Biologic dressings: Current applications and limitations in dermatologic surgery

Dermatologic Surgery

Volumn 35, Issue 6, 2009, Pages 891-906

  Chern, Peggy L ^a   Baum, Christian L ^b   Arpey, Christopher J ^b  

^a SCRIPPS CLINIC   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE DISEASE; ADVERSE OUTCOME; ALLOGRAFT; CADAVER DONOR; COMPOSITE GRAFT; MEDLINE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SKIN AUTOGRAFT; SKIN SURGERY; SURGICAL WOUND; WOUND DRESSING;

BIOLOGICAL DRESSINGS; DERMATOLOGY; HUMANS; SKIN TRANSPLANTATION; WOUND HEALING; WOUNDS AND INJURIES;

EID: 66449101145     PISSN: 10760512     EISSN: 15244725     Source Type: Journal    
DOI: 10.1111/j.1524-4725.2009.01153.x     Document Type: Review

References (109)

1. Pruitt BA, Levine NS. Characteristics and uses of biologic dressings and skin substitutes. Arch Surg 1984 119 : 312 22.
2. Baum CL, Arpey CJ. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 2005 31 : 674 86.
3. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T. Living tissues formed in vitro and accepted as a skin-equivalent tissue of full thickness. Science 1981 211 : 1052 4.
4. Wilkins LM, Watson SR, Prosky SJ, et al. Development of a bilayered living skin construct for clinical applications. Biotechnol Bioeng 1994 43 : 747 56.
5. Apligraf web-site : [accessed March 20, 2008].
6. Eaglestein WH, Iriondo M, Laszlo K. A composite skin substitute (graftskin) for surgical wounds. A clinical experience. Dermatol Surg 1995 21 : 839 42.
7. Falanga V, Margolis D, Alvarez O, et al. Rapid healing of venous ulcers and lack of clinical rejection with an allogenic cultured human skin equivalent. Human skin equivalent investigators group. Arch Dermatol 1998 134 : 293 300.
8. Falanga V, Sabolinski M. A bilayered living skin construct (Apligraf) accelerates complete closure of hard-to-heal venous ulcers. Wound Rep Regen 1999 7 : 201 7.
9. Brem H, Balledux J, Sukkarieh T, et al. Healing of venous ulcers of long duration with a bilayered living skin substitute: results from a general surgery and dermatology department. Dermatol Surg 2001 27 : 915 9.
10. Veves A, Falanga V, Armstrong DG, Sabolinski ML. Graftskin, a human skin equivalent, is effective in the management of noninfected neuropathic diabetic foot ulcers: a prospective randomized multicenter clinical trial. Diabetes Care 2001 24 : 290 5.
11. Brem H, Balledux J, Bloom T, et al. Healing of diabetic foot ulcers and pressure ulcers with human skin equivalent: a new paradigm in wound healing. Arch Surg 2000 135 : 627 34.
12. Phillips TJ, Manzoor J, Rojas A, et al. The longevity of a bilayered skin substitute after application to venous ulcers. Arch Dermatol 2002 138 : 1079 81.
13. Griffiths M, Ojeh N, Livingstone R, et al. Survival of Apligraf in acute human wounds. Tissue Eng 2004 10 : 1080 95.
14. Hu S, Kirsner RS, Falanga V, et al. Evaluation of Apligraf persistence and basement membrane restoration in donor site wounds: a pilot study. Wound Reg Reg 2006 14 : 427 33.
15. Osborne CS, Schmid P. Epidermal-dermal interactions regulate gelatinase activity in Apligraf, a tissue-engineered human skin equivalent. Br J Dermatol 2002 146 : 26 31. (Pubitemid 34158405)
16. Muhart M, McFalls S, Kirsner RS, et al. Behavior of tissue-engineered skin. Arch Dermatol 1999 135 : 913 8.
17. Eaglestein WH, Alvarez OM, Auletta M, et al. Acute excisional wounds treated with a tissue-engineered skin (Apligraf). Dermatol Surg 1999 25 : 195 201. (Pubitemid 29146985)
18. Gohari S, Gambla C, Healey M, et al. Evaluation of tissue-engineered skin (human skin substitute) and secondary intention healing in the treatment of full thickness wounds after Mohs micrographic or excisional surgery. Dermatol Surg 2002 28 : 1107 14.
