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Research Papers

The Effect of Trabeculae Carneae on Left Ventricular Diastolic Compliance: Improvement in Compliance With Trabecular Cutting

[+] Author and Article Information
David L. Halaney, Daniel Escobedo

Department of Medicine,
The University of Texas Health Science
Center at San Antonio,
San Antonio, TX 78229;
Department of Veterans Affairs,
South Texas Veterans Health Care System,
San Antonio, TX 78229

Arnav Sanyal

Department of Mechanical Engineering,
University of Texas at San Antonio,
San Antonio, TX 78249

Navid A. Nafissi, G. Patricia Escobar

Department of Medicine,
The University of Texas Health Science
Center at San Antonio,
San Antonio, TX 78229

Martin Goros, Joel Michalek

Department of Epidemiology and Biostatistics,
The University of Texas Health Science
Center at San Antonio,
San Antonio, TX 78229

Pedro J. Acevedo

Department of Anatomy,
University of Environmental
and Applied Sciences U.D.C.A.,
Bogotá, Cundinamarca, Colombia

William Pérez

Department of Anatomy,
Faculty of Veterinary Medicine,
University of the Republic,
Montevideo 11200, Uruguay

Marc D. Feldman

Department of Medicine,
The University of Texas Health Science
Center at San Antonio,
San Antonio, TX 78229;
Department of Veterans Affairs,
South Texas Veterans Health Care System,
San Antonio, TX 78229
e-mail: feldmanm@uthscsa.edu

Hai-Chao Han

Fellow ASME
Department of Mechanical Engineering,
University of Texas at San Antonio,
San Antonio, TX 78249

1Corresponding author.

Manuscript received May 25, 2016; final manuscript received December 13, 2016; published online January 24, 2017. Assoc. Editor: Thao (Vicky) Nguyen.

J Biomech Eng 139(3), 031012 (Jan 24, 2017) (8 pages) Paper No: BIO-16-1225; doi: 10.1115/1.4035585 History: Received May 25, 2016; Revised December 13, 2016

The role of trabeculae carneae in modulating left ventricular (LV) diastolic compliance remains unclear. The objective of this study was to determine the contribution of trabeculae carneae to the LV diastolic compliance. LV pressure–volume compliance curves were measured in six human heart explants from patients with LV hypertrophy at baseline and following trabecular cutting. The effect of trabecular cutting was also analyzed with finite-element model (FEM) simulations. Our results demonstrated that LV compliance improved after trabecular cutting (p < 0.001). Finite-element simulations further demonstrated that stiffer trabeculae reduce LV compliance further, and that the presence of trabeculae reduced the wall stress in the apex. In conclusion, we demonstrate that integrity of the LV and trabeculae is important to maintain LV stiffness and loss in trabeculae leads to more LV compliance.

