Polypropylene surgical mesh coated with extracellular matrix mitigates the host foreign body response
Matthew T. Wolf
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher A. Carruthers
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher L. Dearth
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorPeter M. Crapo
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
C. R. Bard Inc., Warwick, Rhode Island
Search for more papers by this authorAlexander Huber
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorOlivia A. Burnsed
Department of Biomedical Engineering, Georgia Institute of Technology, Altanta, Georgia
Search for more papers by this authorRicardo Londono
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorScott A. Johnson
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorKerry A. Daly
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorElizabeth C. Stahl
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorJohn M. Freund
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher J. Medberry
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorLisa E. Carey
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorAlejandro Nieponice
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorNicholas J. Amoroso
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorCorresponding Author
Stephen F. Badylak
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Correspondence to: S. F. Badylak; e-mail: [email protected]Search for more papers by this authorMatthew T. Wolf
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher A. Carruthers
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher L. Dearth
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorPeter M. Crapo
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
C. R. Bard Inc., Warwick, Rhode Island
Search for more papers by this authorAlexander Huber
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorOlivia A. Burnsed
Department of Biomedical Engineering, Georgia Institute of Technology, Altanta, Georgia
Search for more papers by this authorRicardo Londono
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorScott A. Johnson
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorKerry A. Daly
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorElizabeth C. Stahl
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorJohn M. Freund
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorChristopher J. Medberry
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorLisa E. Carey
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorAlejandro Nieponice
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorNicholas J. Amoroso
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Search for more papers by this authorCorresponding Author
Stephen F. Badylak
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Correspondence to: S. F. Badylak; e-mail: [email protected]Search for more papers by this authorAbstract
Surgical mesh devices composed of synthetic materials are commonly used for ventral hernia repair. These materials provide robust mechanical strength and are quickly incorporated into host tissue; factors that contribute to reduced hernia recurrence rates. However, such mesh devices cause a foreign body response with the associated complications of fibrosis and patient discomfort. In contrast, surgical mesh devices composed of naturally occurring extracellular matrix (ECM) are associated with constructive tissue remodeling, but lack the mechanical strength of synthetic materials. A method for applying a porcine dermal ECM hydrogel coating to a polypropylene mesh is described herein with the associated effects upon the host tissue response and biaxial mechanical behavior. Uncoated and ECM coated heavy-weight BARD™ Mesh were compared to the light-weight ULTRAPRO™ and BARD™ Soft Mesh devices in a rat partial thickness abdominal defect overlay model. The ECM coated mesh attenuated the pro-inflammatory response compared to all other devices, with a reduced cell accumulation and fewer foreign body giant cells. The ECM coating degraded by 35 days, and was replaced with loose connective tissue compared to the dense collagenous tissue associated with the uncoated polypropylene mesh device. Biaxial mechanical characterization showed that all of the mesh devices were of similar isotropic stiffness. Upon explanation, the light-weight mesh devices were more compliant than the coated or uncoated heavy-weight devices. This study shows that an ECM coating alters the default host response to a polypropylene mesh, but not the mechanical properties in an acute in vivo abdominal repair model. © 2013 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 102A: 234–246, 2014.
Supporting Information
Additional Supporting Information may be found in the online version of this article.
| Filename | Description |
|---|---|
| jbma34671-sup-0001-suppfig1.tif5 MB | Supplementary Figure 1. Histologic appearance of mesh devices after 3 and 14 days of in vivo implantation. Representative H&E stained histologic cross sections of each mesh/time point were imaged at 100X magnification (bottom of each figure panel). Two 400X magnification images immunolabeled for the macrophage marker CD68 (brown) were focused on the area adjacent to mesh fibers (top left of each panel) and the area between mesh fibers (top right of each panel). Dotted line in C and D encloses the ECM coating surrounding the mesh fibers. Scale bars represents 100 μm. |
| jbma34671-sup-0002-suppfig2.tif666.7 KB | Supplementary Figure 2. Picrosirius red staining and imaging with polarized light microscopy comparing (A) BARD™ Mesh and (B) ECM coated BARD™ Mesh after 3 days of in vivo implantation. Scale bar represents 100 μm. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Usher FC. Hernia repair with knitted polypropylene mesh. Surg Gynecol Obstet 1963; 117: 239–240.
- 2George CD, Ellis H. The results of incisional hernia repair: A twelve year review. Ann R Coll Surg Engl 1986; 68: 185–187.
