Ординатура / Офтальмология / Английские материалы / Biomaterials and regenerative medicine in ophthalmology_Chirila_2010
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deposited collagen was observed in the device skirt.37 Implantation was also performed in feline corneas, which resulted in device extrusion between 15 and 150 days, but these results may not be representative of human wound healing as felines demonstrated complete cornea regeneration which is not possible in humans.38
5.4.7Aachen keratoprosthesis
The Aachen KPro is made of silicone rubber, and the design boasts easy surgical handling and flexibility.39 Following short-term implantation into ten patients, there were no occurrences of retinal detachment, clear visual acuity in four eyes, and edema in three eyes.39 The type II Aachen KPro, with immobilized fibronectin for increased cellular attachment, was implanted as a temporary implant prior to retinal surgery or corneal grafting.40,41 It also allows for intraocular pressure measurements in porcine eyes.42
5.4.8Other keratoprostheses in development
AninterpenetratingpolymernetworkofPDMSandpoly(N-isopropylacrylamide) (PNIPAAM) has been fabricated to combine the mechanical strength, transparency, wettability and glucose permeability of these two materials for ophthalmic applications.43
Elsewhere, three porous materials, polybutylene:polypropylene (80:20), poly(ethylene terephthalate) and PTFE, intended for application as a KPro, were evaluated in rabbit corneal stroma over 12 weeks.44 PTFE demonstrated decreased inflammation and stromal cell migration, while edema and neovascularization were similar among the implants.44
A poly(ethylene glycol)–poly(acrylic acid) (PEG–PAA) interpenetrating polymer network hydrogel, with glucose permeability comparable with the
human cornea, was evaluated over 2 weeks in rabbit stromas and was well tolerated in nine out of ten eyes.45,46 Further development in fabrication
lead to the usage of photolithography to form a patterned skirt of poly(2- hydroxyethyl acrylate) (PHEA) around the PEG–PAA core.47
5.4.9Biological keratoprostheses
KPro devices have been fabricated using biological components – such as extracellular matrix components including collagen, fibronectin and laminin, or oligopeptides – to render the device more able to interact with host cells and tissue.6,7 To aid with epithelialization and tissue integration, collagen type I was tethered to a PEG–PAA hydrogel; however, corneal epithelial migration and wound healing rates were decreased from 2–3 days to 14 days.46 This was attributed by the authors to antimicrobials leaching from
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the hydrogel, improper surgical technique and the choice of collagen that did not properly mimic the corneal basement membrane.48 Elsewhere, a poly(vinyl alcohol) (PVA) hydrogel with tethered collagen demonstrated enhanced epithelialization in vitro,48 but required modification with an amniotic membrane (PVA-AM) to result in epithelialization, reduced inflammation and opacification in vivo.49
Corneal onlays fabricated from porous perfluoropolyether (PFPE) coated with collagen type I enhanced epithelialization in four feline corneas for 39 days.50 In another study, porous polycarbonate membranes coated with collagen type I, collagen type IV, or laminin enhanced corneal epithelial cell migration and adhesion in vivo, while fibronectin, endothelial extracellular matrix, hyaluronic acid or chondroitin sulfate did not support epithelialization.51
PHEMA–MAA–PEG hydrogels were fabricated with extracellular matrix components (fibronectin, laminin, substance P and insulin-like growth factor) or peptide sequences such as arginine–glycine–aspartic acid (RGD) or fibronectin adhesion-promoting (FAP); FAP enhanced epithelialization significantly.52 Previous work showed that tethered FAP and laminin had better epithelial adhesion compared with fibronectin.53 Furthermore, cornea epithelial cell adhesion was increased in vitro on PHEMA hydrogels through tethering of RGDS (arginin–glycine–asparticacid–serine) and YIGSR (tyrosine–isoleucine–glycine–serine–arginine) cell adhesion peptides.54
Incorporation of growth factors, including epidermal growth factor (EGF) and transforming growth factor beta (TGF-b), has been utilized to manipulate epithelialization.7 Specifically, EGF was tethered to PDMS through a PEG spacer to improve epithelialization of the surface, which was found to rely heavily on the underlying surface chemistry.55–57 Tethered TGF-b2 was also demonstrated to enhance epithelialization and to hinder stromal cell adhesion.58
5.5Tissue-engineered corneal equivalents
