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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 2  |  Issue : 3  |  Page : 89-95

A comparative analysis of ventral hernia repair with a porcine hepatic-derived matrix and porcine dermal matrix


1 Department of Surgery, Division of General Surgery, University of Kentucky, Lexington, KY, USA
2 Department of Pathology and Laboratory Medicine, University of Kentucky, Lexington, KY, USA

Date of Submission13-Jun-2019
Date of Acceptance08-Jul-2019
Date of Web Publication30-Aug-2019

Correspondence Address:
Dr. John Scott Roth
Department of Surgery, University of Kentucky Medical Center, 800 Rose Street, C 240 UKMC, Lexington, KY 40536-0293
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijawhs.ijawhs_20_19

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  Abstract 


PURPOSE: Complex abdominal wall hernia repairs present unique challenges for patients and surgeons, often requiring mesh placement. Biologic materials may be utilized in repairs with high risk for postoperative complications. Porcine dermal meshes (PDM) are among the most commonly utilized biologic grafts. Porcine hepatic biologic mesh (PHM) was developed due to its unique characteristics. This study investigates outcomes following acute ventral hernia repair with a porcine-derived hepatic biologic mesh (Miromesh®) and porcine dermis (Strattice™) in a porcine animal model.
MATERIALS AND METHODS: Twenty Yucatan pigs underwent hernia creation followed by immediate retrorectus ventral hernia repair and were survived for 1 (n = 4), 2 (n = 6), 6 (n = 5), or 12 (n = 5) months. Animals underwent excision of the anterior abdominal wall and immediate repair with both PDM and PHM positioned in the retrorectus space with 3 cm between grafts. Animals were survived and evaluated for tensiometric strength, histology, and protein analyses.
RESULTS: Twenty animals underwent successful hernia creation and repair. Tensiometric strength was similar between repair groups at 1 (63.8 vs. 67.0 N, NS) and 2 months (80.0 vs. 76.1 N, NS), whereas at 6 (72.2 vs. 44.9 N, P= 0.01) and 12 months (66.7 vs. 46.3, P= 0.004), repair strength was greater in PHM. Histological evaluation demonstrated greater inflammation and fibrosis at 12 months in the PHM repairs. Collagen 1 deposition was greater in PHM at 1 (P = 0.1) and 2 (P = 0.015) months. There was no difference in collagen 3 deposition between groups.
CONCLUSIONS: Ventral hernia repair with a porcine hepatic mesh results in greater repair strength than repair with porcine dermal grafts.

Keywords: Animal model, dermal mesh, hernia repair, outcomes


How to cite this article:
Tharappel J, Wennergren JE, Lee EY, Madabhushi VV, Plymale MA, Roth JS. A comparative analysis of ventral hernia repair with a porcine hepatic-derived matrix and porcine dermal matrix. Int J Abdom Wall Hernia Surg 2019;2:89-95

How to cite this URL:
Tharappel J, Wennergren JE, Lee EY, Madabhushi VV, Plymale MA, Roth JS. A comparative analysis of ventral hernia repair with a porcine hepatic-derived matrix and porcine dermal matrix. Int J Abdom Wall Hernia Surg [serial online] 2019 [cited 2020 Feb 19];2:89-95. Available from: http://www.herniasurgeryjournal.org/text.asp?2019/2/3/89/265863




  Introduction Top


Ventral hernias represent one of the most prominent surgical problems, affecting 11%–20% undergoing abdominal surgery, with recurrence rates as high as 40%.[1],[2],[3] Hernia repairs are either repaired primarily or using a mesh to reinforce the repair. The latter is the standard of care for most ventral hernia repairs.[1],[2],[3],[4],[5] Clinical conditions such as active infections create potential challenges for mesh repairs.[6],[7] Synthetic mesh is widely utilized in noncontaminated hernia repairs due to their low cost and excellent outcomes but is associated with increasing rates of complications among patients with increased level of contamination.[8],[9] Biological mesh is typically derived from human, bovine, or porcine tissue that is decellularized, leaving behind a collagen matrix. The biological mesh supports the abdominal wall until collagen tissue replaces the mesh and creates a stable anterior abdominal wall.[10],[11] Through this process, the entire biologic mesh can be turned over, leaving nothing behind to serve as a nidus for infection.[12] Most biological scaffolds are generated by immersion decellularization, by which the tissue is soaked in various solutions to remove the cellular components and leaving the extracellular matrix (ECM) behind.[12] Since it involves an outside-to-inside soaking process, it is limited to relatively thin tissues. However, Miromesh™ (Miromesh™, Miromatrix, Eden Prairie, Minnesota) is a novel mesh derived from porcine hepatic tissue processed through a perfusion decellularization. In this mesh, the hepatic vessels are cannulated to facilitate perfusion of the organ with mild solutions, allowing decelluarization while retaining the ECM and the vascular network throughout the tissue. This results in a noncross linked biologic material, which has the potential for rapid incorporation within host tissue.[12]

