Evaluation of a bilayered, micropatterned hydrogel dressing for full-thickness wound healing

Experimental Biology and Medicine

Volumn 241, Issue 9, 2016, Pages 986-995

  Magin, Chelsea M ^a   Neale, Dylan B ^b   Drinker, Michael C ^a   Willenberg, Bradley J ^b,c,d   Reddy, Shravanthi T ^a   La Perle, Krista M D ^e   Schultz, Gregory S ^b   Brennan, Anthony B ^a,b,d  

^a Sharklet Technologies   (United States)

^b J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

^c UNIVERSITY OF CENTRAL FLORIDA   (United States)

^d Saisijin Biotech   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f UNIVERSITY OF FLORIDA   (United States)

Author keywords

biomaterials; gelatin; hydrogel; microarchitecture; Micropattern; wound healing

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION ASSAY; CELL VIABILITY; CLINICAL EVALUATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM CELL; EPITHELIZATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROGEL DRESSING; INFLAMMATION; MALE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; RAT; SCANNING ELECTRON MICROSCOPY; TOPOGRAPHY; WOUND HEALING; ANIMAL; BANDAGE; CELL MOTION; CHEMISTRY; CYTOLOGY; KERATINOCYTE; MATERIALS TESTING; SPRAGUE DAWLEY RAT;

BIOMATERIAL;

ANIMALS; BANDAGES; BIOCOMPATIBLE MATERIALS; CELL MOVEMENT; HUMANS; KERATINOCYTES; MALE; MATERIALS TESTING; RATS, SPRAGUE-DAWLEY; WOUND HEALING;

EID: 84971655074     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370216640943     Document Type: Article

References (66)

