Pone 0257038
Pone 0257038
Pone 0257038
RESEARCH ARTICLE
services have been received or will be received Here, an optimal suture stability is essential, allowing for early mobilization and, thus,
from a commercial party related directly or reduced adhesion formation and post-operative recovery time [7, 8]. The established standard
indirectly to the subject of this article. The authors
technique for a tendon transfer was first described by Pulvertaft (PT) et al. [9–11]. Interest-
alone are responsible for experiments, data
analysis, and writing of the paper. This does not ingly, recent studies demonstrated that a new technique, the side-to-side tenorrhaphy by Fri-
alter our adherence to PLOS ONE policies on dén (FR) et al., provides both efficient force transmission and high suture strength. Indeed,
sharing data and materials. repair stiffness, load at first failure and ultimate failure load of the FR suture were significantly
higher when compared to PT sutures [7, 8, 12, 13].
The aim of this biomechanical study was therefore to optimize the technique of side-to-side
tenorrhaphies. We assessed the biomechanical properties of PT, FR, and a potential improve-
ment of the FR technique, termed Woven-Fridén (WF) tenorrhaphy.
Tenorrhaphies
PT and FR tenorrhaphies were performed as described previously by Brown et al. [7] (Fig 1).
Additionally, we tested a varied approach to the FR technique, termed WF (Fig 2). Each tenor-
rhaphy was performed with a 30 mm tendon-tendon overlap. Ethibond™ 3–0 (Ethicon, Inc.
Somerville, NJ, USA) was used as suture material.
Fig 1. Overview of suture techniques used. The different techniques Pulvertaft (PT), Fridén (FR) and Woven-Fridén
(WF) are illustrated: The donor tendon (above) was woven through incisions in the recipient tendon (below). For each
suture technique the same amount of connection points between the tendons was used. The threads were cut in
standardized fashion at 10 mm length.
https://doi.org/10.1371/journal.pone.0257038.g001
of 100 mm/min [7, 12, 17]. The tensile load test outputs were plotted on a load-deformation
curve (TestXpert V12.0 ZwickRoell GmbH & Co. KG, Ulm, Baden-Württemberg, Germany).
We used a custom written MATLAB code (MATLAB R2017b, The MathWorks, Inc. Natick,
MA, USA) to determine load at first failure, ultimate load and repair stiffness. The stiffness of
the tenorrhaphy was determined within the linear elastic area of the load-deformation curve.
The preconditioning data were removed and by means of the coefficient of determination
(R2), the linear elastic area was identified to calculate the stiffness of the tenorrhaphy [19].
Means and standard deviations were calculated for the different groups. Tensile testing was
filmed using a Legria HF M31 video camera (Canon Co. Ltd., Ohta-ku, Tokyo, Japan) to docu-
ment the mode of failure (pull-out vs. suture breakage) [20, 21].
Statistical analysis
Data are given as means and standard deviation (SD). One-way analysis of variance
(ANOVA), followed by the Tukey-Kramer test for multiple comparisons was conducted to
assess effects of tenorrhaphy techniques on bulk ratio, repair stiffness, first failure load, and
ultimate load. A p-value of < 0.05 was considered statistically significant. GraphPad Prism 6
(GraphPad Software, Inc., San Diego, CA, USA) was used as software for statistical analysis.
