Noncontact, low-frequency ultrasound therapy enhances neovascularization and wound healing in diabetic mice

Plastic and Reconstructive Surgery

Volumn 134, Issue 3, 2014, Pages

  Maan, Zeshaan N ^a   Januszyk, Michael ^a   Rennert, Robert C ^a   Duscher, Dominik ^a   Rodrigues, Melanie ^a   Fujiwara, Toshihiro ^a   Ho, Natalie ^a   Whitmore, Arnetha ^a   Hu, Michael S ^a   Longaker, Michael T ^a   Gurtner, Geoffrey C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

ANGIOGENESIS; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; EVALUATION STUDY; EXPERIMENTAL DIABETES MELLITUS; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; TREATMENT OUTCOME; ULTRASOUND THERAPY; WOUND HEALING;

ANIMALS; BIOLOGICAL MARKERS; DIABETES MELLITUS, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN; TREATMENT OUTCOME; ULTRASONIC THERAPY; WOUND HEALING;

EID: 84907314851     PISSN: 00321052     EISSN: None     Source Type: Journal    
DOI: 10.1097/PRS.0000000000000467     Document Type: Article

References (48)

1. Sen CK, Gordillo GM, Roy S, et al. Human skin wounds: A major and snowballing threat to public health and the economy. Wound Repair Regen. 2009;17:763-771.
2. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest. 2007;117: 1219-1222.
3. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature 2008;453:314-321.
4. American Diabetes Association. Economic costs of diabetes in the U.S. In 2007. Diabetes Care 2008;31:596-615.
5. American Diabetes Association. Economic costs of diabetes in the U.S. in 2012. Diabetes Care 2013;36:1033-1046.
6. Johannsen F, Gam AN, Karlsmark T. Ultrasound therapy in chronic leg ulceration: A meta-analysis. Wound Repair Regen. 1998;6:121-126.
7. Houghton PE, Campbell KE. Choosing an adjunctive therapy for the treatment of chronic wounds. Ostomy Wound Manage. 1999;45:43-52; quiz 53.
8. Seth AK, Nguyen KT, Geringer MR, et al. Noncontact, low-frequency ultrasound as an effective therapy against Pseudomonas aeruginosa-infected biofilm wounds. Wound Repair Regen. 2013;21:266-274.
9. Young SR, Dyson M. The effect of therapeutic ultrasound on angiogenesis. Ultrasound Med Biol. 1990;16:261-269.
10. Maxwell L, Collecutt T, Gledhill M, Sharma S, Edgar S, Gavin JB. The augmentation of leucocyte adhesion to endothelium by therapeutic ultrasound. Ultrasound Med Biol. 1994;20:383-390.
11. Young SR, Dyson M. Macrophage responsiveness to therapeutic ultrasound. Ultrasound Med Biol. 1990;16:809-816.
12. Lu C, Saless N, Hu D, et al. Mechanical stability affects angiogenesis during early fracture healing. J Orthop Trauma 2011;25:494-499.
13. Rustad KC, Wong VW, Gurtner GC. The role of focal adhesion complexes in fibroblast mechanotransduction during scar formation. Differentiation 2013;86:87-91.
14. Wong VW, Longaker MT, Gurtner GC. Soft tissue mechanotransduction in wound healing and fibrosis. Semin Cell Dev Biol. 2012;23:981-986.
15. Wong VW, Paterno J, Sorkin M, et al. Mechanical force prolongs acute inflammation via T-cell-dependent pathways during scar formation. FASEB J. 2011;25:4498-4510.
16. Zhang H, Landmann F, Zahreddine H, Rodriguez D, Koch M, Labouesse M. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 2011;471:99-103.
17. Lancerotto L, Bayer LR, Orgill DP. Mechanisms of action of microdeformational wound therapy. Semin Cell Dev Biol. 2012;23:987-992.
18. Ennis WJ, Foremann P, Mozen N, Massey J, Conner-Kerr T, Meneses P. Ultrasound therapy for recalcitrant diabetic foot ulcers: Results of a randomized, double-blind, controlled, multicenter study. Ostomy Wound Manage. 2005;51:24-39.
19. Wollina U, Heinig B, Naumann G, Scheibe A, Schmidt WD, Neugebauer R. Effects of low-frequency ultrasound on microcirculation in venous leg ulcers. Indian J Dermatol. 2011;56:174-179.
20. Lai J, Pittelkow MR. Physiological effects of ultrasound mist on fibroblasts. Int J Dermatol. 2007;46:587-593.
21. Galiano RD, Michaels J V, Dobryansky M, Levine JP, Gurtner GC. Quantitative and reproducible murine model of excisional wound healing. Wound Repair Regen. 2004;12:485-492.
22. Keltie K, Reay CA, Bousfield DR, et al. Characterization of the ultrasound beam produced by the MIST therapy, wound healing system. Ultrasound Med Biol. 2013;39:1233-1240.
23. Nauta AC, Grova M, Montoro DT, et al. Evidence that mast cells are not required for healing of splinted cutaneous excisional wounds in mice. PLoS One 2013;8:e59167.
