Tendons serve primarily to transmit muscle-derived force to bone, which provides the capacity for locomotion, as well as to work in concert with ligamentous structures to achieve dynamic joint stability, which provides secondary static restraint to joint translation.1,2 Mechanisms of tendinous injury include acute, chronic, or iatrogenic trauma as well as secondary degenerative inflammatory processes.1–4 Tendon laceration accounts for 0.7% of all appendicular musculoskeletal diagnoses.5 The outcome of tendinous repair in dogs can be variable and is dependent on multiple factors. Factors affecting the ultimate outcome of tendon repair include the nature and location of the injury, suture material and pattern used for repair, tendon blood supply, limb immobilization, weight bearing during the postoperative period, passive range of motion, and chronicity of the tendinous injury.1–4 Surgical techniques used for repair must ensure tendinous apposition while preventing the development of gap formation.
Identification of tenorrhaphy techniques that resist gap formation at physiologic loads is a necessary step in determining the efficacy of epitendinous sutures in tendon repair before clinical application in canine patients. In contrast to the controlled range of motion, formulated rehabilitation protocols, and protected weight bearing achievable in human hand surgery, it is often difficult to implement controlled postsurgical restrictions of weight bearing and limb use in dogs. Thus, large loads exerted on a repair may increase the risk of early rerupture and development of gap formation at the surgical site.6–9 Therefore, surgical tendon repairs need to withstand considerable tensile forces in the immediate postoperative period. Methods of adjunctive support after tendon repair in dogs include insertion of polypropylene mesh,10 tendon plating,11 use of a fascia lata autograft,12 use of a semitendinosus flap,13 and reinforcement with porcine intestinal submucosa.14 Internal or external coaptation in dogs is often used to further protect the repair from extreme loads during postoperative healing; however, coaptation is associated with a high degree of morbidity.15
Epitendinous sutures, also known as peripheral circumferential sutures, are commonly used in flexor tendon surgery in humans and have been recently described as an adjunct to core suture repair techniques for veterinary patients.a Epitendinous sutures play an important role in overall strength of a repair,6,7,16,a increasing strength of the repair site by 10% to 50% over that achieved by use of core sutures alone.8 However, epitendinous sutures are considered to be weaker than core sutures as a component of the repair.9
In general, failure is initiated by the development of a gap between ends of the tendon.9 Gap formation leads to a reduction in strength of the repair and risk of reinjury at the repair site.1 Load transmission to the suture component of the tenorrhaphy is considered to be the initiating factor for failure.17 In humans, up to 64% to 77% of applied load is borne by the peripheral suture alone.18,19 Given that peripheral epitendinous sutures are weaker than core sutures, attention should be focused to improve this aspect of tendon repair.
The primary objective of the study reported here was to determine whether bite depth for placement of epitendinous sutures would affect biomechanical strength and gap formation of repaired tendons. Our null hypothesis was that gap formation and rupture rates would remain consistent for epitendinous sutures placed in a continuous nonlocking pattern at various depths of suture bite penetration for tenorrhaphy repairs.
Materials and Methods
Sample
Forty-eight SDFTs were harvested from cadavers of 24 healthy mixed-breed adult dogs immediately after the dogs were euthanized at a local animal shelter. Dogs were > 1 year old and weighed between 20 and 30 kg. Dogs were euthanized with an IV infusion of sodium pentobarbitalb; dogs were euthanized for reasons unrelated to the study reported here. Dogs with a history of orthopedic disease or evidence of orthopedic disease during examination were excluded.
