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Published in: Lung 4/2014

01-08-2014

Diagnostic Value of Strain Echocardiography, Galectin-3, and Tenascin-C Levels for the Identification of Patients with Pulmonary and Cardiac Sarcoidosis

Authors: Seref Kul, Hatice Kutbay Ozcelik, Huseyin Uyarel, Gultekin Karakus, Tolga Sinan Guvenc, Murat Yalcınsoy, Emin Asoglu, Ahu Sarbay Kemik, Abdurrahman Tasal, Sinem Gungor, Ercan Karaarslan, Levent Kart, Omer Goktekin

Published in: Lung | Issue 4/2014

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Abstract

Background

Cardiac involvement in sarcoidosis has been associated with poor prognosis. We evaluated myocardial contractility quantitatively in a cohort of pulmonary sarcoidosis (PS) patients with and without cardiac involvement. We also studied markers of fibrosis (tenascin-C [Tn-C] and galectin-3 [Gl-3]) as diagnostic tools for PS and cardiac sarcoidosis (CS).

Methods

Forty ambulatory patients with PS of grades 1–2 and 26 healthy subjects were prospectively enrolled. All patients with PS underwent cardiac magnetic resonance (CMR) to explore the presence of CS. The study population was divided into three groups: controls (n = 26), non-CS patients (n = 34), and CS patients (n = 6). Speckle-tracking strain echocardiography (STE) was performed on all patients, and Gl-3 and Tn-C values were measured in all patients and controls.

Results

PS patients had higher levels of Gl-3 and Tn-C than did controls, and the STE parameters of PS patients, including global longitudinal strain (GLS) and global circumferential strain (GCS), were lower than those of controls (p < 0.001 for all comparisons). GLS values were lower in CS patients than in the other groups (p = 0.05).

