• View in gallery
    Figure 1—

    Schematic representation of the palmar surface of a canine cadaveric forelimb with a tenotomy site in the SDFT indicated (red square; A). One tendon repair group comprised a locking-loop (LL) construct (B) that consisted of insertion of an LL core suture pattern (left) with the suture tightened so that the tendon ends were closely apposed without bunching at the tenorrhaphy site (right). Three other tendon repair groups comprised an LL construct and an IHMES (C) with bites placed 5 (left), 10 (middle), and 15 (right) mm from the transection site.

  • View in gallery
    Figure 2—

    Photographs of a mechanical tensile testing apparatus with an SDFT specimen loaded in the custom testing jig (A). Notice the tenorrhaphy site (square). A magnified view of the tenorrhaphy site and a construct consisting of a locking-loop core suture (size-0 polypropylene) and an IHMES (3–0 polypropylene) with suture bites placed 5 mm from the transection site (inset; B). The scale on the right side is in centimeters.

  • View in gallery
    Figure 3—

    Box-and-whisker plots for yield force of tenorrhaphies repaired with a core locking-loop suture pattern (LL construct) or an LL construct and an IHMES with suture bites placed 5 (LL + 5ES construct), 10 (LL + I0ES construct), and 15 (LL + I5ES construct) mm from the tenotomy site (18 specimens/group). Use of IHMES patterns significantly (P < 0.00I) increased overall construct strength, compared with that for the LL construct. Boxes represent the interquartile (25th to 75th percentile) range, the horizontal line in each box represents the median, whiskers represent the maximum and minimum values, and circles represent outliers.

  • 1. Frank CB. Chapter 11: form and function of tendon and ligament. In: O'Keefe RJ, Jacobs JJ, Chu CR, et al, eds. Orthopaedic basic science: foundations of clinical practice. 4th ed. Rosemont, Ill: Lippincott Williams & Wilkins, 2018;191223.

    • Search Google Scholar
    • Export Citation
  • 2. Gelberman RH, Boyer MI, Brodt MD, et al. The effect of gap formation at the repair site on the strength and excursion of intrasynovial flexor tendons. An experimental study on the early stages of tendon-healing in dogs. J Bone Joint Surg Am 1999;81:975982.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Dy CJ, Hernandez-Soria A, Ma Y, et al. Complications after flexor tendon repair: a systematic review and meta-analysis. J Hand Surg Am 2012;37:543551.

  • 4. Wieskötter B, Herbort M, Langer M, et al. The impact of different peripheral suture techniques on the biomechanical stability in flexor tendon repair. Arch Orthop Trauma Surg 2018;138:139145.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5. Lister GD, Kleinert HE, Kutz JE, et al. Primary flexor tendon repair followed by immediate controlled mobilization. J Hand Surg Am 1977;2:441451.

  • 6. Wade PJ, Muir IF, Hutcheon LL. Primary flexor tendon repair: the mechanical limitations of the modified Kessler technique. J Hand Surg Br 1986;11:7176.

  • 7. Silfverskiöld KL, May EJ. Flexor tendon repair in zone II with a new suture technique and an early mobilization program combining passive and active flexion. J Hand Surg Am 1994;19:5360.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Silfverskiöld KL, May EJ. Gap formation after flexor tendon repair in zone II. Results with a new controlled motion programme. Scand J Plast Reconstr Surg Hand Surg 1993;27:263268.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9. Lin GT, An KN, Amadio PC, et al. Biomechanical studies of running suture for flexor tendon repair in dogs. J Hand Surg Am 1988;13:553558.

  • 10. Lotz JC, Hariharan JS, Diao E. Analytic model to predict the strength of tendon repairs. J Orthop Res 1998;16:399405.

  • 11. Pruitt DL, Manske PR, Fink B. Cyclic stress analysis of flexor tendon repair. J Hand Surg Am 1991;16:701707.

  • 12. Chang MK, Wong YR, Tay SC. Biomechanical comparison of modified Lim/Tsai tendon repairs with intra− and extratendinous knots. J Hand Surg Eur Vol 2018;43:919924.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13. Strickland JW. Development of flexor tendon surgery: twenty-five years of progress. J Hand Surg Am 2000;25:214235.

  • 14. Diao E, Hariharan JS, Soejima O, et al. Effect of peripheral suture depth on strength of tendon repairs. J Hand Surg Am 1996;21:234239.

  • 15. Galvez MG, Comer GC, Chattopadhyay A, et al. Gliding resistance after epitendinous-first repair of flexor digitorum profundus in zone II. J Hand Surg Am 2017;42:662.e1–662.e9.

