Histopathology of aortic complications in bicuspid aortic valve versus Marfan syndrome: relevance for therapy?

Heart and Vessels

Volumn 31, Issue 5, 2016, Pages 795-806

  Grewal, Nimrat ^a   Franken, Romy ^b   Mulder, Barbara J M ^b   Goumans, Marie José ^a   Lindeman, Johannes H N ^a   Jongbloed, Monique R M ^a   DeRuiter, Marco C ^a   Klautz, Robert J M ^a   Bogers, Ad J J C ^c   Poelmann, Robert E ^a   Groot, Adriana C Gittenberger de ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Aneurysm; Aorta; Immunohistochemistry; Molecular biology; Pathology

Indexed keywords

FIBRILLIN 1; LAMIN A; LAMIN C; STEM CELL FACTOR; BIOLOGICAL MARKER; FBN1 PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR;

ADULT; AGED; AGING; AGING LIKE INFLAMMATION; AORTA DISEASE; AORTA DISSECTION; AORTIC DILATION; APOPTOSIS; ARTICLE; ASCENDING AORTIC WALL BIOPSY; BICUSPID AORTIC VALVE; BIOPSY TECHNIQUE; CARDIOVASCULAR AGING; CELL DEGENERATION; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOLYSIS; CYTOLYTIC NECROSIS; DISEASE ASSOCIATION; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MARFAN SYNDROME; MIDDLE AGED; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VASCULAR SMOOTH MUSCLE CELL; ABNORMALITIES; ANEURYSM, DISSECTING; AORTA; AORTA VALVE; AORTIC ANEURYSM; BIOPSY; CHEMISTRY; COMPLICATION; IMMUNOHISTOCHEMISTRY; LESIONS AND DEFECTS; METABOLISM; NECROSIS; PATHOLOGY; VALVULAR HEART DISEASE; VASCULAR SMOOTH MUSCLE; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANEURYSM, DISSECTING; AORTA; AORTIC ANEURYSM; AORTIC VALVE; APOPTOSIS; BIOMARKERS; BIOPSY; DILATATION, PATHOLOGIC; FEMALE; FIBRILLIN-1; HEART VALVE DISEASES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MARFAN SYNDROME; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; NECROSIS; PROTO-ONCOGENE PROTEINS C-KIT; YOUNG ADULT;

EID: 84934776998     PISSN: 09108327     EISSN: 16152573     Source Type: Journal    
DOI: 10.1007/s00380-015-0703-z     Document Type: Article

References (39)