Conclusions

PS patients demonstrate reduced cardiac contractility, independent of CMR-proven structural cardiac lesions, while patients with structural lesions have a more pronounced drop in strain parameters. Tn-C and Gl-3 are promising markers for the diagnosis of PS, but they are not specific for cardiac involvement.
Literature
1.
go back to reference Kim JS, Judson MA, Donnino R, Gold M, Cooper LT Jr, Prystowsky EN, Prystowsky S (2009) Cardiac sarcoidosis. Am Heart J 157(1):9–21CrossRefPubMed Kim JS, Judson MA, Donnino R, Gold M, Cooper LT Jr, Prystowsky EN, Prystowsky S (2009) Cardiac sarcoidosis. Am Heart J 157(1):9–21CrossRefPubMed
3.
go back to reference Iwai K, Tachibana T, Takemura T (1993) Pathological studies on sarcoidosis autopsy. I. Epidemiological features of 320 cases in Japan. Acta Pathol Jpn 43:372–376PubMed Iwai K, Tachibana T, Takemura T (1993) Pathological studies on sarcoidosis autopsy. I. Epidemiological features of 320 cases in Japan. Acta Pathol Jpn 43:372–376PubMed
5.
go back to reference Shimoni S, Gendelman G, Ayzenberg O, Smirin N, Lysyansky P, Edri O, Deutsch L, Caspi A, Friedman Z (2011) Differential effects of coronary artery stenosis on myocardial function: the value of myocardial strain analysis for the detection of coronary artery disease. J Am Soc Echocardiogr 24:748–757CrossRefPubMed Shimoni S, Gendelman G, Ayzenberg O, Smirin N, Lysyansky P, Edri O, Deutsch L, Caspi A, Friedman Z (2011) Differential effects of coronary artery stenosis on myocardial function: the value of myocardial strain analysis for the detection of coronary artery disease. J Am Soc Echocardiogr 24:748–757CrossRefPubMed
6.
go back to reference Petersen JW, Nazir TF, Lee L, Garvan CS, Karimi A (2013) Speckle tracking echocardiography-determined measures of global and regional left ventricular function correlate with functional capacity in patients with and without preserved ejection fraction. Cardiovasc Ultrasound 11:20. doi:10.1186/1476-7120-11-20 PubMedCentralCrossRefPubMed Petersen JW, Nazir TF, Lee L, Garvan CS, Karimi A (2013) Speckle tracking echocardiography-determined measures of global and regional left ventricular function correlate with functional capacity in patients with and without preserved ejection fraction. Cardiovasc Ultrasound 11:20. doi:10.​1186/​1476-7120-11-20 PubMedCentralCrossRefPubMed
7.
go back to reference Galderisi M, Esposito R, Schiano-Lomoriello V, Santoro A, Ippolito R, Schiattarella P, Strazzullo P, de Simone G (2012) Correlates of global area strain in native hypertensive patients: a three-dimensional speckle-tracking echocardiography study. Eur Heart J Cardiovasc Imaging 13(9):730–738CrossRefPubMed Galderisi M, Esposito R, Schiano-Lomoriello V, Santoro A, Ippolito R, Schiattarella P, Strazzullo P, de Simone G (2012) Correlates of global area strain in native hypertensive patients: a three-dimensional speckle-tracking echocardiography study. Eur Heart J Cardiovasc Imaging 13(9):730–738CrossRefPubMed
8.
go back to reference American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias (2002) This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med 165:277–304CrossRef American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias (2002) This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med 165:277–304CrossRef
9.
go back to reference Hunninghake GW, Costabel U, Ando M, Baughman R, Cordier JF, du Bois R, Eklund A, Kitaichi M, Lynch J, Rizzato G, Rose C, Selroos O, Semenzato G, Sharma OP (1999) ATS/ERS/WASOG statement on sarcoidosis. American Thoracic Society/European Respiratory Society/World Association of Sarcoidosis and other Granulomatous Disorders. Sarcoidosis Vasc Diffuse Lung Dis 16:149–173PubMed Hunninghake GW, Costabel U, Ando M, Baughman R, Cordier JF, du Bois R, Eklund A, Kitaichi M, Lynch J, Rizzato G, Rose C, Selroos O, Semenzato G, Sharma OP (1999) ATS/ERS/WASOG statement on sarcoidosis. American Thoracic Society/European Respiratory Society/World Association of Sarcoidosis and other Granulomatous Disorders. Sarcoidosis Vasc Diffuse Lung Dis 16:149–173PubMed
10.
