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Abstract
Inhibition of axonal outgrowth accompanied by neuroma formation appears in microsurgical nerve repair as reaction to common microsuture materials like silk, nylon, or polyglycolic acid. In contrast, recent findings revealed advantages of spider silk fibers in guiding Schwann cells in nerve regeneration. Here, we asked if we could braid microsutures from native spider silk fibers. Microsutures braided of native spider dragline silk were manufactured, containing either 2 × 15 or 3 × 10 single fibres strands. Morphologic appearance was studied and tensile strength and stress-strain ratio (SSR) were calculated. The constructed spider silk sutures showed a median thickness of 25 µm, matching the USP definition of 10-0. Maximum load and tensile strength for both spider silk microsutures were significantly more than 2-fold higher than for nylon suture; SSR was 1.5-fold higher. All values except elasticity were higher in 3 × 10 strand sutures compared to 2 × 15 strand sutures, but not significantly. In this pilot study, we demonstrate the successful manufacture of microsutures from spider silk. With regards to the mechanical properties, these sutures were superior to nylon sutures. As spider silk displays high biocompatibility in nerve regeneration, its usage in microsurgical nerve repair should be considered. © 2011 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 2011.
INTRODUCTION
1. Top of page
2. Abstract
3. INTRODUCTION
4. MATERIALS AND METHODS
5. RESULTS AND DISCUSSION
6. Acknowledgements
7. REFERENCES
One of the major problems in neurosurgery is neuroma formation, which often results in neuropathic pain that can be unbearable for the patient. Neuromas are caused by irritation of nerve fibers following transection or scar formation due to inflammation, fibrosis, and foreign body reaction (FBR).1–4 FBR and fibrosis have been found to interrupt the continuity of the axon and thus deflect the growth of the proximal regenerating axon.5 If the regenerating axon sprouts do not reach and elongate through the trophic distal Schwann cell tube, they will grow in a more random manner and can form a neuroma. This occurs frequently after traumatic peripheral nerve injury including limb amputation. The axonal sprouts within the bulbous neuroma show increased mechano- and chemosensitivity.1 These hyperexcitability changes are often associated with paraesthesia and painful events including phantom limb in the case of limb amputation. Interestingly, sensory neurons show distinct changes in sodium and potassium channels on their cell bodies and axons after nerve injury.2, 3 Neuromas are painful and can reduce patients' quality of life, the usual management of neuromas is neurotomy to dampen excitability in the neuroma.4 This can be gained either pharmacologically, i.e. injection of local anaesthetics directly into the neuroma or surgically by excision of the neuroma.
Neuroma formation can be influenced by the material of suture fibers used in nerve repair, which can induce granuloma formation as well as invasion of immune cells and connective tissue.6, 7
To improve nerve repair, efforts have been made concerning suture techniques, for example, either perineurial, epineurial, periepineurial, end-to-side suture, or use of tubules, either made of silicone or collagen around the lesion.8, 9 Others promoted the use of carbon-dioxide laser or adhesives, for example, mostly fibrin glue, instead of microsurgical repair.6, 7, 10, 11 An advantage is that adhesives provide an atraumatic and faster coaptation, if compared to traditional microsuture.
Few studies have investigated the influence of the suture material itself. Efforts in search for an alternative material resulted even in the use of human hair.12 But again, granulomatous inflammation could be observed, although autologous hair was used.
Another interesting study dealt with ultrastrong polyethylene as microsuture material, which also fulfilled some requirements of microsurgical suture material. Nevertheless, it was used in ophthalmic surgery, where no immunological reactions occur due to the lack of immune cells in the cornea.13
While nearly every suture material results in granuloma formation, giant cell invasion and fibrosis,7, 14–16 nylon suture caused less FBR than other materials, thus becoming the gold standard in microsurgical nerve repair. The nomenclature of the subtypes of nylon follows its chemical composition with a numerical suffix specifying the numbers of carbons donated either by the diamine and the diacid monomers or by caprolactam, respectively.
Thus, the most commonly used nylons are nylon 6,6, which was also the first nylon developed, and nylon 6.
