A review of tissue-engineered skin bioconstructs available for skin reconstruction

Situations where normal autografts cannot be used to replace damaged skin often lead to a greater risk of mortality, prolonged hospital stay and increased expenditure for the National Health Service. There is a substantial need for tissue-engineered skin bioconstructs and research is active in this field. Significant progress has been made over the years in the development and clinical use of bioengineered components of the various skin layers. Off-the-shelf availability of such constructs, or production of sufficient quantities of biological materials to aid rapid wound closure, are often the only means to help patients with major skin loss. The aim of this review is to describe those materials already commercially available for clinical use as well as to give a short insight to those under development. It seeks to provide skin scientists/tissue engineers with the information required to not only develop in vitro models of skin, but to move closer to achieving the ultimate goal of an off-the-shelf, complete full-thickness skin replacement.

[1]  JOHN F. BURKE,et al.  Successful Use of a Physiologically Acceptable Artificial Skin in the Treatment of Extensive Burn Injury , 1981, Annals of surgery.

[2]  H. Carsin,et al.  Cultured epithelial autografts in extensive burn coverage of severely traumatized patients: a five year single-center experience with 30 patients. , 2000, Burns : journal of the International Society for Burn Injuries.

[3]  Peter X Ma,et al.  Biomimetic materials for tissue engineering. , 2008, Advanced drug delivery reviews.

[4]  S. Homer-Vanniasinkam,et al.  Treatment of venous leg ulcers with Dermagraft. , 2004, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[5]  S. MacNeil,et al.  Fibroblasts play a regulatory role in the control of pigmentation in reconstructed human skin from skin types I and II. , 2002, Pigment cell research.

[6]  L. Kamolz,et al.  First experiences with the collagen-elastin matrix Matriderm as a dermal substitute in severe burn injuries of the hand. , 2007, Burns : journal of the International Society for Burn Injuries.

[7]  M. Dentini,et al.  Comparative chemical evaluation of two commercially available derivatives of hyaluronic acid (Hylaform® from rooster combs and Restylane® from streptococcus) used for soft tissue augmentation , 1999, Journal of the European Academy of Dermatology and Venereology : JEADV.

[8]  R. Sheridan,et al.  Skin substitutes in burns. , 1999, Burns : journal of the International Society for Burn Injuries.

[9]  J. Raffetto Effectiveness of an extracellular matrix graft (OASIS Wound Matrix) in the treatment of chronic leg ulcers: A randomized clinical trial , 2007 .

[10]  T. Tumbar Epithelial skin stem cells. , 2006, Methods in enzymology.

[11]  M Helen Grant,et al.  The mechanical strength of collagen gels containing glycosaminoglycans and populated with fibroblasts. , 2009, Journal of biomedical materials research. Part A.

[12]  S. Badylak,et al.  Porcine small intestinal submucosa (SIS): a bioscaffold supporting in vitro primary human epidermal cell differentiation and synthesis of basement membrane proteins. , 2001, Burns : journal of the International Society for Burn Injuries.

[13]  K. Newman,et al.  The use of a bioactive skin substitute decreases length of stay for pediatric burn patients. , 2001, Journal of pediatric surgery.

[14]  W. Fitzgerald,et al.  Isolation and Clonal Analysis of Human Epidermal Keratinocyte Stem Cells in Long‐Term Culture , 2003, Stem cells.

[15]  D L Chester,et al.  A review of keratinocyte delivery to the wound bed. , 2004, The Journal of burn care & rehabilitation.

[16]  N. Pallua,et al.  Update on the use of collagen/glycosaminoglycate skin substitute-six years of experiences with artificial skin in 15 German burn centers. , 2004, Burns : journal of the International Society for Burn Injuries.

[17]  M. Ferguson,et al.  Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration , 2007, Journal of The Royal Society Interface.

[18]  T. Cubison,et al.  Evidence for the link between healing time and the development of hypertrophic scars (HTS) in paediatric burns due to scald injury. , 2006, Burns : journal of the International Society for Burn Injuries.

[19]  C C Compton,et al.  Vascularized Collagen‐Glycosaminoglycan Matrix Provides a Dermal Substrate and Improves Take of Cultured Epithelial Autografts , 1998, Plastic and reconstructive surgery.

[20]  B. Hull,et al.  ACCEPTANCE OF ALLOGENEIC FIBROBLASTS IN SKIN EQUIVALENT TRANSPLANTS , 1983, Transplantation.

[21]  J. Still,et al.  The use of a collagen sponge/living cell composite material to treat donor sites in burn patients. , 2003, Burns : journal of the International Society for Burn Injuries.

