Research Papers

In Vivo Layer-Specific Mechanical Characterization of Porcine Stomach Tissue Using a Customized Ultrasound Elastography System

[+] Author and Article Information
Saurabh Dargar, Uwe Kruger

Center for Modeling, Simulation and
Imaging in Medicine (CeMSIM),
Rensselaer Polytechnic Institute,
Troy, NY 12180;
Department of Biomedical Engineering,
Rensselaer Polytechnic Institute,
Troy, NY 12180


Center for Modeling, Simulation and
Imaging in Medicine (CeMSIM),
Rensselaer Polytechnic Institute,
Troy, NY 12180

Suvranu De

Center for Modeling, Simulation and
Imaging in Medicine (CeMSIM),
Rensselaer Polytechnic Institute,
Troy, NY 12180;
Department of Biomedical Engineering,
Rensselaer Polytechnic Institute,
Troy, NY 12180;
Department of Mechanical, Aerospace, and
Nuclear Engineering,
Rensselaer Polytechnic Institute,
Troy, NY 12180

1Corresponding author.

Manuscript received March 24, 2018; final manuscript received March 4, 2019; published online July 11, 2019. Assoc. Editor: Raffaella De Vita.

J Biomech Eng 141(10), 101004 (Jul 11, 2019) (10 pages) Paper No: BIO-18-1154; doi: 10.1115/1.4043259 History: Received March 24, 2018; Revised March 04, 2019

This paper presents in vivo mechanical characterization of the muscularis, submucosa, and mucosa of the porcine stomach wall under large deformation loading. This is particularly important for the development of gastrointestinal pathology-specific surgical intervention techniques. The study is based on testing the cardiac and fundic glandular stomach regions using a custom-developed compression ultrasound elastography system. Particular attention has been paid to elucidate the heterogeneity and anisotropy of tissue response. A Fung hyperelastic material model has been used to model the mechanical response of each tissue layer. A univariate analysis comparing the initial shear moduli of the three layers indicates that the muscularis (5.69 ± 4.06 kPa) is the stiffest followed by the submucosa (3.04 ± 3.32 kPa) and the mucosa (0.56 ± 0.28 kPa). The muscularis is found to be strongly distinguishable from the mucosa tissue in the cardiac and fundic regions based on a multivariate discriminant analysis. The cardiac muscularis is observed to be stiffer than the fundic muscularis tissue (shear moduli of 7.96 ± 3.82 kPa versus 3.42 ± 2.96 kPa), more anisotropic (anisotropic parameter of 2.21 ± 0.77 versus 1.41 ± 0.38), and strongly distinguishable from its fundic counterpart. The results are consistent with the tissue morphology and are in accordance with our previous ex vivo tissue study. Finally, a univariate comparison of the in vivo and ex vivo initial shear moduli for each layer shows that the muscularis and submucosa tissues are softer while in vivo, but the mucosa tissue is stiffer while in vivo. The results concerning the mechanical properties highlight the inhomogeneity and anisotropy of multilayer stomach tissue.

