Research progress of adipose-derived stem cells in promoting the repair of peripheral nerve injury_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHANG Fengling , DENG Chengliang , XIAO Shun’e ,  WEI Zairong

Department of Burn Plastic Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi Guizhou, 563003, P.R.China;

Corresponding author：

WEI Zairong, Email: zairongwei@163.com

Keywords：

Adipose-derived stem cells; peripheral nerve injury; repair; mechanism; application

DOI：

10.7507/1002-1892.201910009

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of adipose-derived stem cells (ADSCs) in promoting the repair of peripheral nerve injury.Methods The related literature at home and abroad in recent years was widely reviewed, the mechanism of ADSCs promoting the repair of peripheral nerve injury was introduced, and its basic research progress was analyzed and summarized. Finally, the clinical transformation application of ADSCs in the treatment of peripheral nerve injury was introduced, the existing problems were pointed out, and the new treatment regimen was prospected.Results ADSCs have the function of differentiation and paracrine, and their secreted neurotrophic factors, antiapoptosis, and antioxidant factors can promote the repair of peripheral nerve injury.Conclusion ADSCs are rich in content and easy to obtain, which has a definite effectiveness on the repair of peripheral nerve injury with potential clinical prospect.

Citation： ZHANG Fengling, DENG Chengliang, XIAO Shun’e, WEI Zairong. Research progress of adipose-derived stem cells in promoting the repair of peripheral nerve injury. Chinese Journal of Reparative and Reconstructive Surgery, 2020, 34(8): 1059-1064. doi: 10.7507/1002-1892.201910009 Copy

