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Collagen Fiber Orientation at the Tendon to Bone Insertion and Its

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Collagen Fiber Orientation at the Tendon to Bone Insertion and Its ARTICLE IN PRESS Journal of Biomechanics 39 (2006) 1842–1851 www.elsevier.com/locate/jbiomech www.JBiomech.com Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations Stavros Thomopoulosa,Ã, Juan P. Marqueza, Bradley Weinbergera, Victor Birmanb, Guy M. Genina aDepartment of Orthopaedic Surgery, Washington University, 1 Barnes-Jewish Hospital Plaza, Suite 11300, Campus Box 8233, St. Louis, MO 63110, USA bUniversity of Missouri—Rolla, Engineering Education Center, St. Louis, MO 63121, USA Accepted 20 May 2005 Abstract The tendon to bone insertion serves the mechanical role of transferring loads from a relatively compliant tendon to a relatively rigid bone. The details of the mechanism of load transfer are of great importance, since current surgical procedures for tendon reattachment have high failure rates. We hypothesized that the microscopic structure of the insertion is optimized to minimize stress concentrations associated with this load transfer. To explore this, collagen fiber orientation distributions were measured in the supraspinatus tendons of rats. The angular deviation of fibers was fairly uniform across the insertion, and the mean angles of the local distributions deviated mildly from the tendon axis. To explore how these observed property distributions could influence load transfer, these distributions were used to derive material properties for an idealized two-dimensional mechanical model of an insertion. Comparison between stress concentrations in this idealized model and those in three comparison models suggests that the microstructure serves to (1) simultaneously reduce stress concentrations and material mass, and (2) shield the insertion’s outward splay from the highest stresses. r 2005 Elsevier Ltd. All rights reserved. Keywords: Tendon; Insertion site; Stress concentration; Modeling; Collagen 1. Introduction over long area, e.g., the medial collateral ligament) (Benjamin et al., 2002). It is expected that stress concen- Tendon attaches to bone through a fibrocartilaginous trations would arise at the interface of these two transition zone (the ‘enthesis’ or ‘insertion site’) which materials. The enthesis is prone to injury, and generally functions to transfer load between two very different heals poorly (Fujioka et al., 1998; Leddy and Packer, materials (Benjamin et al., 2002; Woo et al., 1987). Using 1977; Rodeo et al., 1993; St. Pierre et al., 1995; the terminology of Benjamin et al., this load transfer can Thomopoulos et al., 2002, 2003a). Repair of the rotator occur through a fibrocartilaginous enthesis (typically cuff tendon to bone insertion, for example, is at high risk over a small area, e.g., the supraspinatus tendon of for early failure (Galatz et al., 2004; Harryman et al., the rotator cuff) or through a fibrous enthesis (typically 1991). The incidence of recurrence of injury after massive rotator cuff injury and repair has been reported to be as high as 94% (Galatz et al., 2004). Understanding the ÃCorresponding author. Tel.: +1 314 362 8650; fax: +1 314 362 0334. mechanical behavior of the normal tendon to bone E-mail address: [email protected] insertion will allow for the development of devices and (S. Thomopoulos). tissue engineering replacements to improve the repair. 0021-9290/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2005.05.021 ARTICLE IN PRESS S. Thomopoulos et al. / Journal of Biomechanics 39 (2006) 1842–1851 1843 The fibrocartilaginous tendon to bone insertion Committee regulations at Washington University site has classically been categorized into four zones School of Medicine. Sections were stained with 0.1% (Benjamin et al., 2002; Woo et al., 1987). It was Picrosirius Red solution, destained in 1% acetic acid, previously demonstrated that the structure, composition, counterstained with hematoxylin, and differentiated in and the mechanical properties of the normal insertion 1% HCl in 70% ethanol. Collagen fiber angle distribu- varies along these zones (Fukuta et al., 1998; Niyibizi et tions were measured at 5 locations along the length of al., 1996; Raspanti et al., 1996; Thomopoulos et al., the insertion, both in the fibrocartilage (FC) zone and in 2003b; Waggett et al., 1998). The first zone consists of the mineralized fibrocartilage zone (MC), at positions tendon proper, and is composed of well aligned type I on both sides of the tidemark (points A–E in Fig. 1), for collagen fibers with small amounts of the proteoglycan a total of 10 locations per specimen. Sampling positions decorin. The second zone consists of fibrocartilage and is were chosen at 5 equidistant points along the arc defined composed of types II and III collagen, with