Advertisement

Evaluation of left and right ventricle by two-dimensional speckle tracking echocardiography in systemic sclerosis patients without overt cardiac disease

Abstract

Background/objective

The aim was to evaluate the left and right ventricular functions concurrently by two-dimensional speckle tracking echocardiography (STE) in systemic sclerosis (SSc) patients without overt cardiac disease.

Methods

A total of 47 patients with SSc and 36 age- and sex-matched controls were evaluated cross-sectionally. Two-dimensional STE was used to assess the longitudinal peak systolic strains (PSS) of both ventricles including apical long-axis (APLAX), apical four-chamber (4-CH), apical two-chamber (2-CH), and global longitudinal measurements. Any association of metabolic, cardiac, and inflammatory biomarkers with PSS was investigated.

Results

The longitudinal PSS of the left ventricle [APLAX, 4-CH, 2-CH and global] were significantly lower in SSc patients than controls (− 18.2 ± 3.2 vs − 19.8 ± 2.7% p = 0.02; − 17.8 ± 3.5 vs. − 20.3 ± 3.3% p = 0.001; − 18.6 ± 3.1 vs. − 21.8 ± 3% p < 0.001; − 17.5 ± 5.7 vs. − 20.6 ± 2.7% p = 0.003, respectively). No difference was found between the groups for right ventricular strains. The longitudinal PSS-4CH correlated positively with CRP and ESR (r = 0.349, p = 0.016; r = 0.356, p = 0.014, respectively) and negatively with serum Galectin-3 (r = − 0.362, p = 0.012). Global longitudinal PSS-left ventricle (LV) correlated positively with CRP and homocysteine (r = 0.297, p = 0.043; r = 0.313, p = 0.041, respectively) and negatively with serum Galectin-3 (r = −0.314, p = 0.041). After multivariable adjustment, CRP remained the only predictor of longitudinal PSS-4CH (95% CI 0.35, 0.70, p = 0.028) and global longitudinal PSS of left ventricle (95% CI 0.004, 0.22, p = 0.043).

Conclusions

Biventricular evaluation of patients with SSc by two dimensional STE revealed reduced left ventricular longitudinal strains, despite preserved right ventricular strain, and no diastolic dysfunction. In SSc without overt cardiac disease, global cardiac assessment with 2DSTE is a promising method which seems to contribute to the detection of patients without clinical findings.

Key Points

Two dimensional STE revealed reduced left ventricular longitudinal strains, despite preserved right ventricular strain in SSc patients without overt cardiac disease.

CRP was the predictor of decreased longitudinal strains.

Cardiac assessment in SSc should be made globally.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1

References

  1. 1.

    Gabrielli A, Avvedimento EV, Krieg T (2009) Scleroderma. N Engl J Med 360(19):1989–2003. https://doi.org/10.1056/NEJMra0806188

  2. 2.

    Ferri C, Giuggioli D, Sebastiani M, Colaci M, Emdin M (2005) Heart involvement and systemic sclerosis. Lupus 14(9):702–707

  3. 3.

    Tyndall AJ, Bannert B, Vonk M, Airò P, Cozzi F, Carreira PE et al (2010) Causes and risk factors for death in systemic sclerosis: a study from the EULAR scleroderma trials and research (EUSTAR) database. Ann Rheum Dis 69(10):1809–1815. https://doi.org/10.1136/ard.2009.114264

  4. 4.

    Meier FM, Frommer KW, Dinser R, Walker UA, Czirjak L, Denton CP et al (2012) Update on the profile of the EUSTAR cohort: an analysis of the EULAR scleroderma trials and research group database. Ann Rheum Dis 71:1355–1360. https://doi.org/10.1136/annrheumdis-2011-200742

  5. 5.

    Lambova S (2014) Cardiac manifestations in systemic sclerosis. World J Cardiol 6(9):993–1005. https://doi.org/10.4330/wjc.v6.i9.993

  6. 6.

    Ross L, Prior D, Proudman S, Vacca A, Baron M, Nikpour M (2018) Defining primary systemic sclerosis heart involvement: a scoping literature review. Semin Arthritis Rheum 48:874–887. https://doi.org/10.1016/j.semarthrit.2018.07.008

  7. 7.

    Guerra F, Stronati G, Fischietti C, Ferrarini A, Zuliani L, Pomponio G, Capucci A, Danieli MG, Gabrielli A (2018) Global longitudinal strain measured by speckle tracking identifies subclinical heart involvement in patients with systemic sclerosis. Eur J Prev Cardiol 25(15):1598–1606. https://doi.org/10.1177/2047487318786315

  8. 8.