Experimental procedures
All soft tissues were removed, except for the musculotendinous unit of the SDFT from its origin on the medial aspect of the humeral condyle to its insertion on the manus. Each tendon was wrapped separately in gauze soaked in saline (0.9% NaCl) solution; both tendons of each cadaver were stored in the same plastic bagc at −20°C until the time of testing. Tendons were thawed at room temperature (21°C) for 8 to 10 hours prior to mechanical testing by use of a validated technique.20
Each tendon was sharply transected in a transverse plane with a No. 10 scalpel blade. Tendons were transected 2.0 cm distal to the musculotendinous junction. Tendon transection was performed on a hard and durable surface to facilitate a perpendicular standardized cut across each tendon. After the tendons were transected, the cut surfaces of each tendon were placed beside a calibrated ruler (ruler was placed 5 cm from and parallel to the cut edges of the tendon) and photographed.d Cross-sectional area of each tendon was measured by 1 investigator (Y-JC) by use of an imaging software program.e
Tendon repair
Tendons were assigned by use of a random number generatorf to 1 of 3 groups (16 tendons/ group); both limbs from a dog were not allowed to be placed in the same group. All epitendinous sutures were performed with 3–0 polypropylene suture on a swaged V-20, 26-mm, 1/2-circle taper needle.g Each suture package was sterile, was used before the manufacturer's expiration date, and was opened immediately prior to use. All suturing was performed by a board-certified veterinary surgeon (DJD) who was experienced with tendon repair. Suturing was performed by use of optical magnification,h with 8 to 10 strands crossing the repair site in a continuous nonlocking circumferential manner, as described elsewhere.9 A simple continuous epitendinous suture pattern was chosen because it is frequently used in human patients with flexor tendon injuries.16
Tendons of group 1 were repaired with sutures placed 1 mm from the tendon edge and at a depth of 1 mm on each needle pass (Figure 1). Tendons of group 2 were repaired with sutures placed 2 mm from the tendon edge and at a depth of 2 mm on each needle pass. Tendons of group 3 were repaired with sutures placed 3 mm from the tendon edge and at a depth of 3 mm on each needle pass. A calibrated surgical ruler and fine-tip markeri were used to ensure consistent depth of needle penetration associated with each needle pass. Sutures were placed 2 to 3 mm apart with bites placed 10 mm from the tenotomy in a proximodistal direction in each tendon segment. A single square knot followed by 3 throws was used after ends of the tendon were drawn together into close apposition without tissue bunching at the repair site. Although subjectively assessed, a standard amount of tension was placed on the suture before the knot was tied. Suture ends were then cut at a length of 3 mm. Because the objective of the study was to evaluate effects of only epitendinous sutures, a core repair technique was not used for any tendons. Throughout the duration of testing, all specimens were moistened with saline solution from a spray bottle to prevent tissue desiccation.
Tensile testing
All testing was performed in a uniaxial material tensile testing machinej at room temperature. The distal aspect of the humerus of each surgically repaired tendon was rigidly attached to a custom jig, and a 4.5-mm-diameter stainless steel bolt was placed in a mediolateral direction through the gsupratrochlear foramen. This bolt then was connected to a 500-N load cell mounted on the crosshead of the machine. The distal aspect of the manus was affixed securely in a custom bone clamp.k Musculotendinous units were positioned in a vertical orientation to mimic the in vivo direction of a load applied to a repaired SDFT placed in extension in a splint immediately after surgery. A preload of 2 N was applied, and elongation measurements were calibrated to 0 to ensure a consistent starting point for all test specimens. Constructs were then distracted to failure at an extension rate of 20 mm/min. Load and displacement data were collected by the test system softwarel at a frequency of 100 Hz. During testing, gap formation was recorded by use of a high-definition cameram synchronized with the test system software; the camera was positioned 15 cm from the tenorrhaphy site. A calibrated ruler was aligned adjacent to the tendon within the field of view during recording of each test.
A load displacement curve was generated by the test system software. Yield force, peak force, and failure force were determined by evaluation of the load displacement curve. Yield force was defined as the point at which the first deviation from linearity in the load displacement curve was detected. Peak force was defined as the maximum force measured during each test. Finally, failure force was defined as the force at which the epitendinous suture failed or was pulled through the tendinous tissue. A custom programn was developed to assist with selection of these data points. In addition, mode of failure was visually determined by 1 investigator (Y-JC) at the time of testing and confirmed by review of the videotaped data.
Gap formation was determined by review of the videotaped data. A minimum gap distance between tendon ends of 1 and 3 mm, was measured by use of a digital caliper calibrated by use of an imaging software program.e Videotaped images were sequentially assessed to determine the exact time points when gaps of 1 and 3 mm were detected at the repair site. These time points were cross-referenced with the load data to establish the force required to create gaps of 1 and 3 mm.
Statistical analysis
A sample size calculation was performed by use of failure forces detected in another study21 and results of preliminary experiments. Results of that calculation indicated that 16 tendons/ group would provide 90% power (95% confidence level) to detect a mean ± SD difference of 20 ± 8 N between groups. Data were assessed for parametric distribution by use of the Shapiro-Wilk test for normality. Continuous variables were normally distributed and reported as mean ± SD. Differences in means among groups were assessed by use of a mixed linear model that controlled for tendon cross-sectional area and included group as a fixed effect and each cadaver as a random effect. Pairwise comparisons of least squares means were conducted with the Bonferroni adjustment for multiple comparisons. Proportional distributions for failure mode were compared among groups by use of the Pearson χ2 test of association. All analyses were performed with commercially available software.o Values of P < 0.05 were considered significant.
