Altered Mechanical Behavior of Epicardium Under Isothermal Biaxial Loading

[+] Author and Article Information
P. B. Wells, J. L. Harris, J. D. Humphrey

Department of Biomedical Engineering, Texas A&M University, College Station, TX 77843-3120

J Biomech Eng 126(4), 492-497 (Sep 27, 2004) (6 pages) doi:10.1115/1.1785807 History: Received December 19, 2003; Revised March 22, 2004; Online September 27, 2004
Copyright © 2004 by ASME
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Humphrey,  J. D., 2003, “Continuum Thermomechanics and the Clinical Treatment of Disease and Injury,” Appl. Mech. Rev., 56(2), pp. 231–260.
Lennox,  F. G., 1949, “Shrinkage of collagen,” Biochim. Biophys. Acta, 3, pp. 170–187.
Weir,  C. E., 1949, “Rate of shrinkage of tendon collagen-Heat, entropy and free energy of activation of the shrinkage of untreated tendon. Effect of acid salt, pickle, and tannage on the activation of tendon collagen,” J. Am. Leather. Chem. Assoc., 44, pp. 108–140.
Rasmussen,  D. M., Wakim,  K. G., and Winkelmann,  R. K., 1964, “Isotonic and Isometric Thermal Contraction of Human Dermis. I. Technic and Controlled Study,” J. Invest. Dermatol., Nov., 43, pp. 333–339.
Allain,  J. C., Le Lous,  M., Bazin,  S., Bailey,  A. J., and Delaunay,  A., 1978, “Isometric Tension Developed During Heating of Collagenous Tissues: Relationships with Collagen Cross-Linking,” Biochim. Biophys. Acta, Mar. 28, 533(1), pp. 147–155.
Le Lous,  M., Allain,  J. C., Cohen-Solal,  L., and Maroteaux,  P., 1982, “The Rate of Collagen Maturation in Rat and Human Skin,” Connect. Tissue Res., 9(4), pp. 253–262.
Le Lous,  M., Cohen-Solal,  L., Allain,  J. C., Bonaventure,  J., and Maroteaux,  P., 1985, “Age Related Evolution of Stable Collagen Reticulation in Human Skin,” Connect. Tissue Res., 13(2), pp. 145–155.
Andreassen,  T. T., Seyer-Hansen,  K., and Bailey,  A. J., 1981, “Thermal Stability, Mechanical Properties and Reducible Cross-Links of Rat Tail Tendon in Experimental Diabetes,” Biochemica et Biophysica Acta, 677, pp. 313–317.
Lee,  J. M., Pereira,  C. A., Abdulla,  D., Naimark,  W. A., and Crawford,  I., 1995, “A multi-sample denaturation temperature tester for collagenous biomaterials,” Med. Eng. Phys., 17(2), pp. 115–121.
Chachra,  D., Gratzer,  P. F., Pereira,  C. A., and Lee,  J. M., 1996, “Effect of Applied Uniaxial Stress on Rate and Mechanical Effects of Cross-Linking in Tissue-Derived Biomaterials,” Biomaterials, 17(19), pp. 1865–1875.
De Deyne,  P., and Haut,  R. C., 1991, “Some effects of gamma irradiation on patellar tendon allografts,” Connect. Tissue Res., 27(1), pp. 51–62.
Wiederhorn,  N. H., and Reardon,  G. V., 1953, “Studies concerned with the structure of collagen. II Stress-strain behavior of thermally contracted collagen,” J. Poly. Sci., 9, pp. 315–325.
Consigny,  P. M., Teitelbaum,  G. P., Gardiner,  G. A., and Kerns,  W. D., 1989, “Effects of Laser Thermal Angioplasty on Arterial Contractions and Mechanics,” Cardiovasc. Intervent Radiol., 12, pp. 83–87.
Morgan,  J. E., Ellingham,  R. B., Young,  R. D., and Trmal,  G. J., 1996, “The mechanical properties of the human lens capsule following capsulorhexis or radiofrequency diathermy capsulotomy,” Arch. Ophthalmol. (Chicago), 114, pp. 1110–1115.
Wallace,  A. L., Hollinshead,  R. M., and Frank,  C. B., 2001, “Electrothermal shrinkage reduces laxity but alters creep behavior in a lapine ligament model,” J. Shoulder Elbow Surg., 10(1), pp. 1–6.
