SUBCUTANEOUS TISSUE RESPONSE TO THE TWO IMPLANTED COLLAGEN-BASED MEMBRANES OF DIFFERENT ORIGIN
Abstract
Collagen, as the main structural protein in mammals, fulfils the fundamental requirements to be a ssuitable biomaterial component used in tissue engineering. Due to its biocompatibility and biodegradability, collagen can be utilized in various forms for guided soft and bone tissue regeneration. Collagen-based membranes, frequently used for both soft and hard tissue regeneration, can differ in their origin (porcine, bovine, equine), physicochemical characteristics such as architecture, porosity, absorption ability, and manufacturing processes which may influence tissue response and final outcome. In this study, we examined and compared tissue response to the two implanted collagen membranes of different origins: porcine vs. equine. The subcutaneous implantation model in BALB/c mice was used, and tissue response was evaluated 3, 10 and 30 days after implantation. Tissue was analyzed by histological and histomorphometric methods. Our study revealed variations in subcutaneous tissue response, patterns of cell infiltration into collagen membranes, and changes in membrane thickness and resorption that may be attributed to the differences in membrane origin but also to the differences in the manufacturing process. We can conclude that both membranes are suitable for application in guided tissue regeneration.
References
Abou Fadel R, Samarani R, Chakar C. Guided bone regeneration in calvarial critical size bony defect using a double-layer resorbable collagen membrane covering a xenograft: a histological and histomorphometric study in rats. Oral Maxillofac Surg 2018; 22(2): 203–13. [CrossRef] [PubMed]
Barbeck M, Lorenz J, Holthaus MG, Raetscho N, Kubesch A, Booms P, et al. Porcine Dermis and Pericardium-Based, Non–Cross-Linked Materials Induce Multinucleated Giant Cells After Their In Vivo Implantation: A Physiological Reaction? J Oral Implantol 2015; 41(6): e267–81. [CrossRef] [PubMed]
Barbeck M, Lorenz J, Kubesch A, Böhm N, Booms P, Choukroun J, et al. Porcine Dermis-Derived Collagen Membranes Induce Implantation Bed Vascularization Via Multinucleated Giant Cells: A Physiological Reaction? J Oral Implantol 2015; 41(6): e238–51. [CrossRef] [PubMed]
Behring J, Junker R, Walboomers XF, Chessnut B, Jansen JA. Toward guided tissue and bone regeneration: morphology, attachment, proliferation, and migration of cells cultured on collagen barrier membranes. A systematic review. Odontology 2008; 96(1): 1-11. [CrossRef] [PubMed]
Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu TM, Kowolik MJ, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—A materials perspective. Dental Mater 2012; 28(7): 703–21. [CrossRef] [PubMed]
Bozkurt A, Apel C, Sellhaus B, et al. Differences in degradation behavior of two non-cross-linked collagen barrier membranes: an in vitro and in vivo study. Clin Oral Impl Res 2014; 25(12): 1403-1411. [CrossRef] [PubMed]
Brunel G, Piantoni P, Elharar F, Benqué E, Marin P, Zahedi S. Regeneration of Rat Calvarial Defects Using a Bioabsorbable Membrane Technique: Influence of Collagen Cross-linking. J Periodontol 1996; 67(12): 1342-1348. [CrossRef] [PubMed]
Bunyaratavej P, Wang H-L. Collagen Membranes: A Review. Journal of Periodontol 2001; 72(2): 215-229. [CrossRef] [PubMed]
Calciolari E, Ravanetti F, Strange A, Mardas N, Bozec L, Cacchioli A, et al. Degradation pattern of a porcine collagen membrane in an in vivo model of guided bone regeneration. J Periodontal Res. 2018; 53(3): 430-439. [CrossRef] [PubMed]
Chevallay B, Herbage D. Collagen-based biomaterials as 3D scaffold for cell cultures: applications for tissue engineering and gene therapy. Med Biol Eng Comput 2000; 38(2):211-218. [CrossRef] [PubMed]
Ferreira AM, Gentile P, Chiono V, Ciardelli G. Collagen for bone tissue regeneration. Acta Biomaterialia 2012; 8(9):3191–200. [CrossRef] [PubMed]