- 3Cobb WS, Kercher KW, Heniford BT. The argument for lightweight polypropylene mesh in hernia repair. Surg Innov 2005; 12: 63–69.
- 4Feola A, Barone W, Moalli P, Abramowitch S. Characterizing the ex vivo textile and structural properties of synthetic prolapse mesh products. Int Urogynecol J 2013; 24: 559–564.
- 5Klosterhalfen B, Junge K, Klinge U. The lightweight and large porous mesh concept for hernia repair. Expert Rev Med Devices 2005; 2: 103–117.
- 6Hernandez-Gascon B, Pena E, Melero H, Pascual G, Doblare M, Ginebra MP, Bellon JM, Calvo B. Mechanical behaviour of synthetic surgical meshes: Finite element simulation of the herniated abdominal wall. Acta Biomater 2011; 7: 3905–3913.
- 7Chu CC, Welch L. Characterization of morphologic and mechanical properties of surgical mesh fabrics. J Biomed Mater Res 1985; 19: 903–916.
- 8Ozog Y, Konstantinovic M, Werbrouck E, De Ridder D, Mazza E, Deprest J. Persistence of polypropylene mesh anisotropy after implantation: an experimental study. BJOG 2011; 118: 1180–1185.
- 9Klinge U, Klosterhalfen B, Muller M, Schumpelick V. Foreign body reaction to meshes used for the repair of abdominal wall hernias. Eur J Surg 1999; 165: 665–673.
- 10Leber GE, Garb JL, Alexander AI, Reed WP. Long-term complications associated with prosthetic repair of incisional hernias. Arch Surg 1998; 133: 378–382.
- 11Brown CN, Finch JG. Which mesh for hernia repair? Ann R Coll Surg Engl 2010; 92: 272–278.
- 12Hollinsky C, Sandberg S, Koch T, Seidler S. Biomechanical properties of lightweight versus heavyweight meshes for laparoscopic inguinal hernia repair and their impact on recurrence rates. Surg Endosc 2008; 22: 2679–2685.
- 13Weyhe D, Schmitz I, Belyaev O, Grabs R, Muller KM, Uhl W, Zumtobel V. Experimental comparison of monofile light and heavy polypropylene meshes: Less weight does not mean less biological response. World J Surg 2006; 30: 1586–1591.
- 14Conze J, Rosch R, Klinge U, Weiss C, Anurov M, Titkowa S, Oettinger A, Schumpelick V. Polypropylene in the intra-abdominal position: influence of pore size and surface area. Hernia 2004; 8: 365–372.
- 15Ansaloni L, Catena F, Coccolini F, Gazzotti F, D'Alessandro L, Pinna AD. Inguinal hernia repair with porcine small intestine submucosa: 3-Year follow-up results of a randomized controlled trial of Lichtenstein's repair with polypropylene mesh versus Surgisis Inguinal Hernia Matrix. Am J Surg 2009; 198: 303–312.
- 16Medberry CJ, Tottey S, Jiang H, Johnson SA, Badylak SF. Resistance to infection of five different materials in a rat body wall model. J Surg Res 2010; 173: 38–44.
- 17Holton LH III, Chung T, Silverman RP, Haerian H, Goldberg NH, Burrows WM, Gobin A, Butler CE. Comparison of acellular dermal matrix and synthetic mesh for lateral chest wall reconstruction in a rabbit model. Plast Reconstr Surg 2007; 119: 1238–1246.
- 18Valentin JE, Turner NJ, Gilbert TW, Badylak SF. Functional skeletal muscle formation with a biologic scaffold. Biomaterials 2010; 31: 7475–7484.
- 19Hiles M, Record Ritchie RD, Altizer AM. Are biologic grafts effective for hernia repair? A systematic review of the literature. Surg Innov 2009; 16: 26–37.
- 20Valentin JE, Stewart-Akers AM, Gilbert TW, Badylak SF. Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng Part A 2009; 15: 1687–1694.
- 21Deeken CR, Melman L, Jenkins ED, Greco SC, Frisella MM, Matthews BD. Histologic and biomechanical evaluation of crosslinked and non-crosslinked biologic meshes in a porcine model of ventral incisional hernia repair. J Am Coll Surg 2011; 212: 880–888.
- 22Bellows CF, Wheatley BM, Moroz K, Rosales SC, Morici LA. The effect of bacterial infection on the biomechanical properties of biological mesh in a rat model. PLoS One 2011; 6: e21228.
