Advertisement

Noncompaction Cardiomyopathy, a Novel Clinical Entity (Historical Perspective)

  • Rolf Engberding
  • Birgit Gerecke
Chapter

Abstract

Initially, the abnormal myocardial morphology with a typical spongy pattern has been described in newborns and infants, based on necropsy findings in cases with complex congenital heart disease. Only after introduction of echocardiography, a breakthrough in the ante mortem diagnosis has been achieved, increasing the awareness of the disease.

It was in 1984, when the first isolated case with this abnormal myocardial pattern was published, presenting the ante mortem diagnosis by echocardiography for the first time. A subsequent publication in 1986 confirmed the result of the initial report. Both studies used the term “persistence of isolated myocardial sinusoids”, recognizing the persistence of embryonic myocardial morphology found in the absence of other cardiac anomalies. In 1990, the term “isolated noncompaction of left ventricular myocardium” was introduced, assuming that this disease was due to an arrest of the normal compaction process during endomyocardial morphogenesis. But new data suggest, that no real compaction process may be present during normal cardiac development. In case of left ventricular noncompaction it was observed, that the excessive trabeculations did not have the identity of the normal embryonic trabeculations, suggesting, that noncompaction may not be the result of a failure in a compaction process but instead results from the compacted myocardium of the ventricular wall, growing into the ventricular lumen in a trabecular fashion.

However, a lot of evidence exists, that the complex developmental processes of the heart are genetically regulated and the myocardial patterns of left ventricular noncompaction may occur as a mutation based failure of normal endomyocardial morphogenesis. Current data suggest, that in future, genetic testing may allow to distinguish a non-genetic phenotype of left ventricular noncompaction (LVNC) from genetic noncompaction cardiomyopathy (NCCM), thus improving adequate risk stratification and proper management.

Keywords

Compacted myocardium Noncompacted myocardium Excessive trabeculations Left ventricular noncompaction (LVNC) Isolated noncompaction cardiomyopathy (NCCM) Left ventricular hypertrabeculation (LVHT) Genetics in LVNC Phenotype LVNC Cardiomyopathy NCCM Myocardial remodeling 

