Elsevier

Acta Biomaterialia

Volume 70, 1 April 2018, Pages 165-176
Acta Biomaterialia

Full length article
Enhanced tendon-to-bone repair through adhesive films

https://doi.org/10.1016/j.actbio.2018.01.032Get rights and content

Abstract

Tendon-to-bone surgical repairs have unacceptably high failure rates, possibly due to their inability to recreate the load transfer mechanisms of the native enthesis. Instead of distributing load across a wide attachment footprint area, surgical repairs concentrate shear stress on a small number of suture anchor points. This motivates development of technologies that distribute shear stresses away from suture anchors and across the enthesis footprint. Here, we present predictions and proof-of-concept experiments showing that mechanically-optimized adhesive films can mimic the natural load transfer mechanisms of the healthy attachment and increase the load tolerance of a repair. Mechanical optimization, based upon a shear lag model corroborated by a finite element analysis, revealed that adhesives with relatively high strength and low stiffness can, theoretically, strengthen tendon-to-bone repairs by over 10-fold. Lap shear testing using tendon and bone planks validated the mechanical models for a range of adhesive stiffnesses and strengths. Ex vivo human supraspinatus repairs of cadaveric tissues using multipartite adhesives showed substantial increase in strength. Results suggest that adhesive-enhanced repair can improve repair strength, and motivate a search for optimal adhesives.

Statement of Significance

Current surgical techniques for tendon-to-bone repair have unacceptably high failure rates, indicating that the initial repair strength is insufficient to prevent gapping or rupture. In the rotator cuff, repair techniques apply compression over the repair interface to achieve contact healing between tendon and bone, but transfer almost all force in shear across only a few points where sutures puncture the tendon. Therefore, we evaluated the ability of an adhesive film, implanted between tendon and bone, to enhance repair strength and minimize the likelihood of rupture. Mechanical models demonstrated that optimally designed adhesives would improve repair strength by over 10-fold. Experiments using idealized and clinically-relevant repairs validated these models. This work demonstrates an opportunity to dramatically improve tendon-to-bone repair strength using adhesive films with appropriate material properties.

Introduction

Tendon-to-bone repair presents a challenging mechanical problem: repairs require strength and resilience to accommodate forces from activities of daily living and to avoid repair site elongation or rupture; however, the strong anchor sutures used for repairs cause stress concentrations that limit attachment strength. This is compounded by stress concentrations associated with the mismatch between compliant tendon and stiff bone [1]. The healthy tendon enthesis facilitates load transfer from tendon to bone in several ways, including by (i) distributing force over a relatively large footprint area to reduce local stresses, (ii) using a compliant transitional fibrocartilaginous tissue to minimize stress concentrations and toughen the attachment [2], [3], [4], [5], and (iii) using randomness of composition and structure to distribute stress during failure [6].

Surgical repairs have high failure rates, possibly because they not only fail to recreate these resilience mechanisms, but also introduce stress concentrations at sutures. For example, rotator cuff healing after repair is notoriously challenging, with post-repair rupture rates ranging from 20% for young, healthy patients with small tears to as high as 94% for massive tears in elderly patients [7], [8]. These failure rates are not surprising from a mechanical perspective. While current double-row suture bridge repair techniques apply compression to the tendon over a large portion (78%) of the bony footprint [9], almost all of the force from muscle to bone is transferred in shear across only two anchor points, where the suture from a bone anchor punctures through the tendon near the musculotendinous junction (Fig. 1A). These stress concentrations, coupled with possible vascular compromise in the same region due to strangulation from inappropriately tensioned repairs [10], lead to the vast majority (86%) of rotator cuff repair ruptures by the tendon pulling through the sutures at those anchor points [11]. Approaches that distribute shear stresses and increase strength without causing tissue strangulation would theoretically decrease failure rates. Approximately half of the US population over 60 years old has a rotator cuff tear, leading to over 500,000 repairs annually [12]. With a growing aging and elderly population, improving on these failure rates is critical to reinstate shoulder function in these patients.