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References

Wenink, A. C. , and Gittenberger-de Groot, A. C. , 1982, “ Left and Right Ventricular Trabecular Patterns. Consequence of Ventricular Septation and Valve Development,” Br. Heart J., 48(5), pp. 462–468. [CrossRef] [PubMed]
Chuang, M. L. , Gona, P. , Hautvast, G. L. , Salton, C. J. , Blease, S. J. , Yeon, S. B. , Breeuwer, M. , O'Donnell, C. J. , and Manning, W. J. , 2012, “ Correlation of Trabeculae and Papillary Muscles With Clinical and Cardiac Characteristics and Impact on CMR Measures of LV Anatomy and Function,” JACC Cardiovasc. Imaging, 5(11), pp. 1115–1123. [CrossRef] [PubMed]
Gati, S. , Papadakis, M. , Papamichael, N. D. , Zaidi, A. , Sheikh, N. , Reed, M. , Sharma, R. , Thilaganathan, B. , and Sharma, S. , 2014, “ Reversible de Novo Left Ventricular Trabeculations in Pregnant Women: Implications for the Diagnosis of Left Ventricular Noncompaction in Low-Risk Populations,” Circulation, 130(6), pp. 475–483. [CrossRef] [PubMed]
Mor-Avi, V. , Jenkins, C. , Kuhl, H. P. , Nesser, H. J. , Marwick, T. , Franke, A. , Ebner, C. , Freed, B. H. , Steringer-Mascherbauer, R. , Pollard, H. , Weinert, L. , Niel, J. , Sugeng, L. , and Lang, R. M. , 2008, “ Real-Time 3-Dimensional Echocardiographic Quantification of Left Ventricular Volumes: Multicenter Study for Validation With Magnetic Resonance Imaging and Investigation of Sources of Error,” JACC Cardiovasc. Imaging, 1(4), pp. 413–423. [CrossRef] [PubMed]
van de Veerdonk, M. C. , Dusoswa, S. A. , Marcus, J. T. , Bogaard, H. J. , Spruijt, O. , Kind, T. , Westerhof, N. , and Vonk-Noordegraaf, A. , 2014, “ The Importance of Trabecular Hypertrophy in Right Ventricular Adaptation to Chronic Pressure Overload,” Int. J. Cardiovasc. Imaging, 30(2), pp. 357–365. [CrossRef] [PubMed]
Bartram, U. , Bauer, J. , and Schranz, D. , 2007, “ Primary Noncompaction of the Ventricular Myocardium From the Morphogenetic Standpoint,” Pediatr. Cardiol., 28(5), pp. 325–332. [CrossRef] [PubMed]
Ho, S. Y. , 2009, “ Anatomy and Myoarchitecture of the Left Ventricular Wall in Normal and in Disease,” Eur. J. Echocardiography, 10(8), pp. iii3–7. [CrossRef]
Greenbaum, R. A. , Ho, S. Y. , Gibson, D. G. , Becker, A. E. , and Anderson, R. H. , 1981, “ Left Ventricular Fibre Architecture in Man,” Br. Heart J., 45(3), pp. 248–263. [CrossRef] [PubMed]
Taylor, J. R. , and Taylor, A. J. , 1999, “ The Thebesian Circulation to Developing Conducting Tissue: A Nutrient-Nodal Hypothesis of Cardiogenesis,” Can. J. Cardiol., 15(8), pp. 859–866. [PubMed]
Burch, G. , 1975, “ The Trabeculae Carneae—A Thought,” Am. Heart J., 89(2), p. 261. [CrossRef] [PubMed]
Burch, G. E. , Ray, C. T. , and Cronvich, J. A. , 1952, “ Certain Mechanical Peculiarities of the Human Cardiac Pump in Normal and Diseased States,” Circulation, 5(4), pp. 504–513. [CrossRef] [PubMed]
Captur, G. , and Nihoyannopoulos, P. , 2010, “ Left Ventricular Non-Compaction: Genetic Heterogeneity, Diagnosis and Clinical Course,” Int. J. Cardiol., 140(2), pp. 145–153. [CrossRef] [PubMed]
Franqui-Rivera, H. , Martinez-Ojeda, J. , Calderon, R. E. , and Gonzalez-Keelan, C. , 2008, “ Ventricular Non-Compaction Cardiomyopathy,” P. R. Health Sci. J., 27(4), pp. 377–381. [PubMed]
Towbin, J. A. , Lorts, A. , and Jefferies, J. L. , 2015, “ Left Ventricular Non-Compaction Cardiomyopathy,” Lancet, 386(9995), pp. 813–825. [CrossRef] [PubMed]
Arbustini, E. , Weidemann, F. , and Hall, J. L. , 2014, “ Left Ventricular Noncompaction: A Distinct Cardiomyopathy or a Trait Shared by Different Cardiac Diseases?,” J. Am. Coll. Cardiol., 64(17), pp. 1840–1850. [CrossRef] [PubMed]
Fernandez-Golfin, C. , Pachon, M. , Corros, C. , Bustos, A. , Cabeza, B. , Ferreiros, J. , de Isla, L. P. , Macaya, C. , and Zamorano, J. , 2009, “ Left Ventricular Trabeculae: Quantification in Different Cardiac Diseases and Impact on Left Ventricular Morphological and Functional Parameters Assessed With Cardiac Magnetic Resonance,” J. Cardiovasc. Med. (Hagerstown), 10(11), pp. 827–833. [CrossRef] [PubMed]