Results
When analyzing different tenorrhaphy techniques, the WF group had the lowest relative cross-
sectional area (bulk ratio), which was significantly lower when compared to the PT group
(p < 0.001) (Fig 3). Results for biomechanical analysis of different tenorrhaphies are shown in
Fig 4. Ultimate load was highest in the WF group (compared to both FR and PT tenorrhaphies;
p of 0.02 and < 0.001, respectively). Stiffness was highest for WF and FR sutures (p = 0.005 for
PT vs. FR and p < 0.001 for PT vs. WF). WF sutures therefore showed highest stability while
suture failure occurred earliest in the PT technique. All side-to-side tenorrhaphies failed by
Fig 2. Schematic model of the Woven-Fridén tenorrhaphy (WF) (30 mm tendon-tendon overlap) using brown and white strings. 1. Mark incisions
and overlap for donor- (brown) and recipient tendon (white) with a surgical pen and make three incisions in the recipient tendon using a No. 15 scalpel
blade. 2. Interlace the donor tendon (brown) through the recipient tendon (white). 3. Perform two double-loop sutures at proximal and distal end of
tenorrhaphy (arrows). 4. Perform eight running cross stitches at the radial side (R) and 5. ulnar side (U) of the tenorrhaphy. 6. WF tenorrhaphy (the
overlap has been reduced to approximately 27 mm due to interlacing of tendons).
https://doi.org/10.1371/journal.pone.0257038.g002
pull-out. For all experiments, first failure load was identical or highly similar to ultimate failure
load (also see S1 Data).
Discussion
In our study, we set out to determine the biomechanical properties of the FR side-to-side
tenorrhaphy, which was recently proposed as an alternative to PT sutures with superior bio-
mechanical stability [7, 12, 13]. Furthermore, we aimed to improve the FR technique by adding
two horizontal weaves (Fig 2). We termed this variation WF.
A high bulk of tendon-to-tendon sutures can lead to friction between tendons and adjacent
tissue. This results in formation of adhesions that compromise the natural gliding mechanics
of tendons [18, 22–24]. Moreover, a strong mechanical tenorrhaphy is essential for an optimal
clinical outcome as it permits immediate active mobilization thereby minimizing adhesion for-
mation and providing optimal conditions for healing and mobility [8, 25]. Recent studies with
a similar set-up demonstrated that the ultimate load of the FR technique was significantly
higher when compared to PT sutures [7, 12, 13]. We were able to confirm these findings (Fig
4). Moreover, the highest ultimate failure load and lowest bulk formation was measured for
the WF group (Figs 3 and 4). The findings of this study therefore advocate an advantage of FR
Fig 3. Effects of suture techniques Pulvertaft (PT), Fridén (FR) and Woven-Fridén (WF) on bulk ratio in % (ratio
of the cross-sectional area of the sutured tendons and the native tendons; for details see S1 Data). Data is expressed
as means, standard deviation bars are shown. Different superscripts indicate statistically significant differences among
groups at p < 0.001. For each experimental group, 12 side-to-side tenorrhaphies were tested.
https://doi.org/10.1371/journal.pone.0257038.g003
Fig 4. Effects of suture techniques Pulvertaft (PT), Fridén (FR) and Woven-Fridén (WF) on stiffness (resistance of
sutures to deformation) in N/mm (crosshatched bars) and on ultimate load in N (single-colour bars). Data is
expressed as means, standard deviation bars are shown. Different superscripts indicate statistically significant
differences among groups at p < 0.05 and for WF vs. PT at p < 0.0001. For each experimental group, 12 side-to-side
tenorrhaphies were tested.
https://doi.org/10.1371/journal.pone.0257038.g004
these stitches seems likely as all three suture techniques had the same number of connection
points (Fig 1). Indeed, a previous biomechanical study demonstrated the superior ultimate
load bearing capacities of cross-stitches over mattress sutures [26]. Equally, Brown et al. argue
that running cross-stitches permit force distribution over a larger area when compared to mat-
tress sutures used in the PT technique [7]. The mattress suture in the PT tenorrhaphy that is
tightest might act as a focused transmission of tensile load from one tendon to the next and,
thus, could facilitate suture failure. Differences between WF and FR sutures may be explained
by a similar mechanism: more than one weave results in a more balanced load of force in com-
bination with a stabilizing interlocking effect between the two tendons [4]. Hereby increasing
the ultimate load of WF tenorrhaphies. However, if these hypotheses prove to be correct, it has
to be argued whether the usage of cross-stitches instead of mattress sutures improves the bio-
mechanical properties of the PT suture. Thus, matching those of FR or even WF
tenorrhaphies.
