A review of the role of mechanical forces in cutaneous wound healing

Journal of Surgical Research

Volumn 171, Issue 2, 2011, Pages 700-708

  Agha, Riaz ^a,e   Ogawa, Rei ^b   Pietramaggiori, Giorgio ^c   Orgill, Dennis P ^d  

^a CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e QUEEN VICTORIA HOSPITAL   (United Kingdom)

Author keywords

angiogenesis; cutaneous; keloid hypertrophic scarring; micromechanical forces; VAC; wound healing; wound tension

Indexed keywords

GROWTH FACTOR;

CELL PROLIFERATION; CONNECTIVE TISSUE; CUTANEOUS WOUND HEALING; EXPERIMENTAL MODEL; GENE EXPRESSION; HUMAN; KELOID; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKIN; SKIN DEFECT; SKIN SCAR; SOFT TISSUE; SYNTHESIS; TISSUE EXPANSION; TISSUE GROWTH; TISSUE REPAIR; WOUND HEALING;

ANIMALS; HUMANS; KELOID; NEOVASCULARIZATION, PHYSIOLOGIC; SKIN; SKIN PHYSIOLOGICAL PHENOMENA; STRESS, MECHANICAL; WOUND HEALING;

EID: 81155123663     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2011.07.007     Document Type: Review

References (133)