Hayashi,  K., Peters,  D. M., Thabit,  G., Hecht,  P., Vanderby,  R., Fanton,  G. S., and Markel,  M. D., 2000, “The Mechanism of Joint Capsule Thermal Modification in an In Vitro Sheep Model,” Clin. Orthop., Jan, 370, pp. 236–249.
Harris,  J. L., Wells,  P. B., and Humphrey,  J. D., 2003, “Altered Mechanical Behavior of Epicardium Due to Isothermal Heating Under Biaxial Isotonic Loads,” ASME J. Biomech. Eng., 125, pp. 381–388.
Jun,  J.-H., Harris,  J. L., Humphrey,  J. D., and Rastegar,  S., 2003, “Effect of Thermal Damage and Biaxial Loading on the Optical Properties of a Collagenous Tissue,” ASME J. Biomech. Eng., 125, pp. 540–548.
Sacks,  M. S., Smith,  D. B., and Hiester,  E. D., 1997, “A Small Angle Light Scattering Device for Planar Connective Tissue Microstructural Analysis,” Ann. Biomed. Eng., 25(4), pp. 678–689.
Harris,  J. L., and Humphrey,  J. D., 2004, “Kinetics of Thermal Damage of a Collagenous Membrane Under Biaxial Isotonic Loading,” IEEE Trans. Biomed. Eng., 51, pp. 371–379.
Humphrey,  J. D., Strumpf,  R. K., and Yin,  F. C. P., 1992, “A constitutive theory for biomembranes: Application to epicardium,” ASME J. Biomech. Eng., 114, pp. 461–466.
Le Lous,  M., Allain,  J. C., Cohen-Solal,  L., and Maroteaux,  P., 1983, “Hydrothermal Isometric Tension Curves from Different Connective Tissues. Role of Collagen Genetic Types and Noncollagenous Components,” Connect. Tissue Res., 11(2–3), pp. 199–206.
Horgan,  D. J., King,  N. L., Kurth,  L. B., and Kuypers,  R., 1990, “Collagen Crosslinks and Their Relationship to the Thermal Properties of Calf Tendons,” Arch. Biochem. Biophys., 281(1), pp. 21–26.
Brinkmann,  R., Radt,  B., Flamm,  C., Kampmeier,  J., Koop,  N., and Birngruber,  R., 2000, “Influence of temperature and time on thermally induced forces in corneal collagen and the effect on laser thermokeratoplasty,” Intell. Data Anal., 26, pp. 744–754.
Kang,  T., Humphrey,  J. D., and Yin,  F. P. C, 1996, “Comparison of biaxial mechanical properties of excised endocardium and epicardium,” Am. J. Physiol., 270, pp. H2169–H2176.
Lee,  B. I., Becker,  G. J., Waller,  B. F., Barry,  K. J., Connolly,  R. J., Kaplan,  J., Shapiro,  A. R., and Nardella,  P. C., 1989, “Thermal compression and molding of atherosclerotic vascular tissue with use of radiofrequency energy: Implications for radiofrequency balloon angioplasty,” J. Am. Coll. Cardiol., 13, pp. 1167–1175.
Levy,  O., Wilson,  H., Williams,  H., Bruguera,  J. A., Dodenhoff,  R., Sforza,  G., and Copeland,  S., 2001, “Thermal capsular shrinkage for shoulder instability. Midterm longitudinal outcome study,” J. Bone Jt. Surg. Br., 83(5), pp. 640–645.
Hayashi,  K., Thabit,  G., Massa,  K. L., Bogdanske,  J. J., Cooley,  A. J., Orwin,  J. F., and Markel,  M. D., 1997, “The effect of thermal heating on the length and histologic properties of the glenohumeral joint capsule,” Am. J. Sports , 25(1), pp. 107–112.
Moran,  K., Anderson,  P., Hutcheson,  J., and Flock,  S., 2000, “Thermally induced shrinkage of joint capsule,” Clin. Orthop., 381, pp. 248–255.
Doi, M., and Edwards, S. F., 1986, The Theory of Polymer Dynamics, Clarendon Press, Oxford.
Miles,  C. A., and Ghelashvili,  M., 1999, “Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers,” Biophys. J., 76(6), pp. 3243–3252.
Chen,  S. S., and Humphrey,  J. D., 1998, “Heat-induced changes in the mechanics of a collagenous tissue: Pseudoelastic behavior at 37°C,” J. Biomech., 31, pp. 211–216.