1.	Mackinnon SE, Hudson AR. Clinical application of peripheral nerve transplantation. Plast Reconstr Surg, 1992, 90(4): 695-699.
2.	Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci, 2007, 30: 209-233.
3.	Riccio M, Marchesini A, Pugliese P, et al. Nerve repair and regeneration: Biological tubulization limits and future perspectives. J Cell Physiol, 2019, 234(4): 3362-3375.
4.	Assinck P, Duncan GJ, Hilton BJ, et al. Cell transplantation therapy for spinal cord injury. Nat Neurosci, 2017, 20(5): 637-647.
5.	Faroni A, Terenghi G, Reid AJ. Adipose-derived stem cells and nerve regeneration: promises and pitfalls. Int Rev Neurobiol, 2013, 108: 121-136.
6.	Watanabe Y, Sasaki R, Matsumine H, et al. Undifferentiated and differentiated adipose-derived stem cells improve nerve regeneration in a rat model of facial nerve defect. J Tissue Eng Regen Med, 2017, 11(2): 362-374.
7.	Orbay H, Uysal AC, Hyakusoku H, et al. Differentiated and undifferentiated adipose-derived stem cells improve function in rats with peripheral nerve gaps. J Plast Reconstr Aesthet Surg, 2012, 65(5): 657-664.
8.	Shen CC, Yang YC, Liu BS. Peripheral nerve repair of transplanted undifferentiated adipose tissue-derived stem cells in a biodegradable reinforced nerve conduit. J Biomed Mater Res A, 2012, 100(1): 48-63.
9.	Hsu MN, Liao HT, Li KC, et al. Adipose-derived stem cell sheets functionalized by hybrid baculovirus for prolonged GDNF expression and improved nerve regeneration. Biomaterials, 2017, 140: 189-200.
10.	Sowa Y, Imura T, Numajiri T, et al. Adipose-derived stem cells produce factors enhancing peripheral nerve regeneration: influence of age and anatomic site of origin. Stem Cells Dev, 2012, 21(11): 1852-1862.
11.	Scheib J, Höke A. Advances in peripheral nerve regeneration. Nat Rev Neurol, 2013, 9(12): 668-676.
12.	Arthur-Farraj PJ, Latouche M, Wilton DK, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron, 2012, 75(4): 633-647.
13.	Cattin AL, Burden JJ, Van Emmenis L, et al. Macrophage-induced blood vessels guide Schwann cell-mediated regeneration of peripheral nerves. Cell, 2015, 162(5): 1127-1139.
14.	Kolar MK, Kingham PJ. Regenerative effects of adipose-tissue-derived stem cells for treatment of peripheral nerve injuries. Biochem Soc Trans, 2014, 42(3): 697-701.
15.	Phinney DG, Pittenger MF. Concise review: MSC-derived exosomes for cell-free therapy. Stem Cells, 2017, 35(4): 851-858.
16.	Salgado AJ, Reis RL, Sousa NJ, et al. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther, 2010, 5(2): 103-110.
17.	Lopatina T, Kalinina N, Karagyaur M, et al. Adipose-derived stem cells stimulate regeneration of peripheral nerves: BDNF secreted by these cells promotes nerve healing and axon growth de novo. PLoS One, 2011, 6(3): e17899.
18.	Kingham PJ, Kolar MK, Novikova LN, et al. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. Stem Cells Dev, 2014, 23(7): 741-754.
19.	Suga H, Glotzbach JP, Sorkin M, et al. Paracrine mechanism of angiogenesis in adipose-derived stem cell transplantation. Ann Plast Surg, 2014, 72(2): 234-241.
20.	Han Y, Ren J, Bai Y, et al. Exosomes from hypoxia-treated human adipose-derived mesenchymal stem cells enhance angiogenesis through VEGF/VEGF-R. Int J Biochem Cell Biol, 2019, 109: 59-68.