The conclusions of this study are predominantly limited by its in vitro set-up. Porcine
extensor tendons differ from human tendons in size and structure and our findings on load
bearing capacity may therefore differ in human tendons, in particular when tendons with a dif-
ferent caliber are used [14, 27–31]. Moreover, by using a cadaver model we were unable to
reproduce normal tissue biology. During the healing process with a subsequent inflammatory
stage, the stability of the sutured tendons is reported to decline [32, 33]. Indeed, several studies
that assessed the stability of tendon sutures in vivo during the healing period indicate that ten-
sile strength of sutured tendons decreases during the first weeks postoperatively [34, 35]. High
suture stability in vitro may therefore not ensure equal biomechanical properties in vivo. Being
aware of this limitation, we advocate for subsequent studies that assess the three sutures in an
in vivo set-up similar to previous publications that explored tendon biology [36–38].
This study demonstrated the superior biomechanical properties of FR side-to-side tenor-
rhaphies over PT sutures. Additionally, our proposed modifications of the FR technique,
termed WF tenorrhaphy, further improved load bearing capacities. FR and, in particular, WF
tenorrhaphies therefore seem to be a superior alternative to the established standard technique
for side-to-side tenorrhaphies, thereby increasing probability of successful immediate active
mobilization after surgery.
Supporting information
S1 Table. Standardized experimental protocol using block randomization. A-C stand for
Pulvertaft (PT), Fridén (FR) and Woven-Fridén (WF) suture techniques. Four tendons of por-
cine hind limbs were used: M. extensor digitalis lateralis (I), M. extensor digiti III et IV (II) M.
extensor digiti III (III) and M. extensor digiti I longus (IV). Tendons were cut in half before
combining the proximal part (prox.) of one tendon with the distal part (dist.) of another ten-
don for a suture. The lateral (I) and the medial tendon (IV) had a smaller caliber and were
therefor used as donors, median tendons (II and III) were used as recipients. Every combina-
tion of donor- and recipient-tendon was equally often used for each experimental group.
(DOCX)
S2 Table. Comparison of different characteristics of three different suture techniques: Pul-
vertaft (PT), Fridén (FR) and Woven-Fridén (WF). Values are expressed as mean (SD). Dif-
ferent superscripts indicate statistically significant differences among groups at p of at
least < 0.05.
(DOCX)
S1 File. Calculation of the Bulk Ratio (BR). The formula to calculate the BR is given and
derived.
(DOCX)
S1 Data. Tabular listing and graphical representation of all collected data.
(PDF)
Author Contributions
Conceptualization: Marc A. Englbrecht, Christine S. Hagen, Nikolaus Wachtel.
Data curation: Carina Micheler, Jan Lang.
Formal analysis: Christina J. Wilhelm.
Investigation: Christina J. Wilhelm.
Methodology: Christina J. Wilhelm, Marc A. Englbrecht, Carina Micheler, Jan Lang, Nikolaus
Wachtel.
Project administration: Nikolaus Wachtel.
Resources: Rainer Burgkart, Riccardo E. Giunta.
Software: Carina Micheler, Jan Lang.
Supervision: Marc A. Englbrecht, Rainer Burgkart, Christine S. Hagen, Riccardo E. Giunta.
Validation: Carina Micheler, Jan Lang, Nikolaus Wachtel.
Visualization: Christina J. Wilhelm, Nikolaus Wachtel.
Writing – original draft: Christina J. Wilhelm.
Writing – review & editing: Riccardo E. Giunta, Nikolaus Wachtel.