1. Ambulatory and Hospital Care Statistics, Centers for Disease Control. National Hospital Ambulatory Medical Care Survey: 2010 Emergency Department Summary Tables. Available at: http://www.cdc.gov/nchs/data/ahcd/nhamcs_emergency/2010_ed_web_tables.pdf (2010, accessed 22 March 2016).
2. T.M.JohnsonD.RatnerB.R.Nelson. Soft tissue reconstruction with skin grafting. J Am Acad Dermatol1992; 27: 151–151.
3. A.D.McGregor. Free skin grafts, Fundamental Techniques of Plastic Surgery, 10th ed. London: Churchill Livingstone, 2000, pp. 35–59.
4. S.ÜnalG.ErsozF.DemirkanE.ArslanN.TütüncüA.Sari. Analysis of skin-graft loss due to infection: infection-related graft loss. Ann Plast Sur2005; 55: 102–102.
5. Branham GH. Facial soft tissue reconstruction. Shelton, CT: PMPH-USA, 2011
6. Y.DemirtasC.YagmurF.SoylemezN.OzturkA.Demir. Management of split-thickness skin graft donor site: a prospective clinical trial for comparison of five different dressing materials. Burns2010; 36: 999–999.
7. J.OrlikP.HorwichC.BartlettJ.TritesR.HartS.Taylor. Long-term functional donor site morbidity of the free radial forearm flap in head and neck cancer survivors. J Otolaryngol2014; 43: 1–1.
8. R.SgoncJ.Gruber. Age-related aspects of cutaneous wound healing: A mini-review. Gerontology2013; 59: 159–159.
9. J.S.BoatengK.H.MatthewsH.N.E.StevensG.M.Eccleston. Wound healing dressings and drug delivery systems: a review. J Pharmaceut Sci2008; 97: 2892–2892.
10. A.S.MoghaddamL.P.KamolzW.WeningerD.ParviziM.WiednerD.B.Lumenta. The use of Keratinocytes: Things we should keep in mind!. Eur Surg2013; 45: 154–154.
11. A.J.SingerR.A.F.Clark. Cutaneous wound healing. New Engl J Med1999; 341: 738–738.
12. Brett DA. Review of collagen and collagen-based wound dressings. Wounds 2008;20:347–56
13. H.ElgharablyS.RoyS.KhannaM.AbasP.DasGhatakA.DasK.MohammedC.K.Sen. A modified collagen gel enhances healing outcome in a preclinical swine model of excisional wounds. Wound Repair Regen2013; 21: 473–473.
14. H.ElgharablyK.GaneshJ.DickersonS.KhannaM.AbasP.D.GhatakS.DixitV.BergdallS.RoyC.K.Sen. A modified collagen gel dressing promotes angiogenesis in a preclinical swine model of chronic ischemic wounds. Wound Repair Regen2014; 22: 720–720.
15. W.S.Krawczyk. A pattern of epidermal cell migration during wound healing. J Cell Biol1971; 49: 247–247.
16. G.F.Odland. The morphology of the attachment between the dermis and the epidermis. Anat Rec1950; 108: 399–399.
17. K.A.BushG.D.Pins. Development of microfabricated dermal epidermal regenerative matrices to evaluate the role of cellular microenvironments on epidermal morphogenesis. Tissue Eng2012; 18: 2343–2343.
18. B.A.DaltonX.F.WalboomersM.DziegielewskiM.D.M.EvansS.TaylorJ.A.JansenJ.G.Steele. Modulation of epithelial tissue and cell migration by microgrooves. J Biomed Mater Res2001; 56: 195–195.
19. R.Harrison. The reaction of embryonic cells to solid structures. J Exp Zool1914; 17: 521–521.
20. P.UttayaratG.K.ToworfeF.DietrichP.I.LelkesR.J.Composto. Topographic guidance of endothelial cells on silicone surfaces with micro- to nanogrooves: Orientation of actin filaments and focal adhesions. J Biomed Mater Res Part A2005; 75A: 668–668.
21. J.M.CaplaD.J.CeradiniO.M.TepperM.J.CallaghanK.A.BhattR.D.GalianoJ.P.LevineG.C.Gurtner. Skin graft vascularization involves precisely regulated regression and replacement of endothelial cells through both angiogenesis and vasculogenesis. Plast Reconstr Surg2006; 117: 836–836.
22. A.MarmarasT.LendenmannG.CivenniD.FrancoD.PoulikakosV.KurtcuogluA.Ferrari. Topography-mediated apical guidance in epidermal wound healing. Soft Matter2012; 8: 6922–6922.
23. J.J.MoonM.HahnI.KimB.NsiahJ.L.West. Micropatterning of poly(ethylene glycol) diacrylate hydrogels with biomolecules to regulate and guide endothelial morphogenesis. Tissue Eng2009; 15: 579–579.
24. B.J.WillenbergT.ZhengF.-W.MengJ.C.MenesesC.RossignolC.D.BatichN.TeradaD.A.SteindlerM.D.Weiss. Gelatinized copper-capillary alginate gel functions as an injectable tissue scaffolding system for stem cell transplants. J Biomater Sci Polymer Ed2011; 22: 1621–1621.
