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Collagen-Based Medical Devices for Regenerative Medicine and Tissue Engineering

  • Review Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Assisted reproductive technologies are key to solving the problems of aging and organ defects. Collagen is compatible with living tissues and has many different chemical properties; it has great potential for use in reproductive medicine and the engineering of reproductive tissues. It is a natural substance that has been used a lot in science and medicine. Collagen is a substance that can be obtained from many different animals. It can be made naturally or created using scientific methods. Using pure collagen has some drawbacks regarding its physical and chemical characteristics. Because of this, when collagen is processed in various ways, it can better meet the specific needs as a material for repairing tissues. In simpler terms, collagen can be used to help regenerate bones, cartilage, and skin. It can also be used in cardiovascular repair and other areas. There are different ways to process collagen, such as cross-linking it, making it more structured, adding minerals to it, or using it as a carrier for other substances. All of these methods help advance the field of tissue engineering. This review summarizes and discusses the current progress of collagen-based materials for reproductive medicine.

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Abbreviations

GBR:

Guided bone regeneration

PTFE:

Polytetrafluoroethylene

GA:

Glutaraldehyde

hUC:

Human umbilical cords

MSCs:

Mesenchymal stem cells

PRP:

Platelet-rich plasma

HA:

Hydroxyapatite

TCP:

Tricalcium phosphate

GAGs:

Glycosaminoglycans

CG:

Collagen–glycosaminoglycans

PDGF:

Platelet-derived growth factor

CTC:

collagen-thermosensitive hydrogel-calcium phosphate

References

  1. Aamodt, J. M., & Grainger, D. W. (2016). Extracellular matrix-based biomaterial scaffolds and the host response. Biomaterials, 86, 68–82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Abou Fadel, R., Samarani, R., & Chakar, C. (2018). 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 and Maxillofacial Surgery, 22, 203–213.

    Article  PubMed  Google Scholar 

  3. Al-Nawas, B., & Schiegnitz, E. (2014). Augmentation procedures using bone substitute materials or autogenous bone - a systematic review and meta-analysis. European Journal of Oral Implantology, 7(Suppl 2), S219-234.

    PubMed  Google Scholar 

  4. Alford, A. I., Nicolaou, D., Hake, M., & McBride-Gagyi, S. (2021). Masquelet’s induced membrane technique: Review of current concepts and future directions. Journal of Orthopaedic Research, 39, 707–718.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Allan, B., Ruan, R., Landao-Bassonga, E., Gillman, N., Wang, T., Gao, J., Ruan, Y., Xu, Y., Lee, C., & Goonewardene, M. (2021). Collagen membrane for guided bone regeneration in dental and orthopedic applications. Tissue Engineering Part A, 27, 372–381.

    Article  PubMed  CAS  Google Scholar 

  6. Almutairi, A. S. (2019). A descriptive analysis of patient’s preferences in bone graft therapy in dentistry. International Journal of Health Sciences, 13, 24.

    PubMed  PubMed Central  Google Scholar 

  7. Alnojeidi, H., Kilani, R. T., & Ghahary, A. (2022). Evaluating the biocompatibility of an injectable wound matrix in a murine model. Gels, 8, 49.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Aluko, R. E. (2015). Antihypertensive peptides from food proteins. Annual Review of Food Science and Technology, 6, 235–262.

    Article  PubMed  CAS  Google Scholar 

  9. Amirrah, I. N., Lokanathan, Y., Zulkiflee, I., Wee, M., Motta, A., & Fauzi, M. B. (2022). A comprehensive review on collagen type I development of biomaterials for tissue engineering: from biosynthesis to bioscaffold. Biomedicines, 10(9), 2307.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Astachov, L., Vago, R., Aviv, M., & Nevo, Z. (2011). Hyaluronan and mesenchymal stem cells: From germ layer to cartilage and bone. Frontiers in Bioscience - Landmark, 16, 261–276.

    Article  CAS  Google Scholar 

  11. Attenello, N. H., & Maas, C. S. (2015). Injectable fillers: Review of material and properties. Facial Plastic Surgery, 31, 29–34.

    Article  PubMed  CAS  Google Scholar 

  12. Avila Rodriguez, M. I., Rodriguez Barroso, L. G., & Sanchez, M. L. (2018). Collagen: A review on its sources and potential cosmetic applications. Journal of Cosmetic Dermatology, 17, 20–26.

    Article  PubMed  Google Scholar 

  13. Awad, S., Dharmavaram, S., Wearn, C. S., Dube, M. G., & Lobo, D. N. (2012). Effects of an intraoperative infusion of 4% succinylated gelatine (Gelofusine(R)) and 6% hydroxyethyl starch (Voluven(R)) on blood volume. British Journal of Anaesthesia, 109, 168–176.

    Article  PubMed  CAS  Google Scholar 

  14. Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016). Molecular mechanisms of stress-responsive changes in collagen and elastin networks in skin. Skin Pharmacology and Physiology, 29, 190–203.

    Article  PubMed  CAS  Google Scholar 

  15. Balaji, V., Manikandan, D., & Ramsundar, A. (2020). Bone grafts in periodontics. Matrix Science Medica, 4, 57–63.

    Article  Google Scholar 

  16. Banerjee, I., Mishra, D., Das, T., Maiti, S., & Maiti, T. K. (2012). Caprine (goat) collagen: A potential biomaterial for skin tissue engineering. Journal of Biomaterials Science, Polymer Edition, 23, 355–373.

    Article  PubMed  CAS  Google Scholar 

  17. Bathla, S. C., Fry, R. R., & Majumdar, K. (2018). Maxillary sinus augmentation. Journal of Indian Society of Periodontology, 22, 468.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Baumann, L. S., Shamban, A. T., Lupo, M. P., Monheit, G. D., Thomas, J. A., Murphy, D. K., Walker, P. S., & Group, Jv. Z. N. F. S. (2007). Comparison of smooth-gel hyaluronic acid dermal fillers with cross-linked bovine collagen: a multicenter, double-masked, randomized, within-subject study. Dermatologic Surgery, 33(Suppl 2), S128-135.

    PubMed  CAS  Google Scholar 

  19. Bayrak, A., Pruger, P., Stock, U. A., & Seifert, M. (2013). Absence of immune responses with xenogeneic collagen and elastin. Tissue Engineering Part A, 19, 1592–1600.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Becker, J., Al-Nawas, B., Klein, M. O., Schliephake, H., Terheyden, H., & Schwarz, F. (2009). Use of a new cross-linked collagen membrane for the treatment of dehiscence-type defects at titanium implants: A prospective, randomized-controlled double-blinded clinical multicenter study. Clinical Oral Implants Research, 20, 742–749.

    Article  PubMed  Google Scholar 

  21. Becker, W., Dahlin, C., Becker, B. E., Lekholm, U., van Steenberghe, D., Higuchi, K., & Kultje, C. (1994). The use of e-PTFE barrier membranes for bone promotion around titanium implants placed into extraction sockets: A prospective multicenter study. International Journal of Oral and Maxillofacial Implants, 9, 31–40.

    PubMed  CAS  Google Scholar 

  22. Behring, J., Junker, R., Walboomers, X. F., Chessnut, B., & Jansen, J. A. (2008). Toward guided tissue and bone regeneration: Morphology, attachment, proliferation, and migration of cells cultured on collagen barrier membranes. A systematic review. Odontology, 96, 1–11.

    Article  PubMed  CAS  Google Scholar 

  23. Benic, G. I., Eisner, B. M., Jung, R. E., Basler, T., Schneider, D., & Hammerle, C. H. F. (2019). Hard tissue changes after guided bone regeneration of peri-implant defects comparing block versus particulate bone substitutes: 6-month results of a randomized controlled clinical trial. Clinical Oral Implants Research, 30, 1016–1026.

    Article  PubMed  Google Scholar 

  24. Benic, G. I., & Hammerle, C. H. (2000). (2014) Horizontal bone augmentation by means of guided bone regeneration. Periodontology, 66, 13–40.

    Article  Google Scholar 

  25. Benic, G. I., Thoma, D. S., Jung, R. E., Sanz-Martin, I., Unger, S., Cantalapiedra, A., & Hammerle, C. H. F. (2017). Guided bone regeneration with particulate vs. block xenogenic bone substitutes: A pilot cone beam computed tomographic investigation. Clinical Oral Implants Research, 28, e262–e270.

