Elsevier

Journal of Biomechanics

Volume 43, Issue 16, 1 December 2010, Pages 3177-3182
Journal of Biomechanics

The biomechanical effects of limb lengthening and botulinum toxin type A on rabbit tendon

https://doi.org/10.1016/j.jbiomech.2010.07.032Get rights and content

Abstract

Numerous studies have examined the effects of distraction osteogenesis (DO) on bone, but relatively fewer have explored muscle adaptation, and even less have addressed the concomitant alterations that occur in the tendon. The purpose herein was to characterize the biomechanical properties of normal and elongated rabbit (N=20) tendons with and without prophylactic botulinum toxin type A (BTX-A) treatment. Elastic and viscoelastic properties of Achilles and Tibialis anterior (TA) tendons were evaluated through pull to failure and stress relaxation tests.

All TA tendons displayed nonlinear viscoelastic responses that were strain dependent. A power law formulation was used to model tendon viscoelastic responses and tendon elastic responses were fit with a microstructural model. Distraction-elongated tendons displayed increases in compliance and stress relaxation rates over undistracted tendons; BTX-A administration offset this result. The elastic moduli of distraction-lengthened TA tendons were diminished (p=0.010) when distraction was combined with gastrocnemius (GA) BTX-A administration, elastic moduli were further decreased (p=0.004) and distraction following TA BTX-A administration resulted in TA tendons with moduli not different from contralateral control (p>0.05). Compared to contralateral control, distraction and GA BTX-A administration displayed shortened toe regions, (p=0.031 and 0.038, respectively), while tendons receiving BTX-A in the TA had no differences in the toe region (p>0.05). Ultimate tensile stress was unaltered by DO, but stress at the transition from the toe to the linear region of the stress–stretch curve was diminished in all distraction-elongated TA tendons (p<0.05). The data suggest that prophylactic BTX-A treatment to the TA protects some tendon biomechanical properties.

Introduction

Corrective limb lengthening is frequently utilized in treating limb length inequalities, angulation deformities, non-unions, complex fractures, deficiencies after tumor resection, and in more recent years, persons of short stature (Williams et al., 1999, Nogueira et al., 2003, Segev and Hayek, 2003). The adaptation of bone during distraction osteogenesis (DO) is reliable and predictable; however, there are universal reports of soft tissue complications that are long term and often even permanent (Fink et al., 2001, Makarov et al., 2001, Williams et al., 2001, De Deyne et al., 2002, Yamazaki et al., 2003). Multiple studies have established that the surrounding muscle often becomes stiffer as a result of limb lengthening procedures (Simpson et al., 1995, Lindsey et al., 2002, Olabisi et al., 2007). In an attempt to overcome the more debilitating complications of DO such as muscle-tendon stiffness and loss in range of motion, physicians have utilized botulinum toxin type A (BTX-A) (Finley and Platt, 2009) Although basic science research has demonstrated that the histomorphological and elastic properties of tendons are altered by distraction (Fink et al., 1999a, Fink et al., 1999b, Szoke et al., 2005), the literature is lacking a complete description of the viscoelastic responses of these tendons. In particular, the effect of prophylactic BTX-A treatment during DO on the elastic and viscoelastic properties of tendons has not yet been described.

The purpose of this study therefore was to determine whether BTX-A can attenuate the biomechanical alterations that occur in elongated tendons undergoing DO. Following DO (Olabisi et al., 2007), stress–stretch, pull to failure and stress relaxation behavior were examined in rabbit TA and Achilles tendons in an effort to characterize the elastic and viscoelastic response of these tendons to BTX-A. The nonlinear stress–stretch behavior accounts for tendon compliance at low loads and stiffening at higher loads, which serve to guide joint motion, providing free joint excursion for physiologic motions but preventing excessive motion or displacement (Woo and Tkach, 1990). Accordingly, a more complete characterization of the low load behavior of tendons undergoing DO and the effects of BTX-A may provide important insights to a more optimal clinical use of this treatment strategy.

We expect that in addition to increased tendon compliance the stress relaxation rate of distraction-elongated tendons will increase compared to tendons that were not distracted. The increased tendon compliance is expected because it is a result others have observed in distracted tendons (Fink et al., 1999a, Fink et al., 1999b, Szoke et al., 2005) and although increased stress relaxation has not been demonstrated in such tendons, when healing ligaments display increased compliance they also demonstrate increased stress relaxation rates (Woo and Tkach, 1990). Our hypothesis is that prophylactic BTX-A administration will diminish the distraction-induced increases in the stress relaxation rates and compliance of the associated tendons. We expect this result because we observed that prophylactic BTX-A administration preserved joint range of motion whereas uninjected limbs suffered a profound equinus contracture (Olabisi et al., 2007). Our expectation is that preserved joint excursion will correspond to preserved tendon properties.

Section snippets

Surgical procedures

All procedures were performed in accordance with the guidelines and approval of the University of Wisconsin’s Institutional Animal Care and Use Committee (IACUC). Surgical procedures were performed on animals anesthetized with vaporized isoflurane, adjusted as needed.

The left tibias of 20 skeletally mature New Zealand White rabbits, weighing 3.0–4.0 kg, were distracted as previously described (Olabisi et al., 2007). Briefly, an anteromedial longitudinal incision was performed along the

Tendon length

Data were not included for 1 of the 20 animals due to file corruption during data recovery. All limbs were successfully elongated by 20 mm. Harvested TA tendons were longer than their contralateral controls by 9, 8, and 11 mm for Saline, BTX-ATA, and BTX-AGA groups, respectively. We previously reported the total elongation of the muscle-tendon unit of these groups by 22, 21, and 18 mm, respectively (Olabisi et al., 2007). Thus, the tendon accounted for 41, 38 and 61 percent of the elongation.

Discussion

Results from this study support our hypotheses that DO increases both tendon compliance and the viscous response and that BTX-A administration prior to DO can attenuate these mechanical responses. We have previously shown that during limb lengthening, the TA muscle is adversely affected when directly injected with BTX-A, yet the muscle is protected when the toxin is injected into the antagonist GA (Olabisi et al., 2007, Olabisi et al., 2008). Herein, we show that BTX-A injection into the TA

Conflict of interest

The authors report no conflict of interest.

Acknowledgements

This research was financially supported by the University of Wisconsin Department of Orthpedics and Rehabilitation, and the Orthopaedic Research and Education Foundation (OREF).

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