1. On the anatomy and physiology of the skin. III The elasticity of the cutis by Professor K. Langer presented at the meeting of 27th November 1861 Br J Plast Surg 31 1978 185
2. F.H. Silver, L.M. Siperko, and G.P. Seehra Mechanobiology of force transduction in dermal tissue Skin Res Technol 9 2003 3
3. D.M. Raab, T.D. Crenshaw, and D.B. Kimmel A histomorphometric study of cortical bone activity during increased weight-bearing exercise J Bone Miner Res 6 1991 741
4. R. Agha Space exploration: Surgical insights and future perspectives Int J Surg 3 2005 263
5. G.S. Cummings, and L.J. Tillman Remodelling of dense connective tissue in normal adult tissues D.P. Currier, R.M. Nelson, Dynamics of human biologic tissues, contemporary perspectives in rehabilitation 1992 F.A. Davis Philadelphia
6. G.A. Ilizarov The tension-stress effect on the genesis and growth of tissues: Part I. The influence of stability of fixation and soft-tissue preservation Clin Orthop Relat Res 238 1989 249
7. G.A. Ilizarov The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction Clin Orthop Relat Res 239 1989 263
8. R. Agha, and B. Webb A cadaveric investigation into the links between macroscopic and microscopic osteoarthritic changes at the hip Clin Anat 19 2006 115
9. Wolff J. The law of bone remodeling. Maquet P, Furlong R, translators. Berlin: Springer Verlag, 1986 [translation of the German 1892 edition].
10. J. Folkman, and A. Moscon Role of cell shape in growth control Nature 273 1978 345
11. S. Huang, C.S. Chen, and D.E. Ingber Control of cyclin D1, p27 (Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension Mol Biol Cell 9 1998 3179
12. S. Huang, and D.E. Ingber Shape-dependent control of cell growth, differentiation, and apoptosis: Switching between attractors in cell regulatory networks Exp Cell Res 261 2000 913
13. J. Zhang, W. Li, and M.A. Sanders Regulation of the intestinal epithelial response to cyclic strain by extracellular matrix proteins FASEB J 17 2003 926
14. B. Hinz, G. Celetta, and J.J. Tomasek Alpha-smooth muscle actin expression upregulates fibroblast contractile activity Mol Biol Cell 12 2001 2730
15. J.R. Couchman, M.R. Austria, and A. Woods Fibronectin-cell interactions J Invest Dermatol 94 6 Suppl 1990 7S
16. T.W. Gilbert, A.M. Stewart-Akers, and J. Sydeski Gene expression by fibroblasts seeded on small intestinal submucosa and subjected to cyclic stretching Tissue Eng 13 2007 1313
17. S. Stolberg, and K.E. McCloskey Can shear stress direct stem cell fate? Biotechnol Prog 25 2009 10
18. M. Denda, M. Nakatani, and K. Ikeyama Epidermal keratinocytes as the forefront of the sensory system Exp Dermatol 16 2007 1571
19. T. Lund, H. Onarheim, and R.K. Reed Pathogenesis of edema formation in burn injuries World J Surg 16 1992 2
20. L.E. Lanyon, and C.T. Rubin Static vs dynamic loads as an influence on bone remodelling J Biomech 17 1984 897
21. E.K. Chu, J. Cheng, and J.S. Foley Am J Respir Cell Mol Biol 35 2006 628
22. E.K. Chu, J.S. Foley, and J. Cheng Bronchial epithelial compression regulates epidermal growth factor receptor family ligand expression in an autocrine manner Am J Respir Cell Mol Biol 32 2005 373
23. H. Tanaka, P.R. Manske, and D.L. Pruitt Effect of cyclic tension on lacerated flexor tendons in vitro J Hand Surg 20 1995 467
24. J. Waninger, G.W. Kauffmann, and I.A. Shah Influence of the distance between interrupted sutures and the tension of sutures on the healing of experimental colonic anastomoses Am J Surg 163 1992 319
25. G. Gabbiani The myofibroblast in wound healing and fibrocontractive diseases J Pathol 200 2003 500
26. B. Hinz Formation and function of the myofibroblast during tissue repair J Invest Dermatol 127 2007 526
27. P.J. Wipff, D.B. Rifkin, and J.J. Meister Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix J Cell Biol 179 2007 1311
28. T.M. Freyman, I.V. Yannas, and Y.S. Pek Micromechanics of fibroblast contraction of a collagen-GAG matrix Exp Cell Res 269 2001 140