    Article  PubMed  Google Scholar 

  26. Boogaard, M. J., & Romanos, G. E. (2021). Allograft customized bone blocks for ridge reconstruction: A case report and radiological analysis. Applied Sciences, 11, 10413.

    Article  CAS  Google Scholar 

  27. Brum, I. S., Elias, C. N., de Carvalho, J. J., Pires, J. L. S., Pereira, M. J. S., & de Biasi, R. S. (2021). Properties of a bovine collagen type I membrane for guided bone regeneration applications. e-Polymers, 21, 210–221.

    Article  CAS  Google Scholar 

  28. Brunel, G., Piantoni, P., Elharar, F., Benque, E., Marin, P., & Zahedi, S. (1996). Regeneration of rat calvarial defects using a bioabsorbable membrane technique: Influence of collagen cross-linking. Journal of Periodontology, 67, 1342–1348.

    Article  PubMed  CAS  Google Scholar 

  29. Bunyaratavej, P., & Wang, H. L. (2001). Collagen membranes: A review. Journal of Periodontology, 72, 215–229.

    Article  PubMed  CAS  Google Scholar 

  30. Buser, D., Martin, W., & Belser, U. C. (2004). Optimizing esthetics for implant restorations in the anterior maxilla: Anatomic and surgical considerations. International Journal of Oral and Maxillofacial Implants, 19(Suppl), 43–61.

    PubMed  Google Scholar 

  31. Calciolari, E., Ravanetti, F., Strange, A., Mardas, N., Bozec, L., Cacchioli, A., Kostomitsopoulos, N., & Donos, N. (2018). Degradation pattern of a porcine collagen membrane in an in vivo model of guided bone regeneration. Journal of Periodontal Research, 53, 430–439.

    Article  PubMed  CAS  Google Scholar 

  32. Carpio, L., Loza, J., Lynch, S., & Genco, R. (2000). Guided bone regeneration around endosseous implants with anorganic bovine bone mineral. A randomized controlled trial comparing bioabsorbable versus non-resorbable barriers. Journal of Periodontology, 71, 1743–1749.

    Article  PubMed  CAS  Google Scholar 

  33. Cascone, S., & Lamberti, G. (2020). Hydrogel-based commercial products for biomedical applications: A review. International Journal of Pharmaceutics, 573, 118803.

    Article  PubMed  CAS  Google Scholar 

  34. Cespedes, R. D. (2000). Collagen injection or artificial sphincter for postprostatectomy incontinence: Collagen 1. Urology, 55, 5–7.

    Article  PubMed  CAS  Google Scholar 

  35. Chappuis, V., Araújo, M. G., & Buser, D. (2000). (2017) Clinical relevance of dimensional bone and soft tissue alterations post-extraction in esthetic sites. Periodontology, 73, 73–83.

    Article  Google Scholar 

  36. Charriere, G., Bejot, M., Schnitzler, L., Ville, G., & Hartmann, D. J. (1989). Reactions to a bovine collagen implant. Clinical and immunologic study in 705 patients. Journal of the American Academy of Dermatology, 21, 1203–1208.

    Article  PubMed  CAS  Google Scholar 

  37. Cheah, C. W., Al-Namnam, N. M., Lau, M. N., Lim, G. S., Raman, R., Fairbairn, P., & Ngeow, W. C. (2021). Synthetic material for bone, periodontal, and dental tissue regeneration: Where are we now, and where are we heading next? Materials, 14, 6123.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Chen, K., Sivaraj, D., Davitt, M. F., Leeolou, M. C., Henn, D., Steele, S. R., Huskins, S. L., Trotsyuk, A. A., Kussie, H. C., Greco, A. H., Padmanabhan, J., Perrault, D. P., Zamaleeva, A. I., Longaker, M. T., & Gurtner, G. C. (2022). Pullulan-collagen hydrogel wound dressing promotes dermal remodelling and wound healing compared to commercially available collagen dressings. Wound Repair and Regeneration, 30, 397–408.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Cheng, L.-Y., Sun, X.-M., Tang, M.-Y., Jin, R., Cui, W.-G., & Zhang, Y.-G. (2016). An update review on recent skin fillers. Plastic and Aesthetic Research, 3, 92–99.

    Article  Google Scholar 

  40. Cheng, L., Lin, T., Khalaf, A. T., Zhang, Y., He, H., Yang, L., Yan, S., Zhu, J., & Shi, Z. (2021). The preparation and application of calcium phosphate biomedical composites in filling of weight-bearing bone defects. Science and Reports, 11, 4283.

    Article  CAS  Google Scholar 

  41. Chia-Lai, P. J., Orlowska, A., Al-Maawi, S., Dias, A., Zhang, Y., Wang, X., Zender, N., Sader, R., Kirkpatrick, C. J., & Ghanaati, S. (2018). Sugar-based collagen membrane cross-linking increases barrier capacity of membranes. Clinical Oral Investigations, 22, 1851–1863.

    Article  PubMed  Google Scholar 

  42. Cho, K.-H., Uthaman, S., Park, I.-K., & Cho, C.-S. (2018). Injectable biomaterials in plastic and reconstructive surgery: A review of the current status. Tissue Eng. Regen. Med., 15, 559–574.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Choi, H. K., Cho, H. Y., Lee, S. J., Cho, I. W., Shin, H. S., Koo, K. T., Lim, H. C., & Park, J. C. (2017). Alveolar ridge preservation with an open-healing approach using single-layer or double-layer coverage with collagen membranes. Journal of Periodontal & Implant Science, 47, 372–380.

    Article  Google Scholar 

  44. Choi, S. M., Chaudhry, P., Zo, S. M., & Han, S. S. (2018). Advances in protein-based materials: From origin to novel biomaterials. Advances in Experimental Medicine and Biology, 1078, 161–210.

    Article  PubMed  CAS  Google Scholar 

  45. Coppola, D., Oliviero, M., Vitale, G. A., Lauritano, C., D’Ambra, I., Iannace, S., & de Pascale, D. (2020). Marine collagen from alternative and sustainable sources: Extraction, processing and applications. Marine Drugs, 18, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. D’Amato, S., Tartaro, G., Itro, A., Nastri, L., & Santagata, M. (2015). Block versus particulate/titanium mesh for ridge augmentation for mandibular lateral incisor defects: Clinical and histologic analysis. The International Journal of Periodontics & Restorative Dentistry, 35, e1-8.

    Article  Google Scholar 

  47. Davison-Kotler, E., Marshall, W. S., & Garcia-Gareta, E. (2019). Sources of collagen for biomaterials in skin wound healing. Bioengineering (Basel), 6, 56.

    Article  PubMed  CAS  Google Scholar 

  48. Davison-Kotler, E., Marshall, W. S., & García-Gareta, E. (2019). Sources of collagen for biomaterials in skin wound healing. Bioengineering, 6, 56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. De Witte, T.-M., Fratila-Apachitei, L. E., Zadpoor, A. A., & Peppas, N. A. (2018). Bone tissue engineering via growth factor delivery: From scaffolds to complex matrices. Regenerative Biomaterials, 5, 197–211.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Derkach, S. R., Voron’ko, N. G., Kuchina, Y. A., & Kolotova, D. S. (2020). Modified fish gelatin as an alternative to mammalian gelatin in modern food technologies. Polymers, 12, 3051.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Donaghue, V. M., Chrzan, J. S., Rosenblum, B. I., Giurini, J. M., Habershaw, G. M., & Veves, A. (1998). Evaluation of a collagen-alginate wound dressing in the management of diabetic foot ulcers. Advances in Wound Care, 11, 114–119.

    PubMed  CAS  Google Scholar 

  52. Ellingsworth, L. R., DeLustro, F., Brennan, J. E., Sawamura, S., & McPherson, J. (1986). The human immune response to reconstituted bovine collagen. The Journal of Immunology, 136, 877–882.

    Article  PubMed  CAS  Google Scholar 

  53. Eppley, B. L., & Dadvand, B. (2006). Injectable soft-tissue fillers: Clinical overview. Plastic and Reconstructive Surgery, 118, 98e–106e.

