The shear mechanical properties of diabetic and non-diabetic plantar soft tissue
Introduction
The risk of plantar ulceration, and subsequent amputation, is disproportionately increased in the diabetic population (CDCP, 2011). Improving ulcer prevention measures requires a better understanding of any underlying detrimental plantar soft tissue changes induced by this disease. Specifically, knowledge of mechanical property alterations under relevant plantar loading, i.e., compression and shear, is needed. Our group and several others have examined diabetes-induced changes in the compressive elastic (Pai and Ledoux, 2010; Cheung et al., 2006, Gefen et al., 2001, Hsu et al., 2009, Hsu et al., 2007, Hsu et al., 2002, Hsu et al., 2000, Klaesner et al., 2002, Piaggesi et al., 1999) and viscoelastic (Pai and Ledoux, 2011) parameters of the plantar soft tissue. However, little is known about alterations in the plantar soft tissue shear properties despite the fact that shear loading beneath the foot is estimated to be between one half and one seventh of the vertical peak loads depending on plantar location (Hosein and Lord, 2000, Yavuz et al., 2008). A recent study (Yavuz et al., 2008) indicates increased shear loading with diabetes, thereby further motivating the need to study shear properties. Additionally, increased shear stresses at certain plantar locations or regions may play a role in ulceration (Yavuz et al., 2007a, Yavuz et al., 2007b, Zou et al., 2007).
Beyond shear stress, little is known about the plantar soft tissue shear properties. One group measured the in vivo shear modulus of the subcalcaneal soft tissue using MR elastography imaging and found that the shear modulus increased from 8 kPa to 12 kPa with increasing pressure (Weaver et al., 2005). These results provide a first approximation of the shear properties of plantar tissue but examined one plantar location, used small shear deformations (20 μm), and did not study the effect of diabetes.
A common approach to induce a state of shear in many soft tissues is through torsion tests of cylindrical samples using standard rheology equipment (Bilston et al., 1997, Holt et al., 2008, Iatridis et al., 1999, Iatridis et al., 1997, Liu and Bilston, 2002, Shuck and Advani, 1972). Staying within the linear elastic range allows for computation of the complex modulus. However, this approach is limited for large strains that are not within the linear elastic region, such as those observed in the plantar soft tissue. Another common shear testing approach is the simple shear method whereby the tissue being sheared is sandwiched between two parallel plates before applying a lateral or shear displacement (Arbogast and Margulies, 1998, Carew et al., 1999, Chan and Rodriguez, 2008, Darvish and Crandall, 2001, Hayes and Bodine, 1978, Prange and Margulies, 2002, Tanaka et al., 2008). Although sometimes used for small strain experiments, this method is also able to conduct large strain studies that better represent the in vivo plantar soft tissue shear strains.
While previous estimates for plantar shear loads (Yavuz et al., 2007a, Yavuz et al., 2007a, Yavuz et al., 2008) could be used to apply biomechanically realistic deformations during in vitro mechanical tests using the simple shear method, it remains unclear whether any adjustment to account for isolating the plantar soft tissue would be needed. Further, it is unclear what shear strains would correspond to these shear loads. We recently measured the in vivo plantar soft tissue shear strains using fluoroscope imaging in one healthy subject (Pai, 2011) these strains would be ideal for applying realistic deformations.
Thus, the purpose of this study is to examine the elastic and viscoelastic shear behavior of both diabetic and non-diabetic plantar tissue at relevant locations beneath the foot using biomechanically realistic testing methods with previously obtained shear strains as input. Characterizing these shear properties is essential to fully understanding the role, if any, that shear property changes play with ulcer formation in diabetic patients.
Section snippets
Experimental protocol
Plantar tissue specimens (n=54) at six plantar locations (Fig. 1, hallux, first, third, and fifth metatarsal heads, lateral midfoot, and calcaneus) from four fresh frozen cadaveric older diabetic feet (20.3±8.1 years post-diagnosis) and five non-diabetic older feet (Table 1) were used in this study. These specimens were previously dissected and tested in compression (Pai and Ledoux, 2010, Pai and Ledoux, 2011) after which they had been wrapped in saline soaked paper towels, placed in a plastic
Results
No differences were found between specimen parameters by disease status (Table 2). Examination of the shear stress–strain response for specimens from all locations in a sample non-diabetic foot showed a nonlinear S-shaped curve for both the 50% and 85% shear strain data (Fig. 3). Comparison of curves in one specimen at both strain levels indicated a longer toe region with reduced stress for the same strains in the second test group at 85% strain, indicating stress softening effects, yet higher
Discussion
Characterizing the plantar soft tissue shear properties is essential to fully understanding the role that diabetes plays in ulcer formation in diabetic patients at-risk for ulceration. This study examines the elastic and viscoelastic shear behavior of both diabetic and non-diabetic plantar tissue at relevant locations beneath the foot by applying previously obtained in vivo shear strains in simple shear.
Several differences were found between diabetic and non-diabetic shear elastic and
Conflict of Interest Statement
The authors have no conflicts to report.
Acknowledgments
This study was supported by the National Institutes of Health grant 1R01 DK75633-03 and the Department of Veterans Affairs, RR&D Service grant A4843C. The authors would also like to thank Jane Shofer for the statistical analysis, Michael Fassbind for equipment design, and Paul Vawter for assisting with data analysis.
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