Skin replacement in burn wounds

Journal of Trauma - Injury, Infection and Critical Care

Volumn 68, Issue 2, 2010, Pages 490-501

  Brusselaers, Nele ^a,b   Pirayesh, Ali ^a   Hoeksema, Henk ^a,b   Richters, Cornelia D ^c   Verbelen, Jozef ^a,b   Beele, Hilde ^a,b   Blot, Stijn I ^a,b,d   Monstrey, Stan ^a,b  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY COLLEGE GHENT   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; CYCLOSPORIN; HYALURONIC ACID;

BURN; CELL CULTURE; CRYOPRESERVATION; DERMIS; EPIDERMIS; EXTRACELLULAR MATRIX; GRAFT REJECTION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; REVIEW; SKIN ALLOGRAFT; SKIN TRANSPLANTATION; WOUND CLOSURE;

ANIMALS; BIOCOMPATIBLE MATERIALS; BURNS; CELLS, CULTURED; CICATRIX; COLLAGEN; CONTRACTURE; DEBRIDEMENT; GRAFT REJECTION; HUMANS; HYALURONIC ACID; KERATINOCYTES; SKIN TRANSPLANTATION; SKIN, ARTIFICIAL; WOUND HEALING;

EID: 77249121700     PISSN: 00225282     EISSN: 15298809     Source Type: Journal    
DOI: 10.1097/TA.0b013e3181c9c074     Document Type: Review

References (197)

1. Brusselaers N, Hoste EA, Monstrey S, et al. Outcome and changes over time in survival following severe burns from 1985 to 2004. Intensive Care Med. 2005;31:1648-1653.
2. Barret JP, Herndon DN. Effects of burn wound excision on bacterial colonization and invasion. Plast Reconstr Surg. 2003;111:744 -750; discussion 751-1742
3. Blot S, Brusselaers N, Monstrey S, et al. Belgian Outcome in Burn Injury Study Group. Development and validation of a model for prediction of mortality in patients with acute burn injury. Br J Surg. 2009;96:111-117.
4. Brusselaers N, Juhasz I, Erdei I, Monstrey S, Blot S. Evaluation of mortality following severe burns injury in Hungary: external validation of a prediction model developed on Belgian burn data. Burns. 2009; 35:1009 -1014; doi: 10.1016/j.burns.2008.1012.1017.
5. Monstrey S, Hoeksema H, Verbelen J, Pirayesh A, Blondeel P. Assessment of burn depth and burn wound healing potential. Burns. 2008;34:761-769.
6. Brusselaers N, Lafaire C, Ortiz S, Jacquemin D, Monstrey S. The consensus of the surgical treatment of burn injuries in Belgium. Acta Chir Belg. 2008;108:645-650.
7. Morimoto N, Takemoto S, Kawazoe T, Suzuki S, Tomihata K, Taira T. In vivo culturing of a bilayered substitute with adipo-stromal cells. J Surg Res. 2008;146:246-253.
8. de Backere AC. Euro Skin Bank: large scale skin-banking in Europe based on glycerol-preservation of donor skin. Burns. 1994;20(Suppl 1):S4-S9.
9. Bravo D, Rigley TH, Gibran N, Strong DM, Newman-Gage H. Effect of storage and preservation methods on viability in transplantable human skin allografts. Burns. 2000;26:367-378.
10. Cassidy C, St Peter SD, Lacey S, et al. Biobrane versus duoderm for the treatment of intermediate thickness burns in children: a prospective, randomized trial. Burns. 2005;31:890-893.
11. Lorenz HP, Adzick NS. Scarless skin wound repair in the fetus. West J Med. 1993;159:350-355.
12. Ehrenfried A. Reverdin and other methods of skin grafting. Boston Med Surg J. 1909;26:911-917.
13. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell. 1975;6:331-343.
14. Beele H, Naeyaert JM, Goeteyn M, De Mil M, Kint A. Repeated cultured epidermal allografts in the treatment of chronic leg ulcers of various origins. Dermatologica. 1991;183:31-35.
15. Monstrey S, Beele H, Kettler M, et al. Allogeneic cultured keratinocytes vs. cadaveric skin to cover wide-mesh autogenous split-thickness skin grafts. Ann Plast Surg. 1999;43:268-272.
16. Cuono C, Langdon R, McGuire J. Use of cultured epidermal autografts and dermal allografts as skin replacement after burn injury. Lancet. 1986;1:1123-1124.
17. Cuono CB, Langdon R, Birchall N, Barttelbort S, McGuire J. Composite autologous-allogeneic skin replacement: development and clinical application. Plast Reconstr Surg. 1987;80:626-637.
18. Hafner J, Kuhne A, Trueb RM. Successful grafting with EpiDex in pyoderma gangrenosum. Dermatology. 2006;212:258-259.
19. Lam PK, Chan ES, To EW, Lau CH, Yen SC, King WW. Development and evaluation of a new composite Laserskin graft. J Trauma. 1999; 47:918-922.
