Top

Published in:

01-11-2017

The MOGE(S) classification for cardiomyopathies: current status and future outlook

Authors: Julian G. Westphal, Angelos G. Rigopoulos, Constantinos Bakogiannis, Sarah E. Ludwig, Sophie Mavrogeni, Boris Bigalke, Torsten Doenst, Matthias Pauschinger, Carsten Tschöpe, P. Christian Schulze, Michel Noutsias

Published in: Heart Failure Reviews | Issue 6/2017

Abstract

Cardiomyopathies are complex diseases of multifactorial pathogenesis and have a high morbidity and mortality. Over the past decades, several revisions of classifications and definitions of cardiomyopathies have been proposed, primarily focusing on the phenotypic characterization of cardiomyopathies. The MOGE(S) classification system published in 2013 encompasses the classification of rapidly growing knowledge on genetic mutations, acquired causes (i.e., intramyocardial inflammation, viral infections), and further conditions involved in the induction of cardiomyopathies (e.g., storage diseases, toxicity). It is based on five attributes, including morphofunctional characteristics (M), organ involvement (O), genetic or familial inheritance pattern (G), etiological annotation (E), and optional information about the heart failure functional status (S). This review summarizes the development, the cornerstones of the MOGE(S) classification, and the published data on the clinical relevance of the MOGE(S) classification. We furthermore discuss new issues which might be considered for future updates of the MOGE(S) classification of cardiomyopathies.

(1980) Report of the WHO/ISFC task force on the definition and classification of cardiomyopathies Br Heart J 44(6):672–673

Richardson P, McKenna W, Bristow M, Maisch B, Mautner B, O’Connell J, Olsen E, Thiene G, Goodwin J, Gyarfas I, Martin I, Nordet P (1996) Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies. Circulation 93(5):841–842CrossRefPubMed

Elliott PM, Poloniecki J, Dickie S, Sharma S, Monserrat L, Varnava A, Mahon NG, McKenna WJ (2000) Sudden death in hypertrophic cardiomyopathy: identification of high risk patients. J Am Coll Cardiol 36(7):2212–2218CrossRefPubMed

Olbrich HG (2001) Epidemiology-etiology of dilated cardiomyopathy. Zeitschrift fur Kardiologie 90(Suppl 1):2–9CrossRefPubMed

Maron BJ, Ommen SR, Semsarian C, Spirito P, Olivotto I, Maron MS (2014) Hypertrophic cardiomyopathy: present and future, with translation into contemporary cardiovascular medicine. J Am Coll Cardiol 64(1):83–99. doi:10.1016/j.jacc.2014.05.003 CrossRefPubMed

Brigden W (1957) Uncommon myocardial diseases; the non-coronary cardiomyopathies. Lancet 273(7007):1179–1184CrossRefPubMed

Goodwin JF, Oakley CM (1972) The cardiomyopathies. Br Heart J 34(6):545–552CrossRefPubMedPubMedCentral

Maron BJ, Towbin JA, Thiene G, Antzelevitch C, Corrado D, Arnett D, Moss AJ, Seidman CE, Young JB (2006) Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from 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 Council on Epidemiology and Prevention. Circulation 113(14):1807–1816CrossRefPubMed

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 (2008) Classification of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 29(2):270–276CrossRefPubMed

10.

Elliott PM (2013) Classification of cardiomyopathies: evolution or revolution? J Am Coll Cardiol 62(22):2073–2074. doi:10.1016/j.jacc.2013.10.008 CrossRefPubMed

11.

Arbustini E, Narula N, Dec GW, Reddy KS, Greenberg B, Kushwaha S, Marwick T, Pinney S, Bellazzi R, Favalli V, Kramer C, Roberts R, Zoghbi WA, Bonow R, Tavazzi L, Fuster V, Narula J (2013) The MOGE(S) classification for a phenotype-genotype nomenclature of cardiomyopathy: endorsed by the World Heart Federation. J Am Coll Cardiol 62(22):2046–2072. doi:10.1016/j.jacc.2013.08.1644 CrossRefPubMed

12.

Vaikhanskaya T, Sivitskaya L, Danilenko N, Davydenko O, Kurushka T, Sidorenko I (2014) LMNA-related dilated cardiomyopathy. Oxf Med Case Rep 2014(6):102–104. doi:10.1093/omcr/omu040 CrossRef

13.

