Formation and Malformation of Cardiac Trabeculae: Biological Basis, Clinical Significance, and Special Yield of Magnetic Resonance Imaging in Assessment

Canadian Journal of Cardiology

Volumn 31, Issue 11, 2015, Pages 1325-1337

  Captur, Gabriella ^a,b   Syrris, Petros ^a   Obianyo, Chinwe ^a   Limongelli, Giuseppe ^c   Moon, James C ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ST BARTHOLOMEW S HOSPITAL   (United Kingdom)

^c MONALDI HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; CARDIAC IMAGING; CARDIOVASCULAR MAGNETIC RESONANCE; CLINICAL FEATURE; CONGENITAL HEART MALFORMATION; DEVELOPMENTAL BIOLOGY; HEART DEVELOPMENT; HEART TRABECULAR MUSCLE; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POPULATION; REVIEW; VENTRICULAR NONCOMPACTION; DISEASE COURSE; HEART VENTRICLE; ISOLATED NONCOMPACTION OF THE VENTRICULAR MYOCARDIUM; PATHOLOGY; PROCEDURES; REPRODUCIBILITY;

DISEASE PROGRESSION; HEART VENTRICLES; HUMANS; ISOLATED NONCOMPACTION OF THE VENTRICULAR MYOCARDIUM; MAGNETIC RESONANCE IMAGING, CINE; REPRODUCIBILITY OF RESULTS;

EID: 84945292512     PISSN: 0828282X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cjca.2015.07.003     Document Type: Review

References (106)

1. Sedmera D., Pexieder T., Hu N., Clark E.B. Developmental changes in the myocardial architecture of the chick. Anat Rec 1997, 248:421-432.
2. Tian X., Hu T., Zhang H., et al. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res 2013, 23:1075-1090.
3. Samsa L.A., Yang B., Liu J. Embryonic cardiac chamber maturation: Trabeculation, conduction, and cardiomyocyte proliferation. Am J Med Genet C Semin Med Genet 2013, 163C:157-168.
4. Iso T., Kedes L., Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 2003, 194:237-255.
5. Kokubo H., Miyagawa-Tomita S., Johnson R.L. Hesr, a mediator of the Notch signaling, functions in heart and vessel development. Trends Cardiovasc Med 2005, 15:190-194.
6. Grego-Bessa J., Luna-Zurita L., del Monte G., et al. Notch signaling is essential for ventricular chamber development. Dev Cell 2007, 12:415-429.
7. Chen H., Shi S., Acosta L., et al. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 2004, 131:2219-2231.
8. Jones F.E., Golding J.P., Gassmann M. ErbB4 signaling during breast and neural development: novel genetic models reveal unique ErbB4 activities. Cell Cycle 2003, 2:555-559.
9. Hertig C.M., Kubalak S.W., Wang Y., Chien K.R. Synergistic roles of neuregulin-1 and insulin-like growth factor-I in activation of the phosphatidylinositol 3-kinase pathway and cardiac chamber morphogenesis. J Biol Chem 1999, 274:37362-37369.
10. Gassmann M., Casagranda F., Orioli D., et al. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 1995, 378:390-394.
11. Wang H.U., Chen Z.F., Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753.
12. Catela C., Kratsios P., Hede M., Lang F., Rosenthal N. Serum and glucocorticoid-inducible kinase 1 (SGK1) is necessary for vascular remodeling during angiogenesis. Dev Dyn 2010, 239:2149-2160.
13. Kokubo H., Miyagawa-Tomita S., Nakazawa M., Saga Y., Johnson R.L. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev Biol 2005, 278:301-309.
14. Yang J., Bücker S., Jungblut B., et al. Inhibition of Notch2 by Numb/Numblike controls myocardial compaction in the heart. Cardiovasc Res 2012, 96:276-285.
