Advances in stem cell transplantation for thromboangiitis obliterans_West China Medical Journal

Authors：

YANG Jinjiang ^1,2 ,  YANG Yong ^1,2 , MA Zhenhuan ^1,2

1. Department of Vascular Surgery, the Fourth Affiliated Hospital of Kunming Medical University, Kunming, Yunnan 650000, P. R. China;
2. Vascular Surgery Center of Yunnan Province, Kunming, Yunnan 650000, P. R. China;

Corresponding author：

YANG Yong, Email: yncvs126@126.com

Keywords：

Stem cell transplant; Thromboangiitis obliterans; Clinical research; Efficacy evaluation; Serious adverse event

DOI：

10.7507/1002-0179.201912123

Video：

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Abstract Full text Figures/Tables Video References Cited by

Stem cell transplantation is one of the main methods to treat thromboangiitis obliterans (TAO). In recent years, research on the treatment mechanism of stem cell transplantation has made some progress. The results of a number of stem cell clinical trials specifically for TAO have been published. Some new stem cell types have gradually been used in the clinic. There is no major dispute over security. In addition, research shows that the efficacy of stem cell transplantation is affected in many ways, and some factors have a certain predictive effect on the possibility of amputation after transplantation. This paper reviews the clinical research progress of stem cell transplantation for TAO, and aims to provide some basis for the better use of stem cell transplantation in the treatment of TAO.

Citation： YANG Jinjiang, YANG Yong, MA Zhenhuan. Advances in stem cell transplantation for thromboangiitis obliterans. West China Medical Journal, 2020, 35(3): 357-362. doi: 10.7507/1002-0179.201912123 Copy

