Abstract
Mitral valve (MV) closure depends upon the proper function of each component of the valve apparatus, which includes the annulus, leaflets, and chordae tendineae (CT). Geometry plays a major role in MV mechanics and thus highly impacts the accuracy of computational models simulating MV function and repair. While the physiological geometry of the leaflets and annulus have been previously investigated, little effort has been made to quantitatively and objectively describe CT geometry. The CT constitute a fibrous tendon-like structure projecting from the papillary muscles (PMs) to the leaflets, thereby evenly distributing the loads placed on the MV during closure. Because CT play a major role in determining the shape and stress state of the MV as a whole, their geometry must be well characterized. In the present work, a novel and comprehensive investigation of MV CT geometry was performed to more fully quantify CT anatomy. In vitro micro-tomography 3D images of ovine MVs were acquired, segmented, then analyzed using a curve-skeleton transform. The resulting data was used to construct B-spline geometric representations of the CT structures, enriched with a continuous field of cross-sectional area (CSA) data. Next, Reeb graph models were developed to analyze overall topological patterns, along with dimensional attributes such as segment lengths, 3D orientations, and CSA. Reeb graph results revealed that the topology of ovine MV CT followed a full binary tree structure. Moreover, individual chords are mostly planar geometries that together form a 3D load-bearing support for the MV leaflets. We further demonstrated that, unlike flow-based branching patterns, while individual CT branches became thinner as they propagated further away from the PM heads towards the leaflets, the total CSA almost doubled. Overall, our findings indicate a certain level of regularity in structure, and suggest that population-based MV CT geometric models can be generated to improve current MV repair procedures.
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Abbreviations
- MV:
-
Mitral valve
- LV:
-
Left ventricle
- PM:
-
Papillary muscle
- CSA:
-
Cross sectional area
- Micro-CT:
-
Micro computed tomography
- TVP:
-
Trans-valvular pressure
- MLE:
-
Maximum likelihood estimation
References
Biasotti, S., D. Giorgi, M. Spagnuolo, and B. Falcidieno. Reeb graphs for shape analysis and applications. Theor. Comput. Sci. 392(1):5–22, 2008.
Bloodworth, C. H., E. L. Pierce, T. F. Easley, A. Drach, A. H. Khalighi, M. Toma, M. O. Jensen, M. S. Sacks, and A. P. Yoganathan. Ex vivo methods for informing computational models of the mitral valve. Ann. Biomed. Eng. 1–12, 2016.
Bouma, W., E. K. Lai, M. M. Levack, E. K. Shang, A. M. Pouch, T. J. Eperjesi, T. J. Plappert, P. A. Yushkevich, M. A. Mariani, K. R. Khabbaz, T. G. Gleason, F. Mahmood, M. A. Acker, Y. J. Woo, A. T. Cheung, B. M. Jackson, J. H. Gorman, 3rd, and R. C. Gorman. Preoperative three-dimensional valve analysis predicts recurrent ischemic mitral regurgitation after mitral annuloplasty. Ann. Thorac. Surg. 101(2):567–575, 2016.
Braunberger, E., A. Deloche, A. Berrebi, F. Abdallah, J. A. Celestin, P. Meimoun, G. Chatellier, S. Chauvaud, J. N. Fabiani, and A. Carpentier. Very long-term results (more than 20 years) of valve repair with carpentier’s techniques in nonrheumatic mitral valve insufficiency. Circulation 104(12 Suppl 1):I8–I11, 2001.
Caiani, E. G., L. Fusini, F. Veronesi, G. Tamborini, F. Maffessanti, P. Gripari, C. Corsi, M. Naliato, M. Zanobini, and F. Alamanni. Quantification of mitral annulus dynamic morphology in patients with mitral valve prolapse undergoing repair and annuloplasty during a 6-month follow-up. Eur. Heart J.-Cardiovasc. Imaging jer016, 2011.
