Digestive Diseases and Sciences

, Volume 53, Issue 12, pp 3145–3151 | Cite as

Phasic and Tonic Stress–Strain Data Obtained in Intact Intestinal Segment In Vitro

Original Paper

Abstract

The function of the small intestine is to a large degree mechanical, and it has the capability of deforming its shape by generating phasic (short-lasting) and tonic (sustained) contraction of the smooth muscle layers. The aim of this study was to obtain phasic and tonic stress–strain (normalized force–length) curves during distension of isolated rat jejunum and ileum (somewhat similar to the isometric length–tension diagram known from in vitro studies of muscle strips). We hypothesized that the circumferential stress–strain data depend on longitudinal stretch of the intestine. Intestinal segments were isolated from ten Wistar rats and put into an organ bath containing 37°C aerated Krebs solution. Ramp distension was done on active and passive intestinal segments at longitudinal stretch ratios of 0, 10, and 20%. Ramp pressures from 0 to 7.5 cmH2O were applied to the intestinal lumen at each longitudinal stretch ratio. Passive conditions were obtained by adding the calcium antagonist papaverine to the solution. Total and passive circumferential stress and strain were computed from the length, diameter and pressure data and from the zero-stress state geometry. The active stress was defined as the total stress minus the passive stress. The total and passive circumferential stresses increased exponentially as a function of the strain. The amplitude of both the total and passive stress was biggest in the jejunum. The total circumferential stress decreased whereas the passive circumferential stress increased when the intestine was stretched longitudinally. Consequently, longitudinal stretching caused the active circumferential stress to decrease. The passive circumferential stress during longitudinal stretching increased more in the jejunum than in the ileum. Therefore, the active circumferential stress decreased most in the jejunum. In conclusion, the circumferential active-passive stress and strain depend on the longitudinal stretch and differs between the jejunum and ileum.

Keywords

Intestine Rat Active stress Passive stress Length–tension diagram 

Notes

Acknowledgments

This study were partly financially supported by a grant from Karen Elise Jensen’s Foundation for Jingbo Zhao and NIH grant 1RO1DK072616-01A2. The technicians Ole Sørensen, Torben Madsen, and Jens Sørensen are thanked for handling the animals.

