Orthopedics

Feature Article 

Mechanisms of Suture Integration in Living Tissue: Biomechanical and Histological In Vivo Analysis in Sheep

Dominik C. Meyer, MD; Anita Hasler, MD; Seraina Wyss, M Med; Katja Nuss, DMV; Mario C. Benn, DMV; Christian Gerber, MD, FRCS; Karl Wieser, MD

Abstract

The potential of nonabsorbable suture material to augment tissue strength in the long-term is by far not exploited by most of the currently used sutures. The authors hypothesized that different sutures yield specific histological tissue reactions associated with specific mechanical shear resistance of the suture against the tissue. Four different suture types (Orthocord, Ethibond, FiberTape, and FiberWire) were implanted in 36 sheep shoulders (supraspinatus/greater tuberosity). One thread at each time point (6, 16, and 22 weeks) was used for histology, and 11 threads at each time point (0, 6, 16, and 22 weeks) were used for biomechanical longitudinal pullout testing. Histology included tissue maturity, activity of tissue reaction, and invasion of cells and tissue into the suture material. Fiber-Tape had the highest mean pullout strength at 6, 16, and 22 weeks of 4.4 N/cm (SD, 2.1 N/cm), 10.1 N/cm (SD, 5.1 N/cm), and 12.8 N/cm (SD, 6.0 N/cm), respectively. However, general pullout strength at 22 weeks was surprisingly low, particularly for Ethibond, Orthocord and FiberWire. The overall maturity of the surrounding tissue correlated (r=0.84, P=.001) with mechanical performance. Interestingly, in all 4 suture types, an intimate in- and on-growth of fibrous tissue to the filaments and into the space between suture fibers could be shown. However, for Ethibond, Orthocord, and FiberWire, the authors found an unexpected circumferential space around the sutures, often forming an inner and outer capsule, separating the sutures from the surrounding tissue with a shifting layer. [Orthopedics. 2019; 42(3):168–175.]

Abstract

The potential of nonabsorbable suture material to augment tissue strength in the long-term is by far not exploited by most of the currently used sutures. The authors hypothesized that different sutures yield specific histological tissue reactions associated with specific mechanical shear resistance of the suture against the tissue. Four different suture types (Orthocord, Ethibond, FiberTape, and FiberWire) were implanted in 36 sheep shoulders (supraspinatus/greater tuberosity). One thread at each time point (6, 16, and 22 weeks) was used for histology, and 11 threads at each time point (0, 6, 16, and 22 weeks) were used for biomechanical longitudinal pullout testing. Histology included tissue maturity, activity of tissue reaction, and invasion of cells and tissue into the suture material. Fiber-Tape had the highest mean pullout strength at 6, 16, and 22 weeks of 4.4 N/cm (SD, 2.1 N/cm), 10.1 N/cm (SD, 5.1 N/cm), and 12.8 N/cm (SD, 6.0 N/cm), respectively. However, general pullout strength at 22 weeks was surprisingly low, particularly for Ethibond, Orthocord and FiberWire. The overall maturity of the surrounding tissue correlated (r=0.84, P=.001) with mechanical performance. Interestingly, in all 4 suture types, an intimate in- and on-growth of fibrous tissue to the filaments and into the space between suture fibers could be shown. However, for Ethibond, Orthocord, and FiberWire, the authors found an unexpected circumferential space around the sutures, often forming an inner and outer capsule, separating the sutures from the surrounding tissue with a shifting layer. [Orthopedics. 2019; 42(3):168–175.]

Suture material is essential, effective, and omnipresent in surgery. It positions and secures tissue such as tendons, ligaments, or fascia until healing has occurred. A stable initial fixation is necessary for sufficient tissue healing at these critical junctions. Therefore, nonabsorbable suture material is often used in orthopedic surgery. Previous research has focused on improving the biomechanical properties of suture material, including different tendon grasping techniques, various knot techniques, and suture positioning.1–7 However, in the long-term (eg, in the context of degenerative rotator cuff tears), it would appear desirable that the remaining suture material be integrated into the repaired tissue, thereby contributing to the overall stability by augmentation of fixation.8,9 In the authors' experience, even during revision surgery many years after primary implantation, the suture material can often be pulled out extremely easily. Considering the almost nonexistent longitudinal mechanical resistance to suture material, the authors conclude that there is little long-term tissue augmentation by the suture material.10,11 This is consistent with previous reports identifying the suture–tendon interface as the weakest point in rotator cuff repair via suture pullout.12,13

The authors hypothesized that different suture types elicit different histological responses and consequently different amounts of tissue in- or on-growth, leading to variable but unknown shear resistance of the suture in the tissue. The second hypothesis was therefore that the interaction of the suture and the tissue has an effect on the biomechanical characteristics of the tissue repair. Therefore, this experimental animal study was initiated to examine the histological and biomechanical tissue adherence to soft tissue and bone of 4 different, commonly used, nonabsorbable suture materials for tendon to bone repair. A structural integration of the suture material may reinforce the repaired soft tissue in the long-term.