21.	Kim WS, Park BS, Sung JH. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin Biol Ther, 2009, 9(7): 879-887.
22.	Liu CY, Yin G, Sun YD, et al. Effect of exosomes from adipose-derived stem cells on the apoptosis of Schwann cells in peripheral nerve injury. CNS Neurosci Ther, 2020, 26(2): 189-196.
23.	Schweizer R, Gorantla VS, Plock JA. Premise and promise of mesenchymal stem cell-based therapies in clinical vascularized composite allotransplantation. Curr Opin Organ Transplant, 2015, 20(6): 608-614.
24.	Cui L, Yin S, Liu W, et al. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng, 2007, 13(6): 1185-1195.
25.	Crop MJ, Baan CC, Korevaar SS, et al. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clin Exp Immunol, 2010, 162(3): 474-486.
26.	Kuo YR, Chen CC, Chen YC, et al. Recipient adipose-derived stem cells enhance recipient cell engraftment and prolong allotransplant survival in a miniature swine hind-limb model. Cell Transplant, 2017, 26(8): 1418-1427.
27.	Chen S, Cui G, Peng C, et al. Transplantation of adipose-derived mesenchymal stem cells attenuates pulmonary fibrosis of silicosis via anti-inflammatory and anti-apoptosis effects in rats. Stem Cell Res Ther, 2018, 9(1): 110.
28.	Kapur SK, Katz AJ. Review of the adipose derived stem cell secretome. Biochimie, 2013, 95(12): 2222-2228.
29.	Kingham PJ, Kalbermatten DF, Mahay D, et al. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol, 2007, 207(2): 267-274.
30.	Moosazadeh Moghaddam M, Bonakdar S, Shokrgozar MA, et al. Engineered substrates with imprinted cell-like topographies induce direct differentiation of adipose-derived mesenchymal stem cells into Schwann cells. Artif Cells Nanomed Biotechnol, 2019, 47(1): 1022-1035.
31.	Lu P, Blesch A, Tuszynski MH. Induction of bone marrow stromal cells to neurons: Differentiation, transdifferentiation, or artifact? J Neurosci Res, 2004, 77(2): 174-191.
32.	Chen Y, Teng FY, Tang BL. Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: progress and uncertainties. Cell Mol Life Sci, 2006, 63(14): 1649-1657.
33.	Faroni A, Smith RJ, Lu L, et al. Human Schwann-like cells derived from adipose-derived mesenchymal stem cells rapidly de-differentiate in the absence of stimulating medium. Eur J Neurosci, 2016, 43(3): 417-430.
34.	Kang Y, Liu Y, Liu Z, et al. Differentiated human adipose-derived stromal cells exhibit the phenotypic and functional characteristics of mature Schwann cells through a modified approach. Cytotherapy, 2019, 21(9): 987-1003.
35.	Abdanipour A, Tiraihi T. Induction of adipose-derived stem cell into motoneuron-like cells using selegiline as preinducer. Brain Res, 2012, 1440: 23-33.
36.	Liqing Y, Jia G, Jiqing C, et al. Directed differentiation of motor neuron cell-like cells from human adipose-derived stem cells in vitro. Neuroreport, 2011, 22(8): 370-373.
37.	Moon MY, Kim HJ, Choi BY, et al. Zinc Promotes adipose-derived mesenchymal stem cell proliferation and differentiation towards a neuronal fate. Stem Cells Int, 2018, 2018: 5736535.
38.	Ying CC, Yang M, Wang Y, et al. Neural-like cells from adipose-derived stem cells for cavernous nerve injury in rats. Neural Regen Res, 2019, 14(6): 1085-1090.
39.	赵斌, 马剑雄, 马信龙. 组织工程周围神经血管化研究进展. 中国修复重建外科杂志, 2019, 33(8): 1029-1032.