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Fung, Y. , 2013, Biomechanics: Mechanical Properties of Living Tissues, Springer Science & Business Media, New York.
Krouskop, T. A. , Wheeler, T. M. , Kallel, F. , Garra, B. S. , and Hall, T. , 1998, “ Elastic Moduli of Breast and Prostate Tissues Under Compression,” Ultrason. Imaging, 20(4), pp. 260–274. [CrossRef] [PubMed]
Ottensmeyer, M. P. , and Salisbury, J. K., Jr. , 2001, In Vivo Data Acquisition Instrument for Solid Organ Mechanical Property Measurement, Springer, Berlin, pp. 975–982.
Gotoda, T. , Yamamoto, H. , and Soetikno, R. M. , 2006, “ Endoscopic Submucosal Dissection of Early Gastric Cancer,” J. Gastroenterol., 41(10), pp. 929–942. [CrossRef] [PubMed]
Ono, H. , Kondo, H. , Gotoda, T. , Shirao, K. , Yamaguchi, H. , Saito, D. , Hosokawa, K. , Shimoda, T. , and Yoshida, S. , 2001, “ Endoscopic Mucosal Resection for Treatment of Early Gastric Cancer,” Gut, 48(2), pp. 225–229. [CrossRef] [PubMed]
Inoue, H. , Minami, H. , Kobayashi, Y. , Sato, Y. , Kaga, M. , Suzuki, M. , Satodate, H. , Odaka, N. , Itoh, H. , and Kudo, S. , 2010, “ Peroral Endoscopic Myotomy (POEM) for Esophageal Achalasia,” Endoscopy, 42(4), pp. 265–271. [CrossRef] [PubMed]
Ikeda, K. , Mosse, C. A. , Park, P.-O. , Fritscher-Ravens, A. , Bergström, M. , Mills, T. , Tajiri, H. , and Swain, C. P. , 2006, “ Endoscopic Full-Thickness Resection: Circumferential Cutting Method,” Gastrointest. Endosc., 64(1), pp. 82–89. [CrossRef] [PubMed]
Cai, M. , Zhou, P. , Lourenço, L. C. , and Zhang, D. , 2016, “ Endoscopic Full-Thickness Resection (EFTR) for Gastrointestinal Subepithelial Tumors,” Gastrointest. Endosc. Clin. N. Am., 26(2), pp. 283–295. [CrossRef] [PubMed]
Reddy, N. , and Rao, P. , 2004, “ Per Oral Transgastric Endoscopic Appendectomy Human,” 45th Annual Conference of the Society of Gastrointestinal Endoscopy of India, Jaipur, India, pp. 28–29.
de Sousa, L. , de Sousa, J. , de Sousa Filho, L. , de Sousa, M. , de Sousa, V. , de Sousa, A. , and Zorron, R. , 2009, “ Totally NOTES (T-NOTES) Transvaginal Cholecystectomy Using Two Endoscopes: Preliminary Report,” Surg. Endosc., 23(11), pp. 2550–2555–2555. [CrossRef] [PubMed]
Rao, S. , Hayek, B. , and Summers, R. , 1995, “ Impedance Planimetry: An Integrated Approach for Assessing Sensory, Active, and Passive Biomechanical Properties of the Human Esophagus,” Am. J. Gastroenterol., 90(3), pp. 431–438. https://www.ncbi.nlm.nih.gov/pubmed/7872283 [PubMed]
Villadsen, G. E. , Storkholm, J. H. , Hendel, L. , Vilstrup, H. , and Gregersen, H. , 1997, “ Impedance Planimetric Characterization of Esophagus in Systemic Sclerosis Patients With Severe Involvement of Esophagus,” Dig. Dis. Sci., 42(11), pp. 2317–2326. [CrossRef] [PubMed]
Patel, R. S. , and Rao, S. S. C. , 1998, “ Biomechanical and Sensory Parameters of the Human Esophagus at Four Levels,” Am. J. Physiol.-Gastrointest. Liver Physiol., 275(2), pp. G187–G191. [CrossRef]
Assentoft, J. , Gregersen, H. , and O'brien, W. , 2000, “ Determination of Biomechanical Properties in Guinea Pig Esophagus by Means of High Frequency Ultrasound and Impedance Planimetry,” Dig. Dis. Sci., 45(7), pp. 1260–1266. [CrossRef] [PubMed]
Kwiatek, M. A. , Hirano, I. , Kahrilas, P. J. , Rothe, J. , Luger, D. , and Pandolfino, J. E. , 2011, “ Mechanical Properties of the Esophagus in Eosinophilic Esophagitis,” Gastroenterology, 140(1), pp. 82–90. [CrossRef] [PubMed]
McMahon, B. P. , Rao, S. S. C. , Gregersen, H. , Kwiatek, M. A. , Pandolfino, J. E. , Drewes, A. M. , Krarup, A. L. , Lottrup, C. , and Frøkjaer, J. B. , 2011, “ Distensibility Testing of the Esophagus,” Ann. N. Y. Acad. Sci., 1232(1), pp. 331–340. [CrossRef] [PubMed]
Takeda, T. , Nabae, T. , Kassab, G. , Liu, J. , and Mittal, R. K. , 2004, “ Oesophageal Wall Stretch: The Stimulus for Distension Induced Oesophageal Sensation,” Neurogastroenterol. Motil., 16(6), pp. 721–728. [CrossRef] [PubMed]
Jørgensen, C. , Dall, F. , Jensen, S. , and Gregersen, H. , 1995, “ A New Combined High-Frequency Ultrasound-Impedance Planimetry Measuring System for the Quantification of Organ Wall Biomechanics In Vivo,” J. Biomech., 28(7), pp. 863–867. [CrossRef] [PubMed]
Sokolis, D. P. , Orfanidis, I. K. , and Peroulis, M. , 2011, “ Biomechanical Testing and Material Characterization for the Rat Large Intestine: Regional Dependence of Material Parameters,” Physiol. Meas., 32(12), pp. 1969–1982. [CrossRef] [PubMed]