[22]  J. Converse,et al.  Inosculation of vessels of skin graft and host bed: a fortuitous encounter. , 1975, British journal of plastic surgery.

[23]  M. Sabolinski,et al.  The effect of a tissue engineered bilayered living skin analog, over meshed split-thickness autografts on the healing of excised burn wounds. The Apligraf Burn Study Group. , 2000, Burns : journal of the International Society for Burn Injuries.

[24]  Sheila MacNeil,et al.  Plasma polymer coated surfaces for serum-free culture of limbal epithelium for ocular surface disease , 2007, Journal of materials science. Materials in medicine.

[25]  I. Yannas Similarities and differences between induced organ regeneration in adults and early foetal regeneration , 2005, Journal of The Royal Society Interface.

[26]  C. Tsai,et al.  The use of composite acellular allodermis-ultrathin autograft on joint area in major burn patients--one year follow-up. , 1999, The Kaohsiung journal of medical sciences.

[27]  O. Damour,et al.  Evolutive skin reconstructions: from the dermal collagen-glycosaminoglycan-chitosane substrate to an immunocompetent reconstructed skin. , 2006, Bio-medical materials and engineering.

[28]  Biaxial failure properties of planar living tissue equivalents. , 2005, Journal of biomedical materials research. Part A.

[29]  L. Ansaloni,et al.  Use of porcine dermal collagen graft (Permacol) for hernia repair in contaminated fields , 2007, Hernia.

[30]  P. Clugston,et al.  Cultured epithelial autograft: five years of clinical experience with twenty-eight patients. , 1995, The Journal of trauma.

[31]  B. Bay,et al.  Evaluation of electrospun PCL/gelatin nanofibrous scaffold for wound healing and layered dermal reconstitution. , 2007, Acta biomaterialia.

[32]  S. Boyce,et al.  Engineered human skin fabricated using electrospun collagen-PCL blends: morphogenesis and mechanical properties. , 2009, Tissue engineering. Part A.

[33]  P E Allaire,et al.  Practical applications of skin biomechanics. , 1977, Clinics in plastic surgery.

[34]  Y. Barrandon,et al.  LONG-TERM REGENERATION OF HUMAN EPIDERMIS ON THIRD DEGREE BURNS TRANSPLANTED WITH AUTOLOGOUS CULTURED EPITHELIUM GROWN ON A FIBRIN MATRIX1,2 , 2000, Transplantation.

[35]  S. MacNeil,et al.  Enhancement of keratinocyte performance in the production of tissue‐engineered skin using a low‐calcium medium , 2007, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[36]  C. Compton,et al.  Permanent Coverage of Large Burn Wounds with Autologous Cultured Human Epithelium , 1984 .

[37]  J. Riesle,et al.  Static and dynamic fibroblast seeding and cultivation in porous PEO/PBT scaffolds , 1999, Journal of materials science. Materials in medicine.

[38]  K. Bessho,et al.  The use of a new bilayer artificial dermis for vestibular extension. , 1998, The British journal of oral & maxillofacial surgery.

[39]  R. M. Warner,et al.  Treatment of burns and chronic wounds using a new cell transfer dressing for delivery of autologous keratinocytes , 2005, European Journal of Plastic Surgery.

[40]  W. Marston,et al.  The efficacy and safety of Dermagraft in improving the healing of chronic diabetic foot ulcers: results of a prospective randomized trial. , 2003, Diabetes care.

[41]  K. Woodhouse,et al.  Characterization of biodegradable polyurethane microfibers for tissue engineering , 2007, Journal of biomaterials science. Polymer edition.

[42]  C. Williams Treatment of venous leg ulcers: 1. , 1996, British journal of nursing.

[43]  H. Green,et al.  Seria cultivation of strains of human epidemal keratinocytes: the formation keratinizin colonies from single cell is , 1975, Cell.

[44]  K. V. Van Vliet,et al.  Probing mechanical properties of fully hydrated gels and biological tissues. , 2008, Journal of biomechanics.

[45]  E. Fuchs,et al.  Defining the Epithelial Stem Cell Niche in Skin , 2004, Science.

[46]  R. Goss,et al.  Epimorphic vs. tissue regeneration in Xenopus forelimbs. , 1992, The Journal of experimental zoology.

[47]  Sheila MacNeil,et al.  Progress and opportunities for tissue-engineered skin , 2007, Nature.

[48]  Z Ruszczak,et al.  Update on tissue-engineered biological dressings. , 2006, Tissue engineering.

