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Mechanical versus enzymatic isolation of stromal vascular fraction cells from adipose tissue
Open accessAbstract
Clinical use of adipose-derived stem cells (ASCs) for a variety of indications is rapidly expanding in medicine. Most commonly, ASCs are isolated at the point of care from lipoaspirate tissue as the stromal vascular fraction (SVF). The cells are immediately administered to the patient as an injection or used to enrich fat grafts. Isolation of ASCs from adipose tissue is a relatively simple process performed routinely in cell biology laboratories, but isolation at the point of care for immediate clinical administration requires special methodology to prevent contamination, ensure integrity of clinical research and comply with regulatory requirements. A lack of practical laboratory experience, regulatory uncertainty and a relative paucity of objective published data can make selection of the optimum separation method for specific indications a difficult task for the clinician and can discourage clinical adoption. In this paper, we discuss the processes which can be used to separate SVF cells from fat tissue. We compare the various mechanical and enzymatic methods. We discuss the practical considerations involved in selecting an appropriate method from a clinical perspective. Studies consistently show that breakdown of the extracellular matrix achieved with proteolytic enzymes affords significantly greater efficiency to the separation process. SVF isolated through mechanical methods is equally safe, less costly and less time consuming but the product contains a higher frequency of blood mononuclear cells and fewer progenitor cells. Mechanical methods can provide a low cost, rapid and simple alternative to enzymatic isolation methods, and are attractive when smaller quantities of ASCs are sufficient.
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“The most commonly used tissue dissociation method is enzymatic digestion, which disolves the ECM46.”
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Multilineage Cells from Human Adipose Tissue: Implications for Cell-Based Therapies
Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., & Hedrick, M. H. (2001) · Tissue Engineering · doi:10.1089/107632701300062859 · Cited by 7,956
Liao, J., Wei, Q., Zou, Y., Fan, J., Song, D., Cui, J., Zhang, W., Zhu, Y., Ma, C., Hu, X., et al. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000471945 · Cited by 2,742
Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells
Rehman, J., Traktuev, D., Li, J., Merfeld-Clauss, S., Temm-Grove, C. J., Bovenkerk, J. E., Pell, C. L., Johnstone, B. H., Considine, R. V., & March, K. L. (2004) · Circulation · doi:10.1161/01.cir.0000121425.42966.f1 · Cited by 2,269
Bourin, P., Bunnell, B. A., Casteilla, L., Dominici, M., Katz, A. J., March, K. L., Redl, H., Rubin, J. P., Yoshimura, K., & Gimble, J. M. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.02.006 · Cited by 1,890 · cited 1×
“SVF contains a variety of cells including macrophages, various blood cells, pericytes, fibroblasts, smooth muscle cells, vascular endothelial progenitors and adipose-derived stem cells (Yoshimura et al. 2006; Bourin et al. 2013; Han et al. 2010; McIntosh et al. 2006; Bonab et al. 2006; Yoshimura et al. 2009).”
BackgroundPlanat-Benard, V., Silvestre, J.-S., Cousin, B., André, M., Nibbelink, M., Tamarat, R., Clergue, M., Manneville, C., Saillan-Barreau, C., Duriez, M., et al. (2004) · Circulation · doi:10.1161/01.cir.0000114522.38265.61 · Cited by 1,382
Mitchell, J. B., McIntosh, K. R., Zvonic, S., Garrett, S. M., Floyd, Z. E., Kloster, A. L., Halvorsen, Y. D. C., Storms, R. W., Goh, B. C. K., Kilroy, G. E., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0234 · Cited by 1,138
Aging of mesenchymal stem cell in vitro
Bonab, M. M., Alimoghaddam, K., Talebian, F., Ghaffari, S. H., Ghavamzadeh, A., & Nikbin, B. (2006) · BMC Cell Biology · doi:10.1186/1471-2121-7-14 · Cited by 914
Yoshimura, K., Shigeura, T., Matsumoto, D., Sato, T., Takaki, Y., Aiba‐Kojima, E., Sato, K., Inoue, K., Nagase, T., Koshima, I., et al. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20636 · Cited by 803
