Skip to main content
Top
Published in: Rheumatology International 1/2017

01-01-2017 | Observational Research

Cardiac mechanics and heart rate variability in patients with systemic sclerosis: the association that we should not miss

Authors: Maja Zlatanovic, Marijana Tadic, Vera Celic, Branislava Ivanovic, Ana Stevanovic, Nemanja Damjanov

Published in: Rheumatology International | Issue 1/2017

Login to get access

Abstract

We aimed to determine left ventricular (LV) and right ventricular (RV) structure, function and mechanics, as well as heart rate variability (HRV), and their relationship, in patients with systemic sclerosis (SSc). The study included 41 SSc patients and 30 age-matched healthy volunteers. All the patients underwent clinical examination, serological tests, pulmonary function testing, 24-h Holter monitoring and complete two-dimensional echocardiography including strain analysis. The parameters of LV structure (interventricular septum thickness and LV mass index) and RV structure (RV wall thickness) were significantly higher in SSc patients. LV and RV diastolic function (estimated by mitral and tricuspid E/e′ ratio) was significantly impaired in SSc group comparing with the healthy controls. LV and RV longitudinal function was significantly deteriorated in SSc patients. LV circumferential strain was also significantly lower in SSc group, whereas LV radial strain was similar between the observed groups. All parameters of time and frequency domain of HRV were decreased in SSc patients. LV and RV cardiac remodeling parameters, particularly diastolic function and longitudinal strain, were associated with HRV indices without regard to the main demographic or the clinical and echocardiographic characteristics. Rodnan Skin Score was also independently associated with biventricular cardiac remodeling in SSc patients. LV and RV structure, function and mechanics, as well as autonomic nervous function, were significantly impaired in SSc patients. There is the significant association between biventricular cardiac remodeling and autonomic function in these patients, which could be useful for their everyday clinical assessment.
Literature
1.
go back to reference D’Angelo WA, Fries JF, Masi AT, Shulman LE (1969) Pathologic observations in systemic sclerosis (scleroderma): study of fifty-eight autopsy cases and fifty-eight matched controls. Am J Med 46:428–440CrossRefPubMed D’Angelo WA, Fries JF, Masi AT, Shulman LE (1969) Pathologic observations in systemic sclerosis (scleroderma): study of fifty-eight autopsy cases and fifty-eight matched controls. Am J Med 46:428–440CrossRefPubMed
2.
go back to reference Bulkley BH, Ridolfi RL, Salyer WR, Hutchins GM (1976) Myocardial lesions of progressive systemic sclerosis. A cause of cardiac dysfunction. Circulation 53:483–490CrossRefPubMed Bulkley BH, Ridolfi RL, Salyer WR, Hutchins GM (1976) Myocardial lesions of progressive systemic sclerosis. A cause of cardiac dysfunction. Circulation 53:483–490CrossRefPubMed
3.
go back to reference 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 15:202–205PubMed 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 15:202–205PubMed
4.
go back to reference Ferri C, Giuggioli D, Sebastiani M, Colaci M, Emdin M (2005) Heart involvement and systemic sclerosis. Lupus 14:702–707CrossRefPubMed Ferri C, Giuggioli D, Sebastiani M, Colaci M, Emdin M (2005) Heart involvement and systemic sclerosis. Lupus 14:702–707CrossRefPubMed
5.
go back to reference 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):407–418CrossRefPubMed 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):407–418CrossRefPubMed
6.
