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Published in: Pediatric Radiology 4/2014

01-04-2014 | Original Article

Diffuse myocardial fibrosis following tetralogy of Fallot repair: a T1 mapping cardiac magnetic resonance study

Authors: Marcelo F. Kozak, Andrew Redington, Shi-Joon Yoo, Mike Seed, Andreas Greiser, Lars Grosse-Wortmann

Published in: Pediatric Radiology | Issue 4/2014

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Abstract

Background

Adverse ventricular remodeling after tetralogy of Fallot (TOF) repair is associated with diffuse myocardial fibrosis.

Objective

The goal of this study was to measure post-contrast myocardial T1 in pediatric patients after TOF repair as surrogates of myocardial fibrosis.

Materials and methods

Children after TOF repair who underwent cardiac magnetic resonance imaging with T1 mapping using the modified look-locker inversion recovery (MOLLI) sequence were included. In addition to routine volumetric and flow data, we measured post-contrast T1 values of the basal interventricular septum, the left ventricular (LV) lateral wall, and the inferior and anterior walls of the right ventricle (RV). Results were compared to data from age-matched healthy controls.

Results

The scans of 18 children who had undergone TOF repair and 12 healthy children were included. Post-contrast T1 values of the left ventricular lateral wall (443 ± 54 vs. 510 ± 77 ms, P = 0.0168) and of the right ventricular anterior wall (333 ± 62 vs. 392 ± 72 ms, P = 0.0423) were significantly shorter in children with TOF repair than in controls, suggesting a higher degree of fibrosis. In children with TOF repair, but not in controls, post-contrast T1 values were shorter in the right ventricle than the left ventricle and shorter in the anterior wall of the right ventricle than in the inferior segments. In the TOF group, post-contrast T1 values of the RV anterior wall correlated with the RV end-systolic volume indexed to body surface area (r = 0.54; r2 = 0.30; P = 0.0238).

