The precision of macroscale mechanical measurements is limited by the inherent structural heterogeneity of human stratum corneum

Abstract

Biological tissues are structurally heterogenous mosaics at cellular and sub-cellular length scales. Some tissues, like the outermost layer of human skin, or stratum corneum (SC), also exhibit a rich topography of microchannels at larger mesoscopic length scales. Although this is well understood, modern studies continue to characterize the mechanical properties of biological tissues, including the SC, using macroscale techniques that assume these materials are homogenous in structure, thickness, and composition. Macroscale failure testing of SC is commonly associated with large sample to sample variability. We anticipate that microscale heterogeneities play an important role in defining the global mechanical response of the tissue. To evaluate the validity of the prevailing paradigm that macroscopic testing techniques can provide meaningful information about failure in soft heterogenous tissues, the macroscale work of fracture in isolated human SC samples is measured using conventional macroscale testing techniques and compared with the energy cost of creating new crack interfaces at the microscale, measured using a modified traction force microscopy technique. Results show that measured micro- and macroscale energy costs per unit crack path length are highly consistent. However, crack propagation is found to be guided by microscale topographical features in the tissue. This correlation reveals that macroscale mechanical sample to sample variability is caused by notable differences in crack propagation pathways. Statement of significanceAlthough designed to test homogeneous materials, macroscopic uniaxial tensometry is currently the gold standard for measuring the mechanical properties of biological tissues. All tissues, including human stratum corneum are structurally heterogeneous at the microscale and mechanical measurements are commonly highly variable, even for specimens from the same source. This study explores the fundamental causes of this disparity and evaluates the prevailing paradigm that macroscopic testing techniques can provide meaningful information about failure in soft heterogeneous tissues. Results conclude that the cause of large variability in mechanical work of fracture is due to inherent structural heterogeneities governing crack propagation pathways and altering the total crack length. Structural heterogeneities in tissue therefore limits the precision of macroscale biomechanical testing.