- 23Zhang J, Wang GY, Xiao YP, Fan LY, Wang Q. The biomechanical behavior and host response to porcine-derived small intestine submucosa, pericardium and dermal matrix acellular grafts in a rat abdominal defect model. Biomaterials 2011; 32: 7086–7095.
- 24Badylak SF, Freytes DO, Gilbert TW. Extracellular matrix as a biological scaffold material: Structure and function. Acta Biomater 2009; 5: 1–13.
- 25Reing JE, Brown BN, Daly KA, Freund JM, Gilbert TW, Hsiong SX, Huber A, Kullas KE, Tottey S, Wolf MT, Badylak SF. The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials 2010; 31: 8626–8633.
- 26Freytes DO, Martin J, Velankar SS, Lee AS, Badylak SF. Preparation and rheological characterization of a gel form of the porcine urinary bladder matrix. Biomaterials 2008; 29: 1630–1637.
- 27Wolf MT, Daly KA, Brennan-Pierce EP, Johnson SA, Carruthers CA, D'Amore A, Nagarkar SP, Velankar SS, Badylak SF. A hydrogel derived from decellularized dermal extracellular matrix. Biomaterials 2012; 33: 7028–7038.
- 28Rich L, Whittaker P. Collagen and picrosirius red staining: a polarized light assesment of fibrillar hue and spatial distribution. Braz J morphol Sci 2005; 22: 97–104.
- 29Nadkarni SK, Pierce MC, Park BH, de Boer JF, Whittaker P, Bouma BE, Bressner JE, Halpern E, Houser SL, Tearney GJ. Measurement of collagen and smooth muscle cell content in atherosclerotic plaques using polarization-sensitive optical coherence tomography. J Am Coll Cardiol 2007; 49: 1474–1481.
- 30Billiar KL, Sacks MS. Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp--Part I: Experimental results. J Biomech Eng 2000; 122: 23–30.
- 31Sun W, Sacks MS, Scott MJ. Effects of boundary conditions on the estimation of the planar biaxial mechanical properties of soft tissues. J Biomech Eng 2005; 127: 709–715.
- 32Di Vita G, D'Agostino P, Patti R, Arcara M, Caruso G, Davi V, Cillari E. Acute inflammatory response after inguinal and incisional hernia repair with implantation of polypropylene mesh of different size. Langenbecks Arch Surg 2005; 390: 306–311.
- 33Garcia-Urena MA, Vega Ruiz V, Diaz Godoy A, Baez Perea JM, Marin Gomez LM, Carnero Hernandez FJ, Velasco Garcia MA. Differences in polypropylene shrinkage depending on mesh position in an experimental study. Am J Surg 2007; 193: 538–542.
- 34Costello CR, Bachman SL, Ramshaw BJ, Grant SA. Materials characterization of explanted polypropylene hernia meshes. J Biomed Mater Res B Appl Biomater 2007; 83: 44–49.
- 35Brandt CJ, Kammer D, Fiebeler A, Klinge U. Beneficial effects of hydrocortisone or spironolactone coating on foreign body response to mesh biomaterial in a mouse model. J Biomed Mater Res A 2011; 99: 335–343.
- 36Harth KC, Rosen MJ, Thatiparti TR, Jacobs MR, Halaweish I, Bajaksouzian S, Furlan J, von Recum HA. Antibiotic-releasing mesh coating to reduce prosthetic sepsis: An in vivo study. J Surg Res 2010; 163: 337–343.
- 37Engelsman AF, Krom BP, Busscher HJ, van Dam GM, Ploeg RJ, van der Mei HC. Antimicrobial effects of an NO-releasing poly(ethylene vinylacetate) coating on soft-tissue implants in vitro and in a murine model. Acta Biomater 2009; 5: 1905–1910.
- 38Altinel Y, Ozturk E, Ozkaya G, Akyildiz EU, Ulcay Y, Ozguc H. The effect of a chitosan coating on the adhesive potential and tensile strength of polypropylene meshes. Hernia 2012; 16: 709–716.
- 39Schreinemacher MH, Emans PJ, Gijbels MJ, Greve JW, Beets GL, Bouvy ND. Degradation of mesh coatings and intraperitoneal adhesion formation in an experimental model. Br J Surg 2009; 96: 305–313.
- 40van't Riet M, Burger JW, Bonthuis F, Jeekel J, Bonjer HJ. Prevention of adhesion formation to polypropylene mesh by collagen coating: a randomized controlled study in a rat model of ventral hernia repair. Surg Endosc 2004; 18: 681–685.
