Mechanisms of extracorporeal shock wave therapy in promoting healing of diabetic foot ulcer_West China Medical Journal

Authors：

LIANG Likan ¹ , LIU Xiaogang ² , Huang Jianjun ² , GONG Fei ¹ ,  ZHANG Jingchun ²

1. Graduate School, Shanxi University of Chinese Medicine, Taiyuan, Shanxi 030000, P. R. China;
2. Department of Orthopaedics, Shanxi Provincial Hospital of Traditional Chinese Medicine, Taiyuan, Shanxi 030000, P. R. China;

Corresponding?author：

ZHANG Jingchun, Email: zhjch1461@163.com

Keywords：

Diabetic foot ulcer; Extracorporeal shock wave therapy; Mechanism

DOI：

10.7507/1002-0179.201912103

Video：

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Diabetic foot ulcer is one of the severe chronic complications that lead to disability and death of diabetic patients. In order to solve this problem, adjuvant therapy studies of diabetic foot ulcers have increased in recent years. Extracorporeal shock wave therapy is a novel adjuvant therapy that has been approved by the US Food and Drug Administration for diabetic foot ulcers wounds. In this paper, the mechanisms of extracorporeal shock wave therapy for diabetic foot ulcers are described, including wound angiogenesis, wound tissue blood perfusion, nerve regeneration, granulation tissue proliferation, inflammatory response, anti-infection, migration and differentiation of mesenchymal stem cells and endothelial progenitor cells. This study aims to provide a theoretical basis for the clinical application of extracorporeal shock wave therapy in clinical treatment of diabetic foot ulcers.

Citation： LIANG Likan, LIU Xiaogang, Huang Jianjun, GONG Fei, ZHANG Jingchun. Mechanisms of extracorporeal shock wave therapy in promoting healing of diabetic foot ulcer. West China Medical Journal, 2020, 35(3): 363-366. doi: 10.7507/1002-0179.201912103 Copy