[49]  A. Sadikot,et al.  Isolation of multipotent adult stem cells from the dermis of mammalian skin , 2001, Nature Cell Biology.

[50]  D. Salomon,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 , 2003, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[51]  Seeram Ramakrishna,et al.  In vitro culture of human dermal fibroblasts on electrospun polycaprolactone collagen nanofibrous membrane. , 2006, Artificial organs.

[52]  C. Baird,et al.  The pilot study. , 2000, Orthopedic nursing.

[53]  Penny A. Johnson,et al.  Integration and persistence of an investigational human living skin equivalent (ICX-SKN) in human surgical wounds. , 2007, Regenerative medicine.

[54]  P. Fratino,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. , 2003, Diabetes care.

[55]  H. Cleland,et al.  Bioengineered skin substitutes for the management of burns: a systematic review. , 2007, Burns : journal of the International Society for Burn Injuries.

[56]  S. Lal,et al.  Biobrane improves wound healing in burned children without increased risk of infection. , 2000, Shock.

[57]  K. Ghosh,et al.  Tissue engineering for cutaneous wounds. , 2007, The Journal of investigative dermatology.

[58]  C. Compton,et al.  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. , 1989, Laboratory investigation; a journal of technical methods and pathology.

[59]  A. Hirano,et al.  Lower extremity reconstruction after necrotising fasciitis and necrotic skin lesions using a porcine-derived skin substitute. , 2006, Journal of plastic, reconstructive & aesthetic surgery : JPRAS.

[60]  Jie Li,et al.  Pathophysiology of acute wound healing. , 2007, Clinics in dermatology.

[61]  H O Ho,et al.  Characterization of collagen gel solutions and collagen matrices for cell culture. , 2001, Biomaterials.

[62]  S. Inokuchi,et al.  An in vivo model of human skin acute graft-versus-host disease: transplantation of cultured human epidermal cells and dermal fibroblasts with human lymphocytes into SCID mice. , 1999, Experimental hematology.

[63]  D. Billmire,et al.  Skin resurfacing for the burned patient. , 2002, Clinics in plastic surgery.

[64]  Anubhav Tripathi,et al.  Viscoelastic response of human skin to low magnitude physiologically relevant shear. , 2008, Journal of biomechanics.

[65]  M. Auletta,et al.  Acute excisional wounds treated with a tissue-engineered skin (Apligraf). , 1999, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[66]  Sheila MacNeil,et al.  Clinical experience using cultured epithelial autografts leads to an alternative methodology for transferring skin cells from the laboratory to the patient. , 2006, Regenerative medicine.

[67]  S. E. James,et al.  Upward migration of cultured autologous keratinocytes in Integra™ artificial skin: a preliminary report , 2003, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[68]  S. Boyce,et al.  EDC cross-linking improves skin substitute strength and stability. , 2006, Biomaterials.

[69]  A. Condurache,et al.  VEGF(165) and bFGF protein-based therapy in a slow release system to improve angiogenesis in a bioartificial dermal substitute in vitro and in vivo. , 2007, Langenbeck's archives of surgery (Print).

[70]  E. Doolin,et al.  In vitro bioartificial skin culture model of tissue rejection and inflammatory/immune mechanisms. , 1997, Transplantation proceedings.

[71]  S. Carreirão,et al.  Subcutaneous Mastectomy and Immediate Breast Reconstruction by Local Dermofat Flap , 1979, Annals of plastic surgery.

[72]  Yi-Wen Chen,et al.  Composite nano-titanium oxide-chitosan artificial skin exhibits strong wound-healing effect-an approach with anti-inflammatory and bactericidal kinetics. , 2008, Macromolecular bioscience.

[73]  Xiaoyan Yuan,et al.  Hybrid nanofibrous membranes of PLGA/chitosan fabricated via an electrospinning array. , 2007, Journal of biomedical materials research. Part A.

[74]  P. Kelemen,et al.  Subcutaneous mastectomy and immediate reconstruction for prevention of breast cancer for high-risk patients , 2008, Breast cancer.

[75]  A study of mortality in a burns unit: a revised estimate. , 1954 .

[76]  B. Atiyeh,et al.  Cultured epithelial autograft (CEA) in burn treatment: three decades later. , 2007, Burns : journal of the International Society for Burn Injuries.

[77]  B. Atiyeh,et al.  New technologies for burn wound closure and healing--review of the literature. , 2005, Burns : journal of the International Society for Burn Injuries.