Pasotti M (2014) The MOGE(S) classification for a phenotype-genotype nomenclature of cardiomyopathy: more questions than answers? J Am Coll Cardiol 63(23):2584. doi:10.1016/j.jacc.2014.01.078 CrossRefPubMed

14.

Arbustini E, Narula N, Tavazzi L, Serio A, Grasso M, Favalli V, Bellazzi R, Tajik JA, Bonow RO, Fuster V, Narula J (2014) The MOGE(S) classification of cardiomyopathy for clinicians. J Am Coll Cardiol 64(3):304–318. doi:10.1016/j.jacc.2014.05.027 CrossRefPubMed

15.

Arbustini E, Narula N, Dec GW, Reddy KS, Greenberg B, Kushwaha S, Marwick T, Pinney S, Bellazzi R, Favalli V, Kramer C, Roberts R, Zoghbi WA, Bonow R, Tavazzi L, Fuster V, Narula J (2014) Reply: the MOGE(S) classification for a phenotype-genotype nomenclature of cardiomyopathy: more questions than answers? J Am Coll Cardiol 63(23):2584–2586. doi:10.1016/j.jacc.2014.03.028 CrossRefPubMed

16.

Hazebroek MR, Moors S, Dennert R, van den Wijngaard A, Krapels I, Hoos M, Verdonschot J, Merken JJ, de Vries B, Wolffs PF, Crijns HJ, Brunner-La Rocca HP, Heymans S (2015) Prognostic relevance of gene-environment interactions in patients with dilated cardiomyopathy: applying the MOGE(S) classification. J Am Coll Cardiol 66(12):1313–1323. doi:10.1016/j.jacc.2015.07.023 CrossRefPubMed

17.

Agarwal A, Yousefzai R, Jan MF, Cho C, Shetabi K, Bush M, Khandheria BK, Paterick TE, Treiber S, Sra J, Werner P, Allaqaband S, Bajwa T, Tajik AJ (2015) Clinical application of WHF-MOGE(S) classification for hypertrophic cardiomyopathy. Glob Heart 10(3):209–219. doi:10.1016/j.gheart.2015.01.001 CrossRefPubMed

18.

Cheitlin MD, Armstrong WF, Aurigemma GP, Beller GA, Bierman FZ, Davis JL, Douglas PS, Faxon DP, Gillam LD, Kimball TR, Kussmaul WG, Pearlman AS, Philbrick JT, Rakowski H, Thys DM, Antman EM, Smith SC Jr, Alpert JS, Gregoratos G, Anderson JL, Hiratzka LF, Hunt SA, Fuster V, Jacobs AK, Gibbons RJ, Russell RO, American College of C, American Heart A, American Society of E (2003) ACC/AHA/ASE 2003 guideline update for the clinical application of echocardiography: summary article: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (ACC/AHA/ASE Committee to Update the 1997 Guidelines for the Clinical Application of Echocardiography). Circulation 108(9):1146–1162. doi:10.1161/01.CIR.0000073597.57414.A9 CrossRefPubMed

19.

Habib G, Bucciarelli-Ducci C, Caforio ALP, Cardim N, Charron P, Cosyns B, Dehaene A, Derumeaux G, Donal E, Dweck MR, Edvardsen T, Erba PA, Ernande L, Gaemperli O, Galderisi M, Grapsa J, Jacquier A, Klingel K, Lancellotti P, Neglia D, Pepe A, Perrone-Filardi P, Petersen SE, Plein S, Popescu BA, Reant P, Sade LE, Salaun E, Slart R, Tribouilloy C, Zamorano J, Reviewers: Victoria Delgado KH, Vijayaraghavan G (2017) Multimodality imaging in restrictive cardiomyopathies: an EACVI expert consensus document: In collaboration with the ‘Working Group on myocardial and pericardial diseases’ of the European Society of Cardiology Endorsed by the Indian Academy of Echocardiography. Eur Heart J Cardiovasc Imaging. doi:10.1093/ehjci/jex034

20.

Saeed M, Liu H, Liang CH, Wilson MW (2017) Magnetic resonance imaging for characterizing myocardial diseases. Int J Cardiovasc Imaging. doi:10.1007/s10554-017-1127-x

21.

Grun S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, Kispert EM, Hill S, Ong P, Klingel K, Kandolf R, Sechtem U, Mahrholdt H (2012) Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery. J Am Coll Cardiol 59(18):1604–1615. doi:10.1016/j.jacc.2012.01.007 CrossRefPubMed

22.

