0
Research Papers

Surface Strains of Porcine Tricuspid Valve Septal Leaflets Measured in Ex Vivo Beating Hearts

[+] Author and Article Information
Keyvan Amini Khoiy

Department of Biomedical Engineering,
The University of Akron,
Akron, OH 44325
e-mail: ka67@zips.uakron.edu

Dipankar Biswas

Department of Mechanical Engineering,
The University of Akron,
Akron, OH 44325
e-mail: db76@zips.uakron.edu

Thomas N. Decker

Department of Biomedical Engineering,
The University of Akron,
Akron, OH 44325
e-mail: tnd14@zips.uakron.edu

Kourosh T. Asgarian

Cardiothoracic Surgery,
St. Joseph's Regional Medical Center,
Paterson, NJ 07503
e-mail: ktacardiac@aol.com

Francis Loth

Department of Mechanical Engineering,
The University of Akron,
Akron, OH 44325
e-mail: loth@uakron.edu

Rouzbeh Amini

Mem. ASME
Department of Biomedical Engineering,
The University of Akron,
260 S Forge Street,
Olson Research Center Room 301F,
Akron, OH 44325
e-mail: ramini@uakron.edu

1Corresponding author.

Manuscript received May 22, 2016; final manuscript received August 23, 2016; published online October 21, 2016. Assoc. Editor: Jessica E. Wagenseil.

J Biomech Eng 138(11), 111006 (Oct 21, 2016) (9 pages) Paper No: BIO-16-1216; doi: 10.1115/1.4034621 History: Received May 22, 2016; Revised August 23, 2016

Quantification of the tricuspid valve (TV) leaflets mechanical strain is important in order to understand valve pathophysiology and to develop effective treatment strategies. Many of the traditional methods used to dynamically open and close the cardiac valves in vitro via flow simulators require valve dissection. Recent studies, however, have shown that restriction of the atrioventricular valve annuli could significantly change their in vivo deformation. For the first time, the porcine valve leaflets deformation was measured in a passive ex vivo beating heart without isolating and remounting the valve annuli. In particular, the right ventricular apexes of porcine hearts (n = 8) were connected to a pulse-duplicator pump that maintained a pulsatile flow from and to a reservoir connected to the right atrium and the pulmonary arteries. This pump provided a right ventricular pressure (RVP) waveform that closely matched physiological values, leading to opening and closure of the tricuspid and pulmonary valves (PVs). At the midsection of the valve leaflets, the peak areal strain was 9.8 ± 2.0% (mean±standard error). The peak strain was 5.6 ± 1.1% and 4.3 ± 1.0% in the circumferential and radial directions, respectively. Although the right ventricle was beating passively, the leaflet peak areal strains closely matched the values measured in other atrioventricular valves (i.e., the mitral valve (MV)) in vivo. This technique can be used to measure leaflet strains with and without the presence of valve lesions to help develop/evaluate treatment strategies to restore normal valve deformation.

FIGURES IN THIS ARTICLE
<>
Copyright © 2016 by ASME
Your Session has timed out. Please sign back in to continue.