15. McCright B., Lozier J., Gridley T. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 2002, 129:1075-1082.
16. Luxán G., Casanova J.C., Martínez-Poveda B., et al. Mutations in the NOTCH pathway regulator MIB1 cause left ventricular noncompaction cardiomyopathy. Nat Med 2013, 19:193-201.
17. Liu J., Bressan M., Hassel D., et al. A dual role for ErbB2 signaling in cardiac trabeculation. Development 2010, 137:3867-3875.
18. Koshiba-Takeuchi K., Mori A.D., Kaynak B.L., et al. Reptilian heart development and the molecular basis of cardiac chamber evolution. Nature 2009, 461:95-98.
19. Hagensen M.K., Abe A.S., Falk E., Wang T. Physiological importance of the coronary arterial blood supply to the rattlesnake heart. J Exp Biol 2008, 211:3588-3593.
20. Saunders R., Farrell A., Knox D. Progression of coronary arterial lesions in Atlantic salmon as a function of growth rate. J Fish Aquat Sci 1992, 49:878-884.
21. Gati S., Chandra N., Bennett R.L., et al. Increased left ventricular trabeculation in highly trained athletes: do we need more stringent criteria for the diagnosis of left ventricular non-compaction in athletes?. Heart 2013, 99:401-408.
22. Finsterer J., Stollberger C. Definite, probable, or possible left ventricular hypertrabeculation/noncompaction. Int J Cardiol 2008, 123:175-176.
23. Arbustini E., Weidemann F., Hall J.L. Left ventricular noncompaction: a distinct cardiomyopathy or a trait shared by different cardiac diseases?. J Am Coll Cardiol 2014, 64:1840-1850.
24. Captur G., Zemrak F., Muthurangu V., et al. Fractal analysis of myocardial trabeculations in 2547 subjects: the Multi-Ethnic Study of Atherosclerosis. Radiology 2015, 10:1-9.
25. Captur G., Muthurangu V., Cook C., et al. Quantification of left ventricular trabeculae using fractal analysis. J Cardiovasc Magn Reson 2013, 15:36.
26. Zemrak F., Ahlman M.A., Captur G., et al. The relationship of left ventricular trabeculation to ventricular function and structure over a 9.5-year follow-up. J Am Coll Cardiol 2014, 64:1971-1980.
27. Freedom R.M., Yoo S.J., Perrin D., et al. The morphological spectrum of ventricular noncompaction. Cardiol Young 2005, 15:345-364.
28. Oechslin E., Jenni R. Left ventricular non-compaction revisited: a distinct phenotype with genetic heterogeneity?. Eur Heart J 2011, 32:1446-1456.
29. Shou W., Aghdasi B., Armstrong D.L., et al. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 1998, 391:489-492.
30. Ashraf H., Pradhan L., Chang E.I., et al. A mouse model of human congenital heart disease: high incidence of diverse cardiac anomalies and ventricular noncompaction produced by heterozygous Nkx2-5 homeodomain missense mutation. Circ Cardiovasc Genet 2014, 7:423-433.
31. Phoon C.K., Acehan D., Schlame M., et al. Tafazzin knockdown in mice leads to a developmental cardiomyopathy with early diastolic dysfunction preceding myocardial noncompaction. J Am Heart Assoc 2012, 1:1-13.
32. Nakamura T., Colbert M., Krenz M., et al. Mediating ERK1 / 2 signaling rescues congenital heart defects in a mouse model of Noonan syndrome. J Clin Invest 2007, 117:2123-2132.
33. Amberger J.S., Bocchini C.A., Schiettecatte F., Scott A.F., Hamosh A. OMIM.org: Online Mendelian Inheritance in Man (OMIM), an online catalog of human genes and genetic disorders. Nucleic Acids Res 2015, 43:D789-D798.
34. Klaassen S., Probst S., Oechslin E., et al. Mutations in sarcomere protein genes in left ventricular noncompaction. Circulation 2008, 117:2893-2901.