go back to reference Schattke S, Knebel F, Grohmann A, Dreger H, Kmezik F, Riemekasten G, Baumann G, Borges AC (2010) Early right ventricular systolic dysfunction in patients with systemic sclerosis without pulmonary hypertension: a Doppler Tissue and Speckle Tracking echocardiography study. Cardiovasc Ultrasound 8:3CrossRefPubMedPubMedCentral Schattke S, Knebel F, Grohmann A, Dreger H, Kmezik F, Riemekasten G, Baumann G, Borges AC (2010) Early right ventricular systolic dysfunction in patients with systemic sclerosis without pulmonary hypertension: a Doppler Tissue and Speckle Tracking echocardiography study. Cardiovasc Ultrasound 8:3CrossRefPubMedPubMedCentral
7.
go back to reference Nordin A, Björnådal L, Larsson A, Svenungsson E, Jensen-Urstad K (2014) Electrocardiography in 110 patients with systemic sclerosis: a cross-sectional comparison with population-based controls. Scand J Rheumatol 43(3):221–225CrossRefPubMed Nordin A, Björnådal L, Larsson A, Svenungsson E, Jensen-Urstad K (2014) Electrocardiography in 110 patients with systemic sclerosis: a cross-sectional comparison with population-based controls. Scand J Rheumatol 43(3):221–225CrossRefPubMed
8.
go back to reference Dessein PH, Joffe BI, Metz RM, Millar DL, Lawson M, Stanwix AE (1992) Autonomic dysfunction in systemic sclerosis: sympathetic overactivity and instability. Am J Med 93(2):143–150CrossRefPubMed Dessein PH, Joffe BI, Metz RM, Millar DL, Lawson M, Stanwix AE (1992) Autonomic dysfunction in systemic sclerosis: sympathetic overactivity and instability. Am J Med 93(2):143–150CrossRefPubMed
9.
go back to reference Di Franco M, Paradiso M, Riccieri V, Basili S, Mammarella A, Valesini G (2007) Autonomic dysfunction and microvascular damage in systemic sclerosis. Clin Rheumatol 26(8):1278–1283CrossRefPubMed Di Franco M, Paradiso M, Riccieri V, Basili S, Mammarella A, Valesini G (2007) Autonomic dysfunction and microvascular damage in systemic sclerosis. Clin Rheumatol 26(8):1278–1283CrossRefPubMed
10.
go back to reference Gigante A, Rosato E, Liberatori M, Barbano B, Cianci R, Gasperini ML, Sardo L, Marra AM, Amoroso A, Salsano F, Fiorentini A, Tubani L (2014) Autonomic dysfunction in patients with systemic sclerosis: correlation with intrarenal arterial stiffness. Int J Cardiol 177(2):578–580CrossRefPubMed Gigante A, Rosato E, Liberatori M, Barbano B, Cianci R, Gasperini ML, Sardo L, Marra AM, Amoroso A, Salsano F, Fiorentini A, Tubani L (2014) Autonomic dysfunction in patients with systemic sclerosis: correlation with intrarenal arterial stiffness. Int J Cardiol 177(2):578–580CrossRefPubMed
11.
go back to reference Othman KM, Assaf NY, Farouk HM, Aly Hassan IM (2010) Autonomic dysfunction predicts early cardiac affection in patients with systemic sclerosis. Clin Med Insights Arthritis Musculoskelet Disord 3:43–54PubMedPubMedCentral Othman KM, Assaf NY, Farouk HM, Aly Hassan IM (2010) Autonomic dysfunction predicts early cardiac affection in patients with systemic sclerosis. Clin Med Insights Arthritis Musculoskelet Disord 3:43–54PubMedPubMedCentral
12.
go back to reference Xhyheri B, Manfrini O, Mazzolini M, Pizzi C, Bugiardini R (2012) Heart rate variability today. Prog Cardiovasc Dis 55(3):321–331CrossRefPubMed Xhyheri B, Manfrini O, Mazzolini M, Pizzi C, Bugiardini R (2012) Heart rate variability today. Prog Cardiovasc Dis 55(3):321–331CrossRefPubMed
13.
go back to reference Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American society of echocardiography and the European association of cardiovascular imaging. J Am Soc Echocardiogr 28:1–39CrossRefPubMed Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American society of echocardiography and the European association of cardiovascular imaging. J Am Soc Echocardiogr 28:1–39CrossRefPubMed
14.
