Introduction
The frequency of tendon injuries in dogs is relatively low1; however, surgical intervention is recommended because of the severe clinical signs and limb dysfunction associated with musculotendinous disruption.2,3 Prior studies4,5,6 have demonstrated that the ideal suture technique used at the repair site should provide direct tendon-end anastomosis with adequate tensile strength while preventing gap formation while allowing the progression of direct contact healing. Formation of a gap > 3 mm leads to delayed healing times, decreased repair site strength, and an increased risk of rerupture during the early stages of tendon healing.7
In the human medical literature, variations in regard to suture technique have been evaluated to assess their influence on tensile strength and their ability to prevent gap formation.4,8,9 Experimental variables such as suture caliber,10,11,12 the number of suture strands traversing the repair,13,14 the depth of core suture placement,15,16 peripheral epitendinous suture use,11,17 bite depth of the epitendinous suture,18 and bite distance of the epitendinous suture from the transection site19 have been shown to positively affect resistance of the suture construct against deformation under loading in both human and veterinary medical studies. These repair principles have the clinical importance of aiding a surgeon's ability to determine the most appropriate technique and repair methodology for use in clinical cases.8,20
To the authors’ knowledge, no studies in the human or veterinary medical literature have directly examined the effects of increasing the number of suture strands on construct strength in an experimental model of canine tendon repair. Research studies have been performed with ovine,21 porcine,22 and canine13,14,23 tendons owing to their anatomic and biomechanical similarities. A previous study24 of cadaveric human tendons showed that primary repair pattern modifications affect the tensile strength of repairs.
The objective of the study reported here was to determine the effects of 2-, 4-, 6- and 8-strand repairs on the biomechanical properties of canine gastrocnemius tenorrhaphy constructs. Our hypothesis was that construct strength would be positively associated with an increasing number of suture strands crossing the repair site in this controlled canine research model. The fact that published studies to date have used a variety of suture patterns and tendons means that variables such as the number and size of locking loops, length of suture purchase, and core suture bite depth differ, which can make comparisons among studies challenging.13,14,25 Therefore, we selected a simple interrupted pattern to evaluate the effect of increasing the number of strands crossing the repair site while controlling for other variables that have previously been shown to affect construct strength. Having this information could help to inform suture pattern refinement, repair methods, and pattern selection in clinical cases and improve our understanding of the contribution that suture strand number makes to repair strength.
Materials and Methods
Specimen collection
We harvested 56 hind limbs from 28 large-breed adult dogs immediately following euthanasia by IV administration of a commercial euthanasia solution (Beuthanasia-D solution; Merck) for reasons unrelated to this study. All dogs were euthanized for reasons unrelated to musculoskeletal disease states on the basis of a focused orthopedic examination prior to specimen dissection by 1 author certified by the American College of Veterinary Surgeons as a specialist in veterinary surgery (DJD). The body weight of the dogs ranged from 28 to 35 kg. The secondary use of cadaveric tissues for study purposes did not require institutional animal care and use committee approval.
Specimen preparation
Gastrocnemius musculotendinous units were dissected free of other tissues from the proximal attachments at the supracondylar eminence on the caudodistal aspect of the femur to the tendinous insertion on the tuber calcanei for each limb. All other muscular attachments and contributions comprising the common calcanean tendon were carefully removed, including the accessory tendon and superficial digital flexor tendon. Transection of the collateral ligaments at the femorotibial and talocrural joints allowed for removal of the musculotendinous unit attached proximally to the femoral metaphysis and distally to the tuber calcanei. A sagittal bone saw (Delta Power Equipment Corp) was used to transect the distal aspect of the femur transversely 5 cm proximal to the stifle joint, and a 4.5-mm bone tunnel was drilled at a measured distance of 1 cm proximal to the femoral trochlear groove in a mediolateral direction to facilitate specimen attachment to the materials testing machine (MTM) for biomechanical testing. Musculotendinous units with their proximal and distal bony attachments were then wrapped in gauze laparotomy sponges soaked in saline (0.9% NaCl) solution and stored as pairs (units from the left and right hind limbs of the same dog) in sealed plastic bags (Ziploc 1 gallon bag; SC Johnson & Johnson Inc) at–20 °C prior to testing. All specimens were thawed at room temperature (21 °C) for 10 hours prior to definitive testing by use of a previously validated technique.26
On the day of testing, a sharp tenotomy was performed for each gastrocnemius tendon (GT) with a No. 10 Bard-Parker scalpel blade 20 mm proximal to the tuber calcanei. The distance to the transection site was measured with a surgical ruler (Sterile Surgical Ruler; Medline) that had 1-mm markings. The transected end of the distal tendon stump was then photographed (iPhone8 Camera, Apple Inc) perpendicular to a ruler (Sterile Surgical Ruler; Medline) that was positioned at a set distance of 10 cm from a handheld camera. Tendon cross-sectional area was then measured by a trained investigator (Y-JC) using an imaging software program (ImageJ; National Institute of Health).