Materials and Methods

Animals

All animal experiments were performed according to Swiss laws of animal welfare and were authorized through the responsible authorities. There were 36 female, Swiss alpine sheep with a mean age of 25±4 months and a mean weight of 53±5 kg. This study was part of an experimental study investigating infraspinatus muscle degeneration caused by tenotomy of the infraspinatus tendon or neurectomy in the spinoglenoid notch of the suprascapular nerve in sheep.14,15 The right supraspinatus muscle was not affected in the framework of this study. The left shoulders were used as a control group for the previous study.

Sutures

The authors tested 4 different nonabsorbable suture materials of United States Pharmacopeia number 2 that are commonly used in orthopedic surgery. The suture materials were Orthocord (DePuy Mitek, Raynham, Massachusetts), Ethibond (Ethicon, Somerville, New Jersey), FiberTape (Arthrex, Naples, Florida), and FiberWire (Arthrex) (Table 1).

Characteristics of the 4 Types of Suture

Table 1:

Characteristics of the 4 Types of Suture

Surgical Technique

The sheep were placed in the lateral position, and the surgery was performed on the right shoulder of the sheep. Through a 15-cm curved incision, 2-cm cranial to the scapular spine, the supraspinatus muscle was exposed. In controlled distribution, four different suture types were implanted in a knotted loop configuration (3 to 4 cm in the tissue) in each sheep using a straight Mayo needle (Medline Industries, Northfield, Illinois) in the right supraspinatus musculotendinous junction and a fifth in 6 sheep for immediately pullout. Additionally, in 6 sheep, all 4 suture types were placed through a bone tunnel in the greater tuberosity at one time point (Figure 1A).

Intraoperative situs in the sheep model. Suture loops in the supraspinatus at the myotendinous junction (asterisk). Suture loops in the greater tuberosity through a bone tunnel (arrowhead) (A). Schematic representation of the biomechanical setup. Arrow indicates direction of applied tensile load (B).

Figure 1:

Intraoperative situs in the sheep model. Suture loops in the supraspinatus at the myotendinous junction (asterisk). Suture loops in the greater tuberosity through a bone tunnel (arrowhead) (A). Schematic representation of the biomechanical setup. Arrow indicates direction of applied tensile load (B).

The study was designed such that when the animals were killed at 22 weeks, different retention periods of the sutures were available for the histological and biomechanical testing.

For time point 0 weeks, 6 sutures per suture type were immediately pulled out and tested biomechanically. For each of the other time points—6, 16, and 22 weeks—11 sutures per suture type were available for mechanical testing and 1 suture per suture type was available for histological analysis in soft tissue. For pullout testing from bone, 6 suture loops per suture type were implanted and mechanically tested after 22 weeks.

Biomechanical Testing

Immediately after the sheep were killed, the loops were cut open and the protruding part of the suture tail was grasped with a surgical needle clamp, which was connected to a force sensor (Model Type 9203; Kistler, Winterthur, Switzerland). In the longitudinal direction of the suture, a tensile load to failure (peak force until suture extraction) was increasingly applied during approximately 30 seconds. The length of the suture tail within the soft tissue or bone was measured and correlated to calculate suture hold in N/cm (Figure 1B). Suture hold in the bone was additionally tested at week 22 with the same test protocol.