Conclusion

In children who underwent tetralogy of Fallot repair the myocardium of both ventricles appears to bear an abnormally high fibrosis burden.
Literature
1.
go back to reference Broberg CS, Chugh SS, Conklin C et al (2010) Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging 3:727–734PubMedCentralPubMedCrossRef Broberg CS, Chugh SS, Conklin C et al (2010) Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging 3:727–734PubMedCentralPubMedCrossRef
2.
go back to reference Conrad CH, Brooks WW, Hayes JA et al (1995) Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation 91:161–170PubMedCrossRef Conrad CH, Brooks WW, Hayes JA et al (1995) Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation 91:161–170PubMedCrossRef
3.
go back to reference Ellims AH, Iles LM, Ling LH et al (2012) Diffuse myocardial fibrosis in hypertrophic cardiomyopathy can be identified by cardiovascular magnetic resonance, and is associated with left ventricular diastolic dysfunction. J Cardiovasc Magn Reson 14:76PubMedCentralPubMedCrossRef Ellims AH, Iles LM, Ling LH et al (2012) Diffuse myocardial fibrosis in hypertrophic cardiomyopathy can be identified by cardiovascular magnetic resonance, and is associated with left ventricular diastolic dysfunction. J Cardiovasc Magn Reson 14:76PubMedCentralPubMedCrossRef
4.
go back to reference Ng AC, Auger D, Delgado V et al (2012) Association between diffuse myocardial fibrosis by cardiac magnetic resonance contrast-enhanced T(1) mapping and subclinical myocardial dysfunction in diabetic patients: a pilot study. Circ Cardiovasc Imaging 5:51–59PubMedCrossRef Ng AC, Auger D, Delgado V et al (2012) Association between diffuse myocardial fibrosis by cardiac magnetic resonance contrast-enhanced T(1) mapping and subclinical myocardial dysfunction in diabetic patients: a pilot study. Circ Cardiovasc Imaging 5:51–59PubMedCrossRef
5.
go back to reference Schwarz F, Mall G, Zebe H et al (1983) Quantitative morphologic findings of the myocardium in idiopathic dilated cardiomyopathy. Am J Cardiol 51:501–506PubMedCrossRef Schwarz F, Mall G, Zebe H et al (1983) Quantitative morphologic findings of the myocardium in idiopathic dilated cardiomyopathy. Am J Cardiol 51:501–506PubMedCrossRef
6.
go back to reference Wong TC, Piehler K, Meier CG et al (2012) Association between extracellular matrix expansion quantified by cardiovascular magnetic resonance and short-term mortality. Circulation 126:1206–1216PubMedCentralPubMedCrossRef Wong TC, Piehler K, Meier CG et al (2012) Association between extracellular matrix expansion quantified by cardiovascular magnetic resonance and short-term mortality. Circulation 126:1206–1216PubMedCentralPubMedCrossRef
7.
go back to reference Babu-Narayan SV, Kilner PJ, Li W et al (2006) Ventricular fibrosis suggested by cardiovascular magnetic resonance in adults with repaired tetralogy of Fallot and its relationship to adverse markers of clinical outcome. Circulation 113:405–413PubMedCrossRef Babu-Narayan SV, Kilner PJ, Li W et al (2006) Ventricular fibrosis suggested by cardiovascular magnetic resonance in adults with repaired tetralogy of Fallot and its relationship to adverse markers of clinical outcome. Circulation 113:405–413PubMedCrossRef
8.
go back to reference Chowdhury UK, Sathia S, Ray R et al (2006) Histopathology of the right ventricular outflow tract and its relationship to clinical outcomes and arrhythmias in patients with tetralogy of Fallot. J Thorac Cardiovasc Surg 132:270–277PubMedCrossRef Chowdhury UK, Sathia S, Ray R et al (2006) Histopathology of the right ventricular outflow tract and its relationship to clinical outcomes and arrhythmias in patients with tetralogy of Fallot. J Thorac Cardiovasc Surg 132:270–277PubMedCrossRef
9.
10.