GT repair
A computerized random number generator (Research Randomizer version 4.0; Geoffrey C. Urbaniak and Scott Plous) was used to assign each GT to a repair technique (n = 14/group). Paired GTs from left and right hind limbs of the same dog were controlled from being placed in the same experimental group. A number (1 to 28) was assigned to each dog and then specific treatments were assigned for repair of the left and right GTs. The specimens were allocated to 4 groups according to the number of strands used in the repair (2, 4, 6, or 8 strands).
All construct repairs were performed by 1 trained investigator (Y-JC) under the direct supervision of a board-certified small animal surgeon (DJD). All repairs were performed with size 2-0 United States Pharmacopeia polypropylene suture (Surgipro; Covidien Ltd) on a swaged 26-mm 1/2 circle V-20 (taper cutting) needle, and the suture placements were equidistant around the tendon circumference. For all repairs, each suture strand was placed as a simple interrupted suture at a standardized depth of 2 mm, with bites taken 5 mm away from the tenotomy site in the proximal and distal directions (Figure 1). Upon completion, equal tension was subjectively assessed and maintained at the proximal and distal site of the tendon and suture material by one investigator (DJD) using mosquito hemostats, and sutures were tied by the other investigator (Y-JC) using a square knot followed by 4 square throws. The ends of the suture were cut 4 mm away from the knot.
Photographic images showing 4 types of repairs performed on cadaveric canine gastrocnemius tendons following tenotomy. There were 56 gastrocnemius musculotendinous units randomly allocated to the 4 repair groups shown. Tenorrhaphies were performed by equidistant placement of 2-0 polypropylene sutures at a depth of 2 mm and a distance of 5 mm from the gastrocnemius tendon transection site and are shown in a loose and unloaded form to aid in pattern replication for illustration purposes only. A—2-strand technique. B—4-strand technique. C—6-strand technique. D—8-strand technique.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.20.11.0199
Biomechanical testing
All specimens were evaluated with a uniaxial MTM (Instron Model 5967; Instron Inc) at room temperature (21 °C). Once the designated repair was complete, the femoral bone segment was securely fixed to a custom testing jig designed by one of the investigators (DJD) by use of a 4-mm-diameter stainless steel bolt that was passed through the previously drilled bone tunnel. The distal aspect of the pes was affixed with a modified fixation clamp (Bone clamp; Sawbones) that was connected to a 500-N load cell affixed to the testing apparatus. Each specimen was vertically aligned (without torsion or tilt), and axial in regard to the direction of MTM load application. A high-speed digital camera (Panasonic Lumix DMC-FZ200; Panasonic Corp) was placed at a measured distance of 20 cm from the sutured specimen to video-record the biomechanical test at a speed of 10 frames/s, with a ruler (marked in millimeters) placed alongside the construct for computed assessment of gap formation after the video recordings were obtained (Figure 2). Following application of 2-N preload, elongation and loading parameters were zeroed to ensure that the starting load was consistent among repairs. Continuous distraction was then applied at a rate of 20 mm/min until the point of construct failure, defined as the point when the tissue or suture failed or the applied load dropped by > 50% during a single test event.