Histological Assessment

After the animals were killed, the implanted suture loops with their surrounding tissue were harvested. Tissue samples were embedded in 4% formalin for 7 days, after which they were washed 3 times for 60 minutes in water and dehydrated in ethanol (with 50%, 70%, 80%, 90%, 96%, and 100% ethanol). Subsequently, the samples were conserved in xylene twice for each 2 days in vacuum and then stored under vacuum in methylmethacrylate for 7 to 10 days in the refrigerator. Thereafter, on thick sections of 400 µm, Giemsa staining was performed. The goal was to have 4 different thick sections at each time period/suture type. Sometimes during the processing, the suture was inadvertently detached from the histological slice, resulting in the sections at each time period/suture type being a mean of 2.9 samples (range, 1–4 samples). Evaluations were performed using an IX50 microscope (Olympus Schweiz AG, Volketswil, Switzerland). Images were recorded with a digital camera (DP71; Olympus Schweiz AG).

Capsule. Measurements of the thickness of the capsule were made with cellSens Dimension software (Olympus Schweiz AG) on the basis of the image recordings. Picture editing of microscopic fields was performed with Photoshop CC (Adobe Systems Inc, San Jose, California). The thickness of the fibrous capsule around the suture was measured at 4 points—3, 6, 9, and 12 o'clock.

Tissue Reaction and Maturity. The tissue reaction and maturity were assessed with a cell measurement in comparison to the Ehrlich and Hunt scale.16 These were counted in a quadrant of the visual field at a magnification of 200. Tissue maturity was determined qualitatively on the basis of the ratio of fibroblasts and fibrocytes.

The maturity of the surrounding connective tissue was classified according to the proportion of fibroblasts and fibrocytes as well as the fiber orientation and density (Table 2).17

Classification of the Maturity of Connective Tissuea

Table 2:

Classification of the Maturity of Connective Tissue

Cell and Tissue Invasion. The cell and tissue integration into the thread was divided into 5 classes.17 An invasion of the outer one third of the thread represented a class 1 invasion, and invasion of cells up to the two thirds or three thirds represented class 2 and class 3, respectively. Class 4 had a homogeneous organization, and class 5 had complete biodegradation.

Statistical Analysis

Strength measurements were logarithmically transformed for statistical analysis. Weeks and fibers were compared using a 2-way factorial analysis of variance followed by post hoc Bonferroni tests. For illustration, 1-way analyses of variance with post hoc Bonferroni comparisons of weeks were performed for each fiber separately, and those of fibers for each week, respectively.

At each time point (weeks 6, 16, and 22), the sutures were compared using a 2-tailed t test regarding capsular thickness, tissue reaction and tissue maturity, cell invasion, and tissue invasion. Moreover, for each suture type, the evaluation over time was monitored. Because of various variances, the authors used a 2-tailed t test for unequal variances (Welch's 2-sample t test). To identify a correlation between suture hold and histological findings, the correlation coefficient r by Bravais–Pearson was calculated. Significance was set at P<.05 (r=0.10, weak; r=0.30, medium; and r= 0.50, strong correlation effect). Values were reported as mean±SD. SPSS Statistics version 21.0 software (IBM, Armonk, New York) was used.

Results

Biomechanical Testing

FiberTape, with a mean of 0.66 N/cm (SD, 0.3 N/cm), showed the highest immediate resistance in the tendon. This was significantly higher compared with the other 3 sutures (P=.004 for Ethibond and FiberWire and P=.001 for Orthocord), which had retraction forces between 0.15 N/cm (SD, 0.1 N/cm) (Orthocord) and 0.24 N/cm (SD, 0.1 N/cm) (Ethibond). This higher suture retention of Fiber-Tape compared with other tested sutures remained significant (P<.05) during the entire observation period—4.4 N/cm (SD, 2.1 N/cm) after 6 weeks; 10.1 N/cm (SD, 5.1 N/cm) after 16 weeks; and 12.8 N/cm (SD, 6.0 N/cm) after 22 weeks (Figure 2, Table 3).

Suture–tendon pullout strength. The tendon pullout strength for the 4 different suture materials during 22 weeks. Standard deviation is provided in Table 3. There was significantly (P<.05) higher retention of FiberTape compared with other tested sutures. Until week 16, a significantly (P>.002) increasing suture hold of all sutures except Orthocord was seen.

Figure 2:

Suture–tendon pullout strength. The tendon pullout strength for the 4 different suture materials during 22 weeks. Standard deviation is provided in Table 3. There was significantly (P<.05) higher retention of FiberTape compared with other tested sutures. Until week 16, a significantly (P>.002) increasing suture hold of all sutures except Orthocord was seen.