Janik, M. , Cham, M. D. , Ross, M. I. , Wang, Y. , Codella, N. , Min, J. K. , Prince, M. R. , Manoushagian, S. , Okin, P. M. , Devereux, R. B. , and Weinsaft, J. W. , 2008, “ Effects of Papillary Muscles and Trabeculae on Left Ventricular Quantification: Increased Impact of Methodological Variability in Patients With Left Ventricular Hypertrophy,” J. Hypertens., 26(8), pp. 1677–1685. [CrossRef] [PubMed]
Richter, G. W. , and Kellner, A. , 1963, “ Hypertrophy of the Human Heart at the Level of Fine Structure. An Analysis and Two Postulates,” J. Cell Biol., 18(1), pp. 195–206. [CrossRef] [PubMed]
Gati, S. , Papadakis, M. , Van Niekerk, N. , Reed, M. , Yeghen, T. , and Sharma, S. , 2013, “ Increased Left Ventricular Trabeculation in Individuals With Sickle Cell Anaemia: Physiology or Pathology?,” Int. J. Cardiol., 168(2), pp. 1658–1660. [CrossRef] [PubMed]
Gati, S. , Chandra, N. , Bennett, R. L. , Reed, M. , Kervio, G. , Panoulas, V. F. , Ghani, S. , Sheikh, N. , Zaidi, A. , Wilson, M. , Papadakis, M. , Carre, F. , and Sharma, S. , 2013, “ Increased Left Ventricular Trabeculation in Highly Trained Athletes: Do We Need More Stringent Criteria for the Diagnosis of Left Ventricular Non-Compaction in Athletes?,” Heart, 99(6), pp. 401–408. [CrossRef] [PubMed]
Gruver, E. J. , Morgan, J. P. , Stambler, B. S. , and Gwathmey, J. K. , 1994, “ Uniformity of Calcium Channel Number and Isometric Contraction in Human Right and Left Ventricular Myocardium,” Basic Res. Cardiol., 89(2), pp. 139–148. [PubMed]
Deniz, M. , Kilinc, M. , and Hatipoglu, E. S. , 2004, “ Morphologic Study of Left Ventricular Bands,” Surg. Radiol. Anat., 26(3), pp. 230–234. [CrossRef] [PubMed]
Levin, H. R. , Oz, M. C. , Chen, J. M. , Packer, M. , Rose, E. A. , and Burkhoff, D. , 1995, “ Reversal of Chronic Ventricular Dilation in Patients With End-Stage Cardiomyopathy by Prolonged Mechanical Unloading,” Circulation, 91(11), pp. 2717–2720. [CrossRef] [PubMed]
Streeter, D. D., Jr. , and Hanna, W. T. , 1973, “ Engineering Mechanics for Successive States in Canine Left Ventricular Myocardium. I. Cavity and Wall Geometry,” Circ. Res., 33(6), pp. 639–655. [CrossRef] [PubMed]
Omens, J. H. , MacKenna, D. A. , and McCulloch, A. D. , 1993, “ Measurement of Strain and Analysis of Stress in Resting Rat Left Ventricular Myocardium,” J. Biomech., 26(6), pp. 665–676. [CrossRef] [PubMed]
Voorhees, A. P. , and Han, H. C. , 2015, “ Biomechanics of Cardiac Function,” Compr Physiol., 5(4), pp. 1623–1644. [PubMed]
Lee, L. C. , Wenk, J. F. , Zhong, L. , Klepach, D. , Zhang, Z. , Ge, L. , Ratcliffe, M. B. , Zohdi, T. I. , Hsu, E. , Navia, J. L. , Kassab, G. S. , and Guccione, J. M. , 2013, “ Analysis of Patient-Specific Surgical Ventricular Restoration: Importance of an Ellipsoidal Left Ventricular Geometry for Diastolic and Systolic Function,” J. Appl. Physiol. (1985), 115(1), pp. 136–144. [CrossRef] [PubMed]
Aurigemma, G. P. , and Gaasch, W. H. , 2004, “ Clinical Practice. Diastolic Heart Failure,” N. Engl. J. Med., 351(11), pp. 1097–1105. [CrossRef] [PubMed]
Lang, R. M. , Bierig, M. , Devereux, R. B. , Flachskampf, F. A. , Foster, E. , Pellikka, P. A. , Picard, M. H. , Roman, M. J. , Seward, J. , Shanewise, J. S. , Solomon, S. D. , Spencer, K. T. , Sutton, M. S. , and Stewart, W. J. , 2005, “ Recommendations for Chamber Quantification: A Report From the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, Developed in Conjunction With the European Association of Echocardiography, a Branch of the European Society of Cardiology,” J. Am. Soc. Echocardiography, 18(12), pp. 1440–1463. [CrossRef]
Hutchins, G. M. , and Anaya, O. A. , 1973, “ Measurements of Cardiac Size, Chamber Volumes and Valve Orifices at Autopsy,” Johns Hopkins Med. J., 133(2), pp. 96–106. [PubMed]
Voorhees, A. P. , DeLeon-Pennell, K. Y. , Ma, Y. , Halade, G. V. , Yabluchanskiy, A. , Iyer, R. P. , Flynn, E. , Cates, C. A. , Lindsey, M. L. , and Han, H. C. , 2015, “ Building a Better Infarct: Modulation of Collagen Cross-Linking to Increase Infarct Stiffness and Reduce Left Ventricular Dilation Post-Myocardial Infarction,” J. Mol. Cell. Cardiol., 85, pp. 229–239. [CrossRef] [PubMed]
