Matrix mechanical properties of transversalis fascia in inguinal herniation as a model for tissue expansion

Abstract

Inguinal herniation represents a common condition requiring surgical intervention. Despite being regarded as a connective tissue disorder of uncertain cause, research has focused predominantly on biochemical changes in the key tissue layer, the transversalis fascia (TF) with little direct analysis of functional tissue mechanics. Connective tissue tensile properties are dominated by collagen fibril density and architecture. This study has correlated mechanical properties of herniated TF (HTF) and non-herniated TF (NHTF) with fibrillar properties at the ultrastructural level by quasi-static tensile mechanical analysis and image analysis of collagen electron micrographs. No significant difference was found between any of the key mechanical properties (break stress, strain or modulus) for HTF and NHTF. In addition, no significant differences were found in average collagen fibril diameter, density or fibre bundle spacing. However, both groups displayed anisotropy with greater break stress (p=0.001) on average in the transverse anatomical plane compared to the longitudinal plane in a mean ratio of 2:1 (anisotropy ratio), though there was no evidence of a difference in this ratio for HTF and NHTF for both break stress and modulus. It was noted that this anisotropy ratio corresponds closely with the expected force distribution on a model cylindrical structure loaded axially. The absence of other functional differences does not support the idea of a failing (injured) tissue but is consistent with it being a tissue undergoing chronic growth/expansion under multi-vectored mechanical loading. These findings provide new clues to collagen tissue herniation for mathematical modelling and model tissue engineering.

Introduction

Herniation represents the abnormal protrusion or extension of one tissue into another or into an adjacent space. It is a dynamic process where the failure of tissue function produces altered local anatomy. Abdominal hernias, of which inguinal hernias are the most common type, account for approximately 1,00,000 operations per year in the UK. The transversalis fascia (TF) (a thin collagen sheet on the internal surface of the abdominal muscle wall) has long been the focus of inguinal hernia pathophysiology. In 1804, Cooper described the anatomy of the TF and postulated that the TF is the layer that presents the main barrier to herniation (reviewed by Rutkow, 1997).

The longstanding belief that increased intra-abdominal pressure (straining from coughing, lifting heavy weight, etc.) is the primary stimulus for hernia formation has been questioned by a variety of authors like Pans et al. (1997); Read (1998); Jansen et al. (2004) and Bendavid (2004) who have proposed that the hernia is a form of a connective tissue disorder. This has led to a range of TF studies implicating changes in collagen types, cell responses, gene expression and protease pathway activation (Abci et al., 2005; Rodrigues et al., 1990, Rodrigues et al., 2002; Bellon et al., 2001, Bellon et al., 1997; Nikolov and Beltschev, 1990). Fibrillar collagen is central to the extracellular matrix tensile properties including break strength, and it is clear that collagen function is a key for understanding any changes in TF mechano-biology. Of the different collagen types, Type I is predominantly found in mature load-bearing tissues including the TF (Klinge et al., 1999). Changes in the ratio of Type I and III collagen (common in embryonic, micro repair and vascular tissues) have been implicated in hernia tissues (Friedman et al., 1993), though it is unclear if this predisposes to altered TF function or is simply a consequence of micro repair (localized repair around microscopic tears). Friedman et al. have postulated that altered collagen fibril assembly due to increasing Type III content could eventually lead to the development of inguinal hernias. This reflects one of the basic tenets that the primary functional defect in hernia is reduced TF collagen mechanical strength and this predisposes the tissue to failure under load. This idea is apparently flawed if it is accepted that the process of TF herniation actually represents a natural model of tissue expansion rather than failure under tensile load. The mechanism by which the cells of a formerly stable, load-bearing collagen matrix come to ‘grow’ or extend that matrix in response to mechanical loading is of wide interest, especially in the fields of connective pathology and engineering.

There has been a recent focus on biochemical aspects of TF collagen and protease composition but despite its clear mechanical role there have been a few studies of its material properties to correlate with its actual function. Pans et al. (1997) measured the mechanical properties of two fasciae in combination—the rectus abdominus aponeurosis (flat tendon sheet which anchors the rectus abdominus muscle to the pelvis) together with the TF. However no measurements were made on TF in isolation. They concluded that there is no significant difference between the mechanical properties of control and hernia patients, though it seems likely that the stronger material properties of the aponeurosis would dominate such a composite.

The aim of this study was to determine whether any differences existed in mechanical properties and ultra-structure of normal and hernia TF. The core objective was to identify whether the gross TF deformation that occurs during herniation together with the associated matrix remodeling, alters the functional (mechanical) properties as might be expected based on other systems.