References

Hall, J. E. , 2010, Guyton and Hall Textbook of Medical Physiology, Elsevier Health Sciences, Philadelphia, PA.
Vassileva, C. M. , Shabosky, J. , Boley, T. , Markwell, S. , and Hazelrigg, S. , 2012, “ Tricuspid Valve Surgery: The Past 10 Years From the Nationwide Inpatient Sample (NIS) Database,” J. Thorac. Cardiovasc. Surg., 143(5), pp. 1043–1049. [CrossRef] [PubMed]
Guenther, T. , Noebauer, C. , Mazzitelli, D. , Busch, R. , Tassani-Prell, P. , and Lange, R. , 2008, “ Tricuspid Valve Surgery: A Thirty-Year Assessment of Early and Late Outcome,” Eur. J. Cardio-Thorac. Surg., 34(2), pp. 402–409. [CrossRef]
Come, P. C. , and Riley, M. F. , 1985, “ Tricuspid Anular Dilatation and Failure of Tricuspid Leaflet Coaptation in Tricuspid Regurgitation,” Am. J. Cardiol., 55(5), pp. 599–601. [CrossRef] [PubMed]
Rausch, M. K. , Bothe, W. , Kvitting, J. E. , Göktepe, S. , Miller, D. C. , and Kuhl, E. , 2011, “ In Vivo Dynamic Strains of the Ovine Anterior Mitral Valve Leaflet,” J. Biomech., 44(6), pp. 1149–1157. [CrossRef] [PubMed]
Amini, R. , Eckert, C. E. , Koomalsingh, K. , McGarvey, J. , Minakawa, M. , Gorman, J. H. , Gorman, R. C. , and Sacks, M. S. , 2012, “ On the In Vivo Deformation of the Mitral Valve Anterior Leaflet: Effects of Annular Geometry and Referential Configuration,” Ann. Biomed. Eng., 40(7), pp. 1455–1467. [CrossRef] [PubMed]
Sacks, M. S. , Enomoto, Y. , Graybill, J. R. , Merryman, W. D. , Zeeshan, A. , Yoganathan, A. P. , Levy, R. J. , Gorman, R. C. , and Gorman, J. H. , 2006, “ In-Vivo Dynamic Deformation of the Mitral Valve Anterior Leaflet,” Ann. Thorac. Surg., 82(4), pp. 1369–1377. [CrossRef] [PubMed]
Sacks, M. S. , Merryman, W. D. , and Schmidt, D. E. , 2009, “ On the Biomechanics of Heart Valve Function,” J. Biomech., 42(12), pp. 1804–1824. [CrossRef] [PubMed]
Eckert, C. E. , Zubiate, B. , Vergnat, M. , Gorman, J. H., III , Gorman, R. C. , and Sacks, M. S. , 2009, “ In Vivo Dynamic Deformation of the Mitral Valve Annulus,” Ann. Biomed. Eng., 37(9), pp. 1757–1771. [CrossRef] [PubMed]
Krishnamurthy, G. , Itoh, A. , Bothe, W. , Swanson, J. C. , Kuhl, E. , Karlsson, M. , Miller, D. C. , and Ingels, N. B. , 2009, “ Stress–Strain Behavior of Mitral Valve Leaflets in the Beating Ovine Heart,” J. Biomech., 42(12), pp. 1909–1916. [CrossRef] [PubMed]
Krishnamurthy, G. , Itoh, A. , Swanson, J. C. , Bothe, W. , Karlsson, M. , Kuhl, E. , Miller, D. C. , and Ingels, N. B. , 2009, “ Regional Stiffening of the Mitral Valve Anterior Leaflet in the Beating Ovine Heart,” J. Biomech., 42(16), pp. 2697–2701. [CrossRef] [PubMed]
Sacks, M. S. , He, Z. , Baijens, L. , Wanant, S. , Shah, P. , Sugimoto, H. , and Yoganathan, A. P. , 2002, “ Surface Strains in the Anterior Leaflet of the Functioning Mitral Valve,” Ann. Biomed. Eng., 30(10), pp. 1281–1290. [CrossRef] [PubMed]
Hiro, M. E. , Jouan, J. , Pagel, M. R. , Lansac, E. , Lim, K. H. , Lim, H. , and Duran, C. M. , 2004, “ Sonometric Study of the Normal Tricuspid Valve Annulus in Sheep,” J. Heart Valve Dis., 13(3), pp. 452–460. [PubMed]
Fawzy, H. , Fukamachi, K. , Mazer, C. D. , Harrington, A. , Latter, D. , Bonneau, D. , and Errett, L. , 2011, “ Complete Mapping of the Tricuspid Valve Apparatus Using Three-Dimensional Sonomicrometry,” J. Thorac. Cardiovasc. Surg., 141(4), pp. 1037–1043. [CrossRef] [PubMed]