go back to reference Prasse A, Katic C, Germann M, Buchwald A, Zissel G, Müller-Quernheim J (2008) Phenotyping sarcoidosis from a pulmonary perspective. Am J Respir Crit Care Med 177(3):330–336CrossRefPubMed Prasse A, Katic C, Germann M, Buchwald A, Zissel G, Müller-Quernheim J (2008) Phenotyping sarcoidosis from a pulmonary perspective. Am J Respir Crit Care Med 177(3):330–336CrossRefPubMed
11.
go back to reference Soejima K, Yada H (2009) The work-up and management of patients with apparent or subclinical cardiac sarcoidosis: with emphasis on the associated heart rhythm abnormalities. J Cardiovasc Electrophysiol 20:578CrossRefPubMed Soejima K, Yada H (2009) The work-up and management of patients with apparent or subclinical cardiac sarcoidosis: with emphasis on the associated heart rhythm abnormalities. J Cardiovasc Electrophysiol 20:578CrossRefPubMed
12.
go back to reference Cerqueira MD, Weissman NJ, Dilsizian V, Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS; AHA Writing Group on Myocardial Segmentation and Registration for Cardiac Imaging (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. Circulation 105:539–542CrossRef Cerqueira MD, Weissman NJ, Dilsizian V, Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS; AHA Writing Group on Myocardial Segmentation and Registration for Cardiac Imaging (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. Circulation 105:539–542CrossRef
13.
go back to reference Smedema JP, Snoep G, van Kroonenburgh MP, van Geuns RJ, Dassen WR, Gorgels AP, Crijns HJ (2005) Evaluation of the accuracy of gadolinium-enhanced cardiovascular magnetic resonance in the diagnosis of cardiac sarcoidosis. J Am Coll Cardiol 45(10):1683–1690CrossRefPubMed Smedema JP, Snoep G, van Kroonenburgh MP, van Geuns RJ, Dassen WR, Gorgels AP, Crijns HJ (2005) Evaluation of the accuracy of gadolinium-enhanced cardiovascular magnetic resonance in the diagnosis of cardiac sarcoidosis. J Am Coll Cardiol 45(10):1683–1690CrossRefPubMed
14.
go back to reference Vignaux O, Dhote R, Duboc D, Blanche P, Dusser D, Weber S, Legmann P (2002) Clinical significance of myocardial magnetic resonance abnormalities in patients with sarcoidosis: a 1-year follow-up study. Chest 122:1895–1901CrossRefPubMed Vignaux O, Dhote R, Duboc D, Blanche P, Dusser D, Weber S, Legmann P (2002) Clinical significance of myocardial magnetic resonance abnormalities in patients with sarcoidosis: a 1-year follow-up study. Chest 122:1895–1901CrossRefPubMed
15.
go back to reference Hunninghake GW, Garrett KC, Richerson HB, Fantone JC, Ward PA, Rennard SI, Bitterman PB, Crystal RG (1984) Pathogenesis of the granulomatous lung diseases. Am Rev Respir Dis 130(3):476–496PubMed Hunninghake GW, Garrett KC, Richerson HB, Fantone JC, Ward PA, Rennard SI, Bitterman PB, Crystal RG (1984) Pathogenesis of the granulomatous lung diseases. Am Rev Respir Dis 130(3):476–496PubMed
16.
go back to reference Lok DJ, Van Der Meer P, de la Porte PW, Lipsic E, Van Wijngaarden J, Hillege HL, van Veldhuisen DJ (2010) Prognostic value of galectin-3, a novel marker of fibrosis, in patients with chronic heart failure: data from the DEAL-HF study. Clin Res Cardiol 99(5):323–328PubMedCentralCrossRefPubMed Lok DJ, Van Der Meer P, de la Porte PW, Lipsic E, Van Wijngaarden J, Hillege HL, van Veldhuisen DJ (2010) Prognostic value of galectin-3, a novel marker of fibrosis, in patients with chronic heart failure: data from the DEAL-HF study. Clin Res Cardiol 99(5):323–328PubMedCentralCrossRefPubMed
17.
go back to reference Cullinane AR, Yeager C, Dorward H, Carmona-Rivera C, Wu HP, Moss J, O’Brien KJ, Nathan SD, Meyer KC, Rosas IO, Helip-Wooley A, Huizing M, Gahl WA, Gochuico BR (2014) Dysregulation of galectin-3: Implications for Hermansky-Pudlak Syndrome pulmonary fibrosis. Am J Respir Cell Mol Biol 50(3):605–613PubMedCentralCrossRefPubMed Cullinane AR, Yeager C, Dorward H, Carmona-Rivera C, Wu HP, Moss J, O’Brien KJ, Nathan SD, Meyer KC, Rosas IO, Helip-Wooley A, Huizing M, Gahl WA, Gochuico BR (2014) Dysregulation of galectin-3: Implications for Hermansky-Pudlak Syndrome pulmonary fibrosis. Am J Respir Cell Mol Biol 50(3):605–613PubMedCentralCrossRefPubMed
18.
