Tendinous laceration involving the common calcaneal tendon (CCT) is the most commonly encountered tendinous injury in dogs.1,2 Historically attributed to traumatic laceration or penetrating trauma, CCT tendinopathy in large-breed dogs occurs predominantly as a result of chronic degenerative changes.1–4 Despite the initial cause of canine CCT injury, surgical correction by suture tenorrhaphy has been associated with increased success rates, return to clinical function, and active limb use postoperatively.2–4 Success of primary surgical CCT tenorrhaphy is dependent on high initial tensile strength at the repair site and resistance to gap formation of more than 3 mm.5 Multiple tenorrhaphy suture patterns have been described and used clinically in dogs, with the 3-loop–pulley (3LP) pattern being biomechanically superior.6 Other patterns such as locking-loop sutures and modified Bunnell-Mayer techniques are frequently used on flat tendons.7–10 Although biomechanically advantageous, the 3LP alone does not adequately counteract the theoretically calculated physiologic load of ∼400 N applied to the CCT, which may predispose to overloading and repair failure.7
Methods of tendon augmentation using either biologic or synthetic nonabsorbable implants have been investigated to improve the biomechanical properties of the repair—specifically, loads to construct failure.11–13 Augmentation using nonabsorbable sutures may increase the risk of surgical site infection, may introduce foreign material to an area with poor soft tissue coverage, and may act as a nidus for bacterial adherence if contaminated intraoperatively.11,14 Support of the primary CCT tenorrhaphy via calcaneotibial screw placement can be beneficial for maintaining talocrural joint extension and offloading the repair site; however, implant fatigue or screw loosening, bending, or failure may necessitate early implant removal.15 Both internal and external coaptation techniques can predispose to additional soft tissue injury, leading to the development of pressure sores, pyoderma, and pin tract morbidity requiring additional medical care, client costs, or surgical reintervention.16–18 Meeson et al16 reported complication rates for soft tissue injuries with cast application in ∼60% of patients with 20% of these complications classified as severe. Regardless of the technique used intraoperatively for tendon repair, use of repair site protection is considered a necessary postoperative treatment modality for 6 to 10 weeks.16
Use of autografts has been widely studied and implemented clinically in human patients with chronic CCT ruptures,19 although there is currently a paucity of information in dogs, with autologous tissues used for the successful treatment of tendonitis and tendon lacerations in equids.20,21 Purported benefits of superficial digital flexor tendon (SDFT) autograft use during CCT tenorrhaphy include its close proximity to the repair site, use of a single incision for graft harvest, minimal cost, and a low risk of tissue reactivity.2 In addition, tendinous autografts may serve as an internal biologic scaffold for fibroblast and tenocyte migration to the repair site.2 Although limited information currently exists to support the use of autologous grafts in dogs, use of the lateral digital extensor and flexor digitorum lateralis tendons, fascia lata graft autograft, and fibularis brevis and fibularis longus muscles have all been reported.20–24 If deemed to be biomechanically efficacious, SDFT autograft use in dogs may provide a locally available and affordable autograft that is easily accessible for graft harvest and tendon augmentation during surgery. Biomechanical evaluation prior to clinical application is required to allow informed use of these grafts for tendinous repair.
The objective of this study was to evaluate the influence of SDFT graft augmentation on the biomechanical properties and resistance to gap formation in a canine gastrocnemius tendon (GT) repair model. We hypothesized that SDFT graft augmentation in addition to a core 3LP pattern would improve the biomechanical properties of the repair. Our secondary hypothesis was that SDFT graft augmentation would decrease the occurrence of gap formation between tendon ends at the repair site compared to the use of a 3LP pattern alone.
Materials and Methods
Specimen collection
A pilot study determined the method of specimen acquisition, tendon preservation, SDFT graft harvest, and biomechanical testing protocol to be used after construct repair. Whole hindlimbs from canine cadaveric specimens were obtained from a small animal shelter following euthanasia (Beuthanasia-D solution, Merck) for reasons unrelated to this study. Inclusion criteria included adult dogs weighing 25 to 32 kg, free from orthopedic disease based on a focused examination by a single board-certified surgeon (DJD). An animal care and use committee protocol was not required by the North Carolina State Veterinary Teaching Hospital for the purposes of this study because of the secondary use of cadaveric tissues. Dogs were excluded if they had evidence of hindlimb pathology. Stifle and talocrural joints were evaluated after a focused orthopedic examination and mini-medial parapatellar stifle arthrotomy, and after transection of the tibiotarsal collateral ligaments, respectively, performed by one of the study authors (DJD).
