Journal of Surgical Research 167, e157–e162 (2011)doi:10.1016/j.jss.2009.11.710

Cyanoacrylate Glue for Intra-abdominal Mesh Fixation

of Polypropylene-Polyvinylidene Fluoride Meshes in a Rabbit Model

Roland Ladurner, M.D.,*,1 Inga Drosse, M.D.,* Dominik Burklein, M.D.,* Wolfgang Plitz, M.D., Ph.D.,†Gregor Barbaryka, M.D.,‡ Chlodwig Kirchhoff, M.D.,* Sonja Kirchhoff, M.D.,§ Wolf Mutschler, M.D., Ph.D.,*

Matthias Schieker, M.D., Ph.D.,* and Thomas Mussack, M.D., Ph.D.*

*Department of Surgery Innenstadt; †Department of Orthopaedics Großhadern; ‡Department of Pathology Innenstadt; and§Department of Radiology Großhadern, University of Munich (LMU), Munich, Germany

Submitted for publication July 18, 2009

Background. Cyanoacrylate glues are tissue adhe-sive with high adherent and hemostatic properties.The aim of this study was to evaluate the efficacy ofcyanoacrylates glue for polypropylene-polyvinylidenefluoride (PP-PVDF) intraperitoneal onlay mesh(IPOM) fixation in a rabbit model.

Materials and Methods. In 40 New Zealand whiterabbits, three pieces (3 3 3 cm) of a PP-PVDF mesh(n [ 120) were fixed in IPOM technique on both sidesof a midline laparotomy. For mesh fixation we used spi-ral tacks, nonabsorbable sutures, or cyanoacrylateglue in a randomized manner. All animals were killedafter 12 wk. The prosthetic materials were exciseden bloc with the anterior abdominal wall for evaluationof the tensile strength and histologic analysis. Resultsare presented as mean and standard deviation.

Results. Meshes fixed with glue showed a signifi-cantly higher tenacity of adhesions (2.75 ± 0.97) com-pared with those with tacks (2.44 ± 0.97 sutures versus1.91 ± 0.92 tacks). The percentage of adhesions in theglue group was comparable to the suture group(36.50% ± 27.60% glue, 37.62% ± 27.36% suture). The ten-sile strength of stapled and sutured meshes was signif-icantly higher than the tensile strength glued mesh(14.15 ± 0.97 N suture versus 14.84 ± 0.74 stapler versus9.64 ± 0.78 N glue). Mesh shrinkage was irrespective ofthe fixation technique. The inflammation reactionwas more pronounced in the glue group.

Conclusions. Although cyanoacrylate glue showeda considerable cellular ingrowth in this rabbit model,sutures and tacks proved to be superior for IPOM

1 To whom correspondence and reprint requests should be ad-dressed at Department of Surgery Innenstadt, University of Munich(LMU) Nussbaumstrasse 20,D-80336 Munchen, Germany. E-mail:Roland.Ladurner@med.uni-muenchen.de.

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fixation of PP-PVDF meshes in terms of tensilestrength. � 2011 Elsevier Inc. All rights reserved.

Key Words: laparoscopic incisional hernia repair;cyanoacrylate glue; tensile strength; intra-abdominaladhesion; mesh fixation.

INTRODUCTION

Since the first report of laparoscopic ventral herniarepair in 1991 [1], numerous studies and publicationsare propagating the advantages of the minimal inva-sive technique [2–5]. The standard technique of laparo-scopic ventral hernia repair is covering the fascialdefect with a nonabsorbable mesh with a minimal over-lap of 3–5 cm. The recurrence rate of laparoscopic ven-tral hernia repair varies between 2% and 6.5% [6–9].The current gold standards for mesh fixation are trans-fascial suture, nitinol anchors, spiral tacks of titanium,or absorbable stapler. Fixation of the implants is gener-ally required until the mesh is well integrated intothe abdominal wall and to prevent internal herniationbetween the mesh and the peritoneum. One majordrawback of this procedure is the increased incidenceof persistent pain. One possible explanation may bethat any kind of fixation device entraps intercostalnerves, causes muscle ischemia, or leads to local hema-toma. This theory is supported by the fact that localanesthetics and tying the knots gently help to relievethe suture site pain [10]. Another possible mechanismis the adhesion of the viscera with the implantedmesh or the fixation devices with the possibility ofbowel obstruction, fistulas, and chronic abdominalpain. Finally, mesh contraction, which is thought tobe the outcome of the host tissue reaction to the type,