TECEs combine natural polymers or biological components – including but not restricted to proteins, polysaccharides, nucleic acids or polyphenols – and corneal cells to fabricate a device that could mimic one or more native corneal tissue layers for seamless integration into the host.2 There are generally three approaches to TECE devices: seeding cells directly on a surface or gel that can be reorganized by the cells; seeding cells on to a substrate where they secrete their own extracellular matrix scaffold;59 and using a preformed substrate or scaffold that allows integration of either pre-seeded progenitor cells or in-growing host cells. Many TECEs are based on collagen, as the cornea is mainly type I collagen.7 TECEs with cellular components include cells from immortalized cell lines60 or from primary/low-passage limbal or central corneal cells.61–63
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5.5.1Cell-based tissue-engineered corneal equivalent (Okano laboratory, Japan)
Corneal or oral mucosal epithelial stem cell sheets are grown on a temperature-
sensitive layer of PNIPAAM, which allows cell growth and cell sheet detachment at 37 oC and below 32 oC, respectively.64,65 Cells are removed
from the PNIPAAM coating without digestive enzymes – retaining cell–cell junctions, cellular proteins and their extracellular matrix – and multiple sheets can be layered to form three-dimensional matrices.64 During surgery, cell sheets are transplanted to the host using a donut-shaped support that can be removed following attachment of the cell sheets; cell sheets do not need to be sutured in place.64 In order to aid availability, a device was fabricated for transportation of the cell sheets at 37 oC for 8 hours.66 A regenerated epithelium and improved visual acuity 1 year postoperatively has been achieved with this technique.64
5.5.2Collagen sponge-based tissue-engineered corneal equivalent (Hubel laboratory, USA)
A collagen sponge, fabricated through dehydrothermal crosslinking and lyophilization, supported epithelial, keratocyte and endothelial cell proliferation and migration, and extracellular matrix production in vitro.63 Further studies investigated the development of a corneal stromal equivalent, whereby stromal cells cultured on these collagen sponges demonstrated a myofibroblast phenotype, evident via alpha smooth muscle actin staining, matrix contraction and matrix remodelin.67,68 Transparency was further enhanced with the addition of chondroitin sulphate, while matrix contraction decreased.67 Recently, collagen matrices were created with glucose-mediated ultraviolet (UV) crosslinking, with improved mechanical strength and transparency.69 Microgroove patterning (2 mm) resulted in stromal cell alignment along the grooves after 1 week in culture.69
5.5.3Chemically crosslinked collagen and cell-based tissue-engineered corneal equivalent (Griffith and Fagerholm laboratories, Canada and Sweden)
The Griffith group has developed various porcine and recombinant human collagen-based corneal substitutes that have been implanted successfully into mice, rabbits, guinea pigs, dogs and pigs as either deep lamellar grafts or full-thickness implants that aim to promote regeneration of corneal tissue by mobilizing endogenous progenitor cells. The hydrogels were fabricated by moulding to the appropriate dimensions and curvatures, which allow for transmission of 90% or higher of white light. Crosslinking, co-polymerization
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and development of interpenetrating networks have been used to enhance the mechanical properties of the gels to allow suturing and resist biodegradation. They demonstrated that a simple type I collagen-based corneal stroma mimic (fabricated by crosslinking porcine or recombinant collagen with 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride (EDC) and N-hydroxysuccinimide (NHS)) could be successfully implanted into mini-pigs with stable host–graft integration.70,71 At 12 months post-implantation, the implants had regenerated an epithelium, the stroma and corneal nerves. Results of recent Phase I human clinical trials in Sweden of corneal transplantation with the EDC crosslinked recombinant human collagen corneas as deep lamellar grafts are shown in Fig. 5.1. Early postoperative results show regeneration of corneal epithelium, stroma and early signs of nerve regeneration.72 These implants, which are completely synthetic, using a synthethically produced recombinant human collagen did not cause adverse reactions and therefore are suitable as temporary grafts or patches. However, longer-term monitoring is needed to determine whether or not they will be useful as substitutes for donor tissue. In addition, further modifications are probably needed in order to be useful in a wider range of clinical indications.