go back to reference van der Velde AR, Gullestad L, Ueland T, Aukrust P, Guo Y, Adourian A, Muntendam P, van Veldhuisen DJ, de Boer RA (2013) Prognostic value of changes in galectin-3 levels over time in patients with heart failure: data from CORONA and COACH. Circ Heart Fail 6(2):219–226CrossRefPubMed van der Velde AR, Gullestad L, Ueland T, Aukrust P, Guo Y, Adourian A, Muntendam P, van Veldhuisen DJ, de Boer RA (2013) Prognostic value of changes in galectin-3 levels over time in patients with heart failure: data from CORONA and COACH. Circ Heart Fail 6(2):219–226CrossRefPubMed
19.
go back to reference Golledge J, Clancy P, Maguire J, Lincz L, Koblar S (2011) The role of tenascin C in cardiovascular disease. Cardiovasc Res 92(1):19–28CrossRefPubMed Golledge J, Clancy P, Maguire J, Lincz L, Koblar S (2011) The role of tenascin C in cardiovascular disease. Cardiovasc Res 92(1):19–28CrossRefPubMed
20.
go back to reference Niebroj-Dobosz I (2012) Tenascin-C in human cardiac pathology. Clin Chim Acta 413(19–20):1516–1518CrossRefPubMed Niebroj-Dobosz I (2012) Tenascin-C in human cardiac pathology. Clin Chim Acta 413(19–20):1516–1518CrossRefPubMed
21.
go back to reference Fujita H, Sakamoto N, Ishimatsu Y, Kakugawa T, Nakashima S, Hara S, Hara A, Mukae H, Kohno S (2012) Elevated tenascin-C levels in bronchoalveolar lavage fluid of patients with sarcoidosis. Lung 190(5):537–543CrossRefPubMed Fujita H, Sakamoto N, Ishimatsu Y, Kakugawa T, Nakashima S, Hara S, Hara A, Mukae H, Kohno S (2012) Elevated tenascin-C levels in bronchoalveolar lavage fluid of patients with sarcoidosis. Lung 190(5):537–543CrossRefPubMed
22.
go back to reference Greulich S, Deluigi CC, Gloekler S, Wahl A, Zürn C, Kramer U, Nothnagel D, Bültel H, Schumm J, Grün S, Ong P, Wagner A, Schneider S, Nassenstein K, Gawaz M, Sechtem U, Bruder O, Mahrholdt H (2013) CMR imaging predicts death and other adverse events in suspected cardiac sarcoidosis. JACC Cardiovasc Imaging 6(4):501–511CrossRefPubMed Greulich S, Deluigi CC, Gloekler S, Wahl A, Zürn C, Kramer U, Nothnagel D, Bültel H, Schumm J, Grün S, Ong P, Wagner A, Schneider S, Nassenstein K, Gawaz M, Sechtem U, Bruder O, Mahrholdt H (2013) CMR imaging predicts death and other adverse events in suspected cardiac sarcoidosis. JACC Cardiovasc Imaging 6(4):501–511CrossRefPubMed
23.
go back to reference Mehta D, Lubitz SA, Frankel Z, Wisnivesky JP, Einstein AJ, Goldman M, Machac J, Teirstein A (2008) Cardiac involvement in patients with sarcoidosis: diagnostic and prognostic value of outpatient testing. Chest 133(6):1426–1435CrossRefPubMed Mehta D, Lubitz SA, Frankel Z, Wisnivesky JP, Einstein AJ, Goldman M, Machac J, Teirstein A (2008) Cardiac involvement in patients with sarcoidosis: diagnostic and prognostic value of outpatient testing. Chest 133(6):1426–1435CrossRefPubMed
24.
go back to reference Watanabe E, Kimura F, Nakajima T, Hiroe M, Kasai Y, Nagata M, Kawana M, Hagiwara N (2013) Late gadolinium enhancement in cardiac sarcoidosis: characteristic magnetic resonance findings and relationship with left ventricular function. J Thorac Imaging 28(1):60–66CrossRefPubMed Watanabe E, Kimura F, Nakajima T, Hiroe M, Kasai Y, Nagata M, Kawana M, Hagiwara N (2013) Late gadolinium enhancement in cardiac sarcoidosis: characteristic magnetic resonance findings and relationship with left ventricular function. J Thorac Imaging 28(1):60–66CrossRefPubMed
25.
go back to reference Suzuki T, Kanda T, Kubota S, Imai S, Murata K (1994) Holter monitoring as a noninvasive indicator of cardiac involvement in sarcoidosis. Chest 106(4):1021–1024CrossRefPubMed Suzuki T, Kanda T, Kubota S, Imai S, Murata K (1994) Holter monitoring as a noninvasive indicator of cardiac involvement in sarcoidosis. Chest 106(4):1021–1024CrossRefPubMed
26.
go back to reference Aydin Kaderli A, Gullulu S, Coskun F, Yilmaz D, Uzaslan E (2010) Impaired left ventricular systolic and diastolic functions in patients with early grade pulmonary sarcoidosis. Eur J Echocardiogr 11(10):809–813CrossRefPubMed Aydin Kaderli A, Gullulu S, Coskun F, Yilmaz D, Uzaslan E (2010) Impaired left ventricular systolic and diastolic functions in patients with early grade pulmonary sarcoidosis. Eur J Echocardiogr 11(10):809–813CrossRefPubMed
27.