    Article  PubMed  Google Scholar 

  54. Feng, X. (2009). Chemical and biochemical basis of cell-bone matrix interaction in health and disease. Current Chemical Biology, 3, 189–196.

    PubMed  PubMed Central  CAS  Google Scholar 

  55. Ferraz, M. P. (2023). Bone grafts in dental medicine: An overview of autografts, allografts and synthetic materials. Materials, 16, 4117.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Ferreira, A. M., Gentile, P., Chiono, V., & Ciardelli, G. (2012). Collagen for bone tissue regeneration. Acta Biomaterialia, 8, 3191–3200.

    Article  PubMed  CAS  Google Scholar 

  57. Fertala, A. (2020). Three decades of research on recombinant collagens: reinventing the wheel or developing new biomedical products? Bioengineering (Basel), 7(4), 155.

    Article  PubMed  CAS  Google Scholar 

  58. Foegeding, E., Lanier, T., & Hultin, H. (1996). Collagen. Food Chemistry, 3, 902–906.

    Google Scholar 

  59. Friedmann, A., Gissel, K., Soudan, M., Kleber, B. M., Pitaru, S., & Dietrich, T. (2011). Randomized controlled trial on lateral augmentation using two collagen membranes: Morphometric results on mineralized tissue compound. Journal of Clinical Periodontology, 38, 677–685.

    Article  PubMed  CAS  Google Scholar 

  60. Fu, Y., Young, J. F., Løkke, M. M., Lametsch, R., Aluko, R. E., & Therkildsen, M. (2016). Revalorisation of bovine collagen as a potential precursor of angiotensin I-converting enzyme (ACE) inhibitory peptides based on in silico and in vitro protein digestions. Journal of Functional Foods, 24, 196–206.

    Article  CAS  Google Scholar 

  61. Gallo, N., Natali, M. L., Sannino, A., & Salvatore, L. (2020). An overview of the use of equine collagen as emerging material for biomedical applications. Journal of Functional Biomaterials, 11, 79.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Ge, B., Wang, H., Li, J., Liu, H., Yin, Y., Zhang, N., & Qin, S. (2020). Comprehensive assessment of Nile tilapia skin (Oreochromis niloticus) collagen hydrogels for wound dressings. Marine Drugs, 18, 178.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Ghadimi, K., Levy, J. H., & Welsby, I. J. (2016). Perioperative management of the bleeding patient. British Journal of Anaesthesia, 117, iii18–iii30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Grabowski, G., & Cornett, C. A. (2013). Bone graft and bone graft substitutes in spine surgery: Current concepts and controversies. Journal of American Academy of Orthopaedic Surgeons, 21, 51–60.

    Article  Google Scholar 

  65. Guarnieri, R., DeVilliers, P., & Belleggia, F. (2015). GBR using cross-linked collagen membrane and a new highly purified bovine xenograft (Laddec) in horizontal ridge augmentation: Case report of clinical and histomorphometric analysis. Quintessence International, 46, 717–724.

    PubMed  Google Scholar 

  66. Guo, Y., Cheng, N., Sun, H., Hou, J., Zhang, Y., Wang, D., Zhang, W., & Chen, Z. (2023). Advances in the development and optimization strategies of the hemostatic biomaterials. Frontiers in Bioengineering and Biotechnology, 10, 1062676.

  67. Guo, Y., Su, L., Chen, C., Liu, Y., & Li, J. (2022). Clinical efficacy and safety of different dental prosthetic membranes in guided bone regeneration during dental implants: a meta-analysis. Computational Intelligence and Neuroscience, 2022, 3245014.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Hammerle, C. H., & Jung, R. E. (2000). (2003) Bone augmentation by means of barrier membranes. Periodontology, 33, 36–53.

    Article  Google Scholar 

  69. Haugen, H. J., Lyngstadaas, S. P., Rossi, F., & Perale, G. (2019). Bone grafts: Which is the ideal biomaterial? Journal of Clinical Periodontology, 46, 92–102.

    Article  PubMed  Google Scholar 

  70. He, L., & Theato, P. (2013). Collagen and collagen mimetic peptide conjugates in polymer science. European Polymer Journal, 49, 2986–2997.

    Article  CAS  Google Scholar 

  71. Heng, C. H. Y., Snow, M., & Dave, L. Y. H. (2021). Single-stage arthroscopic cartilage repair with injectable scaffold and BMAC. Arthroscopy Techniques, 10, e751–e756.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Hirche, C., Senghaas, A., Fischer, S., Hollenbeck, S. T., Kremer, T., & Kneser, U. (2016). Novel use of a flowable collagen-glycosaminoglycan matrix (Integra Flowable Wound Matrix) combined with percutaneous cannula scar tissue release in treatment of post-burn malfunction of the hand–a preliminary 6 month follow-up. Burns, 42, e1–e7.

    Article  PubMed  CAS  Google Scholar 

  73. Hurzeler, M. B., Kohal, R. J., Naghshbandi, J., Mota, L. F., Conradt, J., Hutmacher, D., & Caffesse, R. G. (1998). Evaluation of a new bioresorbable barrier to facilitate guided bone regeneration around exposed implant threads. An experimental study in the monkey. International Journal of Oral and Maxillofacial Surgery, 27, 315–320.

    Article  PubMed  CAS  Google Scholar 

  74. Iasella, J. M., Greenwell, H., Miller, R. L., Hill, M., Drisko, C., Bohra, A. A., & Scheetz, J. P. (2003). Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: A clinical and histologic study in humans. Journal of Periodontology, 74, 990–999.

    Article  PubMed  Google Scholar 

  75. Inglefield, C., Samuelson, U. E., Landau, M., & DeVore, D. (2018). Bio-dermal restoration with rapidly polymerizing collagen: A multicenter clinical study. Aesthetic Surgery Journal, 38, 1131–1138.

    Article  PubMed  Google Scholar 

  76. Ionescu, A., Dodi, A., Petcu, L. C., & Nicolescu, M. I. (2022). Open healing: A minimally invasive protocol with flapless ridge preservation in implant patients. Biology, 11, 142.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Islam, M. S., Ebrahimi-Barough, S., Al Mahtab, M., Shirian, S., Aghayan, H. R., Arjmand, B., Allahverdi, A., Ranjbar, F. E., Sadeg, A. B., & Ai, J. (2022). Encapsulation of rat bone marrow-derived mesenchymal stem cells (rBMMSCs) in collagen type I containing platelet-rich plasma for osteoarthritis treatment in rat model. Progress in Biomaterials, 11, 385–396.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Jamal, N., Mundi, J., & Chhetri, D. K. (2014). Higher risk of superficial injection during injection laryngoplasty in women. American Journal of Otolaryngology, 35, 159–163.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Jang, C. H., Kim, W., & Kim, G. (2021). Effects of fibrous collagen/CDHA/hUCS biocomposites on bone tissue regeneration. International Journal of Biological Macromolecules, 176, 479–489.

    Article  PubMed  CAS  Google Scholar 

  80. Jiao, S., Zhang, X., Cai, H., Wu, S., Ou, X., Han, G., Zhao, J., Li, Y., Guo, W., Liu, T., & Qu, W. (2023). Recent advances in biomimetic hemostatic materials. Materials Today Bio, 19, 100592.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Jimenez Garcia, J., Berghezan, S., Carames, J. M. M., Dard, M. M., & Marques, D. N. S. (2017). Effect of cross-linked vs non-cross-linked collagen membranes on bone: A systematic review. Journal of Periodontal Research, 52, 955–964.

    Article  PubMed  CAS  Google Scholar 

  82. Kattimani, V. S., Kondaka, S., & Lingamaneni, K. P. (2016). Hydroxyapatite–past, present, and future in bone regeneration. Bone and Tissue Regeneration Insights, 7, BTRI.S36138.

    Article  Google Scholar 

  83. Keefe, J., Wauk, L., Chu, S., & DeLustro, F. (1992). Clinical use of injectable bovine collagen: A decade of experience. Clinical Materials, 9, 155–162.