small by the supraspinatus tendon insertion tidemark. The amounts of types I, IX, and X collagen, and small endpoints (A and E in Fig. 1) were chosen based on the amounts of the proteoglycans aggrecan and decorin. The clearly evident edges of the tendon. When defining a third zone contains mineralized fibrocartilage and the sampling point in the mineralized vs. the un-mineralized predominant collagen is type II, with significant amounts portions of the insertion, 0.5 mm2 areas were sampled on of type X collagen as well as aggrecan. The border either side of the tidemark, ensuring that the area did between these two fibrocartilaginous regions is demar- not encroach over the tidemark line. A polarized light cated by a ‘‘tidemark’’, a basophilic line that represents method for quantitative collagen orientation analysis the calcification front. Finally, zone four consists of bone, was used to quantify collagen fiber orientation at each which is made up predominantly of type I collagen with a location (Dickey et al., 1998; Thomopoulos et al., high mineral content. It has been proposed that this 2003a, b; Whittaker and Canham, 1991). Tissue sections continuous change in tissue composition and structure is were documented and analyzed using a polarized light necessary to minimize stress concentrations and aid in the microscope (Olympus BX51P) and an Olympus DP70 efficient transfer of load between tendon and bone digital microscope camera (36 bit, color, 1360 Â 1040, 2/ (Benjamin et al., 1992, 2002; Matyas et al., 1995; 3 in CCD chip). The specimen was illuminated with light Thomopoulos et al., 2003b). However, the mechanism filtered through a crossed polarizer (east–west position) by which structure (i.e., collagen organization) and and analyzer (north–south position) (Bennett, 1964). variation in mechanical properties minimizes stress Images were captured at section orientations from 451 to concentrations has not been elucidated. 1351 in 51 increments (the long axis of the tendon was The objective of our study was to determine whether aligned with 901). A compensator (l/4 wave plate) was there is a microstructural basis for minimizing stress then engaged in a diagonal position (NW–SE) and concentrations at the tendon to bone insertion site. We additional images were recorded at section orientations hypothesized that collagen fiber organization at the from 451 to 1351 in 51 increments. Software designed insertion is optimized to minimize the stress concentra- with Matlab (The Mathworks, Natick, MA) was used to tions that would develop at the interface of the two determine the angle of extinction (y). The software’s materials (tendon and bone). graphical interface allows the user to interactively vary inputs such as the area of interest and the sampling frequency. An image of the tissue illuminated with 2. Methods linearly polarized light is displayed. A grid is overlaid on the image and defines the points of interest for analysis. 2.1. Experimental studies A plot of light intensity vs. section orientation for each point of interest is then created. y was determined by Supraspinatus tendon to bone insertions from 5 male, examining the plot of light intensity vs. section orienta- 5–6 months old, skeletally mature, Fisher 344 rats were tion and then locating the angle associated with the dissected free of surrounding tissues. Specimens were minimum light intensity. y was determined at each point fixed in 10% buffered formalin with the tendon oriented on the grid (note that each grid point consisted of a 3 Â 3 parallel to the humerus (i.e., equivalent to a shoulder pixel square). In order to determine whether the collagen position of approximately 901 abduction). Applying orientation was at y or y7901 (i.e., whether the slow tension to the tendon during fixation could affect axis of the collagen is aligned with the analyzer or the collagen fiber orientation. Since an appropriate in vivo polarizer), the color hue was examined at y7451 using tension is unknown, the tendons in our study were fixed images taken with the compensator in place. A under zero tension. Specimens were processed for histogram was generated to display the distribution of standard paraffin embedded histology and sectioned in collagen fiber orientations for all of the pixel bundles. the transverse plane (5 mm section thickness). All animal The angular deviation of the collagen orientations for all procedures were in compliance with the Animal Studies pixel bundles was then calculated (Karlon et al., 1999). ARTICLE IN PRESS 1844 S. Thomopoulos et al. / Journal of Biomechanics 39 (2006) 1842–1851 Fig. 1. (a) Collagen orientations were measured at 5 locations (A–E) on both sides of the tidemark (MC, FC). (b) A representative image of the insertion site under brightfield microscopy (Picrosirius Red stain, 10 Â objective).
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