go back to reference Flacke SJ, Fischer SE, Lorenz CH (2001) Measurement of the gadopentetate dimeglumine partition coefficient in human myocardium in vivo: normal distribution and elevation in acute and chronic infarction. Radiology 218:703–710PubMedCrossRef Flacke SJ, Fischer SE, Lorenz CH (2001) Measurement of the gadopentetate dimeglumine partition coefficient in human myocardium in vivo: normal distribution and elevation in acute and chronic infarction. Radiology 218:703–710PubMedCrossRef
11.
go back to reference Flett AS, Hayward MP, Ashworth MT et al (2010) Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation 122:138–144PubMedCrossRef Flett AS, Hayward MP, Ashworth MT et al (2010) Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation 122:138–144PubMedCrossRef
12.
go back to reference Iles L, Pfluger H, Phrommintikul A et al (2008) Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol 52:1574–1580PubMedCrossRef Iles L, Pfluger H, Phrommintikul A et al (2008) Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol 52:1574–1580PubMedCrossRef
13.
go back to reference Kellman P, Wilson JR, Xue H et al (2012) Extracellular volume fraction mapping in the myocardium, part 2: initial clinical experience. J Cardiovasc Magn Reson 14:64PubMedCentralPubMedCrossRef Kellman P, Wilson JR, Xue H et al (2012) Extracellular volume fraction mapping in the myocardium, part 2: initial clinical experience. J Cardiovasc Magn Reson 14:64PubMedCentralPubMedCrossRef
14.
go back to reference Messroghli DR, Nordmeyer S, Dietrich T et al (2011) Assessment of diffuse myocardial fibrosis in rats using small-animal look-locker inversion recovery T1 mapping. Circ Cardiovasc Imaging 4:636–640PubMedCrossRef Messroghli DR, Nordmeyer S, Dietrich T et al (2011) Assessment of diffuse myocardial fibrosis in rats using small-animal look-locker inversion recovery T1 mapping. Circ Cardiovasc Imaging 4:636–640PubMedCrossRef
15.
go back to reference Plymen CM, Sado DM, Taylor AM et al (2013) Diffuse myocardial fibrosis in the systemic right ventricle of patients late after Mustard or Senning surgery: an equilibrium contrast cardiovascular magnetic resonance study. Eur Heart J Cardiovasc Imaging 14:963–968PubMedCrossRef Plymen CM, Sado DM, Taylor AM et al (2013) Diffuse myocardial fibrosis in the systemic right ventricle of patients late after Mustard or Senning surgery: an equilibrium contrast cardiovascular magnetic resonance study. Eur Heart J Cardiovasc Imaging 14:963–968PubMedCrossRef
16.
go back to reference Puntmann VO, Voigt T, Chen Z et al (2013) Native T1 mapping in differentiation of normal myocardium from diffuse disease in hypertrophic and dilated cardiomyopathy. JACC Cardiovasc Imaging 6:475–484PubMedCrossRef Puntmann VO, Voigt T, Chen Z et al (2013) Native T1 mapping in differentiation of normal myocardium from diffuse disease in hypertrophic and dilated cardiomyopathy. JACC Cardiovasc Imaging 6:475–484PubMedCrossRef
17.
18.
go back to reference Sparrow P, Messroghli DR, Reid S et al (2006) Myocardial T1 mapping for detection of left ventricular myocardial fibrosis in chronic aortic regurgitation: pilot study. AJR Am J Roentgenol 187:W630–W635PubMedCrossRef Sparrow P, Messroghli DR, Reid S et al (2006) Myocardial T1 mapping for detection of left ventricular myocardial fibrosis in chronic aortic regurgitation: pilot study. AJR Am J Roentgenol 187:W630–W635PubMedCrossRef
19.
go back to reference Ugander M, Oki AJ, Hsu LY et al (2012) Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J 33:1268–1278PubMedCentralPubMedCrossRef Ugander M, Oki AJ, Hsu LY et al (2012) Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J 33:1268–1278PubMedCentralPubMedCrossRef
20.
go back to reference White SK, Sado DM, Flett AS et al (2012) Characterizing the myocardial interstitial space: the clinical relevance of non-invasive imaging. Heart 98:773–779PubMedCrossRef White SK, Sado DM, Flett AS et al (2012) Characterizing the myocardial interstitial space: the clinical relevance of non-invasive imaging. Heart 98:773–779PubMedCrossRef
21.
