Skip to main content

Main menu

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Advertisers
    • Editorial Board
  • Other Publications
    • Anticancer Research
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
  • About Us
    • General Policy
    • Contact
  • Other Publications
    • In Vivo
    • Anticancer Research
    • Cancer Genomics & Proteomics

User menu

  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart

Search

  • Advanced search
In Vivo
  • Other Publications
    • In Vivo
    • Anticancer Research
    • Cancer Genomics & Proteomics
  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart
In Vivo

Advanced Search

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Advertisers
    • Editorial Board
  • Other Publications
    • Anticancer Research
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
  • About Us
    • General Policy
    • Contact
  • Visit iiar on Facebook
  • Follow us on Linkedin
Research ArticleExperimental Studies

Republication: In Vitro and Ex Vivo Analysis of Collagen Foams for Soft and Hard Tissue Regeneration

OLE JUNG, MIKE BARBECK, LU FAN, FABIAN KORTE, CUIFENG ZHAO, RUMEN KRASTEV, SVEN PANTERMEHL and XIN XIONG
In Vivo January 2023, 37 (1) 320-328; DOI: https://doi.org/10.21873/invivo.13082
OLE JUNG
1Clinic and Policlinic for Dermatology and Venereology, University Medical Center Rostock, Rostock, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
MIKE BARBECK
2BerlinAnalytix GmbH, Berlin, Germany;
3Department of Ceramic Materials, Chair of Advanced Ceramic Materials, Institute for Materials Science and Technologies, Technical University Berlin, Berlin, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
LU FAN
4NMI Natural and Medical Sciences Institute at the University of Tübingen, Reutlingen, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
FABIAN KORTE
4NMI Natural and Medical Sciences Institute at the University of Tübingen, Reutlingen, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
CUIFENG ZHAO
5Faculty of Applied Chemistry, Reutlingen University, Reutlingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
RUMEN KRASTEV
4NMI Natural and Medical Sciences Institute at the University of Tübingen, Reutlingen, Germany;
5Faculty of Applied Chemistry, Reutlingen University, Reutlingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
SVEN PANTERMEHL
1Clinic and Policlinic for Dermatology and Venereology, University Medical Center Rostock, Rostock, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
XIN XIONG
2BerlinAnalytix GmbH, Berlin, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: xin.xiong@nmi.de
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Abstract

Background/Aim: The aim of this study was the conception, production, material analysis and cytocompatibility analysis of a new collagen foam for medical applications. Materials and Methods: After the innovative production of various collagen sponges from bovine sources, the foams were analyzed ex vivo in terms of their structure (including pore size) and in vitro in terms of cytocompatibility according to EN ISO 10993-5/-12. In vitro, the collagen foams were compared with the established biomaterials cerabone and Jason membrane. Materials cerabone and Jason membrane. Results: Collagen foams with different compositions were successfully produced from bovine sources. Ex vivo, the foams showed a stable and long-lasting primary structure quality with a bubble area of 1,000 to 2,000 μm2. In vitro, all foams showed sufficient cytocompatibility. Conclusion: Collagen sponges represent a promising material for hard and soft tissue regeneration. Future studies could focus on integrating and investigating different additives in the foams.

Key Words:
  • Collagen
  • collagen foam
  • tissue regeneration
  • macrophages
  • vascularization
  • soft tissue
  • hard tissue

Collagen is the most abundant protein in the human body and constitutes around 25-30% of the total amount of protein (1, 2). Up to now, 28 different types of collagen have been discovered (3). As an essential part of the extracellular matrix (ECM), different collagen types can be found in bones, cartilage, tendons and skin, as well as in teeth, cornea and blood vessels (4-6). Collagen is biocompatible and completely biodegradable by endogenous human proteases (7, 8). In addition, it is characterized by its ability to positively influence cell adhesion, cell proliferation, and differentiation (1, 4, 9). These qualities can be further increased by adding growth and differentiation factors to the collagen matrix (10, 11). Antibacterial properties can be developed by adding nanoparticles such as AgNP (12, 13). By additional physical as well as chemical cross-linking (6-8, 14) or the combination of different types of collagen with and without additional bioabsorbable materials, the usually short-lasting degradation time of natural collagen can be further extended, which ensures a sufficient durability (e.g., in wound dressings) (15, 16).

These properties make collagen as one of the most promising biomaterials in modern medicine. Depending on the area of application, it is obtained autogenously, allogenically or xenogenically (17, 18). Collagen is widely used as a wound dressing in the treatment of acute or chronic wounds (19), burn wounds (20, 21) or sites of skin donation and skin grafts (22), through its ability of shielding the wound from infection and contamination, reducing scarring, absorbing wound exudate, and promoting the skin’s natural regeneration ability (19, 23, 24). In addition, collagen is able to bind platelets and thus activate the coagulation cascade (25, 26), which makes it very suitable for acute use in wound care. Resorbable barrier membranes made of collagen are of great importance in guided bone regeneration (GBR) for dentistry and oral and maxillofacial surgery, in order to shield the regenerating bone from the ingrowth of the surrounding tissue (27-29). Furthermore, different compositions of collagen can be used as tissue grafts in peripheral nerve regeneration, vascular prostheses and arterial reconstruction (30-33). In addition, by promoting cell growth and adhesion, collagen is ideally suited as a substance in tissue engineering, where it can be used as part of bioinks to encapsulate cells (34, 35) or as basic substance for scaffold production (2, 22). Thereby, it is essential for the development of artificial skin implants (36, 37).

The present study aimed to develop a new collagen foam based on bovine split skin for tissue regeneration. The regeneration-promoting properties of collagen are extensively described in literature (4, 15, 38). Especially for wound regeneration, collagen foams appear to be a promising approach, since a foam can optimally adapt to a wound bed in terms of area and volume and has both a shielding and cushioning effect on the tissue (19). The approach of using biomaterials as applicable foams in wound management has already been implemented in a different context. The wound foams that have been used up to now are primarily designed for the care of moist or weeping chronic wounds, as their base materials have good exudate-absorbing characteristics (19).