20. Phillips TJ, Gilchrest BA. Cultured allogenic keratinocyte grafts in the management of wound healing: prognostic factors. J Dermatol Surg Oncol. 1989;15:1169-1176.
21. Navarro FA, Stoner ML, Park CS, et al. Sprayed keratinocyte suspensions accelerate epidermal coverage in a porcine microwound model. J Burn Care Rehabil. 2000;21:513-518.
22. Rouabhia M, Germain L, Bergeron J, Auger FA. Allogeneic-syngeneic cultured epithelia. A successful therapeutic option for skin regeneration. Transplantation. 1995;59:1229-1235.
23. Larochelle F, Ross G, Rouabhia M. Permanent skin replacement using engineered epidermis containing fewer than 5% syngeneic keratinocytes. Lab Invest. 1998;78:1089-1099.
24. De Luca M, Albanese E, Bondanza S, et al. Multicentre experience in the treatment of burns with autologous and allogenic cultured epithelium, fresh or preserved in a frozen state. Burns. 1989;15:303-309.
25. Regnier M, Staquet MJ, Schmitt D, Schmidt R. Integration of Langerhans cells into a pigmented reconstructed human epidermis. J Invest Dermatol. 1997;109:510-512.
26. Munster AM. Use of cultured epidermal autograft in ten patients. J Burn Care Rehabil. 1992;13:124-126.
27. Wood FM, Stoner M. Implication of basement membrane development on the underlying scar in partial-thickness burn injury. Burns. 1996; 22:459-462.
28. Chester DL, Balderson DS, Papini RP. A review of keratinocyte delivery to the wound bed. J Burn Care Rehabil. 2004;25:266-275.
29. Compton CC, Gill JM, Bradford DA, Regauer S, Gallico GG, O'Connor NE. Skin regenerated from cultured epithelial autografts on full-thickness burn wounds from 6 days to 5 years after grafting. A light, electron microscopic and immunohistochemical study. Lab Invest. 1989;60:600-612.
30. Barret JP, Wolf SE, Desai MH, Herndon DN. Cost-efficacy of cultured epidermal autografts in massive pediatric burns. Ann Surg. 2000;231: 869-876.
31. Braye F, Oddou L, Bertin-Maghit M, et al. Widely meshed autograft associated with cultured autologous epithelium for the treatment of major burns in children: report of 12 cases. Eur J Pediatr Surg. 2000;10:35-40.
32. Herndon DN, Rutan RL. Comparison of cultured epidermal autograft and massive excision with serial autografting plus homograft overlay. J Burn Care Rehabil. 1992;13:154-157.
33. Ronfard V, Broly H, Mitchell V, et al. Use of human keratinocytes cultured on fibrin glue in the treatment of burn wounds. Burns. 1991;17:181-184.
34. Grinnell F. Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol. 1994;124:401-404.
35. van den Bogaerdt AJ, van Zuijlen PP, van Galen M, Lamme EN, Middelkoop E. The suitability of cells from different tissues for use in tissue-engineered skin substitutes. Arch Dermatol Res. 2002;294:135-142.
36. Ralston DR, Layton C, Dalley AJ, Boyce SG, Freedlander E, MacNeil S. Keratinocytes contract human dermal extracellular matrix and reduce soluble fibronectin production by fibroblasts in a skin composite model. Br J Plast Surg. 1997;50:408-415.
37. Kolenik SA III, Leffell DJ. The use of cryopreserved human skin allografts in wound healing following Mohs surgery. Dermatol Surg. 1995;21:615-620.
38. Braye F, Hautier A, Bouez C, Damour O. Skin substitutes reconstructed in the laboratory: application in burn treatment [in French]. Pathol Biol (Paris). 2005;53:613-617.
39. Yannas IV, Burke JF. Design of an artificial skin. I. Basic design principles. J Biomed Mater Res. 1980;14:65-81.
40. Yannas IV, Burke JF, Gordon PL, Huang C, Rubenstein RH. Design of an artificial skin. II. Control of chemical composition. J Biomed Mater Res. 1980;14:107-132.
41. Pachence JM. Collagen-based devices for soft tissue repair. J Biomed Mater Res. 1996;33:35-40.
42. Achauer BM, Hewitt CW, Black KS, et al. Long-term skin allograft survival after short-term cyclosporin treatment in a patient with massive burns. Lancet. 1986;1:14-15.
43. Burke JF, Bondoc CC, Quinby WC. Primary burn excision and immediate grafting: a method shortening illness. J Trauma. 1974;14:389-395.
44. Hewitt CW, Black KS, Achauer BM, Patel MP. Reconstructive allotransplantation: considerations regarding integumentary musculoskeletal grafts, cyclosporine, wound coverage in thermal injury and the immune response. J Burn Care Rehabil. 1990;11:74-85.
45. Nave M. Wound bed preparation: approaches to replacement of dermis. J Burn Care Rehabil. 1992;13:147-153.
46. Yang C, Shih T-S, Chu T-A. The intermingled transplantation of auto and homograft in severe burns. Burns. 1980;6:141.
