Active and passive material response of urinary bladder smooth muscle tissue in uniaxial and biaxial tensile testing

Abstract

The urinary bladder is a hollow organ that undergoes significant deformation as it receives, stores, and releases urine. To understand the organ mechanics, it is necessary to obtain information about the material properties of the tissues involved. In displacement-controlled tensile tests, tissue samples are mounted on a device that applies stretches to the tissue in one or more directions, resulting in a specific stress response. For this study, we performed uniaxial and biaxial stretch experiments on tissue samples (n = 36) from the body region of the porcine urinary bladder. We analyzed the stress-relaxation, activation dynamics, and passive and active stretch-stress response. Main findings of our experiments are: (1) For uniaxial and biaxial stretching, the time constants for stress-relaxation depend on the stretch amplitude, (2) biaxially stretched samples experienced slower activation with ${\tau }_{act}$ increasing by +63% compared to uniaxial stretching, (3) biaxial tests are characterized by reduced optimum stretches ${\lambda }_{opt}$ by -18%, and (4) biaxial and uniaxial tests showed no significant difference in maximum active stresses ${\sigma }_{\mathrm{opt}}$. To interpret the results, we present a continuum mechanical model based on a viscoelastic, isotropic solid extended by a set of active muscle fibers. Model predictions show that results (3) and (4) can be explained by a uniform distribution of fiber orientations and a specific shape of the active fiber stress-stretch relationship. This study highlights how deformation modes during tensile testing affects smooth muscle mechanics, proving insights for interpreting experimental data and improving organ modeling.

Statement of Significance

In this study, we examined the mechanical properties of porcine bladder smooth muscle using uniaxial and equibiaxial tensile tests. To our knowledge, this is the first instance where the active stress-stretch relationships of smooth muscle tissue have been analysed under equibiaxial stretch. The data collected offer a detailed understanding of the connection between deformation and active stress production, surpassing the insights provided by existing uniaxial tests in the literature. These findings are crucial for comprehending the physiology of smooth muscle tissue and for developing constitutive muscle models that can make more accurate predictions about the functionality of hollow organs in both health and disease. Additionally, our findings on smooth muscle active stress could aid in the creation of biomaterials that interact with or even replace natural muscle.