Higa, M. , Luo, Y. , Okuyama, T. , Takagi, T. , Shiraishi, Y. , and Yambe, T. , 2007, “ Passive Mechanical Properties of Large Intestine Under In Vivo and In Vivo Compression,” Med. Eng. Phys., 29(8), pp. 840–844. [CrossRef] [PubMed]
Zhao, J. , Liao, D. , Chen, P. , Kunwald, P. , and Gregersen, H. , 2008, “ Stomach Stress and Strain Depend on Location, Direction and the Layered Structure,” J. Biomech., 41(16), pp. 3441–3447. [CrossRef] [PubMed]
Jia, Z. , Li, W. , and Zhou, Z. , 2015, “ Mechanical Characterization of Stomach Tissue Under Uniaxial Tensile Action,” J. Biomech., 48(4), pp. 651–658. [CrossRef] [PubMed]
Tottrup, A. , Forman, A. , Uldbjerg, N. , Funch-Jensen, P. , and Andersson, K. E. , 1990, “ Mechanical Properties of Isolated Human Esophageal Smooth Muscle,” Am. J. Physiol.-Gastrointest. Liver Physiol., 258(3), pp. G338–G343. [CrossRef]
Yang, J. , Zhao, J. , Liao, D. , and Gregersen, H. , 2006, “ Biomechanical Properties of the Layered Oesophagus and Its Remodelling in Experimental Type-1 Diabetes,” J. Biomech., 39(5), pp. 894–904. [CrossRef] [PubMed]
Stavropoulou, E. A. , Dafalias, Y. F. , and Sokolis, D. P. , 2009, “ Biomechanical and Histological Characteristics of Passive Esophagus: Experimental Investigation and Comparative Constitutive Modeling,” J. Biomech., 42(16), pp. 2654–2663. [CrossRef] [PubMed]
Natali, A. N. , Carniel, E. L. , and Gregersen, H. , 2009, “ Biomechanical Behaviour of Oesophageal Tissues: Material and Structural Configuration, Experimental Data and Constitutive Analysis,” Med. Eng. Phys., 31(9), pp. 1056–1062. [CrossRef] [PubMed]
Sommer, G. , Schriefl, A. , Zeindlinger, G. , Katzensteiner, A. , Ainödhofer, H. , Saxena, A. , and Holzapfel, G. A. , 2013, “ Multiaxial Mechanical Response and Constitutive Modeling of Esophageal Tissues: Impact on Esophageal Tissue Engineering,” Acta Biomater., 9(12), pp. 9379–9391. [CrossRef] [PubMed]
Dargar, S. , Akyildiz, A. C. , and De, S. , 2017, “ In Situ Mechanical Characterization of Multilayer Soft Tissue Using Ultrasound Imaging,” IEEE Trans. Biomed. Eng., 64(11), pp. 2595–2606. https://www.ncbi.nlm.nih.gov/pubmed/28026748 [PubMed]
Zhao, J. , Liao, D. , and Gregersen, H. , 2005, “ Tension and Stress in the Rat and Rabbit Stomach Are Location‐and Direction‐Dependent,” Neurogastroenterol. Motil., 17(3), pp. 388–398. [CrossRef] [PubMed]
Klein, S. , Staring, M. , Murphy, K. , Viergever, M. , and Pluim, J. P. , 2010, “ Elastix: A Toolbox for Intensity-Based Medical Image Registration,” IEEE Trans. Med. Imaging, 29(1), pp. 196–205. [CrossRef] [PubMed]
Tong, P. , and Fung, Y.-C. , 1976, “ The Stress-Strain Relationship for the Skin,” J. Biomech., 9(10), pp. 649–657. [CrossRef] [PubMed]
Humphrey, J. , Vawter, D. , and Vito, R. , 1986, “ Mechanical Behavior of Excised Canine Visceral Pleura,” Ann. Biomed. Eng., 14(5), pp. 451–466. [CrossRef] [PubMed]
Humphrey, J. , Strumpf, R. , and Yin, F. , 1992, “ A Constitutive Theory for Biomembranes: Application to Epicardial Mechanics,” ASME J. Biomech. Eng., 114(4), pp. 461–466. https://biomechanical.asmedigitalcollection.asme.org/article.aspx?articleid=1398946
Chew, P. H. , Yin, F. C. , and Zeger, S. L. , 1986, “ Biaxial Stress-Strain Properties of Canine Pericardium,” J. Mol. Cell. Cardiol., 18(6), pp. 567–578. [CrossRef] [PubMed]
Holzapfel, G. A. , Gasser, T. C. , and Ogden, R. W. , 2004, “ Comparison of a Multi-Layer Structural Model for Arterial Walls With a Fung-Type Model, and Issues of Material Stability,” ASME J. Biomech. Eng., 126(2), pp. 264–275. [CrossRef]
Holzapfel, G. A. , 2006, “ Determination of Material Models for Arterial Walls From Uniaxial Extension Tests and Histological Structure,” J. Theor. Biol., 238(2), pp. 290–302. [CrossRef] [PubMed]
Spilker, R. L. , Donzelli, P. S. , and Mow, V. C. , 1992, “ A Transversely Isotropic Biphasic Finite Element Model of the Meniscus,” J. Biomech., 25(9), pp. 1027–1045. [CrossRef] [PubMed]
Donzelli, P. S. , Spilker, R. L. , Ateshian, G. A. , and Mow, V. C. , 1999, “ Contact Analysis of Biphasic Transversely Isotropic Cartilage Layers and Correlations With Tissue Failure,” J. Biomech., 32(10), pp. 1037–1047. [CrossRef] [PubMed]
Feng, Y. , Okamoto, R. J. , Namani, R. , Genin, G. M. , and Bayly, P. V. , 2013, “ Measurements of Mechanical Anisotropy in Brain Tissue and Implications for Transversely Isotropic Material Models of White Matter,” J. Mech. Behav. Biomed. Mater., 23, pp. 117–132. [CrossRef] [PubMed]