47. Moulin V, Auger FA, O'Connor-McCourt M, Germain L. Fetal and postnatal sera differentially modulate human dermal fibroblast phenotypic and functional features in vitro. J Cell Physiol. 1997;171:1-10.
48. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T. Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science. 1981;211:1052-1054.
49. Bell E, Sher S, Hull B, et al. The reconstitution of living skin. J Invest Dermatol. 1983;81:2S-10S.
50. Germain L, Jean A, Auger FA, Garrel DR. Human wound healing fibroblasts have greater contractile properties than dermal fibroblasts. J Surg Res. 1994;57:268-273.
51. Bouvard V, Germain L, Rompre P, Roy B, Auger FA. Influence of dermal equivalent maturation on the development of a cultured skin equivalent. Biochem Cell Biol. 1992;70:34-42.
52. Auger FA, Rouabhia M, Goulet F, Berthod F, Moulin V, Germain L. Tissue-engineered human skin substitutes developed from collagenpopulated hydrated gels: clinical and fundamental applications. Med Biol Eng Comput. 1998;36:801-812.
53. Wainwright D, Madden M, Luterman A, et al. Clinical evaluation of an acellular allograft dermal matrix in full-thickness burns. J Burn Care Rehabil. 1996;17:124-136.
54. Schulz JT III, Tompkins RG, Burke JF. Artificial skin. Annu Rev Med. 2000;51:231-244.
55. Bell E, Ivarsson B, Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci USA. 1979;76: 1274-1278.
56. de Vries HJ, Middelkoop E, van Heemstra-Hoen M, Wildevuur CH, Westerhof W. Stromal cells from subcutaneous adipose tissue seeded in a native collagen/elastin dermal substitute reduce wound contraction in full thickness skin defects. Lab Invest. 1995;73:532-540.
57. de Vries HJ, Middelkoop E, Mekkes JR, Dutrieux RP, Wildevuur CH, Westerhof H. Dermal regeneration in native non-cross-linked collagen sponges with different extracellular matrix molecules. Wound Repair Regen. 1994;2:37-47.
58. Suzuki S, Kawai K, Ashoori F, Morimoto N, Nishimura Y, Ikada Y. Long-term follow-up study of artificial dermis composed of outer silicone layer and inner collagen sponge. Br J Plast Surg. 2000;53: 659-666.
59. Rucker RB, Lefevre IL, Tom K. Arterial elastin synthesis in the growing chick. Adv Exp Med Biol. 1977;79:461-475.
60. Casasco M, Casasco A, Icaro Cornaglia A, Farina A, Calligaro A. Differential distribution of elastic tissue in human natural skin and tissue-engineered skin. J Mol Histol. 2004;35:421-428.
61. Fatini G, Gallenga G, Veltroni A. Treatment of burns with hyaluronic acid. Clinical study. Osp Ital Chir. 1968;19:283-287.
62. Price RD, Berry MG, Navsaria HA. Hyaluronic acid: the scientific and clinical evidence. J Plast Reconstr Aesthet Surg. 2007;60:1110-1119.
63. Narins RS, Bowman PH. Injectable skin fillers. Clin Plast Surg. 2005;32:151-162.
64. WHO Report of the World Health Organisation: Consultation on Medicinal and other products in relation to human and animal Transmssible Spongigform Encephalopathies-With the participation of the Office International des Epizooties (OIE), Geneva, Switzerland, 1997.
65. Belcher HJ, Zic R. Adverse effect of porcine collagen interposition after trapeziectomy: a comparative study. J Hand Surg. 2001;26:159-164.
66. Burke JF, Yannas IV, Quinby WC Jr, Bondoc CC, Jung WK. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg. 1981;194:413-428.
67. Yannas IV, Burke JF, Warpehoski M, et al. Prompt, long-term functional replacement of skin. Trans Am Soc Artif Intern Organs. 1981; 27:19-23.
68. Yannas IV. What criteria should be used for designing artificial skin replacements and how well do the current grafting materials meet these criteria? J Trauma. 1984;24:S29-S39.
69. Dantzer E, Braye FM. Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts. Br J Plast Surg. 2001;54:659-664.
70. Heimbach D, Luterman A, Burke J, et al. Artificial dermis for major burns. A multi-center randomized clinical trial. Ann Surg. 1988;208: 313-320.
71. Jaksic T, Burke JF. The use of "artificial skin" for burns. Annu Rev Med. 1987;38:107-117.
72. Matsuda K, Suzuki S, Isshiki N, et al. A bilayer "artificial skin" capable of sustained release of an antibiotic. Br J Plast Surg. 1991;44:142-146.
73. Téot L, Otman S, Faure C. [Les substituts dermiques: Caractéristiques techniques et intéret dans les plaies aigues et chroniques.] Journal des plaies et cicatrisations. 2008:27-33.
74. Scherer LA, Shiver S, Chang M, Meredith JW, Owings JT. He vacuum assisted closure device: a method of securing skin grafts and improving graft survival. Arch Surg. 2002;137:930 -934; discussion 933-934.
