Abstract
Significant stress softening recovery after potassium chloride (KCl) administration was previously demonstrated in the intact rat esophageal wall. The aim of this study is to investigate the effect of KCl activation on stress softening recovery in the separated mucosa–submucosa layer and muscle layer of rat esophagus. Three series of loading–unloading distensions were carried out on 10 rat esophagi where the two separated layers were distended at luminal pressure levels 0.5, 1.0 and 2.0 kPa. Numerous distension cycles were done in \(\hbox {Ca}^{2+}\)-free Krebs solution before and after activation with KCl (110 mmol) for 3 min in calcium-containing media. The diameter and luminal pressure were recorded for stress and strain calculation. During KCl activation, the muscle layer responded with a high-amplitude contraction, and the mucosa–submucosa layer responded with a longer-lasting low-amplitude contraction. The hysteresis loop areas from the muscle layer were significantly bigger than those from the mucosa–submucosa layer at distension pressures 1.0 and 2.0 kPa (\({F}>4.9, {p}<0.001\)). The calculated stiffness in the mucosa–submucosa layer was significantly higher than that in the muscle layer (\({p}<0.001\)). After activation with KCl, the stored energy and the stiffness after the stress and viscoelasticity softening increased in both layers, indicating that the reversible stress softening in esophagus after KCl activation is existed in both layers.
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D’Angelo WA, Fries JF, Masi AT, Shulman LE (1969) Pathologic observations in systemic sclerosis (scleroderma). A study of fifty-eight autopsy cases and fifty-eight matched controls. Am J Med 46(3):428–440
Fan Y, Gregersen H, Kassab GS (2004) A two-layered mechanical model of the rat esophagus. Experiment and theory. Biomed Eng Online. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC528839/
Fan Y, Zhao J, Liao D, Gregersen H (2005) The effect of digestion of collagen and elastin on histomorphometry and the zero-stress state in rat esophagus. Dig Dis Sci 50(8):1497–1505
Gregersen H, Emery JL, McCulloch AD (1998) History-dependent mechanical behavior of guinea-pig small intestine. Ann Biomed Eng 26(5):850–858
Gregersen H, Lee TC, Chien S, Skalak R, Fung YC (1999) Strain distribution in the layered wall of the esophagus. J Biomech Eng 121(5):442–448
Gregersen H (2002) Biomechanics of the gastrointestinal tract: new perspective in motility research and diagnostics. Springer, London
Gregersen H, Liao D, Fung YC (2008) Determination of homeostatic elastic moduli in two layers of the esophagus. J Biomech Eng 130(1):011005
Gregersen H, Villadsen GE, Liao D (2011) Mechanical characteristics of distension-evoked peristaltic contractions in the esophagus of systemic sclerosis patients. Dig Dis Sci 56(12):3559–3568
Jiang H, Liao D, Zhao J, Wang G, Gregersen H (2014) Contractions reverse stress softening in rat esophagus. Ann Biomed Eng 42(8):1717–1728
Kuo B, Urma D (2006) Esophagus: anatomy and development. GI Motil online. http://www.nature.com/gimo/contents/pt1/full/gimo6.html. Accessed 16 May 2006
Liao D, Fan Y, Zeng Y, Gregersen H (2003) Stress distribution in the layered wall of the rat oesophagus. Med Eng Phys 25(9):731–738
Liao D, Zhao J, Fan Y, Gregersen H (2004) Two-layered quasi-3D finite element model of the oesophagus. Med Eng Phys 26(7):535–543
Liao D, Zhao J, Kunwald P, Gregersen H (2009) Tissue softening of guinea pig oesophagus tested by the tri-axial test machine. J Biomech 42(7):804–810
Lu X, Gregersen H (2001) Regional distribution of axial strain and circumferential residual strain in the layered rabbit oesophagus. J Biomech 34(2):225–233
Matsumoto T, Hayashi K (1996) Stress and strain distribution in hypertensive and normotensive rat aorta considering residual strain. J Biomech Eng 118(1):62–73
Moonen A, Boeckxstaens G (2014) Measuring mechanical properties of the esophageal wall using impedance planimetry. Gastrointest Endosc Clin N Am 24(4):607–618
Natali AN, Carniel EL, Gregersen H (2009) Biomechanical behaviour of oesophageal tissues: material and structural configuration, experimental data and constitutive analysis. Med Eng Phys 31(9):1056–1062
Nurko S, Rosen R (2008) Esophageal dysmotility in patients who have eosinophilic esophagitis. Gastrointest Endosc Clin N Am 18(1):73–89
