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Abnormal aortic stiffness in patients with bicuspid aortic valve: phenotypic variation determined by magnetic resonance imaging

  • Thananya BoonyasirinantEmail author
  • Prabhakar Rajiah
  • Scott D. Flamm
Original Paper
  • 87 Downloads

Abstract

The aim of this study was to assess aortic stiffness in patients with bicuspid aortic valve (BAV), and to determine if differences exist among the BAV phenotypes. Stiffness was measured by pulse wave velocity (PWV) determined using velocity-encoded magnetic resonance imaging (VENC-MRI). VENC-MRI was performed in 100 BAV patients and 45 normal controls. PWV was determined between the mid ascending and mid descending aorta. The BAV phenotypes were characterized using steady-state free precession (SSFP) images acquired across the face of the aortic valve, and classified as follows: right-left cusp (R-L) fusion, right and non-coronary cusp (R-NC) fusion, and left and non-coronary cusp (L-NC) fusion. The following BAV phenotypes were identified: 76 R-L, 23 R-NC, and 1 L-NC fusion. BAV patients demonstrated significantly greater PWV compared to normal controls, after adjusting for age (9.16 vs. 3.83 m/s; p < 0.0001). Furthermore, PWV was significantly greater in patients with R-NC fusion than those with R-L fusion phenotype (12.27 vs. 7.97 m/s; p < 0.001). There was significantly increased PWV from VENC-MRI in BAV patients compared to normal controls. Thisis the first to demonstrate the association of different BAV phenotypes and aortic stiffness. VENC-MRI PWV assessment potentially represents a novel parameter for enhanced surveillance and may alter surgical triage of aorta in this high risk group.

Keywords

Bicuspid aortic valve Valve phenotype Aortic stiffness Pulse wave velocity 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Roberts WC (1970) The congenitally bicuspid aortic valve. A study of 85 autopsy cases. Am J Cardiol 26(1):72–83Google Scholar
  2. 2.
    Sabet HY, Edwards WD, Tazelaar HD, Daly RC (1999) Congenitally bicuspid aortic valves: a surgical pathology study of 542 cases (1991 through 1996) and a literature review of 2,715 additional cases. Mayo Clin Proc. 74(1):14–26Google Scholar
  3. 3.
    Basso C, Boschello M, Perrone C, Mecenero A, Cera A, Bicego D et al (2004) An echocardiographic survey of primary school children for bicuspid aortic valve. Am J Cardiol 93(5):661–663Google Scholar
  4. 4.
    Fernandes SM, Sanders SP, Khairy P, Jenkins KJ, Gauvreau K, Lang P et al (2004) Morphology of bicuspid aortic valve in children and adolescents. J Am Coll Cardiol 44(8):1648–1651Google Scholar
  5. 5.
    Friedman T, Mani A, Elefteriades JA (2008) Bicuspid aortic valve: clinical approach and scientific review of a common clinical entity. Expert Rev Cardiovasc Ther 6(2):235–248Google Scholar
  6. 6.
    Tzemos N, Therrien J, Yip J, Thanassoulis G, Tremblay S, Jamorski MT et al (2008) Outcomes in adults with bicuspid aortic valves. JAMA 300(11):1317–1325Google Scholar
  7. 7.
    Michelena HI, Desjardins VA, Avierinos JF, Russo A, Nkomo VT, Sundt TM et al (2008) Natural history of asymptomatic patients with normally functioning or minimally dysfunctional bicuspid aortic valve in the community. Circulation 117(21):2776–2784Google Scholar
  8. 8.
    Forsell C, Bjorck HM, Eriksson P, Franco-Cereceda A, Gasser TC (2014) Biomechanical properties of the thoracic aneurysmal wall: differences between bicuspid aortic valve and tricuspid aortic valve patients. Ann Thorac Surg 98(1):65–71Google Scholar
  9. 9.
    Fernandes SM, Khairy P, Sanders SP, Colan SD (2007) Bicuspid aortic valve morphology and interventions in the young. J Am Coll Cardiol 49(22):2211–2214Google Scholar
  10. 10.
    Ciotti GR, Vlahos AP, Silverman NH (2006) Morphology and function of the bicuspid aortic valve with and without coarctation of the aorta in the young. Am J Cardiol 98(8):1096–1102Google Scholar
  11. 11.