Summary of Pullout Strength for the 4 Types of Suture

Table 3:

Summary of Pullout Strength for the 4 Types of Suture

Overall, univariate analysis revealed a significantly (P>.002) increasing suture hold of all sutures except Orthocord until week 16. The difference between week 16 and week 22 was not significant for all types of sutures. Furthermore, there was no significant difference between Ethibond, Orthocord, and FiberWire at any tested time point.

This difference and higher suture retention forces of FiberTape was even more significant (P<.01) in the suture–bone pullout testing, which was only performed after 22 weeks. FiberTape showed a pullout strength of 31.8 N/cm (SD, 18.1 N/cm), followed by Ethibond showing 6.7 N/cm (SD, 3.9 N/cm), Orthocord showing 3.1 N/cm (SD, 1.3 N/cm), and FiberWire showing 3.0 N/cm (SD, 1.6 N/cm) (Figure 3).

Suture–bone pullout strength after 22 weeks. FiberTape showed pullout strength that was significantly (*P<.01) higher than that of the other sutures.

Figure 3:

Suture–bone pullout strength after 22 weeks. FiberTape showed pullout strength that was significantly (*P<.01) higher than that of the other sutures.

Histological Assessment

Capsule. In all suture materials, the formation of an inner and an outer capsule was observed. The inner capsule was concentric around the suture and consisted of organized fibers and various cells. The outer capsule was always less organized and in cross-section rather spindle shaped, so that it had been integrated into the surrounding tissue. In addition, it often contained numerous blood vessels. Over time, the outer capsule increased and showed integration in the surroundings. In Ethibond, FiberTape, and FiberWire, the thickness of the inner capsule decreased over time, but this finding was not significant. The thickest inner capsule was seen after 6 weeks in FiberWire (mean, 304±142 µm), decreasing to 215±56 µm after 22 weeks. With Orthocord, because there was no contact between the suture and the surrounding tissue after 16 weeks and just an outer capsule after 22 weeks, it was not possible to evaluate the thickness over the period (Figure 4).

Orthocord. At week 16, suture surrounded with muscle tissue. There was little tissue reaction and no measurable inner capsule (a). At week 22, sutures were separated in filaments with numerous inflammatory cells and multinuclear giant cells (red arrows). Black arrows are in the area of polydioxanone suture material, which is in resolution (b).

Figure 4:

Orthocord. At week 16, suture surrounded with muscle tissue. There was little tissue reaction and no measurable inner capsule (a). At week 22, sutures were separated in filaments with numerous inflammatory cells and multinuclear giant cells (red arrows). Black arrows are in the area of polydioxanone suture material, which is in resolution (b).

For FiberWire, a preparation after 6 and 22 weeks showed a space between the inner and the outer capsule. Both FiberTape and FiberWire were covered by a large external capsule after 22 weeks (Figure 5). In Ethibond, there was a clear space after 16 weeks with an epithelial-like surface (Figure 6).

FiberTape. At week 6, multinuclear giant cells (black arrows) close to the suture and numerous inflammatory cells in the suture (red arrows) (a). At week 22, inner capsule (arrows) with variable thickness around the irregular surface texture of the suture (b).

Figure 5:

FiberTape. At week 6, multinuclear giant cells (black arrows) close to the suture and numerous inflammatory cells in the suture (red arrows) (a). At week 22, inner capsule (arrows) with variable thickness around the irregular surface texture of the suture (b).

Ethibond. At week 6, inner capsule (*) and external capsule (**) with unorganized tissue and numerous vessels (a). At week 16, dissection of the inner and the outer capsule, covered by an epithelioid tissue (arrows). Well-organized surrounding tissue (b).

Figure 6:

Ethibond. At week 6, inner capsule (*) and external capsule (**) with unorganized tissue and numerous vessels (a). At week 16, dissection of the inner and the outer capsule, covered by an epithelioid tissue (arrows). Well-organized surrounding tissue (b).

Tissue Reaction and Maturity

Regarding tissue reaction, the cell measurement for multinucleated giant cells, monocytes, polymorphonuclear neutrophils, and vessels did not show significance in one direction or the other over time (Table 4).

Summary of Histological Data for the 4 Types of Suture

Table 4:

Summary of Histological Data for the 4 Types of Suture

The maturity of the surrounding connective tissue increased over time with all suture materials. At 22 weeks, all tissue samples showed predominantly fibroblasts with loosely well-oriented fibers. After 16 and 22 weeks, Ethibond showed a significantly higher maturity than Orthocord (P=.022 and P=.038). Otherwise, there was no significant difference regarding maturity between the suture types.