Tendinous dissection and repair
Hindlimbs were acquired serially from 14 skeletally mature dogs. The sex and reproductive status of each dog were not recorded. Specimens were inspected carefully for any abnormalities affecting the bone, tendon, or musculotendinous apparatus. Initially, all components of the common calcaneal tendon were isolated carefully from underlying tissues. Paired GT and associated proximal musculocutaneous contributions were dissected from their origin at the supracondylar eminence of the distal femur to their insertion point on the proximocentral aspect of the tuber calcanei. Further dissection to isolate the individual components of the CCT, including the GT, SDFT, and accessory tendon, were performed by a single trained investigator (Y-JC).
A reciprocating saw (DeWalt) was used to create a transverse osteotomy in the distal femur, 2 cm proximal to the trochlear groove. A mediolateral bone tunnel was made using a 4.5-mm drill bit equidistant between the cranial and caudal cortical margins. The talocrural joint was disarticulated using a 10 blade to cut the collateral ligaments and joint capsular attachments. All tissue remaining distal to the tarsus was left unaltered to aid with distal specimen fixation. After tendinous dissection, specimens were stored at –20°C in a thermostatically controlled environment until the time of testing, after being wrapped individually in moist 0.9% sodium chloride–soaked gauze. Prior to definitive testing, each limb was thawed completely at 21°C for 10 to 12 hours. A tenotomy was then performed in a transverse plane across each paired GT regardless of group assignment using a #10 scalpel blade at a measured distance 2 cm proximal to the GT enthesis on the calcanean tuberosity. This measurement was made using a calibrated ruler (Surgical Ruler, Medline). Each tenotomy was performed on a stable surface that provided counter pressure during transection. After tendon transection, the cut surface of each of the paired GTs was held 5 cm from a digital camera to obtain a digital photograph (iPhone 10XR, Apple). The mean tendon cross-sectional area (CSA) was then calculated (Image J version 1.41; NIH) by a single trained investigator (JKD).
Experimental groups
Each hindlimb was assigned randomly to 1 of 2 equally sized treatment groups (n = 14) using a random number generator (Research Randomizer). Because this was a paired study, each hindlimb acted as its own control, with an equal number of hindlimbs assigned to each experimental group. Repairs were performed in a randomized manner to minimize any potential bias or learning curve using a variables data sheet. In the 3LP group, core repairs were performed using 2-0 USP monofilament polypropylene suture (Surgipro, Covidien) according to a previously described technique.8 Suture bites were taken at 5, 10, and 15 mm from the transected edge of the tendon. Each loop was oriented 120° to the prior, resulting in loops oriented 60° from each another. Core 3LP repairs were tightened sequentially until tendon end approximation occurred, taking care to avoid visually evident bunching at the repair site. A square knot followed by 3 additional throws was used with the suture cut 3 mm from the knot. In this group, the SDFT was removed at the level of the calcaneal–quartal–central joint, the flexor retinaculum incised, and the SDFT transected at the myotendinous junction using a #15 blade to remove this musculotendinous attachment en bloc.
For the 3LP + SDFT graft group, the contralateral hindlimb from each cadaver was repaired initially using a core 3LP technique as described earlier.6,8 After 3LP completion, the distal aspect of the SDFT was isolated carefully and dissected further to allow for graft mobilization prior to 3LP augmentation. After mobilization, the SDFT was opposed closely to the caudal aspect of the primary GT repair using a total of 12 full-thickness cruciate sutures of 3-0 polypropylene (Surgipro, Covidien) to secure the SDFT to the underlying GT. Sutures were placed starting immediately proximal and distal to underlying 3LP suture bites (Figure 1). In total, 6 full-thickness sutures were placed on the medial and lateral aspects of the repair, respectively, to secure the SDFT graft. Each suture was tightened subjectively without tissue compression and completed using a square knot, followed by 3 additional throws. Suture tags were cut to a length of 3 mm. In both groups, GT ends were held in close apposition during repair using 20-gauge needles supported by a single investigator (Y-JC). All constructs were repaired by a single board-certified surgeon (DJD) experienced with tendinous repair in both clinical and research settings. An unopened, sterile suture packet was used for each test. Testing was completed in three separate laboratory sessions and data subsequently collated by a single investigator (JKD).