1.	Folkman J. Therapeutic angiogenesis in ischemic limbs. Circulation, 1998, 97(12): 1108-1110.
2.	Tateishi-Yuyama E, Matsubara H, Murohara T, et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study anda randomised controlled trial. Lancet, 2002, 360(9331): 427-435.
3.	中华医学会医学工程学分会干细胞工程专业委员会, 中华医学会外科学分会血管外科学组. 自体干细胞移植规范化治疗下肢慢性缺血性疾病的专家共识. 中华细胞与干细胞杂志 (电子版), 2012, 2(1): 1-4.
4.	Dong Z, Pan T, Fang Y, et al. Purified CD34⁺ cells versus peripheral blood mononuclear cells in the treatment of angiitis-induced no-option critical limb ischaemia: 12-month results of a prospective randomised single-blinded non-inferiority trial. EBioMedicine, 2018, 35: 46-57.
5.	Fang Y, Wei Z, Chen B, et al. A five-year study of the efficacy of purified CD34⁺ cell therapy for angiitis-induced no-option critical limb ischemia. Stem Cells Transl Med, 2018, 7(8): 583-590.
6.	Martin-Rufino JD, Lozano FS, Redondo AM, et al. Sequential intravenous allogeneic mesenchymal stromal cells as a potential treatment for thromboangiitis obliterans (Buerger’s disease). Stem Cell Res Ther, 2018, 9(1): 150.
7.	Ra JC, Jeong EC, Kang SK, et al. A prospective, nonrandomized, no placebo-controlled, phase Ⅰ/Ⅱ clinical trial assessing the safety and efficacy of intramuscular injection of autologous adipose tissue-derived mesenchymal stem cells in patients with severe Buerger’s disease. Cell Med, 2016, 9(3): 87-102.
8.	Xie B, Luo H, Zhang Y, et al. Autologous stem cell therapy in critical limb ischemia: a meta-analysis of randomized controlled trials. Stem Cells Int, 2018, 2018: 7528464.
9.	Wan J, Yang Y, Ma ZH, et al. Autologous peripheral blood stem cell transplantation to treat thromboangiitis obliterans: preliminary results. Eur Rev Med Pharmacol Sci, 2016, 20(3): 509-513.
10.	于靖宜, 李尚珠, 吴立华, 等. 自体外周血单个核细胞治疗血栓闭塞性脉管炎重度下肢缺血的初步疗效评价. 中国实验血液学杂志, 2016, 24(3): 892-896.
11.	张涛, 万华辉, 郭雪艳, 等. 自体外周血干细胞治疗早期血栓闭塞性脉管炎的疗效观察. 陕西医学杂志, 2014(4): 431-433.
12.	Guo J, Guo L, Cui S, et al. Autologous bone marrow-derived mononuclear cell therapy in Chinese patients with critical limb ischemia due to thromboangiitis obliterans: 10-year results. Stem Cell Res Ther, 2018, 9(1): 43.
13.	Heo SH, Park YS, Kang ES, et al. Early results of clinical application of autologous whole bone marrow stem cell transplantation for critical limb ischemia with Buerger’s disease. Sci Rep, 2016, 6: 19690.
14.	唐石晶, 郭发才, 汤敬东. 射频消融、干细胞移植及药物灌注治疗血栓闭塞性脉管炎的有效性及安全性. 血管与腔内血管外科杂志, 2019, 5(2): 103-108.
15.	白超, 郭晨明, 罗军. 自体骨髓干细胞移植治疗血栓闭塞性脉管炎: 5 年随访. 中国组织工程研究, 2015(23): 3692-3697.
16.	Baran Ç, Durdu S, Özçınar E, et al. Long-term follow-up of patients with Buerger’s disease after autologous stem cell therapy. Anatol J Cardiol, 2019, 21(3): 155-162.
17.	Parikh PP, Liu ZJ, Velazquez OC. A molecular and clinical review of stem cell therapy in critical limb ischemia. Stem Cells Int, 2017: 3750829.
18.	Clayton ZE, Yuen GS, Sadeghipour S, et al. A comparison of the pro-angiogenic potential of human induced pluripotent stem cell derived endothelial cells and induced endothelial cells in a murine model of peripheral arterial disease. Int J Cardiol, 2017, 234: 81-89.
19.	Kim DH, Ko YG, Ahn CM, et al. Immediate and late outcomes of endovascular therapy for lower extremity arteries in Buerger disease. J Vasc Surg, 2018, 67(6): 1769-1777.
20.	Cooper LT, Tse TS, Mikhail MA, et al. Long-term survival and amputation risk in thromboangiitis obliterans (Buerger’s disease). J Am Coll Cardiol, 2004, 44(12): 2410-2411.
21.	Cacione DG, Macedo CR, Baptista-Silva JC. Pharmacological treatment for Buerger’s disease. Cochrane Database Syst Rev, 2016, 3: CD011033.
22.	Shapouri-Moghaddam A, Saeed Modaghegh MH, Rahimi HR, et al. Molecular mechanisms regulating immune responses in thromboangiitis obliterans: a comprehensive review. Iran J Basic Med Sci, 2019, 22(3): 215-224.