    • Search Google Scholar
    • Export Citation
  • 16. Fufa DT, Osei DA, Calfee RP, et al. The effect of core and epitendinous suture modifications on repair of intrasynovial flexor tendons in an in vivo canine model. J Hand Surg Am 2012;37:25262531.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Merrell GA, Wolfe SW, Kacena WJ, et al. The effect of increased peripheral suture purchase on the strength of flexor tendon repairs. J Hand Surg Am 2003;28:464468.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18. Dona E, Turner AWL, Gianoutsos MP, et al. Biomechanical properties of four circumferential flexor tendon suture techniques. J Hand Surg Am 2003;28:824831.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19. Silfverskiöld KL, Andersson CH. Two new methods of tendon repair: an in vitro evaluation of tensile strength and gap formation. J Hand Surg Am 1993;18:5865.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Barrie KA, Tomak SL, Cholewicki J, et al. Effect of suture locking and suture caliber on fatigue strength of flexor tendon repairs. J Hand Surg Am 2001;26:340346.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21. Gil-Santos L, Monleón-Pradas M, Gomar-Sancho F, et al. Positioning of the cross-stitch on the modified Kessler core tendon suture. J Mech Behav Biomed Mater 2018;80:2732.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22. Hirpara KM, Sullivan PJ, Raheem O, et al. A biomechanical analysis of multistrand repairs with the Silfverskiöld peripheral cross-stitch. J Bone Joint Surg Br 2007;89:13961401.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23. Moores AP, Owen MR, Tarlton JF. The three-loop pulley suture versus two locking-loop sutures for the repair of canine Achilles tendons. Vet Surg 2004;33:131137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24. Guzzini M, Lanzetti RM, Proietti L, et al. Interlocking horizontal mattress suture versus Kakiuchi technique in repair of Achilles tendon rupture: a biomechanical study. J Orthop Traumatol 2017;18:251257.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25. Johnson J, Austin C, Breur G. Incidence of canine appendicular musculoskeletal disorders in 16 veterinary teaching hospitals from 1980 through 1989. Vet Comp Orthop Traumatol 1994;7:5669.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Meeson RL, Davidson C, Arthurs GI. Soft-tissue injuries associated with cast application for distal limb orthopaedic conditions: a retrospective study of sixty dogs and cats. Vet Comp Orthop Traumatol 2011;24:126131.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27. Gall TT, Santoni BG, Egger EL, et al. In vitro biomechanical comparison of polypropylene mesh, modified three-loop pulley suture pattern, and a combination for repair of distal canine Achilles' tendon injuries. Vet Surg 2009;38:845851.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Duffy DJ, Main RP, Moore GE, et al. Ex vivo biomechanical comparison of barbed suture and standard polypropylene suture for acute tendon laceration in a canine model. Vet Comp Orthop Traumatol 2015;28:263269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Kamal RN, Yao J. Evidence-based medicine: surgical management of flexor tendon lacerations. Plast Reconstr Surg 2017;140:130e139e.

Advertisement

Effect of bite distance of an epitendinous suture from the repair site on the tensile strength of canine tendon constructs

Daniel J. Duffy1Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27607

Search for other papers by Daniel J. Duffy in
Current site
Google Scholar
PubMed
Close
 BVM&s, MS
,
Christina J. Cocca2Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802

Search for other papers by Christina J. Cocca in
Current site
Google Scholar
PubMed
Close
 DVM
,
Mariana E. Kersh3Department of Mechanical Science and Engineering, College of Engineering, University of Illinois, Urbana, IL 61801

Search for other papers by Mariana E. Kersh in
Current site
Google Scholar
PubMed
Close
 PhD
,
Woojae Kim3Department of Mechanical Science and Engineering, College of Engineering, University of Illinois, Urbana, IL 61801

Search for other papers by Woojae Kim in
Current site
Google Scholar
PubMed
Close
 MS
, and
George E. Moore4Veterinary Administration, College of Veterinary Medicine, Purdue University, West Lafayette, IN 47906

Search for other papers by George E. Moore in
Current site
Google Scholar
PubMed
Close
 DVM, PhD

Abstract

OBJECTIVE

To evaluate effects of bite distance of an interlocking horizontal mattress epitendinous suture (IHMES) from the repair site on tensile strength of canine tendon repairs.

SAMPLE

72 canine cadaveric superficial digital flexor tendons (SDFTs).

PROCEDURES

Transverse tenotomy was performed, and SDFTs were repaired with a locking-loop construct (LL construct) or 3 LL constructs with IHMES suture bites placed 5 (LL + 5ES construct), 10 (LL + 10ES construct), or 15 (LL + 15ES construct) mm from the transection site (18 SDFTs/group). Constructs were loaded to failure. Load at 1− and 3-mm gapping, yield force, failure load, and failure mode were evaluated.

RESULTS

Mean ± SD yield force and failure load for LL constructs were significantly lower than for IHMES constructs. Load at 1− and 3-mm gapping was significantly higher for IHMES constructs. Increasing the bite distance significantly increased construct strength (134.4 ± 26.1 N, 151.0 ± 16.8 N, and 182.1 ± 23.6 N for LL + 5ES, LL + 10ES, and LL + 15ES constructs, respectively), compared with strength for the LL construct. Failure mode differed significantly among constructs when an IHMES was used.

CONCLUSIONS AND CLINICAL RELEVANCE

Addition of an IHMES to an LL construct led to increased ultimate tensile strength by 2.5 times and significantly reduced gap formation. Increasing the IHMES bite distance increased yield force by 2.1, 2.3, and 2.7 times for bites placed 5, 10, and 15 mm from the tenotomy, respectively. Positioning an IHMES at a greater distance from the repair site provided superior biomechanical strength for tendon repairs in dogs.

Abstract

OBJECTIVE

To evaluate effects of bite distance of an interlocking horizontal mattress epitendinous suture (IHMES) from the repair site on tensile strength of canine tendon repairs.

SAMPLE

72 canine cadaveric superficial digital flexor tendons (SDFTs).

PROCEDURES

Transverse tenotomy was performed, and SDFTs were repaired with a locking-loop construct (LL construct) or 3 LL constructs with IHMES suture bites placed 5 (LL + 5ES construct), 10 (LL + 10ES construct), or 15 (LL + 15ES construct) mm from the transection site (18 SDFTs/group). Constructs were loaded to failure. Load at 1− and 3-mm gapping, yield force, failure load, and failure mode were evaluated.

RESULTS

Mean ± SD yield force and failure load for LL constructs were significantly lower than for IHMES constructs. Load at 1− and 3-mm gapping was significantly higher for IHMES constructs. Increasing the bite distance significantly increased construct strength (134.4 ± 26.1 N, 151.0 ± 16.8 N, and 182.1 ± 23.6 N for LL + 5ES, LL + 10ES, and LL + 15ES constructs, respectively), compared with strength for the LL construct. Failure mode differed significantly among constructs when an IHMES was used.

