Skip to main content
SpringerLink
Log in

Simulation studies of the role of esophageal mucosa in bolus transport

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

Based on a fully coupled computational model for esophageal transport, we analyzed the role of the mucosa (including the submucosa) in esophageal bolus transport and how bolus transport is affected by mucosal stiffness. Two groups of studies were conducted using a computational model. In the first group, a base case that represents normal esophageal transport and two hypothetical cases were simulated: (1) esophageal mucosa replaced by muscle and (2) esophagus without mucosa. For the base case, the geometric configuration of the esophageal wall was examined and the mechanical role of mucosa was analyzed. For the hypothetical cases, the pressure field and transport features were examined. In the second group of studies, cases with mucosa of varying stiffness were simulated. Overall transport characteristics were examined, and both pressure and geometry were analyzed. Results show that a compliant mucosa helped accommodate the incoming bolus and lubricate the moving bolus. Bolus transport was marginally achieved without mucosa or with mucosa replaced by muscle. A stiff mucosa greatly impaired bolus transport due to the lowered esophageal distensibility and increased luminal pressure. We conclude that mucosa is essential for normal esophageal transport function. Mechanically stiffened mucosa reduces the distensibility of the esophagus by obstructing luminal opening and bolus transport. Mucosal stiffening may be relevant in diseases characterized by reduced esophageal distensibility, elevated intrabolus pressure, and/or hypertensive muscle contraction such as eosinophilic esophagitis and jackhammer esophagus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aceves SS, Ackerman SJ (2009) Relationships between eosinophilic inflammation, tissue remodeling, and fibrosis in eosinophilic esophagitis. Immunol Allergy Clin N Am 29(1):197–211

    Article  Google Scholar 

  • Brasseur JG, Nicosia MA, Pal A, Miller LS (2007) Function of longitudinal versus circular muscle fibers in esophageal peristalsis, deduced with mathematical modeling. World J Gastroenterol 13(9):1335–1346

    Article  Google Scholar 

  • Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, Cook IJ, Lang IM (1990) Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol Gastrointest Liver Physiol 258(5 Pt 1):G675–G681

    Google Scholar 

  • Ghosh SK, Kahrilas PJ, Zaki T, Pandolfino JE, Joehl RJ, Brasseur JG (2005) The mechanical basis of impaired esophageal emptying postfundoplication. Am J Physiol Gastrointest Liver Physiol 289(1):G21–G35

    Article  Google Scholar 

  • Gilbert RJ, Gaige TA, Wang R, Benner T, Dai G, Glickman JN, Wedeen VJ (2008) Resolving the three-dimensional myoarchitecture of bovine esophageal wall with diffusion spectrum imaging and tractography. Cell Tissue Res 332(3):461–468

    Article  Google Scholar 

  • Gregersen H, Kassab GS, Fung YC (2000) The zero-stress state of the gastrointestinal tract: biomechanical and functional implications. Dig Dis Sci 45(12):2271–2281

    Article  Google Scholar 

  • Griffith BE, Hornung RD, McQueen DM, Peskin CS (2007) An adaptive, formally second order accurate version of the immersed boundary method. J Comput Phys 223(1):10–49

    Article  MathSciNet  MATH  Google Scholar 

  • Jung HY, Puckett JL, Bhalla V, Rojas M, Bhargava V, Liu JM, Mittal RK (2004) Discoordination between circular and longitudinal muscle contractions in patients with high amplitude esophageal contractions. Gastroenterology 126(4):A637–A637

    Google Scholar 

  • Kou W, Bhalla APS, Griffith BE, Pandolfino JE, Kahrilas PJ, Patankar NA (2015a) A fully resolved active musculo-mechanical model for esophageal transport. J Comput Phys 298:446–465

    Article  MathSciNet  MATH  Google Scholar 

  • Kou W, Pandolfino JE, Kahrilas PJ, Patankar NA (2015b) Simulation studies of circular muscle contraction, longitudinal muscle shortening, and their coordination in esophageal transport. Am J Physiol Gastrointest Liver Physiol 309(4):G238–G247

    Article  Google Scholar 

  • Kwiatek MA, Pandolfino JE, Hirano I, Kahrilas PJ (2010) Esophagogastric junction distensibility assessed with an endoscopic functional luminal imaging probe (endoflip). Gastrointest Endosc 72(2):272–278

    Article  Google Scholar 

  • Kwiatek MA, Hirano I, Kahrilas PJ, Rothe J, Luger D, Pandolfino JE (2011) Mechanical properties of the esophagus in eosinophilic esophagitis. Gastroenterology 140(1):82–90

    Article  Google Scholar 

  • Li B, Cao YP, Feng XQ (2011a) Growth and surface folding of esophageal mucosa: a biomechanical model. J Biomech 44(1):182–188

    Article  Google Scholar 

  • Li B, Cao YP, Feng XQ, Gao H (2011b) Surface wrinkling of mucosa induced by volumetric growth: theory, simulation and experiment. J Mech Phys Solids 59(4):758–774

    Article  MathSciNet  Google Scholar 

  • Lin Z, Yim B, Gawron A, Imam H, Kahrilas PJ, Pandolfino JE (2014) The four phases of esophageal bolus transit defined by high-resolution impedance manometry and fluoroscopy. Am J Physiol Gastrointest Liver Physiol 307(4):G437–G444

    Article  Google Scholar 

  • Meyer GW, Austin RM, Brady RCE, Castell DO (1986) Muscle anatomy of the human esophagus. J Clin Gastroenterol 8(2):131–134