Tepole, A. B. , Gosain, A. K. , and Kuhl, E. , 2012, “ Stretching Skin: The Physiological Limit and Beyond,” Int. J. Non-Linear Mech., 47(8), pp. 938–949. [CrossRef] [PubMed]
Prot, V. , Skallerud, B. , and Holzapfel, G. , 2007, “ Transversely Isotropic Membrane Shells With Application to Mitral Valve Mechanics—Constitutive Modelling and Finite Element Implementation,” Int. J. Numer. Methods Eng., 71(8), pp. 987–1008. [CrossRef]
Chui, C. , Kobayashi, E. , Chen, X. , Hisada, T. , and Sakuma, I. , 2007, “ Transversely Isotropic Properties of Porcine Liver Tissue: Experiments and Constitutive Modelling,” Med. Biol. Eng. Comput., 45(1), pp. 99–106. [CrossRef] [PubMed]
Morrow, D. A. , Donahue, T. L. H. , Odegard, G. M. , and Kaufman, K. R. , 2010, “ Transversely Isotropic Tensile Material Properties of Skeletal Muscle Tissue,” J. Mech. Behav. Biomed. Mater., 3(1), pp. 124–129. [CrossRef] [PubMed]
Barbone, P. E. , and Gokhale, N. H. , 2004, “ Elastic Modulus Imaging: On the Uniqueness and Nonuniqueness of the Elastography Inverse Problem in Two Dimensions,” Inverse Probl., 20(1), p. 283. [CrossRef]
Byrd, R. H. , Schnabel, R. B. , and Shultz, G. A. , 1988, “ Approximate Solution of the Trust Region Problem by Minimization Over Two-Dimensional Subspaces,” Math. Program., 40(1–3), pp. 247–263. https://link.springer.com/article/10.1007/BF01580735
Speirs, D. , de Souza Neto, E. , and Perić, D. , 2008, “ An Approach to the Mechanical Constitutive Modelling of Arterial Tissue Based on Homogenization and Optimization,” J. Biomech., 41(12), pp. 2673–2680. [CrossRef] [PubMed]
Davis, F. M. , and De Vita, R. , 2012, “ A Nonlinear Constitutive Model for Stress Relaxation in Ligaments and Tendons,” Ann. Biomed. Eng., 40(12), pp. 2541–2550. [CrossRef] [PubMed]
Zhong, Q. , Zeng, W. , Huang, X. , Su, M. , and Luo, Y. , 2014, “ Constitutive Modeling and Finite Element Analysis of Myxomatous Mitral Leaflet Tissue,” J. Mech. Med. Biol., 14(3), p. 1450031. [CrossRef]
Voigt, W. , 2014, Lehrbuch Der Kristallphysik (Mit Ausschluss Der Kristalloptik), Springer-Verlag, Wiesbaden, Germany.
Mika, S. , Ratsch, G. , Weston, J. , Scholkopf, B. , and Mullers, K.-R. , 1999, “ Fisher Discriminant Analysis With Kernels,” Neural Networks for Signal Processing IX: Proceedings of the 1999 IEEE Signal Processing Society Workshop, Madison, WI, Aug. 25, pp. 41–48.
Izenman, A. J. , 2013, “ Linear Discriminant Analysis,” Modern Multivariate Statistical Techniques, Springer, Berlin, pp. 237–280.
Silverman, B. W. , 1986, Density Estimation for Statistics and Data Analysis, CRC Press, New York.
Gazis, D. , Tadjbakhsh, I. , and Toupin, R. , 1963, “ The Elastic Tensor of Given Symmetry Nearest to an Anisotropic Elastic Tensor,” Acta Crystallogr., 16(9), pp. 917–922. [CrossRef]
Norris, A. N. , 2007, “ Quadratic Invariants of Elastic Moduli,” Q. J. Mech. Appl. Math., 60(3), pp. 367–389. [CrossRef]
Norris, A. N. , 2006, “ Elastic Moduli Approximation of Higher Symmetry for the Acoustical Properties of an Anisotropic Material,” J. Acoust. Soc. Am., 119(4), pp. 2114–2121. [CrossRef] [PubMed]
Moakher, M. , and Norris, A. N. , 2006, “ The Closest Elastic Tensor of Arbitrary Symmetry to an Elasticity Tensor of Lower Symmetry,” J. Elast., 85(3), pp. 215–263. [CrossRef]
Fedorov, F. I. , 2013, Theory of Elastic Waves in Crystals, Springer Science & Business Media, New York.
Schummer, A. , Nickel, R. , and Sack, W. , 1979, “ The Viscera of the Domestic Mammals,” Textb. Anat. Domest. Anim., 2, pp. 52–56. https://books.google.com/books/about/The_Viscera_of_the_Domestic_Mammals.html?id=0rDhBwAAQBAJ&printsec=frontcover&source=kp_read_button#v=onepage&q&f=false
Stachura, J. , Tarnawski, A. , and Dąbroś, W. , 1993, “ Apoptosis: Genetically Programmed Physiologic Cell Loss in Normal Gastric Oxyntic Mucosa and in Mucosa of Grossly Healed Gastric Ulcer,” J. Clin. Gastroenterol., 17, pp. S70–S77. [CrossRef] [PubMed]
Konturek, P. C. , Brzozowski, T. , Konturek, S. , Pajdo, R. , Konturek, J. , Kwiecień, S. , Taut, A. , and Hahn, E. , 1999, “ Apoptosis in Gastric Mucosa With Stress-Induced Gastric Ulcers,” J. Physiol. Pharmacol. Off. J. Pol. Physiol. Soc., 50(2), pp. 211–225. https://europepmc.org/abstract/med/10424718
Ito, S. , and Lacy, E. R. , 1985, “ Morphology of Rat Gastric Mucosal Damage, Defense, and Restitution in the Presence of Luminal Ethanol,” Gastroenterology, 88(1), pp. 250–260. [CrossRef] [PubMed]