The usefulness of biological mesh is still an area of controversy, with some authors supporting the use of biological mesh in contaminated fields.[11],[13],[14] However, others have shown decreased surgical site infections with synthetic mesh in a contaminated field, and there is no conclusive evidence from prospective, randomized studies.[15] When repairing acute abdominal hernias, biologic mesh can be used to reinforce the fascial closure, especially in patients undergoing delayed closure of an open abdomen.[16],[17]

The purpose of this study was to evaluate mesh integration and tensile strength of porcine hepatic mesh in a retrorectus hernia repair model when compared to a porcine dermal matrix (Strattice™, Allergan, Branchburg, NJ, USA) in a clean operative field, in the acute setting.


  Materials and Methods Top


Ethics approval

This study involving animals was determined ethically acceptable and approved by our Institutional Animal Care and Use Committee.

Study design

Twenty six-month-old Yucatan miniature swine with average weights 15–16 kg were purchased from Sinclair BioResources, MO. Swine were acclimatized for 5 days before experimental procedures. Two full-thickness 3 cm × 3 cm midline defects were created in each of the 20 swine, with defects separated by 10 cm. Each animal underwent placement of two separate 10 × 8 cm meshes, one porcine hepatic mesh (PHM), and one porcine dermal matrix (PDM). Meshes were sutured in the retrorectus space with polydioxanone suture allowing for a 3 cm gap between grafts [Figure 1]. The anterior rectus sheath was approximated over the meshes with a running polydioxanone suture. Animals were survived for 1 month (n = 4), 2 months (n = 6), 6 months (n = 5), or 12 months (n = 5) and evaluated for clinical hernia recurrence, mesh implant size, breaking strength of the hernia repair, histology, matrix metalloproteinases (MMPs 2 and 9), and collagen types 1 and 3.
Figure 1: Surgical placement of porcine dermal matrix (left) and porcine hepatic matrix (right) in the retrorectus space in pig

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Mechanical testing

Mechanical testing of the repaired hernia defect was performed immediately following euthanasia. The abdominal wall was harvested surrounding the repair area and was fashioned into a strip of tissue 5 cm long and 1.5 cm wide with the mesh-repaired area in the center. The tissue was loaded into the pneumatic grips of an Instron E3000 (Instron Corp., Canton, MA, USA) equipped with a 250 N load cell. Tissue samples preloaded with 1 N force was then loaded at a rate of 10 mm/min until failure. Load and displacement were recorded and utilized to determine the maximum force required for failure of repaired tissue. Peel strength was performed by attaching the mesh to the upper pneumatic grip and native tissue to the lower pneumatic grip. Data analysis was conducted using Instron's Bluehill software package.

Portions of the resected abdominal wall, including the mesh material, underwent histologic analysis using standard hematoxylin-eosin staining [Figure 2] and additional tissue underwent testing for biomarkers including MMPs and collagen subtypes 1 and 3.
Figure 2: Hematoxylin and eosin stains at ×10