Example specimen in the 3-loop–pully (3LP) + superficial digital flexor tendon (SDFT) graft group showing the paired gastrocnemius tendons that were repaired using (A) the 3LP followed by augmentation using the SDFT (mediolateral orientation) and (B) the 3LP + SDFT graft (craniocaudal orientation). The core suture was applied using a 2-0 USP polypropylene suture; the SDFT graft was adhered using six 3-0 USP polypropylene sutures in a cruciate pattern placed medially and laterally, respectively. A millimeter ruler is positioned to the right of each construct. Please note the core suture has been placed loosely for illustrative purposes only to allow 3LP bites to be identified clearly within the photograph.
Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.22.03.0039
Biomechanical testing protocol
Biomechanical testing was conducted using a uniaxial testing machine (model 5944, Instron), with all tests performed at room temperature (21°C). A modified bone fixation clamp (shoulder clamp, Sawbones) was mounted to the testing apparatus to secure the pes. A 4-mm stainless steel rod was placed transversely through the predrilled hole in the femur to secure the specimen proximally to the custom 3-D–printed testing jig. Repaired limbs, regardless of group assignment, were positioned in a vertical orientation to mimic a postoperative GT repair splinted or held in extension using a calcaneotibial screw. Each repair was filmed at rate of 50 frames/second using a high-speed camera (Panasonic) aligned with the repair site at a distance of 20 cm from the plantar aspect of the tenorrhaphy. A ruler was placed next to each hindlimb within view of the camera.
Initially, a preload of 2 N was applied to establish a consistent resting length among repaired specimens. After this preload was reached, the system was calibrated/balanced to allow for a consistent starting point among independent measures. An automated trigger system allowed for synchronization of load and obtained video data. Repairs were then distracted at a rate of 20 mm/minute until the point of failure or until the load applied reached 800 N. This point was chosen because it represented 2X the theoretical force of 400 N being applied through the CCT at the trot in dogs.5,8 Variables of interest analyzed included load (measured in Newtons) and displacement (measured in millimeters), which were recorded at a frequency of 100 Hz, with data collected using test system software (Bluehill 3, Instron). Yield, peak, and failure loads were identified visually by a single investigator (JKD) who derived the desired data points from curves by selecting regions on the curve manually using a coded scientific program (Matlab R2018b, MathWorks). Yield load was described as the point where nonlinear deformation of the construct occurred. Peak load was described as the maximum force measured during each test.25 Failure load was described as the load where the construct failed or a greater than 50% drop in the load displacement curve occurred.25 Construct failure was defined to occur as a result of suture breakage, suture pull-through, or tissue failure distant to the repair site.25
Obtained high-speed video footage was reviewed by a single investigator (JKD) for evaluation of both 1- and 3-mm gap formations at the tenorrhaphy site using a digital caliper that was calibrated to a known length within an imaging software program (Image J version 1.41; NIH). Sequential frames from each test were evaluated to determine the time points and resultant loads at which 1- and 3-mm gaps developed. A single study investigator (JKD) documented the mechanism of construct failure. A single investigator (DJD) reviewed all collated data.
Statistical analysis
Pilot data were used to perform a sample size calculation that determined ≥ 12 tendons/group would provide at least an 80% power to detect a mean difference of 40 ± 5 N at a 95% CI (5% alpha error rate among independent measures). Collated data were evaluated for a parametric distribution using the Shapiro-Wilk test to assess those data for normality. Tendon CSA data were distributed nonparametrically and compared between groups using the Wilcoxon rank-sum test. Summary statistics for CSA are described using median and range. All other continuous variables were normally distributed and are described as mean ± SD. Differences in group means were evaluated using covariance analysis to allow for control of CSA between hindlimbs from the same cadaver. The Fisher exact test was used to compare proportional distributions in failure mode between groups. All analyses were performed using statistical software (SAS version 9.4, SAS Institute), with P < .05 considered to be statistically significant.
