Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of a laminin-alginate biomaterial, adipocytes, and adipocyte-derived stem cells interaction in animal autologous fat grafting model using 7-Tesla magnetic resonance imaging

  • Biomaterials Synthesis and Characterization
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Biomaterials are often added to autologous fat grafts both as supporting matrices for the grafted adipocytes and as cell carrier for adipose-derived stem cells (ADSCs). This in vivo study used an autologous fat graft model to test a lamininalginate biomaterial, adipocytes, and ADSCs in immune-competent rats. We transplanted different combinations of shredded autologous adipose tissue [designated “A” for adipose tissue]), laminin-alginate beads [designated “B” for bead], and ADSCs [designated “C” for cell]) into the backs of 15 Sprague-Dawley rats. Group A received only adipocytes, Group B received only laminin-alginate beads, Group AB received adipocytes mixed with laminin-alginate beads, Group BC received laminin-alginate beads encapsulating ADSCs, and Group ABC received adipocytes and laminin-alginate beads containing ADSCs. Seven-tesla magnetic resonance imaging was used to evaluate the rats at the 1st, 6th, and 12th weeks after transplantation. At the 12th week, the rats were sacrificed and the implanted materials were retrieved for gross examination and histological evaluation. The results based on MRI, gross evaluation, and histological data all showed that implants in Group ABC had better resorption of the biomaterial, improved survival of the grafted adipocytes, and adipogenic differentiation of ADSCs. Volume retention of grafts in Group ABC (89%) was also significantly greater than those in Group A (58%) (p < 0.01). Our findings support that the combination of shredded adipose tissue with ADSCs in laminin-alginate beads provided the best overall outcome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Coleman SR. Structural fat grafts: the ideal filler? Clin Plast Surg. 2001;28:111–9.

    Google Scholar 

  2. Bircoll M. Cosmetic breast augmentation utilizing autologous fat and liposuction techniques. Plast Reconstr Surg. 1987;79:267–71.

    Article  Google Scholar 

  3. Claro F Jr, Figueiredo JC, Zampar AG, Pinto-Neto AM. Applicability and safety of autologous fat for reconstruction of the breast. Br J Surg. 2012;99(6):768–80.

    Article  Google Scholar 

  4. Lu F, Li J, Gao J, et al. Improvement of the survival of human autologous fat transplantation by using VEGF-transfected adipose-derived stem cells. Plast Reconstr Surg. 2009;124:1437–46.

    Article  Google Scholar 

  5. Hong SJ, Lee JH, Hong SM, Park CH. Enhancing the viability of fat grafts using new transfer medium containing insulin and fibroblast growth factor in autologous fat transplantation. J Plast Reconstr Aesthet Surg. 2010;63:1202–08.

    Article  Google Scholar 

  6. Mackay DR, Manders EK, Saggers GC, Schenden MJ, Zaino R. The fate of dermal and dermal-fat grafts. Ann Plast Surg. 1993;31:42–6.

    Article  Google Scholar 

  7. Kim HY, Jung BK, Lew DH, Lee DW. Autologous fat graft in the reconstructed breast: fat absorption rate and safety based on sonographic identification. Arch Plast Surg. 2014;41(6):740–7.

    Article  Google Scholar 

  8. Mineda K, Kuno S, Kato H, Kinoshita K, Doi K, Hashimoto I, et al. Chronic inflammation and progressive calcification as a result of fat necrosis: the worst outcome in fat grafting. Plast Reconstr Surg. 2014;133(5):1064–72.

    Article  Google Scholar 

  9. Kirkham JC, Lee JH, Medina MA 3rd, McCormack MC, Randolph MA, Austen WG Jr. The impact of liposuction cannula size on adipocyte viability. Ann Plast Surg. 2012;69(4):479–81.

    Article  Google Scholar 

  10. Gause TM, Kling RE, Sivak WN, Marra KG, Rubin JP, Kokai LE. Particle size in fat graft retention: a review on the impact of harvesting technique in lipofilling surgical outcomes. Adipocyte. 2014;3(4):273–9.

    Article  Google Scholar 

  11. Pu LL. Towards more rationalized approach to autologous fat grafting. J Plast Reconstr Aesthet Surg. 2012;65(4):413–9.

    Article  Google Scholar 

  12. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy. 2013;15(6):641–8.

    Article  Google Scholar 

  13. Minteer DM, Marra KG, Rubin JP. Adipose stem cells: biology, safety, regulation, and regenerative potential. Clin Plast Surg. 2015;42(2):169–79.