    Article  Google Scholar 

  • Mittal RK, Padda B, Bhalla V, Bhargava V, Liu JM (2006) Synchrony between circular and longitudinal muscle contractions during peristalsis in normal subjects. Am J Physiol Gastrointest Liver Physiol 290(3):G431–G438

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nicodeme F, Hirano I, Chen J, Robinson K, Lin Z, Xiao Y, Gonsalves N, Kwasny MJ, Kahrilas PJ, Pandolfino JE (2013) Esophageal distensibility as a measure of disease severity in patients with eosinophilic esophagitis. Clin Gastroenterol Hepatol 11(9):1101–1107

    Article  Google Scholar 

  • Nicosia MA, Brasseur JG (2002) A mathematical model for estimating muscle tension in vivo during esophageal bolus transport. J Theor Biol 219(2):235–255

    Article  MathSciNet  Google Scholar 

  • Nicosia MA, Brasseur JG, Liu JB, Miller LS (2001) Local longitudinal muscle shortening of the human esophagus from high-frequency ultrasonography. Am J Physiol Gastrointest Liver Physiol 281(4):G1022–G1033

    Google Scholar 

  • Orlando RC (2006) Esophageal mucosal defense mechanisms. GI Motility online

  • Pandolfino JE, Shi G, Curry J, Joehl RJ, Brasseur JG, Kahrilas PJ (2002) Esophagogastric junction distensibility: a factor contributing to sphincter incompetence. Am J Physiol Gastrointest Liver Physiol 282(6):G1052–G1058

    Article  Google Scholar 

  • Pandolfino JE, de Ruigh A, Nicodéme F, Xiao Y, Boris L, Kahrilas PJ (2013) Distensibility of the esophagogastric junction assessed with the functional lumen imaging probe (flip) in achalasia patients. Neurogastroenterol Motil 25(6):496

    Article  Google Scholar 

  • Peskin CS (1972) Flow patterns around heart valves: a numerical method. J Computat Phys 10(2):252–271

    Article  MathSciNet  MATH  Google Scholar 

  • Peskin CS (1977) Numerical analysis of blood flow in the heart. J Comput Phys 25(3):220–252

    Article  MathSciNet  MATH  Google Scholar 

  • Peskin CS (2002) The immersed boundary method. Acta Numer 11:479–517

    Article  MathSciNet  MATH  Google Scholar 

  • Pouderoux P, Lin S, Kahrilas PJ (1997) Timing, propagation, coordination, and effect of esophageal shortening during peristalsis. Gastroenterology 112(4):1147–1154

    Article  Google Scholar 

  • Puckett JL, Bhalla V, Liu J, Kassab G, Mittal RK (2005) Oesophageal wall stress and muscle hypertrophy in high amplitude oesophageal contractions. Neurogastroenterol Motil 17(6):791–799

    Article  Google Scholar 

  • Sarosiek J, McCallum RW (2000) Mechanisms of oesophageal mucosal defence. Best Pract Res Clin Gastroenterol 14(5):701–717

    Article  Google Scholar 

  • Stavropoulou EA, Dafalias YF, Sokolis DP (2009) Biomechanical and histological characteristics of passive esophagus: experimental investigation and comparative constitutive modeling. J Biomech 42(16):2654–2663

    Article  Google Scholar 

  • Yang W, Fung TC, Chian KS, Chong CK (2006a) 3D mechanical properties of the layered esophagus: experiment and constitutive model. J Biomech Eng 128(6):899–908

    Article  Google Scholar 

  • Yang W, Fung TC, Chian KS, Chong CK (2006b) 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

    Article  Google Scholar 

  • Yang W, Fung TC, Chian KS, Chong CK (2007) Instability of the two-layered thick-walled esophageal model under the external pressure and circular outer boundary condition. J Biomech 40(3):481–490

    Article  Google Scholar 

  • Zhao J, Jorgensen CS, Liao D, Gregersen H (2007) Dimensions and circumferential stress-strain relation in the porcine esophagus in vitro determined by combined impedance planimetry and high-frequency ultrasound. Dig Dis Sci 52(5):1338–1344

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Public Health Service Grants DK056033 (to P.J.K) and DK079902 (to J.E.P.).

Author information

Authors and Affiliations

  1. Theoretical and Applied Mechanics, Northwestern University, 2145 Sheridan Road, Evanston, IL, 60208, USA

    Wenjun Kou

  2. Department of Medicine, Feinberg School of Medicine, Northwestern University, 676 North Saint Clair Street, 14th Floor, Chicago, IL, 60611, USA

    John E. Pandolfino & Peter J. Kahrilas

  3. Department of Mechanical Engineering, Northwestern University, 2145 Sheridan Road, Evanston, IL, 60208, USA

    Neelesh A. Patankar

Authors
  1. Wenjun Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John E. Pandolfino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter J. Kahrilas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Neelesh A. Patankar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neelesh A. Patankar.

Ethics declarations

Conflicts of interest

John E. Pandolfino discloses consulting and educational association with Given Imaging and Sandhill Scientific. Wenjun Kou, Peter J. Kahrilas and Neelesh A. Patankar declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kou, W., Pandolfino, J.E., Kahrilas, P.J. et al. Simulation studies of the role of esophageal mucosa in bolus transport. Biomech Model Mechanobiol 16, 1001–1009 (2017). https://doi.org/10.1007/s10237-016-0867-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-016-0867-1

Keywords

Search

Navigation