Walker, J. C. , Ratcliffe, M. B. , Zhang, P. , Wallace, A. W. , Fata, B. , Hsu, E. W. , Saloner, D. , and Guccione, J. M. , 2005, “ MRI-Based Finite-Element Analysis of Left Ventricular Aneurysm,” Am. J. Physiol.: Heart Circ. Physiol., 289(2), pp. H692–700. [CrossRef] [PubMed]
Jobsis, P. D. , Ashikaga, H. , Wen, H. , Rothstein, E. C. , Horvath, K. A. , McVeigh, E. R. , and Balaban, R. S. , 2007, “ The Visceral Pericardium: Macromolecular Structure and Contribution to Passive Mechanical Properties of the Left Ventricle,” Am. J. Physiol.: Heart Circ. Physiol., 293(6), pp. H3379–3387. [CrossRef] [PubMed]
Schaff, H. V. , Brown, M. L. , Dearani, J. A. , Abel, M. D. , Ommen, S. R. , Sorajja, P. , Tajik, A. J. , and Nishimura, R. A. , 2010, “ Apical Myectomy: A New Surgical Technique for Management of Severely Symptomatic Patients With Apical Hypertrophic Cardiomyopathy,” J. Thorac. Cardiovasc. Surg., 139(3), pp. 634–640. [CrossRef] [PubMed]
Yancy, C. W. , Jessup, M. , Bozkurt, B. , Butler, J. , Casey, D. E., Jr. , Drazner, M. H. , Fonarow, G. C. , Geraci, S. A. , Horwich, T. , Januzzi, J. L. , Johnson, M. R. , Kasper, E. K. , Levy, W. C. , Masoudi, F. A. , McBride, P. E. , McMurray, J. J. , Mitchell, J. E. , Peterson, P. N. , Riegel, B. , Sam, F. , Stevenson, L. W. , Tang, W. H. , Tsai, E. J. , and Wilkoff, B. L. , 2013, “ 2013 ACCF/AHA Guideline for the Management of Heart Failure: A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines,” J. Am. Coll. Cardiol., 62(16), pp. e147–239. [CrossRef] [PubMed]
Pitt, B. , Pfeffer, M. A. , Assmann, S. F. , Boineau, R. , Anand, I. S. , Claggett, B. , Clausell, N. , Desai, A. S. , Diaz, R. , Fleg, J. L. , Gordeev, I. , Harty, B. , Heitner, J. F. , Kenwood, C. T. , Lewis, E. F. , O'Meara, E. , Probstfield, J. L. , Shaburishvili, T. , Shah, S. J. , Solomon, S. D. , Sweitzer, N. K. , Yang, S. , and McKinlay, S. M. , 2014, “ Spironolactone for Heart Failure With Preserved Ejection Fraction,” N. Engl. J. Med., 370(15), pp. 1383–1392. [CrossRef] [PubMed]
Wan, S. H. , Vogel, M. W. , and Chen, H. H. , 2014, “ Pre-Clinical Diastolic Dysfunction,” J. Am. Coll. Cardiol., 63(5), pp. 407–416. [CrossRef] [PubMed]
McMurray, J. J. , Adamopoulos, S. , Anker, S. D. , Auricchio, A. , Bohm, M. , Dickstein, K. , Falk, V. , Filippatos, G. , Fonseca, C. , Gomez-Sanchez, M. A. , Jaarsma, T. , Kober, L. , Lip, G. Y. , Maggioni, A. P. , Parkhomenko, A. , Pieske, B. M. , Popescu, B. A. , Ronnevik, P. K. , Rutten, F. H. , Schwitter, J. , Seferovic, P. , Stepinska, J. , Trindade, P. T. , Voors, A. A. , Zannad, F. , Zeiher, A. , Bax, J. J. , Baumgartner, H. , Ceconi, C. , Dean, V. , Deaton, C. , Fagard, R. , Funck-Brentano, C. , Hasdai, D. , Hoes, A. , Kirchhof, P. , Knuuti, J. , Kolh, P. , McDonagh, T. , Moulin, C. , Reiner, Z. , Sechtem, U. , Sirnes, P. A. , Tendera, M. , Torbicki, A. , Vahanian, A. , Windecker, S. , Bonet, L. A. , Avraamides, P. , Ben Lamin, H. A. , Brignole, M. , Coca, A. , Cowburn, P. , Dargie, H. , Elliott, P. , Flachskampf, F. A. , Guida, G. F. , Hardman, S. , Iung, B. , Merkely, B. , Mueller, C. , Nanas, J. N. , Nielsen, O. W. , Orn, S. , Parissis, J. T. , and Ponikowski, P. , 2012, “ ESC Guidelines for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012: The Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in Collaboration With the Heart Failure Association (HFA) of the ESC,” Eur. J. Heart Failure, 14(8), pp. 803–869. [CrossRef]
Han, H. C. , Oshinski, J. N. , Ku, D. N. , and Pettigrew, R. I. , 2002, “ A Left Ventricle Model to Predict Post-Revascularization Ejection Fraction Based on Cine Magnetic Resonance Images,” ASME J. Biomech. Eng., 124(1), pp. 52–55. [CrossRef]
Hunter, P. J. , Pullan, A. J. , and Smaill, B. H. , 2003, “ Modeling Total Heart Function,” Annu. Rev. Biomed. Eng., 5(1), pp. 147–177. [CrossRef] [PubMed]
Messas, E. , Yosefy, C. , Chaput, M. , Guerrero, J. L. , Sullivan, S. , Menasche, P. , Carpentier, A. , Desnos, M. , Hagege, A. A. , Vlahakes, G. J. , and Levine, R. A. , 2006, “ Chordal Cutting Does Not Adversely Affect Left Ventricle Contractile Function,” Circulation, 114(1 Suppl.), pp. I524–528. [PubMed]