Yield of human adipose-derived adult stem cells from liposuction aspirates
Aust, L., Devlin, B., Foster, S. J., Halvorsen, Y. D. C., Hicok, K., du Laney, T., Sen, A., Willingmyre, G. D., & Gimble, J. M. (2004) · Cytotherapy · doi:10.1080/14653240310004539 · Cited by 708
The Fate of Adipocytes after Nonvascularized Fat Grafting
D, H. E. M., D, H. K. M., D, H. S. M., D, N. A. M., Doi, K., Kuno, S., & Yoshimura, K. (2012) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e31824a2b19 · Cited by 664
Matsumoto, D., D, K. S. M., Gonda, K., Takaki, Y., Shigeura, T., Sato, T., Aiba‐Kojima, E., Iizuka, F., Inoue, K., Suga, H., et al. (2006) · Tissue Engineering · doi:10.1089/ten.2006.12.3375 · Cited by 628
The Immunogenicity of Human Adipose‐Derived Cells: Temporal Changes In Vitro
McIntosh, K. R., Zvonic, S., Garrett, S. M., Mitchell, J. B., Floyd, Z. E., Hammill, L., Kloster, A. L., Halvorsen, Y. D. C., Ting, J. P. ‐., Storms, R. W., et al. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0235 · Cited by 579
Baer, P. C., & Geiger, H. (2012) · Stem Cells International · doi:10.1155/2012/812693 · Cited by 523
Stromal vascular progenitors in adult human adipose tissue
Zimmerlin, L., Donnenberg, V. S., Pfeifer, M. E., Meyer, E. M., Péault, B., Rubin, J. P., & Donnenberg, A. D. (2009) · Cytometry Part A · doi:10.1002/cyto.a.20813 · Cited by 501
Jurgens, W. J. F. M., Oedayrajsingh-Varma, M., Helder, M. N., Zandieh‐Doulabi, B., Schouten, T. E., Kuik, D. J., Ritt, M. J. P. F., & van Milligen, F. J. (2008) · Cell and Tissue Research · doi:10.1007/s00441-007-0555-7 · Cited by 385
Degeneration, Regeneration, and Cicatrization after Fat Grafting
D, H. K. M., Mineda, K., D, H. E. M., Doi, K., Kuno, S., Kinoshita, K., Kanayama, K., & Yoshimura, K. (2014) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000000066 · Cited by 360
Review of the adipose derived stem cell secretome
Kapur, S. K., & Katz, A. J. (2013) · Biochimie · doi:10.1016/j.biochi.2013.06.001 · Cited by 305
Suga, H., Eto, H., Aoi, N., D, H. K. M., Araki, J., Doi, K., Higashino, T., & Yoshimura, K. (2010) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e3181f4468b · Cited by 275
Yoshimura, K., Suga, H., & Eto, H. (2009) · Regenerative Medicine · doi:10.2217/17460751.4.2.265 · Cited by 260
Adipose tissue is an extramedullary reservoir for functional hematopoietic stem and progenitor cells
Han, J., Koh, Y. J., Moon, H. R., Ryoo, H. G., Cho, C., Kim, I., & Koh, G. Y. (2009) · Blood · doi:10.1182/blood-2009-05-219923 · Cited by 219
Characterization of adipose tissue-derived cells isolated with the Celution™ system
Lin, K., Matsubara, Y., Masuda, Y. M., Togashi, K., Ohno, T., TAMURA, T., Toyoshima, Y., Sugimachi, K., TOYODA, M., Marc, H., et al. (2008) · Cytotherapy · doi:10.1080/14653240801982979 · Cited by 205
Adipose Stromal Vascular Fraction Isolation
Aronowitz, J. A., & Ellenhorn, J. D. I. (2013) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e3182a80652 · Cited by 153
Self-citationMarino, G., Moraci, M., Armenia, E., Orabona, C., Sergio, R., Sena, G. D., Capuozzo, V., Barbarisi, M., Rosso, F., Giordano, G. G., et al. (2013) · Journal of Surgical Research · doi:10.1016/j.jss.2013.05.024 · Cited by 145
A non-enzymatic method for isolating human adipose tissue-derived stromal stem cells
Shah, F. S., Wu, X., Dietrich, M. A., Rood, J., & Gimble, J. M. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.04.001 · Cited by 138
Isolation of adipose-derived stem cells: a comparison among different methods
Franke, C., Frey, G. Z., Silveira, M. D., Chem, E. M., Milani, A. R., Ely, P. B., Horn, A. P., Nardi, N. B., & Camassola, M. (2013) · Biotechnology Letters · doi:10.1007/s10529-013-1425-x · Cited by 132
Domenis, R., Lazzaro, L., Calabrese, S., Mangoni, D., Gallelli, A., Bourkoula, E., Manini, I., Bergamin, N., Toffoletto, B., Beltrami, C. A., et al. (2015) · Stem Cell Research & Therapy · doi:10.1186/scrt536 · Cited by 131
Doi, K., Tanaka, S., Iida, H., D, H. E. M., D, H. K. M., D, N. A. M., Kuno, S., Hirohi, T., & Yoshimura, K. (2012) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.1478 · Cited by 107