75. Narotam PK, Jose S, Nathoo N, Taylon C, Vora Y. Collagen matrix (DuraGen) in dural repair: analysis of a new modified technique. Spine (Phila Pa 1976). 2004;29:2861-2867; discussion 2868-2869.
76. Mizunuma M, Yanai H, Seno H, et al. Experience in repair utilizing artificial skin for exposed bone surfaces. Eur J Plast Surg. 2000;23: 305-308.
77. Mizuno H, Takeda A, Uchinuma E. Creation of an acellular dermal matrix from frozen skin. Aesthetic Plast Surg. 1999;23:316-322.
78. Suzuki S, Matsuda K, Maruguchi T, Nishimura Y, Ikada Y. Further applications of "bilayer artificial skin." Br J Plast Surg. 1995;48:222-229.
79. Soejima K, Nozaki M, Sasaki K, Takeuchi M, Negishi N. Reconstruction of burn deformity using artificial dermis combined with thin split-skin grafting. Burns. 1997;23:501-504.
80. Suzuki S, Matsuda K, Isshiki N, Tamada Y, Ikada Y. Experimental study of a newly developed bilayer artificial skin. Biomaterials. 1990; 11:356-360.
81. Suzuki S, Matsuda K, Isshiki N, Tamada Y, Yoshioka K, Ikada Y. Clinical evaluation of a new bilayer "artificial skin" composed of collagen sponge and silicone layer. Br J Plast Surg. 1990;43:47-54.
82. Matsuda K, Suzuki S, Isshiki N, Ikada Y. Re-freeze dried bilayer artificial skin. Biomaterials. 1993;14:1030-1035.
83. Matsuda K, Suzuki S, Isshiki N, Yoshioka K, Okada T, Ikada Y. Influence of glycosaminoglycans on the collagen sponge component of a bilayer artificial skin. Biomaterials. 1990;11:351-355.
84. Matsuda K, Suzuki S, Isshiki N, et al. Evaluation of a bilayer artificial skin capable of sustained release of an antibiotic. Biomaterials. 1992; 13:119-122.
85. Iida N, Fukushima K, Kanazaki A. A two-stage technique using a bovine dermal substitute to treat axillary hidradenitis. Eur J Plast Surg. 2005;28:359-363.
86. Matsui R, Okura N, Osaki K, Konishi J, Ikegami K, Koide M. Histological evaluation of skin reconstruction using artificial dermis. Biomaterials. 1996;17:995-1000. (Pubitemid 26153955)
87. Matsui R, Osaki K, Konishi J, Ikegami K, Koide M. Evaluation of an artificial dermis full-thickness skin defect model in the rat. Biomaterials. 1996;17:989-994. (Pubitemid 26153954)
88. Fabienne B, Daniel H, Odile D, et al. Development of a new bilayer dermal matrix, RENOSKIN-: preclinical data. Burns. 2007;33S:S1-S172.
89. Middelkoop E, de Vries HJ, Ruuls L, Everts V, Wildevuur CH, Westerhof W. Adherence, proliferation and collagen turnover by human fibroblasts seeded into different types of collagen sponges. Cell Tissue Res. 1995;280:447-453.
90. van Zuijlen PP, Vloemans JF, van Trier AJ, et al. Dermal substitution in acute burns and reconstructive surgery: a subjective and objective long-term follow-up. Plast Reconstr Surg. 2001;108:1938-1946.
91. Haslik W, Kamolz LP, Nathschlager G, Andel H, Meissl G, Frey M. First experiences with the collagen-elastin matrix Matriderm as a dermal substitute in severe burn injuries of the hand. Burns. 2007;33: 364-368.
92. Ryssel H, Gazyakan E, Germann G, Ohlbauer M. The use of Matri- Derm in early excision and simultaneous autologous skin grafting in burns-a pilot study. Burns. 2008;34:93-97.
93. Van Zuijlen PP, Van Trier AJ, Vloemans AF, Groenevelt F, Kreis RW, Middelkoop E. Graft survival and effectictiveness of dermal substitution in burns and reconstructive surgery in a one-stage grafting model. Plast Reconstr Surg. 2000;106:615-621.
94. Prasertsung IK, Bunaprasert T, Thanakit V, Thanakit V, Damrongsakkul S. Development of acellular dermis from porcine skin using periodic pressurized technique. J Biomed Mater Res B Appl Biomater. 2008;85:210-219.
95. Tang LL, Liu H, Wang YL, Xian CY, Su AH. Evaluation of the biocompatobility of acellular porcine dermis. Colloids Surf B Biointerfaces. 2007;57:215-218.
96. MacLeod TM, Cambrey A, Williams G, Sanders R, Green CJ. Evaluation of Permacol as a cultured skin equivalent. Burns. 2008;34:1169-1175.
97. Shevchenko RV, Sibbons PD, Sharpe JR, James SE. Use of a novel porcine collagen paste as a dermal substitute in full-thickness wounds. Wound Repair Regen. 2008;16:198-207.