29. D. Li, T. Tang, and J. Lu Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor Tissue Eng Part A 15 2009 2773
30. G. García-Cardeña, J. Comander, and K.R. Anderson Biomechanical activation of vascular endothelium as a determinant of its functional phenotype PNAS 98 2001 4478
31. P.F. Davies, A. Remuzzi, and E.J. Gordon Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro Proc Natl Acad Sci USA 83 1986 2114
32. C.V. Gemmiti, and R.E. Guldberg Shear stress magnitude and duration modulates matrix composition and tensile mechanical properties in engineered cartilaginous tissue Biotechnol Bioeng 104 2009 809
33. G.M. Riha, P.H. Lin, and A.B. Lumsden Roles of hemodynamic forces in vascular cell differentiation Ann Biomed Eng 33 2005 772
34. S. Lehoux, Y. Castier, and A. Tedgui Molecular mechanism of the vascular response to haemodynamic forces J Int Med 259 2006 381
35. J.D. Kakisis, C.D. Liapis, and B.E. Sumpio Effects of cyclic strain on vascular cells Endothelium 11 2004 17
36. C. Li, and Q. Xu Mechanical stress-initiated signal transduction in vascular smooth muscle cells in vitro and in vivo Cell. Signaling 19 2007 881
37. J.H. Haga, Y.J. Li, and S. Chien Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells J Biomech 40 2007 947
38. J. Sadoshima, Y. Xu, and H.S. Slayter Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro Cell 75 1993 977
39. J. Lammerding, R.D. Kamm, and R.T. Lee Mechanotransduction in cardiac myocytes Ann NY Acad Sci 1015 2004 53
40. K.S. Gunningham, and A.I. Gotlieb The role of shear stress in the pathogenesis of atherosclerosis Lab Invest 85 2005 9
41. A.W. Orr, and B.P. Helmke Mechanisms of mechanotransduction Dev Cell 10 2006 11
42. S. Lehoux Redox signaling in vascular responses to shear and stretch Cardiovasc Res 71 2006 269
43. R. Knoll, M. Hoshijima, and K. Chien Cardiac mechanotransduction and implications for heart disease J Mol Med 81 2003 750
44. S.L. Edwards Tissue viability: Understanding the mechanisms of injury and repair Nurs Stand 21 2006 48
45. M.B. Myers, G. Cherry, and S. Heimburger The effect of edema and external pressure on wound healing Arch Surg 94 1967 218
46. R.M. Farahani, and L.A. DiPietro Microgravity and the implications for wound healing Int Wound J 5 2008 552
47. L.B. Buravkova, and Y.A. Romanov The role of cytoskeleton in cell changes under condition of simulated microgravity Acta Astronautica 48 2001 647
48. R.M. Farahani, and L.A. DiPietro Microgravity and the implications for wound healing Int Wound J 5 2008 552
49. L.C. Argenta, and M.J. Morykwas Vacuum-assisted closure: A new method for wound control and treatment: Clinical experience Ann Plast Surg 38 1997 563
50. M.J. Morykwas, L.C. Argenta, and E.I. Shelton-Brown Vacuum-assisted closure: A new method for wound control and treatment: Animal studies and basic foundation Ann Plast Surg 38 1997 553
51. S. Scherer, G. Pietramaggiori, and J. Mathews The mechanism of action of the vacuum assisted closure device Plast Reconstr Surg 122 2008 786
52. A.K. McNulty, M. Schmidt, and T. Feeley Effects of negative pressure wound therapy on fibroblast viability, chemotactic signaling, and proliferation in a provisional wound (fibrin) matrix Wound Rep Regen 15 2007 838
53. K. Nishimura, P. Blume, and S. Ohgi Effect of different frequencies of tensile strain on human dermal fibroblast proliferation and survival Wound Rep Regen 15 2007 646
54. S. Jacobs, D.A. Simhaee, and A. Marsano Efficacy and mechanisms of vacuum-assisted closure (VAC) therapy in promoting wound healing: A rodent model J Plast Reconstr Aesthet Surg 62 2009 1331
55. V. Saxena, C.W. Hwang, and S. Huang Vacuum-assisted closure: Microdeformations of wounds and cell proliferation Plast Reconstr Surg 114 2004 1086
56. S. Huang, C.S. Chen, and D.E. Ingber Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension Mol Biol Cell 9 1998 3179
57. C.S. Chen, M. Mrksich, and S. Huang Geometric control of cell life and death Science 276 1997 1425