Fidler AL, Boudko SP, Rokas A, Hudson BG. The triple helix of collagens – an ancient protein structure that enabled animal multicellularity and tissue evolution. J Cell Sci 2018; 131(7):jcs203950. [CrossRef] [PubMed]
Flaig I, Radenković M, Najman S, Pröhl A, Jung O, Barbeck M. In Vivo Analysis of the Biocompatibility and Immune Response of Jellyfish Collagen Scaffolds and its Suitability for Bone Regeneration. IJMS 2020; 21(12): 4518. [CrossRef] [PubMed]
Gauza-Włodarczyk M, Kubisz L, Włodarczyk D. Amino acid composition in determination of collagen origin and assessment ophysical factors effects.International Journal of Biological Macromolecules 2017; 104: 987–91. [CrossRef] [PubMed]
Ghanaati S. Non-cross-linked porcine-based collagen I–III membranes do not require high vascularization rates for their integration within the implantation bed: A paradigm shift. Acta Biomater 2012; 8(8): 3061–72 [CrossRef] [PubMed]
Gueldenpfennig T, Houshmand A, Najman S, Stojanovic S, Korzinskas T, Smeets R, et al. The Condensation of Collagen Leads to an Extended Standing Time and a Decreased Pro-inflammatory Tissue Response to a Newly Developed Pericardium-based Barrier Membrane for Guided Bone Regeneration. In Vivo 2020; 34(3): 985-1000. [CrossRef] [PubMed]
Herrera-Vizcaíno C, Al-Maawi S, Sader R, Kirkpatrick CJ, Choukroun J, Ghanaati S. Modification of collagen-based sponges can induce an upshift of the early inflammatory response and a chronic inflammatory reaction led by M1 macrophages: an in vivo study. Clin Oral Invest 2020; 24(10): 3485–500. [CrossRef] [PubMed]
Kazakos K, Lyras DN, Thomaidis V, et al. Application of PRP gel alone or in combination with guided bone regeneration does not enhance bone healing process: An experimental study in rabbits. J of Cranio-Maxillofac Surg 2011; 39(1): 49-53. [CrossRef] [PubMed]
Khan R, Khan M. Use of collagen as a biomaterial: An update. J Indian Soc Periodontol 2013; 17(4): 539. [CrossRef] [PubMed]
Khorramirouz R, Go JL, Noble C, Jana S, Maxson E, Lerman A, et al. A novel surgical technique for a rat subcutaneous implantation of a tissue engineered scaffold. Acta Histochem 2018; 120(3): 282-291. [CrossRef] [PubMed]
Korzinskas T, Jung O, Smeets R, Stojanovic S, Najman S, Glenske K, et al. In Vivo Analysis of the Biocompatibility and Macrophage Response of a Non-Resorbable PTFE Membrane for Guided Bone Regeneration. IJMS 2018; 19(10):2952. [CrossRef] [PubMed]
Kumar V, Cotran RS, Robbins SL. Osnove patologije, II. izdanje, Školska knjiga, Zagreb, 2000. (Serbian)
Lin K, Zhang D, Macedo MH, Cui W, Sarmento B, Shen G. Advanced Collagen-Based Biomaterials for Regenerative Biomedicine. Adv Funct Mater 2019; 29(3): 1804943. [CrossRef] [PubMed]
Meyer M. Processing of collagen based biomaterials and the resulting materials properties. BioMed Eng OnLine 2019; 18(1): 24. [CrossRef] [PubMed]
Moses O, Vitrial D, Aboodi G, Sculean A, Tal H, Kozlovsky A, et al. Biodegradation of Three Different Collagen Membranes in the Rat Calvarium: A Comparative Study. J Periodontol 2008; 79(5): 905-911. [CrossRef] [PubMed]
Owens KW, Yukna RA. Collagen Membrane Resorption in Dogs: A Comparative Study. Implant Dent 2001; 10(1): 49-58. [CrossRef] [PubMed]
Parvini P, Mihatovic I, Sahin D, Becker J, Schwarz F. Lateral alveolar ridge augmentation using an equine-derived collagen-containing bone block: A prospective case series. Clin Oral Implants Res 2022; 33(2): 142– 149. [CrossRef] [PubMed]
Rothamel D, Schwarz F, Sager M, Herten M, Sculean A, Becker J. Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat. Clin Oral Implants Res 2005; 16(3): 369-378. [CrossRef] [PubMed]
Wagner-Ecker M, Voltz P, Egermann M, Richter W. The collagen component of biological bone graft substitutes promotes ectopic bone formation by human mesenchymal stem cells. Acta Biomaterialia 2013; 9(7): 7298-7307. [CrossRef] [PubMed]
Willershausen I, Barbeck M, Boehm N, et al. Non-cross-linked collagen type I/III materials enhance cell proliferation: in vitro and in vivo evidence. J Appl Oral Sci 2014; 22(1): 29–37. [CrossRef] [PubMed]