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Fig. 1

(a) Schematic of the porcine stomach with the respective regions and (b) a schematic illustrating the in vivo stomach placed onto the tissue-staging platform for compression testing

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Fig. 2

The experimental setup in the operating room with the testing apparatus visualized

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Fig. 3

Thickness of each layer measured by ultrasound (*statistically significant)

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Fig. 4

Stress-stretch behavior of the full thickness stomach in the fundic and cardiac glandular regions in response to 20% compression loading

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Fig. 5

(a) Comparison of force and displacement from the experiment and optimized simulation for three representative cases and (b) the total error for each time point used in the optimization routine for three representative samples (A, B, and C)

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Fig. 6

Comparison of the in-plane and out-of-plane stress stretch responses calculated from the optimized material models for the cardiac (a) muscularis, (b) submucosa, (c) mucosa and the fundic, (d) muscularis, (e) submucosa, and (f) mucosa. (C indicates cardiac and F indicates fundic)

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Fig. 7

(a) Comparison of the shear modulus between the cardiac and fundic regions for each layer and (b) comparison of the shear moduli for in vivo and ex vivo porcine stomach tissue layers (* statistically significant)

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Fig. 8

((a) and (c)) The PDFs obtained using kernel density estimation from a linear combination of the six material parameters for the muscularis, submucosa, and mucosal layers from ten animals in two locations accompanied by ((b) and (d)) the scatter plots of the t1 and t2 scores from the LDA for each layer. (* statistically significant)

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Fig. 9

The LDA classification results and the corresponding misclassification results for ((a) and (b)) fundic muscularis and mucosa, ((c) and (d)) cardiac muscularis and mucosa, and ((e) and (f)) fundic and cardiac muscularis. The type I error is defined as 0.05. The misclassification error is defined as the error rate of a particular layer being incorrectly classified.

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Fig. 10

Comparison of the anisotropic distance parameter between the cardiac and fundic regions for each layer (* statistically significant)



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