Abstract
This study aimed to assess coronary microvascular dysfunction (CMD) differences in hypertrophic cardiomyopathy (HCM) patients using cardiac magnetic resonance (CMR) first-pass perfusion and late gadolinium enhancement imaging. Forty-seven patients with HCM and twenty-one healthy volunteers underwent CMR at rest. Imaging protocols included short axis cine, first-pass myocardial perfusion, and late gadolinium enhancement (LGE). Left ventricular end-diastolic wall thickness (EDTH), LGE, time to peak (Tpeak), maximal up-slope (Slopemax), and peak signal intensity (SIpeak) were assessed for each myocardial segment. The HCM myocardial segments were grouped by the degree of LGE and hypertrophy. Tpeak, SIpeak, Slopemax and EDTH in multiple groups were assessed and compared by ANOVA test/Kruskal–Wallis test. The Spearman correlation test was used to determine the relationships between EDTH, LGE and perfusion parameters (Tpeak, Slopemax and SIpeak). Compared to control group segments, Tpeak increased while Slopemax and SIpeak decreased in non-LGE/non-hypertrophic segments and LGE/hypertrophic segments in the HCM group, while Tpeak increased more significantly in LGE/hypertrophic segments (all p < 0.05). Tpeak statistically increased with increasing degrees of myocardial LGE (p < 0.01). Differences in Tpeak, SIpeak and EDTH were observed between segments with and without hypertrophy (p < 0.05). EDTH and LGE were positively correlated with Tpeak (r = 0.279, p = 0.031 and r = 0.237, p < 0.001). 3.0 T magnetic resonance myocardial perfusion imaging identifies abnormal perfusion in non-LGE and non-hypertrophic segments of HCM patients, and it may be helpful in the early diagnosis of coronary microvascular dysfunction in HCM. This abnormal perfusion is associated with the severity of myocardial fibrosis and the degree of hypertrophy.
Similar content being viewed by others
References
Maron BJ (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287(10):1308–1320
Elliott P, McKenna WJ (2004) Hypertrophic cardiomyopathy. Lancet 363(9424):1881–1891
Marian AJ (2003) On predictors of sudden cardiac death in hypertrophic cardiomyopathy. J Am Coll Cardiol 41(6):994–996
Decker JA, Rossano JW, Smith EO, Cannon B, Clunie SK, Gates C, Jefferies JL, Kim JJ, Price JF, Dreyer WJ et al (2009) Risk factors and mode of death in isolated hypertrophic cardiomyopathy in children. J Am Coll Cardiol 54(3):250–254
Chiribiri A, Conte MR, Bonamini R, Gaita F, Nagel E (2011) Late gadolinium enhancement and sudden cardiac death in hypertrophic cardiomyopathy. J Am Coll Cardiol, 57(12):1402 (author reply 1402–1403)
Petersen SE, Jerosch-Herold M, Hudsmith LE, Robson MD, Francis JM, Doll HA, Selvanayagam JB, Neubauer S, Watkins H (2007) Evidence for microvascular dysfunction in hypertrophic cardiomyopathy: new insights from multiparametric magnetic resonance imaging. Circulation 115(18):2418–2425
Uren NG, Camici PG, Melin JA, Bol A, de Bruyne B, Radvan J, Olivotto I, Rosen SD, Impallomeni M, Wijns W (1995) Effect of aging on myocardial perfusion reserve. J Nucl Med 36(11):2032–2036
Cortigiani L, Rigo F, Gherardi S, Galderisi M, Sicari R, Picano E (2008) Prognostic implications of coronary flow reserve on left anterior descending coronary artery in hypertrophic cardiomyopathy. Am J Cardiol 102(12):1718–1723
Porter TR, Xie F (2010) Myocardial perfusion imaging with contrast ultrasound. JACC Cardiovascular imaging 3(2):176–187
Li X, He S, Zhang YS, Chen Y, He JC (2016) Resting Myocardial contrast echocardiography for the evaluation of coronary microcirculation dysfunction in patients with early coronary artery disease. Clin Cardiol 39(8):453–458