Nylon 6,6 or polyamide 6,6, according to its chemical composition poly(hexamethylneadipamide), is composed of two structural units connected via condensation polymerization.17 The monomers are the residues of hexamethylendiamine (1,6-diaminohexane, H2N(CH2)6NH2) and adipic acid (hexane-1,6-dicarboxylic acid, HOOC(CH2)4COOH). Since each monomer in this copolymer has the same reactive group on both ends, the direction of the amide bond reverses between each monomer. As a result, the polymerization process results in directionality from N-terminal to C-terminal, unlike natural polyamide proteins which have overall directionality from C-terminal to N-terminal. Nylon 6 or poly(6-caprolactam) is a homopolymer formed by ring-opening polymerization of a single structural unit, namely the apparent residue of caprolactam (6-aminocaproic acid, H2N(CH2)4COOH).17 The peptide bond within the caprolactam is broken with the exposed active groups on each side being incorporated into two new bonds as the monomer becomes part of the polymer backbone. In this case, all amide bonds lie in the same direction. While the use of either silk or nylon in peripheral nerve microsurgery has not been questioned according to the dates of the latest publications dealing with comparisons of different materials, we asked if we could outline the use of alternative materials. In this study, we used spider dragline silk, which has been described as a high-performance fiber with an excellent combination of tensile strength and light-weight.18 Its biocompatibility has been recently described19, 20 and, additionally, we could show its ability to promote nerve regeneration.21, 22 We used a commercially available nylon suture (Ethilon 10-0®, Ethicon, Germany, Norderstedt Germany), chemically composed equally of nylon 6 and nylon 6,6, as control, which is the common gold standard in peripheral nerve surgery.
MATERIALS AND METHODS
1. Top of page
2. Abstract
3. INTRODUCTION
4. MATERIALS AND METHODS
5. RESULTS AND DISCUSSION
6. Acknowledgements
7. REFERENCES
Animal handling
Spiders were held in rooms of our local animal facility and were fed three times a week with crickets. The webs were sprayed with tap water daily. Only female adults of Nephila spp. with an age ranging between 3 and 12 month after the last molt were used. After harvesting the silk, spiders were fed an extra time and received some water with a tooth brush.
Rearing of the silk
According to the German Animal Welfare Law as well as the European Directives, spiders as invertebrates do not need special allowances like vertebrate animals. Additionally, the silking is a physiological process for the spider, so no animals were harmed. For rearing of the silk, the spiders were fixed on styropore cubes with a gauze and pin needles without use of anesthesia. For silking, a method previously described has been used with modifications.23 Briefly, spiders were immobilized by coverage of gauze fixed with small needles to a styropor cube (Figure 1, arrow). Silk was pulled out of the major ampullate gland, which is the adequate stimulus for production. Fibers were reared on a device of 30 cm in diameter (asterisk), which was mounted on a motorized drum (Figure 1).
Figure 1. Apparatus for harvesting spider silk. Displaying machine used for harvesting spider silk. Spiders were fixed on styropore cube (arrow), fixed, and spider silk fibers were pulled out manually and guided to the rearing device (asterisk). Bundles of either 10 or 15 spider silk fiber, i.e. strands, were then transferred to the braiding apparatus in Figure 2. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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Braiding of the silk fibers
Sutures were defined as consisting of different strands, i.e. bundles of fibers, either 2 strands of 15 turns or 3 strands of 10 turns, respectively (Table I). For the braiding of the silk, a miniature machine was originally designed and constructed in which up to seven strands can be braided to a suture (Figure 2, arrow). On one side the strands were fixed [Figure 2(A), marking I], on the other side the free ends were taken together and also fixed [Figure 2(A), marking III]. The strands were fixed between a device and a bolt, which were fastened tightly by a setscrew [Figure 2(B), on the right]. All free ends rotated consensual while the pooled end turned in the opposite direction. In this manner, we could prevent a too strong eccentricity. The velocity of the drilling could be set with a computer-assisted control unit using a simple program exclusively written for that purpose [Figure 2(A), marking IV]. To prevent a random drill in the suture, a carriage with seven holes in equal distances was used to guide the strands [Figure 2(A), marking II]. This carriage was versatile to determine the angle in which the strands were put together. For the manufacture of the suture, the strands were brought together with an angle between 25° and 35° against the horizontal [Figure 2(B), arrow]. Optimum tightness and thickness were evaluated with scanning electron microscopy (SEM); nylon sutures of a standardized United States Pharmacopeia (USP) thickness of 10-0 were referred to as a reference for the thickness.