    Article  PubMed  CAS  Google Scholar 

  84. Kesik-Brodacka, M. (2018). Progress in biopharmaceutical development. Biotechnology and Applied Biochemistry, 65, 306–322.

    Article  PubMed  CAS  Google Scholar 

  85. Khalaf, A. T., Wei, Y., Wan, J., Zhu, J., Peng, Y., Abdul Kadir, S. Y., Zainol, J., Oglah, Z., Cheng, L., & Shi, Z. (2022). Bone tissue engineering through 3D bioprinting of bioceramic scaffolds: A review and update. Life, 12, 903.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Kim, B. S., Choi, J. S., Kim, J. D., Yoon, H. I., Choi, Y. C., & Cho, Y. W. (2012). Human collagen isolated from adipose tissue. Biotechnology Progress, 28, 973–980.

    Article  PubMed  CAS  Google Scholar 

  87. Kim, H.-H., Lee, K. J., Kang, D. R., Lee, J. H., & Youn, Y.-N. (2023). Hemostatic efficacy of a flowable collagen-thrombin matrix during coronary artery bypass grafting: A double-blind randomized controlled trial. Journal of Cardiothoracic Surgery, 18, 193.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Kim, S. H., Kim, D. Y., Kim, K. H., Ku, Y., Rhyu, I. C., & Lee, Y. M. (2009). The efficacy of a double-layer collagen membrane technique for overlaying block grafts in a rabbit calvarium model. Clinical Oral Implants Research, 20, 1124–1132.

    Article  PubMed  Google Scholar 

  89. Kim, Y.-K., & Ku, J.-K. (2020). Extraction socket preservation. Journal of the Korean Association of Oral and Maxillofacial Surgeons, 46, 435–439.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Kim, Y.-K., Lee, J., Um, I.-W., Kim, K.-W., Murata, M., Akazawa, T., & Mitsugi, M. (2013). Tooth-derived bone graft material. Journal of the Korean Association of Oral and Maxillofacial Surgeons, 39, 103.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Kolerman, R., Qahaz, N., Barnea, E., Mijiritsky, E., Chaushu, L., Tal, H., & Nissan, J. (2020). Allograft and collagen membrane augmentation procedures preserve the bone level around implants after immediate placement and restoration. International Journal of Environmental Research and Public Health, 17(4), 1133.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Kontis, T. C., & Rivkin, A. (2009). The history of injectable facial fillers. Facial Plastic Surgery, 25, 67–72.

    Article  PubMed  CAS  Google Scholar 

  93. Kostopoulos, L., & Karring, T. (1994). Augmentation of the rat mandible using guided tissue regeneration. Clinical Oral Implants Research, 5, 75–82.

    Article  PubMed  CAS  Google Scholar 

  94. Kozlovsky, A., Aboodi, G., Moses, O., Tal, H., Artzi, Z., Weinreb, M., & Nemcovsky, C. E. (2009). Bio-degradation of a resorbable collagen membrane (Bio-Gide) applied in a double-layer technique in rats. Clinical Oral Implants Research, 20, 1116–1123.

    Article  PubMed  Google Scholar 

  95. Kretlow, J. D., Young, S., Klouda, L., Wong, M., & Mikos, A. G. (2009). Injectable biomaterials for regenerating complex craniofacial tissues. Advanced Materials, 21, 3368–3393.

    Article  PubMed  CAS  Google Scholar 

  96. Lake, S. P., Bradbury, K., Gagne, D. H., Deeken, C. R., Badhwar, A., & Bohnen, A. (2023). Efficacy of flowable collagen hemostat evaluated in preclinical models of liver injury and spinal cord exposure. Medical Devices (Auckl), 16, 123–132.

    CAS  Google Scholar 

  97. Laurano, R., Boffito, M., Ciardelli, G., & Chiono, V. (2022). Wound dressing products: A translational investigation from the bench to the market. Engineered Regeneration, 3, 182–200.

    Article  Google Scholar 

  98. Lee, C. R., Grodzinsky, A. J., & Spector, M. (2001). The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials, 22, 3145–3154.

    Article  PubMed  CAS  Google Scholar 

  99. Lee, D. W., Kim, K. T., Joo, Y. S., Yoo, M. K., Yu, J. A., & Ryu, J. J. (2015). The role of two different collagen membranes for dehiscence defect around implants in humans. The Journal of Oral Implantology, 41, 445–448.

    Article  PubMed  Google Scholar 

  100. Lee, H. S., Oh, K. J., Moon, Y. W., In, Y., Lee, H. J., & Kwon, S. Y. (2021). Intra-articular injection of type I atelocollagen to alleviate knee pain: A double-blind, randomized controlled trial. Cartilage, 13, 342S-350S.

    Article  PubMed  CAS  Google Scholar 

  101. León-López, A., Morales-Peñaloza, A., Martínez-Juárez, V. M., Vargas-Torres, A., Zeugolis, D. I., & Aguirre-Álvarez, G. (2019). Hydrolyzed collagen-sources and applications. Molecules, 24(22), 4031.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Li, D., Gao, Y., Wang, Y., Yang, X., He, C., Zhu, M., Zhang, S., & Mo, X. (2019). Evaluation of biocompatibility and immunogenicity of micro/nanofiber materials based on tilapia skin collagen. Journal of Biomaterials Applications, 33, 1118–1127.

    Article  PubMed  CAS  Google Scholar 

  103. Li, X. Y., Deng, W. S., Wang, Z. Q., Li, Z. C., Chen, S. L., Song, Z., Zhang, Q., Liang, J., & Chen, X. Y. (2023). Injectable collagen scaffold with human umbilical cord-derived mesenchymal stem cells promotes functional recovery in patients with spontaneous intracerebral hemorrhage: Phase I clinical trial. Neural Regeneration Research, 18, 1999–2004.

    PubMed  PubMed Central  CAS  Google Scholar 

  104. Li, Z., Du, T., Ruan, C., & Niu, X. (2021). Bioinspired mineralized collagen scaffolds for bone tissue engineering. Bioactive Materials, 6, 1491–1511.

    Article  PubMed  CAS  Google Scholar 

  105. Lim, Y.-S., Ok, Y.-J., Hwang, S.-Y., Kwak, J.-Y., & Yoon, S. (2019). Marine collagen as a promising biomaterial for biomedical applications. Marine Drugs, 17, 467.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Liu, S., Li, D., Chen, X., & Jiang, L. (2022). Biomimetic cuttlebone polyvinyl alcohol/carbon nanotubes/hydroxyapatite aerogel scaffolds enhanced bone regeneration. Colloids and Surfaces B, 210, 112221.

    Article  CAS  Google Scholar 

  107. Liu, W., Lin, H., Zhao, P., Xing, L., Li, J., Wang, Z., Ju, S., Shi, X., Liu, Y., Deng, G., Gao, G., Sun, L., & Zhang, X. (2022). A regulatory perspective on recombinant collagen-based medical devices. Bioactive Materials, 12, 198–202.

    Article  PubMed  CAS  Google Scholar 

  108. Liu, X., Fan, B., Abdelrehem, A., Ma, Z., & Yang, C. (2020). Membrane fixation for osseous graft stabilization in periodontally accelerated osteogenic orthodontics: A comparative study. BMC Oral Health, 20, 22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Liu, Y., Li, X., Jiang, C., Guo, H., Luo, G., Huang, Y., & Yuan, C. (2022). Clinical applications of concentrated growth factors membrane for sealing the socket in alveolar ridge preservation: A randomized controlled trial. International Journal of Implant Dentistry, 8, 46.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Lutz, R., & Kesting, M. (2023). Oral and maxillofacial surgery: surgical textbook and atlas (pp. 109–133). Springer.

    Book  Google Scholar 

  111. Mamede, A. P., Vassalo, A. R., Cunha, E., Goncalves, D., Parker, S. F., Batista de Carvalho, L. A. E., & Marques, M. P. M. (2018). Biomaterials from human bone - probing organic fraction removal by chemical and enzymatic methods. RSC Advances, 8, 27260–27267.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Martins, S. B., Oliveira, E., Castro, R. A., Sartori, M. G., Baracat, E. C., Lima, G. R., & Girao, M. J. (2007). Clinical and urodynamic evaluation in women with stress urinary incontinence treated by periurethral collagen injection. International Brazilian journal of urology, 33, 695–702. discussion 702-693.