Barletta G, Del Bene MR (2015) Myocardial perfusion echocardiography and coronary microvascular dysfunction. World J Cardiol 7(12):861–874
Schindler TH, Schelbert HR, Quercioli A, Dilsizian V (2010) Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health. JACC Cardiovascular imaging 3(6):623–640
Mohy-Ud-Din H, Lodge MA, Rahmim A (2015) Quantitative myocardial perfusion PET parametric imaging at the voxel-level. Phys Med Biol 60(15):6013–6037
Zhang YD, Li M, Qi L, Wu CJ, Wang X (2015) Hypertrophic cardiomyopathy: cardiac structural and microvascular abnormalities as evaluated with multi-parametric MRI. Eur J Radiol 84(8):1480–1486
Huang L, Han R, Ai T, Sun Z, Bai Y, Cao Z, Morelli JN, Xia L (2013) Assessment of coronary microvascular dysfunction in hypertrophic cardiomyopathy: first-pass myocardial perfusion cardiovascular magnetic resonance imaging at 1.5 T. Clin Radiol 68(7):676–682
Xu HY, Yang ZG, Sun JY, Wen LY, Zhang G, Zhang S, Guo YK (2014) The regional myocardial microvascular dysfunction differences in hypertrophic cardiomyopathy patients with or without left ventricular outflow tract obstruction: assessment with first-pass perfusion imaging using 3.0-T cardiac magnetic resonance. Eur J Radiol 83(4):665–672
Chiribiri A, Leuzzi S, Conte MR, Bongioanni S, Bratis K, Olivotti L, De Rosa C, Lardone E, Di Donna P, Villa AD et al (2015) Rest perfusion abnormalities in hypertrophic cardiomyopathy: correlation with myocardial fibrosis and risk factors for sudden cardiac death. Clin Radiol 70(5):495–501
American College of Cardiology Foundation Task Force on Expert Consensus D, Hundley WG, Bluemke DA, Finn JP, Flamm SD, Fogel MA, Friedrich MG, Ho VB, Jerosch-Herold M, Kramer CM et al (2010) ACCF/ACR/AHA/NASCI/SCMR 2010 expert consensus document on cardiovascular magnetic resonance: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol 55(23):2614–2662
Harrigan CJ, Peters DC, Gibson CM, Maron BJ, Manning WJ, Maron MS, Appelbaum E (2011) Hypertrophic cardiomyopathy: quantification of late gadolinium enhancement with contrast-enhanced cardiovascular MR imaging. Radiology 258(1):128–133
Barbosa CA, Castro CC, Avila LF, Parga Filho JR, Hattem DM, Fernandez EA (2009) Late enhancement and myocardial perfusion in hypertrophic cardiomyopathy (comparison between groups). Arq Bras Cardiol 426–433(4):418–425
Cecchi F, Olivotto I, Gistri R, Lorenzoni R, Chiriatti G, Camici PG (2003) Coronary microvascular dysfunction and prognosis in hypertrophic cardiomyopathy. N Engl J Med 349(11):1027–1035
Basso C, Thiene G, Corrado D, Buja G, Melacini P, Nava A (2000) Hypertrophic cardiomyopathy and sudden death in the young: pathologic evidence of myocardial ischemia. Hum Pathol 31(8):988–998
Moon JC, McKenna WJ, McCrohon JA, Elliott PM, Smith GC, Pennell DJ (2003) Toward clinical risk assessment in hypertrophic cardiomyopathy with gadolinium cardiovascular magnetic resonance. J Am Coll Cardiol 41(9):1561–1567
Hussain ST, Chiribiri A, Morton G, Bettencourt N, Schuster A, Paul M, Perera D, Nagel E (2016) Perfusion cardiovascular magnetic resonance and fractional flow reserve in patients with angiographic multi-vessel coronary artery disease. J Cardiovasc Magn Reson 18(1):44
Freed BH, Narang A, Bhave NM, Czobor P, Mor-Avi V, Zaran ER, Turner KM, Cavanaugh KP, Chandra S, Tanaka SM et al (2013) Prognostic value of normal regadenoson stress perfusion cardiovascular magnetic resonance. J Cardiovasc Magn Reson 15:108
Larghat A, Biglands J, Maredia N, Greenwood JP, Ball SG, Jerosch-Herold M, Radjenovic A, Plein S (2012) Endocardial and epicardial myocardial perfusion determined by semi-quantitative and quantitative myocardial perfusion magnetic resonance. Int J Cardiovasc Imaging 28(6):1499–1511