Jouan, J. , Pagel, M. R. , Hiro, M. E. , Lim, K. H. , Lansac, E. , and Duran, C. M. , 2007, “ Further Information From a Sonometric Study of the Normal Tricuspid Valve Annulus in Sheep: Geometric Changes During the Cardiac Cycle,” J. Heart Valve Dis., 16(5), pp. 511–518. [PubMed]
He, Z. , Ritchie, J. , Grashow, J. S. , Sacks, M. S. , and Yoganathan, A. P. , 2005, “ In Vitro Dynamic Strain Behavior of the Mitral Valve Posterior Leaflet,” ASME J. Biomech. Eng., 127(3), pp. 504–511. [CrossRef]
He, Z. , Sacks, M. S. , Baijens, L. , Wanant, S. , Shah, P. , and Yoganathan, A. P. , 2003, “ Effects of Papillary Muscle Position on In-Vitro Dynamic Strain on the Porcine Mitral Valve,” J. Heart Valve Dis., 12(4), pp. 488–494. [PubMed]
Leopaldi, A. , Vismara, R. , Lemma, M. , Valerio, L. , Cervo, M. , Mangini, A. , Contino, M. , Redaelli, A. , Antona, C. , and Fiore, G. , 2012, “ In Vitro Hemodynamics and Valve Imaging in Passive Beating Hearts,” J. Biomech., 45(7), pp. 1133–1139. [CrossRef] [PubMed]
Chaudhury, R. A. , Atlasman, V. , Pathangey, G. , Pracht, N. , Adrian, R. J. , and Frakes, D. H. , 2016, “ A High Performance Pulsatile Pump for Aortic Flow Experiments in 3-Dimensional Models,” Cardiovasc. Eng. Technol., 7(2), pp. 1–11. [CrossRef] [PubMed]
Evin, M. , Guivier-Curien, C. , Pibarot, P. , Kadem, L. , and Rieu, R. , 2016, “ Are the Current Doppler Echocardiography Criteria Able to Discriminate Mitral Bileaflet Mechanical Heart Valve Malfunction? An In Vitro Study,” Artif. Organs, 40(5), pp. 52–60. [CrossRef]
Trawiński, Z. , Wójcik, J. , Nowicki, A. , Olszewski, R. , Balcerzak, A. , Frankowska, E. , Zegadło, A. , and Rydzyński, P. , 2015, “ Strain Examinations of the Left Ventricle Phantom by Ultrasound and Multislices Computed Tomography Imaging,” Biocybern. Biomed. Eng., 35(4), pp. 255–263. [CrossRef]
Rahmani, B. , Tzamtzis, S. , Ghanbari, H. , Burriesci, G. , and Seifalian, A. M. , 2012, “ Manufacturing and Hydrodynamic Assessment of a Novel Aortic Valve Made of a New Nanocomposite Polymer,” J. Biomech., 45(7), pp. 1205–1211. [CrossRef] [PubMed]
Cygan, S. , Werys, K. , Błaszczyk, Ł. , Kubik, T. , and Kałużyński, K. , 2014, “ Left Ventricle Phantom and Experimental Setup for MRI and Echocardiography–Preliminary Results of Data Acquisitions,” Biocybern. Biomed. Eng., 34(1), pp. 19–24. [CrossRef]
Nolan, S. P. , 1994, “ The International Standard Cardiovascular Implants—Cardiac Valve Prostheses (ISO 5840:1989) and the FDA Draft Replacement Heart Valve Guidance (Version 4.0),” J. Heart Valve Dis., 3(4), pp. 347–349. [PubMed]
Amini, R. , Voycheck, C. A. , and Debski, R. E. , 2014, “ A Method for Predicting Collagen Fiber Realignment in Non-Planar Tissue Surfaces as Applied to Glenohumeral Capsule During Clinically Relevant Deformation,” ASME J. Biomech. Eng., 136(3), p. 031003. [CrossRef]
Filas, B. A. , Knutsen, A. K. , Bayly, P. V. , and Taber, L. A. , 2008, “ A New Method for Measuring Deformation of Folding Surfaces During Morphogenesis,” ASME J. Biomech. Eng., 130(6), p. 061010. [CrossRef]
Mohrman, D. E. , and Heller, L. J. , 2002, Cardiovascular Physiology, McGraw-Hill, New York.
Greyson, C. , Xu, Y. , Cohen, J. , and Schwartz, G. G. , 1997, “ Right Ventricular Dysfunction Persists Following Brief Right Ventricular Pressure Overload,” Cardiovasc. Res., 34(2), pp. 281–288. [CrossRef] [PubMed]