98. Harper C. Permacol: clinical experience with a new biomaterial. Hosp Med. 2001;62:90-95.
99. Bello Y, Falabella AF, Eaglstein WH. Tissue-engineered skin: current status in wound healing. Am J Clin Dermatol. 2001;2:305-313.
100. Mostow EN, Haraway GD, Dalsing M, Hodde JP, King D; OASIS Venus Ulcer Study Group. Effectiveness of an extracellular matrix graft (OASIS Wound Matrix) in the treatment of chronic leg ulcers: a randomized clinical trial. J Vasc Surg. 2005;41:837-843.
101. Oliver RF, Grant RA, Kent CM. The fate of cutaneously and subcutaneously implanted trypsin purified dermal collagen in the pig. Br J Exp Pathol. 1972;53:540-549.
102. Fang CH, Robb EC, Yu GS, Alexander JW, Warden GD. Observations on stability and contraction of composite skin grafts: xenodermis or allodermis with an isograft overlay. J Burn Care Rehabil. 1990;11: 538-542.
103. Sasamoto Y, Alexander JW, Babcock GF. Prolonged survival of reconstituted skin grafts without immunosuppression. J Burn Care Rehabil. 1990;11:190-200.
104. Grillo HC, McKhann CF. The Acceptance and Evolution of Dermal Homografts Freed of Viable Cells. Transplantation. 1964;2:48-59.
105. Oliver RF, Barker H, Cooke A, Stephen L. 3H-collagen turnover in non-cross-linked and aldehyde-cross-linked dermal collagen grafts. Br J Exp Pathol. 1982;63:13-17.
106. Oliver RF, Grant RA. Reconstruction of full-thickness loss skin wounds using skin collagen allografts. Br J Plast Surg. 1979;32:87-90.
107. Ben-Bassat H, Eldad A, Chaouat M, et al. Structural and functional evaluation of modifications in the composite skin graft: cryopreserved dermis and cultured keratinocytes. Plast Reconstr Surg. 1992;89:510-520.
108. Medalie DA, Eming SA, Tompkins RG, Yarmush ML, Krueger GG, Morgan JR. Evaluation of human skin reconstituted from composite grafts of cultured keratinocytes and human acellular dermis transplanted to athymic mice. J Invest Dermatol. 1996;107:121-127.
109. Medalie DA, Tompkins RG, Morgan JR. Evaluation of acellular human dermis as a dermal analog in a composite skin graft. Asaio J. 1996;42: M455-M462.
110. Regnier M, Pautrat G, Pauly G, Prunieras M. Natural substrates for the reconstruction of skin in vitro. Br J Dermatol. 1984;111(Suppl 27): 223-224.
111. Oliver RF, Barker H, Cooke A, Grant RA. Dermal collagen implants. Biomaterials. 1982;3:38-40.
112. Walter RJ, Matsuda T, Reyes HM, Walter JM, Hanumadass M. Characterization of acellular dermal matrices (ADMs) prepared by two different methods. Burns. 1998;24:104-113.
113. Wainwright DJ. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full-thickness burns. Burns. 1995;21:243-248.
114. Livesey SA, Herndon DN, Hollyoak MA, Atkinson YH, Nag A. Transplanted acellular allograft dermal matrix. Potential as a template for the reconstruction of viable dermis. Transplantation. 1995;60:1-9.
115. Kirsner RS, Falanga V, Eaglstein WH. The development of bioengineered skin. Trends Biotechnol. 1998;16:246-249.
116. Rennekampff HO, Hansbrough JF, Woods V Jr, Kiessig V. Integrin and matrix molecule expression in cultured skin replacements. J Burn Care Rehabil. 1996;17:213-221.
117. Jones I, Currie L, Martin R. A guide to biological skin substitutes. Br J Plast Surg. 2002;55:185-193.
118. Becker S, Saint-Cyr M, Wong C, et al. AlloDerm versus DermaMatrix in immediate expander-based breast reconstruction: a preliminary comparison of complication profiles and material compliance. Plast Reconstr Surg. 2009;123:1- 6; discussion 107-108.
119. Shores JT, Gabriel A, Gupta S. Skin substitutes and alternatives: a review. Adv Skin Wound Care. 2007;20:493-508.
120. Pirayesh A, Dur AH, Paauw NJ, et al. Evaluation of acellular dermis for closure of abdominal wall defects in a rat model. Eur Surg Res. 2008;41:346-352.
121. Richters CD, Pirayesh A, Hoeksema H, et al. Development of a dermal matrix from glycerol preserved allogeneic skin. Cell Tissue Bank. 2008;9:309-315.
122. Barber C, Watt A, Pham C, et al. Influence of bioengineered skin substitutes on diabetic foot ulcer and venous leg ulcer outcomes. J Wound Care. 2008;17:517-527.
123. Brigido S. The use of an acellular dermal regenerative tissue matrix in the treatment of ower extremity wounds: a prospective 16-weeks pilot study. Int Wound J. 2006;3:181-187.