23.	Narváez J, García-Gómez C, Álvarez L, et al. Efficacy of bosentan in patients with refractory thromboangiitis obliterans (Buerger disease): a case series and review of the literature. Medicine (Baltimore), 2016, 95(48): e5511.
24.	Chao TH, Tseng SY, Chen IC, et al. Cilostazol enhances mobilization and proliferation of endothelial progenitor cells and collateral formation by modifying vasculo-angiogenic biomarkers in peripheral arterial disease. Int J Cardiol, 2014, 172(2): e371-e374.
25.	Hemsinli D, Altun G, Kaplan ST, et al. Hyperbaric oxygen treatment in thromboangiitis obliterans: a retrospective clinical audit. Diving Hyperb Med, 2018, 48(1): 31-35.
26.	谷涌泉, 佟铸, 郭连瑞. 干细胞移植治疗下肢重度缺血. 中华普通外科学文献 (电子版), 2015, 9(1): 8-10.
27.	杜俊文, 吴韬, 张坤, 等. 脐带间充质干细胞联合骨髓干细胞治疗下肢缺血. 中国组织工程研究, 2017, 21(1): 82-86.
28.	周慧敏, 刘璠, 杨爱格, 等. 脐带血单个核细胞移植治疗对 2 型糖尿病下肢血管病变患者血清 VEGF 和 bFGF 的影响. 广东医学, 2015(19): 3021-3023.
29.	Hopman RK, DiPersio JF. Advances in stem cell mobilization. Blood Rev, 2014, 28(1): 31-40.
30.	Yang SS, Kim NR, Park KB, et al. A phase Ⅰ study of human cord blood-derived mesenchymal stem cell therapy in patients with peripheral arterial occlusive disease. Int J Stem Cells, 2013, 6(1): 37-44.
31.	刘璠, 周慧敏, 杨爱格, 等. 不同来源单个核细胞移植对 2 型糖尿病下肢血管病变的疗效比较. 中华细胞与干细胞杂志 (电子版), 2016, 6(6): 351-355.
32.	Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
33.	中国医药生物技术协会皮肤软组织修复与重建技术分会. 脂肪组织来源的干细胞提取、制备及储存质量管理专家共识. 解放军医学杂志, 2018, 43(10): 811-815.
34.	Rathjen PD, Lake J, Whyatt LM, et al. Properties and uses of embryonic stem cells: prospects for application to human biology and gene therapy. Reprod Fertil Dev, 1998, 10(1): 31-47.
35.	孙英伦, 马振桓, 杨镛, 等. 对血栓闭塞性脉管炎患者截肢平面的研究. 中国现代医学杂志, 2017, 27(15): 53-57.
36.	Aicher A, Heeschen C, Sasaki K, et al. Low-energy shock wave for enhancing recruitment of endothelial progenitor cells: a new modality to increase efficacy of cell therapy in chronic hind limb ischemia. Circulation, 2006, 114(25): 2823-2830.
37.	袁大江, 彭吾训, 张飞, 等. 低浓度过氧化氢预处理增强骨髓间充质干细胞抗氧化应激损伤的能力. 中国组织工程研究, 2019, 23(13): 1982-1988.
38.	王倩, 刘羿, 张雨, 等. 低氧条件下人脂肪间充质干细胞分泌多种细胞因子的水平. 中国组织工程研究, 2019, 23(29): 4681-4687.
39.	Nowicki M, Wierzbowska A, Małachowski R, et al. VEGF, ANGPT1, ANGPT2, and MMP-9 expression in the autologous hematopoietic stem cell transplantation and its impact on the time to engraftment. Ann Hematol, 2017, 96(12): 2103-2112.
40.	Hsu MN, Chang YH, Truong VA, et al. CRISPR technologies for stem cell engineering and regenerative medicine. Biotechnol Adv, 2019, 37(8): 107447.
41.	闫波, 苏少飞, 田玉峰, 等. 自体骨髓干细胞移植治疗严重下肢缺血性疾病疗效的影响因素分析. 中国血管外科杂志 (电子版), 2016, 8(2): 146-149.
42.	Jeon YJ, Kim J, Cho JH, et al. Comparative analysis of human mesenchymal stem cells derived from bone marrow, placenta, and adipose tissue as sources of cell therapy. J Cell Biochem, 2016, 117(5): 1112-1125.
43.	Chandra P, Lee SJ. Synthetic extracellular microenvironment for modulating stem cell behaviors. Biomark Insights, 2015, 10(Suppl 1): 105-116.
44.	Jiang YC, Wang XF, Xu YY, et al. Polycaprolactone nanofibers containing vascular endothelial growth factor-encapsulated gelatin particles enhance mesenchymal stem cell differentiation and angiogenesis of endothelial cells. Biomacromolecules, 2018, 19(9): 3747-3753.
45.	Sun L, Wu L, Qiao Z, et al. Analysis of possible factors relating to prognosis in autologous peripheral blood mononuclear cell transplantation for critical limb ischemia. Cytotherapy, 2014, 16(8): 1110-1116.
46.	Aoyama N, Nishinari M, Ohtani S, et al. Clinical features and predictors of patients with critical limb ischemia who responded to autologous mononuclear cell transplantation for therapeutic angiogenesis. Heart Vessels, 2017, 32(9): 1099-1108.
47.	Dash NR, Dash SN, Routray P, et al. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived mesenchymal stem cells. Rejuvenation Res, 2009, 12(5): 359-366.