go back to reference Rapti A, Kouranos V, Gialafos E, Aggeli K, Moyssakis J, Kallianos A, Kostopoulos C, Anagnostopoulou O, Sfikakis PP, Wells AU, Tzelepis GE (2013) Elevated pulmonary arterial systolic pressure in patients with sarcoidosis: prevalence and risk factors. Lung 191(1):61–67CrossRefPubMed Rapti A, Kouranos V, Gialafos E, Aggeli K, Moyssakis J, Kallianos A, Kostopoulos C, Anagnostopoulou O, Sfikakis PP, Wells AU, Tzelepis GE (2013) Elevated pulmonary arterial systolic pressure in patients with sarcoidosis: prevalence and risk factors. Lung 191(1):61–67CrossRefPubMed
28.
go back to reference Moyssakis I, Gialafos E, Tentolouris N, Floudas CS, Papaioannou TG, Kostopoulos C, Latsi P, Vaiopoulos G, Votteas V, Rapti A (2008) Impaired aortic elastic properties in patients with systemic sarcoidosis. Eur J Clin Invest 38(2):82–89CrossRefPubMed Moyssakis I, Gialafos E, Tentolouris N, Floudas CS, Papaioannou TG, Kostopoulos C, Latsi P, Vaiopoulos G, Votteas V, Rapti A (2008) Impaired aortic elastic properties in patients with systemic sarcoidosis. Eur J Clin Invest 38(2):82–89CrossRefPubMed
29.
30.
go back to reference Tsuji T, Tanaka H, Matsumoto K, Miyoshi T, Hiraishi M, Kaneko A, Ryo K, Fukuda Y, Tatsumi K, Onishi T, Kawai H, Hirata KI (2013) Capability of three-dimensional speckle tracking radial strain for identification of patients with cardiac sarcoidosis. Int J Cardiovasc Imaging 29(2):317–324CrossRefPubMed Tsuji T, Tanaka H, Matsumoto K, Miyoshi T, Hiraishi M, Kaneko A, Ryo K, Fukuda Y, Tatsumi K, Onishi T, Kawai H, Hirata KI (2013) Capability of three-dimensional speckle tracking radial strain for identification of patients with cardiac sarcoidosis. Int J Cardiovasc Imaging 29(2):317–324CrossRefPubMed
31.
go back to reference Kansal MM, Panse PM, Abe H, Caracciolo G, Wilansky S, Tajik AJ, Khandheria BK, Sengupta PP (2012) Relationship of contrast-enhanced magnetic resonance imaging-derived intramural scar distribution and speckle tracking echocardiography-derived left ventricular two-dimensional strains. Eur Heart J Cardiovasc Imaging 13(2):152–158CrossRefPubMed Kansal MM, Panse PM, Abe H, Caracciolo G, Wilansky S, Tajik AJ, Khandheria BK, Sengupta PP (2012) Relationship of contrast-enhanced magnetic resonance imaging-derived intramural scar distribution and speckle tracking echocardiography-derived left ventricular two-dimensional strains. Eur Heart J Cardiovasc Imaging 13(2):152–158CrossRefPubMed
33.
go back to reference Date T, Shinozaki T, Yamakawa M, Taniguchi I, Suda A, Hara H, Yamane T, Komukai K, Sugimoto K, Mochizuki S (2007) Elevated plasma brain natriuretic peptide level in cardiac sarcoidosis patients with preserved ejection fraction. Cardiology 107(4):277–280CrossRefPubMed Date T, Shinozaki T, Yamakawa M, Taniguchi I, Suda A, Hara H, Yamane T, Komukai K, Sugimoto K, Mochizuki S (2007) Elevated plasma brain natriuretic peptide level in cardiac sarcoidosis patients with preserved ejection fraction. Cardiology 107(4):277–280CrossRefPubMed
34.
go back to reference Magrì D, Agostoni P, Ricotta A, Pisani L, Cauti FM, Onofri A, Bruno P, Ricci A, Volpe M, Marchitti S, Mariotta S, Rubattu S (2013) NT-proatrial natriuretic peptide as a possible biomarker of cardiopulmonary involvement in sarcoidosis. Eur J Intern Med 24:278–284CrossRefPubMed Magrì D, Agostoni P, Ricotta A, Pisani L, Cauti FM, Onofri A, Bruno P, Ricci A, Volpe M, Marchitti S, Mariotta S, Rubattu S (2013) NT-proatrial natriuretic peptide as a possible biomarker of cardiopulmonary involvement in sarcoidosis. Eur J Intern Med 24:278–284CrossRefPubMed
Metadata
Title
Diagnostic Value of Strain Echocardiography, Galectin-3, and Tenascin-C Levels for the Identification of Patients with Pulmonary and Cardiac Sarcoidosis
Authors
Seref Kul
Hatice Kutbay Ozcelik
Huseyin Uyarel
Gultekin Karakus
Tolga Sinan Guvenc
Murat Yalcınsoy
Emin Asoglu
Ahu Sarbay Kemik
Abdurrahman Tasal
Sinem Gungor
Ercan Karaarslan
Levent Kart
Omer Goktekin
Publication date
01-08-2014
Publisher
Springer US
Published in
Lung / Issue 4/2014
Print ISSN: 0341-2040
Electronic ISSN: 1432-1750
DOI
https://doi.org/10.1007/s00408-014-9586-5

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