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Western blotting

Antibodies for MMP-2, 3, and 9, and collagen type 1 and 3 were purchased from Santa Cruz Biotechnology Inc. (Santa Cruz, CA, USA). The blotting procedure was performed utilizing a previously described protocol.[12] A lysis buffer containing 1% Nonidet P-40, 0.1% sodium dodecyl sulfate, 0.1 mg/mL phenylmethylsulfonyl fluoride, 2 mg/mL aprotinin, 2 mg/mL leupeptin, 2 mg/mL Pepstatin A, and phosphate buffered saline (PBS) was added to the frozen abdominal wall tissue samples (1 part tissue, 4 part buffer), homogenized, homogenates centrifuged at 10,000 g for 20 min, and supernatants centrifuged again at 100,000 g for 20 min. The supernatants were again collected, aliquoted, and stored at −800°C. One aliquot was used for assaying the protein content using the BCA protocol (Pierce Protein Biology Products, Rockford, IL, USA). The samples were denatured by boiling for 5 min with ×2 (one in two dilution or 1:2 diluted) gel loading buffer (17.3% glycerol, 1.25 M b-mercaptoethanol, 5.2% sodium dodecyl sulfate, 0.22MTris, pH 6.8, and 1–2 mg bromophenol blue). Thirty microgram protein from each sample were electrophoresed on a mini gel containing 4% stacking gel and 10% separating gel at 150 V for 1 h. Each sample was, then, electroblotted onto polyvinylidene difluoride membranes (Bio-Rad Laboratories, Inc., Hercules, CA, USA) at 100 V for 1 h. The membranes were then incubated for 1 h in a blocking buffer (5% fat-free dry instant powdered milk, 1 mM Tris-base, 15 mM sodium chloride, and 0.05% Tween-20) at room temperature (RT) with shaking. This was followed by primary and secondary antibodies diluted in blocking buffer for 1 h each at RT with shaking. After primary and secondary antibody incubations, the membranes were washed 3X with washing buffer (1 mM Tris-base, 15 mM sodium chloride, and 0.05% Tween-20). A chemiluminescence detection kit (Pierce, Rockford, IL) was used to detect the antibodies bound to the membrane, and the images were quantified by ImageJ software (NIH, Bethesda, MD, USA).

Histochemistry

Histology was performed through previously described methods.[18],[19] The tissue of the abdominal wall with the implanted mesh was fixed in 10% buffered formalin, processed into cut 4 μm sections, and then mounted on glass slides. After deparaffinizing, they were treated in Bouin's solution in the microwave for 15 s and let stand for 2 more min. After washing, the slides were treated with Weigert's hematoxylin for 10 min. Slides were, then, washed in water after confirming the nuclei were stained blue black. The slides were treated with Biebrich scarlet solution for 3 min, then washed in distilled water and treated with 2% phosphotungstic solution for 10 min. After an additional rinse in distilled water, slides were stained in 2% light green solution for 3 min. Then, they were rerinsed in distilled water, dipped in 1% acetic acid, dehydrated through ascending grades of alcohol, cleared in xylene, and mounted in synthetic resin.

Statistical analysis

The results of the Western blotting experiment and tensiometry data were analyzed by Student's t-test. The results were considered statistically significant if P < 0.05.


  Results Top


Gross findings

All 20 animals survived hernia repair until time of planned euthanasia without complication. Animals grew and gained weight appropriately. There was no evidence of hernia recurrence in any of the animals at any time point either before euthanasia or at the time of abdominal wall harvest. In addition, there were no signs of infection around the implantation sites in all 20 animals. At 1, 2, and 6 months, the PHM and PDM were readily identifiable on gross inspection. The 12-month survival group had no gross evidence of persistent PDM, whereas the PHM remained grossly visible. Following harvest, the PHM grafts were notably thicker [Figure 3] than PDM grafts.
Figure 3: Abdominal wall cross-section at 1 month; PDM (top); PHM (bottom)

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Breaking and peel strength

At 1 and 2 months, there was no significant difference in the breaking strength and peel strength between PHM and PDM repaired hernia defects. At 6- and 12-month time points, the PHM group showed a significantly higher breaking strength compared to PDM [Figure 4].
Figure 4: Tensiometric strength of hernia repair at all time points

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Matrix metalloproteinases

MMP-2 levels in PHM repaired animals were elevated at the 1-month (P < 0.03) and 2-month (P < 0.05) time points. MMP-2 was decreased in the 12-month PHM group compared to PDM repaired animals (P < 0.004) [Figure 5] and [Figure 6]a, [Figure 6]b, [Figure 6]c. MMP-9 was elevated in 1-month PHM samples (P < 0.029). MMP-9 was reduced in 12-month PHM compared to PDM repaired animals (P < 0.03) [Figure 7]a and [Figure 7]b.
Figure 5: Densitometric count measurements of matrix metalloproteinases-2 Western blots

