Abstract
Background
Soft tissue engineering offers new perspectives for improving fat graft survival, for which the appropriate association of cells and scaffold seems essential. This study aimed to analyze the survival of free-cell grafts compared with adipose-derived stem cells (ASCs) seeded on collagen scaffolds.
Methods
Adipose tissue from a single volunteer was used for the following preparations: purified adipose tissue, isolated mature adipocytes (free-cell graft), cultured ASCs without scaffold (free-cell graft), collagen scaffold only, cultured ASCs in collagen scaffold without and with bioactive factors, and freshly-isolated ASCs in collagen scaffold. These were grafted on 18 nude mice for 2 months, after which specimens were evaluated grossly and histologically using hematoxylin-phloxine-safran (HPS), Oil-Red-O, and antivimentin labeling. Specimens and animals were weighed before implantation and after explantation, and weight values were statistically analyzed.
Results
Free-cell grafts (mature adipocytes and free ASCs) showed complete resorption in 50 and 60% of the animals (remaining weight fraction was 22.5 and 5.3%, respectively). The survival of purified adipose tissue was 81.8% (statistically greater compared with free-cell grafts; p < 0.05). In the ASCs–scaffold association, the remaining weight fractions (87.3–70.4%) were statistically greater than in free-cell grafts (5.3–22.5%; p < 0.05), but the difference between ASC–scaffolds and fat grafts was not statistically significant. These results were confirmed by clinical and histologic observations.
Conclusion
Three-dimensional collagen scaffolds seem to improve survival of ASCs compared with free-cell grafts (adipocytes and free ASCs).
Similar content being viewed by others
References
Ashinoff R (2000) Overview: soft tissue augmentation. Clin Plast Surg 27:479–487
Beahm EK, Walton RL, Patrick JW (2003) Progress in adipose tissue construct development. Clin Plast Surg 30:547–558
Coleman SR (1997) Facial recontouring with lipostructure. Clin Plast Surg 24:347–367
Collombel C, Damour O, Gagnieu C, Marichy J, Poinsignon F (1987) Biomaterials with a base of collagen, chitosan, and glycosaminoglycans: process for preparing them and their application in human medicine. French patent 8708252, 1987; European patent 884101948, 1988; U.S. patent PCT/FR/8800303, 1989
Dubois SG, Floyd EZ, Zvonic S et al (2008) Isolation of human adipose-derived stem cells from biopsies and liposuction. Methods Mol Biol 449:69–79
Flynn LE (2010) The use of decellularized adipose tissue to provide an inductive microenvironment for the adipogenic differentiation of human adipose-derived stem cells. Biomaterials 31:4715–4724
Flynn LE, Prestwich GD, Semple JL, Woodhouse KA (2008) Proliferation and differentiation of adipose-derived stem cells on naturally derived scaffolds. Biomaterials 29:1862–1871
Garfein ES, Orgill DP, Pribaz JJ (2003) Clinical applications of tissue engineered constructs. Clin Plast Surg 30:485–496
Gastaldi G, Asti A, Scaffino MF, Visai L, Saino E, Cometa AM, Benazzo F (2010) Human adipose-derived stem cells (hASCs) proliferate and differentiate in osteoblast-like cells on trabecular titanium scaffolds. J Biomed Mater Res A 94:790–799
Gimble J, Guilak F (2003) Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5:362–369
Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100:1249–1260
Gomillion CT, Burg JLK (2006) Stem cells and adipose tissue engineering. Biomaterials 27:6052–6063
Hemmrich K, Van de Sijpe K, Rhodes NP (2008) Autologous in vivo adipose tissue engineering in hyaluronan-based gels: a pilot study. J Surg Res 144:82–88
Jauffret JL, Champsaur P, Robaglia-Schlupp A, Andrac-Meyer L, Magalon G (2001) Arguments in favor of adipocyte grafts with the S.R. Coleman technique. Ann Chir Plast Esthet 46:31–38
Katz AJ, Llull R, Hedrick MH, Futrell JW (1999) Emerging approaches to the tissue engineering of fat. Clin Plast Surg 26:587–603
Klaus S, Ely M, Encke D, Heldmaier G (1995) Functional assessment of white and brown adipocyte development and energy metabolism in cell culture: dissociation of terminal differentiation and thermogenesis in brown adipocytes. J Cell Sci 108:3171–3180
Lequeux C, Oni G, Mojallal A, Damour O, Braown SA (2011) Adipose-derived stem cells: efficiency, toxicity, stability of BrdU labeling and effects on self-renewal and adipose differentiation. Mol Cell Biochem. doi:10.1007/s11010-011-0712-x
