Skip to main content
SpringerLink
Log in

Prognostic value of right atrial strain in systemic sclerosis based on tissue tracking analysis using cine cardiac magnetic resonance imaging: a retrospective observational study

  • Original Article
  • Published:
Heart and Vessels Aims and scope Submit manuscript

Abstract

Interstitial lung disease and cardiac involvement are common manifestations and prognostic factors of systemic sclerosis. However, it is unclear whether impaired right atrial function associated with interstitial lung disease in systemic sclerosis can be used as a prognostic factor in this patient population. Therefore, this study aimed to investigate the relationship between right atrial function, interstitial lung disease, and prognosis in patients with systemic sclerosis using tissue tracking analysis with cine cardiac magnetic resonance imaging. In this retrospective observational study, a total of 40 patients with systemic sclerosis were enrolled. Tissue tracking analysis was used to obtain time curves of right atrial strain. Reservoir (total strain), conduit (passive strain), and booster (active strain) pump function were calculated, and right atrial strain, interstitial lung disease, and clinical outcomes were examined. An adverse clinical event was defined as all-cause death. Overall, 23 patients had interstitial lung disease (58%). Six patients died during the follow-up (median, 44 months). The total skin score and right ventricular systolic pressure on echocardiography were higher in patients with an event than in those without an event (28 ± 16% vs. 13 ± 13%, P = 0.02; 46.3 ± 10.7 mmHg vs. 36.0 ± 8.5 mmHg, P = 0.01, respectively). Further, right atrial total strain and active strain were significantly lower in patients with an event than in those without an event (14.3 ± 11.3% vs. 25.8 ± 11.4%, P = 0.03; 3.48 ± 2.37 vs. 11.7 ± 6.78, P = 0.007, respectively). Multivariate analysis revealed that active strain was an independent predictor of all-cause death (hazard ratio 0.76, P = 0.029). Kaplan–Meier analysis revealed that the survival rate was significantly higher in patients with right atrial active strain levels above the cutoff 7.4 (P < 0.05). In systemic sclerosis, right atrial booster function was predictive of mortality. Hence, right atrial functional assessment may have incremental prognostic value for patients with systemic sclerosis, leading to better risk stratification.

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

Data availability

The deidentified participant data will be shared on a request basis. Please directly contact the corresponding author to request data sharing.

References

  1. Gabrielli A, Avvedimento EV, Krieg T (2009) Scleroderma. N Engl J Med 360(19):1989–2003

    Article  CAS  PubMed  Google Scholar 

  2. van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, Furst DE, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Muller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Ellen Csuka M, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755

    Article  PubMed  Google Scholar 

  3. Lambova S (2014) Cardiac manifestations in systemic sclerosis. World J Cardiol 6(9):993–1005

    Article  PubMed  PubMed Central  Google Scholar 

  4. Venalis P, Kumanovics G, Schulze-Koops H, Distler A, Dees C, Zerr P, Palumbo-Zerr K, Czirjak L, Mackevic Z, Lundberg IE, Distler O, Schett G, Distler JH (2015) Cardiomyopathy in murine models of systemic sclerosis. Arthritis Rheumatol 67(2):508–516

    Article  CAS  PubMed  Google Scholar 

  5. Tzelepis GE, Kelekis NL, Plastiras SC, Mitseas P, Economopoulos N, Kampolis C, Gialafos EJ, Moyssakis I, Moutsopoulos HM (2007) Pattern and distribution of myocardial fibrosis in systemic sclerosis: a delayed enhanced magnetic resonance imaging study. Arthritis Rheum 56(11):3827–3836

    Article  PubMed  Google Scholar 

  6. Vacca A, Meune C, Gordon J, Chung L, Proudman S, Assassi S, Nikpour M, Rodriguez-Reyna TS, Khanna D, Lafyatis R, Matucci-Cerinic M, Distler O, Allanore Y (2014) Cardiac arrhythmias and conduction defects in systemic sclerosis. Rheumatology 53(7):1172–1177