25. D.G.Della RoccaB.J.WillenbergL.F.FerreiraP.S.WateJ.W.PetersenE.M.HandbergT.ZhengD.A.SteindlerN.TeradaC.D.BatichB.J.ByrneC.J.Pepine. A degradable, bioactive, gelatinized alginate hydrogel to improve stem cell/growth factor delivery and facilitate healing after myocardial infarction. Med Hypotheses2012; 79: 673–673.
26. D.G.D.RoccaB.J.WillenbergL.F.FranklinS.L.PorvasnikJ.W.PetersenP.S.WateE.M.HandbergG.SchultzF.RomeoC.D.BatichB.J.ByrneC.J.Pepine. An injectable acellular capillary hydrogel improves left ventricular function after myocardial infarction. J Am Coll Cardiol2012; 59: E856–E856.
27. T.J.StefonekK.S.Masters. Immobilized gradients of epidermal growth factor promote accelerated and directed keratinocyte migration. Wound Repair Regen2007; 15: 847–847.
28. J.T.DeckerC.M.KirschnerC.J.LongJ.A.FinlayM.E.CallowJ.A.CallowA.B.Brennan. Engineered antifouling microtopographies: an energetic model that predicts cell attachment. Langmuir2013; 29: 13023–30.
29. C.M.MaginJ.A.FinlayG.ClayM.E.CallowJ.A.CallowA.B.Brennan. Antifouling performance of cross-linked hydrogels: refinement of an attachment model. Biomacromolecules2011; 12: 915–915.
30. J.F.SchumacherM.L.CarmanT.G.EstesA.W.FeinbergL.H.WilsonM.E.CallowJ.A.CallowJ.A.FinlayA.B.Brennan. Engineered antifouling microtopographies – effect of feature size, geometry, and roughness on settlement of zoospores of the green alga. Ulva Biofouling2007; 23: 55–55.
31. C.Magin. Engineered microtopographies and surface chemistries direct cell attachment and function, Gainesville, FL: University of Florida, 2010.
32. M.L.Carman. Engineered microtopographies to induce in vitro endothelial cell morphologies stable to shear. Biomedical engineering, Gainesville, FL: University of Florida, 2007.
33. C.ChenG.S.SchultzM.BlochP.D.EdwardsS.TebesB.A.Mast. Molecular and mechanistic validation of delayed healing rat wounds as a model for human chronic wounds. Wound Repair Regen1999; 7: 486–486.
34. Gowda SM, Weinstein DA, Blalock TD, Gandhi K, Mast BA, Chin G, Schultz GS. Topical application of recombinant platelet-derived growth factor increases the rate of healing and the level of proteins that regulate this response. International Wound Journal 2013;12:564–71
35. B.J.WillenbergT.HamazakiF.-W.MengN.TeradaC.Batich. Self-assembled copper-capillary alginate gel scaffolds with oligochitosan support embryonic stem cell growth. J Biomed Mater Res Part A2006; 79A: 440–440.
36. K.A.BushB.R.DowningS.E.WalshG.D.Pins. Conjugation of extracellular matrix proteins to basal lamina analogs enhances keratinocyte attachment. J Biomed Mater Res Part A2007; 80A: 444–444.
37. M.L.CarmanT.G.EstesA.W.FeinbergJ.F.SchumacherW.WilkersonL.H.WilsonM.E.CallowJ.A.CallowA.B.Brennan. Engineered antifouling microtopographies – correlating wettability with cell attachment. Biofouling2006; 22: 11–11.
38. A.J.KuijpersG.H.M.EngbersJ.KrijgsveldS.A.J.ZaatJ.DankertJ.Feijen. Cross-linking and characterisation of gelatin matrices for biomedical applications. J Biomater Sci Polymer Ed2000; 11: 225–225.
39. C.M.MaginR.M.MayM.C.DrinkerK.H.CuevasA.B.BrennanS.T.Reddy. Micropatterned protective membranes inhibit lens epithelial cell migration in posterior capsule opacification model. Transl Vis Sci Techol2015; 4: 1–1.
40. C.M.KirschnerK.S.Anseth. In situ control of cell substrate microtopographies using photolabile hydrogels. Small2013; 9: 578–578.
41. G.L.BrownL.B.NanneyJ.GriffenA.B.CramerJ.M.YanceyL.J.CurtsingerL.HoltzinG.S.SchultzM.J.JurkiewiczJ.B.Lynch. Enhancement of wound healing by topical treatment with epidermal growth factor. New Engl J Med1989; 321: 76–76.
42. S.LunS.M.IrvineK.D.JohnsonN.J.FisherE.W.FlodenL.NegronS.G.DempseyR.J.McLaughlinM.VasudevamurthyB.R.WardB.C.H.May. A functional extracellular matrix biomaterial derived from ovine forestomach. Biomaterials2010; 31: 4517–4517.
43. Y.AbramovB.GoldenM.SullivanS.M.BotrosJ.-J.R.MillerA.AlshahrourR.P.GoldbergP.K.Sand. Histologic characterization of vaginal vs. abdominal surgical wound healing in a rabbit model. Wound Repair Regen2007; 15: 80–80.