References

  1. 1.
    Engberding R, Bender F. Identification of a rare congenital anomaly of the myocardium by two-dimensional echocardiography: persistence of isolated myocardial sinusoids. Am J Cardiol. 1984;53:1733–4.CrossRefGoogle Scholar
  2. 2.
    Grant RT. An unusual anomaly of the coronary vessels in the malformed heart of a child. Heart. 1926;1:273–83.Google Scholar
  3. 3.
    Bellet S, Gouley BA. Congenital heart disease with multiple cardiac anomalies. Report of a case showing aortic atresia, fibrous scar in myocardium and embryonal sinusoidal remains. Am J Med Sci. 1932;183:458–65.CrossRefGoogle Scholar
  4. 4.
    Lauer RM, Fink HP, Petry EL, Dunn MI, Diehl AM. Angiographic demonstration of intramyocardial sinusoids in pulmonary-valve atresia with intact ventricular septum and hypoplastic right ventricle. N Engl J Med. 1964;271:68–72.CrossRefGoogle Scholar
  5. 5.
    Feldt RH, Rahimtoola SH, Davis GD, Swan HJ, Titus JL. Anomalous ventricular myocardial patterns in a child with complex congenital heart disease. Am J Cardiol. 1969;23:732–4.CrossRefGoogle Scholar
  6. 6.
    Jenni R, Goebel N, Tartini R, Schneider J, Arbenz U, Oelz O. Persisting myocardial sinusoids of both ventricles as an isolated anomaly: echocardiographic, angiographic, and pathologic anatomical findings. Cardiovasc Intervent Radiol. 1986;9:127–31.CrossRefGoogle Scholar
  7. 7.
    Chin TK, Perloff JK, Williams RG, Jue K, Mohrmann R. Isolated noncompaction of left ventricular myocardium. A study of eight cases. Circulation. 1990;82:507–13.CrossRefGoogle Scholar
  8. 8.
    Dusek J, Ostádal B, Duskova M. Postnatal persistence of spongy myocardium with embryonic blood supply. Arch Pathol. 1975;99:312–7.PubMedGoogle Scholar
  9. 9.
    Harvey RP. Patterning the vertebrate heart. Nat Rev Genet. 2002;7:544–56.CrossRefGoogle Scholar
  10. 10.
    Srivastava D, Olson EN. A genetic blueprint for cardiac development. Nature. 2000;407:221–6.CrossRefGoogle Scholar
  11. 11.
    Eisenberg LM, Markwald RR. Cellular recruitment and the development of the myocardium. Dev Biol. 2004;274:225–32.CrossRefGoogle Scholar
  12. 12.
    Agmon Y, Connolly HM, Olson LJ, Khandheria BK, Seward JB. Noncompaction of the ventricular myocardium. J Am Soc Echocardiogr. 1999;12:859–63.CrossRefGoogle Scholar
  13. 13.
    Bernanke DH, Velkey JM. Development of the coronary blood supply: changing concepts and current ideas. Anat Rec. 2002;269:198–208.CrossRefGoogle Scholar
  14. 14.
    Freedom RM, Yoo SJ, Perrin D, Taylor G, Petersen S, Anderson RH. The morphological spectrum of ventricular noncompaction. Cardiol Young. 2005;15:345–64.CrossRefGoogle Scholar
  15. 15.
    Sedmera D, McQuinn T. Embryogenesis of the heart muscle. Heart Fail Clin. 2008;4:235–45.CrossRefGoogle Scholar
  16. 16.
    Henderson DJ, Anderson RH. The development and structure of the ventricles in the human heart. Pediatr Cardiol. 2009;30:588–96.CrossRefGoogle Scholar
  17. 17.
    Schleich JM, Abdulla T, Summers R, Houyel L. An overview of cardiac morphogenesis. Une anthologie du développement cardiaque normal. Arch Cardiovasc Dis. 2013;106:612–23.CrossRefGoogle Scholar
  18. 18.
    Srivastava D. Making or breaking the heart: from lineage determination to morphogenesis. Cell. 2006;126:1037–48.CrossRefGoogle Scholar
  19. 19.
    Ichida F, Hamamichi Y, Miyawaki T, Ono Y, Kamiya T, Akagi T, Hamada H, Hirose O, Isobe T, Yamada K, Kurotobi S, Mito H, Miyake T, Murakami Y, Nishi T, Shinohara M, Seguchi M, Tashiro S, Tomimatsu H. Clinical features of isolated noncompaction of the ventricular myocardium: long-term clinical course, hemodynamic properties, and genetic background. J Am Coll Cardiol. 1999;34:233–40.CrossRefGoogle Scholar
  20. 20.
    Bennett CE, Freudenberger R. The current approach to diagnosis and management of left ventricular noncompaction cardiomyopathy: review of the literature. Cardiol Res Pract. 2016;2016:5172308.CrossRefGoogle Scholar
  21. 21.
    Paterick TE, Umland MM, Jan MF, Ammar KA, Kramer C, Khandheria BK, Seward JB, Tajik AJ. Left ventricular noncompaction: a 25-year odyssey. J Am Soc Echocardiogr. 2012;25:363–75.CrossRefGoogle Scholar