1. Huntington K, Hunter AG, Chan KL (1997) A prospective study to assess the frequency of familial clustering of congenital bicuspid aortic valve. J Am Coll Cardiol 30:1809–1812
2. Loeys BL, Dietz HC, Braverman AC, Callewaert BL, De BJ, Devereux RB, Hilhorst-Hofstee Y, Jondeau G, Faivre L, Milewicz DM, Pyeritz RE, Sponseller PD, Wordsworth P, De Paepe AM (2010) The revised Ghent nosology for the Marfan syndrome. J Med Genet 47:476–485
3. Jeremy RW, Huang H, Hwa J, McCarron H, Hughes CF, Richards JG (1994) Relation between age, arterial distensibility, and aortic dilatation in the Marfan syndrome. Am J Cardiol 74:369–373
4. Detaint D, Michelena HI, Nkomo VT, Vahanian A, Jondeau G, Sarano ME (2014) Aortic dilatation patterns and rates in adults with bicuspid aortic valves: a comparative study with Marfan syndrome and degenerative aortopathy. Heart 100:126–134
5. Grewal N, Gittenberger-de Groot AC, Poelmann RE, Klautz RJ, Lindeman JH, Goumans MJ, Palmen M, Mohamed SA, Sievers HH, Bogers AJ, DeRuiter MC (2014) Ascending aorta dilation in association with bicuspid aortic valve: a maturation defect of the aortic wall. J Thorac Cardiovasc Surg 148(4):1583–1590
6. Grewal N, Gittenberger-de-Groot AC, DeRuiter MC, Klautz RJM, Poelmann RE, Duim SN, Lindeman JHN, Koenraadt WMC, Jongbloed MRM, Mohamed SA, Sievers HH, Bogers AJJC, Goumans MJ (2014) Bicuspid aortic valve: phosphorylation of c-Kit and downstream targets are prognostic for future aortopathy. Eur J Card Thor Surg 46(5):831–839
7. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, Watanabe T (2003) Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation 108(Suppl 1):II329–II334
8. Fedak PW, de Sa MP, Verma S, Nili N, Kazemian P, Butany J, Strauss BH, Weisel RD, David TE (2003) Vascular matrix remodeling in patients with bicuspid aortic valve malformations: implications for aortic dilatation. J Thorac Cardiovasc Surg 126:797–806
9. Nistri S, Porciani MC, Attanasio M, Abbate R, Gensini GF, Pepe G (2012) Association of Marfan syndrome and bicuspid aortic valve: frequency and outcome. Int J Cardiol 155:324–325
10. Michelena HI, Khanna AD, Mahoney D, Margaryan E, Topilsky Y, Suri RM, Eidem B, Edwards WD, Sundt TM III, Enriquez-Sarano M (2011) Incidence of aortic complications in patients with bicuspid aortic valves. JAMA 306:1104–1112
11. Tzemos N, Therrien J, Yip J, Thanassoulis G, Tremblay S, Jamorski MT, Webb GD, Siu SC (2008) Outcomes in adults with bicuspid aortic valves. JAMA 300:1317–1325
12. Brooke BS, Habashi JP, Judge DP, Patel N, Loeys B, Dietz HC (2008) Angiotensin II blockade and aortic-root dilation in Marfan’s syndrome. N Engl J Med 358(26):2787–2795
13. Gambarin FI, Favalli V, Serio A, Regazzi M, Pasotti M, Klersy C, Dore R, Mannarino S, Vigano M, Odero A, Amato S, Tavazzi L, Arbustini E (2009) Rationale and design of a trial evaluating the effects of losartan vs. nebivolol vs. the association of both on the progression of aortic root dilation in Marfan syndrome with FBN1 gene mutations. J Cardiovasc Med (Hagerstown) 10(4):354–362
14. Detaint D, Aegerter P, Tubach F, Hoffman I, Plauchu H, Dulac Y, Faivre LO, Delrue MA, Collignon P, Odent S, Tchitchinadze M, Bouffard C, Arnoult F, Gautier M, Boileau C, Jondeau G (2010) Rationale and design of a randomized clinical trial (Marfan Sartan) of angiotensin II receptor blocker therapy versus placebo in individuals with Marfan syndrome. Arch Cardiovasc Dis 103(5):317–325
15. Radonic T, de Witte P, Baars MJ, Zwinderman AH, Mulder BJ, Groenink M (2010) Losartan therapy in adults with Marfan syndrome: study protocol of the multi-center randomized controlled COMPARE trial. Trials 11:3–11
16. Moberg K, De NS, Devos D, Goetghebeur E, Segers P, Trachet B, Vervaet C, Renard M, Coucke P, Loeys B, De PA, De BJ (2012) The Ghent Marfan trial—a randomized, double-blind placebo controlled trial with losartan in Marfan patients treated with beta-blockers. Int J Cardiol 157(3):354–358
17. Groenink M, den Hartog AW, Franken R, Radonic T, de Waard V, Timmermans J, Scholte AJ, van den Berg MP, Spijkerboer AM, Marquering HA, Zwinderman AH, Mulder BJ (2013) Losartan reduces aortic dilatation rate in adults with Marfan syndrome: a randomized controlled trial. Eur Heart J 34(45):3491–3500
18. Chiu HH, Wu MH, Wang JK, Lu CW, Chiu SN, Chen CA, Lin MT, Hu FC (2013) Losartan added to beta-blockade therapy for aortic root dilation in Marfan syndrome: a randomized, open-label pilot study. Mayo Clin Proc 88(3):271–276