Photograph showing the materials testing machine used to perform biomechanical testing with a gastrocnemius musculotendinous specimen loaded in the custom testing jig. The proximal aspect of the specimen was attached to the device by use of a 4-mm-diameter stainless steel bolt passed through a bone tunnel 1 cm proximal to the trochlear groove of the femur, which was transected 5 cm proximal to the stifle joint. The distal aspect of the specimen (pes) was attached to a modified fixation clamp connected to the load cell. A high-definition video camera can be seen at the forefront of the image; the camera was synchronized with an automated triggering system to allow synonymous evaluation of load and gap formation data. In this image, sutures are placed loosely to improve visibility in the unloaded gastrocnemius tendons repair construct.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.20.11.0199
Construct tensile strength was collected with testing software (Bluehill 3; Instron Inc) that recorded load curves in Newtons and displacement curves in millimeters, and the yield, peak, and failure forces were determined from the curves. Yield force was defined as the first deviation from linearity along the initial flat portion of the slope, peak force was defined as the highest generated force during each test, and failure force was defined as the force at which the sutured construct failed as previously described. Load data were collected by use of a customized software program (Matlab R2018b; Mathworks) that was used to accurately determine the biomechanical variables of interest. Camera data recorded during testing were converted to individual .JPG files and analyzed for development of 1- and 3-mm gaps between transected tendon ends. Gap formation was assessed through review of the video with an imaging software program (ImageJ; National Institute of Health). The exact time points when 1- and 3-mm gaps developed were recorded, and these data were cross-referenced with the load data obtained from the MTM software (Bluehill 3; Instron Inc) to allow the loads at 1- and 3-mm gap formation to be calculated. For constructs in which a 1- or 3-mm gap did not develop, the result was recorded as no gap formation. Failure mode was recorded at the time of testing by 1 investigator (Y-JC).
Statistical analysis
Results of an a priori power analysis indicated ≥ 11 GTs/group would provide ≥ 80% power to detect a mean difference between groups of 25 ± 10 N at a 95% confidence level. The Shapiro-Wilk test was used to assess data for a parametric distribution, and continuous variables were reported as mean ± SD. A mixed linear model was used to control for left and right limbs and dog cadaver. A least-squares means method was conducted for pairwise comparisons, and Bonferroni adjustments were used for multiple comparisons. A Fisher exact test was used to compare proportional distributions in failure mode among experimental groups. All statistical analyses were performed with a commercially available software program (SAS version 9.4; SAS Institute Inc). Values of P < 0.05 were considered significant.
Results
All tendon repairs were successfully performed, with no specimens excluded during dissection, suturing, or biomechanical testing. Tendons from the left and right hind limbs were equally distributed among groups (P = 1.0), with no difference in cross-sectional area (0.01 ± 0.04 cm2) among groups (P = 0.729).
Biomechanical testing
Load data are summarized (Table 1). The yield force (P < 0.001), peak force (P < 0.001), and failure force (P < 0.001) differed significantly among the 4 repair groups, and each force increased significantly (P < 0.05) as the number of strands crossing the repair site increased.
Mean ± SD yield, peak, and failure forces determined during biomechanical testing of 56 gastrocnemius tendons repair constructs created with 2, 4, 6, or 8 strands of 2-0 United States Pharmacopeia polypropylene suture.
| Group | Force (N) | ||
|---|---|---|---|
| Yield | Peak | Failure | |
| 2-strand | 8.26 ± 3.88a | 12.49 ± 3.50a | 12.18 ± 3.83a |
| 4-strand | 21.97 ± 8.47b | 26.35 ± 7.98b | 25.76 ± 8.69b |
| 6-strand | 31.07 ± 0.50c | 38.02 ± 4.81c | 37.88 ± 4.98c |
| 8-strand | 42.60 ± 8.04d | 55.28 ± 8.92d | 54.51 ± 8.58d |
Within a column, different superscript letters denote significant (P < 0.001) differences between experimental groups.
Gap data were tabulated (Table 2). The force required to create a 1-mm gap or a 3-mm gap was significantly (P < 0.001 for both comparisons) different among repair groups, with 8-strand repairs requiring the greatest force to develop these outcomes. There was no difference in the frequency of 1-mm or 3-mm gap development among groups (P = 1.0 and 0.595, respectively).
Mean ± SD force measured at the time of development of 1- and 3-mm gaps between tendon ends and the frequencies of gap development during biomechanical testing for the 56 gastrocnemius tendon repair constructs.
| Group | 1-mm gap | 3-mm gap | ||
|---|---|---|---|---|
| Force (N) | Proportion (%) | Force (N) | Proportion (%) | |
| 2-strand | 4.91 ± 2.07a | 14/14 (100)a | 9.16 ± 1.92a | 13/14 (93)a |
| 4-strand | 12.75 ± .61b | 14/14 (100)a | 19.24 ± 4.98b | 13/14 (93)a |
| 6-strand | 21.46 ± 9.41c | 13/14 (93)a | 34.59 ± 10.94c | 11/14 (79)a |
| 8-strand | 36.08 ± .09d | 14/14 (100)a | 48.83 ± 9.90d | 11/14 (79)a |
See Table 1 for key.