44. L.Braiman-WiksmanI.SolomonikR.SpiraT.Tennenbaum. Novel insights into wound healing sequence of events. Toxicol Pathol2007; 35: 767–767.
45. M.R.SinghS.SarafA.VyasV.JainD.Singh. Innovative approaches in wound healing: trajectory and advances. Artif Cells Nanomed Biotechnol2013; 41: 202–202.
46. J.M.ReinkeH.Sorg. Wound repair and regeneration. Eur Surg Res2012; 49: 35–35.
47. L.G.Ovington. Advances in wound dressings. Clin Dermatol2007; 25: 33–33.
48. L.I.F.MouraA.M.A.DiasE.CarvalhoH.C.de Sousa. Recent advances on the development of wound dressings for diabetic foot ulcer treatment–-a review. Acta Biomater2013; 9: 7093–7093.
49. C.MartinW.L.LowM.C.I.M.AminI.RadeckaP.RajK.Kenward. Current trends in the development of wound dressings, biomaterials and devices. Pharmaceut Patent Anal2013; 2: 341–341.
50. A.HeitlandA.PiatkowskiE.M.NoahN.Pallua. Update on the use of collagen/glycosaminoglycate skin substitute–six years of experiences with artificial skin in 15 German burn centers. Burns2004; 30: 471–471.
51. N.MoiemenJ.YarrowE.HodgsonJ.ConstantinidesE.ChippH.OakleyE.ShaleM.Freeth. Long-term clinical and histological analysis of Integra dermal regeneration template. Plast Reconstr Surg2011; 127: 1149–1149.
52. A.HalimJ.ShahT.Khoo. Biologic and synthetic skin substitutes: an overview. Indian J Plast Surg2010; 43: 23–23.
53. L.TéotS.OtmanC.TrialA.Brancati. The use of noncellularized artificial dermis in the prevention of scar contracture and hypertrophy. Wound Repair Regen2011; 19: s49–s49.
54. H.F.SeligD.B.LumentaM.GiretzlehnerM.G.JeschkeD.UptonL.P.Kamolz. The properties of an “ideal” burn wound dressing- – what do we need in daily clinical practice? Results of a worldwide online survey among burn care specialists. Burns2012; 38: 960–960.
55. S.Van VlierbergheP.DubruelE.Schacht. Biopolymer-based hydrogels as scaffolds for tissue engineering applications: a review. Biomacromolecules2011; 12: 1387–1387.
56. X.ZhaoQ.LangL.YildirimerZ.Y.LinW.CuiN.AnnabiK.W.NgM.R.DokmeciA.M.GhaemmaghamiA.Khademhosseini. Photocrosslinkable gelatin hydrogel for epidermal tissue engineering. Adv Healthc Mater2016; 5: 108–18.
57. Y.S.ChoiS.B.LeeS.R.HongY.M.LeeK.W.SongM.H.Park. Studies on gelatin-based sponges. Part III: A comparative study of cross-linked gelatin/alginate, gelatin/hyaluronate and chitosan/hyaluronate sponges and their application as a wound dressing in full-thickness skin defect of rat. J Mater Sci Mater Med2001; 12: 67–67.
58. M.B.DainiakI.U.AllanI.N.SavinaL.CornelioE.S.JamesS.L.JamesS.V.MikhalovskyH.JungvidI.Y.Galaev. Gelatin-fibrinogen cryogel dermal matrices for wound repair: preparation, optimisation and in vitro study. Biomaterials2010; 31: 67–67.
59. S.B.LeeY.H.KimM.S.ChongS.H.HongY.M.Lee. Study of gelatin-containing artificial skin V: fabrication of gelatin scaffolds using a salt-leaching method. Biomaterials2005; 26: 1961–1961.
60. A.L.ClementT.J.MoutinhoJrG.D.Pins. Micropatterned dermal-epidermal regeneration matrices create functional niches that enhance epidermal morphogenesis. Acta Biomaterialia2013; 9: 9474–9474.
61. S.A.McClainM.SimonR.A.JonesA.NandiJ.O.GailitM.G.TonnesenD.NewmanR.A.Clark. Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am J Pathol1996; 149: 1257–1257.
62. A.HuttenlocherA.R.Horwitz. Integrins in cell migration. Cold Spring Harbor Perspect Biol2011; 3: a005074–a005074.
63. A.KarkhanehH.MirzadehA.GhaffariyehA.EbrahimiN.HonarpishehM.HosseinzadehM.H.Heidari. Novel materials to enhance corneal epithelial cell migration on keratoprosthesis. Br J Ophthalmol2011; 95: 405–405.
64. A.I.TeixeiraG.A.AbramsP.J.BerticsC.J.MurphyP.F.Nealey. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci2003; 116: 1881–1881.
65. H.JeonH.HidaiD.J.HwangK.E.HealyC.P.Grigoropoulos. The effect of micronscale anisotropic cross patterns on fibroblast migration. Biomaterials2010; 31: 4286–4286.
66. S.RoyS.BiswasS.KhannaG.GordilloV.BergdallJ.GreenC.B.MarshL.J.GouldC.K.Sen. Characterization of a preclinical model of chronic ischemic wound. Physiol Genom2009; 37: 211–211.