  22. 22.
    Finsterer J, Stöllberger C, Towbin JA. Left ventricular noncompaction cardiomyopathy: cardiac, neuromuscular, and genetic factors. Nat Rev Cardiol. 2017;14:224–37.CrossRefGoogle Scholar
  23. 23.
    Engberding R, Stöllberger C, Gerecke BJ. Left ventricular noncompaction: affected wall regions in respect to LV function – data from the German Noncompaction Registry (ALKK). Circulation. 2012;126(Suppl. 21):A14830.Google Scholar
  24. 24.
    van Dalen BM, Caliskan K, Soliman OII, Nemes A, Vletter WB, ten Cate FJ, Geleijnse ML. Left ventricular solid body rotation in non-compaction cardiomyopathy: a potential new objective and quantitative functional diagnostic criterion? Eur J Heart Fail. 2008;10:1088–93.CrossRefGoogle Scholar
  25. 25.
    Sanchez-Quintana D, Garcia-Martinez V, Climent V, Hurle JM. Morphological changes in the normal pattern of ventricular myoarchitecture in the developing human heart. Anat Rec. 1995;243:483–95.CrossRefGoogle Scholar
  26. 26.
    Gittenberger-de Groot AC. Mannheimer lecture. The quintessence of the making of the heart. Cardiol Young. 2003;13:175–83.CrossRefGoogle Scholar
  27. 27.
    Christoffels VM, Habets PE, Franco D, Campione M, de Jong F, Lamers WH, Bao ZZ, Palmer S, Biben C, Harvey RP, Moorman AF. Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol. 2000;223:266–78.CrossRefGoogle Scholar
  28. 28.
    Van Mierop LH, Kutsche LM. Development of the ventricular septum of the heart. Heart Vessel. 1985;1:114–9.CrossRefGoogle Scholar
  29. 29.
    Jensen B, van der Wal AC, Moorman AFM, Christoffels VM. Excessive trabeculations in noncompaction do not have the embryonic identity. Int J Cardiol. 2017;227:325–30.CrossRefGoogle Scholar
  30. 30.
    Sizarov A, Ya J, de Boer BA, Lamers WH, Christoffels VM, Moorman AF. Formation of the buildingplan of the human heart: morphogenesis, growth, and differentiation. Circulation. 2011;123:1125–35.CrossRefGoogle Scholar
  31. 31.
    Sizarov A, Devalla HD, Anderson RH, Passier R, Christoffels VM, Moorman AF. Molecular analysis of the patterning of the conduction tissues in the developing human heart. Circ Arrhythm Electrophysiol. 2011;4:532–42.CrossRefGoogle Scholar
  32. 32.
    Jensen B, Agger P, de Boer BA, Oostra RJ, Pedersen M, van der Wal AC, Nils Planken R, Moorman AF. The hypertrabeculated (noncompacted) left ventricle is different from the ventricle of embryos and ectothermic vertebrates. Biochim Biophys Acta. 2016;1863:1696–706.CrossRefGoogle Scholar
  33. 33.
    Stöllberger C, Finsterer J. Trabeculation and left ventricular hypertrabeculation/noncompaction. J Am Soc Echocardiogr. 2004;17:1120–1.CrossRefGoogle Scholar
  34. 34.
    Maron BJ, Towbin JA, Thiene G, Antzelevitch C, Corrado D, Arnett D, Moss AJ, Seidman CE, Young JB, American Heart Association; Council on Clinical Cardiology, Heart Failure and Transplantation Committee, Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups, Council on Epidemiology and Prevention. Contemporary definitions and classifications of the cardiomyopathies: an American Heart Association scientific statement form the council on clinical cardiology, heart failure and transplantation committee: quality of care and outcomes research and functional genomics and translational biology interdisciplinary working groups; and the council on epidemiology and prevention. Circulation. 2006;113:1807–16.CrossRefGoogle Scholar
  35. 35.
    Elliott P, Andersson B, Arbustini E, Bilinska Z, Cecchi F, Charron P, Dubourg O, Kühl U, Maisch B, McKenna WJ, Monserrat L, Pankuweit S, Rapezzi C, Seferovic P, Tavazzi L, Keren A. Classification of the cardiomyopathies: a position statement from the european society of cardiology working group on myocardial and pericardial diseases. Eur Heart J. 2008;29:270–6.CrossRefGoogle Scholar
  36. 36.
    Klaassen S, Probst S, Oechslin E, Gerull B, Krings G, Schuler P, Greutmann M, Hürlimann D, Yegitbasi M, Pons L, Gramlich M, Drenckhahn JD, Heuser A, Berger F, Jenni R, Thierfelder L. Mutations in sarcomere protein genes in left ventricular noncompaction. Circulation. 2008;117:2893–901.CrossRefGoogle Scholar