    Article  PubMed  Google Scholar 

  7. Galie N, Humbert M, Vachiery JL, Gibbs S, Lang I, Torbicki A, Simonneau G, Peacock A, Vonk Noordegraaf A, Beghetti M, Ghofrani A, Gomez Sanchez MA, Hansmann G, Klepetko W, Lancellotti P, Matucci M, McDonagh T, Pierard LA, Trindade PT, Zompatori M, Hoeper M (2016) 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: the joint task force for the diagnosis and treatment of pulmonary hypertension of the European society of cardiology (ESC) and the European respiratory society (ERS): endorsed by: association for European paediatric and congenital cardiology (AEPC), international society for heart and lung transplantation (ISHLT). Eur Heart J 37(1):67–119

    Article  PubMed  Google Scholar 

  8. Elhai M, Meune C, Boubaya M, Avouac J, Hachulla E, Balbir-Gurman A, Riemekasten G, Airò P, Joven B, Vettori S, Cozzi F, Ullman S, Czirják L, Tikly M, Müller-Ladner U, Caramaschi P, Distler O, Iannone F, Ananieva LP, Hesselstrand R, Becvar R, Gabrielli A, Damjanov N, Salvador MJ, Riccieri V, Mihai C, Szücs G, Walker UA, Hunzelmann N, Martinovic D, Smith V, Müller CS, Montecucco CM, Opris D, Ingegnoli F, Vlachoyiannopoulos PG, Stamenkovic B, Rosato E, Heitmann S, Distler JHW, Zenone T, Seidel M, Vacca A, Langhe E, Novak S, Cutolo M, Mouthon L, Henes J, Chizzolini C, Mühlen CAV, Solanki K, Rednic S, Stamp L, Anic B, Santamaria VO, De Santis M, Yavuz S, Sifuentes-Giraldo WA, Chatelus E, Stork J, Laar JV, Loyo E, de la Peña G, Lefebvre P, Eyerich K, Cosentino V, Alegre-Sancho JJ, Kowal-Bielecka O, Rey G, Matucci-Cerinic M, Allanore Y (2017) Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis 76(11):1897–1905

    Article  PubMed  Google Scholar 

  9. D’Andrea A, Stisi S, Bellissimo S, Vigorito F, Scotto di Uccio F, Tozzi N, Moscato F, Pezzullo E, Calabrò R, Scherillo M (2005) Early impairment of myocardial function in systemic sclerosis: non-invasive assessment by Doppler myocardial and strain rate imaging. Eur J Echocardiogr 6(6):407–418

    Article  PubMed  Google Scholar 

  10. D’Andrea A, D’Alto M, Di Maio M, Vettori S, Benjamin N, Cocchia R, Argiento P, Romeo E, Di Marco G, Russo MG, Valentini G, Calabrò R, Bossone E, Grünig E (2016) Right atrial morphology and function in patients with systemic sclerosis compared to healthy controls: a two-dimensional strain study. Clin Rheumatol 35(7):1733–1742

    Article  PubMed  Google Scholar 

  11. Bhave NM, Visovatti SH, Kulick B, Kolias TJ, McLaughlin VV (2017) Right atrial strain is predictive of clinical outcomes and invasive hemodynamic data in group 1 pulmonary arterial hypertension. Int J Cardiovasc Imaging 33(6):847–855

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gorter TM, van Veldhuisen DJ, Bauersachs J, Borlaug BA, Celutkiene J, Coats AJS, Crespo-Leiro MG, Guazzi M, Harjola VP, Heymans S, Hill L, Lainscak M, Lam CSP, Lund LH, Lyon AR, Mebazaa A, Mueller C, Paulus WJ, Pieske B, Piepoli MF, Ruschitzka F, Rutten FH, Seferovic PM, Solomon SD, Shah SJ, Triposkiadis F, Wachter R, Tschöpe C, de Boer RA (2018) Right heart dysfunction and failure in heart failure with preserved ejection fraction: mechanisms and management. Position statement on behalf of the heart failure association of the European society of cardiology. Eur J Heart Fail 20(1):16–37

    Article  PubMed  Google Scholar 

  13. Allanore Y, Meune C (2010) Primary myocardial involvement in systemic sclerosis: evidence for a microvascular origin. Clin Exp Rheumatol 28(5 Suppl 62):S48–S53