1. Folkman J. Therapeutic angiogenesis in ischemic limbs. Circulation, 1998, 97(12): 1108-1110.
2. Tateishi-Yuyama E, Matsubara H, Murohara T, et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study anda randomised controlled trial. Lancet, 2002, 360(9331): 427-435.
3. 中华医学会医学工程学分会干细胞工程专业委员会, 中华医学会外科学分会血管外科学组. 自体干细胞移植规范化治疗下肢慢性缺血性疾病的专家共识. 中华细胞与干细胞杂志 (电子版), 2012, 2(1): 1-4.
4. Dong Z, Pan T, Fang Y, et al. Purified CD34⁺ cells versus peripheral blood mononuclear cells in the treatment of angiitis-induced no-option critical limb ischaemia: 12-month results of a prospective randomised single-blinded non-inferiority trial. EBioMedicine, 2018, 35: 46-57.
5. Fang Y, Wei Z, Chen B, et al. A five-year study of the efficacy of purified CD34⁺ cell therapy for angiitis-induced no-option critical limb ischemia. Stem Cells Transl Med, 2018, 7(8): 583-590.
6. Martin-Rufino JD, Lozano FS, Redondo AM, et al. Sequential intravenous allogeneic mesenchymal stromal cells as a potential treatment for thromboangiitis obliterans (Buerger’s disease). Stem Cell Res Ther, 2018, 9(1): 150.
7. Ra JC, Jeong EC, Kang SK, et al. A prospective, nonrandomized, no placebo-controlled, phase Ⅰ/Ⅱ clinical trial assessing the safety and efficacy of intramuscular injection of autologous adipose tissue-derived mesenchymal stem cells in patients with severe Buerger’s disease. Cell Med, 2016, 9(3): 87-102.
8. Xie B, Luo H, Zhang Y, et al. Autologous stem cell therapy in critical limb ischemia: a meta-analysis of randomized controlled trials. Stem Cells Int, 2018, 2018: 7528464.
9. Wan J, Yang Y, Ma ZH, et al. Autologous peripheral blood stem cell transplantation to treat thromboangiitis obliterans: preliminary results. Eur Rev Med Pharmacol Sci, 2016, 20(3): 509-513.
10. 于靖宜, 李尚珠, 吴立华, 等. 自体外周血单个核细胞治疗血栓闭塞性脉管炎重度下肢缺血的初步疗效评价. 中国实验血液学杂志, 2016, 24(3): 892-896.
11. 张涛, 万华辉, 郭雪艳, 等. 自体外周血干细胞治疗早期血栓闭塞性脉管炎的疗效观察. 陕西医学杂志, 2014(4): 431-433.
12. Guo J, Guo L, Cui S, et al. Autologous bone marrow-derived mononuclear cell therapy in Chinese patients with critical limb ischemia due to thromboangiitis obliterans: 10-year results. Stem Cell Res Ther, 2018, 9(1): 43.
13. Heo SH, Park YS, Kang ES, et al. Early results of clinical application of autologous whole bone marrow stem cell transplantation for critical limb ischemia with Buerger’s disease. Sci Rep, 2016, 6: 19690.
14. 唐石晶, 郭发才, 汤敬东. 射频消融、干细胞移植及药物灌注治疗血栓闭塞性脉管炎的有效性及安全性. 血管与腔内血管外科杂志, 2019, 5(2): 103-108.
15. 白超, 郭晨明, 罗军. 自体骨髓干细胞移植治疗血栓闭塞性脉管炎: 5 年随访. 中国组织工程研究, 2015(23): 3692-3697.
16. Baran Ç, Durdu S, Özçınar E, et al. Long-term follow-up of patients with Buerger’s disease after autologous stem cell therapy. Anatol J Cardiol, 2019, 21(3): 155-162.
17. Parikh PP, Liu ZJ, Velazquez OC. A molecular and clinical review of stem cell therapy in critical limb ischemia. Stem Cells Int, 2017: 3750829.
18. Clayton ZE, Yuen GS, Sadeghipour S, et al. A comparison of the pro-angiogenic potential of human induced pluripotent stem cell derived endothelial cells and induced endothelial cells in a murine model of peripheral arterial disease. Int J Cardiol, 2017, 234: 81-89.
19. Kim DH, Ko YG, Ahn CM, et al. Immediate and late outcomes of endovascular therapy for lower extremity arteries in Buerger disease. J Vasc Surg, 2018, 67(6): 1769-1777.
20. Cooper LT, Tse TS, Mikhail MA, et al. Long-term survival and amputation risk in thromboangiitis obliterans (Buerger’s disease). J Am Coll Cardiol, 2004, 44(12): 2410-2411.
21. Cacione DG, Macedo CR, Baptista-Silva JC. Pharmacological treatment for Buerger’s disease. Cochrane Database Syst Rev, 2016, 3: CD011033.
22. Shapouri-Moghaddam A, Saeed Modaghegh MH, Rahimi HR, et al. Molecular mechanisms regulating immune responses in thromboangiitis obliterans: a comprehensive review. Iran J Basic Med Sci, 2019, 22(3): 215-224.