58. S.S. Scherer, G. Pietramaggiori, and J.C. Mathews The mechanism of action of the vacuum-assisted closure device Plast Reconstr Surg 122 2008 786
59. S.S. Scherer, G. Pietramaggiori, and J.C. Mathews Short periodic applications of the vacuum-assisted closure device cause an extended tissue response in the diabetic mouse model Plast Reconstr Surg 124 2009 1458
60. K.J. McLeod, R.C. Lee, and H.P. Ehrlich Frequency dependence of electrical field modulation of fibroblast protein synthesis Science 236 1987 1465
61. J. Folkman, and A. Moscon Role of cell shape in growth control Nature 273 1978 345
62. R.C. Lee, E.H. Frank, and A.J. Grodzinsky Oscillatory compressional behavior of articular cartilage and its associated electromechanical properties J Biomech Eng 103 1981 280
63. R.C. Lee, T.R. Gowrishankar, and R.M. Basch Cell shape-dependent rectification of surface receptor transport in a sinusoidal electric field Biophysical J 64 1993 44
64. K.S. Fang, B. Farboud, and R. Nuccitelli Migration of human keratinocytes in electric fields requires growth factors and extracellular calcium J Invest Dermatol 111 1998 751
65. C.G. Neumann The expansion of an area of skin by progressive distention of a subcutaneous balloon Plast Reconstr Surg 19 1957 124
66. N. Pallua, and D. O'Dey II-7.1 Gewebeexpansion - Grundprinzipien und Funktion S. Krupp, S. Rennekampff, N. Pallua, Plastische Chirurgie 2006 Landsberg Ecomed 1 14
67. E.K. Manders, T.E. Oaks, and V.K. Au Soft-tissue expansion in the lower extremities Plast Reconstr Surg 81 1988 208
68. G. Turgut, A. Ozcan, and O. Sümer Reconstruction of complicated scalp defect via skin traction J Craniofacial Surg 20 2009 263
69. C.G. Neumann The expansion of an area of skin by progressive distention of a subcutaneous balloon: Use of the method for securing skin for subtotal reconstruction of the ear Plast Reconstr Surg (1946) 19 1957 124
70. M. Daya, and V. Nair Traction-assisted dermatogenesis by serial intermittent skin tape application Plast Reconstr Surg 122 2008 1047
71. G. Pietramaggiori, P. Liu, and S.S. Scherer Tensile forces stimulate vascular remodelling and epidermal cell proliferation Ann Surg 246 2007 896
72. C.D. Shrader, H.G. Ressetar, and J. Luo Acute stretch promotes endothelial cell proliferation in wounded healing mouse skin Arch Dermatol Res 300 2008 495
73. X. Zhu, D. Hall, and G. Ridenour A mouse model for studying rapic intraoperative methods of skin closure and wound healing Med Sci Monit 9 2003 109
74. Y. Zhu, J. Luo, and J. Barker IdentiWcation of genes induced by rapid intraoperative tissue expansion in mouse skin Arch Dermatol Res 293 2002 560
75. M. Beeson, M.P. Sajan, and M. Dizon Activation of protein kinase C-zeta by insulin and phosphatidylinositol-3,4,5-(PO4)3 is defective in muscle in type 2 diabetes and impaired glucose tolerance: Amelioration by rosiglitazone and exercise Diabetes 52 2003 1926
76. E. Wertheimer, M. Trebicz, and T. Eldar DiVerential roles of insulin receptor and insulin-like growth factor-1 receptor in diVerentiation of murine skin keratinocytes J Invest Dermatol 115 2000 24
77. N.A. Bouffard, K.R. Cutroneo, and G.J. Badger Tissue stretch decreases soluble TGF-b1 and type-1 procollagen in mouse subcutaneous connective tissue: Evidence from ex vivo and in vivo models J Cellular Physiol 214 2008 389
78. M.S. Chin, L. Lancerotto, and D.L. Helm Analysis of neuropeptides in stretched skin Plast Reconstr Surg 124 2009 102
79. P. Holzer Neurogenic vasodilatation and plasma leakage in the skin Gen Pharmacol 30 1998 5
80. E. Senba, and H. Kashiba Sensory afferent processing in multiresponsive DRG neurons Prog Brain Res 113 1996 387
81. R. Ogawa, K. Mitsuhashi, and H. Hyakusoku Postoperative electron-beam irradiation therapy for keloids and hypertrophic scars: Retrospective study of 147 cases followed for more than 18 months Plast Reconstr Surg 111 2003 547