    Meune C, Avouac J, Wahbi K, Cabanes L, Wipff J, Mouthon L, Guillevin L, Kahan A, Allanore Y (2008) Cardiac involvement in systemic sclerosis assessed by tissue-doppler echocardiography during routine care: a controlled study of 100 consecutive patients. Arthritis Rheum 58(6):1803–1809. https://doi.org/10.1002/art.23463

  9. 9.

    Blessberger H, Binder T (2010) Two dimensional speckle tracking echocardiography: basic principles. Heart 96(9):716–722. https://doi.org/10.1136/hrt.2007.141002

  10. 10.

    Taniguchi T, Asano Y, Akamata K, Noda S, Masui Y, Yamada D et al (2012) Serum levels of galectin-3: possible association with fibrosis, aberrant angiogenesis, and immune activation in patients with systemic sclerosis. J Rheumatol 39(3):539–544. https://doi.org/10.3899/jrheum.110755

  11. 11.

    Van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A et al (2013) Classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755. https://doi.org/10.1136/annrheumdis-2013-204424

  12. 12.

    LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15(2):202–205

  13. 13.

    Clements P, Lachenbruch P, Siebold J, White B, Weiner S, Martin R, Weinstein A, Weisman M, Mayes M, Collier D (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22:1281–1285

  14. 14.

    Medsger TA Jr, Bombardieri S, Czirjak L, Scorza R, Della Rossa A, Bencivelli W (2003) Assessment of disease severity and prognosis. Clin Exp Rheumatol 21(3 Suppl 29):S42–S46

  15. 15.

    Valentini G, Iudici M, Walker UA, Jaeger VK, Baron M, Carreira P (2017) The European Scleroderma Trials and Research group (EUSTAR) task force for the development of revised activity criteria for systemic sclerosis: derivation and validation of a preliminarily revised EUSTAR activity index. Ann Rheum Dis 76(1):270–276. https://doi.org/10.1136/annrheumdis-2016-209768

  16. 16.

    Hsu VM, Moreyra AE, Wilson AC, Shinnar M, Shindler DM, Wilson JE, Desai A, Seibold JR (2008) Assessment of pulmonary arterial hypertension in patients with systemic sclerosis: comparison of noninvasive tests with results of right-heart catheterization. J Rheumatol 35(3):458–465

  17. 17.

    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419

  18. 18.

    W. H. O (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO expert committee. World Health Organ Tech Rep Ser 854:1–452

  19. 19.

    Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285(19):2486–2497. https://doi.org/10.1001/jama.285.19.2486

  20. 20.

    Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ, Chamber Quantification Writing Group, American Society of Echocardiography's Guidelines and Standards Committee, European Association of Echocardiography (2005) Chamber quantification writing group; American Society of Echocardiography’s guidelines and standards committee; European Association of Echocardiography. Recommendations for chamber quantification: a report from the American Society of Echocardiography’s guidelines and standards committee and the chamber quantification writing group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18(12):1440–1463. https://doi.org/10.1016/j.echo.2005.10.005

  21. 21.

    Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57:450–458

  22. 22.

    Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Böhm M, Christiaens T, Cifkova R, de Backer G, Dominiczak A, Galderisi M, Grobbee DE, Jaarsma T, Kirchhof P, Kjeldsen SE, Laurent S, Manolis AJ, Nilsson PM, Ruilope LM, Schmieder RE, Sirnes PA, Sleight P, Viigimaa M, Waeber B, Zannad F, Redon J, Dominiczak A, Narkiewicz K, Nilsson PM, Burnier M, Viigimaa M, Ambrosioni E, Caufield M, Coca A, Olsen MH, Schmieder RE, Tsioufis C, van de Borne P, Zamorano JL, Achenbach S, Baumgartner H, Bax JJ, Bueno H, Dean V, Deaton C, Erol C, Fagard R, Ferrari R, Hasdai D, Hoes AW, Kirchhof P, Knuuti J, Kolh P, Lancellotti P, Linhart A, Nihoyannopoulos P, Piepoli MF, Ponikowski P, Sirnes PA, Tamargo JL, Tendera M, Torbicki A, Wijns W, Windecker S, Clement DL, Coca A, Gillebert TC, Tendera M, Rosei EA, Ambrosioni E, Anker SD, Bauersachs J, Hitij JB, Caulfield M, de Buyzere M, de Geest S, Derumeaux GA, Erdine S, Farsang C, Funck-Brentano C, Gerc V, Germano G, Gielen S, Haller H, Hoes AW, Jordan J, Kahan T, Komajda M, Lovic D, Mahrholdt H, Olsen MH, Ostergren J, Parati G, Perk J, Polonia J, Popescu BA, Reiner Z, Rydén L, Sirenko Y, Stanton A, Struijker-Boudier H, Tsioufis C, van de Borne P, Vlachopoulos C, Volpe M, Wood DA (2013) 2013 ESH/ESC guidelines for the management of arterial hypertension: the task force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Heart J 34(28):2159–2219. https://doi.org/10.1093/eurheartj/eht151

  23. 23.

