Abstract
Measurement of pressure–volume relations is a commonly used technique to elucidate small intestinal stiffness. There is a lack of data on the relation between stiffness and history-dependent mechanical properties of the gastrointestinal tract. We aimed to distinguish between passive properties of the tissue that depend on the time-history of load (viscoelastic effects) versus those that depend on the maximum previous load (strain softening effects). Ten repeated pressure–volume relations were measured at each peak pressure level in six isolated, passive guinea-pig jejuni in vitro during balloon inflation and deflation cycles. With inflation to a new higher peak pressure (ranging from 3 to 15 mm Hg), the pressure–volume relation became less stiff, particularly in the low pressure range, without a significant change in unloaded jejunal volume. We computed the jejunal normalized volume change as a function of the integrated volume–time history and maximum volume. Analysis of covariance revealed significant dependence of the normalized volume change on the volume–time history (P <; 0.001) and the maximum volume history (P <; 0.001). Multiple linear regression analysis showed that approximately 90% of the history dependence could be attributed to the maximum volume. Most softening (loss of stiffness) happens in the low pressure range of the curve (0–3 mm Hg). We adopted the Johnson and Beatty strain softening theory and computed the volume amplification factor. This factor was shown to be a linear function of the normalized peak volume (r2 > 0.999). Since strain softening effects were significantly greater than viscoelastic effects, we conclude that history-dependent changes in jejunal stiffness are more likely to involve alterations to elastic rather than viscous structures in the tissue. These effects must be taken into account when performing balloon distension studies in the gastrointestinal tract for studying physiological and pathophysiological problems in which loading conditions are altered, e.g., mechanoreceptor studies in normal intestine and in acute and chronic obstruction, in order to have an accurate description of the biomechanics. © 1998 Biomedical Engineering Society.
PAC98: 8745Bp
Similar content being viewed by others
REFERENCES
Bayliss, V. M., and E. H. Starling. The movements and innervation of the small intestine. J. Physiol. (London)26:125-138, 1901.
Coolsaet, B L. R. A., W. A. van Duyl, R. van Mastrigt, and A. van der Zwart. Viscoelastic properties of the bladder wall. Urol. Int.30:16-26, 1975.
Deng, S. X., J. Tomioka, J. C. Debes, and Y. C. Fung. New experiments on shear modulus of elasticity of arteries. Am. J. Physiol.266:H1-H10, 1994.
Emery, J. L., J. H. Omens, and A. D. McCulloch. Strain softening in rat left ventricular myocardium. J. Biomech. Eng.119:6-12, 1997.
Fackler, K., L. Klein, and A. Hiltner. Polarizing light microscopy of intestine and its relationship to mechanical behaviour. J. Microsc.124:305-311, 1981.
Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissue, 2nd ed. New York: Springer, 1993.
Gabella, G. Structure of muscles and nerves in the gastrointestinal tract. In: Physiology of the Gastrointestinal Tract, 2nd ed., edited by L. R. Johnson, J. Christensen, M. J. Jackson, E. D. Jacobson, and J. H. Walsh. New York: Raven, 1987, pp. 335-382.
Gregersen, H., I. M. Giversen, L. M. Rasmussen, and A. Tøttrup. Biomechanical wall properties and collagen content in the partially obstructed opossum esophagus. Gastroenterology103:1547-1551, 1992.
Gregersen, H., C. S. Jørgensen, and F. H. Dall. Biomechanical wall properties in the isolated perfused porcine duodenum. An experimental study using impedance planimetry. J. Gastrointest. Motil.4:125-135, 1992.
Gregersen, H., G. S. Kassab, E. Pallencoea, C. Lee, S. Chien, R. Skalak, and Y. C. Fung. Morphometry and strain distribution in the guinea-pig duodenum with reference to the zero-stress state. Am. J. Physiol. 273:G865-G874, 1997.
Johnson, M., and M. Beatty. The Mullins effect in uniaxial extension and its influence on the transverse vibration of a rubber string. Continuum Mech. Thermodyn.5:83-115, 1993.
Jørgensen, C. J., F. H. Dall, S. L. Jensen, and H. Gregersen. A new combined ultrasound-impedance planimetry measuring system for quantification of organ wall biomechanics in vivo. J. Biomech.28:863-867, 1995.
Juhl, C. O., L. Vinter-Jensen, J. C. Djurhuus, H. Gregersen, and E. Z. Dajani. Biomechanical properties of the oesophagus damaged by endoscopic sclerotherapy. An impedance planimetric study in minipigs. Scand. J. Gastroenterol.29:867-873, 1994.
Kellow, J. E., T. J. Borody, S. F. Phillips, R. L. Tucker, and A. C. Haddad. Human interdigestive motility: variations in patterns from esophagus to colon. Gastroenterology91:386- 395, 1986.
Mullins, L. Effect of stretching on the properties of rubber. J. Rubber. Res.16:275-289, 1947.
Orberg, J., E. Baer, and J. Hiltner. Organization of collagen fibers in the intestine. Connective Tissue Res.11:285-297, 1983.
Price, J. M., P. J. Patitucci, and Y. C. Fung. Mechanical properties of resting taenia coli smooth muscle. Am. J. Physiol.236:C211-C222, 1979.
Ravinder, K. M., J. Ren, R. W. McCallum, H. A. Shaffer, and J. Sluss. Modulation of feline oesophageal contractions by bolus volume and outflow obstruction. Am. J. Physiol.258:G208-G215, 1990.
Rouillon, J.-M., F. Azpiroz, and J.-R. Malagelada. Reflex changes in intestinal tone: relationship to perception. Am. J. Physiol.261:G280-G286, 1991.
Siegle, M.-L., and H.-J. Ehrlein. Effects of various agents on ileal postprandial motor patterns and transit of chyme in dogs. Am. J. Physiol.257:G698-G703, 1989.
Tanaka, T. T., and Y. C. Fung. Elastic and inelastic properties of the canine aorta and their variation along the aortic tree. J. Biomech.7:357-370, 1974.
Tung, H.-N., K. Schulze-Delrieu, S. Shirazi, S. Noel, Q. Xia, and K. Cue. Hypertrophic smooth muscle in the partially obstructed opossum esophagus. The model: histological and ultrastructural observations. Gastroenterology100:853-864, 1991.
Villadsen, G. E., J. A. K. Petersen, L. Vinter-Jensen, C. O. Juhl, and H. Gregersen. Impedance planimetric characterisation of the normal and diseased oesophagus. Surg. Res. Comm.17:225-242, 1995.
Weems, W. A. Intestinal fluid flow: Its production and control. In: Physiology of the Gastrointestinal Tract, edited by L. R. Johnson, J. Christensen, M. J. Jackson, E. D. Jacobson, and J. H. Walsh. New York: Raven, 1987, pp. 571-593.
Weisbrodt, N. W. Motility of the small intestine. In: Physiology of the Gastrointestinal Tract, 2nd ed., edited by L. R. Johnson, J. Christensen, M. J. Jackson, E. D. Jacobson, and J. H. Walsh. New York: Raven, 1987, pp. 631-664.
Yamada, H. Strength of Biological Materials. Baltimore, MD: Williams and Wilkins, 1970.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gregersen, H., Emery, J.L. & McCulloch, A.D. History-Dependent Mechanical Behavior of Guinea-Pig Small Intestine. Annals of Biomedical Engineering 26, 850–858 (1998). https://doi.org/10.1114/1.109
Issue Date:
DOI: https://doi.org/10.1114/1.109