CONCLUSIONS AND CLINICAL RELEVANCE

Addition of an IHMES to an LL construct led to increased ultimate tensile strength by 2.5 times and significantly reduced gap formation. Increasing the IHMES bite distance increased yield force by 2.1, 2.3, and 2.7 times for bites placed 5, 10, and 15 mm from the tenotomy, respectively. Positioning an IHMES at a greater distance from the repair site provided superior biomechanical strength for tendon repairs in dogs.

Tendons are arranged in a hierarchical and highly organized manner starting with the triple tropocollagen helix that is progressively arranged into microfibrils, fibrils, fascicles, and ultimately a tendon.1 This orchestrated assembly and cross-linking of collagen into microfibrils is critical for the mechanical strength of tendons. Tendons serve the primary purpose of allowing transmission of muscle-derived force to bone, which provides the capacity for voluntary locomotion.1 This is achieved while concurrently providing dynamic joint stability in concert with ligamentous structures, which results in secondary static restraint to joint translation. Surgical methods used for tendon repair are crucial for realignment of collagen fibrils and healing after acute transection.2,3

Circumferential peripheral sutures, also called epitendinous sutures, are commonly used in conjunction with core suture patterns in the repair of human zone II flexor tendon injuries following rupture or laceration.4–9 However, use of epitendinous sutures in veterinary surgical patients has not been reported and is poorly described. Regardless of disease pathogenesis or the inciting cause of injury, epitendinous sutures allow superior apposition of tendon ends while preventing fraying and reducing exposure of suture material on the tendinous surface.4,5 Epitendinous sutures improve glide function and decrease formation of peritendinous adhesions while substantially increasing overall construct strength and decreasing the occurrence of gap formation between transected ends.10,11 Other important factors that affect healing at tenorrhaphy sites are gap formation and blood supply to the tendon.2

Biomechanical characteristics of peripheral suture techniques with and without the addition of a core suture have been described.4,9,12–19 Many epitendinous patterns (eg, simple-running continuous,5 simple locking,4 Halstead mattress,6 Lembert mattress,5 Lin locking,9 and Silfverskiöld cross-stitch10,11,19) have been described and used successfully in clinical patients. The simple-running continuous and IHMES techniques are the patterns most commonly used in human patients in conjunction with a core suture repair.3,13

Epitendinous sutures are the weakest component of a construct for a repaired tendon.4 Failure is initiated after partial anastomotic separation at the tenorrhaphy site, which is followed by progressive gap formation and ultimately failure.20 Gap formation leads to the deposition of disorganized scar tissue with low strain tolerance; this prevents a progressive increase in tensile strength and stiffness, which renders repairs susceptible to rerupture in the early postoperative period.2 Uneven load distribution and stress concentration placed on suture material used for tenorrhaphy is the initiating step in development of gap formation with progression to eventual failure.4,10,20 In a previous study10 conducted to predict the strength of tendon repairs, epitendinous sutures bore 64% to 77% of the load applied to the construct. Because epitendinous sutures are susceptible to failure, more attention should be given to improve this aspect of the suture tenorrhaphy and construct design. Clinically, placement of sutures in the epitenon increases repair strength by 10% to 50% over use of core sutures alone15 and decreases the need for subsequent surgeries because of failure of primary core repairs by 84%.3 In a recent study21 that involved use of mathematical modeling, it was found that sutures would support greater loads when the distance of core suture bites from the transection site was increased. However, to the authors’ knowledge, the effect of placement of epitendinous suture bites in relation to the repair site has not been evaluated. Understanding the configurations for epitendinous sutures and improving load sharing will likely lead to improvements in the quality of repairs and decrease the occurrence of gap formation, which will translate into progressive healing and increased repair strength in vivo. Thus, biomechanical assessment of epitendinous suture techniques that will provide sufficient strength to allow successful tendon union and healing after repair are warranted.

The objective of the study reported here was to evaluate effects of the placement of suture bites for an IHMES in relation to a tendon transection site on the biomechanical stability of flexor tendon repairs. We hypothesized that tendons repaired with a core locking-loop in addition to suture an IHMES would be more resistant to gap formation and achieve higher loads until failure, compared with results for a locking-loop suture alone. We also hypothesized that increasing bite distance for the IHMES from the transection site would increase construct strength and reduce gap formation.

Materials and Methods

Sample

Cadavers of 36 medium− to large-breed skeletally mature dogs were obtained from an animal shelter immediately after the dogs had been euthanized for reasons unrelated to the study reported here. Dogs did not have evidence of soft tissue or musculoskeletal disease and weighed between 25 and 40 kg; sex as well as health status before euthanasia were not recorded. Tendons were rejected when there were visual abnormalities or defects affecting bones, tendons, or the musculotendinous unit.

Preliminary experiments were performed to determine methods for tendon acquisition, cryopreservation, transection, suture placement, and biomechanical evaluation of test constructs and to allow calculations of a power analysis. The resultant protocol was standardized and subsequently used in the study reported here. The protocol for collection and handling of cadaveric specimens was approved by the Animal Care and Use Committee of the Department of Veterinary Clinical Sciences at the University of Illinois (protocol No. 17017).