82. S. Akaishi, R. Ogawa, and H. Hyakusoku Keloid and hypertrophic scar: Neurogenic inflammation hypotheses Med Hypotheses 71 2008 32
83. R. Ogawa Keloid and hypertrophic scarring may result from a mechanoreceptor or mechanosensitive nociceptor disorder Med Hypotheses 71 2008 493
84. S. Akaishi, M. Akimoto, and R. Ogawa The relationship between keloid growth pattern and stretching tension: Visual analysis using the finite element method Ann Plast Surg 60 2008 445
85. S. Aarabi, K.A. Bhatt, and Y. Shi Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis FASEB J 21 2007 3250
86. R. Ogawa The most current algorithms for the treatment and prevention of hypertrophic scars and keloids Plast Reconstr Surg 125 2010 557
87. J.A. Atkinson, K.T. McKenna, and A.G. Barnett A randomized, controlled trial to determine the efficacy of paper tape in preventing hypertrophic scar formation in surgical incisions that traverse Langer's skin tension lines Plast Reconstr Surg 116 2005 1648 discussion 1657
88. M. McCarty An evaluation of evidence regarding application of silicone gel sheeting for the management of hypertrophic scars and keloids J Clin Aesthet Dermatol 3 2010 39
89. L. Borgognoni Biological effects of silicone gel sheeting Wound Repair Regeneration 10 2002 118
90. C.C. Chang, Y.F. Kuo, and M.S. Chiu Hydration, not silicone, modulates the effects of keratinocytes on fibroblasts J Surg Res 59 1995 705
91. T. Suetake, S. Sasai, and Y. Zhen Effects of silicone gel sheet on the stratum corneum hydration Br J Plast Surg 53 2000 503
92. T. Mustoe Evolution of silicone therapy and mechanism of action in scar management Aesthet Plast Surg 32 2008 82
93. S. Akaishi, M. Akimoto, and H. Hyakusoku The tensile reduction effects of silicone gel sheeting Plast Reconstr Surg 126 2010 109e
94. M. Sakuraba, N. Takahashi, and T. Akahoshi Use of silicone gel sheets for prevention of keloid scars after median sternotomy Surg Today 41 2011 496
95. M. Sakuraba, N. Takahashi, and T. Akahoshi Experience of silicone gel sheets for patients with keloid scars after median sternotomy Gen Thorac Cardiovasc Surg 58 2010 467
96. M.H. Gold, T.D. Foster, and M.A. Adair Prevention of hypertrophic scars and keloids by the prophylactic use of topical silicone gel sheets following a surgical procedure in an office setting Dermatol Surg 27 2001 641
97. M.H. Gold Topical silicone gel sheeting in the treatment of hypertrophic scars and keloids. A dermatologic experience J Dermatol Surg Oncol 19 1993 912
98. R. Ogawa Keloid and hypertrophic scarring may result from a mechanoreceptor or mechanosensitive nociceptor disorder Med Hypotheses 71 2008 493
99. S. Akaishi, M. Akimoto, and R. Ogawa The relationship between keloid growth pattern and stretching tension: Visual analysis using the finite element method Ann Plast Surg 60 2008 445
100. K.Q. Zhu, L.H. Engrav, and N.S. Gibran The female, red Duroc pig as an animal model of hypertrophic scarring and the potential role of the cones of skin Burns 29 2003 649
101. D.E. Morris, L. Wu, and L.L. Zhao Acute and chronic animal models for excessive dermal scarring: Quantitative studies Plast Reconstr Surg 100 1997 674
102. K.Q. Zhu, L.H. Engrav, and R. Armendariz Changes in VEGF and nitric oxide after deep dermal injury in the female, red Duroc pig further similarities between female, Duroc scar and human hypertrophic scar Burns 31 2005 5
103. R.R. Reid, J.E. Mogford, and R. Butt Inhibition of procollagen C-proteinase reduces scar hypertrophy in a rabbit model of cutaneous scarring Wound Repair Regen 14 2006 138
104. R. Ogawa, and M.S. Chin Animal models of keloids and hypertrophic scars J Burn Care Res 29 2008 1016
105. Silverstein P, Goodwin MN, Raulston GL. Hypertrophic scarring, etiology, and control. In: Annual Research Progress Report of the US Army Institute of Surgical Research; 30 June 1972 [section 37].
106. P. Silverstein, M.N. Goodwin, and G.L. Raulston Hypertrophic scar in the experimental animal J.J. Longacre, The ultrastructure of collagen 1976 Thomas Springfield, IL