35. Ichida F., Tsubata S., Bowles K.R., et al. Novel gene mutations in patients with left ventricular noncompaction or Barth syndrome. Circulation 2001, 103:1256-1263.
36. Vatta M., Mohapatra B., Jimenez S., et al. Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 2003, 42:2014-2027.
37. Hermida-Prieto M., Monserrat L., Castro-Beiras A., et al. Familial dilated cardiomyopathy and isolated left ventricular noncompaction associated with lamin A/C gene mutations. Am J Cardiol 2004, 94:50-54.
38. Probst S., Oechslin E., Schuler P., et al. Sarcomere gene mutations in isolated left ventricular noncompaction cardiomyopathy do not predict clinical phenotype. Circ Cardiovasc Genet 2011, 4:367-374.
39. Basu R., Hazra S., Shanks M., Paterson D.I., Oudit G.Y. Novel mutation in exon 14 of the sarcomere gene MYH7 in familial left ventricular noncompaction with bicuspid aortic valve. Circ Heart Fail 2014, 7:1059-1062.
40. Arndt A.K., Schafer S., Drenckhahn J.D., et al. Fine mapping of the 1p36 deletion syndrome identifies mutation of PRDM16 as a cause of cardiomyopathy. Am J Hum Genet 2013, 93:67-77.
41. Bleyl S.B., Mumford B.R., Brown-Harrison M.C., et al. Xq28-linked noncompaction of the left ventricular myocardium: prenatal diagnosis and pathologic analysis of affected individuals. Am J Med Genet 1997, 72:257-265.
42. Tang S., Batra A., Zhang Y., Ebenroth E.S., Huang T. Left ventricular noncompaction is associated with mutations in the mitochondrial genome. Mitochondrion 2010, 10:350-357.
43. Ware S.M., El-Hassan N., Kahler S.G., et al. Infantile cardiomyopathy caused by a mutation in the overlapping region of mitochondrial ATPase 6 and 8 genes. J Med Genet 2009, 46:308-314.
44. Finsterer J., Stöllberger C., Schubert B. Acquired left ventricular hypertrabeculation/noncompaction in mitochondriopathy. Cardiology 2004, 102:228-230.
45. Milano A., Vermeer A.M., Lodder E.M., et al. HCN4 mutations in multiple families with bradycardia and left ventricular noncompaction cardiomyopathy. J Am Coll Cardiol 2014, 64:745-756.
46. Yang J., Zhu M., Wang Y., et al. Whole-exome sequencing identify a new mutation of MYH7 in a Chinese family with left ventricular noncompaction. Gene 2015, 558:138-142.
47. Garcia-Pavia P., de la Pompa J.L. Left ventricular noncompaction: a genetic cardiomyopathy looking for diagnostic criteria. J Am Coll Cardiol 2014, 64:1981-1983.
48. Arbustini E., Narula N., Tavazzi L., et al. The MOGE(S) classification of cardiomyopathy for clinicians. J Am Coll Cardiol 2014, 64:304-318.
49. Melendez-Ramirez G., Castillo-Castellon F., Espinola-Zavaleta N., Meave A., Kimura-Hayama E.T. Left ventricular noncompaction: a proposal of new diagnostic criteria by multidetector computed tomography. J Cardiovasc Comput Tomogr 2012, 6:346-354.
50. Petersen S.E., Selvanayagam J.B., Wiesmann F., et al. Left ventricular non-compaction: insights from cardiovascular magnetic resonance imaging. J Am Coll Cardiol 2005, 46:101-105.
51. Anderson R.H. Ventricular non-compaction-a frequently ignored finding?. Eur Heart J 2008, 29:10-11.
52. Captur G., Flett A.S., Jacoby D.L., Moon J.C. Left ventricular non-noncompaction: the mitral valve prolapse of the 21st century?. Int J Cardiol 2013, 164:3-6.