go back to reference Marcus FI, McKenna WJ, Sherril D et al (2010) Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia (ARVC/D). Circulation 121:1533–1541PubMedCentralPubMedCrossRef Marcus FI, McKenna WJ, Sherril D et al (2010) Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia (ARVC/D). Circulation 121:1533–1541PubMedCentralPubMedCrossRef
22.
go back to reference Fernandes FP, Manlhiot C, Roche SL et al (2012) Impaired left ventricular myocardial mechanics and their relation to pulmonary regurgitation, right ventricular enlargement and exercise capacity in asymptomatic children after repair of tetralogy of Fallot. J Am Soc Echocardiogr 25:518–523CrossRef Fernandes FP, Manlhiot C, Roche SL et al (2012) Impaired left ventricular myocardial mechanics and their relation to pulmonary regurgitation, right ventricular enlargement and exercise capacity in asymptomatic children after repair of tetralogy of Fallot. J Am Soc Echocardiogr 25:518–523CrossRef
23.
go back to reference Sun AM, AlHabshan F, Cheung M et al (2011) Delayed onset of tricuspid valve flow in repaired tetralogy of Fallot: an additional mechanism of diastolic dysfunction and interventricular dyssynchrony. J Cardiovasc Magn Reson 13:43PubMedCentralPubMedCrossRef Sun AM, AlHabshan F, Cheung M et al (2011) Delayed onset of tricuspid valve flow in repaired tetralogy of Fallot: an additional mechanism of diastolic dysfunction and interventricular dyssynchrony. J Cardiovasc Magn Reson 13:43PubMedCentralPubMedCrossRef
24.
go back to reference Kim WY, Danias PG, Stuber M et al (2001) Coronary magnetic resonance angiography for the detection of coronary stenosis. N Engl J Med 345:1863–1869PubMedCrossRef Kim WY, Danias PG, Stuber M et al (2001) Coronary magnetic resonance angiography for the detection of coronary stenosis. N Engl J Med 345:1863–1869PubMedCrossRef
25.
go back to reference Messroghli DR, Radjenovic A, Kozerke S et al (2004) Modified look-locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med 52:141–146PubMedCrossRef Messroghli DR, Radjenovic A, Kozerke S et al (2004) Modified look-locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med 52:141–146PubMedCrossRef
26.
go back to reference Oosterhof T, Mulder BJM, Vliegen HW et al (2005) Corrected tetralogy of Fallot: delayed enhancement in right ventricular outflow tract. Radiology 237:868–871PubMedCrossRef Oosterhof T, Mulder BJM, Vliegen HW et al (2005) Corrected tetralogy of Fallot: delayed enhancement in right ventricular outflow tract. Radiology 237:868–871PubMedCrossRef
27.
go back to reference Farah MC, Castro CRP, Moreira VM et al (2010) The impact of preexisting myocardial remodeling on ventricular function early after tetralogy of Fallot repair. J Am Soc Echocardiogr 23:912–918PubMedCrossRef Farah MC, Castro CRP, Moreira VM et al (2010) The impact of preexisting myocardial remodeling on ventricular function early after tetralogy of Fallot repair. J Am Soc Echocardiogr 23:912–918PubMedCrossRef
28.
go back to reference Wald RM, Haber I, Wald R et al (2009) Effects of regional dysfunction and late gadolinium enhancement on global right ventricular function and exercise capacity in patients with repaired tetralogy of Fallot. Circulation 119:1370–1377PubMedCentralPubMedCrossRef Wald RM, Haber I, Wald R et al (2009) Effects of regional dysfunction and late gadolinium enhancement on global right ventricular function and exercise capacity in patients with repaired tetralogy of Fallot. Circulation 119:1370–1377PubMedCentralPubMedCrossRef
29.
go back to reference Schwartz SM, Gordon D, Mosca RS et al (1996) Collagen content in normal, pressure, and pressure-volume overloaded developing human hearts. Am J Cardiol 77:734–738PubMedCrossRef Schwartz SM, Gordon D, Mosca RS et al (1996) Collagen content in normal, pressure, and pressure-volume overloaded developing human hearts. Am J Cardiol 77:734–738PubMedCrossRef
30.