    Article  Google Scholar 

  14. Pill K, Hofmann S, Redl H, Holnthoner W. Vascularization mediated by mesenchymal stem cells from bone marrow and adipose tissue: a comparison. Cell Regen (Lond). 2015;4:8

    Article  Google Scholar 

  15. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Aiba-Kojima E, Iizuka F, Inoue K, Suga H, Yoshimura K. Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng. 2006;12(12):3375–82.

    Article  Google Scholar 

  16. Toyserkani NM, Quaade ML, Sørensen JA. Cell-assisted lipotransfer: a systematic review of its efficacy. Aesthet Plast Surg. 2016;40(2):309–18.

  17. Feisst V, Meidinger S, Locke MB. From bench to bedside: use of human adipose-derived stem cells. Stem Cells Cloning. 2015;8:149–62.

    Google Scholar 

  18. Anderson SB, Lin CC, Kuntzler DV, Anseth KS. The performance of human mesenchymal stem cells encapsulated in cell-degradable polymer-peptide hydrogels. Biomaterials. 2011;32(14):3564–74.

    Article  Google Scholar 

  19. Brännmark C, Paul A, Ribeiro D, Magnusson B, Brolén G, Enejder A, Forslöw A. Increased adipogenesis of human adipose-derived stem cells on polycaprolactone fiber matrices. PLoS One. 2014;9(11):e113620.

    Article  Google Scholar 

  20. Catalán V, Gómez-Ambrosi J, Rodríguez A, Frühbeck G. Role of extracellular matrix remodelling in adipose tissue pathophysiology: relevance in the development of obesity. Histol Histopathol. 2012;27(12):1515–28.

    Google Scholar 

  21. Mori S, Kiuchi S, Ouchi A, Hase T, Murase T. Characteristic expression of extracellular matrix in subcutaneous adipose tissue development and adipogenesis; comparison with visceral adipose tissue. Int J Biol Sci. 2014;10(8):825–33.

    Article  Google Scholar 

  22. Bhat A, Hoch AI, Decaris ML, Leach JK. Alginate hydrogels containing cell-interactive beads for bone formation. FASEB J. 2013;27(12):4844–52.

    Article  Google Scholar 

  23. Glicklis R, Shapiro L, Agbaria R, Merchuk JC, Cohen S. Hepatocyte behavior within three-dimensional porous alginate scaffolds. Biotechnol Bioeng. 2005;67(3):344–53.

    Article  Google Scholar 

  24. Miner JH. Laminins and their roles in mammals. Microsc Res Tech. 2008;71(5):349–56.

    Article  Google Scholar 

  25. Williams SK, Kleinert LB, Patula-Steinbrenner V. Accelerated neovascularization and endothelialization of vascular grafts promoted by covalently bound laminin type 1. J Biomed Mater Res A. 2011;99(1):67–73.

    Article  Google Scholar 

  26. Stamati K, Priestley JV, Mudera V, Cheema U. Laminin promotes vascular network formation in 3D in vitro collagen scaffolds by regulating VEGF uptake. Exp Cell Res. 2014;327(1):68–77.

    Article  Google Scholar 

  27. Chen YS, Chen YY, Hsueh YS, Tai HC, Lin FH. Modifying alginate with early embryonic extracellular matrix, laminin and hyaluronic acid for adipose tissue engineering. J Biomed Mater Res A. 2015;104(3):669–77. doi:10.1002/jbm.a.35606.

  28. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13:4279–95.

    Article  Google Scholar 

  29. Dosier CR, Erdman CP, Park JH, Schwartz Z, Boyan BD, Guldberg RE. Resveratrol effect on osteogenic differentiation of rat and human adipose derived stem cells in a 3-D culture environment. J Mech Behav Biomed Mater. 2011;11:112–22.

    Article  Google Scholar 

  30. Yushkevich PA, Piven J, Hazlett HC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31:1116–28.

    Article  Google Scholar 

  31. Khouri RK, Rigotti G, Cardoso E, Khouri RK Jr, Biggs TM. Megavolume autologous fat transfer: part I. Theory and principles. Plast Reconstr Surg. 2014;133(3):550–7.

    Article  Google Scholar 

  32. Moulonguet I, de Goursac C, Plantier F. Granulomatous reaction after injection of a new resorbable filler Novabel. Am J Dermatopathol. 2011;33:710–1.

    Article  Google Scholar 

  33. Orive G, Hernández RM, Gascón AR, et al. Cell encapsulation: promise and progress. Nat Med. 2003;9:104–7.

    Article  Google Scholar 

  34. Lawson MA, Barralet JE, Wang L, Shelton RM, Triffitt JT. Adhesion and growth of bone marrow stromal cells on modified alginate hydrogels. Tissue Eng. 2004;10:1480–91.