With the use of collagen and the creation of a moisturizing instead of a dehumidifying environment in the wound bed, the foam presented in this study aims to positively influence the self-healing of soft tissue by using the natural regenerative properties of this biomaterial. The newly developed collagen-based foam has the potential to be a new and innovative biomaterial for use in soft tissue regeneration and could play a major role in the care of patients with acute or chronic wounds.

The focus of this preclinical study was to analyze the material characteristics and cytocompatibility of different novel collagen foams. For this purpose, pore size, density and surface structure of the foams were examined and described ex vivo using a dynamic foam analyzer (DFA) and cryo-SEM. In addition, in vitro cytocompatibility studies were carried out in accordance with ISO 10993-5/-12, as already described in previous work (24, 39, 40).

Materials and Methods

Collagen foam preparation. For fabricating the collagen foam, bovine split skin was homogenized via serial mechanical treatment steps, as illustrated in Figure 1. Briefly, split skin was thawed at 4°C. Then, the split skin was rinsed in double-deionized water (ddH2O) which was added at a ratio of 6.5:1 (w/w) to the split skin. The split skin was then rinsed under agitation using a paddle mixer (IKA® Digital 20, IKA® Works, Inc., Wilmington, NC, USA) at 70 rpm for 3 h and pre-homogenized at 720 rpm for another 3 h. The pH value was adjusted to 2.9 with HAc (acetic acid water solution). The suspension was stored at room temperature overnight before further processing. After adjusting the pH value to 3.2, the split skin suspension was homogenized with an IKA® Ultra-Turrax homogenizer (IKA® Works, Inc.) (about 12,000 rpm) for 1 min. The homogenization was then treated in a water bath at 75° for 1 h. The treated suspension was further diluted using 0.1% HAc at a ratio of 1:1 and filtered via a Buchner Funnel. The filtered suspension was then foamed using a foaming paddle to form liquid collagen foam. Foams with a final protein concentration ranging from 10 to 50 mg/ml were prepared.

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

Processing of collagen foam.

Ex vivo analyses. Pore structure and foam characterization. For determination of the bubble size and size distribution of the collagen foams, a dynamic foam analyzer (DFA100, Krüss GmbH, Hamburg, Germany) equipped with a CCD-camera was applied. Size and amount of the bubble fractions were determined via the “bubbles’ different projected area” method (Figures 2 and 3).

Figure 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 2.

Macroscopic and microscopic imaging of the collagen foam. (A) Freshly prepared collagen foam. (B) Freeze dried foam for light-microscopic slides. As the foam was lyophilized, the pore size was not directly correlated to the pore size in foam.

Figure 3.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 3.

FIB-cryo-SEM imaging of the foam. (A) Image with a full width of 100 μm. The structure of the collagen foam can be observed. The bubbles were organized in an oriented structure during foam formation. (B) Image with a full length of 17.09 μm. The bubble shown in the image has a diameter of about 14 μm and the foam lamella can be observed clearly.

Cryo focus ion beam/Scanning electron microscopy (SEM). Collagen foams with a final concentration of 20 mg/ml were analyzed by cryo-SEM. Briefly, the sample was frozen in liquid nitrogen. Without removing the sample from the liquid nitrogen, it was mounted onto a cooled sample holder. The holder was transferred into a vacuum shuttle (Leica EM VCT100, Leica Microsystems GmbH, Wetzlar, Hessen, Germany). After loading, the shuttle was connected immediately to a sputter coater (Balt-Tec SCD 500, Leica Biosystems Division of Leica Microsystems Inc., Buffalo Grove, IL, USA) and evacuated so that the sample could be transferred to the cryo stage of the electron microscope (Zeiss LEO 1540XB with cryo stage, Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Baden-Württemberg, Germany). The sample was then imaged with the electron beam and the stage was heated until sublimation of the ice matrix could be observed, which occurred around −100°C. The sample was transferred after coating with about 10 nm of platinum. Using a focused ion beam, the cross section of the samples was prepared and imaged with SEM.

In vitro experiments. The cytocompatibility analysis was conducted according to the DIN EN ISO 10993-5: 2009/-12: 2012 regulations as previously published (24, 27, 39). In brief, each of two collagen foam samples with final concentrations of 10 mg/ml or 30 mg/ml were used for the extract assays. The samples were extracted for 72±2 h in extraction medium at 37°C, 5% CO2 and 95% humidity. The extraction medium was then transferred to L-929 mouse fibroblasts, purchased from the European Collection of Cell Cultures, ECACC (Salisbury, UK) and incubated with the cells at standard cell culture conditions; 37°C, 5% CO2 and 95% humidity for 24 h. Viability, proliferation and cytotoxicity determinations were carried out using the XTT assay (Roche Diagnostics, Mannheim, Germany), BrdU ELISA (Roche Diagnostics) and LDH assay (BioVision, Milpitas, CA, USA) in four determinations for each test sample. As comparative materials with expectable biocompatibility, Jason® membrane and Cerabone® (both from botiss biomaterials GmbH, Zossen, Germany) were used for additional extract assays and examined under the same conditions, as already described above. Blank values (only medium without cells, also in quadruple determination) were subtracted from all values. Furthermore, RM-A test samples [polyurethane film with 0.1% zinc diethyldithiocarbamate (ZDEC) (Hatano Research Institute, Food and Drug Safety Center, Hadano, Japan) were used as positive control materials. As negative control, grade 4 titanium plates were incubated under the above-described extraction conditions.