The group has also shown that synthetic materials can be combined with collagen to enhance interaction with the host cornea, e.g. by grafting of laminin-derived pentapeptide, YIGSR, on to a synthetic crosslinker of poly(N- isopropylacrylamide-coacrylic acid-coacryloxysuccinimide),73 enhanced nerve regeneration and restoration of corneal touch sensitivity was achieved in pigs within a 6 week period, compared with still insensitive allografts. Constructs could also be stabilized against enzymatic or UV degradation by fabrication of collagen–phosphorylcholine interpenetrating networks.74 Where the patients are lacking endogenous progenitors, these collagen-based constructs have been shown in vitro to support expansion of corneal progenitor cells, e.g. limbal cultures.75
5.5.4Dendrimer crosslinked collagen tissue-engineered corneal equivalent (Sheardown laboratory, Canada)
In order to increase the number of amine groups available for crosslinking, polypropyleneimine octaamine dendrimers were combined with collagen and crosslinked through EDC/NHS chemistry.76 These materials demonstrated high mechanical strength, good optical clarity, biological stability and high crosslinking density.76,77 Epithelial cell adhesion and growth was achieved in vitro,77 and enhanced, as was neurite extension and nerve cell density, through the incorporation of an adhesion peptide, YIGSR.78 Furthermore, incorporation of IKVAVYIGSR or YIGSRIKVAV peptides resulted in increased epithelial stratification, which was dependent on the peptide surface concentration.79
Corneal tissue engineering versus synthetic artificial corneas |
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(a)
(b)
5.1 (a) Slit-lamp photograph of human cornea at 1 day post-transplantation and
(b) 12 months postoperatively.
144 Biomaterials and regenerative medicine in ophthalmology
Heparin was also incorporated into dendrimer crosslinked collagen gels for the soluble delivery of basic fibroblast growth factor (FGF-2) and other heparin-binding growth factors.80 Heparin did not compromise gel integrity, but opacity and FGF-2 retention were dependent on heparin concentration.80
5.5.5Collagen–chitosan–glycosaminoglycan-based tissue-engineered corneal equivalent (Huang laboratory, China)
Collagen, chitosan and glycosaminoglycans were combined to form a degradable hydrogel for corneal replacement.81 Chitosan was incorporated with collagen to decrease collagenase digestion and increase the mechanical strength of the resulting hydrogel, while glycosaminoglycans were also added for increased cell adhesion, flexibility and porosity.81 Following implantation into 18 rabbits, re-epithelialization occurred after 5 days, clarity was maintained with only minor vessel hyperplasia after 10 days, and full degradation was achieved after 6 months with new corneal tissue and keratocytes replacement.81
5.5.6Three-dimensional cell and extracellular matrixbased tissue-engineered corneal equivalent (LOEX group, Canada)
The three-dimensional collagen thermogel was developed by the Laboratoire d’Organogenese Experimentale (LOEX) group, whereby corneal epithelial cells
are seeded atop of a previously cultured multi-layered fibroblast collagenous extracellular matrix to create a reconstructed corneal.59,61,82
5.6Conclusions
The past decade has seen significant advances in the development of corneal substitutes. Extremely promising results have been obtained with synthetic artificial corneas, and a number of different prototypes are available. As a result, replacement of corneal tissue with artificial substitutes, while not commonplace, is certainly possible. The development of new tissue-engineered prototypes will only serve to enhance the potential of these systems for restoring the sight of visually compromised patients.
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