    Article  PubMed  CAS  Google Scholar 

  113. Marx, G., Zacharowski, K., Ichai, C., Asehnoune, K., Cerny, V., Dembinski, R., Ferrer Roca, R., Fries, D., Molnar, Z., Rosenberger, P., Sanchez-Sanchez, M., Schurholz, T., Dehnhardt, T., Schmier, S., von Kleist, E., Brauer, U., & Simon, T. P. (2021). Efficacy and safety of early target-controlled plasma volume replacement with a balanced gelatine solution versus a balanced electrolyte solution in patients with severe sepsis/septic shock: Study protocol, design, and rationale of a prospective, randomized, controlled, double-blind, multicentric, international clinical trial: GENIUS-Gelatine use in ICU and sepsis. Trials, 22, 376.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Mellonig, J. T., Nevins, M., & Sanchez, R. (1998). Evaluation of a bioabsorbable physical barrier for guided bone regeneration. Part I. Material alone. The International Journal of Periodontics & Restorative Dentistry, 18(2), 139–49.

    CAS  Google Scholar 

  115. Meloni, S. M., Jovanovic, S. A., Urban, I., Baldoni, E., Pisano, M., & Tallarico, M. (2019). Horizontal ridge augmentation using GBR with a native collagen membrane and 1:1 ratio of particulate xenograft and autologous bone: A 3-year after final loading prospective clinical study. Clinical Implant Dentistry and Related Research, 21, 669–677.

    Article  PubMed  Google Scholar 

  116. Meloni, S. M., Jovanovic, S. A., Urban, I., Canullo, L., Pisano, M., & Tallarico, M. (2017). Horizontal ridge augmentation using GBR with a native collagen membrane and 1:1 ratio of particulated xenograft and autologous bone: A 1-year prospective clinical study. Clinical Implant Dentistry and Related Research, 19, 38–45.

    Article  PubMed  Google Scholar 

  117. Merli, M., Merli, I., Raffaelli, E., Pagliaro, U., Nastri, L., & Nieri, M. (2016). Bone augmentation at implant dehiscences and fenestrations. A systematic review of randomised controlled trials. European Journal of Oral Implantology, 9, 11–32.

    PubMed  Google Scholar 

  118. Meyer, M. (2019). Processing of collagen based biomaterials and the resulting materials properties. Biomedical Engineering Online, 18, 1–74.

    Article  Google Scholar 

  119. Micarelli, A., Viziano, A., Granito, I., Antonuccio, G., Felicioni, A., Loberti, M., Carlino, P., Micarelli, R. X., & Alessandrini, M. (2021). Combination of in-situ collagen injection and rehabilitative treatment in long-lasting facial nerve palsy: A pilot randomized controlled trial. European Journal of Physical and Rehabilitation Medicine, 57, 366–375.

    Article  PubMed  Google Scholar 

  120. Mir-Mari, J., Wui, H., Jung, R. E., Hammerle, C. H., & Benic, G. I. (2016). Influence of blinded wound closure on the volume stability of different GBR materials: An in vitro cone-beam computed tomographic examination. Clinical Oral Implants Research, 27, 258–265.

    Article  PubMed  Google Scholar 

  121. Mir-Mari, J., Benic, G. I., Valmaseda-Castellón, E., Hämmerle, C. H., & Jung, R. E. (2017). Influence of wound closure on the volume stability of particulate and non-particulate GBR materials: An in vitro cone-beam computed tomographic examination. Part II. Clinical Oral Implants Research, 28, 631–639.

    Article  PubMed  Google Scholar 

  122. Miyoshi, M., & Liu, S. (2018). Collagen-induced arthritis models. Methods in Molecular Biology, 1868, 3–7.

    Article  PubMed  CAS  Google Scholar 

  123. Mo, X., Zhang, D., Liu, K., Zhao, X., Li, X., & Wang, W. (2023). Nano-hydroxyapatite composite scaffolds loaded with bioactive factors and drugs for bone tissue engineering. International Journal of Molecular Sciences, 24, 1291.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Mokrejš, P., Mrázek, P., Gál, R., & Pavlačková, J. (2019). Biotechnological preparation of gelatines from chicken feet. Polymers, 11, 1060.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Monje, A., & Nart, J. (2000). (2022) Management and sequelae of dental implant removal. Periodontology, 88, 182–200.

    Article  Google Scholar 

  126. Moon, S. H., Lee, Y. J., Rhie, J. W., Suh, D. S., Oh, D. Y., Lee, J. H., Kim, Y. J., Kim, S. M., & Jun, Y. J. (2015). Comparative study of the effectiveness and safety of porcine and bovine atelocollagen in Asian nasolabial fold correction. Journal of Plastic Surgery and Hand Surgery, 49, 147–152.

    Article  PubMed  Google Scholar 

  127. Moses, O., Vitrial, D., Aboodi, G., Sculean, A., Tal, H., Kozlovsky, A., Artzi, Z., Weinreb, M., & Nemcovsky, C. E. (2008). Biodegradation of three different collagen membranes in the rat calvarium: A comparative study. Journal of Periodontology, 79, 905–911.

    Article  PubMed  Google Scholar 

  128. Naenni, N., Schneider, D., Jung, R. E., Husler, J., Hammerle, C. H. F., & Thoma, D. S. (2017). Randomized clinical study assessing two membranes for guided bone regeneration of peri-implant bone defects: Clinical and histological outcomes at 6 months. Clinical Oral Implants Research, 28, 1309–1317.

    Article  PubMed  Google Scholar 

  129. Namgung, S., Baik, K. Y., Park, J., & Hong, S. (2011). Controlling the growth and differentiation of human mesenchymal stem cells by the arrangement of individual carbon nanotubes. ACS Nano, 5, 7383–7390.

    Article  PubMed  CAS  Google Scholar 

  130. Nkenke, E., & Neukam, F. W. (2014). Autogenous bone harvesting and grafting in advanced jaw resorption: Morbidity, resorption and implant survival. European Journal of Oral Implantology, 7(Suppl 2), S203-217.

    PubMed  Google Scholar 

  131. Noorzai, S., Verbeek, C. J. R., Lay, M. C., & Swan, J. (2020). Collagen extraction from various waste bovine hide sources. Waste Biomass Valorization., 11, 5687–5698.

    Article  CAS  Google Scholar 

  132. Oosterlaken, B. M., Vena, M. P., & de With, G. (2021). In Vitro Mineralization of Collagen. Advanced Materials, 33, e2004418.

    Article  PubMed  Google Scholar 

  133. Paeng, K. W., Cha, J. K., Thoma, D. S., Jung, R. E., Jung, U. W., & Benic, G. I. (2022). Effect of collagen membrane and of bone substitute on lateral bone augmentation with titanium mesh: An experimental in vivo study. Clinical Oral Implants Research, 33, 413–423.

    Article  PubMed  CAS  Google Scholar 

  134. Parenteau-Bareil, R., Gauvin, R., & Berthod, F. (2010). Collagen-based biomaterials for tissue engineering applications. Materials, 3, 1863–1887.

    Article  PubMed Central  CAS  Google Scholar 

  135. Parisi, J. R., Fernandes, K., Avanzi, I., Dorileo, B., Santana, A., Andrade, A., Gabbai-Armelin, P., Fortulan, C., Trichês, E., & Granito, R. (2019). Incorporation of collagen from marine sponges (spongin) into hydroxyapatite samples: Characterization and in vitro biological evaluation. Marine Biotechnology, 21, 30–37.

    Article  PubMed  CAS  Google Scholar 

  136. Park, S. M., Kang, D. R., Lee, J. H., Jeong, Y. H., Shin, D. A., Yi, S., Ha, Y., & Kim, K. N. (2021). Efficacy and safety of a thrombin-containing collagen-based hemostatic agent in spinal surgery: A randomized clinical trial. World Neurosurgery, 154, e215–e221.