  37. 37.
    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.CrossRefGoogle Scholar
  38. 38.
    Finsterer J, Stöllberger C, Schubert B. Acquired left ventricular hypertrabeculation/ noncompaction in mitochondriopathy. Cardiology. 2004;102:228–30.CrossRefGoogle Scholar
  39. 39.
    Finsterer J, Stöllberger C, Schubert B. Acquired left ventricular noncompaction as a cardiac manifestation of neuromuscular disorders. Scand Cardiovasc J. 2008;42:25–30.CrossRefGoogle Scholar
  40. 40.
    D’Ascenzi F, Pelliccia A, Natali BM, Bonifazi M, Mondillo S. Exercise-induced left-ventricular hypertrabeculation in athlete’s heart. Int J Cardiol. 2015;181:320–2.CrossRefGoogle Scholar
  41. 41.
    Gati S, Papadakis M, Papamichael ND, Zaidi A, Sheikh N, Reed M, Sharma R, Thilaganathan B, Sharma S. Reversible de novo left ventricular trabeculations in pregnant women: implications for the diagnosis of left ventricular noncompaction in low-risk populations. Circulation. 2014;130:475–83.CrossRefGoogle Scholar
  42. 42.
    Anderson RH, Jensen B, Mohun TJ, Petersen SE, Aung N, Zemrak F, Planken RN, MacIver DH. Key questions relating to left ventricular noncompaction cardiomyopathy: is the emperor still wearing any clothes? Can J Cardiol. 2017;33:747–57.CrossRefGoogle Scholar
  43. 43.
    Oechslin E, Jenni R. Nosology of noncompaction cardiomyopathy: the emperor still wears clothes! Can J Cardiol. 2017;33:701–4.CrossRefGoogle Scholar
  44. 44.
    Arbustini E, Favalli V, Narula N, Serio A, Grasso M. Left ventricular noncompaction: a distinct genetic cardiomyopathy? J Am Coll Cardiol. 2016;68:949–66.CrossRefGoogle Scholar
  45. 45.
    Oechslin E, Jenni R. Left ventricular non-compaction revisited: a distinct phenotype with genetic heterogeneity? Eur Heart J. 2011;32:1446–156.CrossRefGoogle Scholar
  46. 46.
    Stöllberger C, Gerecke B, Finsterer J, Engberding R. Refinement of echocardiographic criteria for left ventricular noncompaction. Int J Cardiol. 2013;165:463–7.CrossRefGoogle Scholar
  47. 47.
    Weir-McCall JR, Yeap PM, Papagiorcopulo C, Fitzgerald K, Gandy SJ, Lambert M, Belch JJF, Cavin I, Littleford R, Macfarlane JA, Matthew SZ, Nicholas RS, Struthers AD, Sullivan F, Waugh SA, White RD, Houston JG. Left ventricular noncompaction anatomical phenotype or distinct cardiomyopathy? J Am Coll Cardiol. 2016;68:2157–65.CrossRefGoogle Scholar
  48. 48.
    Oechslin E, Jenni J. Left ventricular noncompaction from physiologic remodeling to noncompaction cardiomyopathy. J Am Coll Cardiol. 2018;71:723–6.CrossRefGoogle Scholar
  49. 49.
    van Waning JI, Caliskan K, Hoedemaekers YM, van Spaendonck-Zwarts KY, Baas AF, Boekholdt SM, van Melle JP, Teske AJ, Asselbergs FW, Backx APCM, du Marchie Sarvaas GJ, Dalinghaus M, Breur JMPJ, Linschoten MPM, Verlooij LA, Kardys I, Dooijes D, Lekanne Deprez RH, IJpma AS, van den Berg MP, Hofstra RMW, van Slegtenhorst MA, Jongbloed JDH, Majoor-Krakauer D. Genetics, clinical features, and long-term outcome of noncompaction cardiomyopathy. J Am Coll Cardiol. 2018;71:711–22.CrossRefGoogle Scholar
  50. 50.
    Jefferies JL, Wilkinson JD, Sleeper LA, Colan SD, Lu M, Pahl E, Kantor PF, Everitt MD, Webber SA, Kaufman BD, Lamour JM, Canter CE, Hsu DT, Addonizio LJ, Lipshultz SE, Towbin JA, Pediatric Cardiomyopathy Registry Investigators. Cardiomyopathy phenotypes and outcomes for children with left ventricular myocardial noncompaction: results from the pediatric cardiomyopathy registry. J Card Fail. 2015;21:877–84.CrossRefGoogle Scholar
  51. 51.
    Engberding R, Yelbuz TM, Breithardt G. Isolated noncompaction of the left ventricular myocardium - a review of the literature two decades after the initial case description. Clin Res Cardiol. 2007;96:481–8.CrossRefGoogle Scholar
  52. 52.
    Stöllberger C, Gerecke B, Engberding R, Grabner B, Wandaller C, Finsterer J, Gietzelt M, Balzereit A. Interobserver agreement of the echocardiographic diagnosis of LV hypertrabeculation/noncompaction. JACC Cardiovasc Imaging. 2015;8:1252–7.CrossRefGoogle Scholar