Baptista, L. S., do Amaral, R. J. F. C., Carias, R. B. V., Aniceto, M., Cláudio-da-Silva, C. S., & Borojević, R. (2009) · Cytotherapy · doi:10.3109/14653240902981144 · Cited by 106
Autologous Cell-Enriched Fat Grafting for Breast Augmentation
Kamakura, T., & Ito, K. (2011) · Aesthetic Plastic Surgery · doi:10.1007/s00266-011-9727-7 · Cited by 103
A Novel and Effective Strategy for the Isolation of Adipose-Derived Stem Cells
Raposio, E., Caruana, G., Bonomini, S., & Libondi, G. (2014) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000000170 · Cited by 103
Fraser, J. K., Hicok, K. C., Shanahan, R., Zhu, M., Miller, S. H., & Arm, D. M. (2014) · Advances in Wound Care · doi:10.1089/wound.2012.0408 · Cited by 102
Cartilage Regeneration by Chondrogenic Induced Adult Stem Cells in Osteoarthritic Sheep Model
Ude, C. C., Sulaiman, S., Min-Hwei, N., Chen, H. C., Ahmad, J., Yahaya, N. M., Saim, A. B., & Idrus, R. B. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098770 · Cited by 93
Stem cell technology for bone regeneration: current status and potential applications
Asatrian, G., Pham, D., Hardy, W. R., James, A. W., & Péault, B. (2015) · Stem Cells and Cloning Advances and Applications · doi:10.2147/sccaa.s48423 · Cited by 87
A Novel and Effective Strategy for the Isolation of Adipose-Derived Stem Cells
Bertheuil, N., & Chaput, B. (2015) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000000927 · Cited by 86
Age influence on stromal vascular fraction cell yield obtained from human lipoaspirates
Dos-Anjos, S., Navarro-Palou, M., & Llull, R. (2014) · Cytotherapy · doi:10.1016/j.jcyt.2014.02.007 · Cited by 86
Adipose tissue cells, lipotransfer and cancer: A challenge for scientists, oncologists and surgeons
Bertolini, F., Lohsiriwat, V., Petit, J., & Kolonin, M. G. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.04.004 · Cited by 83
Buschmann, J., Gao, S., Härter, L., Hemmi, S., Welti, M., Werner, C. M. L., Calcagni, M., Cinelli, P., & Wanner, G. A. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.04.009 · Cited by 82
Güven, S., Karagianni, M., Schwalbe, M., Schreiner, S., Farhadi, J., Bula, S., Bieback, K., Martín, I., & Scherberich, A. (2012) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2011.0617 · Cited by 76
Derivation of Two New Human Embryonic Stem Cell Lines from Nonviable Human Embryos
Gavrilov, S., Marolt, D., Douglas, N. C., Prosser, R. W., Khalid, I., Sauer, M. V., Landry, D. W., Vunjak‐Novakovic, G., & Papaioannou, V. E. (2011) · Stem Cells International · doi:10.4061/2011/765378 · Cited by 72
Rocco, G. D., Gentile, A., Antonini, A., Ceradini, F., Wu, J. C., Capogrossi, M. C., & Toietta, G. (2010) · Stem Cells International · doi:10.4061/2011/304562 · Cited by 71
Adult adipose-derived stem cells and breast cancer: a controversial relationship
Bielli, A., Scioli, M. G., Gentile, P., Agostinelli, S., Tarquini, C., Cervelli, V., & Orlandi, A. (2014) · SpringerPlus · doi:10.1186/2193-1801-3-345 · Cited by 68
McCarthy, R. C., Breite, A. G., Green, M. L., & Dwulet, F. E. (2010) · Transplantation · doi:10.1097/tp.0b013e3181ffff7d · Cited by 62
Stem cell therapy for inflammatory bowel disease
Nagaishi, K., Arimura, Y., & Fujimiya, M. (2015) · Journal of Gastroenterology · doi:10.1007/s00535-015-1040-9 · Cited by 61
Naderi, N., Wilde, C., Haque, T., Francis, W., Seifalian, A. M., Thornton, C. A., Xia, Z., & Whitaker, I. S. (2014) · Journal of Plastic Reconstructive & Aesthetic Surgery · doi:10.1016/j.bjps.2014.08.013 · Cited by 47
Savi, M., Bocchi, L., Fiumana, E., Karam, J., Frati, C., Bonafè, F., Cavalli, S., Morselli, P. G., Guarnieri, C., Caldarera, C. M., et al. (2015) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35442 · Cited by 40
Condé‐Green, A., Rodriguez, R. L., Slezak, S. S., Singh, D. P., Goldberg, N. H., & McLenithan, J. C. (2014) · Plastic & Reconstructive Surgery · doi:10.1097/01.prs.0000455394.06800.62 · Cited by 40
Griffin, P. J., & Fogarty, W. M. (1973) · Applied Microbiology · doi:10.1128/am.26.2.191-195.1973 · Cited by 30
Tissue Dissociation Enzyme Neutral Protease Assessment
Breite, A. G., Dwulet, F. E., & McCarthy, R. C. (2010) · Transplantation Proceedings · doi:10.1016/j.transproceed.2010.05.118 · Cited by 28
[Cell-assisted lipotransfer for breast augmentation: a report of 18 patients].