1.	中華預防醫學會組織感染與損傷預防與控制專業委員會, 中華醫學會腸外腸內營養學分會, 中國中西醫結合學會周圍血管疾病專業委員會糖尿病足學組. 糖尿病足病醫學營養治療指南. 中國組織工程研究, 2019, 23(35): 5682-5689.
2.	中國醫療保健國際交流促進會糖尿病足病分會, 國際血管聯盟中國分部糖尿病足病專家委員會. 中國糖尿病足診治指南. 中國臨床醫生雜志, 2020, 48(1): 19-27.
3.	US Food and Drug Administration. FDA permits marketing of device to treat diabetic foot ulcers. (2017-12-28)[2020-01-17]. https://www.fda.gov/news-events/press-announcements/fda-permits-marketing-device-treat-diabetic-foot-ulcers.
4.	中華醫學會糖尿病學分會, 中華醫學會感染病學分會, 中華醫學會組織修復與再生分會. 中國糖尿病足防治指南(2019版)(Ⅰ). 中華糖尿病雜志, 2019, 11(2): 92-108.
5.	宋薇, 解嘉慧, 肖宇. 糖尿病足潰瘍的危險因素與治療研究進展. 山東醫藥, 2019, 59(4): 88-91.
6.	van Netten JJ, Price PE, Lavery LA, et al. Prevention of foot ulcers in the at-risk patient with diabetes: a systematic review. Diabetes Metab Res Rev, 2016, 32(Suppl 1): 84-98.
7.	中國研究型醫院學會沖擊波醫學專業委員會, 國際沖擊波醫學學會中國部. 骨肌疾病體外沖擊波療法中國專家共識(第2版). 中國醫學前沿雜志(電子版), 2017, 9(2): 25-33.
8.	Haupt G, Chvapil M. Effect of shock waves on the healing of partial-thickness wounds in piglets. J Surg Res, 1990, 49(1): 45-48.
9.	Chamberlain GA, Colborne GR. A review of the cellular and molecular effects of extracorporeal shockwave therapy. Vet Comp Orthop Traumatol, 2016, 29(2): 99-107.
10.	Ha CH1, Kim S, Chung J, et al. Extracorporeal shock wave stimulates expression of the angiogenic genes via mechanosensory complex in endothelial cells: mimetic effect of fluid shear stress in endothelial cells. Int J Cardiol, 2013, 168(4): 4168-4177.
11.	燕曉宇, 楊光, 成亮, 等. 低能量體外震波對糖尿病慢性創面模型血管新生和血管內皮細胞生長因子表達的影響. 中國組織工程研究, 2012, 16(15): 2745-2749.
12.	Birgin E, Gebhardt C, Hetjens S, et al. Extracorporal shock wave therapy enhances receptor for advanced glycated end-product-dependent flap survival and angiogenesis. Ann Plast Surg, 2018, 80(4): 424-431.
13.	Kisch T, Sorg H, Forstmeier V, et al. Remote effects of extracorporeal shock wave therapy on cutaneous microcirculation. J Tissue Viability, 2015, 24(4): 140-145.
14.	Yang JP, Lee YN, Son JW, et al. The impact of extracorporeal shock wave therapy on microcirculation in diabetic feet: a pilot study. Adv Skin Wound Care, 2019, 32(12): 563-567.
15.	Amin N, Doupis J. Diabetic foot disease: from the evaluation of the “foot at risk” to the novel diabetic ulcer treatment modalities. World J Diabetes, 2016, 7(7): 153-164.
16.	Hausner T, Pajer K, Halat G, et al. Improved rate of peripheral nerve regeneration induced by extracorporeal shock wave treatment in the rat. Exp Neurol, 2012, 236(2): 363-370.
17.	Murata R, Ohtori S, Ochiai N, et al. Extracorporeal shockwaves induce the expression of ATF3 and GAP-43 in rat dorsal root ganglion neurons. Auton Neurosci, 2006, 128(1/2): 96-100.
18.	田曉紅, 柏樹令, 田偉, 等. 表皮干細胞在糖尿病創面愈合過程中的動態變化. 中國修復重建外科雜志, 2007, 21(7): 693-697.
19.	Aschermann I, Noor S, Venturelli S, et al. Extracorporal shock waves activate migration, proliferation and inflammatory pathways in fibroblasts and keratinocytes, and improve wound healing in an open-label, single-arm study in patients with therapy-refractory chronic leg ulcers. Cell Physiol Biochem, 2017, 41(2): 890-906.
20.	Qi M, Zhou Q, Zeng W, et al. Growth factors in the pathogenesis of diabetic foot ulcers. Front Biosci (Landmark Ed), 2018, 23: 310-317.
21.	燕曉宇, 楊光, 成亮, 等. 體外震波治療對糖尿病大鼠慢性創面愈合及組織學影響. 中國修復重建外科雜志, 2012, 26(8): 961-967.
22.	Mirza RE, Fang MM, Weinheimer-Haus EM, et al. Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice. Diabetes, 2014, 63(3): 1103-1114.
23.	Mirza RE, Fang MM, Novak ML, et al. Macrophage PPARγ and impaired wound healing in type 2 diabetes. J Pathol, 2015, 236(4): 433-444.
24.	Davis TA, Stojadinovic A, Anam K, et al. Extracorporeal shock wave therapy suppresses the early proinflammatory immune response to a severe cutaneous burn injury. Int Wound J, 2009, 6(1): 11-21.
25.	Jeppesen SM, Yderstraede KB, Rasmussen BS, et al. Extracorporeal shockwave therapy in the treatment of chronic diabetic foot ulcers: a prospective randomised trial. J Wound Care, 2016, 25(11): 641-649.
26.	von Eiff C, Overbeck J, Haupt G, et al. Bactericidal effect of extracorporeal shock waves on Staphylococcus aureus . J Med Microbiol, 2000, 49(8): 709-712.
27.	Qi X, Zhao Y, Zhang J, et al. Increased effects of extracorporeal shock waves combined with gentamicin against Staphylococcus aureus biofilms in vitro and in vivo. Ultrasound Med Biol, 2016, 42(9): 2245-2252.
28.	Lokhandwalla M, McAteer JA, Williams JC Jr, et al. Mechanical haemolysis in shock wave lithotripsy (SWL): Ⅱ. In vitro cell lysis due to shear. Phys Med Biol, 2001, 46(4): 1245-1264.
29.	Gerdesmeyer L, Maier M, Haake M, et al. Physical-technical principles of extracorporeal shockwave therapy (ESWT). Orthopade, 2002, 31(7): 610-617.
30.	Heyboer M 3rd. Hyperbaric oxygen therapy side effects - where do we stand?. J Am Coll Clin Wound Spec, 2016, 8(1/2/3): 2-3.
31.	Guo J, Dardik A, Fang K, et al. Meta-analysis on the treatment of diabetic foot ulcers with autologous stem cells. Stem Cell Res Ther, 2017, 8(1): 228.
32.	Shu X, Shu S, Tang S, et al. Efficiency of stem cell based therapy in the treatment of diabetic foot ulcer: a meta-analysis. Endocr J, 2018, 65(4): 403-413.
33.	Jin P, Zhang X, Wu Y, et al. Streptozotocin-induced diabetic rat-derived bone marrow mesenchymal stem cells have impaired abilities in proliferation, paracrine, antiapoptosis, and myogenic differentiation. Transplant Proc, 2010, 42(7): 2745-2752.
34.	黃鐘煉, 羅紹偉, 林海明, 等. SDF-1/CXCR4介導體外沖擊波促進大鼠骨髓間充質干細胞的黏附、遷移作用. 頸腰痛雜志, 2019, 40(6): 721-726.
35.	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.