    CAS  PubMed  Google Scholar 

  14. Bratis K, Lindholm A, Hesselstrand R, Arheden H, Karabela G, Stavropoulos E, Katsifis G, Kolovou G, Kitas GD, Sfikakis PP, Koutsogeorgopoulou L, Mavrogeni S, Ostenfeld E (2019) CMR feature tracking in cardiac asymptomatic systemic sclerosis: clinical implications. PLoS ONE 14(8):e0221021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. American Thoracic Society (2000) Idiopathic pulmonary fibrosis diagnosis and treatment. International consensus statement American thoracic society (ATS), and the European respiratory society (ERS). Am J Respir Crit Care Med 161(21):646–664

    Google Scholar 

  16. Pedrizzetti G, Claus P, Kilner PJ, Nagel E (2016) Principles of cardiovascular magnetic resonance feature tracking and echocardiographic speckle tracking for informed clinical use. J Cardiovasc Magn Reson 18(1):51

    Article  PubMed  PubMed Central  Google Scholar 

  17. Karaahmet T, Tigen K, Gurel E, Takir M, Avci A, Cevik C, Pala S, Dundar C, Basaran Y (2010) Impact of systemic sclerosis on electromechanical characteristics of the heart. Vessels 25(3):223–228

    Article  Google Scholar 

  18. Sano M, Satoh H, Suwa K, Nobuhara M, Saitoh T, Saotome M, Urushida T, Katoh H, Shimoyama K, Suzuki D, Ogawa N, Takehara Y, Sakahara H, Hayashi H (2015) Characteristics and clinical relevance of late gadolinium enhancement in cardiac magnetic resonance in patients with systemic sclerosis. Heart Vessels 30(6):779–788

    Article  PubMed  Google Scholar 

  19. Bulkley BH, Ridolfi RL, Salyer WR, Hutchins GM (1976) Myocardial lesions of progressive systemic sclerosis. A cause of cardiac dysfunction. Circulation 53(3):483–490

    Article  CAS  PubMed  Google Scholar 

  20. Hinchcliff M, Desai CS, Varga J, Shah SJ (2012) Prevalence, prognosis, and factors associated with left ventricular diastolic dysfunction in systemic sclerosis. Clin Exp Rheumatol 30(2 Suppl 71):S30-37

    PubMed  PubMed Central  Google Scholar 

  21. Yiu KH, Ninaber MK, Kroft LJ, Schouffoer AA, Stolk J, Scherer HU, Meijs J, de Vries-Bouwstra J, Tse HF, Delgado V, Bax JJ, Huizinga TW, Marsan NA (2016) Impact of pulmonary fibrosis and elevated pulmonary pressures on right ventricular function in patients with systemic sclerosis. Rheumatology 55(3):504–512

    PubMed  Google Scholar 

  22. Padeletti M, Cameli M, Lisi M, Zacà V, Tsioulpas C, Bernazzali S, Maccherini M, Mondillo S (2011) Right atrial speckle tracking analysis as a novel noninvasive method for pulmonary hemodynamics assessment in patients with chronic systolic heart failure. Echocardiography 28(6):658–664

    Article  PubMed  Google Scholar 

  23. Lazar EJ, Goldberger J, Peled H, Sherman M, Frishman WH (1988) Atrial infarction: diagnosis and management. Am Heart J 116(4):1058–1063

    Article  CAS  PubMed  Google Scholar 

  24. Rai AB, Lima E, Munir F, Faisal KA, Waqas A, Bughio S, Ul HE, Attique HB, Rahman ZU (2015) Speckle tracking echocardiography of the right atrium: the neglected chamber. Clin Cardiol 38(11):692–697

    Article  PubMed  PubMed Central  Google Scholar 

  25. Durmus E, Sunbul M, Tigen K, Kivrak T, Ozen G, Sari I, Direskeneli H, Basaran Y (2015) Right ventricular and atrial functions in systemic sclerosis patients without pulmonary hypertension Speckle-tracking echocardiographic study. Herz 40(4):709–715

    Article  CAS  PubMed  Google Scholar 

  26. Deschle HA, Amenabar A, Casso NA, Gantesti J, Carnevalini M, Alfie L, Torres Bianqui C, Ottonello P, Katib MC (2018) Behavior of right atrial strain in high systolic pulmonary artery pressure. Echocardiography 35(10):1557–1563

    Article  PubMed  Google Scholar 

  27. Sakata K, Uesugi Y, Isaka A, Minamishima T, Matsushita K, Satoh T, Yoshino H (2016) Evaluation of right atrial function using right atrial speckle tracking analysis in patients with pulmonary artery hypertension. J Echocardiogr 14(1):30–38

