Increase of stiffness in plantar fat tissue in diabetic patients

Abstract

Plantar soft tissue stiffening in diabetes leads to a risk of developing ulcers. There are relatively few studies providing methods for quantifying the mechanical properties of skin and fat in the plantar tissue of diabetic patients. Previous studies used linear or non-linear single layer deformable models or linear multi-layer models. This study aimed to investigate the mechanical properties of plantar soft tissue using multi-layer, non-linear models to estimate more accurate mechanical properties in the plantar tissues of diabetic patients. Ten healthy young (HY) subjects, ten healthy old (HO) subjects, and ten old diabetic patients (DB) volunteered for the study. Indentation tests were performed at two sites in the heel. The subjects underwent computed tomography (CT) to measure the respective thicknesses of the skin and fat at the indentation sites. Subject-specific finite element models were created to estimate the parameters of the first-order Ogden forms of the skin and fat. The initial shear modulus for the fat layer ${\mu }_F$ in DB, HO, and HY were 4.68 MPa (±0.87), 2.71 MPa (±1.25), and 2.27 MPa (±0.87), respectively. The initial shear modulus for the skin layer (${\mu }_S$) in DB, HO, and HY were 5.86 MPa (±2.51), 7.05 MPa (±1.94), and 14.58 MPa (±1.98), respectively. The DB had stiffer fat tissue than the normal subjects in the same age group but had the same soft skin. These aspects can cause different mechanical stress conditions in a diabetic foot than in a normal foot under the same mechanical loading, making the diabetic foot vulnerable to the initiation of mechanical breakdowns such as ulcers.

Introduction

The ulceration of plantar soft tissue is frequently observed in diabetic patients. It can be caused by damaged motor neurons of the foot musculature and/or blood flow reduction (Aumiller and Dollahite, 2015, Boulton et al., 2004). Abnormal plantar foot pressure worsens mechanical stress conditions, initiating and progressing physical damages in the tissue (Boulton et al., 1983, Veves et al., 1992). The mechanical properties of plantar tissues consisting of skin and fat layers can be affected by an increased collagen fibril density with tissue glycation (Teoh and Lee, 2014), which can change the mechanical stress conditions, making the plantar tissue susceptible to ulceration in conjunction with other physiological changes (Hsu et al., 2009, Sun et al., 2011).

The mechanical properties of plantar tissue can be a precursor to foot ulceration, and a biomarker for quantifying a diabetic foot condition. Stiffness in plantar soft tissue has been used to detect the probability of foot ulceration owing to the complications of the diabetic foot (Erdemir et al., 2006, Hsu et al., 2009, Sun et al., 2011, Zheng and Mak, 1996). A linear-elastic model has frequently been used to simplify the stress-strain relationship, or the stiffness of soft tissues (Klaesner et al., 2001, Zheng et al., 2000). However, biological soft tissue behaves like a hyper-elastic material, with a non-linear stress-strain relationship under large deformation conditions (Erdemir et al., 2006, Meunier et al., 2008).

Many previous studies consider the plantar soft tissue as a single layer of uniform material (Erdemir et al., 2006, Xiong et al., 2010, Zheng and Mak, 1996). However, plantar tissue is not homogeneous tissue, but includes multiple layers of skin, fat, and muscle. Each layer of plantar tissue has different constituents and different mechanical properties (Miller-Young et al., 2002). Therefore, the mechanical properties of plantar soft tissue should be investigated separately for multiple layers (Hsu et al., 2007).

A skin surface indentation test is a non-invasive in-vivo method for estimating the mechanical properties of soft tissues (Delalleau et al., 2006). Previously, indentation tests of plantar soft tissue and a single layer linear-elastic model have indicated that diabetic patients have stiffer plantar tissue than normal subjects (Sun et al., 2011, Teoh and Lee, 2014, Zheng et al., 2000). In contrast, when the plantar tissue has been considered in a single layer hyper-elastic model, the stiffness of the plantar tissue was not significantly different between diabetic patients and normal subjects (Erdemir et al., 2006). Hsu et al. (2009) proposed a multi-layer plantar tissue model with microchamber (skin) and macrochamber (fat) layers. A linear-elastic model was used for both layers to investigate the mechanical properties of diabetic patients and healthy subjects (Hsu et al., 2009). They reported that the stiffness of the macrochamber layer was higher in the diabetic group as compared to the healthy group. However, their linear-elastic model, which calculated the stress-strain using a constant cross-section, could not represent the true stress-strain behavior (Delalleau et al., 2006). As the cross-section of a hyper-elastic material changes with deformation, a non-linear model that reflects instantaneous cross-sections should be used.

The objectives of this study were (1) to develop a method to estimate the mechanical properties of a double multi-layer, hyper-elastic model for plantar heel soft tissue, from multiple skin surface indentation tests; and (2) to compare the mechanical properties and the stress-strain behaviors of the plantar heel soft tissues between diabetic patients, normal young subjects, and normal old subjects.