (GLS) in the detection of biopsy proven ACR. We retrospectively analysed 31 heart transplant patients (Mean age 52 ± 14 years) with biopsy proven ACR who underwent serial transthoracic echocardiographic examination and 2D strain analysis. Traditional echocardiographic systolic and diastolic parameters and novel systolic and diastolic strain imaging were measured during (1) early rejection free period (0R); (2) pre-rejection period (pre-1R); and (3) grade 1R acute cellular rejection (1R-ACR). GDSRe was significantly reduced (p = 0.0001) during the pre-rejection period (pre-1R) (0.74/s) when compared with 0R (0.97/s). GLS was only significantly reduced during 1R-ACR (17.7%), p = 0.001 but could not detect pre-1R (19.9%). Global diastolic strain rate at isovolumic relaxation showed no significant differences between any of the rejection periods. Traditional systolic and diastolic indices showed no significant differences. In conclusion, early global diastolic strain rate is the most sensitive parameter to detect subclinical myocardial dysfunction during early periods of pre-1R prior to biopsy confirmed 1R-ACR. GDSRe is a potential new tool for non-invasive screening of early post-transplant cardiac allograft rejection.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Stewart S, Winters GL, Fishbein MC, Tazelaar HD, Kobashigawa J, Abrams J, Andersen CB, Angelini A, Berry GJ, Burke MM, Demetris AJ, Hammond E, Itescu S, Marboe CC, McManus B, Reed EF, Reinsmoen NL, Rodriguez ER, Rose AG, Rose M, Suciu-Focia N, Zeevi A, Billingham ME (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. https://doi.org/10.1016/j.healun.2005.03.019

    Article  PubMed  Google Scholar 

  2. Patel JK, Kittleson M, Kobashigawa JA (2011) Cardiac allograft rejection. Surgeon 9:160–167. https://doi.org/10.1016/j.surge.2010.11.023

    Article  PubMed  Google Scholar 

  3. Miller CA, Fildes JE, Ray SG, Doran H, Yonan N, Williams SG, Schmitt M (2013) Non-invasive approaches for the diagnosis of acute cardiac allograft rejection. Heart 99:445–453. https://doi.org/10.1136/heartjnl-2012-302759

    Article  CAS  PubMed  Google Scholar 

  4. Bader FM, Islam N, Mehta NA, Worthen N, Ishihara S, Stehlik J, Gilbert EM, Litwin SE (2011) Noninvasive diagnosis of cardiac allograft rejection using echocardiography indices of systolic and diastolic function. Transplant Proc 43:3877–3881. https://doi.org/10.1016/j.transproceed.2011.09.039

    Article  CAS  PubMed  Google Scholar 

  5. Palka P, Lange A, Galbraith A, Duhig E, Clarke BE, Parsonage W, Donnelly JE, Stafford WJ, Burstow DJ (2005) The role of left and right ventricular early diastolic Doppler tissue echocardiographic indices in the evaluation of acute rejection in orthotopic heart transplant. J Am Soc Echocardiogr 18:107–115. https://doi.org/10.1016/j.echo.2004.09.021

    Article  PubMed  Google Scholar 

  6. Valantine HA, TK Yeoh, R Gibbons, P McCarthy, EB Stinson, ME Billingham, and RL Popp (1991) Sensitivity and specificity of diastolic indexes for rejection surveillance: temporal correlation with endomyocardial biopsy. J Heart Lung Transplant 10:757–765. https://www.jhltonline.org/

  7. Dandel M, Hummel M, Meyer R, Muller J, Kapell S, Ewert R, Hetzer R (2002) Left ventricular dysfunction during cardiac allograft rejection: early diagnosis, relationship to the histological severity grade, and therapeutic implications. Transplant Proc 34:2169–2173. https://www.journals.elsevier.com/transplantation-proceedings