Results
In total, 1 dog (n = 2 hind limbs from a single cadaver) was excluded from analysis because of craniomedial band pathology affecting the cranial cruciate ligament within the stifle joint. Both hindlimbs from this cadaver were consequently excluded from the study. After recruitment of 1 additional canine cadaver (n = 2 hind limbs from the same dog), all specimens were included within the final statistical model. Right and left limbs from each cadaver were distributed equally among experimental groups. There was no difference in CSA between experimental groups (3LP group, 0.098 ± 0.03 cm2; 3LP + SDFT graft group, 0.094 ± 0.33 cm2; P = .675).
Load data
Load data between groups differed significantly from one another (P < .0001). Yield, peak, and failure loads were all significantly greater in the 3LP + SDFT graft group compared to the 3LP group. Load data are summarized in Table 1.
Mean ± SD for yield, peak, and failure loads for canine gastrocnemius tendons repaired with the 3-loop–pully (3LP) alone or the 3LP augmented with a superficial digital flexor tendon (SDFT) graft. Yield, peak, and failure force differed significantly between groups (P < .0001).
| Group | Yield force (N) | Peak force (N) | Failure force (N) |
|---|---|---|---|
| 3LP | 34.2 ± 6.7 | 34.2 ± 6.7 | 34.0 ± 8.0 |
| 3LP + SDFT | 483.6 ± 148.0 | 485.0 ± 144.5 | 478.3 ± 147.9 |
Gap formation data
Gap formation to both 1 and 3 mm differed significantly between groups (P = .009 and P < .0001, respectively). The 3LP + SDFT graft group required 69.9 ± 54.4 N to create a 1-mm gap, whereas the 3LP group required 19.8 ± 10.0 N to create a 1-mm gap. The 3LP + SDFT graft group required 190.2 ± 70.5 N to produce a 3-mm gap compared to the 3LP group, which required 29.9 ± 8.2 N. Gap data are included in Table 2.
Force, occurrence, and frequency of 1- and 3-mm gap formations between groups. There was a difference between the 3-loop–pully (3LP) and the 3LP + superficial digital flexor tendon (SDFT) groups regarding loads to create a gap formation for both the 1- and 3-mm gaps (P = .009 and P < .0001, respectively).
| Gap formation, 1 mm | Gap formation, 3 mm | |||
|---|---|---|---|---|
| Group | Force (N) | Frequency | Force (N) | Frequency |
| 3LP | 19.8 ± 10.1 | 14/14 (100%) | 29.9 ± 8.2 | 14/14 (100%) |
| 3LP + SDFT | 69.9 ± 54.4 | 14/14 (100%) | 190.2 ± 70.5 | 14/14 (100%) |
Failure mode
Mechanism of repair failure did not differ between groups (P = .120). In the 3LP group, 14/14 constructs (100%) failed as a result of sutures pulling through the tendinous tissue. In the 3LP + SDFT graft group, mode of both the 3LP and SDFT graft failures were recorded. A total of 1/14 constructs (7.6%) failed from core suture breakage of the 3LP, 10/14 (71.4%) failed from the 3LP core suture pulling through the tendinous tissues, with 3/14 (21%) of the 3LP core sutures remaining intact. In 2/14 specimens (14.2%) in the 3LP + SDFT graft group, graft failure occurred because of pull-through of the sutures adhering the SDFT graft to the underlying GT. Twelve of 14 (85.8%) of the SDFT grafts remained intact when tested to a maximum of 800 N.
Discussion
Consistent with our hypothesis, the results of this study support the biomechanical advantages of SDFT graft augmentation when applied in addition to a primary 3LP repair in this canine model. SDFT graft augmentation increased assessed biomechanical variables by 14X, and required a 3.6X and 6.5X greater load to cause both a 1- and 3-mm gap, respectively.