Casado, J. A., S. Diego, D. Ferreño, E. Ruiz, I. Carrascal, D. Méndez, J. M. Revuelta, A. Pontón, J. M. Icardo, and F. Gutiérrez-Solana. Determination of the mechanical properties of normal and calcified human mitral chordae tendineae. J. Mech. Behav. Biomed. Mater. 13:1–13, 2012.
Chikwe, J., and D. H. Adams. State of the art: degenerative mitral valve disease. Heart, Lung Circ. 18(5):319–329, 2009.
Ciarka, A., and N. Van de Veire. Secondary mitral regurgitation: pathophysiology, diagnosis, and treatment. Heart 97(12):1012–1023, 2011.
d’Arcy, J., B. Prendergast, J. Chambers, S. Ray, and B. Bridgewater. Valvular heart disease: the next cardiac epidemic. Heart 97(2):91–93, 2011.
Dal-Bianco, J. P., E. Aikawa, J. Bischoff, J. L. Guerrero, M. D. Handschumacher, S. Sullivan, B. Johnson, J. S. Titus, Y. Iwamoto, J. Wylie-Sears, R. A. Levine, and A. Carpentier. Active adaptation of the tethered mitral valve: insights into a compensatory mechanism for functional mitral regurgitation. Circulation 120(4):334–342, 2009.
David, T. E., S. Armstrong, B. W. McCrindle, and C. Manlhiot. Late outcomes of mitral valve repair for mitral regurgitation due to degenerative disease. Circulation: CIRCULATIONAHA, 112.000699, 2013.
Espino, D. M., D. Shepherd, D. Hukins, and K. G. Buchan. The role of Chordae tendineae in mitral valve competence. J. Heart Valve Dis. 14(5):603–609, 2005.
Faletra, F. F., G. Pedrazzini, E. Pasotti, I. Petrova, A. Drasutiene, M. C. Dequarti, S. Muzzarelli, and T. Moccetti. Role of real-time three dimensional transoesophageal echocardiography as guidance imaging modality during catheter based edge-to-edge mitral valve repair. Heart 99(16):1204–1215, 2013.
Gabbay, U., and C. Yosefy. The underlying causes of chordae tendinae rupture: a systematic review. Int. J. Cardiol. 143(2):113–118, 2010.
Grbic, S., T. F. Easley, T. Mansi, C. H. Bloodworth, E. L. Pierce, I. Voigt, D. Neumann, J. Krebs, D. D. Yuh, and M. O. Jensen. Multi-modal validation framework of mitral valve geometry and functional computational models. Stat. Atlases Comput. Models Heart-Imaging Model. Chall., pp. 239–248, 2015
Gunnal, S., R. Wabale, and M. Farooqui. Morphological study of chordae tendinae in human cadaveric hearts. Heart Views: Off. J. Gulf Heart Assoc. 16(1):1, 2015.
Gunning, G. M., and B. P. Murphy. Characterisation of the fatigue life, dynamic creep and modes of damage accumulation within mitral valve chordae tendineae. Acta Biomater. 24:193–200, 2015.
He, S., M. W. Weston, J. Lemmon, M. Jensen, R. A. Levine, and A. P. Yoganathan. Geometric distribution of chordae tendineae: an important anatomic feature in mitral valve function. J. Heart Valve Dis. 9(4):495–501, 2000; (discussion 502–3).
Hutchison, J., and P. Rea. A comparative study of the morphology of mammalian true chordae tendineae of the atrioventricular valves. J. Morphol. 32(2):71–77, 2015.
Ibrahim, M., C. Rao, and T. Athanasiou. Artificial chordae for degenerative mitral valve disease: critical analysis of current techniques. Interact. Cardiovasc. Thorac. Surg. 15(6):1019–1032, 2012.