40.	Nie C, Yang D, Xu J, et al. Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant, 2011, 20(2): 205-216.
41.	Almalki SG, Llamas Valle Y, Agrawal DK. MMP-2 and MMP-14 silencing inhibits VEGFR2 cleavage and induces the differentiation of porcine adipose-derived mesenchymal stem cells to endothelial cells. Stem Cells Transl Med, 2017, 6(5): 1385-1398.
42.	周虹, 张涛. 脂肪间充质干细胞分化为内皮细胞并体外构建组织工程心脏瓣膜. 中国组织工程研究, 2012, 16(27): 4979-4984.
43.	Syu WZ, Hueng DY, Chen WL, et al. Adipose-derived neural stem cells combined with acellular dermal matrix as a neural conduit enhances peripheral nerve repair. Cell Transplant, 2019, 28(9-10): 1220-1230.
44.	Tomita K, Nishibayashi A, Yano K, et al. Differentiated adipose-derived stem cells promote reinnervation of rat skin flaps. Plast Reconstr Surg Glob Open, 2013, 1(3): e22.
45.	尹刚, 刘蔡钺, 林耀发, 等. 脂肪干细胞来源外泌体对周围神经损伤后再生作用的实验研究. 中国修复重建外科杂志, 2018, 32(12): 103-107.
46.	Bucan V, Vaslaitis D, Peck CT, et al. Effect of exosomes from rat adipose-derived mesenchymal stem cells on neurite outgrowth and sciatic nerve regeneration after crush injury. Mol Neurobiol, 2019, 56(3): 1812-1824.
47.	Chen J, Ren S, Duscher D, et al. Exosomes from human adipose-derived stem cells promote sciatic nerve regeneration via optimizing Schwann cell function. J Cell Physiol, 2019, 234(12): 23097-23110.
48.	Hsu MN, Liao HT, Truong VA, et al. CRISPR-based activation of endogenous neurotrophic genes in adipose stem cell sheets to stimulate peripheral nerve regeneration. Theranostics, 2019, 9(21): 6099-6111.
49.	Thakkar UG, Vanikar AV, Trivedi HL. Co-infusion of autologous adipose tissue derived neuronal differentiated mesenchymal stem cells and bone marrow derived hematopoietic stem cells, a viable therapy for post-traumatic brachial plexus injury: a case report. Biomed J, 2014, 37(4): 237-240.
50.	Haahr MK, Jensen CH, Toyserkani NM, et al. Safety and potential effect of a single intracavernous injection of autologous adipose-derived regenerative cells in patients with erectile dysfunction following radical prostatectomy: An open-label phase Ⅰ clinical trial. EBioMedicine, 2016, 5: 204-210.
51.	Haahr MK, Harken Jensen C, Toyserkani NM, et al. A 12-month follow-up after a single intracavernous injection of autologous adipose-derived regenerative cells in patients with erectile dysfunction following radical prostatectomy: An open-label phase Ⅰ clinical trial. Urology, 2018, 121: 203.
52.	Yao Y, Cai J, Zhang P, et al. Adipose stromal vascular fraction gel grafting: A new method for tissue volumization and rejuvenation. Dermatol Surg, 2018, 44(10): 1278-1286.
53.	Deng CL, Yao YZ, Liu ZY, et al. Chronic wound treatment with high-density nanofat grafting combined with negative pressure wound therapy. Int J Clin Exp Med, 2019, 12(2): 1402-1411.
54.	Deng C, Wang L, Feng J, et al. Treatment of human chronic wounds with autologous extracellular matrix/stromal vascular fraction gel: A STROBE-compliant study. Medicine (Baltimore), 2018, 97(32): e11667.
55.	邓呈亮, 肖顺娥, 刘志远, 等. 脂肪干细胞胶在眶周年轻化中的疗效观察. 中国美容整形外科杂志, 2019, 30(6): 321-323, 327.
56.	Tonnard P, Verpaele A, Peeters G, et al. Nanofat grafting: basic research and clinical applications. Plast Reconstr Surg, 2013, 132(4): 1017-1026.