Paired forelimbs were obtained from each cadaver. For each limb, the SDFT was manually dissected, and all palmar retinacular attachments were carefully removed. The origin of the SDFT on the medial aspect of the humeral condyle, musculotendinous unit, and insertion of the SDFT on the manus were isolated, and all other antebrachial tissues were removed and discarded. Metacarpal bones were transversely severed with a band sawa at a location 5 mm distal to the carpometacarpal joint. All tissues on the manus distal to this point were left intact. The distal aspect of the humerus was transected by use of the same band saw at a location 50 mm proximal to the supratrochlear foramen, which yielded a test specimen consisting of the distal aspect of the humerus, musculotendinous unit, and tendinous insertion on the phalan of the manus. Specimens were kept moist by application of saline (0.9% NaCl) solution during tendon acquisition. Specimens then were wrapped in gauze soaked in saline solution and stored at −20°C as described elsewhere.22

Tenotomy

Specimens were thawed at room temperature (21°C) for 10 to 12 hours before they were used in experiments. A standardized tenotomy was made in a transverse plane with a No. 10 scalpel blade. Specimens were placed on a durable surface to facilitate perpendicular transection across the tissue. Transection was performed at a location 20 mm distal to the level of the musculotendinous junction, as measured with a calibrated ruler (Figure 1). After tenotomy was performed, the distal cut surface of the tendon was photographedb beside a calibrated ruler; the photograph was obtained at a distance of 100 mm and parallel to the cut surface of the tendon. Cross-sectional area of each tendon was measured by 1 investigator (CJC) by use of an imaging software program.c Each tendon was measured 4 separate times, and the mean cross-sectional area was calculated. Specimens were kept moist by application of saline solution during tenotomy, tendon repair, and mechanical testing.

Figure 1—
Figure 1—

Schematic representation of the palmar surface of a canine cadaveric forelimb with a tenotomy site in the SDFT indicated (red square; A). One tendon repair group comprised a locking-loop (LL) construct (B) that consisted of insertion of an LL core suture pattern (left) with the suture tightened so that the tendon ends were closely apposed without bunching at the tenorrhaphy site (right). Three other tendon repair groups comprised an LL construct and an IHMES (C) with bites placed 5 (left), 10 (middle), and 15 (right) mm from the transection site.

Citation: American Journal of Veterinary Research 80, 11; 10.2460/ajvr.80.11.1034

Tendon repair

Tendons were randomly allocated by use of a random number generatord into 4 repair groups (18 specimens/group). All core locking-loop repairs involved use of size-0 polypropylene suture,e whereas all IHMES repairs were performed with 3–0 polypropylene suture.e These sutures were chosen on the basis of sutures used in clinical situations for tendons of similar size. Each suture package was sterile, within the manufacturer's expiration date, and opened immediately before use. A new suture strand was used for each tendon repair. A board-certified veterinary surgeon (DJD), with experience with tendinous repair in both clinical and research settings, performed all surgical tenorrhaphies. Testing was completed in a single session and results recorded.

Specimens of group 1 were repaired with a core locking-loop technique alone (LL construct), as described elsewhere23 (Figure 1). A straight needle was used for suture passage. Suture was tightened so that the tendon ends were closely apposed without bunching at the tenorrhaphy site before knot tying. Suture was tied with a square knot followed by 3 throws; suture was cut 3 mm from the knot.

Specimens of group 2 were repaired by use of a core locking-loop technique with the addition of an IHMES pattern, as described elsewhere,24 with bites placed 5 mm from the tenotomy of each tendon segment (LL + 5ES construct; Figure 1). The core LL suture was completed as described for the LL construct. The IHMES pattern then was placed, which consisted of a running horizontal mattress suture beginning at the proximal end of the tendon. Suture bites were placed parallel 2 mm apart and 5 mm from the transected end of the tendon, as determined by use of a calibrated ruler. Tendons were positioned on a hard surface for repair to ensure precise and consistent suture placement. Each suture pass incorporated each new bite into the preceding suture to effectively lock each throw. This created a locking configuration that continued around the circumference of the tendon. Suture bites were placed with a straight needle to aid in accurate suture placement. A single square knot followed by 3 throws was used at the end of the suture line; suture was cut 3 mm from the knot.

Specimens of group 3 were repaired as described for the LL + 5ES construct, except the bites for the IHMES pattern were placed 10 mm from the tenotomy (LL + 10ES construct; Figure 1). Knots were tied and cut as described for the LL + 5ES construct.

Specimens of group 4 were repaired as described for the LL + 5ES construct, except the bites for the IHMES pattern were placed 15 mm from the tenotomy (LL + 15ES construct; Figure 1). Knots were tied and cut as described for the LL + 5ES construct.

Mechanical testing

Testing was performed at room temperature by use of a uniaxial materials testing machine.f Each manus was secured with a specifically designed bone clampg rigidly mounted to a vise. A custom testing jig was created to secure the humeral bone segment by use of a 3.5-mm-diameter bolt placed transversely through the supracondylar foramen. A calibrated scale was axially aligned during testing to allow computed analysis of gap formation. Each test was filmed at 50 frames/s with a high-speed digital camerah placed at a distance of 25 cm from the construct and aligned with the tenorrhaphy site (Figure 2).

Figure 2—
Figure 2—

Photographs of a mechanical tensile testing apparatus with an SDFT specimen loaded in the custom testing jig (A). Notice the tenorrhaphy site (square). A magnified view of the tenorrhaphy site and a construct consisting of a locking-loop core suture (size-0 polypropylene) and an IHMES (3–0 polypropylene) with suture bites placed 5 mm from the transection site (inset; B). The scale on the right side is in centimeters.

Citation: American Journal of Veterinary Research 80, 11; 10.2460/ajvr.80.11.1034

A preload of 2 N was applied to establish a consistent resting length. Constructs were then distracted at a rate of 20 mm/min until catastrophic failure. Load and displacement data were collected by the test system softwarei at a frequency of 100 Hz. Yield force was defined as the point at which there was nonlinear deformation of the construct, as determined by evaluation of the load displacement curve. Peak force was defined as the maximum force measured during each test. Failure force was defined as the load at which the suture broke or pulled through the tendinous tissue. Failure modes for the suture or tendinous tissue were visually determined by 1 investigator (DJD) at the time of testing and during review of videographic data.