Failure mode
All repair constructs failed exclusively because of suture pull-through (56/56, 100%). There was no difference in mode of failure among repair groups (P = 1.0).
Discussion
In the present study, we assessed the biomechanical effects of increasing the number of suture strands crossing experimentally created tenotomies in an ex vivo model of canine GT repair. Consistent with our hypothesis, increasing the number of suture strands crossing the repair site significantly increased the tensile strength and resistance to gap formation of these constructs.
Despite the fact that previous studies13,25 have demonstrated that the number of suture strands crossing the repair site affects the tensile strength of sutured canine tendon repair constructs, comparisons among studies remain difficult owing to multiple assessed variables that influence the biomechanical properties of the final repair. Dinopoulos et al13 and Thurman et al25 compared the tensile strengths of repairs that had different levels of suture purchase13 and numbers of locking loops13,25 as well as suture strands among groups. Increasing the number of locking loops and increasing the length of suture purchase has been shown to increase the tensile strength of the final sutured construct.16,27 Therefore, differences in tensile strength in previous studies may have been influenced by these other factors. The locking nature of some tenorrhaphy patterns incorporates a greater number of collagen fibrils with locking patterns shown to be superior to nonlocking patterns in prior studies28,29,30 performed with specimens from human or canine cadavers. We recognize that the type of pattern influences the biomechanical properties, gap formation characteristics, and nature and number of contact sites between the suture and apposed tissues. In the study reported here, simple interrupted patterns were chosen specifically for their consistency of placement, which allowed the effect of strand number alone to be assessed without impact from other variables related to suture methods.
The 8-strand suture constructs in our study tolerated forces to yield, peak, and failure that were approximately 5.2, 4.4, and 4.5 times those tolerated by 2-strand suture constructs, respectively. In the human medical literature, increasing the number of suture strands crossing the site of tendon transection is an important surgical consideration that can influence the tensile strength of repaired constructs. Thurman et al25 used human cadaveric digital flexor tendon constructs and demonstrated that 6-strand suture repairs had significantly greater tensile strength (mean, 78.7 N) than 4-strand (mean, 43.0 N) and 2-strand (mean 33.9 N) repair techniques. Winter et al14 used various techniques to repair experimentally transected deep digital flexor tendons in dogs, and assessed the biomechanical properties of the repaired tendons after a 3- or 6-week healing period. Investigators of that study14 showed that repair constructs created with an 8-strand repair technique had greater normalized stiffness values, compared with those repaired by use of modified Savage (4-strand), Tajima (2-strand), and Kessler (2-strand) suture techniques at both postoperative time points. Similarly, Dinopoulos et al13 compared the tensile properties of 4-strand and 8-strand (two 4-strand techniques combined) repairs following experimental transection and 10 days of healing in dogs. In that study,13 the 8-strand technique had a maximum force tolerance that was almost 1.5 times that for an equivalent 4-strand technique. The findings of our study agreed with the results of prior investigations13,14,25 and additionally showed that yield, peak, and failure force increases proportionally when 2, 4, 6, and 8 strands are used for repairs, which to our knowledge has not been previously demonstrated. However, as previously mentioned, prior studies often emphasize a particular repair technique with lack of standardization regarding the level of suture purchase and whether patterns are locking or not. This is of importance, as these variables have been shown to contribute to the holding capacity and interaction of sutures with collagen fibers by improving force distribution throughout repaired constructs.4,13,24,27 The study reported here demonstrated that increasing the number of the strands in a controlled manner affects the tensile strength of tendon repair constructs in the absence of changes in other variables that affect repair site strength.