    Article  CAS  Google Scholar 

  8. Kato TS, Oda N, Hashimura K, Hashimoto S, Nakatani T, Ueda HI, Shishido T, Komamura K (2010) Strain rate imaging would predict sub-clinical acute rejection in heart transplant recipients. Eur J Cardiothorac Surg 37:1104–1110. https://doi.org/10.1016/j.ejcts.2009.11.037

    Article  PubMed  Google Scholar 

  9. Nagueh SF, Bachinski LL, Meyer D, Hill R, Zoghbi WA, Tam JW, Quinones MA, Roberts R, Marian AJ (2001) Tissue Doppler imaging consistently detects myocardial abnormalities in patients with hypertrophic cardiomyopathy and provides a novel means for an early diagnosis before and independently of hypertrophy. Circulation 104:128–130. https://www.ahajournals.org/journal/circ

    Article  CAS  Google Scholar 

  10. Dandel M, Hetzer R (2009) Echocardiographic strain and strain rate imaging–clinical applications. Int J Cardiol 132:11–24. https://doi.org/10.1016/j.ijcard.2008.06.091

    Article  PubMed  Google Scholar 

  11. Nakai H, Takeuchi M, Nishikage T, Lang RM, Otsuji Y (2009) Subclinical left ventricular dysfunction in asymptomatic diabetic patients assessed by two-dimensional speckle tracking echocardiography: correlation with diabetic duration. Eur J Echocardiogr 10:926–932. https://doi.org/10.1093/ejechocard/jep097

    Article  PubMed  Google Scholar 

  12. Kraigher-Krainer E, Shah AM, Gupta DK, Santos A, Claggett B, Pieske B, Zile MR, Voors AA, Lefkowitz MP, Packer M, McMurray JJ, Solomon SD, Investigators P (2014) Impaired systolic function by strain imaging in heart failure with preserved ejection fraction. J Am Coll Cardiol 63:447–456. https://doi.org/10.1016/j.jacc.2013.09.052

    Article  PubMed  Google Scholar 

  13. Pieper GM, Shah A, Harmann L, Cooley BC, Ionova IA, Migrino RQ (2010) Speckle-tracking 2-dimensional strain echocardiography: a new noninvasive imaging tool to evaluate acute rejection in cardiac transplantation. J Heart Lung Transplant 29:1039–1046. https://doi.org/10.1016/j.healun.2010.04.009

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ruiz Ortiz M, Pena ML, Mesa D, Delgado M, Romo E, Santisteban M, Puentes M, Lopez Granados A, Castillo JC, Arizon JM, de Lezo JS (2015) Impact of asymptomatic acute cellular rejection on left ventricle myocardial function evaluated by means of two-dimensional speckle tracking echocardiography in heart transplant recipients. Echocardiography 32:229–237. https://doi.org/10.1111/echo.12623

    Article  PubMed  Google Scholar 

  15. Clemmensen TS, Logstrup BB, Eiskjaer H, Poulsen SH (2015) Changes in longitudinal myocardial deformation during acute cardiac rejection: the clinical role of two-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr 28:330–339. https://doi.org/10.1016/j.echo.2014.10.015

    Article  PubMed  Google Scholar 

  16. Mingo-Santos S, Monivas-Palomero V, Garcia-Lunar I, Mitroi CD, Goirigolzarri-Artaza J, Rivero B, Oteo JF, Castedo E, Gonzalez-Mirelis J, Cavero MA, Gomez-Bueno M, Segovia J, Alonso-Pulpon L (2015) Usefulness of two-dimensional strain parameters to diagnose acute rejection after heart transplantation. J Am Soc Echocardiogr 28:1149–1156. https://doi.org/10.1016/j.echo.2015.06.005

    Article  PubMed  Google Scholar 

  17. Kim H, Cho HO, Cho YK, Nam CW, Han SW, Hur SH, Kim KS, Kim YN, Kim KB (2008) Relationship between early diastolic strain rate imaging and left ventricular geometric patterns in hypertensive patients. Heart Vessels 23:271–278. https://doi.org/10.1007/s00380-008-1042-0