[78]  Elaine Fuchs,et al.  Self-Renewal, Multipotency, and the Existence of Two Cell Populations within an Epithelial Stem Cell Niche , 2004, Cell.

[79]  L. French,et al.  Organotypic cultures of autologous hair follicle keratinocytes for the treatment of recurrent leg ulcers. , 2003, Journal of the American Academy of Dermatology.

[80]  Fiona M Wood,et al.  The use of a non-cultured autologous cell suspension and Integra dermal regeneration template to repair full-thickness skin wounds in a porcine model: a one-step process. , 2007, Burns : journal of the International Society for Burn Injuries.

[81]  M. Schurr,et al.  Clinical experience with Alloderm: a one-staged composite dermal/epidermal replacement utilizing processed cadaver dermis and thin autografts. , 2006, Burns : journal of the International Society for Burn Injuries.

[82]  S. E. James,et al.  A comparison of keratinocyte cell sprays with and without fibrin glue. , 2003, Burns : journal of the International Society for Burn Injuries.

[83]  S. Badylak,et al.  Small Intestinal Submucosa: Utilization as a Wound Dressing in Full‐Thickness Rodent Wounds , 1995, Annals of plastic surgery.

[84]  I. Leigh,et al.  The Role of Allogenic Fibroblasts in an Acute Wound Healing Model , 2004, Plastic and reconstructive surgery.

[85]  Ravi Shankar,et al.  Norepinephrine modulates the inflammatory and proliferative phases of wound healing. , 2006, The Journal of trauma.

[86]  Remo Papini,et al.  Management of burn injuries of various depths , 2004, BMJ : British Medical Journal.

[87]  S. Bryant,et al.  Molecular mechanisms in the control of limb regeneration: the role of homeobox genes. , 1996, The International journal of developmental biology.

[88]  A. Metcalfe,et al.  Bioengineering skin using mechanisms of regeneration and repair. , 2007, Biomaterials.

[89]  P. Andrades,et al.  Utilization of Human Cadaveric Acellular Dermis for Abdominal Hernia Reconstruction , 2007, Annals of plastic surgery.

[90]  C. Song,et al.  Use of skin allograft and its donation rate in Singapore: an 11-year retrospective review for burns treatment. , 2007, Transplantation proceedings.

[91]  Ulrich Kneser,et al.  Tissue engineering of cultured skin substitutes , 2005, Journal of cellular and molecular medicine.

[92]  D. W. Hayes,et al.  Full-thickness burn of the foot: successful treatment with Apligraf. A case report. , 2001, Clinics in podiatric medicine and surgery.

[93]  M. Ponec,et al.  Endothelial network formed with human dermal microvascular endothelial cells in autologous multicellular skin substitutes , 2004, Angiogenesis.

[94]  P. Nielsen,et al.  Estimating material parameters of human skin in vivo , 2009, Biomechanics and modeling in mechanobiology.

[95]  M. Nozaki,et al.  Novel application method of artificial dermis: one-step grafting procedure of artificial dermis and skin, rat experimental study. , 2006, Burns : journal of the International Society for Burn Injuries.

[96]  S. E. James,et al.  Use of a novel porcine collagen paste as a dermal substitute in full‐thickness wounds , 2008, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[97]  M. Abbas,et al.  Combined Endorectal Advancement Flap with Alloderm® Graft Repair of Radiation and Cryoablation-Induced Rectourethral Fistula , 2008, The American surgeon.

[98]  S. Myers,et al.  The development of novel dermal matrices for cutaneous wound repair , 2006 .

[99]  Wei Liu,et al.  Collagen Tissue Engineering: Development of Novel Biomaterials and Applications , 2008, Pediatric Research.

[100]  J. Burke,et al.  Primary excision and immediate wound closure , 2005, Intensive Care Medicine.

[101]  Glenn Silverstein Dermal regeneration template in the surgical management of diabetic foot ulcers: a series of five cases. , 2006, The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons.

[102]  R. Cortivo,et al.  In vitro reconstruction of an endothelialized skin substitute provided with a microcapillary network using biopolymer scaffolds , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[103]  D. Supp,et al.  Engineered skin substitutes: practices and potentials. , 2005, Clinics in dermatology.

[104]  C. Legrand,et al.  Tissue engineering for full-thickness burns: a dermal substitute from bench to bedside. , 2007, Biochemical and biophysical research communications.

[105]  Tazelaar Dj [Treatment of venous leg ulcers]. , 2003, Nederlands tijdschrift voor geneeskunde.

[106]  E. Eriksson,et al.  Basement membrane formation during wound healing is dependent on epidermal transplants. , 2001, Plastic and reconstructive surgery.