  53. 53.
    Engberding R, Stöllberger C, Ong P, Yelbuz TM, Gerecke BJ, Breithardt G. Isolated noncompaction cardiomyopathy. Dtsch Arztebl Int. 2010;107:206–13.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Zemrak F, Ahlman MA, Captur G, Mohiddin SA, Kawel-Boehm N, Prince MR, Moon JC, Hundley WG, Lima JAC, Bluemke DA, Petersen SE. The relationship of left ventricular trabeculation to ventricular function and structure over a 9.5-year follow-up. J Am Coll Cardiol. 2014;64(19):1971–80.CrossRefGoogle Scholar
  55. 55.
    Towbin JA, Jefferies JL. Cardiomyopathies due to left ventricular noncompaction, mitochondrial and storage diseases, and inborn errors of metabolism. Circ Res. 2017;121(7):838–54.CrossRefGoogle Scholar
  56. 56.
    Petersen SE, Selvanayagam JB, Wiesmann F, Robson MD, Francis JM, Anderson RH, Watkins H, Neubauer S. Left ventricular non-compaction. J Am Coll Cardiol. 2005;46(1):101–5.CrossRefGoogle Scholar
  57. 57.
    Belanger AR, Miller MA, Donthireddi UR, Najovits AJ, Goldman ME. New classification scheme of left ventricular noncompaction and correlation with ventricular performance. Am J Cardiol. 2008;102(1):92–6.CrossRefGoogle Scholar
  58. 58.
    Jacquier A, Thuny F, Jop B, Giorgi R, Cohen F, Gaubert JY, Vidal V, Bartoli JM, Habib G, Moulin G. Measurement of trabeculated left ventricular mass using cardiac magnetic resonance imaging in the diagnosis of left ventricular non-compaction. Eur Heart J. 2010;31(9):1098–104.CrossRefGoogle Scholar
  59. 59.
    Gebhard C, Stähli BE, Greutmann M, Biaggi P, Jenni R, Tanner FC. Reduced left ventricular compacta thickness: a novel echocardiographic criterion for non-compaction cardiomyopathy. J Am Soc Echocardiogr. 2012;25(10):1050–7.CrossRefGoogle Scholar
  60. 60.
    Conces DJ, Ryan T, Tarver RD. Noncompaction of ventricular myocardium: CT appearance. Am J Roentgenol. 1991;156(4):717–8.CrossRefGoogle Scholar
  61. 61.
    Jenni R. Echocardiographic and pathoanatomical characteristics of isolated left ventricular non-compaction: a step towards classification as a distinct cardiomyopathy. Heart. 2001;86(6):666–71.CrossRefGoogle Scholar
  62. 62.
    Lowery MH, Martel JA, Zambrano JP, Ferreira A, Eco L, Gallagher A. Noncompaction of the ventricular myocardium: the use of contrast-enhanced echocardiography in diagnosis. J Am Soc Echocardiogr. 2003;16(1):94–6.CrossRefGoogle Scholar
  63. 63.
    Hany TF, Jenni R, Debatin JF. MR appearance of isolated noncompaction of the left ventricle. J Magn Reson Imaging. 1997;7(2):437–8.CrossRefGoogle Scholar
  64. 64.
    Weiss F, Habermann CR, Lilje C, Razek W, Sievers J, Weil J, Adam G. MRI in the diagnosis of non-compacted ventricular myocardium (NCVM) compared to echocardiography. Rofo. 2003;175:1214–9.CrossRefGoogle Scholar
  65. 65.
    Gopalamurugan AB. Left ventricular non-compaction diagnosed by real time three dimensional echocardiography. Heart. 2005;91(10):1274.CrossRefGoogle Scholar
  66. 66.
    Mohrs OK, Magedanz A, Schlosser T. Noncompaction of the left ventricular myocardium detected by 64-slice multidetector computed tomography. Clin Cardiol. 2007;30(1):48.CrossRefGoogle Scholar
  67. 67.
    Bellavia D, Michelena HI, Martinez M, Pellikka PA, Bruce CJ, Connolly HM, Villarraga HR, Veress G, Oh JK, Miller FA. Speckle myocardial imaging modalities for early detection of myocardial impairment in isolated left ventricular non-compaction. Heart. 2010;96(6):440–7.CrossRefGoogle Scholar
  68. 68.
    Niemann M, Liu D, Hu K, Cikes M, Beer M, Herrmann S, Gaudron PD, Hillenbrand H, Voelker W, Ertl G, Weidemann F. Echocardiographic quantification of regional deformation helps to distinguish isolated left ventricular non-compaction from dilated cardiomyopathy. Eur J Heart Fail. 2012;14(2):155–61.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rolf Engberding
    • 1
  • Birgit Gerecke
    • 2
  1. 1.Internal Medicine and CardiologyamO MVZ WolfsburgWolfsburgGermany
  2. 2.Clinic for Cardiology and PneumologyUniversity Medical Center GöttingenGöttingenGermany

Personalised recommendations