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References

  1. Alijotas-Reig J, Fernández-Figueras MT, Puig L. 2013. Inflammatory, immune-mediated adverse reactions related to soft tissue dermal fillers. Semin. Arthritis Rheum. 43: 241-258.
    Pubmed CrossRef
  2. Allemann IB, Baumann L. 2008. Hyaluronic acid gel (Juvéderm™) preparations in the treatment of facial wrinkles and folds. Clin. Interv. Aging 3: 629-656.
    PMC
  3. Baumann LS, Kerdel F. 1999. The treatment of bovine collagen allergy with cyclosporin. Dermatol. Surg. 25: 247-249.
    Pubmed CrossRef
  4. Beasley KL, Weiss MA, Weiss RA. 2009. Hyaluronic acid fillers: a comprehensive review. Facial Plast. Surg. 25: 86-94.
    Pubmed CrossRef
  5. Burgess CM. 2006. Principles of soft tissue augmentation for the aging face. Clin. Interv. Aging 1: 349-355.
    Pubmed PMC CrossRef
  6. Carruthers J, Carruthers A. 2002. Mad cows, prions, and wrinkles. Arch. Dermatol. 138: 667-670.
    Pubmed CrossRef
  7. Cena RB, Park JG, Kim HJ, Son KY, Kim DS, Kang MI, et al. 2014. Effects of crosslinked dextran in hydroxylpropyl methylcellulose on soft tissue augmentation in rats. J. Biomed. Mater. Res. B Appl. Biomater. 102: 131-140.
    Pubmed CrossRef
  8. Davidenko N, Campbell JJ, Thian ES, Watson CJ, Cameron RE. 2010. Collagen-hyaluronic acid scaffolds for adipose tissue engineering. Acta Biomater. 6: 3957-3968.
    Pubmed CrossRef
  9. Eppley BL, Summerlin DJ, Prevel CD, Sadove AM. 1994. Effects of a positively charged biomaterial for dermal and subcutaneous augmentation. Aesthet. Plast. Surg. 18: 413-416.
    Pubmed CrossRef
  10. Falcone SJ, Berg RA. 2008. Crosslinked hyaluronic acid dermal fillers: a comparison of rheological properties. J. Biomed. Mater. Res. A 87: 264-271.
    Pubmed CrossRef
  11. Grunebaum LD, Allemann IB, Dayan S, Mandy S, Baumann L. 2009. The risk of alar necrosis associated with dermal filler injection. Dermatol. Surg. 35: 1635-1640.
    Pubmed CrossRef
  12. Huh SY, Cho S, Kim KH, An JS, Won CH, Chang SE, et al. 2010. A case of complication after matridex? injection. Ann. Dermatol. 22: 81-84.
    Pubmed PMC CrossRef
  13. Kablik J, Monheit GD, Yu L, Chang G, Gershkovich J. 2009. Comparative physical properties of hyaluronic acid dermal fillers. Dermatol. Surg. 35: 302-312.
    Pubmed CrossRef
  14. Kim KO, Lee Y, Hwang JW, Kim H, Lee HS, Choi YS. 2014. Wound healing properties of a 3-D scaffold comprising soluble silkworm gland hydrolysate and human collagen. Colloids Surf. B 116: 318-326.
    Pubmed CrossRef
  15. Kim SJ, Park SY, Kim CW. 2006. A novel approach to the production of hyaluronic acid by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 16: 1849-1855.
  16. Kim SM, Moon SH, Lee Y, Kim GJ, Chung HM, Choi YS. 2013. Alternative xeno-free biomaterials derived from human umbilical cord for the self-renewal ex-vivo expansion of mesenchymal stem cells. Stem Cells Dev. 22: 3025-3038.
    Pubmed CrossRef
  17. Kong MK, Lee PC. 2012. Evaluation of a pretreatment method for two-dimensional gel electrophoresis of synovial fluid using cartilage oligomeric matrix protein as a marker. J. Microbiol. Biotechnol. 22: 654-658.
    Pubmed CrossRef
  18. La Gatta A, Schiraldi C, Papa A, De Rosa M. 2011. Comparative analysis of commercial dermal fillers based on crosslinked hyaluronan: physical characterization and in vitro enzymatic degradation. Polym. Degrad. Stabil. 96: 630-636.
    CrossRef
  19. Laurent TC, Fraser J. 1992. Hyaluronan. FASEB. J. 6: 2397-2404.
    Pubmed
  20. Na K, Kim DW, Park KH. 2001. Certification of fibroblast cell adhesion and spreading mediated by Arg-Gly-Asp (RGD) sequence on thermo-reversible hydrogel. J. Microbiol. Biotechnol. 11: 922-927.
  21. Natarajan V, Krithica N, Madhan B, Sehgal PK. 2013. Preparation and properties of tannic acid cross-linked collagen scaffold and its application in wound healing. J. Biomed. Mater. Res. B Appl. Biomater. 101: 560-567.
    Pubmed CrossRef
  22. Ryou C. 2007. Prions and prion diseases: fundamentals and mechanistic details. J. Microbiol. Biotechnol. 17: 1059-1070.
    Pubmed
  23. Shin JS, Chang HI, Sung HC, Kim CW. 1999. The effects of fetal bovine serum, epidermal growth factor, and retinoic acid on adult rat islets embedded in collagen gels. J. Microbiol. Biotechnol. 9: 150-156.
  24. Simoni RD, Hill RL, Vaughan M, Hascall V, Vaughan M. 2002. The discovery of hyaluronan by Karl Meyer. J. Biol. Chem. 277: e27.
  25. Smith SR, Jones D, Thomas JA, Murphy DK, Beddingfield III FC. 2010. Duration of wrinkle correction following repeat treatment with Juvederm hyaluronic acid fillers. Arch. Dermatol. Res. 302: 757-762.
    Pubmed PMC CrossRef
  26. Tang S, Spector M. 2007. Incorporation of hyaluronic acid into collagen scaffolds for the control of chondrocyte-mediated contraction and chondrogenesis. Biomed. Mater. 2: S135.
    Pubmed CrossRef
  27. Tang S, Vickers SM, Hsu HP, Spector M. 2007. Fabrication and characterization of porous hyaluronic acid-collagen composite scaffolds. J. Biomed. Mater. Res. A 82: 323-335.
    Pubmed CrossRef
  28. Verpaele A, Strand A. 2006. Restylane SubQ, a non-animal stabilized hyaluronic acid gel for soft tissue augmentation of the mid and lower face. Aesthet. Surg. J. 26: S10-S17.
    Pubmed CrossRef
  29. Yoon ES, Han SK, Kim WK. 2003. Advantages of the presence of living dermal fibroblasts within restylane for soft tissue augmentation. Ann. Plast. Surg. 51: 587-592.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(3): 399-406