[107]  S. Khariwala,et al.  Temporomandibular joint reconstruction using a vascularized bone graft with Alloderm. , 2007 .

[108]  Paul Martin,et al.  Inflammatory cells during wound repair: the good, the bad and the ugly. , 2005, Trends in cell biology.

[109]  F. Ashoori,et al.  Long-term follow-up study of artificial dermis composed of outer silicone layer and inner collagen sponge. , 2000, British journal of plastic surgery.

[110]  L. Marrot,et al.  An in vitro strategy to evaluate the phototoxicity of solar UV at the molecular and cellular level: application to photoprotection assessment. , 1998, European journal of dermatology : EJD.

[111]  Yann Barrandon,et al.  Location of stem cells of human hair follicles by clonal analysis , 1994, Cell.

[112]  Stephen A. Brigido,et al.  The use of an acellular dermal regenerative tissue matrix in the treatment of lower extremity wounds: a prospective 16‐week pilot study , 2006, International wound journal.

[113]  S. O'Kane,et al.  Transforming growth factor βs and wound healing , 1997 .

[114]  J. Frizzi,et al.  Porcine dermal collagen (Permacol) for abdominal wall reconstruction. , 2006, Current surgery.

[115]  D. Roh,et al.  Wound healing effect of silk fibroin/alginate-blended sponge in full thickness skin defect of rat , 2006, Journal of materials science. Materials in medicine.

[116]  J. Lagarde,et al.  Model of the viscoelastic behaviour of skin in vivo and study of anisotropy , 2004, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[117]  S. Landis Chronic wound infection and antimicrobial use. , 2008, Advances in skin & wound care.

[118]  John P Fisher,et al.  Biomaterial Scaffolds in Pediatric Tissue Engineering , 2008, Pediatric Research.

[119]  P. Sarathchandra,et al.  The diamond CO2 laser as a method of improving the vascularisation of a permanent collagen implant. , 2004, Burns : journal of the International Society for Burn Injuries.

[120]  A. Shelton,et al.  Transperineal Repair of Persistent Rectovaginal Fistulas Using an Acellular Cadaveric Dermal Graft (AlloDerm®) , 2006, Diseases of the colon and rectum.

[121]  H. G. Vogel,et al.  Age dependence of mechanical and biochemical properties of human skin. I: Stress-strain experiments, skin thickness and biochemical analysis , 1987 .

[122]  S. MacNeil,et al.  A new autologous keratinocyte dressing treatment for non‐healing diabetic neuropathic foot ulcers , 2004, Diabetic medicine : a journal of the British Diabetic Association.

[123]  C. V. van Blitterswijk,et al.  The use of PEGT/PBT as a dermal scaffold for skin tissue engineering. , 2004, Biomaterials.

[124]  W. Eaglstein,et al.  Tissue engineering for skin: an update. , 1998, Journal of the American Academy of Dermatology.

[125]  H. Iioka,et al.  Usefulness and Limitations of Artificial Dermis Implantation for Posttraumatic Deformity , 2002, Aesthetic Plastic Surgery.

[126]  P. Humbert,et al.  Human bone marrow‐derived cells: An attractive source to populate dermal substitutes , 2008, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[127]  Paul Gatenholm,et al.  In vivo biocompatibility of bacterial cellulose. , 2006, Journal of biomedical materials research. Part A.

[128]  George P McCabe,et al.  Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. , 2006, The Journal of bone and joint surgery. American volume.

[129]  Yoshimitsu Kuroyanagi,et al.  Design of artificial skin , 1996 .

[130]  F. Wood,et al.  The use of cultured epithelial autograft in the treatment of major burn injuries: a critical review of the literature. , 2006, Burns : journal of the International Society for Burn Injuries.

[131]  T. Rice,et al.  Closure of a large tracheoesophageal fistula using AlloDerm. , 2008, The Journal of thoracic and cardiovascular surgery.

[132]  R. Price,et al.  Survival of Apligraf in acute human wounds. , 2004, Tissue engineering.

[133]  C. Jahoda Cell movement in the hair follicle dermis - more than a two-way street? , 2003, The Journal of investigative dermatology.

[134]  L. Dubertret,et al.  Advantage of the Presence of Living Dermal Fibroblasts within in Vitro Reconstructed Skin for Grafting in Humans , 1998, Plastic and reconstructive surgery.

[135]  I. Leigh,et al.  A comparison of tissue-engineered hyaluronic acid dermal matrices in a human wound model. , 2006, Tissue engineering.