124. Brigido SA, Boc SF, Lopez RC. Effective management of major lower extremity wounds using an acellular regenerative tissue matrix: a pilot study. Orthopedics. 2004;27:S145-S149.
125. Takami Y, Matsuda T, Yoshitake M, Hanumadass M, Walter RJ. Dispase/detergent treated dermal matrix as a dermal substitute. Burns. 1996;22:182-190.
126. Takami Y, Matsuda T, Hanumadass M, et al. Acellular allogenic dermal matrix as a dermal substitute. Proc Int Conf: Plastic Reconsfruct Aesthet Surg. 1995;55:212-215.
127. Caravaggi C, De Giglio R, Pritelli C, et al. HYAFF 11-based autologous dermal and epidermal grafts in the treatment of noninfected diabetic plantar and dorsal foot ulcers: a prospective, multicenter, controlled, randomized clinical trial. Diabetes Care. 2003;26:2853-2859.
128. Gravante G, Delogu D, Giordan N, Morano G, Montone A, Esposito G. The use of Hyalomatrix PA in the treatment of deep partial-thickness burns. J Burn Care Res. 2007;28:269-274.
129. Price RD, Myers S, Leigh IM, Navsaria HA. The role of hyaluronic acid in wound healing: assessment of clinical evidence. Am J Clin Dermatol. 2005;6:393-402.
130. Tonello C, Zavan B, Cortivo R, Brun P, Panfilo S, Abatangelo G. In vitro reconstruction of human dermal equivalent enriched with endothelial cells. Biomaterials. 2003;24:1205-1211.
131. Galassi G, Brun P, Radice M, et al. In vitro reconstructed dermis implanted in human wounds: degradation studies of the HA-based supporting scaffold. Biomaterials. 2000;21:2183-2191.
132. Sattar A, Rooney S, Kumar D, et al. Application of angiogenetic oligosaccharides of hyaluronan increases blood vessel numbers in rat skin. J Invest Dermatol. 1994;103:576-579.
133. Hultman CS, Brinson GM, Siltharm S, et al. Allogeneic fibroblasts used to grow cultured epidermal autografts persist in vivo and sensitize the graft recipient for accelerated second-set rejection. J Trauma. 1996;41:51-58; discussion 58-60.
134. Ehrlich HP. Understanding experimental biology of skin equivalent: from laboratory to clinical use in patients with burns and chronic wounds. Am J Surg. 2004;187:29S-33S.
135. Gentzkow GD, Iwasaki SD, Hershon KS, et al. Use of dermagraft, a cultured human dermis, to treat diabetic foot ulcers. Diabetes Care. 1996;19:350-354.
136. Falanga V, Margolis D, Alvarez O, et al. Rapid healing of venous ulcers and lack of clinical rejection with an allogeneic cultured human skin equivalent. Human Skin Equivalent Investigators Group. Arch Dermatol. 1998;134:293-300.
137. Purdue GF, Hunt JL, Still JM Jr, et al. A multicenter clinical trial of a biosynthetic skin replacement, Dermagraft-TC, compared with cryopreserved human cadaver skin for temporary coverage of excised burn wounds. J Burn Care Rehabil. 1997;18:52-57.
138. el-Ghalbzouri A, Gibbs S, Lamme E, Van Blitterswijk CA, Ponec M. Effect of fibroblasts on epidermal regeneration. Br J Dermatol. 2002; 147:230-243.
139. Hansbrough JF, Morgan J, Greenleaf G, Underwood J. Development of a temporary living skin replacement composed of human neonatal fibroblasts cultured in Biobrane, a synthetic dressing material. Surgery. 1994;115:633-644.
140. Kumar RJ, Kimble RM, Boots R, Pegg SP. Treatment of partialthickness burns: a prospective, randomized trial using Transcyte. ANZ J Surg. 2004;74:622-626.
141. Hansbrough JF, Cooper ML, Cohen R, et al. Evaluation of a biodegradable matrix containing cultured human fibroblasts as a dermal replacement beneath meshed skin grafts on athymic mice. Surgery. 1992;111:438-446.
142. Economou TP, Rosenquist MD, Lewis RW II, Kealey GP. An experimental study to determine the effects of Dermagraft on skin graft viability in the presence of bacterial wound contamination. J Burn Care Rehabil. 1995;16:27-30.
143. Allenet B, Paree F, Lebrun T, et al. Cost-effectiveness modeling of Dermagraft for the treatment of diabetic foot ulcers in the french context. Diabetes Metab. 2000;26:125-132.
144. Brun P, Grosso F, Galassi G, et al. Use of dermal-like tissue in the management of chronic and acute full-thickness cutaneous wounds. Ostomy Wound Manage. 2000;46:44-48.
145. Hollander D, Soranzo C, Falk S, Windolf J. Extensive traumatic soft tissue loss: reconstruction in severely injured patients using cultured hyaluronan-based three-dimensional dermal and epidermal autografts. J Trauma. 2000;50:1125-1135.