Greyson, C. , Xu, Y. , Lu, L. , and Schwartz, G. G. , 2000, “ Right Ventricular Pressure and Dilation During Pressure Overload Determine Dysfunction After Pressure Overload,” Am. J. Physiol., 278(5), pp. H1414–1420.
Schmitto, J. D. , Doerge, H. , Post, H. , Coulibaly, M. , Sellin, C. , Popov, A. F. , Sossalla, S. , and Schoendube, F. A. , 2009, “ Progressive Right Ventricular Failure is Not Explained by Myocardial Ischemia in a Pig Model of Right Ventricular Pressure Overload,” Eur. J. Cardio-Thorac. Surg., 35(2), pp. 229–234. [CrossRef]
Solomon, S. B. , and Glantz, S. A. , 1999, “ Regional Ischemia Increases Sensitivity of Left Ventricular Relaxation to Volume in Pigs,” Am. J. Physiol., 276(6 Pt 2), pp. H1994–2005. [PubMed]
Redington, A. N. , Gray, H. H. , Hodson, M. E. , Rigby, M. L. , and Oldershaw, P. J. , 1988, “ Characterisation of the Normal Right Ventricular Pressure-Volume Relation by Biplane Angiography and Simultaneous Micromanometer Pressure Measurements,” Br. Heart J., 59(1), pp. 23–30. [CrossRef] [PubMed]
Hannon, J. P. , Bossone, C. A. , and Wade, C. E. , 1990, “ Normal Physiological Values for Conscious Pigs Used in Biomedical Research,” Lab. Anim. Sci., 40(3), pp. 293–298. [PubMed]
May-Newman, K. , and Yin, F. C. , 1995, “ Biaxial Mechanical Behavior of Excised Porcine Mitral Valve Leaflets,” Am. J. Physiol., 269(4 Pt 2), pp. H1319–1327. [PubMed]
Billiar, K. , and Sacks, M. , 1997, “ A Method to Quantify the Fiber Kinematics of Planar Tissues Under Biaxial Stretch,” J. Biomech., 30(7), pp. 753–756. [CrossRef] [PubMed]
Khoiy, K. A. , and Amini, R. , 2016, “ On the Biaxial Mechanical Response of Porcine Tricuspid Valve Leaflets,” ASME J. Biomech. Eng., 138(10), p. 104504. [CrossRef]
Martin, C. , and Sun, W. , 2012, “ Biomechanical Characterization of Aortic Valve Tissue in Humans and Common Animal Models,” J. Biomed. Mater. Res., Part A, 100(6), pp. 1591–1599. [CrossRef]
Gorman, J. H. , Jackson, B. M. , Enomoto, Y. , and Gorman, R. C. , 2004, “ The Effect of Regional Ischemia on Mitral Valve Annular Saddle Shape,” Ann. Thorac. Surg., 77(2), pp. 544–548. [CrossRef] [PubMed]
Gorman, J. H. , Gorman, R. C. , Jackson, B. M. , Enomoto, Y. , John-Sutton, M. G. S. , and Edmunds, L. H. , 2003, “ Annuloplasty Ring Selection for Chronic Ischemic Mitral Regurgitation: Lessons From the Ovine Model,” Ann. Thorac. Surg., 76(5), pp. 1556–1563. [CrossRef] [PubMed]
Gorman, J. H. , Gupta, K. B. , Streicher, J. T. , Gorman, R. C. , Jackson, B. M. , Ratcliffe, M. B. , Bogen, D. K. , and Edmunds, L. H. , 1996, “ Dynamic Three-Dimensional Imaging of the Mitral Valve and Left Ventricle by Rapid Sonomicrometry Array Localization,” J. Thorac. Cardiovasc. Surg., 112(3), pp. 712–724. [CrossRef] [PubMed]
Ge, L. , Morrel, W. G. , Ward, A. , Mishra, R. , Zhang, Z. , Guccione, J. M. , Grossi, E. A. , and Ratcliffe, M. B. , 2014, “ Measurement of Mitral Leaflet and Annular Geometry and Stress After Repair of Posterior Leaflet Prolapse: Virtual Repair Using a Patient-Specific Finite Element Simulation,” Ann. Thorac. Surg., 97(5), pp. 1496–1503. [CrossRef] [PubMed]
Biswas, D. , Casey, D. , Crowder, D. , Steinman, D. A. , Yun, H. Y. , and Loth, F. , 2016, “ Characterization of Transition to Turbulence for Blood in a Straight Pipe Under Steady Flow Conditions,” ASME J. Biomech. Eng., 138(7), p. 071001. [CrossRef]