Jassar, A. S., M. Vergnat, B. M. Jackson, J. R. McGarvey, A. T. Cheung, G. Ferrari, Y. J. Woo, M. A. Acker, R. C. Gorman, and J. H. Gorman. Regional annular geometry in patients with mitral regurgitation: implications for annuloplasty ring selection. Ann. Thorac. Surg. 97(1):64–70, 2014.
Khalighi, A. H., A. Drach, F. M. ter Huurne, C.-H. Lee, C. Bloodworth, E. L. Pierce, M. O. Jensen, A. P. Yoganathan, and M. S. Sacks. A comprehensive framework for the characterization of the complete mitral valve geometry for the development of a population-averaged model. Funct. Imaging Model. Heart, 164–171, 2015
Lee, C. H., C. A. Carruthers, S. Ayoub, R. C. Gorman, J. H. Gorman, 3rd, and M. S. Sacks. Quantification and simulation of layer-specific mitral valve interstitial cells deformation under physiological loading. J. Theor. Biol. 373:26, 2015.
Lee, C. H., J. P. Rabbah, A. P. Yoganathan, R. C. Gorman, J. H. Gorman, 3rd, and M. S. Sacks. On the effects of leaflet microstructure and constitutive model on the closing behavior of the mitral valve. Biomech. Model. Mechanobiol. 14:1281, 2015.
Liao, J., and I. Vesely. A structural basis for the size-related mechanical properties of mitral valve chordae tendineae. J. Biomech. 36(8):1125–1133, 2003.
Lomholt, M., S. L. Nielsen, S. Hansen, N. T. Andersen, and J. M. Hasenkam. Differential tension between secondary and primary mitral chordae in an acute in vivo porcine model. J. Heart Valve Dis. 11(3):337–345, 2002.
Malladi, R., and J. A. Sethian. Image processing via level set curvature flow. Proc. Natl. Acad. Sci. USA 92(15):7046–7050, 1995.
Messas, E., J. L. Guerrero, M. D. Handschumacher, C. Conrad, C. M. Chow, S. Sullivan, A. P. Yoganathan, and R. A. Levine. Chordal cutting: a new therapeutic approach for ischemic mitral regurgitation. Circulation 104(16):1958–1963, 2001.
Millington-Sanders, C., A. Meir, L. Lawrence, and C. Stolinski. Structure of chordae tendineae in the left ventricle of the human heart. J. Anat. 192(04):573–581, 1998.
Neely, R. C., M. Leacche, C. R. Byrne, A. V. Norman, and J. G. Byrne. New approaches to cardiovascular surgery. Curr. Probl. Cardiol. 39(12):427–466, 2014.
Osmundson, P. J., J. A. Callahan, and J. E. Edwards. Ruptured mitral chordae tendineae. Circulation 23(1):42–54, 1961.
Owais, K., M. Montealegre-Gallegos, J. Jeganathan, R. Matyal, K. R. Khabbaz, and F. Mahmood. Dynamic changes in the ischemic mitral annulus: implications for ring sizing. Ann. Card. Anaesth. 19(1):15, 2016.
Pham, T., and W. Sun. Material properties of aged human mitral valve leaflets. J. Biomed. Mater. Res. Part A 102(8):2692–2703, 2014.
Piegl, L., and W. Tiller. The NURBS Book. New York: Springer, 1997.
Rabbah, J.-P., N. Saikrishnan, and A. P. Yoganathan. A novel left heart simulator for the multi-modality characterization of native mitral valve geometry and fluid mechanics. Ann. Biomed. Eng. 41(2):305–315, 2013.
Rao, C., J. Hart, A. Chow, F. Siannis, P. Tsalafouta, B. Murtuza, A. Darzi, F. C. Wells, and T. Athanasiou. Does preservation of the sub-valvular apparatus during mitral valve replacement affect long-term survival and quality of life? A microsimulation study. J. Cardiothorac. Surg. 3(1):17, 2008.