Gap formation between tendon ends has been shown to decrease the loads tolerated by sutured constructs and to increase the risk of rerupture during periods of rehabilitation, which typically occurs 3 to 6 weeks after surgical intervention.7,31 In the aforementioned study by Dinopoulos et al,13 8-strand repairs sustained greater loads, compared with the results for 4-strand repairs, prior to 1-mm gap formation. Thurman et al25 used a cyclical loading protocol to evaluate 2-, 4- and 6-strand sutured constructs for transected cadaveric human flexor tendons, and found that use of a 2-strand technique resulted in a greater occurrence of gap formation, compared with 4- and 6-strand techniques.25 In agreement with the results of prior studies,13,25 our results showed that increasing the number of strands crossing the tendon repair site increases the force required to result in formation of 1- and 3-mm gaps. The 4-, 6-, and 8-strand repairs required approximately 3, 5, and 7 times the force, respectively, to cause development of a 1-mm gap and approximately 2, 4, and 5 times the force, respectively, to cause development of a 3-mm gap, compared with the forces needed to generate the same degree of gapping for 2-strand repairs. It should be noted that in the study by Dinopoulos et al,13 although there were significant differences in the force needed to create a 1-mm gap for 4- versus 8- strand repairs, no difference was found between the groups in regard to the amount of force required to create a 3-mm gap. In that study,13 gap formation forces continued to be recorded following suture failure, in contrast to the methodology used in the study reported here. In our study, 13 of 14 specimens in the 2- and 4- strand repair groups and 11 of 14 specimens in the 6- and 8- strand repair groups had evidence of 3-mm gap formation prior to suture failure. Differences in results among studies may be explained by differences in suture patterns, suture size, and testing methods. In our study, the sutured constructs were composed of simple interrupted sutures and did not combine loop configurations. Loop configurations have been shown to grasp or lock onto the tendon tissue by interacting with the collagen fibers on deep suture penetration, and this has been shown to confer greater strength to the construct.12,27
Suture size for the present study was deemed clinically appropriate for similarly sized dogs evaluated for tendon injuries at our tertiary referral hospital. In the described experiments, all constructs failed by the mechanism of suture pull-through. In another ex vivo study12 by investigators in our group, the use of larger caliber (size 0 and 2-0 United States Pharmacopeia) core locking loop sutures resulted in repairs that had superior biomechanical properties, compared with those of smaller caliber (3-0 to 5-0) sutures. In that study,12 failure occurred by suture pull-through in the larger-caliber constructs. In contrast, smaller gauge sutures were shown to fail by means of suture material breakage.12,32 Results of the present study showed that the strength of the suture material used was superior to the strength of the interaction between the suture and the parallel-natured collagen fibers. In addition, the sutures were applied symmetrically, distributed around the periphery of the repair site. It should be noted that suture size is an important variable that confers substantial strength to the final repair, and it is often chosen on the basis of the surgeon's preference or prior experience. Suture size has to be balanced with the creation of excessive bulk at areas of suture knotting, with knots known to represent a weak point owing to elongation and unraveling in these locations.33,34,35
The study reported here had some inherent limitations. The ex-vivo nature of our experimental design could not accurately represent clinical scenarios where degenerative tendinopathy or trauma causing tendon laceration may decrease the ability of tissues to be uniformly apposed or hold suture. Damage to the tendinous blood supply caused by increased amounts of suture material is an important clinical consideration. However, it has been shown that 8-strand suture repairs do not interfere with the healing of experimentally transected flexor tendons up to 6 weeks after surgery in dogs.36 In the present study, we used a monotonic single load-to-failure testing method rather than cyclical evaluation, which may more accurately reflect the stresses placed on tendons in vivo.37 Our test methods were purposefully chosen to represent an acute load placed on the repair in the immediate postoperative period in dogs. In addition, glide function was not assessed as a variable of interest. We recognize that increasing the number of strands crossing the repair site may increase the gliding resistance, as an increase in the amount of suture material on the tendon surface may lead to increased interactions between suture and surrounding soft tissues, potentially resulting in peritendinous adhesions.14 We did not use a suture tensioning device to standardize the tension placed on the suture or suture knots during pattern completion. Unbalanced tension distribution caused by a discrepancy in suture tension may affect the biomechanical characteristics of tendon repair constructs, including predisposition to gap formation. However, we attempted to minimize this variation by having 1 trained investigator perform the repairs, with tension subjectively assessed and controlled by a board-certified surgeon during knot tying. Further studies are needed to evaluate the effect of suture strand number on the progression of tendon healing and on tendon blood supply in dogs.
Our results revealed that increasing the number of suture strands used for ex vivo repair of canine GTs significantly increased the tensile strength of the repaired constructs, with yield, peak, and failure forces positively correlated with the number of suture strands. Increasing the number of strands also increased resistance to both 1- and 3-mm gap formation and increased the amount of force needed to cause these gaps.
Acknowledgments
No financial support was received in connection with the study. All surgical suture was provided by Medtronic Inc.
The authors declare that there were no conflicts of interest related to the study.
References
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