0022-4804/$36.00� 2011 Elsevier Inc. All rights reserved.

7

FIG. 1. Scoring of the adhesion and mesh explantation.

TABLE 1

Adhesion Scale from Garrard et al. [15]

Type of adhesions Score

No adhesions 1Filmy adhesions, easily broken manually 2Dense adhesions, requiring blunt dissection to separate

viscera from mesh3

Very dense adhesions, viscera matted to mesh surface,requiring sharp dissection to separate viscera from mesh

4

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structure, and amount of the implanted biomaterial aswell as the patient inflammatory response of monocytesto biomaterials, may induce chronic pain [11–14]. Thepurpose of this study was to evaluate the fixation prop-erties of the different methods using PP-PVDF meshesin terms of tensile strength, host tissue response, andadhesion formation. These implants are developed forthe intra-peritoneal only mesh technique with low ad-hesion formation due to the polyvinylidene fluoridecomponent.

FIG. 2. Tensile strength test.

MATERIALS AND METHODS

Forty New Zealand white rabbits, weighing 2500–3000 g, wereused. The animals were acclimated to the vivarium for 2 wk prior tomesh implantation. They were kept under standard laboratory condi-tions (temperature 20�C, relative humidity 50%–60%, 12 h light/12 hdark, fodder and water ad libitum). In each animal, three pieces of3 3 3 cm PP-PVDF mesh (Dyna Mesh-IPOM; P. J. Dahlhausen andCo. GmbH, Aachen, Germany) were implanted intra-abdominallyagainst the peritoneum and fixed with spiral tacks (Protack 5 mm;Covidien Deutschland GmbH, Neustadt a. d. Donau, Germany),transfascial sutures (Prolene 4/0; Johnson and Johnson MedicalGmbH, Norderstedt, Germany), or surgical glue (Glubran 2; GEM,Viareggio, Italy). The distance of the meshes from the midlineand between them was 1 cm, respectively. The implantation side ofeach mesh was randomized prior implantation. The government ofOberbayern approved this study. The study was planed and conducedaccording the German ethical guidelines for research in animalscience.

Operative Procedure

Anesthesia was performed with intramuscular injection of medeto-midine, fentanyl, and midazolam. Surgery was preformed understerile conditions. After removal of the hair from the abdominal walland wound disinfection with Kodan in supine position, a midlinelaparotomy of 10 cm between the xiphoid process and the pubic sym-physis was made. One of each mesh was fixed either with four spiraltacks (Protack 5 mm), four transabdominal Prolene 4/0 sutures, or thecyanoacrylate glue (Glubran 2). The glue was applied punctual on theentire mesh surface. To prevent unwanted adhesions, the glue has tobe consolidated. This takes about 60–90 s. After mesh implantationthe peritoneum and the midline fascia was closed with a runningVicryl 2/0 suture and subcutaneous tissue was closed with a subcutic-ular Vicryl 4/0 suture. Postoperatively, animals received an analgesic

(Tramudin) as needed. The rabbits were sacrificed 12 wk after meshimplantation by a lethal dose of pentobarbital (300 mg/kg, i.v.) asthe majority of tissue ingrowth and strength would have occurred inthis period.

Scoring of Adhesions

The adhesion formation, as shown in Fig. 1, with the viscera and theomentum majus was evaluated using the Garrard scale (Table 1) [15].The percentage of the adhesions covering the mesh surface was alsoestablished [16].