53. Kawel N., Nacif M., Arai A.E., et al. Trabeculated (noncompacted) and compact myocardium in adults: the multi-ethnic study of atherosclerosis. Circ Cardiovasc Imaging 2012, 5:357-366.
54. Jacquier A., Thuny F., Jop B., et al. Measurement of trabeculated left ventricular mass using cardiac magnetic resonance imaging in the diagnosis of left ventricular non-compaction. Eur Heart J 2010, 31:1098-1104.
55. Dawson D.K., Maceira A.M., Raj V.J., et al. Regional thicknesses and thickening of compacted and trabeculated myocardial layers of the normal left ventricle studied by cardiovascular magnetic resonance. Circ Cardiovasc Imaging 2011, 4:139-146.
56. Grothoff M., Pachowsky M., Hoffmann J., et al. Value of cardiovascular MR in diagnosing left ventricular non-compaction cardiomyopathy and in discriminating between other cardiomyopathies. Eur Radiol 2012, 22:2699-2709.
57. Stacey R.B., Andersen M.M., St Clair M., Hundley W.G., Thohan V. Comparison of systolic and diastolic criteria for isolated LV noncompaction in CMR. JACC Cardiovasc Imaging 2013, 6:931-940.
58. Captur G., Lopes L.R., Patel V., et al. Abnormal cardiac formation in hypertrophic cardiomyopathy: fractal analysis of trabeculae and preclinical gene expression. Circ Cardiovasc Genet 2014, 7:241-248.
59. Marchal P., Lairez O., Cognet T., et al. Relationship between left ventricular sphericity and trabeculation indexes in patients with dilated cardiomyopathy: a cardiac magnetic resonance study. Eur Heart J Cardiovasc Imaging 2013, 14:914-920.
60. André F., Burger A., Loßnitzer D., et al. Reference values for left and right ventricular trabeculation and non-compacted myocardium. Int J Cardiol 2015, 185:240-247.
61. Kawel N., Turkbey E.B., Carr J.J., et al. Normal left ventricular myocardial thickness for middle-aged and older subjects with steady-state free precession cardiac magnetic resonance: the multi-ethnic study of atherosclerosis. Circ Cardiovasc Imaging 2012, 5:500-508.
62. Chin T.K., Perloff J.K., Williams R.G., Jue K., Mohrmann R. Isolated noncompaction of left ventricular myocardium. A study of eight cases. Circulation 1990, 82:507-513.
63. Jenni R., Oechslin E., Schneider J., Jost C.A., Kaufmann P.A. Echocardiographic and pathoanatomical characteristics of isolated left ventricular non-compaction: a step towards classification as a distinct cardiomyopathy. Heart 2001, 86:666-671.
64. Stöllberger C., Finsterer J., Blazek G. Left ventricular hypertrabeculation/noncompaction and association with additional cardiac abnormalities and neuromuscular disorders. Am J Cardiol 2002, 90:899-902.
65. Stöllberger C., Finsterer J. Left ventricular hypertrabeculation/noncompaction. J Am Soc Echocardiogr 2004, 17:91-100.
66. Frischknecht B.S., Attenhofer Jost C.H., Oechslin E.N., et al. Validation of noncompaction criteria in dilated cardiomyopathy, and valvular and hypertensive heart disease. J Am Soc Echocardiogr 2005, 18:865-872.
67. Sidhu M., Uthamalingam S., Ahmed W., et al. Defining left ventricular noncompaction using cardiac computed tomography. J Thorac Imaging 2013, 29:60-66.
68. Goo S., Joshi P., Sands G., et al. Trabeculae carneae as models of the ventricular walls: implications for the delivery of oxygen. J Gen Physiol 2009, 134:339-350.
69. Backer D., Cholley B.P., Slama M., Vieillard-Baron A., Vignon P. Hemodynamic Monitoring Using Echocardiography in the Critically Ill 2011, 14-16. Springer-Verlag Berlin Heidelberg, Springer Science & Business Media, Berlin.