Cell and Tissue Invasion

Regarding cell invasion, in all samples except FiberTape, the invasion of cells was rising from 6 to 22 weeks (Table 4). However, this cell invasion was significant only for FiberWire (1.7±0.6 vs 3.0±0.0, P=.037). After 22 weeks, a biodegradation of the polydioxanone suture portion with accumulation of various inflammatory and polynucleated giant cells could be seen around Orthocord (Figure 4). Ethibond showed a significantly weaker cell invasion after 22 weeks compared with FiberTape (P=.047), FiberWire (P=.047), and Orthocord (P=.038)

Correlation Between Histological Findings and Biomechanical Properties

There was a strong correlation between tissue maturity of the surrounding tissue and pullout strength (r=0.84, P=.001). There was no linear relationship among pullout strength, thickness of the capsule, number of vessels, multinucleated giant cells, monocytes, polymorphonuclear neutrophils, and the cell invasion.

Discussion

Significantly increasing pullout strength of all sutures was shown until week 16, with a histologically increasing maturity of the tissue. FiberTape had the highest pull-out strength at 6, 16, and 22 weeks—4.4 N/cm (SD, 2.1 N/cm), 10.1 N/cm (SD, 5.1 N/cm), and 12.8 N/cm (SD, 6.0 N/cm), respectively. However, general pull-out strength at 22 weeks was surprisingly low, particularly for Ethibond, Orthocord, and FiberWire. In comparison, FiberTape showed the highest hold in the tissue, and this increased over time. Histologically, it showed a trend for highest tissue maturity after 22 weeks, also more than FiberWire, with significantly different mechanical hold for FiberWire and FiberTape. Interestingly, as FiberTape and FiberWire are made from the exact same material, the structural form seems to determine the histological pattern and consequently the biomechanical hold. Despite the superior biomechanical properties of FiberTape, early results do not seem to show an effect on re-tear rate at 6 months postoperatively.18 However, a favorable effect in the long-term is not excluded.

Previous studies have described the characteristics of nonabsorbable sutures, but there is little known about the functional tissue response to these sutures.19–21 The authors' hypothesis was that various suture materials would have a different histological response regarding the tissue in- or on-growth, determining the biomechanical hold. In the repair of soft tissue it might be of considerable biomechanical advantage if, after completion of the initial healing process, nonabsorbable suture material permanently enhances the tissue quality (eg, in a rotator cuff repair) by in-growth of the suture material into the surrounding tendon.

In all types of suture material, an inner and an outer capsule were observed, which consisted of organized fibers and various cells. The clear space between the inner and the outer capsule was detected several times, particularly in Ethibond and FiberWire (Figure 6). A similar effect was described in 1970 by Postlethwait22 in a study with rabbits. The reason could be the various viscoelastic properties of the different types of sutures.23,24

Over time, the inner capsule decreased in size and the outer capsule was integrated into the surrounding tissue. This was consistent with the report by Huggins et al.25

Other research has focused on novel strategies for optimal surface design of textile implants with the above-described motivation, using submicron-diameter electro spun fibers as an outer cover of tissue augmentation patches.26 A combination of such a surface with an appropriate macro structure may be a promising design strategy to achieve long-term tissue augmentation with the implanted sutures.

This study had some limitations. Despite the relatively large number of animals involved, the variability of the results was too great to reach broad statistical significance. It is also unclear whether the histological and biomechanical response would have been different if the suture loop had been knotted with tension, which is normally the case in rotator cuff repair.

Further, the comparison of histological and mechanical variables at the same time is, to the authors' knowledge, unique in the setting described. Because FiberTape will possibly change its cross-sectional shape in a narrow canal (eg, due to folding), the authors refrained from attempting to normalize the surface of the suture; however, it is obvious that the larger surface of FiberTape is a relevant factor. Further, the quality of the tissue samples was not homogeneous. Some sutures were separated from the tissue during the histological processing, which was unexpectedly challenging with high-strength suture material and which limited the number of histological samples analyzed. Another limitation was that the authors do not have definitive proof for the described failure mechanism, although the histological findings were highly suggestive. Future detailed analysis of the surface of mechanically retrieved suture material after testing and histology of the sutures in the bone tunnel has to be considered.