Statistics. An analysis of variance (ANOVA), which enabled comparison of the data from the study groups via the GraphPad Prism 8.0 software (GraphPad Software Inc., La Jolla, CA, USA) was conducted for statistical analysis. Statistical differences were designated as significant if the p-values were less than 0.05 (*p≤0.05), and highly significant if the p-values were less than 0.01 (**p≤0.01) or less than 0.001 (***p≤0.001). Finally, the data are shown as mean±standard deviation.

Results

Results of the ex vivo measurements. DFA bubble structure and distribution depending on collagen density.

The number of bubbles and the size distribution of the collagen foam bubbles were analyzed via DFA and shown in Figure 4. The left panel shows the real-time images of the bubbles within the foams. The green dots show the relative uniform sizes of the produced foam. Projection areas of the most foam bubbles were measured between 1000 μm2 and 2000 μm2, indicating diameters ranging from 46μm to 94 μm. The largest bubble population had 28-48 μm diameter (20 mg/ml). The black line and red line for bubble count and mean bubble area, depending on time, showed the relatively high stability and uniformity of the prepared foam.

Figure 4.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 4.

Bubble counts and distribution. The main fraction of the collagen foam has a bubble area of 1,000 to 2,000 μm2, which is equivalent to an average diameter of about 36 to 50 μm.

Results of the in vitro measurements. According to ISO 10993-5:2009, non-toxic ranges are defined for values >70% of the blank sample for BrdU and XTT assays and for values <30% of the positive control for LDH assays. The collagen foam showed satisfactory biocompatibility in both concentrations tested (Figure 5). Thereby, a significant difference (p≤0.001) compared to the positive control was shown in all three assays. In the BrdU and XTT assays, only a minor significant difference (p≤0.01) compared to the negative control was measured at the concentration of 10 mg/ml. At the concentration of 30 mg/ml, however, there was no significant difference compared to the negative control. In the LDH assay, both collagen foams showed significant differences to the positive control and values below the 30%-threshold. The established reference materials Jason® membrane and Cerabone® showed also highly cytocompatible results in both the XTT and BrdU assay with no significant differences to the negative control. In the LDH assay, both materials showed significant differences to the positive control and were below the 30%-threshold (p≤0.001).

Figure 5.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 5.

Cytocompatibility results using L929 cells in the different assays. (A) proliferation measured by BrdU assay; (B) viability measured by the Sodium 3,3′-[1(phenylamino)carbonyl]-3,4-tetrazolium]-3is(4-methoxy-6-nitro) Benzene Sulfonic acid Hydrate (XTT)-assay; (C) cytotoxicity measured by the Lactate Dehydrogenase (LDH) assay. Values were normalized against blind control. Means with error bars indicate standard deviations. Dotted line indicates thresholds which should not be exceeded (LDH) or undershot (XTT, BrdU). Significant differences are declared (*p≤0.01, **p≤0.001). MC: Medium control; NC: negative control (titanium grade 4); PC: positive control; CF: collagen foam.

Discussion

Collagen-based biomaterials are an essential element for soft tissue management with special focus on wound care. For example, collagen materials are frequently used for acute and chronic wounds as well as burns after surgical interventions (15, 16, 19, 20). The advantage of collagen is based on its proliferation-, differentiation- and adhesion-promoting properties, which favor early vascularization and therefore rapid tissue regeneration (1, 4, 9). In addition, collagen-based biomaterials are able to absorb liquids many times of their own weight and bind reactive oxygen as well as nitrogen species, which could also interfere with tissue regeneration (41, 42).

Until today, biomaterials for soft tissue regeneration like wound foams consist mainly of polyurethanes, hydro fibers or mixtures of these two materials, which absorb wound exudate in large volumes and thereby, create favorable conditions for wound healing (43, 44). Depending on the manufacturer, some foam dressings are additionally coated with silicone layers, which fixate the foam in the wound bed. Furthermore, foam dressings provide thermal isolation and protect the wound from bacteria and infections (43, 44). Another favorable advantage of current foams is their ability to completely fill out the wound beds, which reduces the remaining dead space for bacterial colonization and possible infections (45-47).

However, current available foam dressings also feature some disadvantages. Due to their strong fluid-absorbing properties, they are suitable for use on moderately to severely exudative wounds, but are contraindicated e.g., for use in very dry or necrotic wound areas (47). Most foams can be left on the wound bed for up to a week before they need to be removed (48). However, with removal there is always the risk of additional shear stress to the already agitated lesion, especially if newly formed tissue has already grown into the foam. The same applies to patients with very sensitive skin and the use of additional fixations for the foam dressings, which have to be removed with change of the dressing and thus can damage the newly formed tissue.

By using collagen as the basic material for a new type of wound foam, it could be possible to combine the regeneration-promoting properties of collagen with the advantages of a flexible foam, being able to adapt to any size and volume of the wound bed. A major advantage would be the ability to integrate the collagen directly into the wound bed as part of the newly formed ECM, which could make subsequent removal unnecessary and constantly supports tissue regeneration. Furthermore, by adjusting the liquid content of the foam, a moistening environment can be achieved for special indications like dry wounds. Therefore, the aim of the present study was to examine the macro- and micro-structure of an innovative collagen foam ex vivo and to investigate its cytocompatibility in vitro according to DIN ISO 10993. This new foam dressing could address and improve wound management for a broad range of applications.