go back to reference Farah MC, Castro CRP, Moreira VM et al (2009) The myocardium in tetralogy of Fallot: a histological and morphometric study. Arq Bras Cardiol 92:160–171PubMedCrossRef Farah MC, Castro CRP, Moreira VM et al (2009) The myocardium in tetralogy of Fallot: a histological and morphometric study. Arq Bras Cardiol 92:160–171PubMedCrossRef
31.
go back to reference Fontana M, White SK, Banypersad SM et al (2012) Comparison of T1 mapping techniques for ECV quantification. Histological validation and reproducibility of ShMOLLI versus multibreath-hold T1 quantification equilibrium contrast CMR. J Cardiovasc Magn Reson 14:88PubMedCentralPubMedCrossRef Fontana M, White SK, Banypersad SM et al (2012) Comparison of T1 mapping techniques for ECV quantification. Histological validation and reproducibility of ShMOLLI versus multibreath-hold T1 quantification equilibrium contrast CMR. J Cardiovasc Magn Reson 14:88PubMedCentralPubMedCrossRef
32.
go back to reference Wang ZF, Wang NP, Harmouche S et al (2013) Postconditioning promotes the cardiac repair through balancing collagen degradation and synthesis after myocardial infarction in rats. Basic Res Cardiol 108:318PubMedCrossRef Wang ZF, Wang NP, Harmouche S et al (2013) Postconditioning promotes the cardiac repair through balancing collagen degradation and synthesis after myocardial infarction in rats. Basic Res Cardiol 108:318PubMedCrossRef
33.
go back to reference Dass S, Suttie JJ, Piechnik SK et al (2012) Myocardial tissue characterization using magnetic resonance noncontrast T1 mapping in hypertrophic and dilated cardiomyopathy. Circ Cardiovasc Imaging 5:726–733PubMedCrossRef Dass S, Suttie JJ, Piechnik SK et al (2012) Myocardial tissue characterization using magnetic resonance noncontrast T1 mapping in hypertrophic and dilated cardiomyopathy. Circ Cardiovasc Imaging 5:726–733PubMedCrossRef
34.
go back to reference Karamitsos TD, Piechnik SK, Banypersad SM et al (2013) Noncontrast T1 mapping for the diagnosis of cardiac amyloidosis. JACC Cardiovasc Imaging 6:488–497PubMedCrossRef Karamitsos TD, Piechnik SK, Banypersad SM et al (2013) Noncontrast T1 mapping for the diagnosis of cardiac amyloidosis. JACC Cardiovasc Imaging 6:488–497PubMedCrossRef
35.
go back to reference Puntmann VO, D’Cruz D, Smith Z et al (2013) Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 6:295–301PubMedCrossRef Puntmann VO, D’Cruz D, Smith Z et al (2013) Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 6:295–301PubMedCrossRef
36.
go back to reference Reddy S, Osorio JC, Duque AM et al (2006) Failure of right ventricular adaptation in children with tetralogy of Fallot. Circulation 114:I37–I42PubMedCrossRef Reddy S, Osorio JC, Duque AM et al (2006) Failure of right ventricular adaptation in children with tetralogy of Fallot. Circulation 114:I37–I42PubMedCrossRef
37.
go back to reference Jeewa A, Manickaraj AK, Mertens L et al (2012) Genetic determinants of right-ventricular remodeling after tetralogy of Fallot repair. Pediatr Res 72:407–413PubMedCrossRef Jeewa A, Manickaraj AK, Mertens L et al (2012) Genetic determinants of right-ventricular remodeling after tetralogy of Fallot repair. Pediatr Res 72:407–413PubMedCrossRef
38.
go back to reference Friedberg MK, Fernandes FP, Roche SL et al (2012) Impaired right and left ventricular diastolic myocardial mechanics and filling in asymptomatic children and adolescents after repair of tetralogy of fallot. Eur Heart J Cardiovasc Imaging 13:905–913PubMedCrossRef Friedberg MK, Fernandes FP, Roche SL et al (2012) Impaired right and left ventricular diastolic myocardial mechanics and filling in asymptomatic children and adolescents after repair of tetralogy of fallot. Eur Heart J Cardiovasc Imaging 13:905–913PubMedCrossRef
39.
