In vivo  Implantation of a Bovine-Derived Collagen Membrane Leads to Changes in the Physiological Cellular Pattern of Wound Healing by the Induction of Multinucleated Giant Cells: An Adverse Reaction?

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Abstract

The present study evaluated the tissue response toward a resorbable collagen membrane derived from bovine achilles tendon (test group) in comparison to physiological wound healing (control group). After subcutaneous implantation in Wistar rats over 30 days, histochemical and immunohistochemical methods elucidated the cellular inflammatory response, vascularization pattern, membrane protein and cell absorbance capacity. After 30 days, the test-group induced two different inflammatory patterns. On the membrane surface, multinucleated giant cells (MNGCs) were formed after the accumulation of CD-68-positive cells (macrophages), whereas only mononuclear cells (MNCs) were found within the membrane central region. Peri-implant vascularization was significantly enhanced after the formation of MNGCs. No vessels were found within the central region of the membrane. Physiological wound healing revealed no MNGCs at any time point. These dynamic changes in the cellular reaction and vascularization within the test-group are related typical indications of a foreign body reaction. Due to the membrane-specific porosity, mononuclear cells migrated into the central region, and the membrane maintained its integrity over 30 days by showing no breakdown or disintegration. The ex vivo investigation analyzed the interaction between the membrane and a blood concentrate system, liquid platelet-rich fibrin (liquid PRF), derived from human peripheral blood and consisting of platelets, leukocytes and fibrin. PRF penetrated the membrane after just 15 min. The data question the role of biomaterial-induced MNGCs as a pathological reaction and whether this is acceptable to trigger vascularization or should be considered as an adverse reaction. Therefore, further pre-clinical and clinical studies are needed to identify the types of MNGCs that are induced by clinically approved biomaterials.

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Synthetic bone graft substitutes.

Rebecca Moore, Peter Bain, Gabrielle S. Graves (2001)

Replacement of extensive local bone loss is a significant clinical challenge. There are a variety of techniques available to the surgeon to manage this problem, each with their own advantages and disadvantages. It is well known that there is morbidity associated with harvesting of autogenous bone graft and limitations in the quantity of bone available. Alternatively allografts have been reported to have a significant incidence of postoperative infection and fracture as well as the potential risk of disease transmission. During the past 30 years a variety of synthetic bone graft substitutes has been developed with the aim to minimize these complications. The benefits of synthetic grafts include availability, sterility and reduced morbidity. The present article examines the relevance of synthetic bone graft substitutes, their mechanical properties and clinical application.

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Characterization of topographical effects on macrophage behavior in a foreign body response model.

Sulin Chen, Jacqueline Jones, Yongan Xu … (2010)

Current strategies to limit macrophage adhesion, fusion and fibrous capsule formation in the foreign body response have focused on modulating material surface properties. We hypothesize that topography close to biological scale, in the micron and nanometric range, provides a passive approach without bioactive agents to modulate macrophage behavior. In our study, topography-induced changes in macrophage behavior was examined using parallel gratings (250 nm-2 mum line width) imprinted on poly(epsilon-caprolactone) (PCL), poly(lactic acid) (PLA) and poly(dimethyl siloxane) (PDMS). RAW 264.7 cell adhesion and elongation occurred maximally on 500 nm gratings compared to planar controls over 48 h. TNF-alpha and VEGF secretion levels by RAW 264.7 cells showed greatest sensitivity to topographical effects, with reduced levels observed on larger grating sizes at 48 h. In vivo studies at 21 days showed reduced macrophage adhesion density and degree of high cell fusion on 2 mum gratings compared to planar controls. It was concluded that topography affects macrophage behavior in the foreign body response on all polymer surfaces examined. Topography-induced changes, independent of surface chemistry, did not reveal distinctive patterns but do affect cell morphology and cytokine secretion in vitro, and cell adhesion in vivo particularly on larger size topography compared to planar controls. Copyright 2010 Elsevier Ltd. All rights reserved.

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Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat.