First of all, the structure of the newly created collagen foam with a final concentration of 20 mg/ml was examined ex vivo using FIB-cryo-SEM and DFA. It could be shown that the bubbles in the foam were mainly uniform in diameter (~36-50 μm) and area (~1,000-2,000 μm2) and also distributed homogeneously within the foam (~600/mm2). Furthermore, the number and size of the bubbles remained constant over the total observation period of 5 min. These results suggest that the process used to produce the collagen foam can create a uniform microstructure within it. Collagen, as a natural component of human ECM, has binding sites for adhesion of fibroblasts, macrophages and epithelial cells, which is utilized in the creation of wound sponges or scaffolds in 3D-printing, both with defined pore sizes (49, 50). It is assumed that a constant pore size between 100-200 μm is optimal to enable the surrounding cells to proliferate and adhere to the surrounding porous structure (49, 50). These observations suggest that collagen foams should also provide this ideal pore size and distribution, with additional beneficial effect on tissue regeneration. In reference to our own measured values for the projection area and diameter of the bubbles formed, we assume similar advantageous attributes for enabling the foam to have a positive effect on the adhesion and ingrowth of the surrounding connective tissue cells. These possibilities should be further addressed in future studies. Furthermore, bubble size seems to decrease with an increasing viscosity of the foam. Since a higher viscosity could ensure a better hold within the wound and thus make the use of additional fixation systems redundant, it is important to carry out further investigations addressing more closely with the above-mentioned hypotheses.

In vitro, the foam showed sufficient cytocompatibility in all colorimetric assays for both tested concentrations. It could be shown that there were no significant differences to the negative control for the higher concentration (30 mg/ml), while mild significant differences (p≤0.05) to the negative control were found for the lower concentration (20 mg/ml), which, however, appear to be negligible. The results of the reference materials for soft and hard tissue regeneration, Cerabone® and Jason® membrane, showed a good cytocompatibility in all colorimetric assays.

The results obtained for the collagen foam in the present study are congruent with previous observations, revealing that collagen, as natural and ubiquitous component of ECM, shows little to no damaging effects on the surrounding tissue, thus having sufficient biocompatibility (17, 51, 52). However, additional in vitro assays could be used in order to analyze the properties and regenerative qualities of the foam in an even more differentiated manner. For example, it would be possible to further survey the differentiation processes of stem cells or primary cell lines that are potentially induced by the foam (53, 54). In addition, quantitative and qualitative measurement of the release of pro- or anti-inflammatory cytokines by immunologically active cell lines would give additional information about inflammation processes in the presence of the collagen foam. Nevertheless, the presented in vitro results require future in vivo investigations in order to analyze tissue reactions of the foam using histological, histomorphometrical and immunohistochemical assays. In this context, additional loading of the foam, e.g., with silver nanoparticles or platelet-rich plasma (PRP), could be an interesting approach.

Altogether, the present study shows satisfactory in vitro compatibility of the newly developed collagen foams. It also shows that both reference materials, Cerabone® and Jason® membrane, are highly biocompatible materials for soft and hard tissue regeneration. The analysis of the microstructure reveals the effectiveness of the manufacturing process to create a homogeneous microstructure of the foam with mostly consistent bubble size and diameter. Taken together, these results suggest that collagen foams show the potential to be a promising new biomaterial for tissue regeneration, especially for wounds. Future additional studies, particularly addressing tissue responses in vivo, are required to emphasize the present results.

Acknowledgements

This work was supported by the Federal Ministry for Economic Affairs and Energy (BMWI-FKZ: ZF4289210AW8).

Footnotes

  • Authors’ Contributions

    Conceptualization, O.J., M.B. and X.X.; methodology, O.J., M.B. and X.X.; software, X.X.; validation, O.J. and M.B.; formal analysis, O.J and S.P.; Preparation of collagen foams and mixture with BSM, C.F.Z and F.K.; the DFA analysis and data calculation, C.F.Z and F.K.; investigation, O.J. and M.B.; resources, O.J. and M.B.; data curation, S.P.; writing—original draft preparation, O.J. and S.P..; writing—review and editing, M.B and X.X..; visualization, S.P.; supervision, O.J. and M.B.; project administration, O.J., M.B. and X.X.; funding acquisition, O.J., M.B. and R.K.

  • Republication Note

    The paper entitled “In Vitro and Ex Vivo Analysis of Collagen Foams for Soft and Hard Tissue Regeneration” by Jung et al., has been originally published in In Vivo 35(5): 2541–2549, 2021, and was retracted by the journal in September 2022 due to the Authors’ data management failure, which led to misinterpretation of the cytocompatibility results. The retraction note was published in In Vivo 36(5): 2530, 2022. Following careful consideration of the explanations of the researcher responsible for the data analysis, the article is republished with the correct data from the LDH assay. The correction has no impact on the significance of the results nor on the conclusions of the article.

  • This article is freely accessible online.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in relation to this study.

  • Received March 19, 2021.
  • Revision received June 18, 2021.
  • Accepted June 23, 2021.
  • Copyright © 2023, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved

References

  1. ↵
    1. Wang X,
    2. Wang G,
    3. Liu L and
    4. Zhang D
    : The mechanism of a chitosan-collagen composite film used as biomaterial support for MC3T3-E1 cell differentiation. Sci Rep 6: 39322, 2016. PMID: 28000715. DOI: 10.1038/srep39322
    OpenUrlCrossRefPubMed
  2. ↵
    1. Kozłowska J and
    2. Sionkowska A
    : Effects of different crosslinking methods on the properties of collagen-calcium phosphate composite materials. Int J Biol Macromol 74: 397-403, 2015. PMID: 25542169. DOI: 10.1016/j.ijbiomac.2014.12.023
    OpenUrlCrossRefPubMed
  3. ↵
    1. Gordon MK and
    2. Hahn RA
    : Collagens. Cell Tissue Res 339(1): 247-257, 2010. PMID: 19693541. DOI: 10.1007/s00441-009-0844-4
    OpenUrlCrossRefPubMed
  4. ↵
    1. Mousavi S,
    2. Khoshfetrat AB,
    3. Khatami N,
    4. Ahmadian M and
    5. Rahbarghazi R
    : Comparative study of collagen and gelatin in chitosan-based hydrogels for effective wound dressing: Physical properties and fibroblastic cell behavior. Biochem Biophys Res Commun 518(4): 625-631, 2019. PMID: 31447120. DOI: 10.1016/j.bbrc.2019.08.102
    OpenUrlCrossRefPubMed
    1. Aslan B,
    2. Guler S,
    3. Tevlek A and
    4. Aydin HM
    : Evaluation of collagen foam, poly(l-lactic acid) nanofiber mesh, and decellularized matrices for corneal regeneration. J Biomed Mater Res B Appl Biomater 106(6): 2157-2168, 2018. PMID: 29024376. DOI: 10.1002/jbm.b.34022
    OpenUrlCrossRefPubMed
  5. ↵
    1. Sionkowska A
    : Modification of collagen films by ultraviolet irradiation. Polymer Degradation and Stability 68(2): 147-151, 2020. DOI: 10.1016/S0141-3910(99)00176-7
    OpenUrlCrossRef
  6. ↵
    1. Usha R,
    2. Sreeram KJ and
    3. Rajaram A
    : Stabilization of collagen with EDC/NHS in the presence of L-lysine: a comprehensive study. Colloids Surf B Biointerfaces 90: 83-90, 2012. PMID: 22019452. DOI: 10.1016/j.colsurfb.2011.10.002
    OpenUrlCrossRefPubMed
  7. ↵
    1. Chau DY,
    2. Collighan RJ,
    3. Verderio EA,
    4. Addy VL and
    5. Griffin M
    : The cellular response to transglutaminase-cross-linked collagen. Biomaterials 26(33): 6518-6529, 2005. PMID: 15927250. DOI: 10.1016/j.biomaterials.2005.04.017
    OpenUrlCrossRefPubMed
  8. ↵
    1. Cai Z and
    2. Yang G
    : Bacterial cellulose/collagen composite: Characterization and first evaluation of cytocompatibility. J Appl Polymer Sci 120: 2938-2944, 2011. DOI: 10.1002/app.33318
    OpenUrlCrossRef
  9. ↵
    1. McPherson JM
    : The utility of collagen-based vehicles in delivery of growth factors for hard and soft tissue wound repair. Clin Mater 9(3-4): 225-234, 1992. PMID: 10149973. DOI: 10.1016/0267-6605(92)90103-z
    OpenUrlCrossRefPubMed
  10. ↵
    1. Nakamura R,
    2. Katsuno T,
    3. Kitamura M,
    4. Yamashita M,
    5. Tsuji T,
    6. Suzuki R,
    7. Kishimoto Y,
    8. Suehiro A,
    9. Tateya I,
    10. Nakamura T and
    11. Omori K
    : Collagen sponge scaffolds containing growth factors for the functional regeneration of tracheal epithelium. J Tissue Eng Regen Med 13(5): 835-845, 2019. PMID: 30808067. DOI: 10.1002/term.2835
    OpenUrlCrossRefPubMed
  11. ↵
    1. Alarcon EI,
    2. Udekwu K,
    3. Skog M,
    4. Pacioni NL,
    5. Stamplecoskie KG,
    6. González-Béjar M,
    7. Polisetti N,
    8. Wickham A,
    9. Richter-Dahlfors A,
    10. Griffith M and
    11. Scaiano JC
    : The biocompatibility and antibacterial properties of collagen-stabilized, photochemically prepared silver nanoparticles. Biomaterials 33(19): 4947-4956, 2012. PMID: 22494887. DOI: 10.1016/j.biomaterials.2012.03.033
    OpenUrlCrossRefPubMed
  12. ↵
    1. Li R,
    2. Xu Z,
    3. Jiang Q,
    4. Zheng Y,
    5. Chen Z and
    6. Chen X
    : Characterization and biological evaluation of a novel silver nanoparticle-loaded collagen-chitosan dressing. Regen Biomater 7(4): 371-380, 2020. PMID: 32793382. DOI: 10.1093/rb/rbaa008
    OpenUrlCrossRefPubMed
  13. ↵
    1. Sionkowska A,
    2. Skopinska-Wisniewska J,
    3. Gawron M,
    4. Kozlowska J and
    5. Planecka A
    : Chemical and thermal cross-linking of collagen and elastin hydrolysates. Int J Biol Macromol 47(4): 570-577, 2010. PMID: 20713081. DOI: 10.1016/j.ijbiomac.2010.08.004
    OpenUrlCrossRefPubMed
  14. ↵
    1. Pallaske F,
    2. Pallaske A,
    3. Herklotz K and
    4. Boese-Landgraf J
    : The significance of collagen dressings in wound management: a review. J Wound Care 27(10): 692-702, 2018. PMID: 30332361. DOI: 10.12968/jowc.2018.27.10.692
    OpenUrlCrossRefPubMed
  15. ↵
    1. Bunyaratavej P and
    2. Wang HL
    : Collagen membranes: a review. J Periodontol 72(2): 215-229, 2001. PMID: 11288796. DOI: 10.1902/jop.2001.72.2.215
    OpenUrlCrossRefPubMed
  16. ↵
    1. Chattopadhyay S and
    2. Raines RT
    : Review collagen-based biomaterials for wound healing. Biopolymers 101(8): 821-833, 2014. PMID: 24633807. DOI: 10.1002/bip.22486
    OpenUrlCrossRefPubMed
  17. ↵
    1. Avila Rodríguez MI,
    2. Rodríguez Barroso LG and
    3. Sánchez ML
    : Collagen: A review on its sources and potential cosmetic applications. J Cosmet Dermatol 17(1): 20-26, 2018. PMID: 29144022. DOI: 10.1111/jocd.12450
    OpenUrlCrossRefPubMed
  18. ↵
    1. Moura LI,
    2. Dias AM,
    3. Carvalho E and
    4. de Sousa HC
    : Recent advances on the development of wound dressings for diabetic foot ulcer treatment—a review. Acta Biomater 9(7): 7093-7114, 2013. PMID: 23542233. DOI: 10.1016/j.actbio.2013.03.033
    OpenUrlCrossRefPubMed
  19. ↵
    1. Bagheri Miyab K,
    2. Alipoor E,
    3. Vaghardoost R,
    4. Saberi Isfeedvajani M,
    5. Yaseri M,
    6. Djafarian K and