Results
Tendon data
All specimens were successfully transected, sutured, and biomechanically tested without error. None of the specimens were rejected at the time of testing, and all tendons were included in the final statistical analysis. Left and right limbs were equally distributed among the groups (P = 0.779). Mean ± SD cross-sectional area of all tendons was 0.19 ± 0.04 cm2; there was no significant (P = 0.441) difference in cross-sectional area among groups or between contralateral limbs. Yield, peak, and failure forces were significantly (P = 0.003) associated with tendon cross-sectional area; thus, we controlled for cross-sectional area during subsequent statistical analysis.
Load data
Data on yield, peak, and failure forces were summarized (Table 1). Yield force was significantly (P < 0.001) different among groups. Results indicated that as bite depth for placement of an epitendinous suture increased, yield force also increased. Mean ± SD yield force differed significantly (P < 0.001) between groups 1 (64.6 ± 27.6 N) and 3 (127.0 ± 38.6 N) and between groups 2 (75.5 ± 35.7 N) and 3, but yield force did not differ significantly (P = 0.667) between groups 1 and 2 (Figure 2).
Mean ± SD values for yield force, peak force, and failure force for canine SDFTs repaired by use of a continuous nonlocking circumferential epitendinous suture placed at a depth of 1 mm (group 1), 2 mm (group 2), and 3 mm (group 3) from the tendon edge (16 tendons/group).
Group | Yield force (N) | Peak force (N) | Failure force (N) |
---|---|---|---|
1 | 64.6 ± 27.6a | 70.9 ± 28. 1a | 69.3 ± 28.2a |
2 | 75.5 ± 35.7a | 80.8 ± 33.0a | 80.1 ± 33.4a |
3 | 127.0 ± 38.6b | 136.0 ± 41.0b | 135.8 ± 40.6b |
Within a column, values with different superscript letters differ significantly (P < 0.001).
Significantly (P < 0.001) more force was required to reach peak force as bite depth for the epitendinous suture increased. Mean ± SD peak force differed significantly (P < 0.001) between groups 1 (70.9 ± 28.1 N) and 3 (136.0 ± 41.0 N) and between groups 2 (80.8 ± 33.0 N) and 3, but peak force did not differ significantly (P = 0.719) between groups 1 and 2. This pattern was also evident for failure force (Figure 3). Mean failure force differed significantly (P < 0.001) between groups 1 (69.3 ± 28.2 N) and 3 (135.8 ± 40.6 N) and between groups 2 (80.1 ± 33.4 N) and 3 but not between groups 1 and 2.
Gap formation
The force required to create a 1-mm gap at the tenorrhaphy site differed significantly (P < 0.001) among groups. Mean ± SD force required to create a 1-mm gap differed significantly between groups 1 (61.5 ± 31.2 N) and 3 (119.2 ± 42.7 N; P < 0.001) and between groups 2 (70.6 ± 32.8 N) and 3 (P = 0.002), but it did not differ significantly (P = 0.777) between groups 1 and 2. The force required to create a 3-mm gap was significantly (P = 0.010) greater than the force required to create a 1-mm gap, and the force required to create a 3-mm gap was significantly (P = 0.016) greater for group 3 than for groups 1 and 2. However, there was not a significant (P = 0.54) difference in the incidence of 3-mm gaps among the 3 groups (11 specimens from group 1, 8 specimens from group 2, and 10 specimens from group 3 had evidence of a 3-mm gap).
Failure mode
Repairs failed because of suture breakage or suture pulling through the tissue. Failure mode did not differ significantly (P = 0.596) among groups, with suture pulling through the tissue as the most common reason for failure (43/48 [89.6%] specimens), compared with suture breakage (5/48 [10.4%] specimens).
Discussion
Analysis of data for the study reported here indicated that insertion of a continuous epitendinous suture placed at a depth of 3 mm into the tendon substance significantly increased yield force and failure force by > 90%, compared with results for sutures placed at a depth of 1 mm from the tendon surface. Results supported the deeper placement of epitendinous sutures, which is a simple technique modification that could substantially improve strength of tendon repairs.