Papanastasiou G, Williams MC, Dweck MR, Alam S, Cooper A, Mirsadraee S, Newby DE, Semple SI (2016) Quantitative assessment of myocardial blood flow in coronary artery disease by cardiovascular magnetic resonance: comparison of Fermi and distributed parameter modeling against invasive methods. J Cardiovasc Magn Reson 18(1):57
Patel AR, Antkowiak PF, Nandalur KR, West AM, Salerno M, Arora V, Christopher J, Epstein FH, Kramer CM (2010) Assessment of advanced coronary artery disease: advantages of quantitative cardiac magnetic resonance perfusion analysis. J Am Coll Cardiol 56(7):561–569
Al-Saadi N, Nagel E, Gross M, Bornstedt A, Schnackenburg B, Klein C, Klimek W, Oswald H, Fleck E (2000) Noninvasive detection of myocardial ischemia from perfusion reserve based on cardiovascular magnetic resonance. Circulation 101(12):1379–1383
Sipola P, Lauerma K, Husso-Saastamoinen M, Kuikka JT, Vanninen E, Laitinen T, Manninen H, Niemi P, Peuhkurinen K, Jaaskelainen P et al (2003) First-pass MR imaging in the assessment of perfusion impairment in patients with hypertrophic cardiomyopathy and the Asp175Asn mutation of the alpha-tropomyosin gene. Radiology 226(1):129–137
Chan RH, Maron BJ, Olivotto I, Pencina MJ, Assenza GE, Haas T, Lesser JR, Gruner C, Crean AM, Rakowski H et al (2014) Prognostic value of quantitative contrast-enhanced cardiovascular magnetic resonance for the evaluation of sudden death risk in patients with hypertrophic cardiomyopathy. Circulation 130(6):484–495
Chen X, Hu H, Qian Y, Shu J (2014) Relation of late gadolinium enhancement in cardiac magnetic resonance on the diastolic volume recovery of left ventricle with hypertrophic cardiomyopathy. J Thorac Dis 6(7):988–994
O’Hanlon R, Grasso A, Roughton M, Moon JC, Clark S, Wage R, Webb J, Kulkarni M, Dawson D, Sulaibeekh L et al (2010) Prognostic significance of myocardial fibrosis in hypertrophic cardiomyopathy. J Am Coll Cardiol 56(11):867–874
Choi HM, Kim KH, Lee JM, Yoon YE, Lee SP, Park EA, Lee W, Kim YJ, Cho GY, Sohn DW et al (2015) Myocardial fibrosis progression on cardiac magnetic resonance in hypertrophic cardiomyopathy. Heart 101(11):870–876
Lu M, Zhao S, Yin G, Jiang S, Zhao T, Chen X, Tian L, Zhang Y, Wei Y, Liu Q et al (2013) T1 mapping for detection of left ventricular myocardial fibrosis in hypertrophic cardiomyopathy: a preliminary study. Eur J Radiol 82(5):e225–e231
Matoh F, Satoh H, Shiraki K, Saitoh T, Urushida T, Katoh H, Takehara Y, Sakahara H, Hayashi H (2007) Usefulness of delayed enhancement magnetic resonance imaging to differentiate dilated phase of hypertrophic cardiomyopathy and dilated cardiomyopathy. J Card Fail 13(5):372–379
Choudhury L, Mahrholdt H, Wagner A, Choi KM, Elliott MD, Klocke FJ, Bonow RO, Judd RM, Kim RJ (2002) Myocardial scarring in asymptomatic or mildly symptomatic patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 40(12):2156–2164
Mahrholdt H, Wagner A, Judd RM, Sechtem U, Kim RJ (2005) Delayed enhancement cardiovascular magnetic resonance assessment of non-ischaemic cardiomyopathies. Eur Heart J 26(15):1461–1474
Tyan CC, Armstrong S, Scholl D, Stirrat J, Blackwood K, El-Sherif O, Thompson T, Wisenberg G, Prato FS, So A et al (2013) Stress hypoperfusion and tissue injury in hypertrophic cardiomyopathy: spatial characterization using high-resolution 3-Tesla magnetic resonance imaging. Circ Cardiovasc Imaging 6(2):229–238
Ismail TF, Hsu LY, Greve AM, Goncalves C, Jabbour A, Gulati A, Hewins B, Mistry N, Wage R, Roughton M et al (2014) Coronary microvascular ischemia in hypertrophic cardiomyopathy: a pixel-wise quantitative cardiovascular magnetic resonance perfusion study. J Cardiovasc Magn Reson 16:49