Published online March 28, 2015 https://doi.org/10.4014/jmb.1411.11029

Copyright © The Korean Society for Microbiology and Biotechnology.

A Composite Dermal Filler Comprising Cross-Linked Hyaluronic Acid and Human Collagen for Tissue Reconstruction

Z-Hun Kim 1, Yongjun Lee 1, Sun-Mi Kim 1, Hojin Kim 1, Chang-Koo Yun 1 and Yong-Soo Choi 1*

Department of Applied Bioscience, CHA University, Seongnam 463-712, Republic of Korea

Received: November 13, 2014; Accepted: December 4, 2014

Abstract

In this study, we developed a composite filler comprising cross-linked hyaluronic acid (HA)
and human collagen (COL) derived from the human umbilical cord with the aim of improving
its biocompatibility and longevity compared with commercially available fillers. After HA/
COL composite fillers were made in two different ratios (10:1 and 5:1), the physical properties
of the fillers were evaluated. The interior morphologies and in vivo weight change of these
hydrogels were also characterized at 1-16 weeks after injection into mice. To evaluate their
biocompatibility and durability in vivo, we injected the composite fillers into nude mice
subcutaneously. The variations of injected gel weight were measured and compared with the
commercial dermal fillers (Restylane and TheraFill). The composites showed improved or
similar physical properties (complex viscosity of 19-22 × 105 cP, and injection force of 10-
12 N) over the commercial dermal fillers. Sixteen weeks following the injection, the ratio of
remaining composite filler weight to initial weight (75.5 ± 16.9%; 10:1) was shown to be greater
than that of the commercial fillers (43.2 ± 8.1%, Restylane; 12.3 ± 5.3%, TheraFill). In addition,
immunohistochemical analysis with angiogenesis-related markers such as isolectin and vWF
revealed newly formed blood vessels and cellular influx into the composite filler, which were
not observed in the other fillers. These results clearly suggest that the HA/COL composite
filler is a superior candidate for soft tissue reconstruction. The filler we developed may be a
suitable candidate as an injectable dermal filler for tissue augmentation in humans.

Keywords: composite dermal filler, human collagen, hyaluronic acid, umbilical cord