19. Ohnemus D, Oster ME, Gatlin S, Jokhadar M, Mahle WT (2015) The effect of angiotensin-converting enzyme inhibitors on the rate of ascending aorta dilation in patients with bicuspid aortal valve. Congenit Heart Dis 10(1):E1–E5
20. Hiratzka LF, Bakris GL, Beckman JA, Bersin RM, Carr VF, Casey DE Jr, Eagle KA, Hermann LK, Isselbacher EM, Kazerooni EA, Kouchoukos NT, Lytle BW, Milewicz DM, Reich DL, Sen S, Shinn JA, Svensson LG, Williams DM (2010) 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with thoracic aortic disease: executive summary. A report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. Catheter Cardiovasc Interv 76:E43–E86
21. DeRuiter MC, Rensen SS, Coolen GP, Hierck BP, Bergwerff M, Debie WM, Gittenberger-de Groot AC, Van Eys GJ (2001) Smoothelin expression during chicken embryogenesis: detection of an embryonic isoform. Dev Dyn 221:460–463
22. Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD, Kennedy BK (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 20:486–500
23. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801
24. Niwa K, Perloff JK, Bhuta SM, Laks H, Drinkwater DC, Child JS, Miner PD (2001) Structural abnormalities of great arterial walls in congenital heart disease: light and electron microscopic analyses. Circulation 103:393–400
25. Girdauskas E, Disha K, Secknus M, Borger M, Kuntze T (2013) Increased risk of late aortic events after isolated aortic valve replacement in patients with bicuspid aortic valve insufficiency versus stenosis. J Cardiovasc Surg (Torino) 54(5):653–659
26. Wang Y, Wu B, Dong L, Wang C, Wang X, Shu X (2014) Circulating matrix metalloproteinase patterns in association with aortic dilatation in bicuspid aortic valve patients with isolated severe aortic stenosis. Heart Vessels. doi:10.1007/s00380-014-0593-5
27. Grewal N, DeRuiter MC, Jongbloed MR, Goumans MJ, Klautz RJ, Poelmann RE, Gittenberger-de Groot AC (2014) Normal and abnormal development of the aortic wall and valve: correlation with clinical entities. Neth Heart J 22:363–369
28. Matthias Bechtel JF, Noack F, Sayk F, Erasmi AW, Bartels C, Sievers HH (2003) Histopathological grading of ascending aortic aneurysm: comparison of patients with bicuspid versus tricuspid aortic valve. J Heart Valve Dis 12:54–59
29. Collins MJ, Dev V, Strauss BH, Fedak PW, Butany J (2008) Variation in the histopathological features of patients with ascending aortic aneurysms: a study of 111 surgically excised cases. J Clin Pathol 61:519–523
30. Fedak PW, Verma S, David TE, Leask RL, Weisel RD, Butany J (2002) Clinical and pathophysiological implications of a bicuspid aortic valve. Circulation 106:900–904
31. Pepe G, Nistri S, Giusti B, Sticchi E, Attanasio M, Porciani C, Abbate R, Bonow RO, Yacoub M, Gensini GF (2014) Identification of fibrillin 1 gene mutations in patients with bicuspid aortic valve (BAV) without Marfan syndrome. BMC Med Genet 15:23
32. Dietz HC, Pyeritz RE (1995) Mutations in the human gene for fibrillin-1 (FBN1) in the Marfan syndrome and related disorders. Hum Mol Genet 4:1799–1809
33. Kielty CM, Shuttleworth CA (1993) Synthesis and assembly of fibrillin by fibroblasts and smooth muscle cells. J Cell Sci 106(Pt 1):167–173
34. Milewicz DM, Pyeritz RE, Crawford ES, Byers PH (1992) Marfan syndrome: defective synthesis, secretion, and extracellular matrix formation of fibrillin by cultured dermal fibroblasts. J Clin Invest 89(1):79–86
35. Hollister DW, Godfrey M, Sakai LY, Pyeritz RE (1990) Immunohistologic abnormalities of the microfibrillar-fiber system in the Marfan syndrome. N Engl J Med 323(3):152–159
36. Bokenkamp R, Raz V, Venema A, DeRuiter MC, van Munsteren C, Olive M, Nabel EG, Gittenberger-de Groot AC (2011) Differential temporal and spatial progerin expression during closure of the ductus arteriosus in neonates. PLoS One 6:e23975
37. Nagashima H, Sakomura Y, Aoka Y, Uto K, Kameyama K, Ogawa M, Aomi S, Koyanagi H, Ishizuka N, Naruse M, Kawana M, Kasanuki H (2001) Angiotensin II type 2 receptor mediates vascular smooth muscle cell apoptosis in cystic medial degeneration associated with Marfan’s syndrome. Circulation 104(12 Suppl 1):I282–I287
38. Milewicz DM (1994) Identification of defects in the fibrillin gene and protein in individuals with the Marfan syndrome and related disorders. Tex Heart Inst J 21(1):22–29
39. Kagami S, Border WA, Miller DE, Noble NA (1994) Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest 93:2431–2437