Morpho-elasticity of intestinal villi

Balbi, Valentina; Ciarletta, Pasquale

doi:10.1098/rsif.2013.0109

Cited by 52 publications

(41 citation statements)

References 25 publications

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“…The fluid mechanics of the lung have been extensively studied using both idealized and patient-specific models [32,59]. However, existing solid mechanics studies which focus on three-dimensional biological geometries are few [54,63], mainly analytical [7,17], fail to predict emerging surface morphologies beyond the onset of folding [60,73], and typically neglect the characteristic branching of the lung [8, 27, 38]. Here we address these limitations by extending airway remodeling mechanics to realistic patient-specific airway branch models created from magnetic resonance images.…”

Section: Introductionmentioning

confidence: 99%

Patient-Specific Airway Wall Remodeling in Chronic Lung Disease

2015

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Chronic lung disease affects more than a quarter of the adult population; yet, the mechanics of the airways are poorly understood. The pathophysiology of chronic lung disease is commonly characterized by mucosal growth and smooth muscle contraction of the airways, which initiate an inward folding of the mucosal layer and progressive airflow obstruction. Since the degree of obstruction is closely correlated with the number of folds, mucosal folding has been extensively studied in idealized circular cross sections. However, airflow obstruction has never been studied in real airway geometries; the behavior of imperfect, non-cylindrical, continuously branching airways remains unknown. Here we model the effects of chronic lung disease using the nonlinear field theories of mechanics supplemented by the theory of finite growth. We perform finite element analysis of patient-specific Y-branch segments created from magnetic resonance images. We demonstrate that the mucosal folding pattern is insensitive to the specific airway geometry, but that it critically depends on the mucosal and submucosal stiffness, thickness, and loading mechanism. Our results suggests that patient-specific airway models with inherent geometric imperfections are more sensitive to obstruction than idealized circular models. Our models help to explain the pathophysiology of airway obstruction in chronic lung disease and hold promise to improve the diagnostics and treatment of asthma, bronchitis, chronic obstructive pulmonary disease, and respiratory failure.

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Section: Introductionmentioning

confidence: 99%

Patient-Specific Airway Wall Remodeling in Chronic Lung Disease

2015

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“…Increased thickness of the mucosa, submucosa, and stiffness ratios provoke increased wavelengths and fewer folds. Rigorous relationships between these ratios and the number of folds have been established for circular, elliptical, and rectangular geometries [6, 17, 22] and even for irregular patient-specific geometries [23]. …”

Section: Motivationmentioning

confidence: 99%

Elastosis during airway wall remodeling explains multiple co-existing instability patterns

Eskandari

Javili

Kuhl

2016

Journal of Theoretical Biology

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Living structures can undergo morphological changes in response to growth and alterations in microstructural properties in response to remodeling. From a biological perspective, airway wall inflammation and airway elastosis are classical hallmarks of growth and remodeling during chronic lung disease. From a mechanical point of view, growth and remodeling trigger mechanical instabilities that result in inward folding and airway obstruction. While previous analytical and computational studies have focused on identifying the critical parameters at the onset of folding, few have considered the post-buckling behavior. All prior studies assume constant microstructural properties during the folding process; yet, clinical studies now reveal progressive airway elastosis, the degeneration of elastic fibers associated with a gradual stiffening of the inner layer. Here, we explore the influence of temporally evolving material properties on the post-bifurcation behavior of the airway wall. We show that a growing and stiffening inner layer triggers an additional subsequent bifurcation after the first instability occurs. Evolving material stiffnesses provoke failure modes with multiple co-existing wavelengths, associated with the superposition of larger folds evolving on top of the initial smaller folds. This phenomenon is exclusive to material stiffening and conceptually different from the phenomenon of period doubling observed in constant-stiffness growth. Our study suggests that the clinically observed multiple wavelengths in diseased airways are a result of gradual airway wall stiffening. While our evolving material properties are inspired by the clinical phenomenon of airway elastosis, the underlying concept is broadly applicable to other types of remodeling including aneurysm formation or brain folding.

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“…A great attention has been also payed to model the emergence of a more complex network of mucosal patterns, later developing villi and crypts in many vertebrates. Balbi and Ciarletta performed a linear stability analysis on growing one-layered thick-walled cylinders, showing that the initial geometry of the tissue can select a one-dimensional or bi-dimensional instability pattern, according to different villi formation mechanisms observed in several vertebrate species [15]. Accounting for a differential growth between epithelium and mesenchyme, Ben Amar and Jia proposed a weakly nonlinear stability analysis for studying the emergence of the zigzag pattern, which typically develops in the chick embryo as a precursor of villi formation [16].…”

Section: Introductionmentioning

confidence: 99%

Morphoelastic control of gastro-intestinal organogenesis: Theoretical predictions and numerical insights

Balbi

Kuhl

Ciarletta

2015

Journal of the Mechanics and Physics of Solids

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Cite this article as: V. Balbi, E. Kuhl and P. Ciarletta, Morphoelastic control of gastro-intestinal organogenesis: Theoretical predictions and numerical insights, AbstractWith nine meters in length, the gastrointestinal tract is not only our longest, but also our structurally most diverse organ. During embryonic development, it evolves as a bilayered tube with an inner endodermal lining and an outer mesodermal layer. Its inner surface displays a wide variety of morphological patterns, which are closely correlated to digestive function. However, the evolution of these intestinal patterns remains poorly understood. Here we show that geometric and mechanical factors can explain intestinal pattern formation. Using the nonlinear field theories of mechanics, we model surface morphogenesis as the instability problem of constrained differential growth. To allow for internal and external expansion, we model the gastrointestinal tract with homogeneous Neumann boundary conditions. To establish estimates for the folding pattern at the onset of folding, we perform a linear stability analysis supplemented by the perturbation theory. To predict pattern evolution in the post-buckling regime, we perform a series of nonlinear finite element simulations. Our model explains why longitudinal folds emerge in the esophagus with a thick and stiff outer layer, whereas circumferential folds emerge in the jejunum with a thinner and softer outer layer. In intermediate regions like the feline esophagus, longitudinal and circumferential folds emerge simultaneously. Our model could serve as a valuable tool to explain and predict alterations in esophageal morphology as a result of developmental disorders or certain digestive pathologies including food allergies.

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Morpho-elasticity of intestinal villi

Cited by 52 publications

References 25 publications

Patient-Specific Airway Wall Remodeling in Chronic Lung Disease

Patient-Specific Airway Wall Remodeling in Chronic Lung Disease

Elastosis during airway wall remodeling explains multiple co-existing instability patterns

Morphoelastic control of gastro-intestinal organogenesis: Theoretical predictions and numerical insights

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