19. Tarlow MM, Nossa R, Spencer JM. Effective management of difficult surgical defects using tissue-engineered skin. Dermatol Surg 2001 27 : 71 4.
20. Fivenson DP, Scherschun L, Cohen LV. Apligraf in the treatment of severe mitten deformity associated with recessive dystrophic epidermolysis bullosa. Plast Reconst Surg 2003 112 : 584 8.
21. Fivenson DP, Scherschun L, Choucair M, et al. Graftskin therapy in epidermolysis bullosa. J Am Acad Dermatol 2003 48 : 886 92.
22. Lee DK, Serkin AL. Carbon dioxide laser and Apligraf for a painful plantar hypertrophic scar. J Am Podiatr Med Assoc 2004 94 : 61 4.
23. Bui D, Ikeda C. Reconstruction of aplasia cutis congenita (group V) in a newborn. Plast Reconstr Surg 2003 111 : 2119 20.
24. Martin LK, Kirsner RS. Ulcers caused by bullous morphea treated with tissue-engineered skin. Int J Dermatol 2003 42 : 402 4.
25. Culican SM, Custer PL. Repair of cicatricial ectropion in an infant with harlequin ichthyosis using engineered human skin. Am J Ophthalmol 2002 134 : 442 3.
26. Martin LK, Kirsner RS. Use of a meshed bilayered cellular matrix to treat a venous ulcer. Adv Skin Wound Care 2002 15 : 260 262, 264.
27. Eisenberg M, Llewelyn D. Surgical management of hands in children with recessive dystrophic epidermolysis bullosa: use of allogenic composite cultured skin grafts. Br J Plast Surg 1998 51 : 608 13.
28. Ehrenreich M, Ruszczak Z Update on tissue-engineered biological dressings. Tissue Eng 2006 12 : 2407 24.
29. Eldad A, Din A, Weinberg A, et al. Cryopreserved cadaveric allografts for treatment of unexcised partial thickness flame burns: clinical experience with 12 patients. Burns 1997 23 : 608 14.
30. 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 72.
31. Komorowska-Timek E, Gabriel A, Bennett DC, et al. Artificial dermis as an alternative for coverage of complex scalp defects following excision of malignant tumors. Plast Reconstr Surg 2005 115 : 1010 7.
32. Carucci JA, Kolenik SA, Leffell DJ. Human cadaveric allograft for repair of nasal defects after extirpation of basal cell carcinoma by Mohs micrographic surgery. Dermatol Surg 2002 28 : 340 3.
33. Tavis MJ, Thornton JW, Bartlett RH, et al. A new composite skin prosthesis. Burns 1980 7 : 123 30.
34. Ehrenrich M, Ruszczak Z. Tissue-engineered temporary wound coverings. Important options for the clinician. Acta Dermatovenerol Alp Panonica Adriat 2006 15 : 5 13.
35. Smith DJ Jr. Use of Biobrane in wound management. J Burn Care Rehab 1995 16 : 317 20.
36. Supp DM, Boyce ST. Engineered skin substitutes: practices and potentials. Clin Dermatol 2005 23 : 403 12.
37. Biobrane manufacturer (Smith & Nephew) website : [accessed June 20, 2008].
38. Gerding RL, Emerman CL, Effron D, et al. Outpatient management of partial-thickness burns: Biobrane versus 1% silver sulfadiazine. Ann Emerg Med 1990 19 : 121 4.
39. Demling RH. Use of Biobrane in the management of scalds. J Burn Care Rehabil 1995 16 : 329 30.
40. Purdue GF, Hunt JL, Gillespie RW, et al. Biosynthetic skin substitute versus frozen human cadaver allograft for temporary coverage of excised burn wounds. J Trauma 1987 27 : 155 7.
41. Lal S, Barrow RE, Wolf SE, et al. Biobrane improved wound healing in burned children without increased risk of infection. Shock 2000 14 : 314 8.
42. Levy PM, Salomon D. Use of Biobrane after laser resurfacing. Dermatol Surg 1998 24 : 729 34.
43. Melkun ET, Few JW. The use of biosynthetic skin substitute (Biobrane) for axillary reconstruction after surgical excision for hidradenitis suppurativa. Plast Reconstr Surg 2005 115 : 1385 8.