Table I. Definition of the Nomenclature of SuturesSuture A braided combination of either two strands or three strands consisting of either 10 or 15 single fibres
Strand A bundle of either 10 or 15 single fibers, reeled on the motorized apparatus for the forcible silking
Fibre A single spider silk fiber directly harvested out of the spinneret
Figure 2. Braiding apparatus used for braiding of spider silk fibers. Strands of either 10 or 15 spider silk fibers were braided to form braided microsutures. A: Displaying machine and setting used for drilling of single strands to a braided suture. I: Demonstrating device, where the ends of the strands are attached. II: Versatile Carriage for guiding the strands. III: Device, with the strands brought together as braided suture is attached. IV: Computer-assisted control unit for the setting of the drilling speed. B: Detailed view of the device, with the strands brought together as braided suture is attached (arrow). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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Scanning electron microscopy
From each sample, 1 cm was coated with gold using an argon sputter (SEM Coating System (Polaron, East Grinstead, United Kingdom). Specimen were fixed in a vacuum and viewed via SEM (SEM500, Philips, Hamburg, Germany) in magnifications ranging from 20× to 400× at a voltage of 10 kV, visualized by scanning with 1000 lines in horizontal per picture and 32 ms scanning time per picture, resulting in a resolution of 1333 × 1000 pixel. As the drill of the sutures was tendentielly loose directly after the manufacturing process resulting in occurrence of spaces between the strands, sutures were glued to both sides of the specimen devices. In this manner, certain tightness comparable to the tightness of a knotted suture in situ could be achieved.
Mechanical tests
The mechanical testing was implemented with a spring balance and a ruler. Original length L0L1 was defined as length of the suture at a load of 0 N, L1 w was defined as length of the suture at maximum load before the suture was torn apart. Length variation ?L was calculated using formula (1).
* equation image(1)
Elasticity was stated as relative elongation e and was calculated using formula (2)
* equation image(2)
Tensile strength s was defined as maximum load F before the suture was torn apart divided by the cross sectional area A, which was calculated using 25 µm as mean diameter with formula (3).
* equation image(3)
As we could not define the holding of Hooke's Law as the appearance of either elastic or plastic deformation could not clearly be figured out with this measurement setting. Thus we calculated the stress-strain ratio (SSR) by dividing tensile strength s as obtained by formula (3) by relative elongation e as obtained by formula (2). The formula used for calculating SSR was formula (4).
* equation image(4)
All experiments were carried out at five times in duplicates derived by cutting the samples in two parts to compensate intra-individual mechanical variability in one sample, thus obtaining a sample size of n = 10.
Statistical analysis
For each value, mean and standard deviation have been calculated. As high variances occurred, random distribution of the samples has been checked by analysis of variance. The non-parametric Kruska-Wallis test has been applied for the trueness of the null hyptothesis with n = 10 and two degrees of freedom. Differences between the samples were stated as significant or high significant if probability p for type I error, i.e. erroneously reject the null hypothesis, was below 0.05 or 0.01, respectively.
RESULTS AND DISCUSSION
1. Top of page
2. Abstract
3. INTRODUCTION
4. MATERIALS AND METHODS
5. RESULTS AND DISCUSSION
6. Acknowledgements
7. REFERENCES
Rearing and braiding of the silk
Spider silk was harvested as a single fiber pulled out from the major ampullate silk gland (Figure 1, arrow). The amount of harvested silk was defined as number of turnings of the rearing device (Figure 1, asterisk) used for winding up the silk fiber. For each suture of either 2 × 15 or 3 × 10 single fibers, a different spider was used to minimize variability in thickness of fibers, as would occur by excessive harvesting of one single spider due to protein loss and subsequent decrease in silk production (data not shown).
Higher numbers of turns, i.e. more single fibers per strand, resulted in sutures thicker than 30 µm and thus thicker than the reference nylon suture. The strands could be taken off easily from the rearing device, which resulted in a slight contraction of the strand, probably caused by the pull needed to stimulate the ampullate gland to produce silk.23 With the braiding apparatus, we could manufacture braided sutures by braiding either two or three strands of either 15 or 10 single fibers, respectively, around each other. The angle of 25°–35° against the horizontal [Figure 2(B), arrow] resulted in a harmonic coiling and a smooth, moldable suture, while broader angles resulted in a too loose braiding with the strands barely entwining each other (data not shown). Sharper angles resulted in insufficient braided, tight sutures with enharmonic twisting (data not shown).