24. Lerman OZ, Galiano RD, Armour M, Levine JP, Gurtner GC. Cellular dysfunction in the diabetic fibroblast: Impairment in migration, vascular endothelial growth factor production, and response to hypoxia. Am J Pathol. 2003;162:303-312.
25. Michaels J V, Churgin SS, Blechman KM, et al. db/db mice exhibit severe wound-healing impairments compared with other murine diabetic strains in a silicone-splinted excisional wound model. Wound Repair Regen. 2007;15:665-670.
26. Callaghan MJ, Chang EI, Seiser N, et al. Pulsed electromagnetic fields accelerate normal and diabetic wound healing by increasing endogenous FGF-2 release. Plast Reconstr Surg. 2008;121:130-141.
27. Thangarajah H, Yao D, Chang EI, et al. The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues. Proc Natl Acad Sci USA 2009;106:13505-13510.
28. Connolly DT. Vascular permeability factor: A unique regulator of blood vessel function. J Cell Biochem. 1991;47:219-223.
29. Gallagher KA, Liu ZJ, Xiao M, et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. J Clin Invest. 2007;117:1249-1259.
30. Franks PJ, Morgan PA. Health-related quality of life with chronic leg ulceration. Expert Rev Pharmacoecon Outcomes Res. 2003;3:611-622.
31. Gorecki C, Brown JM, Nelson EA, et al. Impact of pressure ulcers on quality of life in older patients: A systematic review. J Am Geriatr Soc. 2009;57:1175-1183.
32. Frykberg RG. Epidemiology of the diabetic foot: Ulcerations and amputations. Adv Wound Care 1999;12:139-141.
33. Wieman TJ, Smiell JM, Su Y. Efficacy and safety of a topical gel formulation of recombinant human plateletderived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers: A phase III randomized placebo-controlled double-blind study. Diabetes Care 1998;21:822-827.
34. Hamou C, Callaghan MJ, Thangarajah H, et al. Mesenchymal stem cells can participate in ischemic neovascularization. Plast Reconstr Surg. 2009;123(2 Suppl):45S-55S.
35. Kavros SJ, Liedl DA, Boon AJ, Miller JL, Hobbs JA, Andrews KL. Expedited wound healing with noncontact, low-frequency ultrasound therapy in chronic wounds: A retrospective analysis. Adv Skin Wound Care 2008;21:416-423.
36. Ramundo J, Gray M. Is ultrasonic mist therapy effective for debriding chronic wounds? J Wound Ostomy Continence Nurs. 2008;35:579-583.
37. Waldrop K, Serfass A. Clinical effectiveness of noncontact, low-frequency, nonthermal ultrasound in burn care. Ostomy Wound Manage. 2008;54:66-69.
38. Ennis WJ, Foremann P, Mozen N, Massey J, Conner-Kerr T, Meneses P. Ultrasound therapy for recalcitrant diabetic foot ulcers: Results of a randomized, double-blind, controlled, multicenter study. Ostomy Wound Manage. 2005;51:24-39.
39. Ennis WJ, Valdes W, Gainer M, Meneses P. Evaluation of clinical effectiveness of MIST ultrasound therapy for the healing of chronic wounds. Adv Skin Wound Care 2006;19:437-446.
40. Kavros SJ, Miller JL, Hanna SW. Treatment of ischemic wounds with noncontact, low-frequency ultrasound: The Mayo clinic experience, 2004-2006. Adv Skin Wound Care 2007;20:221-226.
41. Isaac AL, Armstrong DG. Negative pressure wound therapy and other new therapies for diabetic foot ulceration: The current state of play. Med Clin North Am. 2013;97:899-909.
42. Upton D, Stephens D, Andrews A. Patients' experiences of negative pressure wound therapy for the treatment of wounds: A review. J Wound Care 2013;22:34-39.
43. Clarke DN, Al Ahmad A, Lee B, et al. Perlecan Domain V induces VEGf secretion in brain endothelial cells through integrin alpha5beta1 and ERK-dependent signaling pathways. PLoS One 2012;7:e45257.
44. Treins C, Giorgetti-Peraldi S, Murdaca J, Van Obberghen E. Regulation of vascular endothelial growth factor expression by advanced glycation end products. J Biol Chem. 2001;276:43836-43841.
45. Wong VW, Rustad KC, Akaishi S, et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med. 2012;18:148-152.
46. Mortimer AJ, Dyson M. The effect of therapeutic ultrasound on calcium uptake in fibroblasts. Ultrasound Med Biol. 1988;14:499-506.
47. Reher P, Doan N, Bradnock B, Meghji S, Harris M. Effect of ultrasound on the production of IL-8, basic FGF and VEGF. Cytokine 1999;11:416-423.
48. Doan N, Reher P, Meghji S, Harris M. In vitro effects of therapeutic ultrasound on cell proliferation, protein synthesis, and cytokine production by human fibroblasts, osteoblasts, and monocytes. J Oral Maxillofac Surg. 1999;57:409-419; discussion 420.