44. Bannasch H, Kontny U, Kruger M, et al. A semisynthetic bilaminar skin substitute used to treat pediatric full-body toxic epidermal necrolysis. Arch Dermatol 2005 140 : 160 2.
45. Bradley T, Brown RE, Kucan JO, et al. Toxic epidermal necrolysis: a review and report of the successful use of Biobrane for early wound coverage. Ann Plast Surg 1995 35 : 124 32.
46. Arevalo JM, Lorente JA. Skin coverage with Biobrane biomaterial for the treatment of patients with toxic epidermal necrolysis. J Burn Care Rehabil 1999 20 : 406 10.
47. Vun YY, Lun K, Strutton G. Use of biosynthetic dressings in paraneoplastic pemphigus. Australas J Dermatol 2004 45 : 133 5.
48. Burke J, Yannas I, Quimby, et al. Successful use of physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg 1981 194 : 413 28.
49. Jones I, Currie L, Martin R. A guide to biologic skin substitutes. Br J Plast Surg 2002 55 : 185 93.
50. Bello YM, Falabella AF, Eaglestein WH. Tissue-engineered skin: current status in wound healing. Am J Clin Dermatol 2001 2 : 305 13.
51. Integra manufacturer (Integra Life Sciences Corp.) website : [accessed June 20, 2008].
52. Heimbach D, Luterman A, Burke J, et al. Artificial dermis for major burns. A multi-center randomized clinical trial. Ann Surg 1988 208 : 313 20.
53. Campitiello F, Della Corte A, Fattopace A, et al. The use of artificial dermis in the treatment of chronic and acute wounds: regeneration of dermis and wound healing. Acta Biomed 2005 76 : 69 71. (Pubitemid 43188398)
54. Moiemen NS, Staiano JJ, Ojeh NO, et al. Reconstructive surgery with a dermal regeneration template: clinical and histologic study. Plast Reconstr Surg 2001 108 : 93 103. (Pubitemid 32587029)
55. Yannas IV. Studies on the biological activity of the dermal regeneration template. Wound Repair Regen 1998 6 : 518 23.
56. Dantzer E, Braye FM. Reconstructive surgery using artificial dermis (Integra.): results with 39 grafts. Br J Plast Surg 2001 54 : 659 64.
57. Clayman MA, Clayman SM, Mozingo DW. The use of collagen-glycosaminoglycan copolymer (Integra) for the repair of hypertrophic scars and keloids. J Burn Care Res 2006 27 : 404 9.
58. Ismail A, Jarvi K, Canal AC. Successful resurfacing of scars from previous deliberate self-harm using Integra dermal matrix substitute. J Plast Renconstr Aesthet Surg 2008 61 : 839 41.
59. Abai B, Thayer D, Glat PM. The use of a dermal regeneration template (Integra) for acute resurfacing and reconstruction of defects created by excision of giant hairy nevi. Plast Reconstr Surg 2004 114 : 162 8.
60. Wilensky JS, Rosenthal AH, Bradford CR, Rees RS. The use of a bovine collagen construct for reconstruction of full-thickness scalp defects in the elderly patient with cutaneous malignancy. Ann Plast Surg 2005 54 : 297 301. (Pubitemid 40279481)
61. Ahmed S, Hussein SS, Philp B, Healy C. Use of biologic dressing as a temporary wound dressing in reconstruction of a significant forehead Mohs defect. Dermatol Surg 2006 32 : 765 7.
62. Dagregorio G, Guillet G. Artificial skin as a valuable adjunct to surgical treatment of a large squamous cell carcinoma in a patient with epidermolysis bullosa. Dermatol Surg 2005 31 : 474 6.
63. Dermagraft manufacturer (Advanced Biohealing Inc.) website : [accessed June 20, 2008].
64. Hansbrough JF, Dore C, Hansbrough WB. Clinical trials of a living dermal tissue replacement placed beneath meshed, split-thickness skin grafts on excised burn wounds. J Burn Care Rehabil 1992 13 : 519 29.