SEM of the braided suture
Manufactured silk sutures showed a braided suture with the strands entwining each other in a regular pattern, leaving just small spaces between the single fibers. Figure 3(A) depicts a representative sample of a loose suture, which was slightly thicker than the tightened sutures used in this study. The sample viewed here, however, was selected due to its harmonic twist and its regular pattern. It is possible to track each strand in every second or third coil, displaying a regular braiding pattern. Figure 3(B–D) shows the tightened sutures glued to the specimen device in more detail, which could be scaled to a thickness of 30 µm. In contrast to our manufactured samples, the commercially available nylon suture 10-0 displays a monofilament structure, revealing a uniform smooth surface. All tightened suture samples are around 20–30 µm thick, matching the USP definition of 10-0 suture.
Figure 3. Morphological appearance of braided spider silk sutures. A: SEM of a braided suture, 3 × 10 single strands, not glued to the specimen device and thus not tightened, appearing slightly thicker than the used samples; magnification ×75, scale bar represents 100 µm; B: SEM of a braided suture glued to the specimen device and thus tightened, 2 × 15 single strands, thickness and tightness of drill are representative for the used samples; magnification ×206, scale bar represents 40 µm; C: SEM of a braided suture glued to the specimen device and thus tightened, 3 × 10 single strands, thickness and tightness of drill are representative for the used samples; magnification ×503, scale bar represents 20 µm; D: SEM of a nylon suture, magnification ×1010, scale bar represents 10 µm.
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Mechanical results
Spider silk sutures showed a high maximum load with a median of 0.7 ± 0.2 (SD) N for 2 × 15 single strands or 0.8 ± 0.3 (SD) N for 3 × 10 single strands, which is more than two-fold greater than that of nylon, that is, 0.3 ± 0.02 (SD) N with a high significance (p < 0.01). However, the differences between the two different spider silk samples were not statistically significant (p > 0.05). The values for elasticity were slightly smaller in the spider silk samples than that of nylon, that is, 23.2 ± 1.8 (SD) % (nylon) compared to 17.5 ± 4.8 (SD) % for 2 ×15 single strands or 16.6 ± 2.9 (SD) % for 3 × 10 single strands, respectively (data not shown). Here, the differences were significant for 2 × 15 strands versus nylon (p < 0.05) or high significant for 3 × 10 strands versus nylon (p < 0.01), respectively. Again, no significant differences could be found between spider silk samples (p > 0.05). Tensile strength was also higher than that of nylon, with a value of 0.7 ± 0.2 (SD) MPa for 2 × 15 strands or 0.8 ± 0.3 (SD) MPa for 3 × 10 single strands, respectively, versus 0.3 ± 0.03 (SD) MPa [Figure 4(A)]. Differences were high significant between 2 × 15 strands versus nylon (p < 0.01) or significant between 3 × 10 strands versus nylon (p < 0.05). No significance could be observed between spider silk samples (p > 0.05). SSR was calculated to 0.13 ± 0.03 (SD) MPa for 2 × 15 single strands or 0.13 ± 0.05 (SD) MPa for 3 × 10 single strands and again was higher than that of nylon [0.08 MPa ± 0.007 (SD) MPa] [Figure 4(B)]. Significance could be shown between 2 × 15 strands versus nylon (p < 0.05), but neither between 3 × 10 strands versus nylon nor between spider silk samples (p > 0.05).
Figure 4. Mechanical properties of braided spider silk sutures compared to nylon. A: Comparison of the tensile strength of 2 × 15 silk strands, 3 × 10 silk strands or nylon suture. B: Comparison of the SSR of 2 × 15 silk strands, 3 × 10 silk strands or nylon suture. Error bars indicate standard deviation, asterisks mark significance level p < 0.05.
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Discussion of findings
We could achieve a braided microsurgical suture of native spider silk fibers, so the aim of the study could be met. Loose sutures were around 40–50 cm long and around 35–50 µm thick, probably due to the small spaces between the braided single strands as well as between the single fibers of a strand. This could be proven by tightening of the sutures, which resulted in a thickness of 20–30 µm, which was achieved by decrease of the spaces as well as actual decrease of the diameter according to the extension, which has also been described.24 This thickness is comparable to a USP 10-0 nylon suture, which is around 25 µm thick, but for further comparisons between the two suture materials it has to be taken into concern that, due to its monofilament structure, no spaces between single strands or fibers exist in nylon suture. The mechanical properties of the braided spider silk sutures were superior to those of nylon, what could be expected by the strength of single spider silk fibers described in literature,18 with a maximum load and a tensile strength both more than two-fold higher and also a 1.5-fold higher SSR. Except SSR of 3 × 10 strands spider silk samples versus nylon, all differences were significant with a p-value < 0.05. It has to be considered that the measurement setting we used was not the gold standard of a computer-assisted dynamical mechanical analysis setting as it is used in specialized institutes; however mechanical dimension, i.e. extremely low variances of industrially produced nylon compared to high variances of naturally derived spider silk, could be reproduced correctly.