Figures

Grahic Jump Location
Fig. 1

Longitudinal cross section of a typical human LV illustrating the trabeculae (examples marked by arrowheads). A chordae tendineae is marked by the arrow.

Grahic Jump Location
Fig. 2

Ex vivo experimental setup for human hearts. (a) A custom cap was attached to the heart above the mitral valve. A latex balloon was inserted through the cap into the LV chamber. The cap included a hemostasis valve to allow a high fidelity micromanometer pressure catheter to be placed within the balloon, and a luer lock for volume input. (b) Measurements of LV compliance were conducted with the heart suspended by the cap inside a custom housing chamber which was surrounded by 37 °C water circulation to mimic in vivo conditions.

Grahic Jump Location
Fig. 3

Three-dimensional sectional view of the computational model of the left ventricle with three layers of trabeculae. All dimensions are in mm. The wall thickness is 13.5 mm at the equator and 5.5 mm at the apex.

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Fig. 4

A comparison of a typical LV wall region before (top panel) and after (bottom panel) trabecular cutting

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Fig. 5

Comparison of pressure–volume relationships of human hearts before and after trabecular cutting. Six human heart (a)–(f) and their average (G) pressure–lumen volume curves before (• = uncut) and after (○ = cut) trabecular cutting. For the average, volume was normalized to the highest volume measured for each heart. R2 values correspond to cubic fits in all panels. For all six cases, trabecular cutting increased the compliance of the left ventricle.

Grahic Jump Location
Fig. 6

The pressure–volume relationship of control hearts without trabecular cutting. (a) Comparison of measurements of repeating saline filling in heart #7. The pressure measurement system remains in the LV during the tests. (b) Comparison of measurements after sham operation in heart #8. The pressure measurement system was removed from the heart after the first measurement, and trabecular cutting was mimicked with a blunt tool, but no trabeculae were cut. The pressure measurement system was then placed back into the heart for the second measurement. R2 values correspond to cubic fits of the pressure–volume data. In both cases, there was no significant change in compliance in the absence of trabecular cutting.

Grahic Jump Location
Fig. 7

Pressure–volume relationship obtained from the FEM simulations of the LV model without trabeculae, with three layers of intact and normal trabeculae, with three layers of intact and stiffer trabeculae, and with one layer of intact and normal trabeculae. These results demonstrate that severing trabeculae increases LV compliance and the presence of stiffer trabeculae decreases LV compliance.

Grahic Jump Location
Fig. 8

Color map of circumferential stress distribution obtained from FEM simulations of LV model during a chamber pressure of 10 mm Hg. The stress was obtained for the cases without trabeculae, with three layers of trabeculae, and with only one apical layer of trabeculae. Each color represents the range of stress shown in the scale.

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