Grahic Jump Location
Typical Cauchy membrane stress versus stretch response for native bovine epicardium in the stiffer direction. Shown, too, are the approximate isometric constraints, relative to the native tissue equibiaxial response, imposed during heating. These constraints are called 1.03, Low, Elbow, and High; see text for specific definitions. Note that the High constraint is the only one that imposes a significant pre-stress prior to heating.
Grahic Jump Location
Schema of the overall testing protocol. The specimen is shown with four central tracking markers. βX denotes various traction-free reference configurations. Arrows denote load-induced stretching, and hatched ends denote an isometric biaxial constraint.
Grahic Jump Location
Representative data from a 1.03 test. Panel (a) shows the evolution of forces along both axes during the course of heating (T=75°C,τ=900 s). The direction that achieves the greatest force is generally the mechanically stiffer direction. Recall, therefore, that we incorporated a SALS device to align the preferred fiber direction along the y-axis of our device. The elliptical images were not well defined, in general, when using the right ventricular epicardium, which creates a large degree of uncertainty with respect to the orientation. Therefore, in some cases we actually found the x-axis to be the stiffer of the two. Experimentally, having the stiffer direction aligned with the x-axis yields sub-optimal control and therefore a slightly larger variation between data sets. Nonetheless, trends are not affected by a misalignment of the tissue, and therefore during the analysis we can think of the directions as merely the stiffer and the less-stiff directions irrespective of the x- or y-axis. Panel (b) illustrates the altered mechanical behavior due to heating. Note the non-zero initial slope for the damaged specimen, the loss of extensibility, and in this case a tendency towards decreased anisotropy. All data are plotted relative to βN.
Grahic Jump Location
Plot of the mean (equibiaxial) mechanical data following the 1.03 isometric heating tests (n=5). Circles represent the native tissue mechanical response, whereas the squares represent that of the heated tissue. The stretch magnitudes are calculated relative to the native undeformed configuration, βN. Note that |V|=(√2) in the reference configuration.
Grahic Jump Location
Plot of the mean equibiaxial data from the four test groups (n=5 to 7 per group) and a representative mean native curve (* ). In comparison to Figure 4, the magnitude of V is normalized here to the maximum value in the mean native data. The squares (□), pluses (+), circles (○), and triangles (▵) represent the 1.03, low stretch, elbow, and high constraints, respectively. As the isometric constraint increased (i.e., greater stretch was imposed), given the same temperature level and duration of exposure, the equibiaxial response of the heated tissue differed less from that of the native tissue, suggesting that stretch delays thermal damage.
Grahic Jump Location
Possible linear correlation between the relative extensibility of the damaged tissue (Ψ) at various levels of |T| (15, 25, 35, 45 and 55 N/m) and the relative amount of isometric stretch imposed during heating (Φ). Because physiologic loads are more likely to be high, we chose the data corresponding to |T|=55 N/m (‘filled’ circles) as the basis for a best-fit linear trend-line, which has an R2 value of 0.687. Open circles correspond to |T|=15, 25, 35, and 45 N/m, and as can be seen, they too correspond well to the linear trend.
Grahic Jump Location
Relation between resulting equibiaxial mechanical responses in isometric and isotonic tests. The asterisks (* ) represent the mean native response, the open squares (□), circles (○), and triangles (▵) represent the 1.03, low stretch, and high isometric constraints, respectively. The filled squares (▪), circles (•), and triangles (▴) represent the (T,τ,P) combinations of (65, 900, 0.0), (75, 900, 12.8) and (75, 900, 21.3) from 17, respectively. The latter two were chosen for consistency with respect to the temperature and duration of heating, while the former represents a bound. The solid line shows the combined isotonic/isometric constraint.
Grahic Jump Location
Representative data showing a lack of shrinkage during the test in which high isotonic loads are applied to the tissue during heating. This illustrates that the stretches in both directions remain constant during heating, and therefore an isotonic/isometric constraint is enforced.



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