A high tensile strength has been described as an advantage for microsuture materials.13 The last finding in particular explains that a higher tension per cm relative elongation is possible, indicating a better energy absorbance. The unique nanostructural alignment of the spider silk's proteins, i.e. the dynamic alignment of the highly organized antiparallel beta-sheet crystals and the less orderly semiamorphous, glycine-rich phase, displays a distinct stress–strain curve.25 Loading with smaller stress values results in a large strain in spider silk fibrils, whereas loading with higher stress values leads to nanostructural conformational changes leading to a high stiffness. This suggests that for a small strain, a very high stress has to be loaded.
Nevertheless, the most obvious problem of our sutures is the variances of the single fibers, as native spider silk is a naturally produced material, which underlies inter- and even intra-individual differences macroscopically and ultrastructurally, depending on the amount of harvested silk, but also temperature, pH, and humidity.24, 26–28 We tried to keep the silking as standardized as possible regarding these conditions, while the amount of the reared silk was kept small to avoid too strong variances of the fibers. Analyzing the SEM of the manufactured sutures and the single fibers in particular, a sufficient similarity in thickness could be met [Figure 3(A–C)].
Future directions concerning usage of spider silk as suture
The manufacturing process of spider silk suture material could hardly produce as small tolerances as an industrial produced nylon suture. Another disadvantage was the fact that a braided suture usually damages the nerve more than a monofil suture; the irregular surface tears bigger holes in the epineurium than the sliding of the smooth surface of a monofil suture. However, the manufactured spider silk suture had the ability to mould, which could be displayed by the change in diameter by tightening the suture, indicating that the suture would preferentially mould itself rather than tear holes in the epineurium. On the other hand, a braided structure offers a higher surface area with a more niche-like structure, providing superior possibilities for cells, i.e. Schwann cells, to adhere.
Spider silk was shown to have a very good cyto- and biocompatibility in studies concerning subcutaneous implantation as well as usage of recombinant spider silk protein as wound dressing19, 20, 23, 29 and also to act as an effective matrix and guidance structure for nerve regeneration by our work group.21, 22 Recently, an interesting study has been published which described the modulation of cell growth after exposure to different types of silk, i.e. two silk-worm silks and spider-silk egg sac silk as well as exposure to conditioned media incubated with these silks.30 Spider silk exposure as well as exposure to spider silk conditioned medium silk showed significantly less inhibitory effect on cell growth than one silkworm silk, indicating further investigations concerning the chemotactic effects on silk and spider silk, in particular. Moreover, besides the potential to act as an allergen, silks have proven their high antimicrobial properties, suggesting their use for medical application.31 These antimicrobial potential may lead to lower infection rates in peripheral nerve surgery, which is often caused by trauma and thus offering septic wound conditions. Additionally, recombinant spider silk displayed a very low pyrogenicity, giving further indication concerning its use in trauma surgery, where sepsis is a common problem.31 As spider silk sutures showed mechanical properties at least more than 1.5-fold higher than those of nylon sutures, it seems presumable that during the degradation process mechanical stability may remain extant that hold certain strength. Therefore, spider silk sutures may be a promising alternative to conventional suture materials in microsurgery and neurosurgery in particular. Further studies should also deal with antimicrobial properties of native spider silk fibers as well as determine exact stress–strain curves to verify the promising mechanical promises of this pilot study.
Acknowledgements
1. Top of page
2. Abstract
3. INTRODUCTION
4. MATERIALS AND METHODS
5. RESULTS AND DISCUSSION
6. Acknowledgements
7. REFERENCES
The authors thank Wilhelm Behnsen, Friedbert Gellermann, and Thorleif Hentrop for excellent technical advice and help in the design, construction, and usage of the braiding apparatus. They are also grateful to Hossein Hidaji for superb care and breeding of the spiders.
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2. Abstract
3. INTRODUCTION
4. MATERIALS AND METHODS
5. RESULTS AND DISCUSSION
6. Acknowledgements
7. REFERENCES
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Hakimi O, Gheysens T, Vollrath F, Grahn MF, Knight DP, Vadgama P. Modulation of cell growth on exposure to silkworm and spider silk fibres. J Biomed Mater Res A 2010; 92: 1366.
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