    Article  PubMed  Google Scholar 

  137. Park, W.-B., Crasto, G. J., Han, J.-Y., Kang, P., & Lim, H.-C. (2023). Bone regenerative potential of cross-linked collagen membrane in peri-implant osseous defect: Case series with histologic/micro-computed tomographic findings. Medicina, 59, 176.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Pavelka, K., Jarosova, H., Milani, L., Prochazka, Z., Kostiuk, P., Kotlarova, L., Meroni, A. M., & Sliva, J. (2019). Efficacy and tolerability of injectable collagen-containing products in comparison to trimecaine in patients with acute lumbar spine pain (Study FUTURE-MD-Back Pain). Physiological Research, 68, S65–S74.

    Article  PubMed  CAS  Google Scholar 

  139. Prakash, K. H., Kumar, R., Ooi, C. P., Cheang, P., & Khor, K. A. (2006). Apparent solubility of hydroxyapatite in aqueous medium and its influence on the morphology of nanocrystallites with precipitation temperature. Langmuir, 22, 11002–11008.

    Article  PubMed  CAS  Google Scholar 

  140. Prokopiev, O., & Sevostianov, I. (2006). Dependence of the mechanical properties of sintered hydroxyapatite on the sintering temperature. Materials Science and Engineering: A, 431, 218–227.

    Article  Google Scholar 

  141. Qin, D., Wang, N., You, X.-G., Zhang, A.-D., Chen, X.-G., & Liu, Y. (2022). Collagen-based biocomposites inspired by bone hierarchical structures for advanced bone regeneration: Ongoing research and perspectives. Biomaterials Science, 10, 318–353.

    Article  PubMed  CAS  Google Scholar 

  142. Radenkovic, M., Alkildani, S., Stoewe, I., Bielenstein, J., Sundag, B., Bellmann, O., Jung, O., Najman, S., Stojanovic, S., & Barbeck, M. (2021). Comparative in vivo analysis of the integration behavior and immune response of collagen-based dental barrier membranes for guided bone regeneration (GBR). Membranes (Basel), 11, 712.

    Article  PubMed  CAS  Google Scholar 

  143. Rahman, M. A. (2019). Collagen of extracellular matrix from marine invertebrates and its medical applications. Marine Drugs, 17, 118.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  144. Rakhmatia, Y. D., Ayukawa, Y., Furuhashi, A., & Koyano, K. (2013). Current barrier membranes: Titanium mesh and other membranes for guided bone regeneration in dental applications. Journal of Prosthodontic Research, 57, 3–14.

    Article  PubMed  Google Scholar 

  145. Rana, D., Desai, N., Salave, S., Karunakaran, B., Giri, J., Benival, D., Gorantla, S., & Kommineni, N. (2023). Collagen-based hydrogels for the eye: A comprehensive review. Gels, 9, 643.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Reilly, D. M., & Lozano, J. (2021). Skin collagen through the lifestages: Importance for skin health and beauty. Plastic and Aesthetic Research, 8, 2.

    Article  Google Scholar 

  147. Ren, X., Bischoff, D., Weisgerber, D. W., Lewis, M. S., Tu, V., Yamaguchi, D. T., Miller, T. A., Harley, B. A., & Lee, J. C. (2015). Osteogenesis on nanoparticulate mineralized collagen scaffolds via autogenous activation of the canonical BMP receptor signaling pathway. Biomaterials, 50, 107–114.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Ren, Y., Fan, L., Alkildani, S., Liu, L., Emmert, S., Najman, S., Rimashevskiy, D., Schnettler, R., Jung, O., Xiong, X., & Barbeck, M. (2022). Barrier membranes for guided bone regeneration (GBR): A focus on recent advances in collagen membranes. International Journal of Molecular Sciences, 23, 14987.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Requena, L., Requena, C., Christensen, L., Zimmermann, U. S., Kutzner, H., & Cerroni, L. (2011). Adverse reactions to injectable soft tissue fillers. Journal of the American Academy of Dermatology, 64, 1–34. quiz 35-36.

    Article  PubMed  CAS  Google Scholar 

  150. Revell, C. K., Jensen, O. E., Shearer, T., Lu, Y., Holmes, D. F., & Kadler, K. E. (2021). Collagen fibril assembly: New approaches to unanswered questions. Matrix Biology Plus, 12, 100079.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  151. Rezvani Ghomi, E., Nourbakhsh, N., Akbari Kenari, M., Zare, M., & Ramakrishna, S. (2021). Collagen-based biomaterials for biomedical applications. Journal of Biomedical Materials Research. Part B, Applied Biomaterials, 109, 1986–1999.

    Article  PubMed  CAS  Google Scholar 

  152. Ricard-Blum, S. (2011). The collagen family. Cold Spring Harbor Perspectives in Biology, 3, a004978.

    Article  PubMed  PubMed Central  Google Scholar 

  153. Richt, J. A., Kasinathan, P., Hamir, A. N., Castilla, J., Sathiyaseelan, T., Vargas, F., Sathiyaseelan, J., Wu, H., Matsushita, H., Koster, J., Kato, S., Ishida, I., Soto, C., Robl, J. M., & Kuroiwa, Y. (2007). Production of cattle lacking prion protein. Nature Biotechnology, 25, 132–138.

    Article  PubMed  CAS  Google Scholar 

  154. Rinaldi, F., Pinto, D., Trink, A., Giuliani, G., & Sparavigna, A. (2021). In vitro and in vivo evaluation on the safety and efficacy of a brand-new Intracutaneous filler with α1-R-collagen. Clinical, Cosmetic and Investigational Dermatology, 14, 501–512.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  155. Rossaint, R., Afshari, A., Bouillon, B., Cerny, V., Cimpoesu, D., Curry, N., Duranteau, J., Filipescu, D., Grottke, O., Grønlykke, L., Harrois, A., Hunt, B. J., Kaserer, A., Komadina, R., Madsen, M. H., Maegele, M., Mora, L., Riddez, L., Romero, C. S., Samama, C.-M., Vincent, J.-L., Wiberg, S. and Spahn, D. R. (2023). The European guideline on management of major bleeding and coagulopathy following trauma: sixth edition. Critical Care, 27, 80.

  156. Rothamel, D., Schwarz, F., Sager, M., Herten, M., Sculean, A., & Becker, J. (2005). Biodegradation of differently cross-linked collagen membranes: An experimental study in the rat. Clinical Oral Implants Research, 16, 369–378.

    Article  PubMed  Google Scholar 

  157. Salamanca, E., Tsai, C. Y., Pan, Y. H., Lin, Y. T., Huang, H. M., Teng, N. C., Lin, C. T., Feng, S. W., & Chang, W. J. (2016). In vitro and in vivo study of a novel porcine collagen membrane for guided bone regeneration. Materials (Basel), 9, 949.

    Article  PubMed  Google Scholar 

  158. Salvatore, L., Natali, M. L., Brunetti, C., Sannino, A., & Gallo, N. (2023). An update on the clinical efficacy and safety of collagen injectables for aesthetic and regenerative medicine applications. Polymers, 15, 1020.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  159. Salvatore, L., Natali, M. L., Brunetti, C., Sannino, A., & Gallo, N. (2023). An update on the clinical efficacy and safety of collagen injectables for aesthetic and regenerative medicine applications. Polymers (Basel), 15, 1020.

    Article  PubMed  CAS  Google Scholar 

  160. Salvatore, L., Natali, M. L., Brunetti, C., Sannino, A., & Gallo, N. (2023). Collagen injectables for aesthetic and regenerative medicine applications. Encyclopedia. Available online: https://encyclopedia.pub/entry/43746. Accessed 17 Dec 2023.

  161. Santana, J. C. C., Gardim, R. B., Almeida, P. F., Borini, G. B., Quispe, A. P. B., Llanos, S. A. V., Heredia, J. A., Zamuner, S., Gamarra, F. M. C., Farias, T. M. B., Ho, L. L., & Berssaneti, F. T. (2020). Valorization of chicken feet by-product of the poultry industry: High qualities of gelatin and biofilm from extraction of collagen. Polymers (Basel), 12, 529.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  162. Sbricoli, L., Guazzo, R., Annunziata, M., Gobbato, L., Bressan, E., & Nastri, L. (2020). Selection of collagen membranes for bone regeneration: A literature review. Materials (Basel), 13, 786.