Ritchie, J., J. Jimenez, Z. He, M. S. Sacks, and A. P. Yoganathan. The material properties of the native porcine mitral valve chordae tendineae: an in vitro investigation. J. Biomech. 39(6):1129–1135, 2006.
Siefert, A. W., J. P. M. Rabbah, K. J. Koomalsingh, S. A. Touchton, N. Saikrishnan, J. R. McGarvey, R. C. Gorman, J. H. Gorman, and A. P. Yoganathan. In vitro mitral valve simulator mimics systolic valvular function of chronic ischemic mitral regurgitation ovine model. Ann. Thorac. Surg. 95(3):825–830, 2013.
Sousa, U. M., P. Grare, V. Jebara, J. Fuzelier, M. Portoghese, C. Acar, J. Relland, S. Mihaileanu, J. Fabiani, and A. Carpentier. Transposition of chordae in mitral valve repair. Mid-term results. Circulation 88(5 Pt 2):II35–II38, 1993.
Tagliasacchi, A. Skeletal representations and applications. arXiv preprint arXiv:1301.6809, 2013.
Team, R. C. R: a language and environment for statistical computing, 2013.
Thom, T., N. Haase, W. Rosamond, V. J. Howard, J. Rumsfeld, T. Manolio, Z. J. Zheng, K. Flegal, C. O’Donnell, S. Kittner, D. Lloyd-Jones, D. C. Goff, Jr, Y. Hong, R. Adams, G. Friday, K. Furie, P. Gorelick, B. Kissela, J. Marler, J. Meigs, V. Roger, S. Sidney, P. Sorlie, J. Steinberger, S. Wasserthiel-Smoller, M. Wilson, and P. Wolf. Heart disease and stroke statistics–2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113(6):e85–e151, 2006.
Tibayan, F. A., F. Rodriguez, M. K. Zasio, L. Bailey, D. Liang, G. T. Daughters, F. Langer, N. B. Ingels, and D. C. Miller. Geometric distortions of the mitral valvular-ventricular complex in chronic ischemic mitral regurgitation. Circulation 108(10 suppl 1):II-116–II-121, 2003.
Watanabe, N., Y. Ogasawara, Y. Yamaura, N. Wada, T. Kawamoto, E. Toyota, T. Akasaka, and K. Yoshida. Mitral annulus flattens in ischemic mitral regurgitation: geometric differences between inferior and anterior myocardial infarction a real-time 3-dimensional echocardiographic study. Circulation 112(9 suppl):I-458–I-462, 2005.
Wilcken, D., and A. J. Hickey. Lifetime risk for patients with mitral valve prolapse of developing severe valve regurgitation requiring surgery. Circulation 78(1):10–14, 1988.
Yiu, S. F., M. Enriquez-Sarano, C. Tribouilloy, J. B. Seward, and A. J. Tajik. Determinants of the degree of functional mitral regurgitation in patients with systolic left ventricular dysfunction: a quantitative clinical study. Circulation 102(12):1400–1406, 2000.
Yun, K. L., C. F. Sintek, D. C. Miller, G. T. Schuyler, A. D. Fletcher, T. A. Pfeffer, G. S. Kochamba, S. Khonsari, and M. R. Zile. Randomized trial of partial versus complete chordal preservation methods of mitral valve replacement a preliminary report. Circulation 100(suppl 2):II-90–II-94, 1999.
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Research reported in this publication was supported by National Heart, Lung, and Blood Institute of the National Institutes of Health under Award Number R01-HL119297. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors gratefully acknowledge Bruno V. Rego for helpful discussions.
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Khalighi, A.H., Drach, A., Bloodworth, C.H. et al. Mitral Valve Chordae Tendineae: Topological and Geometrical Characterization. Ann Biomed Eng 45, 378–393 (2017). https://doi.org/10.1007/s10439-016-1775-3
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DOI: https://doi.org/10.1007/s10439-016-1775-3