65. Omar AA, Mavor AI, Homer-Vanniasinkam S. Evaluation of dermagraft as an alternative to grafting for open fasciotomy wounds. J Wound Care 2002 11 : 96 7.
66. Charles CA, Kato T, Tzakis AG, et al. Use of a living dermal equivalent for a refractory abdominal defect after pediatric multivisceral transplantation. Dermatol Surg 2004 30 : 1236 40.
67. Phillips TJ, Manzoor J, Rojas A, et al. The longevity of a bilayered skin substitute after application to venous ulcers. Arch Dermatol 2002 138 : 1079 81.
68. Omar AA, Mavor AID, Jones AM, Homer-Vanniasinkam S. Treatment of venous leg ulcers with Dermagraft. Eur J Vasc Endovasc Surg 2004 27 : 666 72.
69. 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 36.
70. Achauer BM, VanderKam VM, Celikoz B, Jacobson DG. Augmentation of facial soft-tissue defects with Alloderm dermal graft. Ann Plast Surg 1998 41 : 503 7.
71. Sinha UK, Saadat D, Doherty CM, Rice DH. Use of Alloderm inplant to prevent Frey syndrome after parotidectomy. Arch Facial Plast Surg 2003 5 : 109 12.
72. Govindaraj S, Cohen M, Genden EM, et al. The use of acellular dermis in the prevention of Frey's syndrome. Laryngoscope 2001 111 : 1993 8.
73. Simman R, Priebe CJ, Simon M. Reconstruction of aplasia cutis congenita of the trunk of a newborn infant using acellular allogenic dermal graft and cultured epithelial autografts. Ann Plast Surg 2000 44 : 451 4.
74. Rowe NM, Morris L, Delacure MD. Acellular dermal composite allografts for reconstruction of the radial forearm donor site. Ann Plast Surg 2006 57 : 305 11.
75. Ehrenreich M, Ruszczak Z. Update on dermal substitutes. Acta Dermatoven Croat 2006 14 : 172 87.
76. Purdue GF, Hunt JL, Still JM, et al. A multicenter 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 7.
77. Davis DA, Arpey CJ. Porcine heterografts in dermatologic surgery and reconstruction. Dermatol Surg 2000 26 : 76 80. (Pubitemid 30039243)
78. Brennen Medical (EZ Derm) product information; personal communication.
79. Ledgerwood AM, Lucas CE. Massive thigh injuries with vascular disruption. Role of porcine skin grafting of exposed arterial vein grafts. Arch Surg 1973 107 : 201 5.
80. Jozsef B, Jozsef S II., Mihaly D, et al. Pig skin xenograft in burns. I. Technology, laboratory studies. II. Clinical experience. Magy Traumatol Orthop Helyreallito Seb 1976 19 : 138 45.
81. Still J, Law E, Craft-Coffman B. An evaluation of excision with application of autografts or porcine xenografts within 24 hours of burn injury. Ann Plast Surg 1996 36 : 176 9.
82. Ersek R, Hachen H. Porcine xenografts in the treatment of pressure ulcers. Ann Plast Surg 1980 5 : 464.
83. Elleby DH, Weil LS, Sorto LA, Smith SD. The use of porcine xenografts on nail beds following total nail avulsion and phenol chemomatrixectomy. J Foot Surg 1977 16 : 85 91.
84. Gould DJ, Condon P, Cunliffe WJ. Porcine dermis dressings in epidermolysis bullosa. Arch Dermatol 1977 113 : 1456.
85. Breach NM, Davies DM, Yiacoumettis A. Study of effects of porcine skin and bovine dermis on the healing of split-skin graft donor sites in humans. Plast Reconstr Surg 1979 63 : 546 9.
86. Vanstraelen P. Comparison of calcium sodium alginate (KALTOSTAT) and porcine xenograft (E-Z DERM) in the healing of split-thickness skin graft donor sites. Burns 1992 18 : 145 8.
87. Mostow EN, Haraway GD, Dalsing M, et al. 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 43.
88. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of colonies from single cells. Cell 1975 6 : 331 4.
89. Green H, Kehinde O, Thomas J. Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc Natl Acad Sci USA 1979 76 : 5665 8.
90. Limova M, Mauro T. Treatment of pyoderma gangrenosum with cultured keratinocyte autografts. J Dermatol Surg Oncol 1994 20 : 833 6.