1. Mackinnon SE, Hudson AR. Clinical application of peripheral nerve transplantation. Plast Reconstr Surg, 1992, 90(4): 695-699.
2. Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci, 2007, 30: 209-233.
3. Riccio M, Marchesini A, Pugliese P, et al. Nerve repair and regeneration: Biological tubulization limits and future perspectives. J Cell Physiol, 2019, 234(4): 3362-3375.
4. Assinck P, Duncan GJ, Hilton BJ, et al. Cell transplantation therapy for spinal cord injury. Nat Neurosci, 2017, 20(5): 637-647.
5. Faroni A, Terenghi G, Reid AJ. Adipose-derived stem cells and nerve regeneration: promises and pitfalls. Int Rev Neurobiol, 2013, 108: 121-136.
6. Watanabe Y, Sasaki R, Matsumine H, et al. Undifferentiated and differentiated adipose-derived stem cells improve nerve regeneration in a rat model of facial nerve defect. J Tissue Eng Regen Med, 2017, 11(2): 362-374.
7. Orbay H, Uysal AC, Hyakusoku H, et al. Differentiated and undifferentiated adipose-derived stem cells improve function in rats with peripheral nerve gaps. J Plast Reconstr Aesthet Surg, 2012, 65(5): 657-664.
8. Shen CC, Yang YC, Liu BS. Peripheral nerve repair of transplanted undifferentiated adipose tissue-derived stem cells in a biodegradable reinforced nerve conduit. J Biomed Mater Res A, 2012, 100(1): 48-63.
9. Hsu MN, Liao HT, Li KC, et al. Adipose-derived stem cell sheets functionalized by hybrid baculovirus for prolonged GDNF expression and improved nerve regeneration. Biomaterials, 2017, 140: 189-200.
10. Sowa Y, Imura T, Numajiri T, et al. Adipose-derived stem cells produce factors enhancing peripheral nerve regeneration: influence of age and anatomic site of origin. Stem Cells Dev, 2012, 21(11): 1852-1862.
11. Scheib J, Höke A. Advances in peripheral nerve regeneration. Nat Rev Neurol, 2013, 9(12): 668-676.
12. Arthur-Farraj PJ, Latouche M, Wilton DK, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron, 2012, 75(4): 633-647.
13. Cattin AL, Burden JJ, Van Emmenis L, et al. Macrophage-induced blood vessels guide Schwann cell-mediated regeneration of peripheral nerves. Cell, 2015, 162(5): 1127-1139.
14. Kolar MK, Kingham PJ. Regenerative effects of adipose-tissue-derived stem cells for treatment of peripheral nerve injuries. Biochem Soc Trans, 2014, 42(3): 697-701.
15. Phinney DG, Pittenger MF. Concise review: MSC-derived exosomes for cell-free therapy. Stem Cells, 2017, 35(4): 851-858.
16. Salgado AJ, Reis RL, Sousa NJ, et al. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther, 2010, 5(2): 103-110.
17. Lopatina T, Kalinina N, Karagyaur M, et al. Adipose-derived stem cells stimulate regeneration of peripheral nerves: BDNF secreted by these cells promotes nerve healing and axon growth de novo. PLoS One, 2011, 6(3): e17899.
18. Kingham PJ, Kolar MK, Novikova LN, et al. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. Stem Cells Dev, 2014, 23(7): 741-754.
19. Suga H, Glotzbach JP, Sorkin M, et al. Paracrine mechanism of angiogenesis in adipose-derived stem cell transplantation. Ann Plast Surg, 2014, 72(2): 234-241.
20. Han Y, Ren J, Bai Y, et al. Exosomes from hypoxia-treated human adipose-derived mesenchymal stem cells enhance angiogenesis through VEGF/VEGF-R. Int J Biochem Cell Biol, 2019, 109: 59-68.
21. Kim WS, Park BS, Sung JH. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin Biol Ther, 2009, 9(7): 879-887.
22. Liu CY, Yin G, Sun YD, et al. Effect of exosomes from adipose-derived stem cells on the apoptosis of Schwann cells in peripheral nerve injury. CNS Neurosci Ther, 2020, 26(2): 189-196.
23. Schweizer R, Gorantla VS, Plock JA. Premise and promise of mesenchymal stem cell-based therapies in clinical vascularized composite allotransplantation. Curr Opin Organ Transplant, 2015, 20(6): 608-614.
24. Cui L, Yin S, Liu W, et al. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng, 2007, 13(6): 1185-1195.
25. Crop MJ, Baan CC, Korevaar SS, et al. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clin Exp Immunol, 2010, 162(3): 474-486.
26. Kuo YR, Chen CC, Chen YC, et al. Recipient adipose-derived stem cells enhance recipient cell engraftment and prolong allotransplant survival in a miniature swine hind-limb model. Cell Transplant, 2017, 26(8): 1418-1427.
27. Chen S, Cui G, Peng C, et al. Transplantation of adipose-derived mesenchymal stem cells attenuates pulmonary fibrosis of silicosis via anti-inflammatory and anti-apoptosis effects in rats. Stem Cell Res Ther, 2018, 9(1): 110.
28. Kapur SK, Katz AJ. Review of the adipose derived stem cell secretome. Biochimie, 2013, 95(12): 2222-2228.
29. Kingham PJ, Kalbermatten DF, Mahay D, et al. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol, 2007, 207(2): 267-274.
30. Moosazadeh Moghaddam M, Bonakdar S, Shokrgozar MA, et al. Engineered substrates with imprinted cell-like topographies induce direct differentiation of adipose-derived mesenchymal stem cells into Schwann cells. Artif Cells Nanomed Biotechnol, 2019, 47(1): 1022-1035.