go back to reference Quinones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA (2002) Recommendations for quantification of Doppler echocardiography: a report from the Doppler quantification task force of the nomenclature and standards committee of the American Society of Echocardiography. J Am Soc Echocardiogr 15:167–184CrossRefPubMed Quinones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA (2002) Recommendations for quantification of Doppler echocardiography: a report from the Doppler quantification task force of the nomenclature and standards committee of the American Society of Echocardiography. J Am Soc Echocardiogr 15:167–184CrossRefPubMed
15.
go back to reference Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA et al (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 22:107–133CrossRefPubMed Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA et al (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 22:107–133CrossRefPubMed
16.
go back to reference Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K et al (2010) Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23:685–713CrossRefPubMed Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K et al (2010) Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23:685–713CrossRefPubMed
17.
go back to reference Task Force of the European Society of Cardiology, and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17:354–381CrossRef Task Force of the European Society of Cardiology, and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17:354–381CrossRef
18.
go back to reference Mele D, Censi S, La Corte R, Lo Monaco A, Locaputo A, Ceconi C et al (2008) Abnormalities of left ventricular function in asymptomatic patients with systemic sclerosis using Doppler measures of myocardial strain. J Am Soc Echocardiogr 21:1257–1264CrossRefPubMed Mele D, Censi S, La Corte R, Lo Monaco A, Locaputo A, Ceconi C et al (2008) Abnormalities of left ventricular function in asymptomatic patients with systemic sclerosis using Doppler measures of myocardial strain. J Am Soc Echocardiogr 21:1257–1264CrossRefPubMed
19.
go back to reference Kepez A, Akdogan A, Sade LE, Deniz A, Kalyoncu U, Karadag O et al (2008) Detection of subclinical cardiac involvement in systemic sclerosis by echocardiographic strain imaging. Echocardiography 25:191–197CrossRefPubMed Kepez A, Akdogan A, Sade LE, Deniz A, Kalyoncu U, Karadag O et al (2008) Detection of subclinical cardiac involvement in systemic sclerosis by echocardiographic strain imaging. Echocardiography 25:191–197CrossRefPubMed
20.
go back to reference Ivanovic BA, Tadic MV, Zlatanovic MM, Damjanov NN, Ostojić PM, Bonaci-Nikolic BN (2012) Which factors impact myocardial function in systemic sclerosis? Echocardiography 29(3):307–317CrossRefPubMed Ivanovic BA, Tadic MV, Zlatanovic MM, Damjanov NN, Ostojić PM, Bonaci-Nikolic BN (2012) Which factors impact myocardial function in systemic sclerosis? Echocardiography 29(3):307–317CrossRefPubMed
21.
go back to reference 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 an early detection of myocardial involvement. Eur Heart J Cardiovasc Imaging 13(10):863–870CrossRefPubMed 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 an early detection of myocardial involvement. Eur Heart J Cardiovasc Imaging 13(10):863–870CrossRefPubMed
22.
go back to reference Spethmann S, Rieper K, Riemekasten G, Borges AC, Schattke S, Burmester GR, Hewing B, Baumann G, Dreger H, Knebel F (2014) Echocardiographic follow-up of patients with systemic sclerosis by 2D speckle tracking echocardiography of the left ventricle. Cardiovasc Ultrasound 12:13CrossRefPubMedPubMedCentral Spethmann S, Rieper K, Riemekasten G, Borges AC, Schattke S, Burmester GR, Hewing B, Baumann G, Dreger H, Knebel F (2014) Echocardiographic follow-up of patients with systemic sclerosis by 2D speckle tracking echocardiography of the left ventricle. Cardiovasc Ultrasound 12:13CrossRefPubMedPubMedCentral
23.