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Figure 6: (a) Matrix metalloproteinases-2 protein levels in 1-month animal mesh fascia interface (MFI) Western blot; (b) matrix metalloproteinases-2 protein levels in 2-month animal MFI; (c) matrix metalloproteinases-2 protein levels in 12-month animal MFI

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Figure 7: (a) Matrix metalloproteinases-9 protein levels at different time intervals; (b) matrix metalloproteinases-9 protein levels in 12-month animal MFI

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Collagen-1 deposition (P < 0.015) was significantly increased in the PHM group at 2 months, with similar levels at other time points [Figure 8]. Collagen-3 levels did not differ at any time point.
Figure 8: Col-1 protein levels in 2-month animal MFI

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Histology

Hematoxylin and eosin stain demonstrated greater fibrosis in PHM repaired grafts at 1, 2, and 12 months and greater inflammation at 1, 2, and 12 months [Table 1] and [Figure 2]. Mason's trichrome stain demonstrated significantly greater collagen deposition in PHM repaired animals at 2 and 6 months compared to PDM [Figure 9].
Table 1: Histologic evaluation of fibrosis, inflammation, and fibrosis at 1, 2, 6, and 12 months

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Figure 9: (a) Collagen quantification of Mason's trichrome-stained samples at 2 months. (b) Collagen quantification of trichrome stained samples at 6 months

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  Discussion Top


As an initial study evaluating the efficacy of this material, the model chosen was a clean hernia repair without any degree of contamination to avoid confounders. While the authors appreciate that a biologic mesh is rarely utilized in this circumstance, it is prudent to ensure that the porcine hepatic mesh is an excellent alternate to the porcine dermal matrix in a clean environment before investigation of outcomes in a contaminated wound.

In this study, there was no evidence of hernia recurrence in any of the 20 animals at any time point, suggesting reasonable short-term efficacy in hernia repair. Furthermore, there were no surgical site infections or occurrences associated with any of the repairs.

We found it intriguing that the porcine hepatic graft remained grossly visible at 12 months, whereas the porcine dermal matrix was unable to be identified from native surrounding tissue at the 12-month time point. It is not clear if the porcine dermal matrices were imperceptible due to absorption or integration at this time point. In addition, there appears to be a greater level of cellular infiltrate in the porcine hepatic matrix samples in comparison to the porcine dermal matrices at each time interval [Figure 2].

Prior studies have demonstrated that decellularized dermis contains a highly dense collagen matrix that may interfere with cell migration leading to delayed integration of the bioprosthetic.[20],[21] Compared to a much denser dermal matrix, liver is highly vascularized and less dense tissue with a soft consistency.[22] Because of these qualities, the decellularized liver may be better suited than dermal matrix to act as a scaffold for regeneration as it may facilitate host cell migration and vascularization. The use of liver tissue for the generation of an acellular matrix using a novel perfusion decellularization process makes the porcine hepatic mesh more biocompatible when compared to other similar matrices.[18] During a proprietary perfusion decellularization process, the tissue is cleared of all cells and other antigenic debris without disturbing the structure of the ECM scaffold of the liver tissue. This study offers a chance to compare a novel porcine liver prosthetic acellular matrix with a standard noncross-linked porcine acellular dermal matrix to test its tensiometric strength and tissue integration after implantation onto the porcine abdominal wall. In this study, while we did not find any significant difference in 1- and 2-month samples, we found a significantly higher breaking strength in the 6-month and 12-month PHM samples during tensiometric testing. This may, in part, be due to the increased levels of collagen type I deposition in the PHM samples.