1. 中華預防醫學會組織感染與損傷預防與控制專業委員會, 中華醫學會腸外腸內營養學分會, 中國中西醫結合學會周圍血管疾病專業委員會糖尿病足學組. 糖尿病足病醫學營養治療指南. 中國組織工程研究, 2019, 23(35): 5682-5689.
2. 中國醫療保健國際交流促進會糖尿病足病分會, 國際血管聯盟中國分部糖尿病足病專家委員會. 中國糖尿病足診治指南. 中國臨床醫生雜志, 2020, 48(1): 19-27.
3. US Food and Drug Administration. FDA permits marketing of device to treat diabetic foot ulcers. (2017-12-28)[2020-01-17]. https://www.fda.gov/news-events/press-announcements/fda-permits-marketing-device-treat-diabetic-foot-ulcers.
4. 中華醫學會糖尿病學分會, 中華醫學會感染病學分會, 中華醫學會組織修復與再生分會. 中國糖尿病足防治指南(2019版)(Ⅰ). 中華糖尿病雜志, 2019, 11(2): 92-108.
5. 宋薇, 解嘉慧, 肖宇. 糖尿病足潰瘍的危險因素與治療研究進展. 山東醫藥, 2019, 59(4): 88-91.
6. van Netten JJ, Price PE, Lavery LA, et al. Prevention of foot ulcers in the at-risk patient with diabetes: a systematic review. Diabetes Metab Res Rev, 2016, 32(Suppl 1): 84-98.
7. 中國研究型醫院學會沖擊波醫學專業委員會, 國際沖擊波醫學學會中國部. 骨肌疾病體外沖擊波療法中國專家共識(第2版). 中國醫學前沿雜志(電子版), 2017, 9(2): 25-33.
8. Haupt G, Chvapil M. Effect of shock waves on the healing of partial-thickness wounds in piglets. J Surg Res, 1990, 49(1): 45-48.
9. Chamberlain GA, Colborne GR. A review of the cellular and molecular effects of extracorporeal shockwave therapy. Vet Comp Orthop Traumatol, 2016, 29(2): 99-107.
10. Ha CH1, Kim S, Chung J, et al. Extracorporeal shock wave stimulates expression of the angiogenic genes via mechanosensory complex in endothelial cells: mimetic effect of fluid shear stress in endothelial cells. Int J Cardiol, 2013, 168(4): 4168-4177.
11. 燕曉宇, 楊光, 成亮, 等. 低能量體外震波對糖尿病慢性創面模型血管新生和血管內皮細胞生長因子表達的影響. 中國組織工程研究, 2012, 16(15): 2745-2749.
12. Birgin E, Gebhardt C, Hetjens S, et al. Extracorporal shock wave therapy enhances receptor for advanced glycated end-product-dependent flap survival and angiogenesis. Ann Plast Surg, 2018, 80(4): 424-431.
13. Kisch T, Sorg H, Forstmeier V, et al. Remote effects of extracorporeal shock wave therapy on cutaneous microcirculation. J Tissue Viability, 2015, 24(4): 140-145.
14. Yang JP, Lee YN, Son JW, et al. The impact of extracorporeal shock wave therapy on microcirculation in diabetic feet: a pilot study. Adv Skin Wound Care, 2019, 32(12): 563-567.
15. Amin N, Doupis J. Diabetic foot disease: from the evaluation of the “foot at risk” to the novel diabetic ulcer treatment modalities. World J Diabetes, 2016, 7(7): 153-164.
16. Hausner T, Pajer K, Halat G, et al. Improved rate of peripheral nerve regeneration induced by extracorporeal shock wave treatment in the rat. Exp Neurol, 2012, 236(2): 363-370.
17. Murata R, Ohtori S, Ochiai N, et al. Extracorporeal shockwaves induce the expression of ATF3 and GAP-43 in rat dorsal root ganglion neurons. Auton Neurosci, 2006, 128(1/2): 96-100.
18. 田曉紅, 柏樹令, 田偉, 等. 表皮干細胞在糖尿病創面愈合過程中的動態變化. 中國修復重建外科雜志, 2007, 21(7): 693-697.