go back to reference Yiu KH, Schouffoer AA, Marsan NA, Ninaber MK, Stolk J, Vlieland TV, Scherptong RW, Delgado V, Holman ER, Tse HF, Huizinga TW, Bax JJ, Schuerwegh AJ (2011) Left ventricular dysfunction assessed by speckle-tracking strain analysis in patients with systemic sclerosis: relationship to functional capacity and ventricular arrhythmias. Arthritis Rheum 63(12):3969–3978CrossRefPubMed Yiu KH, Schouffoer AA, Marsan NA, Ninaber MK, Stolk J, Vlieland TV, Scherptong RW, Delgado V, Holman ER, Tse HF, Huizinga TW, Bax JJ, Schuerwegh AJ (2011) Left ventricular dysfunction assessed by speckle-tracking strain analysis in patients with systemic sclerosis: relationship to functional capacity and ventricular arrhythmias. Arthritis Rheum 63(12):3969–3978CrossRefPubMed
24.
go back to reference Tigen K, Sunbul M, Ozen G, Durmus E, Kivrak T, Cincin A, Ozben B, Atas H, Direskeneli H, Basaran Y (2014) Regional myocardial dysfunction assessed by two-dimensional speckle tracking echocardiography in systemic sclerosis patients with fragmented QRS complexes. J Electrocardiol 47(5):677–683CrossRefPubMed Tigen K, Sunbul M, Ozen G, Durmus E, Kivrak T, Cincin A, Ozben B, Atas H, Direskeneli H, Basaran Y (2014) Regional myocardial dysfunction assessed by two-dimensional speckle tracking echocardiography in systemic sclerosis patients with fragmented QRS complexes. J Electrocardiol 47(5):677–683CrossRefPubMed
25.
go back to reference 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):709–715CrossRefPubMed 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):709–715CrossRefPubMed
26.
go back to reference Pigatto E, Peluso D, Zanatta E, Polito P, Miatton P, Bourji K, Badano LP, Punzi L, Cozzi F (2015) Evaluation of right ventricular function performed by 3D-echocardiography in scleroderma patients. Reumatismo 66(4):259–263CrossRefPubMed Pigatto E, Peluso D, Zanatta E, Polito P, Miatton P, Bourji K, Badano LP, Punzi L, Cozzi F (2015) Evaluation of right ventricular function performed by 3D-echocardiography in scleroderma patients. Reumatismo 66(4):259–263CrossRefPubMed
27.
go back to reference Mukherjee M, Chung SE, Ton VK, Tedford RJ, Hummers LK, Wigley FM, Abraham TP, Shah AA (2016) Unique abnormalities in right ventricular longitudinal strain in systemic sclerosis patients. Circ Cardiovasc Imaging 9(6):e003792CrossRefPubMed Mukherjee M, Chung SE, Ton VK, Tedford RJ, Hummers LK, Wigley FM, Abraham TP, Shah AA (2016) Unique abnormalities in right ventricular longitudinal strain in systemic sclerosis patients. Circ Cardiovasc Imaging 9(6):e003792CrossRefPubMed
28.
go back to reference Hachulla AL, Launay D, Gaxotte V, de Groote P, Lamblin N, Devos P et al (2009) Cardiac magnetic resonance imaging in systemic sclerosis: a cross-sectional observational study of 52 patients. Ann Rheum Dis 68:1878–1884CrossRefPubMed Hachulla AL, Launay D, Gaxotte V, de Groote P, Lamblin N, Devos P et al (2009) Cardiac magnetic resonance imaging in systemic sclerosis: a cross-sectional observational study of 52 patients. Ann Rheum Dis 68:1878–1884CrossRefPubMed
29.
go back to reference Morelli S, Piccirillo G, Fimognari F et al (1996) Twenty-four hour heart period variability in systemic sclerosis. J Rheumatol 23:643–645PubMed Morelli S, Piccirillo G, Fimognari F et al (1996) Twenty-four hour heart period variability in systemic sclerosis. J Rheumatol 23:643–645PubMed
Metadata
Title
Cardiac mechanics and heart rate variability in patients with systemic sclerosis: the association that we should not miss
Authors
Maja Zlatanovic
Marijana Tadic
Vera Celic
Branislava Ivanovic
Ana Stevanovic
Nemanja Damjanov
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Rheumatology International / Issue 1/2017
Print ISSN: 0172-8172
Electronic ISSN: 1437-160X
DOI
https://doi.org/10.1007/s00296-016-3618-9

Other articles of this Issue 1/2017

Rheumatology International 1/2017 Go to the issue

Original Article - Observational Research

Lipid profile among girls with systemic lupus erythematosus