Acquired data for time, load, and displacement were subsequently entered in a commercially available spreadsheet program.j Videographic data from each construct test were then analyzed by use of an imaging software program.c Data were evaluated by 1 investigator (DJD); a calibrated ruler was used for precise quantification of gap formation, and visual evaluation was used to determine failure modes.

Gap formation was identified by progressive separation of tendon ends and measured at the smallest distance between cut surfaces at the repair site. When there was gap formation between tendon ends, the distance was measured 4 times, and the mean value was calculated. Videographic data were then cross-referenced with load displacement data to determine loads at which there was a 1-mm gap and a 3-mm gap. Mean of the 4 load measurements was used to determine the force required to cause the respective gap formation. Finally, yield, peak, and failure forces were identified visually by examination of a plot of load displacement data obtained from the tensile testing system.

Statistical analysis

On the basis of loads at failure obtained in another study9 and results of the preliminary experiments we conducted, sample size calculation determined that 16 tendons/repair group would provide ≥ 90% power (with 95% confidence) to detect a mean ± SD difference of 30 ± 15 N between repair groups. Each repair group included 2 additional tendons to account for possible errors or rejection of tendinous constructs during testing.

Data were assessed for a parametric distribution by use of the Shapiro-Wilk test for normality. Continuous variables were normally distributed and described as mean ± SD. Differences among means of repair groups were assessed with a mixed linear model. Pairwise comparisons of least squares means were conducted with a Bonferroni adjustment for multiple comparisons. Proportional distributions for mode of failure were compared among repair groups by use of the Pearson χ2 test of association. All analyses were performed with commercially available software.k All applicable test assumptions were met. Values of P < 0.05 were considered significant.

Results

All specimens were successfully transected, sutured, and biomechanically tested without procedural errors. No specimens were rejected at the time of testing, and data for all tendons were included in the analysis. There was not a significant (P = 0.721) difference in the number of left and right limbs among repair groups. Mean ± SD cross-sectional area of all tendons was 0.28 ± 0.03 cm2; there was not a significant (P = 0.201) difference in cross-sectional area among repair groups or between contralateral limbs.

Force data

Yield force differed significantly (P < 0.001) among repair groups. Mean ± SD yield force for the core LL construct was 61.3 ± 19.0 N, which was significantly (P < 0.001) less than for the IHMES groups (LL + 5ES construct, 129.0 ± 26.8 N; LL + 10ES construct, 140.0 ± 16.1 N; and LL + 15ES construct, 167.9 ± 24.1 N). Evaluation of the effect of distance of IHMES bite placement from the tenotomy revealed a significant (P < 0.001) difference between the LL + 5ES and LL + 15ES constructs and between the LL + 10ES and LL + 15ES constructs, but there was not a significant (P = 0.108) difference between the LL + 5ES and LL + 10ES constructs. Overall, results indicated that as distance of the IHMES placement increased from the site of tendinous transection, yield force increased (Figure 3).

Figure 3—
Figure 3—

Box-and-whisker plots for yield force of tenorrhaphies repaired with a core locking-loop suture pattern (LL construct) or an LL construct and an IHMES with suture bites placed 5 (LL + 5ES construct), 10 (LL + I0ES construct), and 15 (LL + I5ES construct) mm from the tenotomy site (18 specimens/group). Use of IHMES patterns significantly (P < 0.00I) increased overall construct strength, compared with that for the LL construct. Boxes represent the interquartile (25th to 75th percentile) range, the horizontal line in each box represents the median, whiskers represent the maximum and minimum values, and circles represent outliers.

Citation: American Journal of Veterinary Research 80, 11; 10.2460/ajvr.80.11.1034

Mean ± SD peak load was significantly (P < 0.001) higher for the IHMES groups (LL + 5ES construct, 134.4 ± 26.1 N; LL + 10ES construct, 151.0 ± 16.8 N; and LL + 15ES construct, 182.1 ± 23.6 N), compared with peak load for the core LL construct (72.5 ± 6.8 N). Evaluation of the effect of distance of the IHMES bite placement from the repair site revealed a significant (P < 0.001) difference between the LL + 5ES and LL + 15ES constructs and between the LL + 10ES and LL + 15ES constructs, but there was not a significant (P = 0.105) difference between the LL + 5ES and LL + 10ES constructs. This pattern was similar to the pattern for failure load. The IHMES groups failed at significantly (P < 0.001) higher loads (LL + 5ES construct, 134.4 ± 26.1 N; LL + 10ES construct, 151.0 ± 16.8 N; and LL + 15ES construct, 182.1 ± 23.6 N), compared with the load at failure for the core LL construct (72.5 ± 6.8 N). Evaluation of the effect of distance of the IHMES bite placement from the repair site revealed a significant (P < 0.001) difference between the LL + 5ES and LL + 15ES constructs and between the LL + 10ES and LL + 15ES constructs, but there was not a significant (P = 0.105) difference between the LL + 5ES and LL + 10ES constructs.

Gap formation

Load required to create a 1-mm gap at the tenorrhaphy site differed significantly (P < 0.001) among repair groups. Mean ± SD load to create a 1-mm gap for constructs with an IHMES was significantly (P < 0.001) higher (LL + 5ES construct, 106.7 ± 53.6 N; LL + 10ES construct, 142.2 ± 15.8 N; and LL + 15ES construct, 143.6 ± 30.5 N), compared with the load required to create a 1-mm gap for the core LL construct (53.3 ± 15.0 N). Evaluation of the effect of distance of IHMES bite placement revealed no significant (P = 0.307) differences among repair groups. However, the proportion of tendons for which the gap was < 1 mm at failure was significantly (P = 0.004) lower for the IHMES groups than for the core LL construct, with 3 of 18 LL + 5ES constructs and 6 of 18 LL + 15ES constructs having a complete lack of gap formation before ultimate failure.