Mesh Shrinkage and Tensile Strength

The meshes were excised, including the entire abdominal wall.Mesh surface (cm2) upon explantation was measured and comparedwith the original size (9 cm2). Each mesh/abdominal wall sampleunderwent fixation strength testing using a tensiometer (Zwick0Z01, Ulm, Germany). The free border of the abdominal wall andthe mesh were fixed in the opposite clamps of the dynamometer andsubsequently removed from each other with a continuous displace-ment rate of 100 mm/min as shown in Fig. 2. The maximum tensilestrength was measured in Newton (N).

Histology

For histologic analysis, from each sample a 0.5 3 3 cm specimenwas fixed in 4% formaldehyde, embedded in paraffin, and sectionedat 7–10 mm. Standard staining procedure was hematoxylin and eosin(HE), Goldner’s trichrome, and Ladewig (fibrin stains) (Fig. 3). To de-termine and to compare the inflammatory response, all nucleatedcells (fibrocytes, macrophages, lymphocytes, endothelial cells, mono-cytes) were counted per high-powered field (HPF) in HE staining.The occurrence of foreign body cells was noted separately.

FIG. 3. (A) tacks, (B) suture, (C) glue. The inflammatory reaction was more pronounced in response to the cyanoacrylate glue than toeither tacks or sutures, respectively, when using the amount of nucleated cells per HPF as an indicator. The occurrence of foreign body giantcells did only differ marginally between the groups.

LADURNER ET AL.: INTRA-ABDOMINAL MESH FIXATION e159

Statistical Analysis

Differences between the intervention groups (spiral tacks, suture,glue) were tested for significance using ANOVA post hoc with Bonfer-roni-Dunn correction. The comparisons were performed usingSTATVIEW 4.5 software (Abacus Concepts, Berkeley, CA). Statisticalsignificance was assumed for P< 0.0167.

RESULTS

All animals had an uneventful recovery after meshimplantation and remained in a clinical and nutritionalgood status until the end of the study.

FIG. 4. Tenacity of adhesion according the Garrard scale [15].Meshes fixed with spiral tacks showed the lowest tenacity ofadhesions, a statistical significance was found in comparison withthe glue group (*P¼ 0.0002). Data are given as boxplots, medians,interquartile ranges and 10th/90th percentiles.

Twenty (12.5%) of the tacks were dislocated in theabdominal cavity at time of re-laparotomy. Neverthe-less, all meshes were in place, and no mesh migrationor dislocation occurred.

Meshes fixed with spiral tacks showed the lowesttenacity of adhesions (2.44 6 0.97 suture versus1.91 6 0.92 stapler versus 2.75 6 0.97 glue). A statisti-cal significance was found in comparison with theglue group (P¼ 0.0002) (Fig. 4). Moreover, regardingthe percentage of adhesions, the lowest values weredetected in the stapler group showing a statistical sig-nificance to the suture group (P¼ 0.0145) (37.62% 6

27.36% suture versus 22.87% 6 24.67% stapler versus36.50% 6 27.60% glue) (Fig. 5). Adhesion location wasindependent of the fixation technique and uniformlyallocated on the entire mesh surface. The shrinkageof the meshes was between 10% and 20% related tooriginal mesh surface (cm2) (7.93 6 1.13 suture versus8.23 6 0.92 stapler versus 8.38 6 0.67 glue); the differ-ences between these three groups were not significant(Fig. 6).

The tensile strength of the stapler and the suturegroups (14.15 6 0.97 N suture versus 14.84 6 0.74stapler) was more or less similar. However, the valueswere significantly higher in comparison to the gluegroup (9.64 6 0.78 N; P< 0.0001) (Fig. 7).