146. Vazquez JR, Short B, Findlow AH, Nixon BP, Boulton AJ, Armstrong DG. Outcomes of hyaluronan therapy in diabetic foot wounds. Diabetes Res Clin Pract. 2003;59:123-127.
147. Ghosh MM, Boyce S, Layton C, Freedlander E, Mac Neil S. A comparison of methodologies for the preparation of human epidermaldermal composites. Ann Plast Surg. 1997;39:390-404.
148. Bell E, Ehrlich HP, Sher S, et al. Development and use of a living skin equivalent. Plast Reconstr Surg. 1981;67:386-392.
149. Eaglstein WH, Iriondo M, Laszlo K. A composite skin substitute (graftskin) for surgical wounds. A clinical experience. Dermatol Surg. 1995;21:839-843.
150. Coulomb B, Friteau L, Baruch J, et al. Advantage of the presence of living dermal fibroblasts within in vitro reconstructed skin for grafting in humans. Plast Reconstr Surg. 1998;101:1891-1903.
151. Wassermann D, Schlotterer M, Toulon A, et al. Preliminary clinical studies of a biological skin equivalent in burned patients. Burns Incl Therm Inj. 1988;14:326-330.
152. Falanga V. Apligraf treatment of venous ulcers and other chronic wounds. J Dermatol. 1998;25:812-817.
153. Hayes DW Jr, Webb GE, Mandracchia VJ, John KJ. Full-thickness burn of the foot: successful treatment with Apligraf. A case report. Clin Podiatr Med Surg. 2001;18:179-188.
154. Kirsner RS. The use of Apligraf in acute wounds. J Dermatol. 1998; 25:805-811.
155. Eaglstein WH, Falanga V. Tissue engineering and the development of Apligraf, a human skin equivalent. Cutis. 1998;62:1-8.
156. Badiavas E, Mehta PP, Falanga V. Retrovirally mediated gene transfer in a skin equivalent model of chronic wounds. J Dermatol Sci. 1996; 13:56-62.
157. Boyce ST, Christianson DJ, Hansbrough JF. Structure of a collagen- GAG dermal skin substitute optimized for cultured human epidermal keratinocytes. J Biomed Mater Res. 1988;22:939-957.
158. Boyce ST, Glafkides MC, Foreman TJ, Hansbrough JF. Reduced wound contraction after grafting of full-thickness burns with a collagen and chondroitin-6-sulfate (GAG) dermal skin substitute and coverage with biobrane. J Burn Care Rehabil. 1988;9:364-370.
159. Boyce ST, Hansbrough JF. Biologic attachment, growth, and differentiation of cultured human epidermal keratinocytes on a graftable collagen and chondroitin-6-sulfate substrate. Surgery. 1988;103:421-431.
160. Boyce S. Skin substitutes from cultured cells and collagen-GAG polymers. Med Biol Eng Comput. 1998;36:791-800.
161. Boyce S. Design principles for composition and performance of cultured skin substitutes. Burns. 2001;27:523-533.
162. Boyce ST, Kagan RJ, Meyer NA, Yakuboff KP, Warden GD. The 1999 clinical research award. Cultured skin substitutes combined with integra artificial skin to replace native skin autograft and allograft for the closure of excised full-thickness burns. J Burn Care Rehabil. 1999;20: 453-461.
163. Supp DM, Boyce ST. Engineered skin substitutes: practices and potentials. Clin Dermatol. 2005;23:403-412.
164. Boyce ST, Supp AP, Harriger MD, Greenhalgh DG, Warden GD. Topical nutrients promote engraftment and inhibit wound contraction of cultured skin substitutes in athymic mice. J Invest Dermatol. 1995; 104:345-349.
165. Still JM Jr, Glat P, Silverstein P, Griswold J, Mozingo D. The use of a collagen sponge/living cell composite material to treat donor sites in burn patients. Burns. 2003;29:837-841.
166. Eisenberg M, Llewelyn D. Surgical managment of hands in children with recesive dystrophic epidermolysis bullosa: use of allogeneic composite cultured skin grafts. Br J Plast Surg. 1998;51:608-613.
167. Xiao S, Zhu S, Ma B, Xia ZF, Yang J, Wang G. A new system for cultivation of human keratinocytes on acellular dermal matrix substitute with the use of human fibroblast feeder layer. Cell Tissue Organs. 2008;187:123-130.
168. Llames S, Garcia E, Garcia V, et al. Clinical results of an autologous engineered skin. Cell Tissue Bank. 2006;7:47-53.
169. Wood FM, Kolybaba P, Allen P. The use of cultured epitheloam autograft in the treatment of major burn wounds: eleven years of clinical experience. Burns. 2006;32:538-544.
170. Ralston DR, Layton C, Dalley AJ, Boyce SG, Freedlander E, Mac Neil S. The requirement for basement membrane antigens in the production of human epidermal/dermal composites in vitro. Br J Dermatol. 1999; 140:605-615.
171. Erdag G, Sheridan RL. Fibroblasts improve performance of cultured composite skin substitutes on athymic mice. Burns. 2004;30:322-328.