    Article  PubMed  CAS  Google Scholar 

  163. Schmidt-Bleek, K., Willie, B. M., Schwabe, P., Seemann, P., & Duda, G. N. (2016). BMPs in bone regeneration: Less is more effective, a paradigm-shift. Cytokine & Growth Factor Reviews, 27, 141–148.

    Article  CAS  Google Scholar 

  164. Schmidt, A. H. (2021). Autologous bone graft: Is it still the gold standard? Injury, 52, S18–S22.

    Article  PubMed  Google Scholar 

  165. Schmidt, M., Dornelles, R., Mello, R., Kubota, E., Mazutti, M., Kempka, A., & Demiate, I. (2016). Collagen extraction process. International Food Research Journal, 23, 913.

    CAS  Google Scholar 

  166. Sheikh, Z., Hamdan, N., Ikeda, Y., Grynpas, M., Ganss, B., & Glogauer, M. (2017). Natural graft tissues and synthetic biomaterials for periodontal and alveolar bone reconstructive applications: A review. Biomaterials Research, 21, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  167. Silva, T. H., Moreira-Silva, J., Marques, A. L., Domingues, A., Bayon, Y., & Reis, R. L. (2014). Marine origin collagens and its potential applications. Marine Drugs, 12, 5881–5901.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Silvipriya, K., Kumar, K. K., Bhat, A., Kumar, B. D., & John, A. (2015). Collagen: Animal sources and biomedical application. Journal of Applied Pharmaceutical Science, 5, 123–127.

    Article  Google Scholar 

  169. Simion, M., Baldoni, M., Rassi, P., & Zaffe, D. (1994). A comparative study of the effectiveness of e-PTFE membranes with and without early exposure during the healing period. International Journal of Periodontics & Restorative Dentistry, 14, 166–180.

  170. Sionkowska, A., Adamiak, K., Musiał, K., & Gadomska, M. (2020). Collagen based materials in cosmetic applications: A review. Materials, 13, 4217.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  171. Slezak, P., Keibl, C., Labahn, D., Schmidbauer, A., Genyk, Y., & Gulle, H. (2021). A comparative efficacy evaluation of recombinant topical thrombin (RECOTHROM®) with a gelatin sponge carrier versus topical oxidized regenerated cellulose (TABOTAMP®/SURGICEL®) in a porcine liver bleeding model. Journal of Investigative Surgery, 34, 862–868.

    Article  PubMed  Google Scholar 

  172. Smith, K. C. (2009). Repair of acne scars with Dermicol-P35. Aesthetic Surgery Journal, 29, S16-18.

    Article  PubMed  Google Scholar 

  173. Sohn, H.-S., & Oh, J.-K. (2019). Review of bone graft and bone substitutes with an emphasis on fracture surgeries. Biomaterials Research, 23, 1–7.

    Article  CAS  Google Scholar 

  174. Song, W.-K., Liu, D., Sun, L.-L., Li, B.-F., & Hou, H. (2019). Physicochemical and biocompatibility properties of type I collagen from the skin of Nile tilapia (Oreochromis niloticus) for biomedical applications. Marine Drugs, 17, 137.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  175. Sordi, M. B., Cruz, A., Fredel, M. C., Magini, R., & Sharpe, P. T. (2021). Three-dimensional bioactive hydrogel-based scaffolds for bone regeneration in implant dentistry. Materials Science and Engineering C, 124, 112055.

    Article  PubMed  CAS  Google Scholar 

  176. Sorushanova, A., Delgado, L. M., Wu, Z., Shologu, N., Kshirsagar, A., Raghunath, R., Mullen, A. M., Bayon, Y., Pandit, A., Raghunath, M., & Zeugolis, D. I. (2019). The collagen suprafamily: From biosynthesis to advanced biomaterial development. Advanced Materials, 31, e1801651.

    Article  PubMed  Google Scholar 

  177. Stock, S. R. (2015). The mineral-collagen interface in bone. Calcified Tissue International, 97, 262–280.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  178. Tal, H., Kozlovsky, A., Artzi, Z., Nemcovsky, C. E., & Moses, O. (2008). Cross-linked and non-cross-linked collagen barrier membranes disintegrate following surgical exposure to the oral environment: A histological study in the cat. Clinical Oral Implants Research, 19, 760–766.

    Article  PubMed  Google Scholar 

  179. Tanzer, M. L. (1973). Cross-linking of collagen: Endogenous aldehydes in collagen react in several ways to form a variety of unique covalent cross-links. Science, 180, 561–566.

    Article  PubMed  CAS  Google Scholar 

  180. Tasiopoulos, C. P., Petronis, S., Sahlin, H., & Hedhammar, M. (2020). Surface functionalization of PTFE membranes intended for guided bone regeneration using recombinant spider silk. ACS Applied Bio Materials, 3, 577–583.

    Article  PubMed  CAS  Google Scholar 

  181. Taub, A. F. (2019). The treatment of acne scars, a 30-year journey. American Journal of Clinical Dermatology, 20, 683–690.

    Article  PubMed  Google Scholar 

  182. Thoma, D. S., Bienz, S. P., Figuero, E., Jung, R. E., & Sanz-Martin, I. (2019). Efficacy of lateral bone augmentation performed simultaneously with dental implant placement: A systematic review and meta-analysis. Journal of Clinical Periodontology, 46(Suppl 21), 257–276.

    Article  PubMed  CAS  Google Scholar 

  183. Titsinides, S., Agrogiannis, G., & Karatzas, T. (2019). Bone grafting materials in dentoalveolar reconstruction: A comprehensive review. Japanese Dental Science Review, 55, 26–32.

    Article  PubMed  CAS  Google Scholar 

  184. Toledano-Osorio, M., Vallecillo, C., Vallecillo-Rivas, M., Manzano-Moreno, F. J., & Osorio, R. (2022). Antibiotic-loaded polymeric barrier membranes for guided bone/tissue regeneration: a mini-review. Polymers (Basel), 14(4), 840.

    Article  PubMed  CAS  Google Scholar 

  185. Tomita, M., Munetsuna, H., Sato, T., Adachi, T., Hino, R., Hayashi, M., Shimizu, K., Nakamura, N., Tamura, T., & Yoshizato, K. (2003). Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nature Biotechnology, 21, 52–56.

    Article  PubMed  CAS  Google Scholar 

  186. Turri, A., Elgali, I., Vazirisani, F., Johansson, A., Emanuelsson, L., Dahlin, C., Thomsen, P., & Omar, O. (2016). Guided bone regeneration is promoted by the molecular events in the membrane compartment. Biomaterials, 84, 167–183.

    Article  PubMed  CAS  Google Scholar 

  187. Urban, I. A., Lozada, J. L., Wessing, B., Suarez-Lopez del Amo, F., & Wang, H. L. (2016). Vertical bone grafting and periosteal vertical mattress suture for the fixation of resorbable membranes and stabilization of particulate grafts in horizontal guided bone regeneration to achieve more predictable results: A technical report. The International Journal of Periodontics & Restorative Dentistry, 36, 153–159.

    Article  Google Scholar 

  188. Urban, I. A., Nagursky, H., Lozada, J. L., & Nagy, K. (2013). Horizontal ridge augmentation with a collagen membrane and a combination of particulated autogenous bone and anorganic bovine bone-derived mineral: A prospective case series in 25 patients. The International Journal of Periodontics & Restorative Dentistry, 33, 299–307.

    Article  Google Scholar 

  189. Vafa, E., Tayebi, L., Abbasi, M., Azizli, M. J., Bazargan-Lari, R., Talaiekhozani, A., Zareshahrabadi, Z., Vaez, A., Amani, A. M., & Kamyab, H. (2022). A better roadmap for designing novel bioactive glasses: effective approaches for the development of innovative revolutionary bioglasses for future biomedical applications. Environmental Science and Pollution Research International, 30, 116960–116983.

  190. Vallecillo, C., Toledano-Osorio, M., Vallecillo-Rivas, M., Toledano, M., Rodriguez-Archilla, A., & Osorio, R. (2021). Collagen matrix vs. autogenous connective tissue graft for soft tissue augmentation: a systematic review and meta-analysis. Polymers (Basel), 13(11), 1810.