Peterson SJ, Okamoto RJ (2000) Effect of residual stress and heterogeneity on circumferential stress in the arterial wall. J Biomech Eng 122(4):454–456
Ratz PH, Berg KM, Urban NH, Miner AS (2005) Regulation of smooth muscle calcium sensitivity: KCl as a calcium-sensitizing stimulus. Am J Physiol Cell Physiol 288(4):C769–783
Ratz PH, Speich JE (2010) Evidence that actomyosin cross bridges contribute to ”passive” tension in detrusor smooth muscle. Am J Physiol Renal Physiol 298(6):F1424–1435
Sokolis DP (2010) Strain-energy function and three-dimensional stress distribution in esophageal biomechanics. J Biomech 43(14):2753–2764
Sokolis DP (2013) Structurally-motivated characterization of the passive pseudo-elastic response of esophagus and its layers. Comput Biol Med 43(9):1273–1285
Sommer G, Schriefl A, Zeindlinger G et al (2013) Multiaxial mechanical response and constitutive modeling of esophageal tissues: Impact on esophageal tissue engineering. Acta Biomater 9(12):9379–9391
Speich JE, Borgsmiller L, Call C, Mohr R, Ratz PH (2005) ROK-induced cross-link formation stiffens passive muscle: reversible strain-induced stress softening in rabbit detrusor. Am J Physiol Cell Physiol 289(1):12–21
Speich JE, Dosier C, Borgsmiller L, Quintero K, Koo HP, Ratz PH (2007) Adjustable passive length-tension curve in rabbit detrusor smooth muscle. J Appl Physiol 102(5):1746–1755
Stavropoulou EA, Dafalias YF, Sokolis DP (2012) Biomechanical behavior and histological organization of the three-layered passive esophagus as a function of topography. Proc Inst Mech Eng Part H 226(6):477–490
Taber LA, Humphrey JD (2001) Stress-modulated growth, residual stress and vascular heterogeneity. J Biomech Eng 123(6):528–535
Villadsen GE, Storkholm J, Zachariae H, Hendel L, Bendtsen F, Gregersen H (2001) Oesophageal pressure-cross-sectional area distributions and secondary peristalsis in relation to subclassification of systemic sclerosis. Neurogastroenterol Motil 13(3):199–210
Williams RB, Pal A, Brasseur JG, Cook IJ (2001) Space-time pressure structure of pharyngo-esophageal segment during swallowing. Am J Physiol Gastrointest Liver Physiol 281(5):G1290–1300
Yang J, Zhao J, Liao D, Gregersen H (2006) Biomechanical properties of the layered oesophagus and its remodeling in experimental type-1 diabetes. J Biomech 39(5):894–904
Yang W, Fung TC, Chian KS, Chong CK (2006a) Directional, regional, and layer variations of mechanical properties of esophageal tissue and its interpretation using a structure-based constitutive model. J Biomech Eng 128(3):409–418
Yang W, Fung TC, Chian KS, Chong CK (2006b) 3D Mechanical properties of the layered esophagus: experiment and constitutive model. J Biomech Eng 128(6):899–908
Yang W, Fung TC, Chian KS, Chong CK (2007) Three-dimensional finite element model of the two-layered oesophagus, including the effects of residual strains and buckling of mucosa. Proc Inst Mech Eng Part H 221(4):417–426
Zhao J, Chen X, Yang J, Liao D, Gregersen H (2007) Opening angle and residual strain in a three-layered model of pig oesophagus. J Biomech 40(14):3187–3192
Zhao J, Liao D, Gregersen H (2010) Biomechanics of the gastrointestinal tract in health and disease. In: Jerrod HL (ed) Biomechanics: principles, trends and applications. Nova Publishers, New York, pp 163–206
Acknowledgements
This study was partially supported by a grant from Chongqing Science and Technology Commission (cstc2013kjrc-ljrccj10003) and National “111 Plan” Base (B06023) and the Public Experiment Center of State Bioindustrial Base (Chongqing), China.
Conflict of interest
Approval of the animal experiment in this study was obtained from the Danish Committee for Animal Experimentation. This study was partially supported by a grant from Chongqing Science and Technology Commission (cstc2013kjrc-ljrccj10003). The authors declare that they have no conflict of interest for this work.
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Jiang, H., Liao, D., Zhao, J. et al. Reversible stress softening in layered rat esophagus in vitro after potassium chloride activation. Biomech Model Mechanobiol 16, 1065–1075 (2017). https://doi.org/10.1007/s10237-017-0873-y
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DOI: https://doi.org/10.1007/s10237-017-0873-y