    Ganau A, Saba PS, Roman MJ, de Simone G, Realdi G, Devereux RB (1995) Ageing induces left ventricular concentric remodelling in normotensive subjects. J Hypertens 13:1818–1822

  24. 24.

    Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 10(2):165–193. https://doi.org/10.1093/ejechocard/jep007

  25. 25.

    Caballero L, Kou S, Dulgheru R, Gonjilashvili N, Athanassopoulos GD, Barone D, Baroni M, Cardim N, Gomez de Diego JJ, Oliva MJ, Hagendorff A, Hristova K, Lopez T, Magne J, Martinez C, de la Morena G, Popescu BA, Penicka M, Ozyigit T, Rodrigo Carbonero JD, Salustri A, van de Veire N, von Bardeleben RS, Vinereanu D, Voigt JU, Zamorano JL, Bernard A, Donal E, Lang RM, Badano LP, Lancellotti P (2015) Echocardiographic reference ranges for normal cardiac Doppler data: results from the NORRE study. Eur Heart J Cardiovasc Imaging 16(9):1031–1041. https://doi.org/10.1093/ehjci/jev083

  26. 26.

    Porter TR, Shillcutt SK, Adams MS, Desjardins G, Glas KE, Olson JJ, Troughton RW (2015) Guidelines for the use of echocardiography as a monitor for therapeutic intervention in adults: a report from the American Society of Echocardiography. J Am Soc Echocardiogr 28(1):40–56. https://doi.org/10.1016/j.echo.2014.09.009

  27. 27.

    Delgado V, Ypenburg C, van Bommel RJ, Tops LF, Mollema SA, Marsan NA, Bleeker GB, Schalij MJ, Bax JJ (2008) Assessment of left ventricular dyssynchrony by speckle tracking strain imaging comparison between longitudinal, circumferential, and radial strain in cardiac resynchronization therapy. J Am Coll Cardiol 51(20):1944–1952. https://doi.org/10.1016/j.jacc.2008.02.040

  28. 28.

    Yilmazer B, Sahin T, Cefle A (2016) Impaired myocardial deformation in psoriatic arthritis patients assessment by speckle tracking echocardiography. Acta Rheumatol Port 41(2):131–137

  29. 29.

    Spethmann S, Dreger H, Schattke S, Riemekasten G, Borges AC, Baumann G, Knebel F (2012) Two-dimensional speckle tracking of the left ventricle in patients with systemic sclerosis for early detection of myocardial involvement. Eur Heart J Cardiovasc Imaging 13(10):863–870. https://doi.org/10.1093/ehjci/jes047

  30. 30.

    Perk G, Tunick PA, Kronzon I (2007) Non-Doppler two-dimensional strain imaging by echocardiography–from technical considerations to clinical applications. J Am Soc Echocardiogr 20(3):234–243. https://doi.org/10.1016/j.echo.2006.08.023

  31. 31.

    Russo C, Jin Z, Elkind MS, Rundek T, Homma S, Sacco RL et al (2014) Prevalence and prognostic value of subclinical left ventricular systolic dysfunction by global longitudinal strain in a community-based cohort. Eur J Heart Fail 16(12):1301–1309. https://doi.org/10.1002/ejhf.154

  32. 32.

    Kepez A, Akdogan A, Sade LE, Deniz A, Kalyoncu U, Karadag O, Hayran M, Aytemir K, Ertenli I, Kiraz S, Calguneri M, Kabakcı G, Tokgozoglu L (2008) Detection of subclinical cardiac involvement in systemic sclerosis by echocardiographic strain imaging. Echocardiography 25(2):191–197. https://doi.org/10.1111/j.1540-8175.2007.00582.x

  33. 33.

    D'Andrea A, Stisi S, Bellissimo S, Vigorito F, Scotto di Uccio F, Tozzi N et al (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. https://doi.org/10.1016/j.euje.2005.01.002

  34. 34.