Comparing the groups, the inflammatory reactionwas more pronounced in response to the cyanoacrylateglue than to either tacks or sutures when using theamount of nucleated cells per HPF as an indicator. Oth-erwise, cells were equally distributed throughout the

FIG. 5. Percentage of the adhesions covering the mesh surface.The lowest adhesions values were detected in the mesh fixed withspiral tacks showing a statistical significance to suture mesh fixation(*P¼ 0.0145). Data are given as boxplots, medians, interquartileranges and 10th/90th percentiles.

FIG. 7. The tensile strength between the spiral tacks and suturegroups was similar. The values were significantly higher in compari-son to the glue group (*P< 0.0001). Data are given as boxplots,medians, interquartile ranges, and 10th/90th percentiles.

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newly formed fibrous tissue. The occurrence of foreignbody giant cells did only differ marginally betweenthe groups, the same (pertained) held true for mesothe-lialization (Fig. 3).

DISCUSSION

Laparoscopic incisional hernia surgery is becomingincreasing popular because of its advantages over theopen technique, especially concerning lesser woundinfection and shorter recovery time [17]. The use ofprosthesis revolutionized hernia surgery, reducing therecurrence rate from 30%–50% to 10% for the open aswell as for the laparoscopic technique [18, 19]. The prin-ciple of laparoscopic ventral hernia repair is coveringthe fascial defect with a nonabsorbable mesh witha minimal overlap of 3–5 cm. Up to now, transfascialsutures, nitinol anchors, titanium spiral tacks, or ab-sorbable staplers alone or in combination were used

FIG. 6. Shrinkage of the meshes was independent of the methodof fixation between 10% and 20% related to original mesh surface.Data are given as boxplots, medians, interquartile ranges, and 10th/90th percentiles.

for mesh fixation. This fixation is required until suffi-cient ingrowth has made the collagen impregnationsufficiently strong to ensure the durable repair ofthe fascial defect and to prevent internal herniationbetween the mesh and the abdominal wall [20, 21].The published recurrence rate of laparoscopic ventralhernia repair lies between 2% and 6.5% [6–8, 22, 23].A recent meta-analysis showed fewer wound-relatedand overall complications and a lower rate of herniarecurrence for laparoscopic ventral hernia repair incontrast to the open procedure [24]. Despite the contem-plated advantages, the use of prosthetic materials isassociated with an increased incidence of seromas,chronic pain, granulomas, and fistulas [25–27] .

Postoperative pain is normally localized at the fixa-tion points of the mesh and typically resolves within 6to 8 weeks [21]. However, 10%–20% of patients indicatepain even after 8 weeks in our own series (unpublisheddata). Obviously, persistent pain appears more oftenthan hernia recurrence. It appears that sutures andspiral tacks play a role in genesis of chronic abdominalpain as well as intra-abdominal adhesion formation[28]. A possible explanation may be nerve entrapment,muscle ischemia, or local hematoma of the abdominalwall. This theory is supported by the fact that localanesthetics and tying the knots gently can relieve thesuture site pain [10]. The other possible mechanism isadhesion of the viscera with the implanted mesh orthe fixation devices with the possibility of bowelobstruction fistulas and chronic abdominal pain.

The ideal mesh should not be physically altered bytissue fluids, be chemical inert, not produce foreignbody reactions, be noncarcinogenic, nonallergenic,have the possibility to resist mechanical strains, andthe ability to be sterilized [12, 29]. The characteristicsof an ideal mesh for intra-abdominal placement shouldinclude adhesion prevention on the visceral side and

LADURNER ET AL.: INTRA-ABDOMINAL MESH FIXATION e161

excellent fibrous ingrowth on the other side. For achiev-ing this aim, recent meshes are composed of two layers.However, no ideal intraperitoneal prosthetic materialhas yet been developed and any intraperitoneal posi-tioned mesh stimulates a foreign body adhesion forma-tion. The inflammatory reaction to the mesh desired formesh ingrowth in the abdominal wall inhibits fibrinoly-sis and the degradation of the fibrinous adhesion. Theinfiltration of fibroblasts with the formation of collagenresults in permanent adhesion [15, 30]. Therefore, anyintra-abdominally placed foreign body will promoteadhesion formation. To prevent mesh migration, thefixation of the prosthesis to the peritoneal surface ofthe abdominal wall is necessary until the fibroblasticresponse to the prosthesis causes it to become com-pletely incorporated into the host’s granulation tissue.