References
1. Wilbur D, Hammert WC. Principles of Tendon Transfer. Hand clinics. 2016; 32(3):283–9. https://doi.org/
10.1016/j.hcl.2016.03.001 PMID: 27387072
2. Fitoussi F, Bachy M. Tendon lengthening and transfer. Orthopaedics & traumatology, surgery &
research: OTSR. 2015; 101(1 Suppl):S149–57. https://doi.org/10.1016/j.otsr.2014.07.033 PMID:
25572471
3. Marsland D, Stephen JM, Calder T, Amis AA, Calder JDF. Strength of Interference Screw Fixation to
Cuboid vs Pulvertaft Weave to Peroneus Brevis for Tibialis Posterior Tendon Transfer for Foot Drop.
Foot & ankle international. 2018; 39(7):858–64. https://doi.org/10.1177/1071100718762442 PMID:
29582684
4. Wagner E, Ortiz C, Wagner P, Guzman R, Ahumada X, Maffulli N. Biomechanical evaluation of various
suture configurations in side-to-side tenorrhaphy. The Journal of bone and joint surgery American vol-
ume. 2014; 96(3):232–6. https://doi.org/10.2106/JBJS.L.01552 PMID: 24500585
5. Abzug JM, Kozin SH. Evaluation and management of brachial plexus birth palsy. The Orthopedic clinics
of North America. 2014; 45(2):225–32. https://doi.org/10.1016/j.ocl.2013.12.004 PMID: 24684916
6. Gutowski KA, Orenstein HH. Restoration of elbow flexion after brachial plexus injury: the role of nerve
and muscle transfers. Plastic and reconstructive surgery. 2000; 106(6):1348–57; quiz 58; discussion
59. https://doi.org/10.1097/00006534-200011000-00020 PMID: 11083569
7. Brown SH, Hentzen ER, Kwan A, Ward SR, Friden J, Lieber RL. Mechanical strength of the side-to-side
versus Pulvertaft weave tendon repair. J Hand Surg Am. 2010; 35(4):540–5. https://doi.org/10.1016/j.
jhsa.2010.01.009 PMID: 20223604
8. Friden J, Reinholdt C. Current concepts in reconstruction of hand function in tetraplegia. Scandinavian
journal of surgery: SJS: official organ for the Finnish Surgical Society and the Scandinavian Surgical
Society. 2008; 97(4):341–6. https://doi.org/10.1177/145749690809700411 PMID: 19211389
9. Pulvertaft RG. Tendon grafts for flexor tendon injuries in the fingers and thumb; a study of technique
and results. The Journal of bone and joint surgery British volume. 1956; 38-b(1):175–94. https://doi.org/
10.1302/0301-620X.38B1.175 PMID: 13295327
10. De Smet L, Schollen W, Degreef I. In vitro biomechanical study to compare the double-loop technique
with the Pulvertaft weave for tendon anastomosis. Scandinavian journal of plastic and reconstructive
surgery and hand surgery. 2008; 42(6):305–7. https://doi.org/10.1080/02844310802401330 PMID:
18991173
11. Cheah AE, Etcheson J, Yao J. Radial Nerve Tendon Transfers. Hand clinics. 2016; 32(3):323–38.
https://doi.org/10.1016/j.hcl.2016.03.003 PMID: 27387076
12. Tsiampa VA, Ignatiadis I, Papalois A, Givissis P, Christodoulou A, Friden J. Structural and mechanical
integrity of tendon-to-tendon attachments used in upper limb tendon transfer surgery. Journal of plastic
surgery and hand surgery. 2012; 46(3–4):262–6. https://doi.org/10.3109/2000656X.2012.684097
PMID: 22616803
13. Rivlin M, Eberlin KR, Kachooei AR, Hosseini A, Zivaljevic N, Li G, et al. Side-to-Side Versus Pulvertaft
Extensor Tenorrhaphy-A Biomechanical Study. The Journal of hand surgery. 2016; 41(11):e393–e7.