19. Aschermann I, Noor S, Venturelli S, et al. Extracorporal shock waves activate migration, proliferation and inflammatory pathways in fibroblasts and keratinocytes, and improve wound healing in an open-label, single-arm study in patients with therapy-refractory chronic leg ulcers. Cell Physiol Biochem, 2017, 41(2): 890-906.
20. Qi M, Zhou Q, Zeng W, et al. Growth factors in the pathogenesis of diabetic foot ulcers. Front Biosci (Landmark Ed), 2018, 23: 310-317.
21. 燕曉宇, 楊光, 成亮, 等. 體外震波治療對糖尿病大鼠慢性創面愈合及組織學影響. 中國修復重建外科雜志, 2012, 26(8): 961-967.
22. Mirza RE, Fang MM, Weinheimer-Haus EM, et al. Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice. Diabetes, 2014, 63(3): 1103-1114.
23. Mirza RE, Fang MM, Novak ML, et al. Macrophage PPARγ and impaired wound healing in type 2 diabetes. J Pathol, 2015, 236(4): 433-444.
24. Davis TA, Stojadinovic A, Anam K, et al. Extracorporeal shock wave therapy suppresses the early proinflammatory immune response to a severe cutaneous burn injury. Int Wound J, 2009, 6(1): 11-21.
25. Jeppesen SM, Yderstraede KB, Rasmussen BS, et al. Extracorporeal shockwave therapy in the treatment of chronic diabetic foot ulcers: a prospective randomised trial. J Wound Care, 2016, 25(11): 641-649.
26. von Eiff C, Overbeck J, Haupt G, et al. Bactericidal effect of extracorporeal shock waves on Staphylococcus aureus . J Med Microbiol, 2000, 49(8): 709-712.
27. Qi X, Zhao Y, Zhang J, et al. Increased effects of extracorporeal shock waves combined with gentamicin against Staphylococcus aureus biofilms in vitro and in vivo. Ultrasound Med Biol, 2016, 42(9): 2245-2252.
28. Lokhandwalla M, McAteer JA, Williams JC Jr, et al. Mechanical haemolysis in shock wave lithotripsy (SWL): Ⅱ. In vitro cell lysis due to shear. Phys Med Biol, 2001, 46(4): 1245-1264.
29. Gerdesmeyer L, Maier M, Haake M, et al. Physical-technical principles of extracorporeal shockwave therapy (ESWT). Orthopade, 2002, 31(7): 610-617.
30. Heyboer M 3rd. Hyperbaric oxygen therapy side effects - where do we stand?. J Am Coll Clin Wound Spec, 2016, 8(1/2/3): 2-3.
31. Guo J, Dardik A, Fang K, et al. Meta-analysis on the treatment of diabetic foot ulcers with autologous stem cells. Stem Cell Res Ther, 2017, 8(1): 228.
32. Shu X, Shu S, Tang S, et al. Efficiency of stem cell based therapy in the treatment of diabetic foot ulcer: a meta-analysis. Endocr J, 2018, 65(4): 403-413.
33. Jin P, Zhang X, Wu Y, et al. Streptozotocin-induced diabetic rat-derived bone marrow mesenchymal stem cells have impaired abilities in proliferation, paracrine, antiapoptosis, and myogenic differentiation. Transplant Proc, 2010, 42(7): 2745-2752.
34. 黃鐘煉, 羅紹偉, 林海明, 等. SDF-1/CXCR4介導體外沖擊波促進大鼠骨髓間充質干細胞的黏附、遷移作用. 頸腰痛雜志, 2019, 40(6): 721-726.
35. 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.

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Mechanisms of extracorporeal shock wave therapy in promoting healing of diabetic foot ulcer

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