References

  1. Alijotas-Reig J, Fernández-Figueras MT, Puig L. 2013. Inflammatory, immune-mediated adverse reactions related to soft tissue dermal fillers. Semin. Arthritis Rheum. 43: 241-258.
    Pubmed CrossRef
  2. Allemann IB, Baumann L. 2008. Hyaluronic acid gel (Juvéderm™) preparations in the treatment of facial wrinkles and folds. Clin. Interv. Aging 3: 629-656.
    KoreaMed
  3. Baumann LS, Kerdel F. 1999. The treatment of bovine collagen allergy with cyclosporin. Dermatol. Surg. 25: 247-249.
    Pubmed CrossRef
  4. Beasley KL, Weiss MA, Weiss RA. 2009. Hyaluronic acid fillers: a comprehensive review. Facial Plast. Surg. 25: 86-94.
    Pubmed CrossRef
  5. Burgess CM. 2006. Principles of soft tissue augmentation for the aging face. Clin. Interv. Aging 1: 349-355.
    Pubmed KoreaMed CrossRef
  6. Carruthers J, Carruthers A. 2002. Mad cows, prions, and wrinkles. Arch. Dermatol. 138: 667-670.
    Pubmed CrossRef
  7. Cena RB, Park JG, Kim HJ, Son KY, Kim DS, Kang MI, et al. 2014. Effects of crosslinked dextran in hydroxylpropyl methylcellulose on soft tissue augmentation in rats. J. Biomed. Mater. Res. B Appl. Biomater. 102: 131-140.
    Pubmed CrossRef
  8. Davidenko N, Campbell JJ, Thian ES, Watson CJ, Cameron RE. 2010. Collagen-hyaluronic acid scaffolds for adipose tissue engineering. Acta Biomater. 6: 3957-3968.
    Pubmed CrossRef
  9. Eppley BL, Summerlin DJ, Prevel CD, Sadove AM. 1994. Effects of a positively charged biomaterial for dermal and subcutaneous augmentation. Aesthet. Plast. Surg. 18: 413-416.
    Pubmed CrossRef
  10. Falcone SJ, Berg RA. 2008. Crosslinked hyaluronic acid dermal fillers: a comparison of rheological properties. J. Biomed. Mater. Res. A 87: 264-271.
    Pubmed CrossRef
  11. Grunebaum LD, Allemann IB, Dayan S, Mandy S, Baumann L. 2009. The risk of alar necrosis associated with dermal filler injection. Dermatol. Surg. 35: 1635-1640.
    Pubmed CrossRef
  12. Huh SY, Cho S, Kim KH, An JS, Won CH, Chang SE, et al. 2010. A case of complication after matridex? injection. Ann. Dermatol. 22: 81-84.
    Pubmed KoreaMed CrossRef
  13. Kablik J, Monheit GD, Yu L, Chang G, Gershkovich J. 2009. Comparative physical properties of hyaluronic acid dermal fillers. Dermatol. Surg. 35: 302-312.
    Pubmed CrossRef
  14. Kim KO, Lee Y, Hwang JW, Kim H, Lee HS, Choi YS. 2014. Wound healing properties of a 3-D scaffold comprising soluble silkworm gland hydrolysate and human collagen. Colloids Surf. B 116: 318-326.
    Pubmed CrossRef
  15. Kim SJ, Park SY, Kim CW. 2006. A novel approach to the production of hyaluronic acid by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 16: 1849-1855.