Lehrke S, Lossnitzer D, Schob M, Steen H, Merten C, Kemmling H, Pribe R, Ehlermann P, Zugck C, Korosoglou G, Giannitsis E, Katus HA (2011) Use of cardiovascular magnetic resonance for risk stratification in chronic heart failure: prognostic value of late gadolinium enhancement in patients with non-ischaemic dilated cardiomyopathy. Heart 97(9):727–732. doi:10.1136/hrt.2010.205542 CrossRefPubMed

23.

Bruder O, Wagner A, Jensen CJ, Schneider S, Ong P, Kispert EM, Nassenstein K, Schlosser T, Sabin GV, Sechtem U, Mahrholdt H (2010) Myocardial scar visualized by cardiovascular magnetic resonance imaging predicts major adverse events in patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 56(11):875–887CrossRefPubMed

24.

Greulich S, Kindermann I, Schumm J, Perne A, Birkmeier S, Grun S, Ong P, Schaufele T, Klingel K, Schneider S, Kandolf R, Bohm M, Sechtem U, Mahrholdt H (2016) Predictors of outcome in patients with parvovirus B19 positive endomyocardial biopsy. Clin Res Cardiol 105(1):37–52. doi:10.1007/s00392-015-0884-6 CrossRefPubMed

25.

Blankstein R, Waller AH (2016) Evaluation of known or suspected cardiac sarcoidosis. Circ Cardiovasc Imaging 9(3):e000867. doi:10.1161/CIRCIMAGING.113.000867 CrossRefPubMed

26.

Aretz HT (1987) Myocarditis: the Dallas criteria. Hum Pathol 18(6):619–624CrossRefPubMed

27.

Grogan M, Redfield MM, Bailey KR, Reeder GS, Gersh BJ, Edwards WD, Rodeheffer RJ (1995) Long-term outcome of patients with biopsy-proved myocarditis: comparison with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 26(1):80–84CrossRefPubMed

28.

Mason JW, O’Connell JB, Herskowitz A, Rose NR, McManus BM, Billingham ME, Moon TE (1995) A clinical trial of immunosuppressive therapy for myocarditis. The Myocarditis Treatment Trial Investigators. N Engl J Med 333(5):269–275CrossRefPubMed

29.

Kindermann I, Kindermann M, Kandolf R, Klingel K, Bultmann B, Muller T, Lindinger A, Bohm M (2008) Predictors of outcome in patients with suspected myocarditis. Circulation 118(6):639–648CrossRefPubMed

30.

Cooper LT Jr, Berry GJ, Shabetai R (1997) Idiopathic giant-cell myocarditis—natural history and treatment. Multicenter Giant Cell Myocarditis Study Group Investigators. N Engl J Med 336(26):1860–1866CrossRefPubMed

31.

Cooper LT, Baughman KL, Feldman AM, Frustaci A, Jessup M, Kühl U, Levine GN, Narula J, Starling RC, Towbin J, Virmani R (2007) The role of endomyocardial biopsy in the management of cardiovascular disease: a scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. Circulation 116(19):2216–2233CrossRefPubMed

32.

Ekstrom K, Lehtonen J, Kandolin R, Raisanen-Sokolowski A, Salmenkivi K, Kupari M (2016) Long-term outcome and its predictors in giant cell myocarditis. Eur J Heart Fail 18(12):1452–1458. doi:10.1002/ejhf.606 CrossRefPubMed

33.

Noutsias M, Tschope C (2016) Giant cell myocarditis: still a conundrum. The need for a worldwide registry. Eur J Heart Fail 18(12):1459–1461. doi:10.1002/ejhf.648 CrossRefPubMed

34.

Wojnicz R, Nowalany-Kozielska E, Wojciechowska C, Glanowska G, Wilczewski P, Niklewski T, Zembala M, Polonski L, Rozek MM, Wodniecki J (2001) Randomized, placebo-controlled study for immunosuppressive treatment of inflammatory dilated cardiomyopathy: two-year follow-up results. Circulation 104(1):39–45CrossRefPubMed

35.

Frustaci A, Russo MA, Chimenti C (2009) Randomized study on the efficacy of immunosuppressive therapy in patients with virus-negative inflammatory cardiomyopathy: the TIMIC study. Eur Heart J 30(16):1995–2002CrossRefPubMed

36.

Springer TA (1990) Adhesion receptors of the immune system. Nature 346(6283):425–434CrossRefPubMed

37.