Jürgen Becker, Frank Schwarz, Daniel Rothamel … (2005)

The aim of the present study was to compare the biodegradation of differently cross-linked collagen membranes in rats. Five commercially available and three experimental membranes (VN) were included: (1) BioGide (BG) (non-cross-linked porcine type I and III collagens), (2) BioMend (BM), (3) BioMendExtend (BME) (glutaraldehyde cross-linked bovine type I collagen), (4) Ossix (OS) (enzymatic-cross-linked bovine type I collagen), (5) TutoDent (TD) (non-cross-linked bovine type I collagen, and (6-8) VN(1-3) (chemical cross-linked porcine type I and III collagens). Specimens were randomly allocated in unconnected subcutaneous pouches separated surgically on the back of 40 wistar rats, which were divided into five groups (2, 4, 8, 16, and 24 weeks), including eight animals each. After 2, 4, 8, 16, and 24 weeks of healing, the rats were sacrificed and explanted specimens were prepared for histologic and histometric analysis. The following parameters were evaluated: biodegradation over time, vascularization, tissue integration, and foreign body reaction. Highest vascularization and tissue integration was noted for BG followed by BM, BME, and VN(1); TD, VN(2), and VN(3) showed prolongated, while OS exhibited no vascularization. Subsequently, biodegradation of BG, BM, BME and VN(1) was faster than TD, VN(2), and VN(3). OS showed only a minute amount of superficial biodegradation 24 weeks following implantation. Biodegradation of TD, BM, BME, VN(2), and VN(3) was associated with the presence of inflammatory cells. Within the limits of the present study, it was concluded that cross-linking of bovine and porcine-derived collagen types I and III was associated with (i) prolonged biodegradation, (ii) decreased tissue integration and vascularization, and (iii) in case of TD, BM, BME, VN(2), and VN(3) foreign body reactions.

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Author and article information

Contributors

Sarah Al-Maawi: URI : http://loop.frontiersin.org/people/534025/overview

Anna Orlowska: URI : http://loop.frontiersin.org/people/533806/overview

Shahram Ghanaati: URI : http://loop.frontiersin.org/people/533224/overview

Journal

Journal ID (nlm-ta): Front Bioeng Biotechnol

Journal ID (iso-abbrev): Front Bioeng Biotechnol

Journal ID (publisher-id): Front. Bioeng. Biotechnol.

Title: Frontiers in Bioengineering and Biotechnology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2296-4185

Publication date (Electronic): 14 August 2018

Publication date Collection: 2018

Volume: 6

Electronic Location Identifier: 104

Affiliations

[1] ¹Department for Oral, Cranio-Maxillofacial and Facial Plastic Surgery, Frankfurt Orofacial Regenerative Medicine Lab, University Hospital Frankfurt Goethe University , Frankfurt am Main, Germany

[2] ²Department of Oral and Maxillofacial Surgery, Medical University of Graz , Graz, Austria

Author notes

Edited by: Amir Ghaemmaghami, University of Nottingham, United Kingdom

Reviewed by: Martin (Marco) Harmsen, University Medical Center Groningen, Netherlands; Saeid Kargozar, Tehran University of Medical Sciences, Iran; Xin Zhao, Hong Kong Polytechnic University, Hong Kong

*Correspondence: Shahram Ghanaati shahram.ghanaati@ 123456kgu.de

This article was submitted to Biomaterials, a section of the journal Frontiers in Bioengineering and Biotechnology

Article

DOI: 10.3389/fbioe.2018.00104

PMC ID: 6102314

PubMed ID: 30155464

SO-VID: 9d260822-5c77-4e40-a98e-9e5f892add62

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This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 04 March 2018

Date accepted : 05 July 2018

Page count

Figures: 6, Tables: 0, Equations: 0, References: 36, Pages: 13, Words: 8860

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In vivo Implantation of a Bovine-Derived Collagen Membrane Leads to Changes in the Physiological Cellular Pattern of Wound Healing by the Induction of Multinucleated Giant Cells: An Adverse Reaction?

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Vascular Biology

Most cited references 28

Synthetic bone graft substitutes.

Characterization of topographical effects on macrophage behavior in a foreign body response model.

Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat.

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