go back to reference Ortega M, Triedman JK, Geva T et al (2011) Relation of left ventricular dyssynchrony measured by cardiac magnetic resonance tissue tracking in repaired tetralogy of Fallot to ventricular tachycardia and death. Am J Cardiol 107:1535–1540PubMedCrossRef Ortega M, Triedman JK, Geva T et al (2011) Relation of left ventricular dyssynchrony measured by cardiac magnetic resonance tissue tracking in repaired tetralogy of Fallot to ventricular tachycardia and death. Am J Cardiol 107:1535–1540PubMedCrossRef
40.
go back to reference Tzemos N, Harris L, Carasso S et al (2009) Adverse left ventricular mechanics in adults with repaired tetralogy of fallot. Am J Cardiol 103:420–425PubMedCrossRef Tzemos N, Harris L, Carasso S et al (2009) Adverse left ventricular mechanics in adults with repaired tetralogy of fallot. Am J Cardiol 103:420–425PubMedCrossRef
41.
go back to reference Redington AN (2006) Physiopathology of right ventricular failure. Semin Thorac Cardiovasc Surg Pediatr Card Surg Ann 2006:3–10CrossRef Redington AN (2006) Physiopathology of right ventricular failure. Semin Thorac Cardiovasc Surg Pediatr Card Surg Ann 2006:3–10CrossRef
42.
go back to reference Apitz C, Honjo O, Humpl T et al (2012) Biventricular structural and functional responses to aortic constriction in a rabbit model of chronic right ventricular pressure overload. J Thorac Cardiovasc Surg 144:1494–1501PubMedCrossRef Apitz C, Honjo O, Humpl T et al (2012) Biventricular structural and functional responses to aortic constriction in a rabbit model of chronic right ventricular pressure overload. J Thorac Cardiovasc Surg 144:1494–1501PubMedCrossRef
43.
go back to reference Anderson RH, Ho SH, Redmann K et al (2005) The anatomical arrangement of the myocardial cells making up the ventricular mass. Eur J Cardiothorac Surg 28:517–525PubMedCrossRef Anderson RH, Ho SH, Redmann K et al (2005) The anatomical arrangement of the myocardial cells making up the ventricular mass. Eur J Cardiothorac Surg 28:517–525PubMedCrossRef
44.
go back to reference Ho SH, Jackson M, Kilpatrick L et al (1996) Fibrous matrix of ventricular myocardium in tricuspid atresia compared with normal heart. Circulation 94:1642–1646PubMedCrossRef Ho SH, Jackson M, Kilpatrick L et al (1996) Fibrous matrix of ventricular myocardium in tricuspid atresia compared with normal heart. Circulation 94:1642–1646PubMedCrossRef
45.
go back to reference Kawel N, Nacif M, Zavodni A et al (2012) T1 mapping of the myocardium: intra-individual assessment of the effect of field strength, cardiac cycle and variation by myocardial region. J Cardiovasc Magn Reson 14:27PubMedCentralPubMedCrossRef Kawel N, Nacif M, Zavodni A et al (2012) T1 mapping of the myocardium: intra-individual assessment of the effect of field strength, cardiac cycle and variation by myocardial region. J Cardiovasc Magn Reson 14:27PubMedCentralPubMedCrossRef
46.
go back to reference Miller CA, Naish JH, Bishop P et al (2013) Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circulation 6:373–383PubMed Miller CA, Naish JH, Bishop P et al (2013) Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circulation 6:373–383PubMed
47.
go back to reference Park SJ, On YK, Kim JS et al (2012) Relation of fragmented QRS complex to right ventricular fibrosis detected by late gadolinium enhancement cardiac magnetic resonance in adults with repaired tetralogy of Fallot. Am J Cardiol 109:110–115PubMedCrossRef Park SJ, On YK, Kim JS et al (2012) Relation of fragmented QRS complex to right ventricular fibrosis detected by late gadolinium enhancement cardiac magnetic resonance in adults with repaired tetralogy of Fallot. Am J Cardiol 109:110–115PubMedCrossRef
Metadata
Title
Diffuse myocardial fibrosis following tetralogy of Fallot repair: a T1 mapping cardiac magnetic resonance study
Authors
Marcelo F. Kozak
Andrew Redington
Shi-Joon Yoo
Mike Seed
Andreas Greiser
Lars Grosse-Wortmann
Publication date
01-04-2014
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Radiology / Issue 4/2014
Print ISSN: 0301-0449
Electronic ISSN: 1432-1998
DOI
https://doi.org/10.1007/s00247-013-2840-9

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