Masuda T, Furue M, Matsuda T (2004) Novel strategy for soft tissue augmentation based on transplantation of fragmented omentum and preadipocytes. Tissue Eng 10:1672–1683
Masuda T, Furue M, Matsuda T (2004) Photocured, styrenated gelatin-based microspheres for de novo adipogenesis through co-release of basic fibroblast grow factor, insulin, and insulin-like growth factor I. Tissue Eng 10:523–535
Meyerrose TE, De Ugarte DA, Hofling AA, Herrbrich PE, Cordonnier TD, Shultz LD et al (2007) In vivo distribution of human adipose-derived mesenchymal stem cells in novel xenotransplantation models. Stem Cells 25:220–227
Mojallal A, Lequeux C, Shipkov C, Breton P, Foyatier JL, Braye F, Damour O (2009) Improvement of skin quality after fat grafting: clinical observation and an animal study. Plast Reconstr Surg 124:765–774
Nakajima I, Yamaguchi T, Ozutsumi K, Aso H (1998) Adipose tissue extracellular matrix: newly organized by adipocytes during differentiation. Differentiation 63:193–200
Patrick CW (2001) Tissue engineering strategies for adipose tissue repair. Anat Rec 4:361–366
Patrick CW (2004) Breast tissue engineering. Annu Rev Biomed Eng 6:109–130
Patrick CW, Miller MJ (2003) Tissue engineering. Clin Plast Surg 1:91–105
Rubin JP, Bennett JM, Doctor JS, Tebbets BM, Marra KG (2007) Collagenous microbeads as a scaffold for tissue engineering with adipose-derived stem cells. Plast Reconstr Surg 120:414–424
Sadat S, Gehmert S, Song YH, Yen Y, Bai X, Gaiser S, Klein H, Alt E (2007) The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 3:674–679
Sandor GKB, Suuronen R (2008) Combining adipose-derived stem cells, resorbable Scaffolds, and growth factors: an overview of tissue engineering. JCDA 74:167–169
Sterodimas A, de Faria J, Nicaretta B, Pitanguy I (2010) Tissue engineering with adipose-derived stem cells (ADSCs): current and future applications. J Plast Reconstr Aesthet Surg 63:1886–1892
Stosich MS, Mao JJ (2007) Adipose tissue engineering from human adult stem cells: clinical implications in plastic and reconstructive surgery. Plast Reconstr Surg 119:71–83
Supronowicz P, Gill E, Trujillo A, Thula T, Zhukauskas R, Ramos T, Cobb R (2010) Human adipose-derived side population stem cells cultured on demineralized bone matrix for bone tissue engineering. Tissue Eng Part A. doi:10.1089/ten.TEA.2010.0357
Tanzi MC, Faré S (2009) Adipose tissue engineering: state of the art, recent advances, and innovative approaches. Expert Rev Med Devices 6:533–551
von Heimburg D, Zachariah S, Heschel I, Kühling H, Schoof H, Hafemann B, Pallua N (2001) Human preadipocytes seeded on freeze-dried collagen scaffolds investigated in vitro and in vivo. Biomaterials 22:429–438
von Heimburg D, Zachariah S, Low A, Pallua N (2001) Influence of different biodegradable carriers on the in vivo behavior of human adipose precursor cells. Plast Reconstr Surg 108:411–420
Weiser B, Prantl L, Schubert TE, Zellner J, Fischbach-Teschl C, Spruss T, Seitz AK, Tessmar J, Goepferich A, Blunk T (2008) In vivo development and long-term survival of engineered adipose tissue depend on in vitro precultivation strategy. Tissue Eng Part A 2:275–284
Yang Q, Peng J, Lu S, Huang J, Yao J, Yang F et al (2008) A cartilage ECM-derived 3D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Tissue Eng Part A 14:800–811
Yoshimura K, Matsumoto D, Gonda K (2005) A clinical trial of soft tissue augmentation by lipoinjection with adipose-derived stromal cells (ASCs). In: Proceedings of the 3rd annual meeting of International Fat Applied Technology Society (IFATS), Charlottesville, VA, pp 9–10
Zhao YN, Lin H, Zhang J, Chen B, Sun WJ, Wang X et al (2009) Cross-linked three-dimensional demineralized bone matrix for the adipose-derived stromal cell proliferation and differentiation. Tissue Eng Part A 15:13–21
Zhu M, Zhou Z, Chen Y, Schreiber R, Ransom JT, Fraser JK, Hedrick MH, Pinkernell K, Kuo HC (2010) Supplementation of fat grafts with adipose-derived regenerative cells improves long-term graft retention. Ann Plast Surg 64:22–28
Acknowledgments
The authors have no financial interests in this research project or in any of the techniques or equipment used in this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mojallal, A., Lequeux, C., Shipkov, C. et al. Stem Cells, Mature Adipocytes, and Extracellular Scaffold: What Does Each Contribute to Fat Graft Survival?. Aesth Plast Surg 35, 1061–1072 (2011). https://doi.org/10.1007/s00266-011-9734-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00266-011-9734-8