    Schaefer BM, Lewin MB, Stout KK, Gill E, Prueitt A, Byers PH et al (2008) The bicuspid aortic valve: an integrated phenotypic classification of leaflet morphology and aortic root shape. Heart 94(12):1634–1638Google Scholar
  12. 12.
    Della Corte A, Bancone C, Dialetto G, Covino FE, Manduca S, Montibello MV et al (2014) The ascending aorta with bicuspid aortic valve: a phenotypic classification with potential prognostic significance. Eur J Cardiothorac Surg 46(2):240–247 (Discussion 7)Google Scholar
  13. 13.
    Della Corte A, Bancone C, Buonocore M, Dialetto G, Covino FE, Manduca S et al (2013) Pattern of ascending aortic dimensions predicts the growth rate of the aorta in patients with bicuspid aortic valve. JACC Cardiovasc Imaging 6(12):1301–1310Google Scholar
  14. 14.
    Groenink M, de Roos A, Mulder BJ, Verbeeten B Jr, Timmermans J, Zwinderman AH et al (2001) Biophysical properties of the normal-sized aorta in patients with Marfan syndrome: evaluation with MR flow mapping. Radiology 219(2):535–540Google Scholar
  15. 15.
    Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D et al (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27(21):2588–2605Google Scholar
  16. 16.
    Nistri S, Grande-Allen J, Noale M, Basso C, Siviero P, Maggi S et al (2008) Aortic elasticity and size in bicuspid aortic valve syndrome. Eur Heart J 29(4):472–479Google Scholar
  17. 17.
    Schaefer BM, Lewin MB, Stout KK, Byers PH, Otto CM (2007) Usefulness of bicuspid aortic valve phenotype to predict elastic properties of the ascending aorta. Am J Cardiol 99(5):686–690Google Scholar
  18. 18.
    Nistri S, Sorbo MD, Basso C, Thiene G (2002) Bicuspid aortic valve: abnormal aortic elastic properties. J Heart Valve Dis 11(3):369–373 (Discussion 73–74)Google Scholar
  19. 19.
    Yap SC, Nemes A, Meijboom FJ, Galema TW, Geleijnse ML, ten Cate FJ et al (2008) Abnormal aortic elastic properties in adults with congenital valvular aortic stenosis. Int J Cardiol 128(3):336–341Google Scholar
  20. 20.
    Nollen GJ, Groenink M, Tijssen JG, Van Der Wall EE, Mulder BJ (2004) Aortic stiffness and diameter predict progressive aortic dilatation in patients with Marfan syndrome. Eur Heart J 25(13):1146–1152Google Scholar
  21. 21.
    Grotenhuis HB, Ottenkamp J, Westenberg JJ, Bax JJ, Kroft LJ, de Roos A (2007) Reduced aortic elasticity and dilatation are associated with aortic regurgitation and left ventricular hypertrophy in nonstenotic bicuspid aortic valve patients. J Am Coll Cardiol 49(15):1660–1665Google Scholar
  22. 22.
    Rogers WJ, Hu YL, Coast D, Vido DA, Kramer CM, Pyeritz RE et al (2001) Age-associated changes in regional aortic pulse wave velocity. J Am Coll Cardiol 38(4):1123–1129Google Scholar
  23. 23.
    Petersen SE, Wiesmann F, Hudsmith LE, Robson MD, Francis JM, Selvanayagam JB et al (2006) Functional and structural vascular remodeling in elite rowers assessed by cardiovascular magnetic resonance. J Am Coll Cardiol 48(4):790–797Google Scholar
  24. 24.
    van der Meer RW, Diamant M, Westenberg JJ, Doornbos J, Bax JJ, de Roos A et al (2007) Magnetic resonance assessment of aortic pulse wave velocity, aortic distensibility, and cardiac function in uncomplicated type 2 diabetes mellitus. J Cardiovasc Magn Reson 9(4):645–651Google Scholar
  25. 25.
    Stevanov M, Baruthio J, Gounot D, Grucker D (2001) In vitro validation of MR measurements of arterial pulse-wave velocity in the presence of reflected waves. J Magn Reson Imaging 14(2):120–127Google Scholar
  26. 26.
    Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1(8476):307–310Google Scholar
  27. 27.
    Ward C (2000) Clinical significance of the bicuspid aortic valve. Heart 83(1):81–85Google Scholar
  28. 28.
    Fedak PW, Verma S, David TE, Leask RL, Weisel RD, Butany J (2002) Clinical and pathophysiological implications of a bicuspid aortic valve. Circulation 106(8):900–904Google Scholar
  29. 29.
    Keane MG, Wiegers SE, Plappert T, Pochettino A, Bavaria JE, Sutton MG (2000) Bicuspid aortic valves are associated with aortic dilatation out of proportion to coexistent valvular lesions. Circulation 102(19 Suppl 3):III35–III39Google Scholar
  30. 30.
    Ferencik M, Pape LA (2003) Changes in size of ascending aorta and aortic valve function with time in patients with congenitally bicuspid aortic valves. Am J Cardiol 92(1):43–46Google Scholar
  31. 31.
    Cecconi M, Manfrin M, Moraca A, Zanoli R, Colonna PL, Bettuzzi MG et al (2005) Aortic dimensions in patients with bicuspid aortic valve without significant valve dysfunction. Am J Cardiol 95(2):292–294Google Scholar
  32. 32.
    Beroukhim RS, Kruzick TL, Taylor AL, Gao D, Yetman AT (2006) Progression of aortic dilation in children with a functionally normal bicuspid aortic valve. Am J Cardiol 98(6):828–830Google Scholar
  33. 33.
    Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127(8):1607–1616Google Scholar
  34. 34.
    Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130(25):6361–6374Google Scholar
  35. 35.
    McKusick VA (1972) Association of congenital bicuspid aortic valve and erdheim’s cystic medial necrosis. Lancet 1(7758):1026–1027Google Scholar
  36. 36.
    Niwa K, Perloff JK, Bhuta SM, Laks H, Drinkwater DC, Child JS et al (2001) Structural abnormalities of great arterial walls in congenital heart disease: light and electron microscopic analyses. Circulation 103(3):393–400Google Scholar
  37. 37.
    Bonderman D, Gharehbaghi-Schnell E, Wollenek G, Maurer G, Baumgartner H, Lang IM (1999) Mechanisms underlying aortic dilatation in congenital aortic valve malformation. Circulation 99(16):2138–2143Google Scholar
  38. 38.
    Shin HJ, Shin JK, Chee HK, Kim JS, Ko SM (2015) Characteristics of aortic valve dysfunction and ascending aorta dimensions according to bicuspid aortic valve morphology. Eur Radiol 25(7):2103–2114Google Scholar
  39. 39.
    Warner PJ, Al-Quthami A, Brooks EL, Kelley-Hedgepeth A, Patvardhan E, Kuvin JT et al (2013) Augmentation index and aortic stiffness in bicuspid aortic valve patients with non-dilated proximal aortas. BMC Cardiovasc Disord 13:19Google Scholar
  40. 40.
    Karamanoglu M (2003) Errors in estimating propagation distances in pulse wave velocity. Hypertension 41(6):e8.Google Scholar
  41. 41.
    Yener N, Oktar GL, Erer D, Yardimci MM, Yener A (2002) Bicuspid aortic valve. Ann Thorac Cardiovasc Surg 8(5):264–267Google Scholar
  42. 42.
    Pachulski RT, Chan KL (1993) Progression of aortic valve dysfunction in 51 adult patients with congenital bicuspid aortic valve: assessment and follow up by Doppler echocardiography. Br Heart J 69(3):237–240Google Scholar
  43. 43.
    Della Corte A, Bancone C, Dialetto G, Covino FE, Manduca S, D’Oria V et al (2014) Towards an individualized approach to bicuspid aortopathy: different valve types have unique determinants of aortic dilatation. Eur J Cardiothorac Surg 45(4):e118–e124 (Discussion e24)Google Scholar
  44. 44.
    Pees C, Michel-Behnke I (2012) Morphology of the bicuspid aortic valve and elasticity of the adjacent aorta in children. Am J Cardiol 110(9):1354–1360Google Scholar
  45. 45.