  191. Verissimo, D. M., Leitao, R. F., Ribeiro, R. A., Figueiro, S. D., Sombra, A. S., Goes, J. C., & Brito, G. A. (2010). Polyanionic collagen membranes for guided tissue regeneration: Effect of progressive glutaraldehyde cross-linking on biocompatibility and degradation. Acta Biomaterialia, 6, 4011–4018.

    Article  PubMed  CAS  Google Scholar 

  192. Viguet-Carrin, S., Garnero, P., & Delmas, P. D. (2006). The role of collagen in bone strength. Osteoporosis International, 17, 319–336.

    Article  PubMed  CAS  Google Scholar 

  193. Volpi, P., Zini, R., Erschbaumer, F., Beggio, M., Busilacchi, A., & Carimati, G. (2021). Effectiveness of a novel hydrolyzed collagen formulation in treating patients with symptomatic knee osteoarthritis: A multicentric retrospective clinical study. International Orthopaedics, 45, 375–380.

    Article  PubMed  Google Scholar 

  194. von Arx, T., & Buser, D. (2006). Horizontal ridge augmentation using autogenous block grafts and the guided bone regeneration technique with collagen membranes: A clinical study with 42 patients. Clinical Oral Implants Research, 17, 359–366.

    Article  Google Scholar 

  195. Wang, H. (2021). A review of the effects of collagen treatment in clinical studies. Polymers (Basel), 13, 3868.

    Article  PubMed  CAS  Google Scholar 

  196. Wang, L., Li, W., Qu, Y., Wang, K., Lv, K., He, X., & Qin, S. (2022). Preparation of super absorbent and highly active fish collagen sponge and its hemostatic effect in vivo and in vitro. Frontiers in Bioengineering and Biotechnology, 10, 862532.

  197. Wickramasinghe, M. L., Dias, G. J., & Premadasa, K. M. G. P. (2022). A novel classification of bone graft materials. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 110, 1724–1749.

    Article  PubMed  CAS  Google Scholar 

  198. Wisanuyotin, T., Paholpak, P., Sirichativapee, W., & Kosuwon, W. (2022). Allograft versus autograft for reconstruction after resection of primary bone tumors: A comparative study of long-term clinical outcomes and risk factors for failure of reconstruction. Science and Reports, 12, 14346.

    Article  CAS  Google Scholar 

  199. Wolkow, N., Jakobiec, F. A., Dryja, T. P., & Lefebvre, D. R. (2018). Mild Complications or unusual persistence of porcine collagen and hyaluronic acid gel following periocular filler injections. Ophthalmic Plastic and Reconstructive Surgery, 34, e143–e146.

    Article  PubMed  Google Scholar 

  200. Wong, R., Geyer, S., Weninger, W., Guimberteau, J. C., & Wong, J. K. (2016). The dynamic anatomy and patterning of skin. Experimental Dermatology, 25, 92–98.

    Article  PubMed  Google Scholar 

  201. Wu, S., Applewhite, A. J., Niezgoda, J., Snyder, R., Shah, J., Cullen, B., Schultz, G., Harrison, J., Hill, R., Howell, M., Speyrer, M., Utra, H., de Leon, J., Lee, W., & Treadwell, T. (2017). Oxidized regenerated cellulose/collagen dressings: Review of evidence and recommendations. Advances in Skin & Wound Care, 30, S1-s18.

    Article  Google Scholar 

  202. Wu, Y., Chen, S., Luo, P., Deng, S., Shan, Z., Fang, J., Liu, X., Xie, J., Liu, R., Wu, S., Wu, X., Chen, Z., Yeung, K. W. K., Liu, Q., & Chen, Z. (2022). Optimizing the bio-degradability and biocompatibility of a biogenic collagen membrane through cross-linking and zinc-doped hydroxyapatite. Acta Biomaterialia, 143, 159–172.

    Article  PubMed  CAS  Google Scholar 

  203. Wyganowska-Swiatkowska, M., Duda-Sobczak, A., Corbo, A., & Matthews-Brzozowska, T. (2020). Atelocollagen application in human periodontal tissue treatment-a pilot study. Life (Basel), 10(7), 114.

    PubMed  Google Scholar 

  204. Yeung, D. A., & Kelly, N. H. (2021). The role of collagen-based biomaterials in chronic wound healing and sports medicine applications. Bioengineering (Basel), 8, 1–8.

    Google Scholar 

  205. Zahedi, S., Legrand, R., Brunel, G., Albert, A., Dewe, W., Coumans, B., & Bernard, J. P. (1998). Evaluation of a diphenylphosphorylazide-crosslinked collagen membrane for guided bone regeneration in mandibular defects in rats. Journal of Periodontology, 69, 1238–1246.

    Article  PubMed  CAS  Google Scholar 

  206. Zhang, D., Wu, X., Chen, J., & Lin, K. (2018). The development of collagen based composite scaffolds for bone regeneration. Bioactive Materials, 3, 129–138.

    Article  PubMed  Google Scholar 

  207. Zhang, Y., Wang, Y., Li, Y., Yang, Y., Jin, M., Lin, X., Zhuang, Z., Guo, K., Zhang, T., & Tan, W. (2023). Application of collagen-based hydrogel in skin wound healing. Gels, 9, 185.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  208. Zhao, R., Yang, R., Cooper, P. R., Khurshid, Z., Shavandi, A., & Ratnayake, J. (2021). Bone grafts and substitutes in dentistry: A review of current trends and developments. Molecules, 26, 3007.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  209. Zhou, H., Liang, C., Wei, Z., Bai, Y., Bhaduri, S. B., Webster, T. J., Bian, L., & Yang, L. (2019). Injectable biomaterials for translational medicine. Materials Today, 28, 81–97.

    Article  CAS  Google Scholar 

  210. Zhou, T., Chen, S., Ding, X., Hu, Z., Cen, L., & Zhang, X. (2021). Fabrication and characterization of collagen/PVA dual-layer membranes for periodontal bone regeneration. Frontiers in Bioengineering and Biotechnology, 9, 630977.

  211. Zhu, J., Li, Z., Zou, Y., Lu, G., Ronca, A., D’Amora, U., Liang, J., Fan, Y., Zhang, X., & Sun, Y. (2022). Advanced application of collagen-based biomaterials in tissue repair and restoration. Journal of Leather Science and Engineering, 4, 30.

    Article  CAS  Google Scholar 

  212. Zhu, L., Xie, Y., Wen, B., Ye, M., Liu, Y., Imam, K. M. S. U., Cai, H., Zhang, C., Wang, F., & Xin, F. (2020). Porcine bone collagen peptides promote osteoblast proliferation and differentiation by activating the PI3K/Akt signaling pathway. Journal of Functional Foods, 64, 103697.

    Article  Google Scholar 

  213. Zitzmann, N. U., Naef, R., & Scharer, P. (1997). Resorbable versus nonresorbable membranes in combination with Bio-Oss for guided bone regeneration. International Journal of Oral and Maxillofacial Implants, 12, 844–852.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Pharmaceutical Science Research Center, Shiraz University of Medical Science, Shiraz, Iran

    Mehdi Abedi & Younes Ghasemi

  2. Research and Development Department, Danesh Salamat Kowsar Co., P.O. Box 7158186496, Shiraz, Iran

    Mehdi Abedi, Mina Shafiee & Hamidreza Mohammadi

  3. Department of Tissue Engineering and Applied Cell Science, School of Advanced Medical Sciences and Technology, Shiraz University of Medical Sciences, Shiraz, Iran

    Farideh Afshari

  4. Department of Pharmaceutical Biotechnology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

    Younes Ghasemi

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Contributions

M.A., M.S., and F. A. designed this study and Y.G. and H.R.M. conducted research. M.A., M.S., and F.A. analyzed the data and wrote the manuscript. H.R.M. provided help and suggestions for this study. All authors contributed to the editorial changes in the manuscript. All authors have read and agreed to the published version of the manuscript.

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Abedi, M., Shafiee, M., Afshari, F. et al. Collagen-Based Medical Devices for Regenerative Medicine and Tissue Engineering. Appl Biochem Biotechnol 196, 5563–5603 (2024). https://doi.org/10.1007/s12010-023-04793-3

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