The theoretical load borne by the Achilles (CCT) mechanism in a 30-kg dog at a trot has been estimated to be ∼400 N.8 When an SDFT graft was used to augment the primary 3LP repair, failure loads were significantly greater compared to a 3LP pattern alone. Our results are in agreement with prior studies12,13 that support the benefits of increased tensile strength afforded to the repair by augmentation using local autologous tissue graft. It should be noted, however, that the failure and peak loads were much greater in our study than in those reported previously in dogs. Based on our results, we can assume that SDFT augmentation may allow the tenorrhaphy to withstand more than 400 N under conditions of tensile loading. A previous study by Duffy et al12 evaluated the effect of an autologous flexor digitorum lateralis graft applied to augment a primary 3LP core suture repair in a canine model, with an average load to failure of 205 ± 46.4 N. In separate study, Duffy et al13 evaluated the effect of an autologous accessory tendon graft (ATG) applied to augment a primary 3LP repair. In that study,13 loads to failure of 282.9 ± 40.2N were recorded. Both these studies12,13 support the benefits of autologous graft techniques to support the primary repair site and to improve the biomechanical properties compared to primary sutured repair techniques alone. The core suture is most vulnerable to breakage and subsequent failure during the first 42 days after surgical intervention because of the effects of local metabolism and changes at the repair site during the lag phase of healing.8,26 Resistance to repair failure is solely dependent on the core suture alone during the inflammatory and proliferative phases of tendon healing.5,8,26 If an autologous graft is used to supplement and augment a core suture repair, it may be of most benefit during this time. Theoretically, graft augmentation may decrease the rate of early core suture overloading, construct elongation, and fatigue, and may increase the loads required to cause re-rupture and repair failure during the immediate postoperative period. Further research is needed in vivo to determine the effect of SDFT harvest and augmentation in clinical patients within naturally occurring tendinopathy.
The addition of autologous graft augmentation may allow hypothetically for decreased reliance on internal or external coaptation methods after surgery, which may allow for the implementation of earlier controlled limb function and weight bearing in dogs. Decreasing the time required for external coaptation use may also decrease the occurrence of bandage morbidity and costs associated with treatment.16 In human patients, early physical rehabilitation is a mainstay of postoperative therapy after primary tendinous repair.19,26–28 Early tendon excursion and gliding during rehabilitation have been shown to increase restoration of repair-site strength, accelerate healing times, and improve joint health in humans, which may also translate clinically to affected canine patients.19,27–30 When tendon loading is restricted during the initial phase of healing, tendon fibrils heal in a disorderly and randomly organized fashion, ultimately increasing the overall time to return of repair-site strength, leading to decreased structural integrity of the repair.31 Although all biomechanical variables evaluated were greater in the 3LP + SDFT graft group, because of the ex vivo design of this study and lack of clinical long-term assessment, we still strongly recommend repair-site protection in patients with naturally occurring tendon pathology.
Clinical application for autologous graft use for repair of the Achilles apparatus in people has long been recommended and advocated for with various local augmentation techniques, including flexor halluces longus tendon transfer, V-Y advancement flaps, and gastrocnemius fascial turndown flaps.19,29 In humans following primary augmentation using autologous grafts, success rates of 75% have been reported, with return to normal function and decreased occurrence of gapping at the repair site.19 Although assessment in clinically affected dogs is currently lacking, clinical success has been reported in multiple canine and equine studies using novel grafts to repair both acute and chronic CCT injuries.20–24,32,33 The success of these augmentation techniques have, however, reiterated the need for standardization of graft harvest techniques and use in dogs. Further evaluation of SDFT graft augmentation methods should be conducted in a controlled population of dogs. Further exploration of the effects of SDFT augmentation using other core suture repairs and methods for adhering the SDFT graft are required. Additional in vivo studies are needed to determine the clinical outcome after SDFT allograft harvest and use, including long-term graft survival and collagen fibril incorporation into the underlying GT.
Synthetic polypropylene mesh used to supplement core 3LP repairs is reported to fail at loads of 376.9 ± 54.5 N.11 Use of SDFT autologous grafts may be biomechanically advantageous compared to these synthetic nonabsorbable materials, although direct extrapolation between studies make comparisons difficult. Although polypropylene mesh implants increase the load required to construct failure, if contaminated intra-operatively, the synthetic nonabsorbable nature of these grafts can predispose to surgical-site infection. Following flexor tendon repair in people, use of monofilament polypropylene mesh is widely accepted by distal-extremity surgeons as an alternative augmentation technique if tissue retraction has occurred or an insufficient length of tendon graft exists.26,34 Proposed benefits of autologous grafts include decreasing the propensity to infection of the surgical site; however, this was not able to be assessed in our study. Additional postulated benefits of autologous graft use may include decreased immunogenicity of local tissues and natural orientation of collagen fibers within the SDFT that are aligned axially in the direction of the applied load.