Conclusion

FiberTape had the highest pullout strength, and the overall maturity of the surrounding tissue seems to be correlated with mechanical performance. For Ethibond, Orthocord, and FiberWire, the authors found an unexpected circumferential space around the sutures, often forming an inner and an outer capsule, separating the sutures from the surrounding tissue with a shifting layer.

References

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Characteristics of the 4 Types of Suture

SutureUSP No.MaterialCoatingStructureBioabsorbabilityManufacturer
Ethibond2Poly/-ethylene terephthalatePolybutilateBraidedNonabsorbableEthicon, Somerville, New Jersey
Orthocord262% Polydioxanone 38% HMWPE90% Caprolactone 10% GlycolideBraidedNonabsorbableDePuy Mitek, Raynham, Massachusetts
FiberWire228% Polyester 72% HMWPESiliconBraidedNonabsorbableArthrex, Naples, Florida
FiberTape28% Polyester 72% HMWPESiliconBraided, tape 2-mm wideNonabsorbableArthrex, Naples, Florida

Classification of the Maturity of Connective Tissuea

ClassDescription
0Immature tissue with many fibroblasts and very few or none fibrocytes, fibers undirected
1Fibroblasts predominantly, tissue loosely oriented
2Fibrocytes predominantly, well-oriented fibers, densely packed
3Mature tissue, fibroblasts at most isolated, very dense, well-oriented fibers with few fibrocytes in between

Summary of Pullout Strength for the 4 Types of Suture

StrengthSuture Type, N/cm

FiberTapeFiberWireEthibondOrthocord
Suture–tendon
  Week 0a
    Mean0.70.20.20.2
    SD0.30.10.10.1
  Week 6b
    Mean4.42.01.22.5
    SD2.11.10.51.3
  Week 16b
    Mean10.15.05.23.1
    SD5.12.61.91.9
  Week 22b
    Mean12.86.75.64.2
    SD6.04.12.62.3
Suture–bone
  Week 22b
    Mean31.83.06.73.1
    SD18.11.63.91.3

Summary of Histological Data for the 4 Types of Suture

Cell/TissueSuture Type, Meana

FiberTapeFiberWireEthibondOrthocord
Inner capsule thickness, µm
  Week 6215 (3)305 (2)187 (2)172 (2)
  Week 16200 (2)230 (1)139 (3)31 (2)
  Week 22146 (3)215 (3)98 (3)250 (1)
Blood vesselsb
  Week 64.33 (3)1.3 (3)4.3 (3)4.5 (2)
  Week 162 (1)2 (1)2.7 (3)NA
  Week 223.3 (3)2.3 (3)2.7 (3)2.5 (2)
Polymorphonuclear neutrophilsb
  Week 66 (3)2.7 (3)6.3 (3)11.5 (2)
  Week 167 (1)2 (1)3.7 (3)NA
  Week 223 (3)5 (3)5.3 (3)3.5 (2)
Multinucleated giant cellsb
  Week 65.3 (3)1 (3)2.7 (3)4 (2)
  Week 161 (1)4 (1)0.7 (3)NA
  Week 222.3 (3)2.7 (3)1.3 (3)8.5 (2)
Cell invasionc
  Week 62.7 (3)2 (4)2.5 (4)3 (2)
  Week 163 (1)1 (1)3.7 (3)3.7 (3)
  Week 223 (3)4.3 (3)3.3 (3)5 (2)
Maturity of surrounding tissued
  Week 60.8 (3)0.3 (3)0.3 (2)0.8 (2)
  Week 161.5 (2)1.0 (1)1.2 (3)0.2 (3)
  Week 221.7 (3)1.3 (3)1.6 (3)1 (2)
Authors

The authors are from the Department of Orthopaedic Surgery, University Hospital Balgrist, University of Zurich (DCM, AH, SW, CG, KW), the Musculoskeletal Research Unit (KN, MCB), and the Center for Applied Biotechnology and Molecular Medicine, Department of Molecular Mechanisms (MCB), Vetsuisse Faculty, University of Zurich, Zurich, Switzerland.

Drs Meyer and Hasler contributed equally to this work and should be considered equal first authors.

The authors have no relevant financial relationships to disclose.

Correspondence should be addressed to: Anita Hasler, MD, Department of Orthopaedic Surgery, University Hospital Balgrist, Forchstrasse 340, 8008, Zurich, Switzerland ( anita.hasler@balgrist.ch).

Received: January 17, 2019
Accepted: April 03, 2019

10.3928/01477447-20190424-09

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