After a graft is implanted, it undergoes remodeling and integration, and often, its scaffold is degraded and resorbed by the host.[13] If this degradation is not followed by cellular infiltration and ECM deposition, the mesh matrix can be replaced by a scar, resulting in the weakening of the repaired tissue.[19] The rate of scaffold degradation and replacement is also a key factor in tissue remodeling.[19] The mechanical properties of the ECM scaffolds change during the process of remodeling, and the changes are dependent on factors such as the microenvironment of the local tissue, the rate of scaffold degradation, and ECM deposition by infiltrating cells.[23],[24] Failure of biologic meshes may be due to a rapid degradation of the graft without adequate replacement by the host.[13] Although studies have shown that noncross-linked grafts showed better remodeling, this remodeling was not associated with stronger native tissue replacement in the long term.[25] In biologic prosthetics, the long-term remodeling ultimately determines future tensiometric strength of the repaired area. We observed that portions of the PDM were replaced by adipocytes in the 2-month group [Figure 7]a and [Figure 7]b that may have contributed to the lower tensiometric strength of the repaired fascia at both the 6- and 12-month time points. The reason for higher tensiometric strength in the PHM samples at 6 and 12 months may be related to the degradation rate of the ECM backbone of the graft. The PDM graft utilized in this study, Strattice™, is manufactured in a proprietary manner to reduce the antigenic response in the host by removing terminal galactose-a-(1,3)-galactose from porcine tissue.[26] This may have reduced the antigenic response of the implanted tissue resulting in weaker cytokine response and downstream-reduced regeneration and/or remodeling. The more robust appearance of the harvested PHM repaired group might have been an indication of a differently remodeled tissue.

The trichrome stains demonstrate a greater percentage of collagenous tissue in the 2-month and 6-month PHM groups when compared to the comparative PDM groups while 12-month samples did not show a significant difference. The structure of the porcine hepatic ECM may facilitate earlier cellular infiltration resulting in more rapid collagen deposition at the repair site. In addition, the hematoxylin and eosin stains demonstrated greater inflammation and fibrosis in the PHM groups at 1, 2, and 12 months [Table 1]. This cellular response may also be contributing to the increased strength of repair.

MMPs are implicated in the degradation of biological meshes in vivo, and they have been shown to reduce the tensile strength of the bioprosthetics in vitro.[27] Immediately after the mesh implantation, during the initial wound healing stages of inflammation and proliferation, many cytokines and MMP levels increase to help in the incorporation of the implant in the remodeling process.[28] We have seen a higher level of MMP-2 and 9 at the 1- and 2-month time points in PHM repairs, but after 6 months, these levels decreased with a significantly lower level of these MMPs seen at 12 months. Although speculative, we feel this corresponds with a reduction in degradation and remodeling at the PHM site, while the PDM continues to demonstrate remodeling and degradation at both 6 and 12 months. It will be interesting to further investigate the relationships between MMP levels, collagen, and tensiometric strength at additional time points to gain a better understanding of these relationships.

There are some limitations associated with this study. The first limitation is that the hernias were repaired in the acute phase. Prior studies in the literature describe the importance of allowing the hernia defect to mature before performing a repair to take into account the fibrosis and changes to the abdominal wall that occur with a chronic hernia.[29],[30] However, the purpose of this study was not to evaluate the hernia repair in the chronic setting, but in the acute setting such as a trauma. We aimed to evaluate the mesh incorporation and strength through this study. Repairing the hernia in the acute setting for evaluation of such factors has been performed in prior studies.[31],[32],[33]

Another limitation of the study is that there were only clean cases examined. Therefore, it is not possible to conclude whether the results will be the same in a contaminated case. However, since there are no prior animal model studies using porcine hepatic mesh for repair of ventral hernias, it is prudent to evaluate the mesh in a clean setting before introducing confounding factors such as contamination. Futures studies evaluating the outcomes of porcine hepatic meshes in contaminated surgical fields are needed.

Given that biologic meshes are effective in improving the strength of a primary closure, the porcine hepatic mesh can be considered a reasonable alternative to the porcine dermal mesh in clean, acute ventral hernia repairs.


  Conclusions Top


In an experimental porcine model, outcomes with a porcine hepatic mesh for a clean ventral hernia repair demonstrated comparable clinical outcomes to repair with a porcine dermal matrix. The tensiometric strength of a ventral hernia repair with a porcine hepatic mesh is significantly greater than that of a porcine dermal graft repair in this model.

Financial support and sponsorship

This study was funded in part from a grant to the University of Kentucky from Miromatrix.

Conflicts of interest

Dr. Roth reports a grant (to University of Kentucky) from Miromatrix during the conduct of the study, personal fees from Miromatrix as a consultant, and stock ownership in Miromatrix; a research grant with Bard; consulting and speaking for Allergan and Bard are outside the scope of the submitted work. The other authors have nothing to disclose.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
 
 
    Tables

  [Table 1]



 

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