    Koenraadt WM, Grewal N, Gaidoukevitch OY, DeRuiter MC, Gittenberger-de Groot AC, Bartelings MM et al (2016) The extent of the raphe in bicuspid aortic valves is associated with aortic regurgitation and aortic root dilatation. Neth Heart J 24(2):127–133Google Scholar
  46. 46.
    Bissell MM, Hess AT, Biasiolli L, Glaze SJ, Loudon M, Pitcher A et al (2013) Aortic dilation in bicuspid aortic valve disease: flow pattern is a major contributor and differs with valve fusion type. Circ Cardiovasc Imaging 6(4):499–507Google Scholar
  47. 47.
    Mahadevia R, Barker AJ, Schnell S, Entezari P, Kansal P, Fedak PW et al (2014) Bicuspid aortic cusp fusion morphology alters aortic three-dimensional outflow patterns, wall shear stress, and expression of aortopathy. Circulation 129(6):673–682Google Scholar
  48. 48.
    Hope MD, Hope TA, Meadows AK, Ordovas KG, Urbania TH, Alley MT et al (2010) Bicuspid aortic valve: four-dimensional MR evaluation of ascending aortic systolic flow patterns. Radiology 255(1):53–61Google Scholar
  49. 49.
    Nistri S, Sorbo MD, Marin M, Palisi M, Scognamiglio R, Thiene G (1999) Aortic root dilatation in young men with normally functioning bicuspid aortic valves. Heart 82(1):19–22Google Scholar
  50. 50.
    Larson EW, Edwards WD (1984) Risk factors for aortic dissection: a necropsy study of 161 cases. Am J Cardiol 53(6):849–855Google Scholar
  51. 51.
    Hardikar AA, Marwick TH (2013) Surgical thresholds for bicuspid aortic valve associated aortopathy. JACC Cardiovasc Imaging 6(12):1311–1320Google Scholar
  52. 52.
    Adamo L, Braverman AC (2015) Surgical threshold for bicuspid aortic valve aneurysm: a case for individual decision-making. Heart 101(17):1361–1367Google Scholar
  53. 53.
    Hiratzka LF, Creager MA, Isselbacher EM, Svensson LG, Nishimura RA, Bonow RO et al (2016) Surgery for aortic dilatation in patients with bicuspid aortic valves: a statement of clarification from the American College of Cardiology/American Heart Association task force on clinical practice guidelines. J Am Coll Cardiol 67(6):724–731Google Scholar
  54. 54.
    Nishimura RA, Otto CM, Bonow RO, Carabello BA, Erwin JP 3rd, Guyton RA et al (2014) 2014 AHA/ACC guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on practice guidelines. Circulation 129(23):e521–e643Google Scholar
  55. 55.
    Joint Task Force on the Management of Valvular Heart Disease of the European Society of Cardiology, European Association for Cardio-Thoracic Surgery, Vahanian A, Alfieri O, Andreotti F, Antunes MJ et al (2012) Guidelines on the management of valvular heart disease (version 2012). Eur Heart J 33(19):2451–2496Google Scholar
  56. 56.
    Yasuda H, Nakatani S, Stugaard M, Tsujita-Kuroda Y, Bando K, Kobayashi J et al (2003) Failure to prevent progressive dilation of ascending aorta by aortic valve replacement in patients with bicuspid aortic valve: comparison with tricuspid aortic valve. Circulation 108(Suppl 1):II291–I4Google Scholar
  57. 57.
    Bonow RO, Carabello BA, Chatterjee K, de Leon AC Jr, Faxon DP, Freed MD et al (2008) 2008 Focused update incorporated into the ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on practice guidelines (Writing Committee to Revise the 1998 Guidelines for the Management of Patients With Valvular Heart Disease): endorsed by the Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. Circulation 118(15):e523–e661Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Thananya Boonyasirinant
    • 1
    • 2
    Email author
  • Prabhakar Rajiah
    • 1
  • Scott D. Flamm
    • 1
    • 3
  1. 1.Cardiovascular Imaging LaboratoryImaging InstituteClevelandUSA
  2. 2.Division of Cardiology, Department of Internal Medicine, Siriraj HospitalMahidol UniversityBangkokThailand
  3. 3.Cardiovascular MedicineHeart and Vascular Institute, Cleveland ClinicClevelandUSA

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