    Article  PubMed  Google Scholar 

  28. McLaughlin VV, Archer SL, Badesch DB, Barst RJ, Farber HW, Lindner JR, Mathier MA, McGoon MD, Park MH, Rosenson RS, Rubin LJ, Tapson VF, Varga J, Harrington RA, Anderson JL, Bates ER, Bridges CR, Eisenberg MJ, Ferrari VA, Grines CL, Hlatky MA, Jacobs AK, Kaul S, Lichtenberg RC, Lindner JR, Moliterno DJ, Mukherjee D, Pohost GM, Rosenson RS, Schofield RS, Shubrooks SJ, Stein JH, Tracy CM, Weitz HH, Wesley DJ (2009) ACCF/AHA 2009 expert consensus document on pulmonary hypertension: a report of the American college of cardiology foundation task force on expert consensus documents and the American heart association: developed in collaboration with the American college of chest physicians, American thoracic society inc, and the pulmonary hypertension association. Circulation 119(16):2250–2294

    Article  PubMed  Google Scholar 

  29. Melenovsky V, Borlaug BA, Rosen B, Hay I, Ferruci L, Morell CH, Lakatta EG, Najjar SS, Kass DA (2007) Cardiovascular features of heart failure with preserved ejection fraction versus nonfailing hypertensive left ventricular hypertrophy in the urban Baltimore community: the role of atrial remodeling/dysfunction. J Am Coll Cardiol 49(2):198–207

    Article  PubMed  Google Scholar 

  30. Freed BH, Daruwalla V, Cheng JY, Aguilar FG, Beussink L, Choi A, Klein DA, Dixon D, Baldridge A, Rasmussen-Torvik LJ, Maganti K, Shah SJ (2016) Prognostic utility and clinical significance of cardiac mechanics in heart failure with preserved ejection fraction: importance of left atrial strain. Circ Cardiovasc Imaging. https://doi.org/10.1161/circimaging.115.003754

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gaynor SL, Maniar HS, Bloch JB, Steendijk P, Moon MR (2005) Right atrial and ventricular adaptation to chronic right ventricular pressure overload. Circulation 112(9 Suppl):I212–I218

    PubMed  Google Scholar 

  32. Carter P, Lagan J, Fortune C, Bhatt DL, Vestbo J, Niven R, Chaudhuri N, Schelbert EB, Potluri R, Miller CA (2019) Association of cardiovascular disease with respiratory disease. J Am Coll Cardiol 73(17):2166–2177

    Article  PubMed  Google Scholar 

  33. Bisbal F, Baranchuk A, Braunwald E, Bayés de Luna A, Bayés-Genís A (2020) Atrial failure as a clinical entity: JACC review topic of the week. J Am Coll Cardiol 75(2):222–232

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

None.

Funding

No extramural funding was provided to support this study.

Author information

Authors and Affiliations

  1. Department of Cardiology, Tokyo Women’s Medical University, 8-1 Kawada-Cho, Shinjyuku-Ku, Tokyo, 162-8666, Japan

    Akiko Sakai, Risako Nakao & Junichi Yamaguchi

  2. Department of Diagnostic Imaging & Nuclear Medicine, Tokyo Women’s Medical University, 8-1 Kawada-Cho, Shinjyuku-Ku, Tokyo, 162-8666, Japan

    Michinobu Nagao, Atsushi Yamamoto & Shuji Sakai

Authors
  1. Akiko Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michinobu Nagao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atsushi Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Risako Nakao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuji Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junichi Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by AS. The first draft of the manuscript was written by AS, and all the authors commented on previous versions of the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Akiko Sakai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the International Review Board of the Tokyo Women’s Medical University.

Disclosure of potential conflicts of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the International Review Board of the Tokyo Women’s Medical University.

Informed consent

Informed consent was obtained from all subjects.

Consent to participate

Informed consent was obtained from all individual participants for participation in this study.

Additional information

Publisher's Note

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

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

Sakai, A., Nagao, M., Yamamoto, A. et al. Prognostic value of right atrial strain in systemic sclerosis based on tissue tracking analysis using cine cardiac magnetic resonance imaging: a retrospective observational study. Heart Vessels 39, 135–143 (2024). https://doi.org/10.1007/s00380-023-02320-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00380-023-02320-2

Keywords

Search

Navigation