    7. Hosseinzadeh-Attar MJ
    : The effect of a hydrolyzed collagen-based supplement on wound healing in patients with burn: A randomized double-blind pilot clinical trial. Burns 46(1): 156-163, 2020. PMID: 31859087. DOI: 10.1016/j.burns.2019.02.015
    OpenUrlCrossRefPubMed
  20. ↵
    1. Yoon D,
    2. Cho YS,
    3. Joo SY,
    4. Seo CH and
    5. Cho YS
    : A clinical trial with a novel collagen dermal substitute for wound healing in burn patients. Biomater Sci 8(3): 823-829, 2020. PMID: 31782425. DOI: 10.1039/c9bm01209e
    OpenUrlCrossRefPubMed
  21. ↵
    1. Ng KW,
    2. Khor HL and
    3. Hutmacher DW
    : In vitro characterization of natural and synthetic dermal matrices cultured with human dermal fibroblasts. Biomaterials 25(14): 2807-2818, 2004. PMID: 14962559. DOI: 10.1016/j.biomaterials.2003.09.058
    OpenUrlCrossRefPubMed
  22. ↵
    1. Ghanaati S,
    2. Kovács A,
    3. Barbeck M,
    4. Lorenz J,
    5. Teiler A,
    6. Sadeghi N,
    7. Kirkpatrick CJ and
    8. Sader R
    : Bilayered, non-cross-linked collagen matrix for regeneration of facial defects after skin cancer removal: a new perspective for biomaterial-based tissue reconstruction. J Cell Commun Signal 10(1): 3-15, 2016. PMID: 26660939. DOI: 10.1007/s12079-015-0313-7
    OpenUrlCrossRefPubMed
  23. ↵
    1. Jung O,
    2. Radenkovic M,
    3. Stojanović S,
    4. Lindner C,
    5. Batinic M,
    6. Görke O,
    7. Pissarek J,
    8. Pröhl A,
    9. Najman S and
    10. Barbeck M
    : In Vitro and In Vivo biocompatibility analysis of a new transparent collagen-based wound membrane for tissue regeneration in different clinical indications. In Vivo 34(5): 2287-2295, 2020. PMID: 32871752. DOI: 10.21873/invivo.12040
    OpenUrlAbstract/FREE Full Text
  24. ↵
    1. Farndale RW,
    2. Sixma JJ,
    3. Barnes MJ and
    4. de Groot PG
    : The role of collagen in thrombosis and hemostasis. J Thromb Haemost 2(4): 561-573, 2004. PMID: 15102010. DOI: 10.1111/j.1538-7836.2004.00665.x
    OpenUrlCrossRefPubMed
  25. ↵
    1. Kawamoto Y and
    2. Kaibara M
    : Procoagulant activity of collagen. Effect of difference in type and structure of collagen. Biochim Biophys Acta 1035(3): 361-368, 1990. PMID: 2207130. DOI: 10.1016/0304-4165(90)90101-2
    OpenUrlCrossRefPubMed
  26. ↵
    1. Barbeck M,
    2. Kühnel L,
    3. Witte F,
    4. Pissarek J,
    5. Precht C,
    6. Xiong X,
    7. Krastev R,
    8. Wegner N,
    9. Walther F and
    10. Jung O
    : Degradation, bone regeneration and tissue response of an innovative volume stable magnesium-supported gbr/gtr barrier membrane. Int J Mol Sci 21(9): 3098, 2020. PMID: 32353983. DOI: 10.3390/ijms21093098
    OpenUrlCrossRefPubMed
    1. Lee SW and
    2. Kim SG
    : Membranes for the guided bone regeneration. Maxillofac Plast Reconstr Surg 36(6): 239-246, 2014. PMID: 27489841. DOI: 10.14402/jkamprs.2014.36.6.239
    OpenUrlCrossRefPubMed
  27. ↵
    1. Tal H,
    2. Moses O,
    3. Kozlovsky A and
    4. Nemcovsky C
    : Bioresorbable collagen membranes for guided bone regeneration. Bone Regeneration, 2016. DOI: 10.5772/34667
    OpenUrlCrossRef
  28. ↵
    1. Griffin JW,
    2. Hogan MV,
    3. Chhabra AB and
    4. Deal DN
    : Peripheral nerve repair and reconstruction. J Bone Joint Surg Am 95(23): 2144-2151, 2013. PMID: 24306702. DOI: 10.2106/JBJS.L.00704
    OpenUrlAbstract/FREE Full Text
    1. Lin MY,
    2. Manzano G and
    3. Gupta R
    : Nerve allografts and conduits in peripheral nerve repair. Hand Clin 29(3): 331-348, 2013. PMID: 23895714. DOI: 10.1016/j.hcl.2013.04.003
    OpenUrlCrossRefPubMed
    1. Zhang F,
    2. Xie Y,
    3. Celik H,
    4. Akkus O,
    5. Bernacki SH and
    6. King MW
    : Engineering small-caliber vascular grafts from collagen filaments and nanofibers with comparable mechanical properties to native vessels. Biofabrication 11(3): 035020, 2019. PMID: 30943452. DOI: 10.1088/1758-5090/ab15ce
    OpenUrlCrossRefPubMed
  29. ↵
    1. Leal BBJ,
    2. Wakabayashi N,
    3. Oyama K,
    4. Kamiya H,
    5. Braghirolli DI and
    6. Pranke P
    : Vascular tissue engineering: Polymers and methodologies for small caliber vascular grafts. Front Cardiovasc Med 7: 592361, 2021. PMID: 33585576. DOI: 10.3389/fcvm.2020.592361
    OpenUrlCrossRefPubMed
  30. ↵
    1. Yeo M,
    2. Lee JS,
    3. Chun W and
    4. Kim GH
    : An innovative collagen-based cell-printing method for obtaining human adipose stem cell-laden structures consisting of core-sheath structures for tissue engineering. Biomacromolecules 17(4): 1365-1375, 2016. PMID: 26998966. DOI: 10.1021/acs.biomac.5b01764
    OpenUrlCrossRefPubMed
  31. ↵
    1. Lee HJ,
    2. Kim YB,
    3. Ahn SH,
    4. Lee JS,
    5. Jang CH,
    6. Yoon H,
    7. Chun W and
    8. Kim GH
    : A new approach for fabricating collagen/ECM-based bioinks using preosteoblasts and human adipose stem cells. Adv Healthc Mater 4(9): 1359-1368, 2015. PMID: 25874573. DOI: 10.1002/adhm.201500193
    OpenUrlCrossRefPubMed
  32. ↵
    1. Lee V,
    2. Singh G,
    3. Trasatti JP,
    4. Bjornsson C,
    5. Xu X,
    6. Tran TN,
    7. Yoo SS,
    8. Dai G and
    9. Karande P
    : Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods 20(6): 473-484, 2014. PMID: 24188635. DOI: 10.1089/ten.TEC.2013.0335
    OpenUrlCrossRefPubMed
  33. ↵
    1. Koch L,
    2. Kuhn S,
    3. Sorg H,
    4. Gruene M,
    5. Schlie S,
    6. Gaebel R,
    7. Polchow B,
    8. Reimers K,
    9. Stoelting S,
    10. Ma N,
    11. Vogt PM,
    12. Steinhoff G and
    13. Chichkov B
    : Laser printing of skin cells and human stem cells. Tissue Eng Part C Methods 16(5): 847-854, 2010. PMID: 19883209. DOI: 10.1089/ten.TEC.2009.0397
