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PLOS ONE

RESEARCH ARTICLE

Fine tuning of the side-to-side tenorrhaphy: A


biomechanical study assessing different side-
to-side suture techniques in a porcine tendon
model
Christina J. Wilhelm ID1☯*, Marc A. Englbrecht1☯¤a, Rainer Burgkart2, Carina Micheler ID2,3,
Jan Lang ID2,4, Christine S. Hagen1¤b, Riccardo E. Giunta1, Nikolaus Wachtel1
a1111111111 1 Division of Hand, Plastic and Aesthetic Surgery, University Hospital, LMU Munich, Munich, Germany,
a1111111111 2 Department of Orthopaedics and Sports Orthopaedics, Klinikum Rechts der Isar, School of Medicine,
a1111111111 Technical University of Munich, Munich, Germany, 3 Department of Mechanical Engineering, Institute for
a1111111111 Machine Tools and Industrial Management, Technical University of Munich, Munich, Germany, 4 Department
of Mechanical Engineering, Chair of Non-Destructive Testing, Technical University of Munich, Munich,
a1111111111
Germany

☯ These authors contributed equally to this work.


¤a Current address: SENO MVZ, Camparihaus Munich, Munich, Germany
¤b Current address: Frauenklinik Dr. Geisenhofer, Munich, Germany
OPEN ACCESS * christina@wilhelm.nu

Citation: Wilhelm CJ, Englbrecht MA, Burgkart R,


Micheler C, Lang J, Hagen CS, et al. (2021) Fine
tuning of the side-to-side tenorrhaphy: A Abstract
biomechanical study assessing different side-to-
side suture techniques in a porcine tendon model. Recent studies conclude that a new technique for tendon transfers, the side-to-side tenor-
PLoS ONE 16(10): e0257038. https://doi.org/ rhaphy by Fridén (FR) provides higher biomechanical stability than the established standard
10.1371/journal.pone.0257038
first described by Pulvertaft (PT). The aim of this study was to optimize side-to-side tenor-
Editor: Gabriel de Araújo, Universidade Federal rhaphies. We compared PT and FR tenorrhaphies as well as a potential improvement,
Fluminense, BRAZIL
termed Woven-Fridén tenorrhaphy (WF), with regard to biomechanical stability. Our results
Received: June 21, 2021 demonstrate superior biomechanical stability and lower bulk of FR and, in particular, WF
Accepted: August 17, 2021 over PT tenorrhaphies. The WF and FR technnique therefore seem to be a notable alterna-
Published: October 5, 2021 tive to the established standard tenorrhaphy as they display lower bulk and higher stability,
permitting successful immediate active mobilization after surgery.
Copyright: © 2021 Wilhelm et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.

Data Availability Statement: All relevant data are Introduction


within the manuscript and its Supporting
information files. Tendon transfers with a subsequent side-to-side tenorrhaphy are predominantly used to
restore limb-function after trauma of the central or peripheral nervous system and/or trauma
Funding: The authors received no specific funding
for this work.
impairing muscle (tendon) function of the extremities [1, 2]. This surgical technique is com-
monly performed in foot and ankle as well as in hand and plastic surgery. Common examples
Competing interests: I have read the journal’s
include the treatment of patients with common peroneal nerve palsy (foot drop) and inser-
policy and the authors of this manuscript have the
following competing interests: M. A. E. works as an
tional or noninsertional tendinopathy of the Achilles tendon [3, 4]. Moreover, side-to-side
instructor for Arthrex Inc educational courses on a tenorrhaphies are used to restore critical grasping motions of the hand after brachial plexus
fee basis. No further external funding, payments, or palsy [5, 6].

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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.

Materials and methods


Ethics statement
Ethical approval for this study was obtained from the Ethics Committee of the Medical Faculty
at LMU Munich, Germany (Approval Number: 19–142). Tendons were obtained from porcine
hind limbs. These were purchased from a local butcher. The Ethics Committee for Animal
Experiments, LMU Munich, granted a formal waiver for current and future experiments using
tendons from porcine hind limbs.

Inclusion, exclusion and randomization


The extensor tendons of porcine hind limbs were harvested as previously described by Fuchs
et al. [14]. After harvesting, tendons were stored in a vacuum bag and fresh-frozen at -28˚C.
Specimens were thawed in water at 37˚C directly before performing the sutures [15, 16]. Block
randomization was used to determine which tendon pairs were used in experimental groups
and to distribute the tendons of each limb to the three groups of one experimental series in a
balanced manner (S1 Data). For each experimental group, 12 side-to-side tenorrhaphies were
tested. Thus, a total of 72 sutures were tested.

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.

Suture characteristics and biomechanical testing


Tendon and suture diameter as well as the length of overlap were measured with a digital cali-
per after tenorrhaphy completion. The bulk ratio of tenorrhaphies was determined by dividing
the cross-sectional area of tendons [13]. For biomechanical testing, stiffness (resistance of
sutures to deformation), first failure load (first local maximum of force in the load-deforma-
tion curve), and ultimate load (highest force (N) achieved before ultimate failure) were mea-
sured as described previously [7, 12, 13, 17].
All experiments were performed following a standardized protocol, similar to protocols of
previous studies [7, 12, 17]. All mechanical tests were performed using a calibrated tensile test-
ing machine (Zwicki 1120, ZwickRoell GmbH & Co. KG, Ulm, Baden-Württemberg, Ger-
many). A preload of 2 N was applied to minimize slack and 5 preconditioning cycles with a
deformation of 5% of the distance between the clamps were imposed [7, 18]. Tenorrhaphies
were then preconditioned at a velocity of 10 mm/min to be elongated until failure at a velocity

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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

and, in particular, WF side-to-side tenorrhaphies over the technique described by PT with


regard to biomechanical stability as well as bulk.
A probable explanation for the higher stiffness and load bearing capacities of both FR and
WF tenorrhaphies is the usage of running cross-stitches for both techniques. An advantage of

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

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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)

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PLOS ONE Fine tuning of the side-to-side tenorrhaphy

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.

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