70. Wong P.C., Miller-Hance W.C. Transesophageal Echocardiography for Congenital Heart Disease 2014, 22-40. Springer-Verlag London, Springer Science & Business Media, London.
71. Petersen SE, Zemrak F. Spot the difference: LV trabeculation vs. LV noncompaction. Cardiology Today, February 2015. Thorofare, NJ: SLACK Incorporated, 2015.
72. Captur G., Lopes L.R., Mohun T.J., et al. Prediction of sarcomere mutations in subclinical hypertrophic cardiomyopathy. Circ Cardiovasc Imaging 2014, 7:863-867.
73. Weninger W.J., Geyer S.H. Episcopic 3D imaging methods: tools for researching gene function. Curr Genomics 2008, 9:282-289.
74. Odgaard A., Andersen K., Melsen F., Gundersen H.J. A direct method for fast three-dimensional serial reconstruction. J Microsc 1990, 159:335-342.
75. Weninger W.J., Meng S., Streicher J., Müller G.B. A new episcopic method for rapid 3-D reconstruction: applications in anatomy and embryology. Anat Embryol (Berl) 1998, 197:341-348.
76. Weninger W.J., Mohun T. Phenotyping transgenic embryos: a rapid 3-D screening method based on episcopic fluorescence image capturing. Nat Genet 2002, 30:59-65.
77. Ewald A.J., Mcbride H., Reddington M., Fraser S.E., Kerschmann R. Surface imaging microscopy, an automated method for visualizing whole embryo samples in three dimensions at high resolution. Dev Dyn 2002, 225:369-375.
78. Mohun T.J., Weninger W.J. Generation of volume data by episcopic three-dimensional imaging of embryos. Cold Spring Harb Protoc 2012, 2012:681-682.
79. Denk W., Horstmann H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2004, 2:e329.
80. Weninger W.J., Geyer S.H., Mohun T.J., et al. High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology. Anat Embryol (Berl) 2006, 211:213-221.
81. Mickoleit M., Schmid B., Weber M., et al. High-resolution reconstruction of the beating zebrafish heart. Nat Methods 2014, 11:1-6.
82. Kohli S.K., Pantazis A., Shah J.S., et al. Diagnosis of left-ventricular non-compaction in patients with left-ventricular systolic dysfunction: time for a reappraisal of diagnostic criteria?. Eur Heart J 2008, 29:89-95.
83. Stöllberger C., Finsterer J. Consider also extracardiac manifestations in left ventricular noncompaction. J Am Soc Echocardiogr 2007, 20:552.
84. Madan S., Mandal S., Bost J.E., et al. Noncompaction cardiomyopathy in children with congenital heart disease: evaluation using cardiovascular magnetic resonance imaging. Pediatr Cardiol 2012, 33:215-221.
85. Jiang B., Yang Y., Li F., et al. Giant aneurysm of right coronary artery fistula into left ventricle coexisting with noncompaction of left ventricular myocardium. Ann Thorac Surg 2014, 98:e85-e86.
86. Hojjati M.R., Rozo J.C., Nazeri A., Cheong B.Y. A rare pairing: myocardial noncompaction and congenital absence of pericardium. Tex Heart Inst J 2013, 40:500-501.
87. Erdogan E., Akkaya M., Bacaksiz A., Tasal A., Sevgili E. A very rare case of coexistence of ventricular noncompaction cardiomyopathy, myocardial bridging and atherosclerosis. Adv Interv Cardiol 2013, 9:176-178.
88. Yiginer O., Uz O., Kardesoglu E., et al. Noncompaction of the myocardium coexistent with vertebral hemangiomas. Tex Heart Inst J 2011, 38:212-213.
89. Finsterer J., Zarrouk-Mahjoub S. Consider a mitochondrial disorder when left ventricular hypertrabeculation/noncompaction is associated with renal cysts. Tex Heart Inst J 2014, 41:677-678.