Noutsias M, Seeberg B, Schultheiss HP, Kühl U (1999) Expression of cell adhesion molecules in dilated cardiomyopathy: evidence for endothelial activation in inflammatory cardiomyopathy. Circulation 99(16):2124–2131CrossRefPubMed

38.

Noutsias M, Pauschinger M, Ostermann K, Escher F, Blohm JH, Schultheiss H, Kühl U (2002) Digital image analysis system for the quantification of infiltrates and cell adhesion molecules in inflammatory cardiomyopathy. Med Sci Monit 8(5):MT59–MT71PubMed

39.

Noutsias M, Hohmann C, Pauschinger M, Schwimmbeck PL, Ostermann K, Rode U, Yacoub MH, Kühl U, Schultheiss HP (2003) sICAM-1 correlates with myocardial ICAM-1 expression in dilated cardiomyopathy. Int J Cardiol 91(2–3):153–161CrossRefPubMed

40.

Baboonian C, Treasure T (1997) Meta-analysis of the association of enteroviruses with human heart disease. Heart 78(6):539–543CrossRefPubMedPubMedCentral

41.

Fujioka S, Kitaura Y, Ukimura A, Deguchi H, Kawamura K, Isomura T, Suma H, Shimizu A (2000) Evaluation of viral infection in the myocardium of patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 36(6):1920–1926CrossRefPubMed

42.

Norja P, Hokynar K, Aaltonen LM, Chen R, Ranki A, Partio EK, Kiviluoto O, Davidkin I, Leivo T, Eis-Hubinger AM, Schneider B, Fischer HP, Tolba R, Vapalahti O, Vaheri A, Soderlund-Venermo M, Hedman K (2006) Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc Natl Acad Sci U S A 103(19):7450–7453CrossRefPubMedPubMedCentral

43.

Verdonschot J, Hazebroek M, Merken J, Debing Y, Dennert R, Brunner-La Rocca HP, Heymans S (2016) Relevance of cardiac parvovirus B19 in myocarditis and dilated cardiomyopathy: review of the literature. Eur J Heart Fail 18(12):1430–1441. doi:10.1002/ejhf.665 CrossRefPubMed

44.

Kuhl U, Lassner D, von Schlippenbach J, Poller W, Schultheiss HP (2012) Interferon-Beta improves survival in enterovirus-associated cardiomyopathy. J Am Coll Cardiol 60(14):1295–1296. doi:10.1016/j.jacc.2012.06.026 CrossRefPubMed

45.

Zimmermann O, Rodewald C, Radermacher M, Vetter M, Wiehe JM, Bienek-Ziolkowski M, Hombach V, Torzewski J (2010) Interferon beta-1b therapy in chronic viral dilated cardiomyopathy—is there a role for specific therapy? J Card Fail 16(4):348–356CrossRefPubMed

46.

Noutsias M (2016) Myocarditis. In: Maisel AS, Filippatos G (eds) Algorithms in heart failure, vol 1. Jaypee Brothers Medical Publishers (P) Ltd, New Delhi, pp 323–345

47.

Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JG, Coats AJ, Falk V, Gonzalez-Juanatey JR, Harjola VP, Jankowska EA, Jessup M, Linde C, Nihoyannopoulos P, Parissis JT, Pieske B, Riley JP, Rosano GM, Ruilope LM, Ruschitzka F, Rutten FH, van der Meer P, Authors/Task Force M (2016) 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC) developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J 37(27):2129–2200. doi:10.1093/eurheartj/ehw128 CrossRefPubMed

48.

Kasner M, Aleksandrov A, Escher F, Al-Saadi N, Makowski M, Spillmann F, Genger M, Schultheiss HP, Kuhl U, Pieske B, Morris DA, Noutsias M, Tschope C (2017) Multimodality imaging approach in the diagnosis of chronic myocarditis with preserved left ventricular ejection fraction (MCpEF): the role of 2D speckle-tracking echocardiography. Int J Cardiol. doi:10.1016/j.ijcard.2017.05.038

49.

Noutsias M, Pauschinger M, Gross U, Lassner D, Schultheiss HP, Kuhl U (2008) Giant-cell myocarditis in a patient presenting with dilated cardiomyopathy and ventricular tachycardias treated by immunosuppression: a case report. Int J Cardiol 128(2):e58–e59CrossRefPubMed

50.