In the ex vivo study reported here, we evaluated the biomechanical properties of a peripheral epitendinous suture alone. Findings indicated that epitendinous sutures were an important structural component, imparting substantial strength to the overall tendon repair and resistance to gap formation. In a study22 conducted to compare pullout strength of a single peripheral suture placed within the epitenon alone or within the epitenon and also incorporating tendon fibers, inclusion of a greater number of tendon fibers significantly increased the strength of the repair (83% as strong as that for sutures in epitenon alone). These findings suggest that increasing depth of penetration of peripheral sutures can improve tensile strength of tendon repair. However, depth of placement of the peripheral sutures into the tendinous core was not controlled in that study.22 In a similar study,19 investigators used flexor digitorum tendons from human cadavers. Tendon lacerations initially were repaired by use of a modified locking-loop (Kessler) core suture, with one group receiving an additional superficial peripheral suture and the other group receiving a supplemental deep (placed at half the depth of the tendon) peripheral suture. In that study,20 mean load to failure of the deep peripheral suture group (38.96 N) was approximately 1.8 times that of the superficial suture group (21.68 N). However, depth of suture penetration was not standardized among specimens. In the present study, we found that increasing the standardized bite depth for a single peripheral epitendinous suture from 1 to 2 mm and from 1 to 3 mm significantly increased yield loads by 17% and 97%, respectively. In a similar manner, increasing bite depth of sutures significantly increased failure loads by 16% and 96%, respectively. These findings supported the contention that there was improvement of the epitendinous suture–tendon interface, wherein deeper placement of a peripheral suture resulted in significantly stronger tendinous repairs. When used with a core suture, an increase in forces borne by the epitendinous suture may decrease the force exerted on the core suture and the core suture pattern, thus leading to superior load sharing between the epitendinous and core sutures. Results for the study reported here are in agreement with those of other reports7,19,23,24 in which the addition of an epitendinous suture was found to provide increases of up to 50% in ultimate load to failure and stiffness. Biomechanical characteristics of complimentary epitendinous-core suture repair methods may result in substantial improvements in overall strength of tendon repairs when traditional core methods of tendon repair (eg, locking loop25 or 3-loop-pulley10) are used and should be investigated further.
Resistance to gap formation between tendon ends is an important attribute for the success and ultimate outcome of repair of canine tendons. Gapping of > 3 mm leads to a decrease in ultimate force and stiffness achieved by the sutured repair.1 Gap formation leads to the deposition of mechanically inferior scar tissue, which increases the risk of rerupture at the surgical site during the first 6 weeks after injury.1,26 In the study reported here, increasing the bite depth of epitendinous sutures reduced the incidence of gap formation, with sutures placed deeper requiring a significantly higher force to cause separation between tendon ends. Results of the present study are in agreement with those of other studies19,21 in which it was found that an epitendinous suture reduces gapping; thus, these findings support deeper placement of epitendinous sutures. Results of a biomechanical evaluation revealed similar findings for an ex vivo canine studya in which there was a complete absence of gapping between tendon ends when a continuous suture was placed in addition to core 3-loop-pulley and locking-loop patterns. Caution must be used when making comparisons among studies. In the aforementioned study,a depth was not directly controlled, and a larger caliber suture (size 0) was used for epitendinous repairs, compared with the controlled depth and size of suture (size 3–0) used in the present study.
Resistance to gap formation is dependent on multiple factors.1,26 In another ex vivo study,27 investigators described modifications to improve strength of tendon repairs and reduce gap formation. These modifications included increasing suture penetration in a proximodistal direction from the repair site (from 7.5 to 12 mm), increasing the size of the epitendinous suture, and use of an anatomic epitendinous repair with deeper placement of the epitendinous suture. These components influence the success of tendinous repair and have been widely adopted by surgeons who perform repairs on the distal portions of the extremities of humans.16,21,27,28 In the present study, forces supported by the repair were positively associated with tendon cross-sectional area. It has been found that the strength of tendon repair is directly proportional to the number of longitudinal stitches that cross the repair zone.28 Increasing the tendon cross-sectional area increases the body of tendinous tissue available for insertion of sutures, which leads to more strands crossing the repair site and thus strengthens the repair, which is in agreement with a biomechanical study29 conducted with cadaveric specimens.