- 41Borrazzo EC, Belmont MF, Boffa D, Fowler DL. Effect of prosthetic material on adhesion formation after laparoscopic ventral hernia repair in a porcine model. Hernia 2004; 8: 108–112.
- 42Fujino K, Kinoshita M, Saitoh A, Yano H, Nishikawa K, Fujie T, Iwaya K, Kakihara M, Takeoka S, Saitoh D and others. Novel technique of overlaying a poly-L-lactic acid nanosheet for adhesion prophylaxis and fixation of intraperitoneal onlay polypropylene mesh in a rabbit model. Surg Endosc 2011; 25: 3428–3436.
- 43Pierce RA, Perrone JM, Nimeri A, Sexton JA, Walcutt J, Frisella MM, Matthews BD. 120-Day comparative analysis of adhesion grade and quantity, mesh contraction, and tissue response to a novel omega-3 fatty acid bioabsorbable barrier macroporous mesh after intraperitoneal placement. Surg Innov 2009; 16: 46–54.
- 44van 't Riet M, de Vos van Steenwijk PJ, Bonthuis F, Marquet RL, Steyerberg EW, Jeekel J, Bonjer HJ. Prevention of adhesion to prosthetic mesh: comparison of different barriers using an incisional hernia model. Ann Surg 2003; 237: 123–128.
- 45Maciver AH, McCall MD, Edgar RL, Thiesen AL, Bigam DL, Churchill TA, Shapiro AM. Sirolimus drug-eluting, hydrogel-impregnated polypropylene mesh reduces intra-abdominal adhesion formation in a mouse model. Surgery 2011; 150: 907–915.
- 46Takaoka R, Hikasa Y, Tabata Y. Vascularization around poly(tetrafluoroethylene) mesh with coating of gelatin hydrogel incorporating basic fibroblast growth factor. J Biomater Sci Polym Ed 2009; 20: 1483–1494.
- 47Badiou W, Lavigne JP, Bousquet PJ, O'Callaghan D, Mares P, de Tayrac R. In vitro and in vivo assessment of silver-coated polypropylene mesh to prevent infection in a rat model. Int Urogynecol J 2011; 22: 265–272.
- 48Junge K, Rosch R, Klinge U, Saklak M, Klosterhalfen B, Peiper C, Schumpelick V. Titanium coating of a polypropylene mesh for hernia repair: Effect on biocompatibilty. Hernia 2005; 9: 115–119.
- 49Brown BN, Londono R, Tottey S, Zhang L, Kukla KA, Wolf MT, Daly KA, Reing JE, Badylak SF. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater 2012; 8: 978–987.
- 50DeQuach JA, Lin JE, Cam C, Hu D, Salvatore MA, Sheikh F, Christman KL. Injectable skeletal muscle matrix hydrogel promotes neovascularization and muscle cell infiltration in a hindlimb ischemia model. Eur Cell Mater 2012; 23: 400–412.
- 51Agrawal V, Johnson SA, Reing J, Zhang L, Tottey S, Wang G, Hirschi KK, Braunhut S, Gudas LJ, Badylak SF. Epimorphic regeneration approach to tissue replacement in adult mammals. Proc Natl Acad Sci USA 2010; 107: 3351–3355.
- 52Badylak SF, Valentin JE, Ravindra AK, McCabe GP, Stewart-Akers AM. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng Part A 2008; 14: 1835–1842.
- 53Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM, Wang J, Mayle KM, Bartels K, Salvatore M and others. Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol 2012; 59: 751–763.
- 54Weyhe D, Belyaev O, Buettner G, Mros K, Mueller C, Meurer K, Papapostolou G, Uhl W. In vitro comparison of three different mesh constructions. ANZ J Surg 2008; 78: 55–60.
- 55Weyhe D, Hoffmann P, Belyaev O, Mros K, Muller C, Uhl W, Schmitz F. The role of TGF-beta1 as a determinant of foreign body reaction to alloplastic materials in rat fibroblast cultures: Comparison of different commercially available polypropylene meshes for hernia repair. Regul Pept 2007; 138: 10–14.
- 56Muellner T, Kwasny O, Loehnert V, Mallinger R, Unfried G, Schabus R, Plenk H Jr. Light and electron microscopic study of stress-shielding effects on rat patellar tendon. Arch Orthop Trauma Surg 2001; 121: 561–565.
Citing Literature