Similarly, the mean ± SD load required to create a 3-mm gap was significantly (P < 0.001) higher for the IHMES groups (LL + 5ES construct, 128.0 ± 23.6 N; LL + 10ES construct, 0 ± 0 N; and LL + 15ES construct, 137.0 ± 0 N), compared with the load for the core LL construct (53.4 ± 24.2 N). The proportion of tendons for which the gap was < 3 mm at failure was significantly (P < 0.001) lower for the IHMES groups (LL + 5ES, 2/18; LL + 10ES construct, 0/18; and LL + 15ES construct, 1/18), compared with the proportion for the core LL construct (16/18).

Failure mode

Mechanisms of construct failure included suture breakage, suture pull-through of the tendinous structure, or a combination of both methods of failure affecting the core and epitendinous sutures. Mechanisms of suture failure differed significantly (P < 0.001) among repair groups, with breakage of both the core and epitendinous sutures being the most frequent mode of failure among the IHMES groups (LL + 5ES construct, 18/18 tendons; LL + 10ES construct, 16/18 tendons; and LL + 15ES construct, 14/18 tendons). In contrast, the principal mechanism of failure for the core LL construct was suture pull-through (14/18 tendons).

Discussion

In support of the hypothesis for the study reported here, results indicated that the addition of an IHMES to a core LL construct resulted in a stronger construct that tolerated significantly greater yield, peak, and failure loads. Gap formation was significantly reduced in constructs for which an IHMES was applied. For the epitendinous repairs, increasing the distance of IHMES bite placement from the tenotomy significantly increased construct strength and decreased the occurrence of gap formation. Results also indicated that the IHMES constructs failed primarily by suture breakage, whereas the majority (14/18 tendons) of failures for the core LL construct was by suture pull-through.

The study reported here was conducted to investigate biomechanical properties of a single epitendinous suture technique with placement of suture bites at various distances from the transection site. To our knowledge, there have been no studies published in the veterinary literature on tensile testing of epitendinous sutures added to a core LL construct. Therefore, comparability of results for the present study with those of other published veterinary studies on tendon repair is impeded by variation of testing methods, suture patterns, suture techniques, materials used for tenorrhaphy, suture sizes, and number of suture strands crossing the repair site. Addition of an IHMES led to a mean increase in ultimate tensile strength by 2.5 times, compared with tensile strength for the LL construct. Results of the present study agree with those in the human literature, whereby the addition of epitendinous suture to core patterns provides an increase in construct strength and stiffness of up to 50%.6,8,9,19 Use of epitendinous sutures for distal extremity tendon repair has resulted in significant increases in ultimate tensile strength and reduced gap formation between transected tendon ends.9 Regardless of whether a core suture was used, the addition of peripheral circumferential sutures increased ultimate tensile strength by a mean of 38% and resistance to gap formation by a mean of 165% in 1 study.11 Extrapolating this information to a clinical setting for acute tendon laceration in dogs,25 we postulate that use of epitendinous suture for routine tendinoplasty may decrease occurrence of gap formation and repair failures. These findings may also translate to decreased reliance on adjuvant techniques (eg, application of a cast), which can be associated with a high rate of soft tissue injury in canine patients.26 However, findings for the present study should be interpreted with caution until additional in vivo investigations are performed.

Epitendinous sutures decrease tendon cross-sectional area, decrease fraying at an anastomosis, and allow uniform apposition along the length of a tendinous transection, compared with traditional patterns such as the 3-loop pulley, which can often bunch and distort a surgical repair site.4,5,23,27 Increased tendon bulk can otherwise predispose flexor tendon repairs to adhesion formation and diminish the ability of sheathed tendons to glide. Although the 3-loop pulley is biomechanically superior in tensile testing of canine tendons,27,28 we specifically chose the locking loop for our core pattern in the interest of accurate apposition and alignment of the cut tendinous surfaces. Accurate alignment of tendon ends improves intrinsic healing by increasing construct strength by up to 22%.24 This allows fibroblast migration to the tendinous core and allows for initiation and propagation of intrinsic healing.29 In the present study, we positioned the knot of the LL construct away from the tendon cut surface because extratendinous knotting is stronger and has superior biomechanical performance, with greater tolerance to knot overtensioning.13

For the IHMES groups, increasing the distance of the suture bite from the repair site led to successive increases in yield force by 2.1, 2.3, and 2.7 times for bites placed 5, 10, and 15 mm from the tenotomy site, respectively, compared with results for the core LL construct. These results are in accordance with results of a study4 in which investigators found that increasing the distance of a peripheral circumferential suture from a tenotomy led to a significant increase in construct strength. Increases in biomechanical strength of the repaired tendon construct as a result of positioning suture bites at a greater distance from the transection site in the present study also agrees with results of another study21 in relation to cross-stitch placement of a modified Kessler core tendon suture. Despite the fact there was an increase in construct strength, longer strands of suture associated with an increase in the distance of an epitendinous suture bite from a tenotomy may be deemed an undesirable quality. Extraneous suture on the tendon surface may catch or impede soft tissues and have a negative impact on glide function and potential loss of stiffness caused by elongation of the suture material as loads are applied. Some repair techniques involve placing most of the sutures within the tendon substance, which may negate suture material exposure on the tendon surface.26 In another study,27 sutures placed closer to the repair site had higher stiffness. However, these sutures also cut through the tendinous tissue sooner, which led to decreased yield force, development of gap formation, and failure at lower load applications. As bite distance increases, greater lengths of suture cross the repair site, thus increasing elasticity of the repaired construct. This linear stretching modulus may compensate for, and more evenly distribute, tension acting on the repair site, which allows a greater degree of load sharing between the suture and collagen bundles. Epitendinous suture strands combined with core sutures placed at a similar distance from the transection site have load imbalance when axial loading is applied to the musculotendinous unit.21 The circumferential design of epitendinous sutures cause the core suture to directly absorb lower loads, as does the peripheral suture component, and transfers some of the applied force from the core to the peripheral suture around the circumference of the repair, thus leading to lower stress concentration at a single suture-tendon interface. The effect of positioning IHMES bites at a greater distance from the repair site is in accordance with results of a study21 on the effect of cross-stitch placement on repaired human flexor tendons.