172. Chakrabarty KH, Dawson RA, Harris P, et al. Development of autologous human dermal-epidermal composites based on sterilized human allodermis for clinical use. Br J Dermatol. 1999;141:811-823.
173. Mewes KR, Raus M, Bernd A, Zoller NN, Sattler A, Graf R. Elastin expression in a newly developed full-thickness skin equivalent. Skin Pharmacol Physiol. 2007;20:85-95.
174. Hansbrough JF, Boyce ST, Cooper ML, Foreman TJ. Burn wound closure with cultured autologous keratinocytes and fibroblasts attached to a collagen-glycosaminoglycan substrate. JAMA. 1989;262:2125-2130.
175. Boyce S, Greenhalgh D, Kagan R, et al. Skin anatomy and antigen expression after burn wound closure with composite grafts of cultured skin cells and biopolymers. Plast Reconstr Surg. 1993;91:632-641.
176. Braye FM, Stefani A, Venet E, Pieptu D, Tissot E, Damour O. Grafting of large pieces of human reconstructed skin in a porcine model. Br J Plast Surg. 2001;54:532-538.
177. Li H, Berthod F, Xu W, Damour O, Germain L, Auger FA. Use of in vitro reconstructed skin to cover skin flap donor site. J Surg Res. 1997;73:143-148.
178. Solomon DE. An in vitro examination of an extracellular matrix scaffold for use in wound healing. Int J Exp Pathol. 2002;83:209-216.
179. Llames SG, Del Rio M, Larcher F, et al. Human plasma as a dermal scaffold for the generation of a completely autologous bioengineered skin. Transplantation. 2004;77:350-355.
180. Lerner AB, Halaban R, Klaus SN, Moellmann GE. Transplantation of human melanocytes. J Invest Dermatol. 1987;89:219-224.
181. Boyce ST, Medrano EE, Abdel-Malek Z, et al. Pigmentation and inhibition of wound contraction by cultured skin substitutes with adult melanocytes after transplantation to athymic mice. J Invest Dermatol. 1993;100:360-365.
182. Mendes FH. External ultrasound-assisted lipoplasty from our own experience. Aesthetic Plast Surg. 2000;24:270-274.
183. Sahota PS, Burn JL, Heaton M, et al. Development of a reconstructed human skin model for angiogenesis. Wound Repair Regen. 2003;11: 275-284.
184. Supp DM, Wilson-Landy K, Boyce ST. Human dermal microvascular endothelial cells form vascular analogs in cultured skin substitutes after grafting to athymic mice. Faseb J. 2002;16:797-804.
185. Black AF, Berthod F, L'Heureux N, Germain L, Auger FA. In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J. 1998;12:1331-1340.
186. Schechner J, Nath A, Zheng L. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA. 2000;97:9191-9196.
187. Conrad C, Huss R. Adult stem cell lines in regenerative medicine and reconstructive surgery. J Surg Res. 2005;124:201-208.
188. Pelled G, G T, Aslan H, Gazit Z, Gazit D. Mesenchymal stem cells for bone gene therapy and tissue engineering. Curr Pharm Des. 2002;8: 1917-1928.
189. Burd A, Ahmed K, Lam S, Ayyappan T, Huang L. Stem cell strategies in burns care. Burns. 2007;33:282-291.
190. Kim DH, Jamal N, Saragosa R, et al. Similar outcomes of cryopreserved allogeneic peripheral stem cell transplants (PBSCT) compared to fresh allografts. Biol Blood Marrow Transplant. 2007;13:1233-1243.
191. Hong L, Peptan I, Clark P, Mao JJ. Ex vivo adipose tissue engineering by human marrow stromal cell seeded gelatin sponge. Ann Biomed Eng. 2005;33:511-517.
192. Alhadlaq A, Tang M, Mao JJ. Engineered adipose tissue from human mesenchymal stem cells maintains predefined shape and dimension: implications in soft tissue augmentation and reconstruction. Tissue Eng. 2005;11:556-566.
193. Choi YS, Park SN, Suh H. Adipose tissue engineering using mesenchymal stem cells attached to injectable PLGA spheres. Biomaterials. 2005;26:5855-5863.
194. Vashi AV, Keramidaris E, Abberton KM, et al. Adipose differentiation of bone marrow-derived mesenchymal stem cells using Pluronic F-127 hydrogel in vitro. Biomaterials. 2008;29:573-579.
195. Hamoen KE, Erdag G, Cusick JL, Rakhorst HA, Morgan JR. Genetically modified skin substitutes. Preparation and use. Methods Mol Med. 2002;69:203-217.
196. Supp DM, Supp AP, Bell SM, Boyce ST. Enhanced vascularization of cultured skin substitutes genetically modified to overexpress vascular endothelial growth factor. J Invest Dermatol. 2000;114:5-13.
197. Morgan JR, Barrandon Y, Green H, Mulligan RC. Expression of an exogenous growth hormone gene in transplantable human epidermal cells. Science. 1987;237:1476-1479.