Sutures and spiral tacks are those materials pres-ently employed to secure the mesh in its intraperitonealpositioning [4, 8, 17, 31–33]. The mechanical resistanceof sutures and tacks is well documented [34]. Neverthe-less, beside the already discussed source for persistentpain, they are associated also with other disadvantages:longer operating time for suture fixation and increasedcosts of materials for spiral tacks.

To date, synthetic glue or fibrin sealants have noclinical significance in laparoscopic intraperitoneal on-lay mesh fixation. In this context, Glubran 2 glue is asynthetic, cyanoacrylic surgical adhesive modified byaddition of a monomer synthesised by the manufac-turer. Cyanoacrylates are a group of rapidly polymeriz-ing adhesives, already used in clinical practice [35–38].The glue starts to solidify due to the polymerizationreaction as soon as it is in contact with blood or tissue,which takes about 60–90 s. The speed of polymerizationis a function of the alkyl side chain and depends on thetype of the tissue with which the glue comes into con-tact, the amount and nature of the fluids present, andthe amount of the adhesive applied [35]. Cyanoacry-lates have also bacteriostatic and bacteriocidal effects[39, 40]. In general, cyanoacrylates generate a tempera-ture of approximately 45�C, produced by the polymeri-zation, a fact that may cause local inflammation andnecrosis. In an experimental study, a mild inflamma-tory reaction with edema disappeared within 2 mo [41].The glue reaches its maximum mechanical strengthupon completion of this reaction. Once set, the glue nolonger possesses adhesive properties so that tissues orsurgical gauzes may be placed in contact with it withoutany risk of unwanted adhesion.

In this study, sutures and tacks were superior com-pared with cyanoacrylate glues in terms of fixationstrength. Obviously, sutures and tacks are a punctualand rigid mesh fixation device, whereas the gluefixation allows a uniform binding of the implant to theabdominal wall.

At time of re-laparotomy, 20 of the 160 used tackswere found to be dislocated into the abdominal cavity.Nevertheless, all meshes were in place and no meshmigration or dislocation occurred. Tack dislocationdoes not seem to cause clinical problems. Complicationssuch as perforation or bowel obstruction of tacks inhernia surgery are rare, and only few case reportswere published on this subject [42–44].

Despite the more pronounced foreign body reactionusing the glue, the mesh shrinkage process did notdiffer in the three groups. At the same time, the lowesttenacity and percentage of adhesions were detectedin meshes fixed with tacks. These results were unex-pected as mesh contraction depends on the inflamma-tory response and on the amount (quantity) and thetype of material used [45]. The fact that adhesion for-mation between suture and glue fixation was not statis-tically different is also reflected by the equal extentof mesothelialization of the visceral surface of themesh in both groups. In contrast to recent results, tis-sue integration of the mesh was not impaired by glueplaques [46].

CONCLUSION

The crucial point in laparoscopic intraperitoneal her-nia repair is the stable fixation of the mesh on the intactperitoneum to prevent mesh migration, resulting inhernia recurrence. In this animal study, the adhesiveshowed a considerable resistance to tensile stress. De-spite a higher inflammatory reaction, the use of syn-thetic glue for mesh fixation did not cause a higherincidence of mesh shrinkage or adhesion formation.Nevertheless, sutures and tacks provide a statisticallysignificant increase in tensile strength compared withglue.

The preliminary results of our animal study showthat glue will not yet replace sutures or takes formesh fixation, but the use of glue could reduce thecurrently required number of them. Further studieswill have to prove this.

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