[136]  Alessandra Pavesio,et al.  Epidermal homeostasis in long-term scaffold-enforced skin equivalents. , 2006, The journal of investigative dermatology. Symposium proceedings.

[137]  C. Green,et al.  Histological evaluation of Permacol as a subcutaneous implant over a 20-week period in the rat model. , 2005, British journal of plastic surgery.

[138]  S. Y. Kim,et al.  The effects of Pva/chitosan/fibroin (PCF)-blended spongy sheets on wound healing in rats. , 2000, Biological & pharmaceutical bulletin.

[139]  H. Navsaria,et al.  Hyaluronic acid: the scientific and clinical evidence. , 2007, Journal of plastic, reconstructive & aesthetic surgery : JPRAS.

[140]  Scott J Hollister,et al.  Non-invasive monitoring of tissue scaffold degradation using ultrasound elasticity imaging. , 2008, Acta biomaterialia.

[141]  H. Lorenz,et al.  Scarless skin wound repair in the fetus. , 1993, The Western journal of medicine.

[142]  K. Billiar,et al.  Biomechanical and biochemical characteristics of a human fibroblast-produced and remodeled matrix. , 2007, Biomaterials.

[143]  G. Abatangelo,et al.  Autologous skin grafting in the treatment of severe scleroderma cutaneous ulcers: a case report. , 2003, Rheumatology.

[144]  M. Rosen,et al.  Staged repair of massive incisional hernias with loss of abdominal domain: a novel approach. , 2008, American journal of surgery.

[145]  P. V. van Zuijlen,et al.  Graft Survival and Effectiveness of Dermal Substitution in Burns and Reconstructive Surgery in a One-Stage Grafting Model , 2000, Plastic and reconstructive surgery.

[146]  M. Ray,et al.  Basement membrane zone. , 1996, Clinics in dermatology.

[147]  L. Prantl,et al.  Suprathel, a New Skin Substitute, in the Management of Partial-Thickness Burn Wounds: Results of a Clinical Study , 2008, Annals of plastic surgery.

[148]  Glenn D Prestwich,et al.  Fibronectin functional domains coupled to hyaluronan stimulate adult human dermal fibroblast responses critical for wound healing. , 2006, Tissue engineering.

[149]  L. Uccioli A Clinical Investigation on the Characteristics and Outcomes of Treating Chronic Lower Extremity Wounds using the TissueTech Autograft System , 2003, The international journal of lower extremity wounds.

[150]  I. Yannas,et al.  Design of an artificial skin. I. Basic design principles. , 1980, Journal of biomedical materials research.

[151]  R Marks,et al.  Evaluation of biomechanical properties of human skin. , 1995, Clinics in dermatology.

[152]  Peter G Shakespeare,et al.  The role of skin substitutes in the treatment of burn injuries. , 2005, Clinics in dermatology.

[153]  J. Burke,et al.  Primary excision and prompt grafting as routine therapy for the treatment of thermal burns in children. , 1976, The Surgical clinics of North America.

[154]  R. White,et al.  Topical antimicrobials in the control of wound bioburden. , 2006, Ostomy/wound management.

[155]  M. Ramos‐e‐Silva,et al.  New dressings, including tissue-engineered living skin. , 2002, Clinics in dermatology.

[156]  D. Foreman,et al.  Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring. , 1995, Journal of cell science.

[157]  R. Clark Biology of dermal wound repair. , 1993, Dermatologic clinics.

[158]  Sante Tura,et al.  Stem cell plasticity: time for a reappraisal? , 2005, Haematologica.

[159]  Giovanni Vozzi,et al.  Biomimetic materials for tissue engineering through enzyme mediated protein modification , 2007 .

[160]  Antonio Giordano,et al.  Smart materials as scaffolds for tissue engineering , 2005, Journal of cellular physiology.

[161]  B. Woodward,et al.  The use of cultured autologous keratinocytes with integra in the resurfacing of acute burns. , 1998, Plastic and reconstructive surgery.

[162]  M. N. Khan,et al.  Antiseptics, iodine, povidone iodine and traumatic wound cleansing. , 2006, Journal of tissue viability.

[163]  M. Serra,et al.  Predictors of morbidity and mortality after the first episode of upper gastrointestinal bleeding in liver cirrhosis. , 2000, Journal of hepatology.

[164]  J. Patton,et al.  Use of human acellular dermal matrix in complex and contaminated abdominal wall reconstructions. , 2007, American journal of surgery.