    OpenUrlCrossRefPubMed
  34. ↵
    1. Ferreira AM,
    2. Gentile P,
    3. Chiono V and
    4. Ciardelli G
    : Collagen for bone tissue regeneration. Acta Biomater 8(9): 3191-3200, 2012. PMID: 22705634. DOI: 10.1016/j.actbio.2012.06.014
    OpenUrlCrossRefPubMed
  35. ↵
    1. Jung O,
    2. Smeets R,
    3. Hartjen P,
    4. Schnettler R,
    5. Feyerabend F,
    6. Klein M,
    7. Wegner N,
    8. Walther F,
    9. Stangier D,
    10. Henningsen A,
    11. Rendenbach C,
    12. Heiland M,
    13. Barbeck M and
    14. Kopp A
    : Improved in vitro test procedure for full assessment of the cytocompatibility of degradable magnesium based on ISO 10993-5/-12. Int J Mol Sci 20(2): 255, 2019. PMID: 30634646. DOI: 10.3390/ijms20020255
    OpenUrlCrossRefPubMed
  36. ↵
    1. Steigmann L,
    2. Jung O,
    3. Kieferle W,
    4. Stojanovic S,
    5. Proehl A,
    6. Görke O,
    7. Emmert S,
    8. Najman S,
    9. Barbeck M and
    10. Rothamel D
    : Biocompatibility and immune response of a newly developed volume-stable magnesium-based barrier membrane in combination with a PVD coating for guided bone regeneration (GBR). Biomedicines 8(12): 636, 2020. PMID: 33419327. DOI: 10.3390/biomedicines8120636
    OpenUrlCrossRefPubMed
  37. ↵
    1. Metzmacher I,
    2. Ruth P,
    3. Abel M and
    4. Friess W
    : In vitro binding of matrix metalloproteinase-2 (MMP-2), MMP-9, and bacterial collagenase on collagenous wound dressings. Wound Repair Regen 15(4): 549-555, 2007. PMID: 17650099. DOI: 10.1111/j.1524-475X.2007.00263.x
    OpenUrlCrossRefPubMed
  38. ↵
    1. Schönfelder U,
    2. Abel M,
    3. Wiegand C,
    4. Klemm D,
    5. Elsner P and
    6. Hipler UC
    : Influence of selected wound dressings on PMN elastase in chronic wound fluid and their antioxidative potential in vitro. Biomaterials 26(33): 6664-6673, 2005. PMID: 15978664. DOI: 10.1016/j.biomaterials.2005.04.030
    OpenUrlCrossRefPubMed
  39. ↵
    1. Chaganti P,
    2. Gordon I,
    3. Chao JH and
    4. Zehtabchi S
    : A systematic review of foam dressings for partial thickness burns. Am J Emerg Med 37(6): 1184-1190, 2019. PMID: 31000315. DOI: 10.1016/j.ajem.2019.04.014
    OpenUrlCrossRefPubMed
  40. ↵
    1. Stoica AE,
    2. Chircov C and
    3. Grumezescu AM
    : Nanomaterials for wound dressings: an up-to-date overview. Molecules 25(11): 2699, 2020. PMID: 32532089. DOI: 10.3390/molecules25112699
    OpenUrlCrossRefPubMed
  41. ↵
    1. Hilton JR,
    2. Williams DT,
    3. Beuker B,
    4. Miller DR and
    5. Harding KG
    : Wound dressings in diabetic foot disease. Clin Infect Dis 39 Suppl 2: S100-S103, 2004. PMID: 15306987. DOI: 10.1086/383270
    OpenUrlCrossRefPubMed
    1. Jeffcoate WJ,
    2. Price P,
    3. Harding KG and International Working Group on Wound Healing and Treatments for People with Diabetic Foot Ulcers
    : Wound healing and treatments for people with diabetic foot ulcers. Diabetes Metab Res Rev 20(Suppl 1): S78-S89, 2004. PMID: 15150819. DOI: 10.1002/dmrr.476
    OpenUrlCrossRefPubMed
  42. ↵
    1. Weller CD,
    2. Team V and
    3. Sussman G
    : First-line interactive wound dressing update: A comprehensive review of the evidence. Front Pharmacol 11: 155, 2020. PMID: 32180720. DOI: 10.3389/fphar.2020.00155
    OpenUrlCrossRefPubMed
  43. ↵
    1. O’Meara S and
    2. Martyn-St James M
    : Foam dressings for venous leg ulcers. Cochrane Database Syst Rev (5): CD009907, 2013. PMID: 23728697. DOI: 10.1002/14651858.CD009907.pub2
    OpenUrlCrossRefPubMed
  44. ↵
    1. Janik H and
    2. Marzec M
    : A review: fabrication of porous polyurethane scaffolds. Mater Sci Eng C Mater Biol Appl 48: 586-591, 2015. PMID: 25579961. DOI: 10.1016/j.msec.2014.12.037
    OpenUrlCrossRefPubMed
  45. ↵
    1. Song X,
    2. Zhu C,
    3. Fan D,
    4. Mi Y,
    5. Li X,
    6. Fu RZ,
    7. Duan Z,
    8. Wang Y and
    9. Feng RR
    : A Novel human-like collagen hydrogel scaffold with porous structure and sponge-like properties. Polymers (Basel) 9(12): 638, 2017. PMID: 30966005. DOI: 10.3390/polym9120638
    OpenUrlCrossRefPubMed
  46. ↵
    1. Jung O,
    2. Radenkovic M,
    3. StojanoviĆ S,
    4. Lindner C,
    5. Batinic M,
    6. Görke O,
    7. Pissarek J,
    8. Pröhl A,
    9. Najman S and
    10. Barbeck M
    : In Vitro and In Vivo biocompatibility analysis of a new transparent collagen-based wound membrane for tissue regeneration in different clinical indications. In Vivo 34(5): 2287-2295, 2020. PMID: 32871752. DOI: 10.21873/invivo.12040
    OpenUrlAbstract/FREE Full Text
  47. ↵
    1. Gueldenpfennig T,
    2. Houshmand A,
    3. Najman S,
    4. Stojanovic S,
    5. Korzinskas T,
    6. Smeets R,
    7. Gosau M,
    8. Pissarek J,
    9. Emmert S,
    10. Jung O and
    11. Barbeck M
    : 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 34(3): 985-1000, 2020. PMID: 32354884. DOI: 10.21873/invivo.11867
    OpenUrlAbstract/FREE Full Text
  48. ↵
    1. Ahmed U,
    2. Ahmed R,
    3. Masoud MS,
    4. Tariq M,
    5. Ashfaq UA,
    6. Augustine R and
    7. Hasan A
    : Stem cells based in vitro models: trends and prospects in biomaterials cytotoxicity studies. Biomed Mater 16(4): 042003, 2021. PMID: 33686970. DOI: 10.1088/1748-605X/abe6d8
    OpenUrlCrossRefPubMed
  49. ↵
    1. Jablonská E,
    2. Horkavcová D,
    3. Rohanová D and
    4. Brauer DS
    : A review of in vitro cell culture testing methods for bioactive glasses and other biomaterials for hard tissue regeneration. J Mater Chem B 8(48): 10941-10953, 2020. DOI: 10.1039/d0tb01493a
    OpenUrlCrossRefPubMed
PreviousNext
Back to top