Kühl U, Pauschinger M, Schwimmbeck PL, Seeberg B, Lober C, Noutsias M, Poller W, Schultheiss HP (2003) Interferon-beta treatment eliminates cardiotropic viruses and improves left ventricular function in patients with myocardial persistence of viral genomes and left ventricular dysfunction. Circulation 107(22):2793–2798CrossRefPubMed

51.

Mayosi BM (2014) Cardiomyopathies: MOGE(S): a standardized classification of cardiomyopathies? Nat Rev Cardiol 11(3):134–135. doi:10.1038/nrcardio.2013.219 CrossRefPubMed

52.

Arbustini E, Narula N, Dec GW, Reddy KS, Greenberg B, Kushwaha S, Marwick T, Pinney S, Bellazzi R, Favalli V, Kramer C, Roberts R, Zoghbi WA, Bonow R, Tavazzi L, Fuster V, Narula J (2014) MOGE(S) nosology in low-to-middle-income countries. Nat Rev Cardiol 11(5):307. doi:10.1038/nrcardio.2013.219-c1 CrossRefPubMed

53.

Bock CT, Klingel K, Kandolf R (2010) Human parvovirus B19-associated myocarditis. N Engl J Med 362(13):1248–1249. doi:10.1056/NEJMc0911362 CrossRefPubMed

54.

Kühl U, Lassner D, Pauschinger M, Gross UM, Seeberg B, Noutsias M, Poller W, Schultheiss HP (2008) Prevalence of erythrovirus genotypes in the myocardium of patients with dilated cardiomyopathy. J Med Virol 80(7):1243–1251CrossRefPubMed

55.

Lindner J, Noutsias M, Lassner D, Wenzel J, Schultheiss HP, Kuehl U, Modrow S (2009) Adaptive immune responses against parvovirus B19 in patients with myocardial disease. J Clin Virol 44(1):27–32CrossRefPubMed

56.

Escher F, Modrow S, Sabi T, Kuhl U, Lassner D, Schultheiss HP, Noutsias M (2008) Parvovirus B19 profiles in patients presenting with acute myocarditis and chronic dilated cardiomyopathy. Med Sci Monit 14(12):CR589–CR597PubMed

57.

Streitz M, Noutsias M, Volkmer R, Rohde M, Brestrich G, Block A, Klippert K, Kotsch K, Ay B, Hummel M, Kühl U, Lassner D, Schultheiss HP, Volk HD, Kern F (2008) NS1 specific CD8+ T-cells with effector function and TRBV11 dominance in a patient with parvovirus B19 associated inflammatory cardiomyopathy. PLoS One 3(6):e2361CrossRefPubMedPubMedCentral

58.

Li Y, Bourlet T, Andreoletti L, Mosnier JF, Peng T, Yang Y, Archard LC, Pozzetto B, Zhang H (2000) Enteroviral capsid protein VP1 is present in myocardial tissues from some patients with myocarditis or dilated cardiomyopathy. Circulation 101(3):231–234CrossRefPubMed

59.

Escher F, Kühl U, Sabi T, Suckau L, Lassner D, Poller W, Schultheiss HP, Noutsias M (2008) Immunohistological detection of Parvovirus B19 capsid proteins in endomyocardial biopsies from dilated cardiomyopathy patients. Med Sci Monit 14(6):CR333–CR338PubMed

Title: The MOGE(S) classification for cardiomyopathies: current status and future outlook
Authors: Julian G. Westphal
Angelos G. Rigopoulos
Constantinos Bakogiannis
Sarah E. Ludwig
Sophie Mavrogeni
Boris Bigalke
Torsten Doenst
Matthias Pauschinger
Carsten Tschöpe
P. Christian Schulze
Michel Noutsias
Publication date: 01-11-2017
Publisher: Springer US
Published in: Heart Failure Reviews / Issue 6/2017
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI: https://doi.org/10.1007/s10741-017-9641-4

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

The MOGE(S) classification for cardiomyopathies: current status and future outlook

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2017

Readmission rate after ultrafiltration in acute decompensated heart failure: a systematic review and meta-analysis

Protein kinase C and cardiac dysfunction: a review

A comprehensive review of the bioenergetics of fatty acid and glucose metabolism in the healthy and failing heart in nondiabetic condition

Human heart failure with preserved ejection versus feline cardiomyopathy: what can we learn from both veterinary and human medicine?

Left ventricular ejection fraction as therapeutic target: is it the ideal marker?

Heart failure with preserved ejection fraction: a nephrologist-directed primer

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page