[165]  R. Martin,et al.  A guide to biological skin substitutes. , 2002, British journal of plastic surgery.

[166]  J. Gerlach,et al.  Culture of subconfluent human fibroblasts and keratinocytes using biodegradable transfer membranes. , 2008, Burns : journal of the International Society for Burn Injuries.

[167]  T. Zwingers,et al.  Treatment of recalcitrant venous leg ulcers with autologous keratinocytes in fibrin sealant: A multinational randomized controlled clinical trial , 2007, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[168]  A. Badikova,et al.  Morphological Changes in Burn Wounds after Transplantation of Allogenic Fibroblasts , 2004, Bulletin of Experimental Biology and Medicine.

[169]  I. Yannas,et al.  Organized skin structure is regenerated in vivo from collagen-GAG matrices seeded with autologous keratinocytes. , 1998, The Journal of investigative dermatology.

[170]  P. Violas,et al.  Integra artificial skin in the management of severe tissue defects, including bone exposure, in injured children , 2005, Journal of pediatric orthopedics. Part B.

[171]  Jong-wook Lee,et al.  Use of the Artificial Dermis for Free Radial Forearm Flap Donor Site , 2005, Annals of plastic surgery.

[172]  William L Hickerson,et al.  Multicenter postapproval clinical trial of Integra dermal regeneration template for burn treatment. , 2003, The Journal of burn care & rehabilitation.

[173]  T. Yoshikawa,et al.  Wound Therapy by Marrow Mesenchymal Cell Transplantation , 2008, Plastic and reconstructive surgery.

[174]  I. Whitaker,et al.  A Critical Evaluation of the Use of Biobrane as a Biologic Skin Substitute: A Versatile Tool for the Plastic and Reconstructive Surgeon , 2008, Annals of plastic surgery.

[175]  P. Hebda,et al.  Impact of transplanted fibroblasts on rabbit skin wounds. , 2003, Archives of otolaryngology--head & neck surgery.

[176]  H Green,et al.  Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. , 1975, Cell.

[177]  Treating severe psoriasis: how to navigate safely between scylla and charybdis? , 2003, The Journal of investigative dermatology.

[178]  J. Hansbrough,et al.  Clinical trials of a living dermal tissue replacement placed beneath meshed, split-thickness skin grafts on excised burn wounds. , 1992, The Journal of burn care & rehabilitation.

[179]  C. Layton,et al.  Use of an in vitro model of tissue‐engineered human skin to study keratinocyte attachment and migration in the process of reepithelialization , 2006, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[180]  G. Gravante,et al.  The Use of Hyalomatrix PA in the Treatment of Deep Partial-Thickness Burns , 2007, Journal of burn care & research : official publication of the American Burn Association.

[181]  J. Boorman,et al.  Comparison of E-Z Derm and Jelonet dressings for partial skin thickness burns. , 1989, Burns, including thermal injury.

[182]  S. Matsushita,et al.  Counter-antigen presentation: fibroblasts produce cytokines by signalling through HLA class II molecules without inducing T-cell proliferation. , 2002, Cytokine.

[183]  C. Soranzo,et al.  Hyalomatrix: a temporary epidermal barrier, hyaluronan delivery, and neodermis induction system for keratinocyte stem cell therapy. , 2007, Tissue engineering.

[184]  P. Lam,et al.  Development and evaluation of a new composite Laserskin graft. , 1999, The Journal of trauma.

[185]  C. Illingworth,et al.  Trapped fingers and amputated finger tips in children. , 1974, Journal of pediatric surgery.

[186]  H. G. Vogel,et al.  Age dependence of mechanical and biochemical properties of human skin. II: Hysteresis, relaxation, creep and repeated strain experiments , 1987 .

[187]  D. Frankel,et al.  Nanoscale viscoelastic properties of an aligned collagen scaffold , 2009, Journal of materials science. Materials in medicine.

[188]  P. Dziewulski,et al.  Biobrane versus 1% Silver Sulfadiazine in Second‐Degree Pediatric Burns , 2000, Plastic and reconstructive surgery.

[189]  R. Lavker,et al.  Re-epithelialization of porcine skin by the sweat apparatus. , 1998, The Journal of investigative dermatology.

[190]  S. Boyce,et al.  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. , 1999, The Journal of burn care & rehabilitation.

[191]  Y. Barrandon,et al.  Three clonal types of keratinocyte with different capacities for multiplication. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[192]  M. Dalsing,et al.  Effectiveness of an extracellular matrix graft (OASIS Wound Matrix) in the treatment of chronic leg ulcers: a randomized clinical trial. , 2005, Journal of vascular surgery.