In this issue

In Vivo: 37 (1)
In Vivo
Vol. 37, Issue 1
January-February 2023
  • Table of Contents
  • Table of Contents (PDF)
  • About the Cover
  • Index by author
  • Back Matter (PDF)
  • Ed Board (PDF)
  • Front Matter (PDF)
Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on In Vivo.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Republication: In Vitro and Ex Vivo Analysis of Collagen Foams for Soft and Hard Tissue Regeneration
(Your Name) has sent you a message from In Vivo
(Your Name) thought you would like to see the In Vivo web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
7 + 3 =
Solve this simple math problem and enter the result. E.g. for 1+3, enter 4.
Citation Tools
Republication: In Vitro and Ex Vivo Analysis of Collagen Foams for Soft and Hard Tissue Regeneration
OLE JUNG, MIKE BARBECK, LU FAN, FABIAN KORTE, CUIFENG ZHAO, RUMEN KRASTEV, SVEN PANTERMEHL, XIN XIONG
In Vivo Jan 2023, 37 (1) 320-328; DOI: 10.21873/invivo.13082

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Reprints and Permissions
Share
Republication: In Vitro and Ex Vivo Analysis of Collagen Foams for Soft and Hard Tissue Regeneration
OLE JUNG, MIKE BARBECK, LU FAN, FABIAN KORTE, CUIFENG ZHAO, RUMEN KRASTEV, SVEN PANTERMEHL, XIN XIONG
In Vivo Jan 2023, 37 (1) 320-328; DOI: 10.21873/invivo.13082
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Materials and Methods
    • Results
    • Discussion
    • Acknowledgements
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

  • No related articles found.
  • PubMed
  • Google Scholar

Cited By...

  • No citing articles found.
  • Google Scholar

More in this TOC Section

  • Systemic Administration of Lipopolysaccharide from Porphyromonas gingivalis Decreases Neprilysin Expression in the Mouse Hippocampus
  • Monitoring T-Cell Kinetics in the Early Recovery Period of Lung Transplantation Cases by Copy Number Levels of T-Cell Receptor Excision Circle
  • Successful Surgical Outcome of Feline Inductive Odontogenic Tumor in Three Cats
Show more Experimental Studies

Similar Articles

Keywords

  • Collagen
  • collagen foam
  • tissue regeneration
  • macrophages
  • vascularization
  • soft tissue
  • hard tissue
In Vivo

© 2023 In Vivo

Powered by HighWire