    Schattke S, Knebel F, Grohmann A, Dreger H, Kmezik F, Riemekasten G et al (2010) Early right ventricular systolic dysfunction in patients with systemic sclerosis without pulmonary hypertension: a Doppler tissue and speckle tracking echocardiography study. Cardiovasc Ultrasound 8:3. https://doi.org/10.1186/1476-7120-8-3

  35. 35.

    de Groote P, Gressin V, Hachulla E, Carpentier P, Guillevin L, Kahan A, Cabane J, Frances C, Lamblin N, Diot E, Patat F, Sibilia J, Petit H, Cracowski JL, Clerson P, Humbert M, for the ItinerAIR-Scleroderma Investigators (2008) Evaluation of cardiac abnormalities by Doppler echocardiography in a large nationwide multicentric cohort of patients with systemic sclerosis. Ann Rheum Dis 67(1):31–36. https://doi.org/10.1136/ard.2006.057760

  36. 36.

    Maione S, Cuomo G, Giunta A, Tanturri de Horatio L, La Montagna G, Manguso F et al (2005) Echocardiographic alterations in systemic sclerosis: a longitudinal study. Semin Arthritis Rheum 34(5):721–727. https://doi.org/10.1016/j.semarthrit.2004.11.001

  37. 37.

    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–S37

  38. 38.

    Mueller KA, Mueller II, Eppler D, Zuern CS, Seizer P, Kramer U et al (2015) Clinical and histopathological features of patients with systemic sclerosis undergoing endomyocardial biopsy. PLoS One 10(5):e0126707. https://doi.org/10.1371/journal.pone.0126707

  39. 39.

    Shang Q, Tam LS, Yip GW, Sanderson JE, Zhang Q, Li EK et al (2011) High prevalence of subclinical left ventricular dysfunction in patients with psoriatic arthritis. J Rheumatol 38(7):1363–1370. https://doi.org/10.3899/jrheum.101136

  40. 40.

    Kania G, Blyszczuk P, Eriksson U (2009) Mechanisms of cardiac fibrosis in inflammatory heart disease. Trends Cardiovasc Med 19(8):247–252. https://doi.org/10.1016/j.tcm.2010.02.005

  41. 41.

    Besler C, Lang D, Urban D, Rommel KP, von Roeder M, Fengler K et al (2017) Plasma and cardiac galectin-3 in patients with heart failure reflects both inflammation and fibrosis: implications for its use as a biomarker. Circ Heart Fail 10(3):e003804. https://doi.org/10.1161/CIRCHEARTFAILURE

  42. 42.

    Song X, Qian X, Shen M, Jiang R, Wagner MB, Ding G, Chen G, Shen B (2015) Protein kinase C promotes cardiac fibrosis and heart failure by modulating galectin-3 expression. Biochim Biophys Acta 1853(2):513–521. https://doi.org/10.1016/j.bbamcr.2014.12.001

  43. 43.

    Koca SS, Akbas F, Ozgen M, Yolbas S, Ilhan N, Gundogdu B, Isik A (2014) Serum galectin-3 level in systemic sclerosis. Clin Rheumatol 33(2):215–220. https://doi.org/10.1007/s10067-013-2346-8

  44. 44.

    Hromádka M, Seidlerová J, Suchý D, Rajdl D, Lhotský J, Ludvík J, Rokyta R, Baxa J (2017) Myocardial fibrosis detected by magnetic resonance in systemic sclerosis patients- relationship with biochemical and echocardiography parameters. Int J Cardiol 249:448–453. https://doi.org/10.1016/j.ijcard.2017.08.072

Download references

Acknowledgments

The authors are grateful to Mr. Jeremy Jones of the Academic Writing Department of Kocaeli University, Izmit, Turkey, for his assistance in editing the English language usage used and for his help and advice concerning the contents of this manuscript.

Author information

Correspondence to Duygu Temiz Karadag.

Ethics declarations

This article does not contain any studies with animals performed by any of the authors. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by Kocaeli University School of Medicine Ethics Committee for non-invasive clinical trials with protocol number 178 and name “Evaluation of the ventricular dysfunction by two-dimensional speckle tracking echocardiography in SSc patients without pulmonary hypertension” in 16 June 2015 (KOU KAEK 2015/178).

Informed consent

Informed consent was obtained from all individual participants included in the study.

Disclosures

None.

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

Verify currency and authenticity via CrossMark

Cite this article

Karadag, D.T., Sahin, T., Tekeoglu, S. et al. Evaluation of left and right ventricle by two-dimensional speckle tracking echocardiography in systemic sclerosis patients without overt cardiac disease. Clin Rheumatol 39, 37–48 (2020). https://doi.org/10.1007/s10067-019-04604-3

Download citation

Keywords

  • Left ventricle
  • Right ventricle
  • Speckle tracking echocardiography
  • Systemic sclerosis
  • Systolic dysfunction