  16. Kim SM, Moon SH, Lee Y, Kim GJ, Chung HM, Choi YS. 2013. Alternative xeno-free biomaterials derived from human umbilical cord for the self-renewal ex-vivo expansion of mesenchymal stem cells. Stem Cells Dev. 22: 3025-3038.
    Pubmed CrossRef
  17. Kong MK, Lee PC. 2012. Evaluation of a pretreatment method for two-dimensional gel electrophoresis of synovial fluid using cartilage oligomeric matrix protein as a marker. J. Microbiol. Biotechnol. 22: 654-658.
    Pubmed CrossRef
  18. La Gatta A, Schiraldi C, Papa A, De Rosa M. 2011. Comparative analysis of commercial dermal fillers based on crosslinked hyaluronan: physical characterization and in vitro enzymatic degradation. Polym. Degrad. Stabil. 96: 630-636.
    CrossRef
  19. Laurent TC, Fraser J. 1992. Hyaluronan. FASEB. J. 6: 2397-2404.
    Pubmed
  20. Na K, Kim DW, Park KH. 2001. Certification of fibroblast cell adhesion and spreading mediated by Arg-Gly-Asp (RGD) sequence on thermo-reversible hydrogel. J. Microbiol. Biotechnol. 11: 922-927.
  21. Natarajan V, Krithica N, Madhan B, Sehgal PK. 2013. Preparation and properties of tannic acid cross-linked collagen scaffold and its application in wound healing. J. Biomed. Mater. Res. B Appl. Biomater. 101: 560-567.
    Pubmed CrossRef
  22. Ryou C. 2007. Prions and prion diseases: fundamentals and mechanistic details. J. Microbiol. Biotechnol. 17: 1059-1070.
    Pubmed
  23. Shin JS, Chang HI, Sung HC, Kim CW. 1999. The effects of fetal bovine serum, epidermal growth factor, and retinoic acid on adult rat islets embedded in collagen gels. J. Microbiol. Biotechnol. 9: 150-156.
  24. Simoni RD, Hill RL, Vaughan M, Hascall V, Vaughan M. 2002. The discovery of hyaluronan by Karl Meyer. J. Biol. Chem. 277: e27.
  25. Smith SR, Jones D, Thomas JA, Murphy DK, Beddingfield III FC. 2010. Duration of wrinkle correction following repeat treatment with Juvederm hyaluronic acid fillers. Arch. Dermatol. Res. 302: 757-762.
    Pubmed KoreaMed CrossRef
  26. Tang S, Spector M. 2007. Incorporation of hyaluronic acid into collagen scaffolds for the control of chondrocyte-mediated contraction and chondrogenesis. Biomed. Mater. 2: S135.
    Pubmed CrossRef
  27. Tang S, Vickers SM, Hsu HP, Spector M. 2007. Fabrication and characterization of porous hyaluronic acid-collagen composite scaffolds. J. Biomed. Mater. Res. A 82: 323-335.
    Pubmed CrossRef
  28. Verpaele A, Strand A. 2006. Restylane SubQ, a non-animal stabilized hyaluronic acid gel for soft tissue augmentation of the mid and lower face. Aesthet. Surg. J. 26: S10-S17.
    Pubmed CrossRef
  29. Yoon ES, Han SK, Kim WK. 2003. Advantages of the presence of living dermal fibroblasts within restylane for soft tissue augmentation. Ann. Plast. Surg. 51: 587-592.
    Pubmed CrossRef