Prevention of gap formation at the repair site is considered one of the most important factors during the immediate postoperative period.5 The 3LP + SDFT group required an 3.6X and 6.5X greater load to cause a 1- and 3-mm gap between tendon ends, respectively. In our study, occurrence of 1- and 3-mm gaps occurred in 100% of constructs in which an SDFT graft was used. Our study is in agreement with prior studies evaluating the use of an ATG autograft in which 100% of the constructs also formed 1-mm gaps and 90% formed 3-mm gaps.13 Differences in gapping characteristics may be a result of the method in which grafts were opposed and attached to the underlying tendon. It is plausible that modified Krackow patterns may be superior while providing additional benefits to the tenorrhaphy,12 compared to the interrupted cruciate sutures used for graft adherence in our study. Cruciate sutures were chosen in our study based on the methodology of prior investigators.13 Further research is required to determine the influence of different methods to secure the graft. It should be noted that, compared to the study by Duffy et al,12 our study required 3.2X greater force prior to the point of failure. We postulate that the increased occurrence of gap formation encountered in our study may also relate to the magnitude of the loads experienced at the repair site.
Mode of failure for the 3LP + SDFT graft group was most commonly a result of core suture pull-through (72%), whereas the majority of the SDFT grafts remained intact (85%). These findings are in agreement with a previous study12 in which the primary mode of failure of the core suture in augmented tendons was sutures pulling through the tendinous tissue. The findings observed in our study differ from a previous study13 in which the primary mode of graft failure was suture breakage of the cruciate sutures adhering the autologous graft compared to pull-through of the cruciate sutures in our study. Potential reasons for these observed differences in failure modes may be attributed to differences in core suture types and size of the suture used,7 CSA of the tendons evaluated, and types of tendon used for graft augmentation.35,36 The larger the tendon’s CSA, the greater the number and volume of collagen bundles, and thus the greater the interaction and holding power of the suture. These anatomic and compositional differences between tendon types indirectly influences the strength of the construct predisposing the suture to failure, because the suture itself may represent the weakest part of the sutured construct when graft augmentation is used to support the 3LP core repair.
Limitations of our study include the controlled and standardized nature of tenotomy creation, which differs from tendons affected clinically by chronic degenerative change. Importantly, our study assumes that the SDFT is normal and intact with normal fiber pattern alignment, as complete rupture involving all components of the CCT is seen in ∼40% of dogs.4 Focused orthopedic examination and ultrasonographic assessment should be recommended when SDFT augmentation is being considered prior to surgery. Our study used a single load-to-failure testing protocol rather than an incremental cyclical evaluation. Cyclical loading within the strain tolerances of native tissues in normal dogs maybe more representative of loads encountered in vivo. Single load-to-failure protocols were used purposefully to simulate events of acute overloading placed on the repair and catastrophic failure. The 3LP + SDFT graft group was tested to a maximum load of 800 N. When loads of 800 N were reached during mechanical testing, instrumentation stopped recording automatically. This situation may have underrepresented the load tolerances of native SDFT in dogs. Last, and importantly, the ex vivo nature of our study precluded the assessment of factors clinically relevant in vivo, such as the effect of age, breed, or sex; degenerative tendinopathy and its effects on collagen fibril quality; and the effects of graft harvest on GT blood supply.
In conclusion SDFT augmentation increased yield, peak, and failure forces by 14X across all examined biomechanical variables compared to 3LP repairs alone. SDFT graft augmentation required a 3.6X and 6.5X greater load to cause a 1- and 3-mm gap, respectively, between tendon ends. Our data support the biomechanical advantages of SDFT graft augmentation by increasing repair-site strength and resistance to gap formation of the tenorrhaphy. Additional in vivo studies are necessary to determine the effect of SDFT augmentation on clinical function and limb use after graft harvest prior to clinical implementation in dogs.
Acknowledgments
No funding was provided for the purposes of this study.
Authors have no disclosures or conflicts of interest to report.
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