31. Lu P, Blesch A, Tuszynski MH. Induction of bone marrow stromal cells to neurons: Differentiation, transdifferentiation, or artifact? J Neurosci Res, 2004, 77(2): 174-191.
32. Chen Y, Teng FY, Tang BL. Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: progress and uncertainties. Cell Mol Life Sci, 2006, 63(14): 1649-1657.
33. Faroni A, Smith RJ, Lu L, et al. Human Schwann-like cells derived from adipose-derived mesenchymal stem cells rapidly de-differentiate in the absence of stimulating medium. Eur J Neurosci, 2016, 43(3): 417-430.
34. Kang Y, Liu Y, Liu Z, et al. Differentiated human adipose-derived stromal cells exhibit the phenotypic and functional characteristics of mature Schwann cells through a modified approach. Cytotherapy, 2019, 21(9): 987-1003.
35. Abdanipour A, Tiraihi T. Induction of adipose-derived stem cell into motoneuron-like cells using selegiline as preinducer. Brain Res, 2012, 1440: 23-33.
36. Liqing Y, Jia G, Jiqing C, et al. Directed differentiation of motor neuron cell-like cells from human adipose-derived stem cells in vitro. Neuroreport, 2011, 22(8): 370-373.
37. Moon MY, Kim HJ, Choi BY, et al. Zinc Promotes adipose-derived mesenchymal stem cell proliferation and differentiation towards a neuronal fate. Stem Cells Int, 2018, 2018: 5736535.
38. Ying CC, Yang M, Wang Y, et al. Neural-like cells from adipose-derived stem cells for cavernous nerve injury in rats. Neural Regen Res, 2019, 14(6): 1085-1090.
39. 赵斌, 马剑雄, 马信龙. 组织工程周围神经血管化研究进展. 中国修复重建外科杂志, 2019, 33(8): 1029-1032.
40. Nie C, Yang D, Xu J, et al. Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant, 2011, 20(2): 205-216.
41. Almalki SG, Llamas Valle Y, Agrawal DK. MMP-2 and MMP-14 silencing inhibits VEGFR2 cleavage and induces the differentiation of porcine adipose-derived mesenchymal stem cells to endothelial cells. Stem Cells Transl Med, 2017, 6(5): 1385-1398.
42. 周虹, 张涛. 脂肪间充质干细胞分化为内皮细胞并体外构建组织工程心脏瓣膜. 中国组织工程研究, 2012, 16(27): 4979-4984.
43. Syu WZ, Hueng DY, Chen WL, et al. Adipose-derived neural stem cells combined with acellular dermal matrix as a neural conduit enhances peripheral nerve repair. Cell Transplant, 2019, 28(9-10): 1220-1230.
44. Tomita K, Nishibayashi A, Yano K, et al. Differentiated adipose-derived stem cells promote reinnervation of rat skin flaps. Plast Reconstr Surg Glob Open, 2013, 1(3): e22.
45. 尹刚, 刘蔡钺, 林耀发, 等. 脂肪干细胞来源外泌体对周围神经损伤后再生作用的实验研究. 中国修复重建外科杂志, 2018, 32(12): 103-107.
46. Bucan V, Vaslaitis D, Peck CT, et al. Effect of exosomes from rat adipose-derived mesenchymal stem cells on neurite outgrowth and sciatic nerve regeneration after crush injury. Mol Neurobiol, 2019, 56(3): 1812-1824.
47. Chen J, Ren S, Duscher D, et al. Exosomes from human adipose-derived stem cells promote sciatic nerve regeneration via optimizing Schwann cell function. J Cell Physiol, 2019, 234(12): 23097-23110.
48. Hsu MN, Liao HT, Truong VA, et al. CRISPR-based activation of endogenous neurotrophic genes in adipose stem cell sheets to stimulate peripheral nerve regeneration. Theranostics, 2019, 9(21): 6099-6111.
49. Thakkar UG, Vanikar AV, Trivedi HL. Co-infusion of autologous adipose tissue derived neuronal differentiated mesenchymal stem cells and bone marrow derived hematopoietic stem cells, a viable therapy for post-traumatic brachial plexus injury: a case report. Biomed J, 2014, 37(4): 237-240.
50. Haahr MK, Jensen CH, Toyserkani NM, et al. Safety and potential effect of a single intracavernous injection of autologous adipose-derived regenerative cells in patients with erectile dysfunction following radical prostatectomy: An open-label phase Ⅰ clinical trial. EBioMedicine, 2016, 5: 204-210.
51. Haahr MK, Harken Jensen C, Toyserkani NM, et al. A 12-month follow-up after a single intracavernous injection of autologous adipose-derived regenerative cells in patients with erectile dysfunction following radical prostatectomy: An open-label phase Ⅰ clinical trial. Urology, 2018, 121: 203.
52. Yao Y, Cai J, Zhang P, et al. Adipose stromal vascular fraction gel grafting: A new method for tissue volumization and rejuvenation. Dermatol Surg, 2018, 44(10): 1278-1286.
53. Deng CL, Yao YZ, Liu ZY, et al. Chronic wound treatment with high-density nanofat grafting combined with negative pressure wound therapy. Int J Clin Exp Med, 2019, 12(2): 1402-1411.
54. Deng C, Wang L, Feng J, et al. Treatment of human chronic wounds with autologous extracellular matrix/stromal vascular fraction gel: A STROBE-compliant study. Medicine (Baltimore), 2018, 97(32): e11667.
55. 邓呈亮, 肖顺娥, 刘志远, 等. 脂肪干细胞胶在眶周年轻化中的疗效观察. 中国美容整形外科杂志, 2019, 30(6): 321-323, 327.
56. Tonnard P, Verpaele A, Peeters G, et al. Nanofat grafting: basic research and clinical applications. Plast Reconstr Surg, 2013, 132(4): 1017-1026.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of adipose-derived stem cells in promoting the repair of peripheral nerve injury

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