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3.0 T magnetic resonance myocardial perfusion imaging for semi-quantitative evaluation of coronary microvascular dysfunction in hypertrophic cardiomyopathy

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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.

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References

  1. Maron BJ (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287(10):1308–1320

    Article  PubMed  Google Scholar 

  2. Elliott P, McKenna WJ (2004) Hypertrophic cardiomyopathy. Lancet 363(9424):1881–1891

    Article  CAS  PubMed  Google Scholar 

  3. Marian AJ (2003) On predictors of sudden cardiac death in hypertrophic cardiomyopathy. J Am Coll Cardiol 41(6):994–996

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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)

    Article  PubMed  Google Scholar 

  6. 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

    Article  PubMed  Google Scholar 

  7. 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

    CAS  PubMed  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. Porter TR, Xie F (2010) Myocardial perfusion imaging with contrast ultrasound. JACC Cardiovascular imaging 3(2):176–187

    Article  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. Barletta G, Del Bene MR (2015) Myocardial perfusion echocardiography and coronary microvascular dysfunction. World J Cardiol 7(12):861–874

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. 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

    Article  PubMed  Google Scholar 

  32. 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

    PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Article  PubMed  Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. 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

    Article  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. Jerosch-Herold M (2010) Quantification of myocardial perfusion by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 12:57

    Article  PubMed  PubMed Central  Google Scholar 

  43. 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

    Article  PubMed  Google Scholar 

  44. 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

    Article  PubMed  Google Scholar 

  45. 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

    Article  PubMed  Google Scholar 

  46. 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

    Article  PubMed  PubMed Central  Google Scholar 

  47. 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

    Article  PubMed  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. 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

    Article  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  PubMed  Google Scholar 

  52. 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

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  PubMed  Google Scholar 

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Funding

The funding was provided by National Natural Science Foundation of China (81660284) and Major project of Natural Science Foundation of Jiangxi Province (20161ACB20013).

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Correspondence to Liang-geng Gong.

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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

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  • DOI: https://doi.org/10.1007/s10554-017-1189-9

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