91. Wollina U, Konrad H, Fischer T. Recessive epidermolysis bullosa dystrophicans (Hallopeau-Siemens)-improvement of wound healing by autologous epidermal grafts on an esterified hyaluronic acid membrane. J Dermatol 2001 28 : 217 20.
92. Carter DM, Lin AN, Varghese MC, et al. Treatment of junctional epidermolysis bullosa with epidermal autografts. J Am Acad Dermatol 1987 17 : 246 50.
93. Yanaba K, Ito M, Sasaki H, et al. A case of febrile ulceronecrotic Mucha-Habermann disease requiring debridement of necrotic skin and epidermal autograft. Br J Dermatol 2002 147 : 1249 53.
94. Limat A, French LE, Blai L, et al. Organotypic cultures of autologous hair follicle keratinocytes for the treatment of recurrent leg ulcers. J Am Acad Dermatol 2003 48 : 207 14.
95. Poskitt KR, James AH, Lloyd-Davies ERV, et al. Pinch skin grafting or porcine dermis in venous ulcers: a randomized clinical trial. BMJ 1987 294 : 674 6.
96. Carsin H, Ainaud P, Bever HL, et al. Cultured epithelial autografts in extensive burn coverage of severly traumatized patients: a five year single-center experience with 30 patients. Burns 2000 26 : 379 87.
97. Tausche A-K, Skaria M, Bohlen L, et al. An autologous epidermal equivalent tissue-engineered from follicular outer root sheath keratinocytes is as effective as split-thickness skin autograft in recalcitrant vascular leg ulcers. Wound Rep Regen 2003 11 : 248 52.
98. Hefton JM, Madden MR, Finkelstein JL, Shires TG. Grafting of burn patients with allografts of cultured epidermal cells. Lancet 1983 2 : 428 30.
99. Brain A, Purkis P, Coates P, et al. Survival of cultured allogeneic keratinocytes transplanted to dermal bed assessed with probe specific for Y chromosome. Br Med J 1989 298 : 917 9.
100. Burt AM, Pallet CD, Sloane JP. Survival of cultured allografts in patients with burns assessed with probe specific for Y chromosome. Br Med J 1989 298 : 915 7.
101. Roseeuw DI, De Coninck A, Lissens W, et al. Allogeneic cultured epidermal grafts heal chronic ulcers although they do not remain as proved by DNA analysis. J Dermatol Sci 1990 1 : 245 52.
102. Phillips TJ, Bhawan J, Leigh IM, et al. Cultured epidermal autografts and allografts: a study of differentiation and allograft survival. J Am Acad Dermatol 1990 23 : 189 98.
103. Duinslaeger L, Verbeken G, Reper P, et al. Lyophilized keratinocyte cell lysates contain multiple mitogenic activities and stimulate closure of meshed skin autograft-covered burn wounds with efficiency similar to that of fresh allogeneic keratinocyte cultures. Plast Reconstr Surg 1996 98 : 110.
104. McKay IA, Leigh IM. Epidermal cytokines and their roles in cutaneous wound healing. Br J Dermatol 1991 124 : 513 8.
105. Eisenberg M, Llewellyn DM, Moran K, Kerr A. Successful engraftment of cultured human epidermal allograft in a child with recessive dystrophic epidermolysis bullosa. Med J Aust 1987 147 : 520 1.
106. Bolivar-Flores YJ, Kuri-Harcuch W. Frozen allogeneic human epidermal cultured sheets for the cure of complicated leg ulcers. Dermatol Surg 1999 25 : 610 7.
107. Teepe RG, Kreis RW, Koebrugge EJ, et al. The use of cultured autologous epidermis in the treatment of extensive burn wound. J Trauma 1990 30 : 269 75.
108. Phillips TJ, Provan A, Colbert D, Easley KW. A randomized single-blinded controlled study of cultured epidermal allografts in the treatment of split-thickness skin graft donor sites. Arch Dermatol 1993 129 : 879 92.
109. Navratilova Z, Slonkova V, Semradova V, Adler J. Cryopreserved and lyophilized cultured epidermal allografts in the treatment of leg ulcers: a pilot study. J Eur Acad Deramtol Venereol 2004 18 : 173 9.