[193]  Fang-gang Ning,et al.  Biomechanical properties of four dermal substitutes. , 2007, Chinese medical journal.

[194]  Valerie Horsley,et al.  Epithelial Stem Cells: Turning over New Leaves , 2007, Cell.

[195]  R. Wolfe Mortality differences and speed of wound closure among specialized burn care facilities , 1985 .

[196]  P. Janmey,et al.  Tissue Cells Feel and Respond to the Stiffness of Their Substrate , 2005, Science.

[197]  A. Patwardhan,et al.  Reconstructed human epidermis composed of keratinocytes, melanocytes and Langerhans cells , 1998, Medical and Biological Engineering and Computing.

[198]  L. Gibson,et al.  Mechanical characterization of collagen-glycosaminoglycan scaffolds. , 2007, Acta biomaterialia.

[199]  H. Slavkin,et al.  Prospects for tooth regeneration in the 21st century: A perspective , 2003, Microscopy research and technique.

[200]  L. R. M. Souto,et al.  Model of human epidermis reconstructed in vitro with keratinocytes and melanocytes on dead de-epidermized human dermis. , 2004, Sao Paulo medical journal = Revista paulista de medicina.

[201]  N. Fausto Liver regeneration. , 2000, Journal of hepatology.

[202]  V. Falanga,et al.  The science of wound bed preparation. , 2009, The Surgical clinics of North America.

[203]  C. Jahoda,et al.  Hair follicle stem cells. , 2007, Seminars in cell & developmental biology.

[204]  F. Wood,et al.  The use of cultured epithelial autograft in the treatment of major burn wounds: eleven years of clinical experience. , 2006, Burns : journal of the International Society for Burn Injuries.

[205]  D. Heimbach,et al.  Artificial Dermis for Major Burns: A Multi‐Center Randomized Clinical Trial , 1988, Annals of surgery.

[206]  P. Hebda,et al.  Transplanted fetal fibroblasts: Survival and distribution over time in normal adult dermis compared with autogenic, allogenic, and xenogenic adult fibroblasts , 1999, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[207]  F. A. Navarro,et al.  Sprayed keratinocyte suspensions accelerate epidermal coverage in a porcine microwound model. , 2000, The Journal of burn care & rehabilitation.

[208]  S. O'Kane,et al.  Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[209]  R. Demling Use of Biobrane in management of scalds. , 1995, The Journal of burn care & rehabilitation.

[210]  William H. Eaglstein,et al.  Tissue-Engineered Skin , 2001 .

[211]  A. Utani,et al.  Incorporation of basic fibroblast growth factor into preconfluent cultured skin substitute to accelerate neovascularisation and skin reconstruction after transplantation , 2007, Scandinavian journal of plastic and reconstructive surgery and hand surgery.

[212]  H. Bannasch,et al.  Treatment of therapy-refractive ulcera cruris of various origins with autologous keratinocytes in fibrin sealant. , 2005, VASA. Zeitschrift fur Gefasskrankheiten.

[213]  H. Ryssel,et al.  The use of MatriDerm in early excision and simultaneous autologous skin grafting in burns--a pilot study. , 2008, Burns : journal of the International Society for Burn Injuries.

[214]  D. Vacher Production de feuillets épidermiques autologues pour la thérapie cellulaire cutanée , 2003 .

[215]  W. Jeffcoate,et al.  Randomized, controlled, single-blind study on use of autologous keratinocytes on a transfer dressing to treat nonhealing diabetic ulcers. , 2007, Regenerative medicine.

[216]  N. Fusenig,et al.  Authentic fibroblast matrix in dermal equivalents normalises epidermal histogenesis and dermoepidermal junction in organotypic co-culture. , 2004, European journal of cell biology.

[217]  A. Pandit,et al.  Towards development of a dermal rudiment for enhanced wound healing response. , 2008, Biomaterials.

[218]  P. Gutiérrez,et al.  Cultured epithelial autografts. , 2006, Australian nursing journal.

[219]  Maurizio Biagioli,et al.  Classification and pathophysiology of skin grafts. , 2005, Clinics in dermatology.

[220]  R. Martin,et al.  The co-application of sprayed cultured autologous keratinocytes and autologous fibrin sealant in a porcine wound model. , 2002, British journal of plastic surgery.

[221]  James A. Johnson,et al.  Efficacy of interference screw and double-docking methods using palmaris longus and GraftJacket for medial collateral ligament reconstruction of the elbow. , 2007, Journal of shoulder and elbow surgery.