References

  1. 1.
    Gregersen H (2002) Biomechanics of the gastrointestinal tract. New perspectives in motility research and diagnostics. Springer, Berlin Heidelberg New YorkGoogle Scholar
  2. 2.
    Dou Y, Gregersen S, Zhao J, Zhuang F, Gregersen H (2002) Morphometric and biomechanical intestinal remodeling induced by fasting in rats. Dig Dis Sci 47:1158–1168. doi: 10.1023/A:1015019030514 PubMedCrossRefGoogle Scholar
  3. 3.
    Dou Y, Lu X, Zhao J, Gregersen H (2002) Morphometric and biomechanical remodelling in the intestine after small bowel resection in the rat. Neurogastroenterol Motil 14:43–53. doi: 10.1046/j.1365-2982.2002.00301.x PubMedCrossRefGoogle Scholar
  4. 4.
    Zhao J, Yang J, Gregersen H (2003) Biomechanical and morphometric intestinal remodelling during experimental diabetes in rats. Diabetologia 46:1688–1697. doi: 10.1007/s00125-003-1233-2 PubMedCrossRefGoogle Scholar
  5. 5.
    Zhao JB, Sha H, Zhuang FY, Gregersen H (2002) Morphological properties and residual strain along the small intestine in rats. World J Gastroenterol 8:312–317PubMedGoogle Scholar
  6. 6.
    Longhurst PA, Kang JS, Wein AJ, Levin RM (1990) Comparative length–tension relationship of urinary bladder strips from hamsters, rats, guinea-pigs, rabbits and cats. Comp Biochem Physiol A 96:221–225. doi: 10.1016/0300-9629(90)90069-5 PubMedCrossRefGoogle Scholar
  7. 7.
    Drewes AM, Schipper KP, Dimcevski G et al (2002) Multi-modal induction and assessment of allodynia and hyperalgesia in the human oesophagus. Eur J Pain 7:539–549. doi: 10.1016/S1090-3801(03)00053-3 CrossRefGoogle Scholar
  8. 8.
    Gao C, Arendt-Nielsen L, Liu W, Petersen P, Drewes AM, Gregersen H (2003) Sensory and biomechanical responses to ramp-controlled distension of the human duodenum. Am J Physiol Gastrointest Liver Physiol 284:G461–G471PubMedGoogle Scholar
  9. 9.
    Gregersen H, Gilja OH, Hausken T et al (2002) Mechanical properties in the human gastric antrum using B-mode ultrasonography and antral distension. Am J Physiol Gastrointest Liver Physiol 283:G368–G375PubMedGoogle Scholar
  10. 10.
    Yang J, Liao D, Zhao J, Gregersen H (2004) Shear modulus of elasticity of the esophagus. Ann Biomed Eng 32(9):1223–1230. doi: 10.1114/B:ABME.0000039356.24821.6c PubMedCrossRefGoogle Scholar
  11. 11.
    Lynn P, Zagorodnyuk V, Hennig G, Costa M, Brookes S (2005) Mechanical activation of rectal intraganglionic laminar endings in the guinea pig distal gut. J Physiol 564(Pt 2):589–601. doi: 10.1113/jphysiol.2004.080879 PubMedCrossRefGoogle Scholar
  12. 12.
    Dickson EJ, Spencer NJ, Hennig GW, Bayguinov PO, Ren J, Heredia DJ, Smith TK (2007) An enteric occult reflex underlies accommodation and slow transit in the distal large bowel. Gastroenterology 132(5):1912–1924. doi: 10.1053/j.gastro.2007.02.047 PubMedCrossRefGoogle Scholar
  13. 13.
    Pedersen J, Drewes AM, Gregersen H (2005) New analysis for the study of the muscle function in the human oesophagus. Neurogastroenterol Motil 17:767–772. doi: 10.1111/j.1365-2982.2005.00652.x PubMedCrossRefGoogle Scholar
  14. 14.
    Pedersen J, Gao C, Egekvist H et al (2003) Pain and biomechanical responses to distention of the duodenum in patients with systemic sclerosis. Gastroenterology 124:1230–1239. doi: 10.1016/S0016-5085(03)00265-8 PubMedCrossRefGoogle Scholar
  15. 15.
    Weems W (1987) Intestinal fluid flow: its production and control. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New YorkGoogle Scholar
  16. 16.
    Tottrup A, Forman A, Uldbjerg N, Funch-Jensen P, Andersson KE (1990) Mechanical properties of isolated human esophageal smooth muscle. Am J Physiol 1990:G338–G343Google Scholar
  17. 17.
    Brookes SJ, D’Antona G, Zagorodnyuk VP, Humphreys CM, Costa M (2001) Propagating contractions of the circular muscle evoked by slow stretch in flat sheets of guinea-pig ileum. Neurogastroenterol Motil 13(6):519–531. doi: 10.1046/j.1365-2982.2001.00290.x PubMedCrossRefGoogle Scholar
  18. 18.
    Gutierrez JA, Perr HA (1999) Mechanical stretch modulates TGF-beta1 and alpha1(I) collagen expression in fetal human intestinal smooth muscle cells. Am J Physiol 277(5 Pt 1):G1074–G1080PubMedGoogle Scholar
  19. 19.
    Koh SD, Sanders KM (2001) Stretch-dependent potassium channels in murine colonic smooth muscle cells. J Physiol 533(Pt 1):155–163. doi: 10.1111/j.1469-7793.2001.0155b.x PubMedCrossRefGoogle Scholar
  20. 20.
    Kunze WA, Furness JB, Bertrand PP, Bornstein JC (1998) Intracellular recording from myenteric neurons of the guinea-pig ileum that respond to stretch. J Physiol 506(Pt 3):827–842. doi: 10.1111/j.1469-7793.1998.827bv.x PubMedCrossRefGoogle Scholar
  21. 21.
    Miller SM, Szurszewski JH (2003) Circumferential, not longitudinal, colonic stretch increases synaptic input to mouse prevertebral ganglion neurons. Am J Physiol Gastrointest Liver Physiol 285(6):G1129–G1138PubMedGoogle Scholar
  22. 22.
    Spencer NJ, Hennig GW, Smith TK (2003) Stretch-activated neuronal pathways to longitudinal and circular muscle in guinea pig distal colon. Am J Physiol Gastrointest Liver Physiol 284(2):G231–G241PubMedGoogle Scholar
  23. 23.
    Miftakhov RN, Wingate DL (1994) Biomechanics of small bowel motility. Med Eng Phys 16(5):406–415. doi: 10.1016/1350-4533(90)90007-U PubMedCrossRefGoogle Scholar
  24. 24.
    Miftahof R, Akhmadeev N (2007) Dynamics of intestinal propulsion. J Theor Biol 246(2):377–393. doi: 10.1016/j.jtbi.2007.01.006 PubMedCrossRefGoogle Scholar
  25. 25.
    Gabella G (1990) Hypertrophy of visceral smooth muscle. Anat Embryol (Berl) 182(5):409–424. doi: 10.1007/BF00178906 Google Scholar
  26. 26.
    Storkholm JH, Zhao J, Villadsen GE, Hager H, Jensen SL, Gregersen H (2007) Biomechanical remodeling of the chronically obstructed Guinea pig small intestine. Dig Dis Sci 52(2):336–346. doi: 10.1007/s10620-006-9431-7 PubMedCrossRefGoogle Scholar
  27. 27.
    Dou Y, Zhao J, Gregersen H (2003) Morphology and stress–strain properties along the small intestine in the rat. J Biomech Eng 125:266–273. doi: 10.1115/1.1560140 PubMedCrossRefGoogle Scholar
  28. 28.
    Dou Y, Fan Y, Zhao J, Gregersen H (2006) Longitudinal residual strain and stress–strain relationship in rat small intestine. Biomed Eng Online 5:37. doi: 10.1186/1475-925X-5-37 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Center of Excellence in Visceral Biomechanics and PainAalborg Hospital Science and Innovation Center (AHSIC)AalborgDenmark
  2. 2.Center of Sensory-Motor InteractionAalborg UniversityAalborgDenmark
  3. 3.La Jolla Bioengineering InstituteLa JollaUSA

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