Wang, L., Lu, Y., Luo, X., Fu, M., Hu, X., Dong, H. F., & Fan, Z.-H. (2012) · PubMed · Cited by 26
Borowski, D. W., Gill, T. S., Agarwal, A. K., Tabaqchali, M. A., Garg, D., & Bhaskar, P. (2015) · Surgical Innovation · doi:10.1177/1553350615572656 · Cited by 24
Production and Purification of the Metalloprotease of Bacillus polymyxa
Fogarty, W. M., & Griffin, P. J. (1973) · Applied Microbiology · doi:10.1128/am.26.2.185-190.1973 · Cited by 20
Williams, S. K., Kosnik, P. E., Kleinert, L. B., Vossman, E. M., Lye, K. D., & Shine, M. H. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0318 · Cited by 14
Production and Purification of the Metalloprotease of Bacillus polymyxa
Fogarty, W. M., & Griffin, P. J. (1973) · Applied Microbiology · doi:10.1128/aem.26.2.185-190.1973 · Cited by 14
Griffin, P. J., & Fogarty, W. M. (1973) · Applied Microbiology · doi:10.1128/aem.26.2.191-195.1973 · Cited by 13
Safety evaluation of a thermolysin enzyme produced from Geobacillus stearothermophilus
Ke, Q., Chen, A., Minoda, M., & Yoshida, H. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.06.046 · Cited by 10
Research works printed but not linked: 1
- Millan A, Landerholm T, Chapman JR (2014) Comparison between collagenase adipose digestion and Stromacell mechanical dissociation for mesenchymal stem cell separation. McNair Scholars J CSUS 15:86–101
Cited by
Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,082
Bora, P., & Majumdar, A. S. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0598-y · Cited by 550
Intra-articular treatment options for knee osteoarthritis
Jones, I. A., Togashi, R., Wilson, M. L., Heckmann, N. D., & Vangsness, C. T. (2018) · Nature Reviews Rheumatology · doi:10.1038/s41584-018-0123-4 · Cited by 559
Gaur, M., Dobke, M. K., & Lunyak, V. V. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18010208 · Cited by 203
Adipose Tissue-Derived Stem Cells: Immunomodulatory Effects and Therapeutic Potential
Al-Ghadban, S. I., & Bunnell, B. A. (2020) · Physiology · doi:10.1152/physiol.00021.2019 · Cited by 190
Metadata
- Authors
- Aronowitz, J. A., Lockhart, R. A., & Hakakian, C. S.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Aronowitz, Joel A.
- Venue
- SpringerPlus
- Published
- 2015-11-23
- Volume
- 4
- Issue
- 1
- Pages
- 713-713
- ISSN
- 2193-1801 (ISSN-L)
- PMC
- PMC4656256
- OpenAlex
- W2173002160
- Cited by
- 275
- References
- 55
- Citations by year
- 2026: 26 · 2025: 24 · 2024: 40 · 2023: 27 · 2022: 43 · 2021: 30 · 2020: 22 · 2019: 27 · 2018: 19 · 2017: 12 · 2016: 4
- FWCI
- 6.53
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- SpringerPlus (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Dentistry › Periodontics › Periodontal Regeneration and Treatments
- Keywords
- adipose-derived stem cells, stromal vascular fraction, enzymatic cell isolation, proteolytic enzymes, lipoaspirate, progenitor cells, fat graft
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