Gupta V, Kirisli HA, Hendriks EA, van der Geest RJ, van de Giessen M, Niessen W, Reiber JH, Lelieveldt BP (2012) Cardiac MR perfusion image processing techniques: a survey. Med Image Anal 16(4):767–785
Jerosch-Herold M (2010) Quantification of myocardial perfusion by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 12:57
Nagel E, Klein C, Paetsch I, Hettwer S, Schnackenburg B, Wegscheider K, Fleck E (2003) Magnetic resonance perfusion measurements for the noninvasive detection of coronary artery disease. Circulation 108(4):432–437
Soler R, Rodriguez E, Monserrat L, Mendez C, Martinez C (2006) Magnetic resonance imaging of delayed enhancement in hypertrophic cardiomyopathy: relationship with left ventricular perfusion and contractile function. J Comput Assist Tomogr 30(3):412–420
Melacini P, Corbetti F, Calore C, Pescatore V, Smaniotto G, Pavei A, Bobbo F, Cacciavillani L, Iliceto S (2008) Cardiovascular magnetic resonance signs of ischemia in hypertrophic cardiomyopathy. Int J Cardiol 128(3):364–373
Aletras AH, Tilak GS, Hsu LY, Arai AE (2011) Heterogeneity of intramural function in hypertrophic cardiomyopathy: mechanistic insights from MRI late gadolinium enhancement and high-resolution displacement encoding with stimulated echoes strain maps. Circ Cardiovasc Imaging 4(4):425–434
Olivotto I, Cecchi F, Gistri R, Lorenzoni R, Chiriatti G, Girolami F, Torricelli F, Camici PG (2006) Relevance of coronary microvascular flow impairment to long-term remodeling and systolic dysfunction in hypertrophic cardiomyopathy. J Am Coll Cardiol 47(5):1043–1048
Krams R, Kofflard MJ, Duncker DJ, Von Birgelen C, Carlier S, Kliffen M, ten Cate FJ, Serruys PW (1998) Decreased coronary flow reserve in hypertrophic cardiomyopathy is related to remodeling of the coronary microcirculation. Circulation 97(3):230–233
Villa AD, Sammut E, Zarinabad N, Carr-White G, Lee J, Bettencourt N, Razavi R, Nagel E, Chiribiri A (2016) Microvascular ischemia in hypertrophic cardiomyopathy: new insights from high-resolution combined quantification of perfusion and late gadolinium enhancement. J Cardiovasc Magn Reson 18:4
Jablonowski R, Fernlund E, Aletras AH, Engblom H, Heiberg E, Liuba P, Arheden H, Carlsson M (2015) Regional stress-induced ischemia in non-fibrotic hypertrophied myocardium in young HCM patients. Pediatr Cardiol 36(8):1662–1669
Mewton N, Liu CY, Croisille P, Bluemke D, Lima JA (2011) Assessment of myocardial fibrosis with cardiovascular magnetic resonance. J Am Coll Cardiol 57(8):891–903
Brouwer WP, Baars EN, Germans T, de Boer K, Beek AM, van der Velden J, van Rossum AC, Hofman MB (2014) In-vivo T1 cardiovascular magnetic resonance study of diffuse myocardial fibrosis in hypertrophic cardiomyopathy. J Cardiovasc Magn Reson 16:28
Hussain T, Dragulescu A, Benson L, Yoo SJ, Meng H, Windram J, Wong D, Greiser A, Friedberg M, Mertens L et al (2015) Quantification and significance of diffuse myocardial fibrosis and diastolic dysfunction in childhood hypertrophic cardiomyopathy. Pediatr Cardiol 36(5):970–978
Funding
The funding was provided by National Natural Science Foundation of China (81660284) and Major project of Natural Science Foundation of Jiangxi Province (20161ACB20013).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared no potential conflicts of interest with respect to the research and publication of this article.
Rights and permissions
About this article
Cite this article
Yin, L., Xu, Hy., Zheng, Ss. et al. 3.0 T magnetic resonance myocardial perfusion imaging for semi-quantitative evaluation of coronary microvascular dysfunction in hypertrophic cardiomyopathy. Int J Cardiovasc Imaging 33, 1949–1959 (2017). https://doi.org/10.1007/s10554-017-1189-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10554-017-1189-9