    Article  PubMed  Google Scholar 

  18. Li VW, Cheuk DK, Cheng FW, Yang JY, Yau JP, Ho KK, Li CK, Li RC, Yuen HL, Ling AS, Chan GC, Cheung YF (2017) Myocardial stiffness as assessed by diastolic wall strain in adult survivors of childhood leukaemias with preserved left ventricular ejection fraction. Eur Heart J Cardiovasc Imaging 18:451–458. https://doi.org/10.1093/ehjci/jew098

    Article  PubMed  Google Scholar 

  19. Liang HY, Cauduro S, Pellikka P, Wang J, Urheim S, Yang EH, Rihal C, Belohlavek M, Khandheria B, Miller FA, Abraham TP (2006) Usefulness of two-dimensional speckle strain for evaluation of left ventricular diastolic deformation in patients with coronary artery disease. Am J Cardiol 98:1581–1586. https://doi.org/10.1016/j.amjcard.2006.07.038

    Article  PubMed  Google Scholar 

  20. Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS, S American Heart Association Writing Group on Myocardial, and I Registration for Cardiac (2002) Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Int J Cardiovasc Imaging 18:539–542. https://www.springer.com/medicine/cardiology/journal/10554

  21. Badano LP, Miglioranza MH, Edvardsen T, Colafranceschi AS, Muraru D, Bacal F, Nieman K, Zoppellaro G, Marcondes Braga FG, Binder T, Habib G, Lancellotti P, Document Reviewers (2015) European Association of Cardiovascular Imaging/Cardiovascular Imaging Department of the Brazilian Society of Cardiology recommendations for the use of cardiac imaging to assess and follow patients after heart transplantation. Eur Heart J Cardiovasc Imaging 16:919–948. https://doi.org/10.1093/ehjci/jev139

    Article  PubMed  Google Scholar 

  22. Stehlik J, Edwards LB, Kucheryavaya AY, Aurora P, Christie JD, Kirk R, Dobbels F, Rahmel AO, Hertz MI (2010) The Registry of the International Society for Heart and Lung Transplantation: twenty-seventh official adult heart transplant report–2010. J Heart Lung Transplant 29:1089–1103. https://doi.org/10.1016/j.healun.2010.08.007

    Article  PubMed  Google Scholar 

  23. Forster T, McGhie J, Rijsterborgh H, van de Borden S, Laird-Meeter K, Balk A, Essed C, Roelandt J (1988) Can we assess the changes of ventricular filling resulting from acute allograft rejection with Doppler echocardiography? J Heart Transplant 7:430–434. https://www.jhltonline.org/

  24. Desruennes M, Corcos T, Cabrol A, Gandjbakhch I, Pavie A, Leger P, Eugene M, Bors V, Cabrol C (1988) Doppler echocardiography for the diagnosis of acute cardiac allograft rejection. J Am Coll Cardiol 12:63–70. https://www.onlinejacc.org/

  25. Valantine HA, Fowler MB, Hunt SA, Naasz C, Hatle LK, Billingham ME, Stinson EB, Popp RL (1987) Changes in Doppler echocardiographic indexes of left ventricular function as potential markers of acute cardiac rejection. Circulation 76:V86–V92

    CAS  PubMed  Google Scholar 

  26. Mouly-Bandini A, Vion-Dury J, Viout P, Mesana T, Cozzone PJ, Monties JR (1996) Value of Doppler echocardiography in the detection of low-grade rejections after cardiac transplantation. Transpl Int 9:131–136. https://www.ahajournals.org/journal/circ

    Article  CAS  Google Scholar 

  27. Puleo JA, Aranda JM, Weston MW, Cintron G, French M, Clark L, Fontanet HL (1998) Noninvasive detection of allograft rejection in heart transplant recipients by use of Doppler tissue imaging. J Heart Lung Transplant 17:176–184. https://www.jhltonline.org/