https://doi.org/10.1016/j.jhsa.2016.07.106 PMID: 27546442
14. Fuchs SP, Walbeehm ET, Hovius SE. Biomechanical evaluation of the Pulvertaft versus the ’wrap
around’ tendon suture technique. The Journal of hand surgery, European volume. 2011; 36(6):461–6.
https://doi.org/10.1177/1753193411402756 PMID: 21447532
15. Viidik A, Lewin T. Changes in tensile strength characteristics and histology of rabbit ligaments induced
by different modes of postmortal storage. Acta orthopaedica Scandinavica. 1966; 37(2):141–55. https://
doi.org/10.3109/17453676608993274 PMID: 5911489
16. Giannini S, Buda R, Di Caprio F, Agati P, Bigi A, De Pasquale V, et al. Effects of freezing on the bio-
mechanical and structural properties of human posterior tibial tendons. International orthopaedics.
2008; 32(2):145–51. https://doi.org/10.1007/s00264-006-0297-2 PMID: 17216243
17. Friden J, Tirrell TF, Bhola S, Lieber RL. The mechanical strength of side-to-side tendon repair with mis-
matched tendon size and shape. The Journal of hand surgery, European volume. 2015; 40(3):239–45.
https://doi.org/10.1177/1753193413517327 PMID: 24413573
18. Jeon SH, Chung MS, Baek GH, Lee YH, Kim SH, Gong HS. Comparison of loop-tendon versus end-
weave methods for tendon transfer or grafting in rabbits. The Journal of hand surgery. 2009; 34
(6):1074–9. https://doi.org/10.1016/j.jhsa.2009.02.025 PMID: 19643292
19. Synek A, Chevalier Y, Baumbach SF, Pahr DH. The influence of bone density and anisotropy in finite
element models of distal radius fracture osteosynthesis: Evaluations and comparison to experiments.
Journal of biomechanics. 2015; 48(15):4116–23. https://doi.org/10.1016/j.jbiomech.2015.10.012 PMID:
26542787
20. Miller B, Dodds SD, deMars A, Zagoreas N, Waitayawinyu T, Trumble TE. Flexor tendon repairs: the
impact of fiberwire on grasping and locking core sutures. The Journal of hand surgery. 2007; 32
(5):591–6. https://doi.org/10.1016/j.jhsa.2007.03.003 PMID: 17481994
21. Barrie KA, Tomak SL, Cholewicki J, Merrell GA, Wolfe SW. Effect of suture locking and suture caliber
on fatigue strength of flexor tendon repairs. The Journal of hand surgery. 2001; 26(2):340–6. https://doi.
org/10.1053/jhsu.2001.22926 PMID: 11279582
22. Amadio PC. Friction of the gliding surface. Implications for tendon surgery and rehabilitation. Journal of
hand therapy: official journal of the American Society of Hand Therapists. 2005; 18(2):112–9. https://
doi.org/10.1197/j.jht.2005.02.005 PMID: 15891969
23. Rawson S, Cartmell S, Wong J. Suture techniques for tendon repair; a comparative review. Muscles,
ligaments and tendons journal. 2013; 3(3):220–8. PMID: 24367784
24. Graham JG, Wang ML, Rivlin M, Beredjiklian PK. Biologic and mechanical aspects of tendon fibrosis
after injury and repair. Connective tissue research. 2019; 60(1):10–20. https://doi.org/10.1080/
03008207.2018.1512979 PMID: 30126313
25. Wangdell J, Bunketorp-Kall L, Koch-Borner S, Friden J. Early Active Rehabilitation After Grip Recon-
structive Surgery in Tetraplegia. Archives of physical medicine and rehabilitation. 2016; 97(6 Suppl):
S117–25. https://doi.org/10.1016/j.apmr.2015.09.025 PMID: 27233586
26. Gabuzda GM, Lovallo JL, Nowak MD. Tensile strength of the end-weave flexor tendon repair. An in
vitro biomechanical study. Journal of hand surgery (Edinburgh, Scotland). 1994; 19(3):397–400. https://
doi.org/10.1016/0266-7681(94)90098-1 PMID: 8077837
27. Mao WF, Wu YF, Zhou YL, Tang JB. A study of the anatomy and repair strengths of porcine flexor and
extensor tendons: are they appropriate experimental models? The Journal of hand surgery, European
volume. 2011; 36(8):663–9. https://doi.org/10.1177/1753193411414117 PMID: 21768214
28. Haddad RJ Jr., Kester MA, McCluskey GM, Brunet ME, Cook SD. Comparative mechanical analysis of
a looped-suture tendon repair. The Journal of hand surgery. 1988; 13(5):709–13. https://doi.org/10.