Epitendinous patterns typically fail as a result of suture breakage or suture pulling through the tissues.19,21,30 In the veterinary literature, it has been reported that knots represent the weakest portion of the suture line.31 Knots also are the weak point in flexor tendon repairs.32 However, we found that in 43 of 48 (89.6%) of the repairs in the present study, failure was attributable to the fact that the epitendinous suture pulled through the tissues, instead of suture breakage or unraveling at the knot, which is in agreement with the findings of other studies.32,a These findings may be explained by differences in the force required to overcome the suture-collagen interaction among repairs and the epitendinous pattern used in the present study. The continuous, circumferential nature of the epitendinous suture placed around the periphery of the repair incorporated a much larger number of collagen bundles than are incorporated in traditional single core repairs. We hypothesize that epitendinous sutures allow uniform load distribution between the suture and tendon substance. In the study reported here, a continuous epitendinous suture was selected for use on the basis of the findings of a recent study9 in which investigators found no difference between various continuous epitendinous patterns in regard to suture elongation or yield loads. The locking nature of some epitendinous suture patterns allows incorporation of an even greater number of collagen fibrils and is superior to nonlocking patterns in bovine tendons.33
Another factor influencing mode of failure is suture size. As suture size increases, the weakest part of the repair becomes the suture-tendon interface, and suture pulling through the tissues becomes more likely. Additional research is needed to elucidate the most appropriate suture size to resist failure while not adversely affecting tendon blood supply, increasing repair site bulk, or impairing glide function.
Limitations of the present study included its ex vivo nature, lack of preconditioning of the tendons and suture, and evaluation by use of a single load to failure rather than evaluation via cyclic loading. Cyclic testing at physiologic loads rather than a single ramp-to-failure test method more accurately represents in vivo conditions and reveals gap formation not readily apparent on load-to-failure testing in flexor tendons of the human hand.34 In the cadaveric study reported here, relevant in vivo factors (eg, tissue reactivity; risk of infection, inflammation, or fibrosis; and the effect of suture placement on blood supply) were not assessed. We were interested in the use of uniaxial loading to determine the biomechanical characteristics of epitendinous repairs without core suture support. Visibly healthy tendons that were sharply transected were used, which differs markedly from tendons in clinical patients, wherein chronic degenerative changes often lead to fraying of the tendon and decreases in suture holding capacity. In clinical scenarios, interactions between the suture and tendon substance and the holding power of tissues may differ from those in the study reported here. As part of the design of the present study, musculotendinous specimens were collected from a homogenous population of medium− to large-breed dogs. Thus, results reported here may not be applicable to smaller dogs or other thinner, flatter tendons.
Results of the study reported here indicated that the in vitro behavior of sutured tendons differed on the basis of depth of suture penetration into the tendinous tissue. Increasing the bite depth from the edge of the tenotomy toward the center of the tendon substance significantly increased strength of the repair site and decreased the incidence of gap formation between tendon ends. Placing epitendinous suture bites at a greater depth should provide increased biomechanical strength to tendon repairs and resistance to gap formation. Epitendinous suture techniques should be investigated in vivo to evaluate effects on tendon healing and blood supply prior to clinical implementation. Studies should be conducted to evaluate use of epitendinous sutures in conjunction with core suture patterns to further elucidate effects on canine tendon repairs.
Acknowledgments
Suture was provided by Medtronic Inc.
The authors did not receive any financial support for the study. The authors declare there were no conflicts of interest related to the study.
The authors thank Jon Hash for assistance with collection and storage of cadaveric specimens.
ABBREVIATIONS
SDFT | Superficial digital flexor tendon |
Footnotes
Putterman AB, Duffy DJ, Kersh ME, et al. Effect of running continuous epitendinous suture pattern for flexor tendon repair in combination with three-loop pulley and locking loop suture patterns in a canine cadaveric model (oral presentation). Am Coll Vet Surg Summit, Phoenix, October 2018.
Euthasol, Virbac AH Inc, Fort Worth, Tex.
Ziplock, 1-gallon, SC Johnson & Son Inc, Racine, Wis.
iPhoneXR, Apple Inc, City, Calif.
ImageJ, National Institute of Health, Bethesda, Md.
Research Randomizer. Available at: www.randomizer.org. Accessed Jun 14, 2019.
Surgipro, Covidien Ltd, Dublin, Ireland.
4.5X surgical loupes, Surgitel, General Scientific Corp, Ann Arbor, Mich.
Medline, Northfield, Ill.
Instron model 5944, Instron, Norwood, Mass.
SKU 1652–1, Sawbones, Vashon Island, Wash.
Bluehill 3, Instron Inc, Norwood, Mass.
Brio 4k Webcam, Logitech, Silicon Valley, Calif.
Matlab, version R2018b, Mathworks, Natick, Mass.
SAS, version 9.4, SAS Institute Inc, Cary, NC.
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