  28. Mena C, Wencker D, Krumholz HM, McNamara RL (2006) Detection of heart transplant rejection in adults by echocardiographic diastolic indices: a systematic review of the literature. J Am Soc Echocardiogr 19:1295–1300. https://doi.org/10.1016/j.echo.2006.04.029

    Article  PubMed  Google Scholar 

  29. Tseng AS, Gorsi US, Barros-Gomes S, Miller FA, Pellikka PA, Clavell AL, Villarraga HR (2018) Use of speckle-tracking echocardiography-derived strain and systolic strain rate measurements to predict rejection in transplant hearts with preserved ejection fraction. BMC Cardiovasc Disord 18:241. https://doi.org/10.1186/s12872-018-0980-4

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ersboll M, Andersen MJ, Valeur N, Mogensen UM, Fakhri Y, Thune JJ, Moller JE, Hassager C, Sogaard P, Kober L (2014) Early diastolic strain rate in relation to systolic and diastolic function and prognosis in acute myocardial infarction: a two-dimensional speckle-tracking study. Eur Heart J 35:648–656. https://doi.org/10.1093/eurheartj/eht179

    Article  PubMed  Google Scholar 

  31. Kasner M, Gaub R, Sinning D, Westermann D, Steendijk P, Hoffmann W, Schultheiss HP, Tschope C (2010) Global strain rate imaging for the estimation of diastolic function in HFNEF compared with pressure-volume loop analysis. Eur J Echocardiogr 11:743–751. https://doi.org/10.1093/ejechocard/jeq060

    Article  PubMed  Google Scholar 

  32. Ambardekar AV, Alluri N, Patel AC, Lindenfeld J, Dorosz JL (2015) Myocardial strain and strain rate from speckle-tracking echocardiography are unable to differentiate asymptomatic biopsy-proven cellular rejection in the first year after cardiac transplantation. J Am Soc Echocardiogr 28:478–485. https://doi.org/10.1016/j.echo.2014.12.013

    Article  PubMed  Google Scholar 

  33. Sun BJ, Park JH, Kim J, Choi JO, Lee JH, Shin MS, Kim MJ, Jung HO, Park JR, Sohn IS, Kim H, Kim HK, Cho GY, Park JS, Shim CY, Shin SH, Kim KH, Kim WS, Park SW (2018) Normal reference values of diastolic strain rate in healthy individuals: chronological trends and the comparison according to genders. Echocardiography 35:1533–1541. https://doi.org/10.1111/echo.14053

    Article  PubMed  Google Scholar 

  34. Ingvarsson A, Werther Evaldsson A, Waktare J, Nilsson J, Smith GJ, Stagmo M, Roijer A, Radegran G, Meurling CJ (2018) Normal reference ranges for transthoracic echocardiography following heart transplantation. J Am Soc Echocardiogr 31:349–360. https://doi.org/10.1016/j.echo.2017.11.003

    Article  PubMed  Google Scholar 

  35. van Grootel RWJ, Kauling RM, Menting ME, McGhie J, Roos-Hesselink JW, van den Bosch AE (2018) Influence of age and sex on left ventricular diastolic strain analysis. Int J Cardiovasc Imaging 35:491–498. https://doi.org/10.1007/s10554-018-1480-4

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan Chan.

Ethics declarations

Conflict of interest

The authors declare that there are no conflict of interest to disclose.

Ethics approval

The study was approved by The Human Research and Ethics Committee at The Prince Charles Hospital, Brisbane, Australia.

Informed consent

The need for informed consent was waived due to a retrospective study design.

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

Chamberlain, R., Scalia, G.M., Shiino, K. et al. Diastolic strain imaging: a new non-invasive tool to detect subclinical myocardial dysfunction in early cardiac allograft rejection. Int J Cardiovasc Imaging 36, 317–323 (2020). https://doi.org/10.1007/s10554-019-01725-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10554-019-01725-3

Keywords

Navigation