    Article  Google Scholar 

  35. Smetana K Jr. Cell biology of hydrogels. Biomaterials. 1993;14:1046–50.

    Article  Google Scholar 

  36. Hohenester E, Tisi D, Talts JF, Timpl R. The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell. 1999;4:783–92.

    Article  Google Scholar 

  37. Kang SW, Cha BH, Park H, Park KS, Lee KY, Lee SH. The effect of conjugating RGD into 3D alginate hydrogels on adipogenic differentiation of human adipose-derived stromal cells. Macromol Biosci. 2011;11(5):673–9.

    Article  Google Scholar 

  38. Chandler EM, Berglund CM, Lee JS, Polacheck WJ, Gleghorn JP, Kirby BJ, et al. Stiffness of photocrosslinked RGD-alginate gels regulates adipose progenitor cell behavior. Biotechnol Bioeng. 2011;108(7):1683–92.

    Article  Google Scholar 

  39. Schuller-Petrović S, Pavlović MD, Schuller SS, Schuller-Lukić B, Neuhold N. Early granulomatous foreign body reactions to a novel alginate dermal filler: the system’s failure? J Eur Acad Dermatol Venereol. 2013;27(1):121–3.

    Article  Google Scholar 

  40. Andre P, Moulonguet I. Alginate (novabel): a new class of injectable filler. Facial Plast Surg. 2014;30(6):644–6.

    Article  Google Scholar 

  41. Coppack SW, Pinkney JH, Mohamed-Ali V. Leptin production in human adipose tissue. Proc Nutr Soc. 1998;57:461–70.

    Article  Google Scholar 

  42. Mohamed-Ali V, Pinkney JH, Coppack SW. Adipose tissue as an endocrine and paracrine organ. Int J Obes Relat Metab Disord. 1998;22:1145–58.

    Article  Google Scholar 

  43. Deng Y, Scherer PE. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N Y Acad Sci. 2010;1212:E1–19.

    Article  Google Scholar 

  44. Stillaert F, Findlay M, Palmer J, et al. Host rather than graft origin of Matrigel-induced adipose tissue in the murine tissue-engineering chamber. Tissue Eng. 2007;13:2291–300.

    Article  Google Scholar 

  45. Wu L, Wang T, Ge Y, Cai X, Wang J, Lin Y. Secreted factors from adipose tissue increase adipogenic differentiation of mesenchymal stem cells. Cell Prolif. 2012;45:311–9.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Ya-Hui Tsai and Hsiao-Fang Wei for technical and statistic assistance. We also thank the 7T Animal MRI Core Lab of the Neurobiology and Cognitive Science Center, National Taiwan University for their technical support.

Funding

The experiments in this study were partially funded by Far Eastern Memorial Hospital (FEMH-2012-C-004). No other funding was received.

Author contributions

Y-S C: First author, partially financed the study and carried out the project. Y-SH: Provided instruction for creating the laminin-alginate beads. Y-YC: Original author of the methods for creating the laminin-alginate biomaterial. C-YL: Pathologist, provided support for histological staining and reading. H-CT: Adviser regarding the medical aspects of this study. F-HL: Professor at the Institute of Biomedical Engineering and project director.

Author information

Authors and Affiliations

  1. Institute of Biomedical Engineering, National Taiwan University, Taipei, 10051, Taiwan

    Yo-Shen Chen, Yu-Sheng Hsueh, Yen-Yu Chen & Feng-Huei Lin

  2. Department of Plastic Surgery, Far Eastern Memorial Hospital, New Taipei City, 22060, Taiwan

    Yo-Shen Chen

  3. Department of Pathology, Far Eastern Memorial Hospital, New Taipei City, 22060, Taiwan

    Cheng-Yu Lo

  4. Department of Plastic Surgery, National Taiwan University Hospital, Taipei, 10051, Taiwan

    Hao-Chih Tai

  5. Institute of Biomedical Engineering and Nanomedicine, National Health Research Institutes, Miaoli, 35053, Taiwan

    Feng-Huei Lin

Authors
  1. Yo-Shen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Sheng Hsueh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yen-Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cheng-Yu Lo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hao-Chih Tai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Feng-Huei Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Feng-Huei Lin.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Presented at the 13th annual meeting of the International Federation for Adipose Therapeutics and Science (IFATS), New Orleans, Louisiana, USA, 2015. Title: Evaluation of biomaterial, adipocytes, and ADSC interaction in pure autologous fat grafting model through 7-TMRI.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, YS., Hsueh, YS., Chen, YY. et al. Evaluation of a laminin-alginate biomaterial, adipocytes, and adipocyte-derived stem cells interaction in animal autologous fat grafting model using 7-Tesla magnetic resonance imaging. J Mater Sci: Mater Med 28, 18 (2017). https://doi.org/10.1007/s10856-016-5826-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-016-5826-y

Keywords

Search

Navigation