Here, an adhesive-film based approach is proposed to augment standard tendon-to-bone repairs, with a particular focus on supraspinatus tendon rotator cuff repairs for proof-of-concept. This adhesive-based surgical augmentation mimics the natural stress distribution across the repair site to improve repair strength and limit ruptures. We hypothesized that, unlike conventional suture repairs with only a few anchor points (Fig. 1A), this adhesive repair scheme would reinstate load transfer over the entire tendon-to-bone insertion footprint (Fig. 1B). This increase in load transfer is expected to result in an improvement in overall repair construct mechanical properties, similar to an adhesive-coated suture case we examined previously [13]. Achieving the full strength of a healthy tendon enthesis may not be necessary, since the enthesis can accommodate higher loads than are applied physiologically during non-traumatic activities. We therefore aim to generate functional repairs that are capable of sustaining activities of daily living and enhanced rehabilitation protocols.

Following a similar approach to [13], we employed a shear lag analysis to predict the ability of adhesive interlayers to improve load transfer across a repaired tendon-to-bone enthesis. We then analyzed a finite element model with the same geometric and material properties to establish the limits of the scaling law from shear lag analysis for adhesive thickness and adhesive shear modulus. Using these models, we identified desirable adhesive mechanical properties for use in adhesive films for tendon-to-bone repair. We then biomechanically tested adhesives between tendon and bone planks and in human cadaver rotator cuff repairs to validate the models and assess adhesives’ potential for clinical usefulness.

Section snippets

Shear lag model

A shear lag model was studied to (i) identify adhesives with desirable properties for tendon-to-bone repair, and (ii) anticipate load transfer in idealized experiments to assess adhesive properties. The model predicted load sharing across an idealized tendon-to-bone insertion site using an interposed adhesive layer at the interface. The idealized repaired tendon and bone were both modeled as isotropic, homogenous tissue planks for this one-dimensional model.

The model, following Volkersen [15]

Idealized ex vivo repairs

To evaluate how the performance of the adhesive system depends upon the adhesive strength between the adherends and the stiffness of the adhesive material, a modified lap shear test was developed. A series of idealized tendon-to-bone plank repairs was performed using 1/8 thick bovine deep digital flexor tendon planks adhered to 1/4 thick bovine femur cortical bone planks (both planks were 15 mm wide, with 10 mm overlap length; Table 1). Fresh-frozen bovine deep digital flexor tendons (age

Shear lag and finite element models

Shear lag and finite element modeling revealed an ideal design space for adhesive mechanical properties to improve load transfer across tendon-to-bone repairs (Fig. 4, band inside blue dotted box, including the elastomer material class). As with adhesive-coatings on sutures [13], mechanically desirable adhesives should be compliant in shear while maintaining high binding and shear strengths. Higher deformation of compliant adhesives facilitates load distribution over larger lengths than stiff

Discussion

Current operative techniques for rotator cuff tendon repair rely on load transfer in shear across only a few suture anchor points (Fig. 1). Variations on this approach have reached a limit for mechanical fixation, where increased numbers of strands or anchor points do not lead to improved outcomes (e.g., most studies have shown that single-row repairs and double-row repairs are equivalent clinically [34]). Recent research has instead focused on biological augmentation to facilitate improved

Conclusion

Strengthening tendon-to-bone repairs is essential to enable adequate healing and functional recovery, particularly for the rotator cuff, where repair outcomes are poor. Modeling and experimental validation indicate that adhesive films can augment current surgical approaches by transferring stress between tendon and bone over the entire enthesis footprint area, instead of relying only on a small number of anchor points. Even the sub-optimal multipartite adhesives evaluated here for model

Author contributions

SWL derived the shear lag model with help from VB and GMG. MG created and executed the finite element model to compare to the shear lag model, with guidance from SWL, GMG, VB, and ST. SWL designed and performed all experiments with guidance from ST, VB, and GMG. WNL performed the cadaver rotator cuff surgeries and provided input into how to apply adhesives during surgeries. SWL, MG, and TRG dissected the cadaver shoulders before and after surgical repair, and performed the shoulder

Acknowledgements

Mr. Donghwan (Eric) Yoon planed many of the tendon planks used here. Tendon planks were planed using a sliding microtome in Professor Spencer Lake’s laboratory at Washington University in St. Louis. This study was supported by the National Institutes of Health (NIH): U01 EB016422 (to ST and GMG), R01 AR062947 (to ST), and F30 AR069491 (to SWL). Additionally, this study was supported by translational research grants from Washington University Institute for Translational and Clinical Sciences and

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