Epitendinous repairs typically fail by suture pull-through or breakage of the suture.16,17,24 In the present study, the predominant failure mode differed between the LL construct and IHMES constructs. Suture breakage of both core and epitendinous sutures occurred in 18 of 18, 16 of 18, and 14 of 18 IHMES repairs placed at 5, 10, and 15 mm from the tenotomy, respectively. These findings agree with results of previous studies18,19,24 conducted with a variety of epitendinous suture patterns. In the study reported here, these findings may be explained on the basis of suture size and differences in tension distribution among repairs. Core locking-loop sutures contain fewer strands that traverse the tenotomy, which results in stress concentration at the tendon-suture interface and leads to subsequent pull-through. In contrast, epitendinous sutures are placed around the periphery of the repair in a circumferential manner that incorporates a larger number of collagen bundles and allows load distribution over a larger surface area, leading to even tension distribution within the tendon substance. The locking nature of the IHMES pattern allows incorporation of a greater number of collagen fibrils and load distribution between the tendon and suture. This pattern is superior to nonlocking patterns in bovine tendons.24 Another factor that influences the mechanism of failure is suture size. As suture size increases, the weakest part of the repair becomes the suture-tendon interface, and pull-through becomes more likely. Additional studies are needed to elucidate the most appropriate suture size to resist failure while not adversely affecting tendon blood supply, size of the repair site, or glide function.

The aim of surgical treatment of acute tendon rupture or laceration is to achieve maximal mechanical stability of the sutured construct, which is crucial to decrease the rate of postoperative gap formation and rerupture at the tenorrhaphy site. Repairs with an IHMES had significantly less gap formation, compared with results for tendinous transection repaired with only a core LL construct. Gap formation in repairs have been associated with a decrease in ultimate force, repair-site rigidity, strength, and stiffness necessary for a functional outcome.2 Until there is substantial accrual of repair site strength between 10 and 42 days after surgery,2 reliance is placed solely on the suture during that time. A strong primary epitendinous and core repair is important in human patients because rehabilitation is often implemented soon after surgery to treat injuries affecting the distal aspect of the extremities.3,15 Results of the present study supported the use of an epitendinous suture to substantially reduce the incidence of gap formation, which may translate to more rapid healing and less deposition of mechanically inferior scar tissue at the repair site and a predisposition to repair failure. Thus, the type of suture and pattern used can affect the clinical outcome and influence the recommended postoperative rehabilitation protocol.

The study reported here had limitations. Apparently healthy tendons that were sharply transected were used, which would differ from those in clinical settings, where chronic degenerative changes often lead to fraying and decreased suture-holding capacity. In the present study, we intended to determine load to failure by simulating clinical failure, in which tendon rerupture occurs in the early postoperative period after surgical intervention. For the purpose of this biomechanical analysis, we used axial distraction to failure without evaluation of cyclic loading, which likely recreated forces to which clinical patients are subjected during the postoperative period.11 The study design was intentionally similar to those of other investigators,12,23,27 whereby cyclic testing was not performed so that we could draw meaningful conclusions in outcome measures between studies.

Results of the study reported here indicated that the in vitro behavior of sutured tendons differed for an IHMES in addition to a core suture repair. Addition of an IHMES led to a mean increase in ultimate tensile strength by 2.5 times, compared with that for the LL construct, and significantly reduced the incidence of gap formation between tendon ends. Within IHMES constructs, increasing the bite distance from the tenotomy increased yield forces by 2.1, 2.3, and 2.7 times for bites placed 5, 10, and 15 mm from the tenotomy, respectively. Positioning an IHMES at a greater distance from the repair site offered increased biomechanical strength to tendon repairs. Techniques should be investigated in vivo to address effects on tendon healing and blood supply before they are clinically implemented.

Acknowledgments

Suture was provided by Covidien 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 Andrew Groenewald for assistance with collection and storage of cadaveric specimens used for the study.

ABBREVIATIONS

IHMES

Interlocking horizontal mattress epitendinous suture

SDFT

Superficial digital flexor tendon

Footnotes

a.

Delta Power Equipment Corp, Anderson, SC.

b.

iPhone 8 camera, Apple Inc, Cupertino, Calif.

c.

ImageJ, National Institute of Health, Bethesda, Md.

d.

Random number generator, Research Randomizer, Lancaster, Pa.

e.

Surgipro, Covidien Ltd, Dublin, Ireland.

f.

Instron model 5967, Instron Inc, Norwood, Mass.

g.

SKU 1652–1, Sawbones, Vashon Island, Wash.

h.

Panasonic Lumix DMC-FZ200, Panasonic Corp, Newark, NJ.

i.

Bluehill 3, Instron Inc, Norwood, Mass.

j.

Microsoft Excel, Microsoft Corp, Redmond, Wash.

k.

SAS, version 9.4, SAS Institute Inc, Cary, NC.

References

  • 1. Frank CB. Chapter 11: form and function of tendon and ligament. In: O'Keefe RJ, Jacobs JJ, Chu CR, et al, eds. Orthopaedic basic science: foundations of clinical practice. 4th ed. Rosemont, Ill: Lippincott Williams & Wilkins, 2018;191223.