90. Kim K.H., Song B.G., Park M.J., et al. Noncompaction of the myocardium coexistent with bronchiectasis and polycystic kidney disease. Heart Lung Circ 2013, 22:312-314.
91. Said S., Cooper C.J., Quevedo K., Rodriguez E., Hernandez G.T. Biventricular non-compaction with predominant right ventricular involvement, reduced left ventricular systolic and diastolic function, and pulmonary hypertension in a Hispanic male. Am J Case Rep 2013, 14:539-542.
92. Ivan D., Flamm S.D., Abrams J., et al. Isolated ventricular non-compaction in adults with idiopathic cardiomyopathy: cardiac magnetic resonance and pathologic characterization of the anomaly. J Heart Lung Transplant 2005, 24:781-786.
93. Dodd J.D., Holmvang G., Hoffmann U., et al. Quantification of left ventricular noncompaction and trabecular delayed hyperenhancement with cardiac MRI: correlation with clinical severity. Am J Roentgenol 2007, 189:974-980.
94. Cho Y.H., Jin S.J., Je H.C., et al. A case of noncompaction of the ventricular myocardium combined with situs ambiguous with polysplenia. Yonsei Med J 2007, 48:1052-1055.
95. Dursun M., Agayev A., Nisli K., et al. MR imaging features of ventricular noncompaction: emphasis on distribution and pattern of fibrosis. Eur J Radiol 2010, 74:147-151.
96. Akhbour S., Fellat I., Fennich N., et al. Electrocardiographic findings in correlation to magnetic resonance imaging patterns in African patients with isolated ventricular noncompaction. Anatol J Cardiol 2015, 15:550-555.
97. Wan J., Zhao S., Cheng H., et al. Varied distributions of late gadolinium enhancement found among patients meeting cardiovascular magnetic resonance criteria for isolated left ventricular non-compaction. J Cardiovasc Magn Reson 2013, 15:20-26.
98. Nucifora G., Aquaro G.D., Masci P.G., Pingitore A., Lombardi M. Magnetic resonance assessment of prevalence and correlates of right ventricular abnormalities in isolated left ventricular noncompaction. Am J Cardiol 2014, 113:142-146.
99. Nucifora G., Aquaro G.D., Pingitore A., Masci P.G., Lombardi M. Myocardial fibrosis in isolated left ventricular non-compaction and its relation to disease severity. Eur J Heart Fail 2011, 13:170-176.
100. Chaowu Y., Li L., Shihua Z. Histopathological features of delayed enhancement cardiovascular magnetic resonance in isolated left ventricular noncompaction. J Am Coll Cardiol 2011, 58:311-312.
101. Burke A., Mont E., Kutys R., Virmani R. Left ventricular noncompaction: a pathological study of 14 cases. Hum Pathol 2005, 36:403-411.
102. Greutmann M., Mah M.L., Silversides C.K., et al. Predictors of adverse outcome in adolescents and adults with isolated left ventricular noncompaction. Am J Cardiol 2012, 109:276-281.
103. Enríquez R.A., Baeza V.R., Gabrielli N.L., Córdova A.S., Castro G.P. Non compaction cardiomyopathy: a series of 15 cases [in Spanish]. Rev Med Chil 2011, 139:864-871.
104. Stöllberger C., Blazek G., Gessner M., et al. Neuromuscular comorbidity, heart failure, and atrial fibrillation as prognostic factors in left ventricular hypertrabeculation/noncompaction. Herz 2015, 40:906-911.
105. Aras D., Tufekcioglu O., Ergun K., et al. Clinical features of isolated ventricular noncompaction in adults long-term clinical course, echocardiographic properties, and predictors of left ventricular failure. J Card Fail 2006, 12:726-733.
106. Lofiego C., Biagini E., Pasquale F., et al. Wide spectrum of presentation and variable outcomes of isolated left ventricular non-compaction. Heart 2007, 93:65-71.