107. K.Q. Zhu, L.H. Engrav, and N.S. Gibran The female, red Duroc pig as an animal model of hypertrophic scarring and the potential role of the cones of skin Burns 29 2003 649
108. K.Q. Zhu, L.H. Engrav, and R.N. Tamura Further similarities between cutaneous scarring in the female, red Duroc pig and human hypertrophic scarring Burns 30 2004 518
109. S. Aarabi, K.A. Bhatt, and Y. Shi Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis FASEB J 21 2007 3250
110. J.D. Burrington Wound healing in the fetal lamb J Pediatr Surg 6 1971 523
111. A.S. Colwell, M.T. Longaker, and H.P. Lorenz Fetal wound healing Front Biosci 8 2003 s1240
112. A.S. Colwell, M.T. Longaker, and H. Peter Lorenz Identification of differentially regulated genes in fetal wounds during regenerative repair Wound Repair Regen 16 2008 450
113. A.S. Colwell, M.T. Longaker, and H.P. Lorenz Mammalian fetal organ regeneration Adv Biochem Eng Biotechnol 93 2005 83
114. H.P. Lorenz, M.T. Longaker, and L.A. Perkocha Scarless wound repair: A human fetal skin model Development 114 1992 253
115. J. Yeh, L.M. Green, and T.X. Jiang Accelerated closure of skin wounds in mice deficient in the homeobox gene Msx2 Wound Repair Regen 17 2009 639
116. M.T. Longaker, D.J. Whitby, and M.W. Ferguson Adult skin wounds in the fetal environment heal with scar formation Ann Surg 219 1994 65
117. D.L. Cass, K.M. Bullard, and K.G. Sylvester Wound size and gestational age modulate scar formation in fetal wound repair J Pediatr Surg 32 1997 411
118. D.C. West, D.M. Shaw, and P. Lorenz Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan Int J Biochem Cell Biol 29 1997 201
119. C. Soo, W.W. Shaw, and X. Zhang Differential expression of matrix metalloproteinases and their tissue-derived inhibitors in cutaneous wound repair Plast Reconstr Surg 105 2000 638
120. M. Hsu, Z.M. Peled, and G.S. Chin Ontogeny of expression of transforming growth factor-β1 (TGF-β1), TGF-β3, and TGF-β receptors I and II in fetal rat fibroblasts and skin Plast Reconstr Surg 107 2001 1787 discussion 1795
121. A. Nauta, G. Gurtner, and M. Longaker Wound healing and regenerative strategies Oral Dis 2011 (in press)
122. S.B. Ting, J. Caddy, and N. Hislop A homolog of Drosophila grainy head is essential for epidermal integrity in mice Science 308 2005 411
123. P. Martin, D. D'Souza, and J. Martin Wound healing in the PU.1 null mouse: Tissue repair is not dependent on inflammatory cells Curr Biol 13 2003 1122
124. A.M. Szpaderska, E.I. Egozi, and R.L. Gamelli The effect of thrombocytopenia on dermal wound healing J Invest Dermatol 120 2003 1130
125. E.I. Egozi, A.M. Ferreira, and A.L. Burns Mast cells modulate the inflammatory but not the proliferative response in healing wounds Wound Repair Regen 11 2003 46
126. M.E. Schrementi, A.M. Ferreira, and C. Zender Site-specific production of TGF-β in oral mucosal and cutaneous wounds Wound Repair Regen 16 2008 80
127. J.M. Rhett, G.S. Ghatnekar, and J.A. Palatinus Novel therapies for scar reduction and regenerative healing of skin wounds Trends Biotechnol 26 2008 173
128. R.K. Chan, E. Garfein, and P.R. Gigante Side population hematopoietic stem cells promote wound healing in diabetic mice Plast Reconstr Surg 120 2007 407 discussion 412
129. L. Chen, E.E. Tredget, and P.Y. Wu Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing PLoS One 3 2008 e1886
130. F.Q. Nie, M. Yamada, and J. Kobayashi On-chip cell migration assay using microfluidic channels Biomaterials 28 2007 4017
131. A.T. O'Neill, N.A. Monteiro-Riviere, and G.M. Walker Characterization of microfluidic human epidermal keratinocyte culture Cytotechnology 56 2008 197
132. W. Zhang, H. Abukawa, and M.J. Troulis Tissue engineered hybrid tooth-bone constructs Methods 47 2009 122
133. R. Ogawa, and D.P. Orgill Mechanobiology of cutaneous wound healing and scarring Studies Mechanobiol Tissue Eng Biomater 1 2009 31