    • Search Google Scholar
    • Export Citation
  • 2. Gelberman RH, Boyer MI, Brodt MD, et al. The effect of gap formation at the repair site on the strength and excursion of intrasynovial flexor tendons. An experimental study on the early stages of tendon-healing in dogs. J Bone Joint Surg Am 1999;81:975982.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Dy CJ, Hernandez-Soria A, Ma Y, et al. Complications after flexor tendon repair: a systematic review and meta-analysis. J Hand Surg Am 2012;37:543551.

  • 4. Wieskötter B, Herbort M, Langer M, et al. The impact of different peripheral suture techniques on the biomechanical stability in flexor tendon repair. Arch Orthop Trauma Surg 2018;138:139145.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5. Lister GD, Kleinert HE, Kutz JE, et al. Primary flexor tendon repair followed by immediate controlled mobilization. J Hand Surg Am 1977;2:441451.

  • 6. Wade PJ, Muir IF, Hutcheon LL. Primary flexor tendon repair: the mechanical limitations of the modified Kessler technique. J Hand Surg Br 1986;11:7176.

  • 7. Silfverskiöld KL, May EJ. Flexor tendon repair in zone II with a new suture technique and an early mobilization program combining passive and active flexion. J Hand Surg Am 1994;19:5360.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Silfverskiöld KL, May EJ. Gap formation after flexor tendon repair in zone II. Results with a new controlled motion programme. Scand J Plast Reconstr Surg Hand Surg 1993;27:263268.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9. Lin GT, An KN, Amadio PC, et al. Biomechanical studies of running suture for flexor tendon repair in dogs. J Hand Surg Am 1988;13:553558.

  • 10. Lotz JC, Hariharan JS, Diao E. Analytic model to predict the strength of tendon repairs. J Orthop Res 1998;16:399405.

  • 11. Pruitt DL, Manske PR, Fink B. Cyclic stress analysis of flexor tendon repair. J Hand Surg Am 1991;16:701707.

  • 12. Chang MK, Wong YR, Tay SC. Biomechanical comparison of modified Lim/Tsai tendon repairs with intra− and extratendinous knots. J Hand Surg Eur Vol 2018;43:919924.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13. Strickland JW. Development of flexor tendon surgery: twenty-five years of progress. J Hand Surg Am 2000;25:214235.

  • 14. Diao E, Hariharan JS, Soejima O, et al. Effect of peripheral suture depth on strength of tendon repairs. J Hand Surg Am 1996;21:234239.

  • 15. Galvez MG, Comer GC, Chattopadhyay A, et al. Gliding resistance after epitendinous-first repair of flexor digitorum profundus in zone II. J Hand Surg Am 2017;42:662.e1–662.e9.

    • Search Google Scholar
    • Export Citation
  • 16. Fufa DT, Osei DA, Calfee RP, et al. The effect of core and epitendinous suture modifications on repair of intrasynovial flexor tendons in an in vivo canine model. J Hand Surg Am 2012;37:25262531.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Merrell GA, Wolfe SW, Kacena WJ, et al. The effect of increased peripheral suture purchase on the strength of flexor tendon repairs. J Hand Surg Am 2003;28:464468.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18. Dona E, Turner AWL, Gianoutsos MP, et al. Biomechanical properties of four circumferential flexor tendon suture techniques. J Hand Surg Am 2003;28:824831.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19. Silfverskiöld KL, Andersson CH. Two new methods of tendon repair: an in vitro evaluation of tensile strength and gap formation. J Hand Surg Am 1993;18:5865.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Barrie KA, Tomak SL, Cholewicki J, et al. Effect of suture locking and suture caliber on fatigue strength of flexor tendon repairs. J Hand Surg Am 2001;26:340346.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21. Gil-Santos L, Monleón-Pradas M, Gomar-Sancho F, et al. Positioning of the cross-stitch on the modified Kessler core tendon suture. J Mech Behav Biomed Mater 2018;80:2732.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22. Hirpara KM, Sullivan PJ, Raheem O, et al. A biomechanical analysis of multistrand repairs with the Silfverskiöld peripheral cross-stitch. J Bone Joint Surg Br 2007;89:13961401.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23. Moores AP, Owen MR, Tarlton JF. The three-loop pulley suture versus two locking-loop sutures for the repair of canine Achilles tendons. Vet Surg 2004;33:131137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24. Guzzini M, Lanzetti RM, Proietti L, et al. Interlocking horizontal mattress suture versus Kakiuchi technique in repair of Achilles tendon rupture: a biomechanical study. J Orthop Traumatol 2017;18:251257.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25. Johnson J, Austin C, Breur G. Incidence of canine appendicular musculoskeletal disorders in 16 veterinary teaching hospitals from 1980 through 1989. Vet Comp Orthop Traumatol 1994;7:5669.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Meeson RL, Davidson C, Arthurs GI. Soft-tissue injuries associated with cast application for distal limb orthopaedic conditions: a retrospective study of sixty dogs and cats. Vet Comp Orthop Traumatol 2011;24:126131.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27. Gall TT, Santoni BG, Egger EL, et al. In vitro biomechanical comparison of polypropylene mesh, modified three-loop pulley suture pattern, and a combination for repair of distal canine Achilles' tendon injuries. Vet Surg 2009;38:845851.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Duffy DJ, Main RP, Moore GE, et al. Ex vivo biomechanical comparison of barbed suture and standard polypropylene suture for acute tendon laceration in a canine model. Vet Comp Orthop Traumatol 2015;28:263269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Kamal RN, Yao J. Evidence-based medicine: surgical management of flexor tendon lacerations. Plast Reconstr Surg 2017;140:130e139e.

Contributor Notes

Address correspondence to Dr. Duffy (djduffy@ncsu.edu).