1016/s0363-5023(88)80130-8 PMID: 3071546
29. Savage R. In vitro studies of a new method of flexor tendon repair. Journal of hand surgery (Edinburgh,
Scotland). 1985; 10(2):135–41. https://doi.org/10.1016/0266-7681(85)90001-4 PMID: 3161963
30. Viinikainen A, Goransson H, Huovinen K, Kellomaki M, Tormala P, Rokkanen P. The strength of the 6-
strand modified Kessler repair performed with triple-stranded or triple-stranded bound suture in a por-
cine extensor tendon model: an ex vivo study. The Journal of hand surgery. 2007; 32(4):510–7. https://
doi.org/10.1016/j.jhsa.2007.01.010 PMID: 17398362
31. Kulikov YI, Dodd S, Gheduzzi S, Miles AW, Giddins GE. An in vitro biomechanical study comparing the
spiral linking technique against the pulvertaft weave for tendon repair. The Journal of hand surgery,
European volume. 2007; 32(4):377–81. https://doi.org/10.1016/J.JHSB.2007.02.009 PMID: 17452067
32. Voleti PB, Buckley MR, Soslowsky LJ. Tendon healing: repair and regeneration. Annual review of bio-
medical engineering. 2012; 14:47–71. https://doi.org/10.1146/annurev-bioeng-071811-150122 PMID:
22809137
33. Hope M, Saxby TS. Tendon healing. Foot and ankle clinics. 2007; 12(4):553–67, v. https://doi.org/10.
1016/j.fcl.2007.07.003 PMID: 17996614
34. Wagner WF Jr., Carroll Ct, Strickland JW, Heck DA, Toombs JP. A biomechanical comparison of tech-
niques of flexor tendon repair. The Journal of hand surgery. 1994; 19(6):979–83. https://doi.org/10.
1016/0363-5023(94)90101-5 PMID: 7876500
35. Mason ML, Allen HS. THE RATE OF HEALING OF TENDONS: AN EXPERIMENTAL STUDY OF TEN-
SILE STRENGTH. Annals of surgery. 1941; 113(3):424–59. https://doi.org/10.1097/00000658-
194103000-00009 PMID: 17857746
36. Dogramaci Y, Uruc V, Ozden R, Duman IG, Kalaci A, Altug ME, et al. The comparison of macroscopic
and histologic healing of side-to-side (SS) tenorrhaphy technique and primer tendon repair in a rabbit
model. Archives of orthopaedic and trauma surgery. 2014; 134(7):1031–5. https://doi.org/10.1007/
s00402-014-2010-z PMID: 24853959
37. Wu YF, Zhou YL, Mao WF, Avanessian B, Liu PY, Tang JB. Cellular apoptosis and proliferation in the
middle and late intrasynovial tendon healing periods. J Hand Surg Am. 2012; 37(2):209–16. https://doi.
org/10.1016/j.jhsa.2011.10.049 PMID: 22209211
38. Lui PP, Cheuk YC, Hung LK, Fu SC, Chan KM. Increased apoptosis at the late stage of tendon healing.
Wound repair and regeneration: official publication of the Wound Healing Society [and] the European
Tissue Repair Society. 2007; 15(5):702–7.