23. Narváez J, García-Gómez C, Álvarez L, et al. Efficacy of bosentan in patients with refractory thromboangiitis obliterans (Buerger disease): a case series and review of the literature. Medicine (Baltimore), 2016, 95(48): e5511.
24. Chao TH, Tseng SY, Chen IC, et al. Cilostazol enhances mobilization and proliferation of endothelial progenitor cells and collateral formation by modifying vasculo-angiogenic biomarkers in peripheral arterial disease. Int J Cardiol, 2014, 172(2): e371-e374.
25. Hemsinli D, Altun G, Kaplan ST, et al. Hyperbaric oxygen treatment in thromboangiitis obliterans: a retrospective clinical audit. Diving Hyperb Med, 2018, 48(1): 31-35.
26. 谷涌泉, 佟铸, 郭连瑞. 干细胞移植治疗下肢重度缺血. 中华普通外科学文献 (电子版), 2015, 9(1): 8-10.
27. 杜俊文, 吴韬, 张坤, 等. 脐带间充质干细胞联合骨髓干细胞治疗下肢缺血. 中国组织工程研究, 2017, 21(1): 82-86.
28. 周慧敏, 刘璠, 杨爱格, 等. 脐带血单个核细胞移植治疗对 2 型糖尿病下肢血管病变患者血清 VEGF 和 bFGF 的影响. 广东医学, 2015(19): 3021-3023.
29. Hopman RK, DiPersio JF. Advances in stem cell mobilization. Blood Rev, 2014, 28(1): 31-40.
30. Yang SS, Kim NR, Park KB, et al. A phase Ⅰ study of human cord blood-derived mesenchymal stem cell therapy in patients with peripheral arterial occlusive disease. Int J Stem Cells, 2013, 6(1): 37-44.
31. 刘璠, 周慧敏, 杨爱格, 等. 不同来源单个核细胞移植对 2 型糖尿病下肢血管病变的疗效比较. 中华细胞与干细胞杂志 (电子版), 2016, 6(6): 351-355.
32. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
33. 中国医药生物技术协会皮肤软组织修复与重建技术分会. 脂肪组织来源的干细胞提取、制备及储存质量管理专家共识. 解放军医学杂志, 2018, 43(10): 811-815.
34. Rathjen PD, Lake J, Whyatt LM, et al. Properties and uses of embryonic stem cells: prospects for application to human biology and gene therapy. Reprod Fertil Dev, 1998, 10(1): 31-47.
35. 孙英伦, 马振桓, 杨镛, 等. 对血栓闭塞性脉管炎患者截肢平面的研究. 中国现代医学杂志, 2017, 27(15): 53-57.
36. Aicher A, Heeschen C, Sasaki K, et al. Low-energy shock wave for enhancing recruitment of endothelial progenitor cells: a new modality to increase efficacy of cell therapy in chronic hind limb ischemia. Circulation, 2006, 114(25): 2823-2830.
37. 袁大江, 彭吾训, 张飞, 等. 低浓度过氧化氢预处理增强骨髓间充质干细胞抗氧化应激损伤的能力. 中国组织工程研究, 2019, 23(13): 1982-1988.
38. 王倩, 刘羿, 张雨, 等. 低氧条件下人脂肪间充质干细胞分泌多种细胞因子的水平. 中国组织工程研究, 2019, 23(29): 4681-4687.
39. Nowicki M, Wierzbowska A, Małachowski R, et al. VEGF, ANGPT1, ANGPT2, and MMP-9 expression in the autologous hematopoietic stem cell transplantation and its impact on the time to engraftment. Ann Hematol, 2017, 96(12): 2103-2112.
40. Hsu MN, Chang YH, Truong VA, et al. CRISPR technologies for stem cell engineering and regenerative medicine. Biotechnol Adv, 2019, 37(8): 107447.
41. 闫波, 苏少飞, 田玉峰, 等. 自体骨髓干细胞移植治疗严重下肢缺血性疾病疗效的影响因素分析. 中国血管外科杂志 (电子版), 2016, 8(2): 146-149.
42. Jeon YJ, Kim J, Cho JH, et al. Comparative analysis of human mesenchymal stem cells derived from bone marrow, placenta, and adipose tissue as sources of cell therapy. J Cell Biochem, 2016, 117(5): 1112-1125.
43. Chandra P, Lee SJ. Synthetic extracellular microenvironment for modulating stem cell behaviors. Biomark Insights, 2015, 10(Suppl 1): 105-116.
44. Jiang YC, Wang XF, Xu YY, et al. Polycaprolactone nanofibers containing vascular endothelial growth factor-encapsulated gelatin particles enhance mesenchymal stem cell differentiation and angiogenesis of endothelial cells. Biomacromolecules, 2018, 19(9): 3747-3753.
45. Sun L, Wu L, Qiao Z, et al. Analysis of possible factors relating to prognosis in autologous peripheral blood mononuclear cell transplantation for critical limb ischemia. Cytotherapy, 2014, 16(8): 1110-1116.
46. Aoyama N, Nishinari M, Ohtani S, et al. Clinical features and predictors of patients with critical limb ischemia who responded to autologous mononuclear cell transplantation for therapeutic angiogenesis. Heart Vessels, 2017, 32(9): 1099-1108.
47. Dash NR, Dash SN, Routray P, et al. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived mesenchymal stem cells. Rejuvenation Res, 2009, 12(5): 359-366.

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