Figures

Grahic Jump Location
Fig. 1

(a) The schematic circulation loop and (b) the ex vivo apparatus

Grahic Jump Location
Fig. 2

The T-shaped pipefitting connected to the right atrium through a straight barbed hose fitting (1). The Luer Lok assembly was connected to the other side of the T-shaped pipe fitting to support the pressure sensor. The other straight barbed hose fitting (2) connected the right ventricle to the pump. Crystal wires came out through the inferior vena cava. The umbilical clamp was used to prevent leakage from the inferior vena cava.

Grahic Jump Location
Fig. 3

Umbilical clamps, cable ties, and worm-drive clamps were used for sealing

Grahic Jump Location
Fig. 4

Crystals are numbered on the leaflet. The straight lines connecting the numbered crystals show the triangular elements used for strain calculation. The radial direction was defined by a vector connecting crystal 4 to crystal 7.

Grahic Jump Location
Fig. 5

Right heart pressure during the cardiac cycle averaged over all of the hearts. The bars are standard errors (n = 8). The vertical lines show the opening and closure of the pulmonary valve (PV) and tricuspid valve (TV): TV closed at 0.2 s and opened at 0.54 s; the pulmonary valve opened at 0.29 s and closed at 0.44 s.

Grahic Jump Location
Fig. 6

Average peak areal, maximum principal (Max Princ), circumferential (Circ), and radial strains at the leaflet midpoint measured with respect to reference 1 (Ref1, minimum RAP) and reference 2 (Ref2, end diastole). The error bars are standard error (n = 8).

Grahic Jump Location
Fig. 7

The temporal strain variations during the cardiac cycle. (a) The areal, (b) maximum principal, (c) circumferential, and (d) radial strains at the leaflet midpoint averaged over all of the hearts. The shaded area shows the standard error (n = 8). Vertical lines show the time points for TV closing, PV opening, maximum RVP, PV closing, and TV opening, respectively, from left to right.

Grahic Jump Location
Fig. 8

The areal, maximum principal, circumferential, and radial strains at maximum RVP. The strains are averaged over all the hearts (n = 8) and are presented on a typical septal leaflet. Minimum RAP is used as the reference for strain calculation. The arrows are showing the direction of the strains at the center of each triangular surface.

Grahic Jump Location
Fig. 9

Distribution of the maximum principal strain over the leaflet during the septal entire cardiac cycle. Maximum principal strain is averaged over all of the hearts (n = 8) and showed over a typical septal leaflet during the cardiac cycle.

Tables

Errata

Discussions

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In