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Nanomaterials 2020, 10, 390 12 of 16 tissue. Synthetic products impregnated with silver used as dressings for the treatment of wounds have been demonstrated to act as a mechanical barrier against exogenous microorganisms, preserving the local temperature and maintaining the humidity of the wound environment [52]. Therefore, the application of sodium alginate/gelatin hydrogels containing AgNPs on the surface of the wounds may work as a biomechanical barrier, protecting the ulcerated bed from the microbial contamination. The silver-induced antibacterial effect has been associated with its ability to interact with bacterial plasma membranes, proteins, and enzymes involved in vital cellular processes, such as the electron transport chain [53]. AgNPs incorporated into dressings have significantly decreased wound-healing time likely as a result of increased bacterial clearance from infected wounds [54,55]. However, other silver nanoparticles-derived biological properties might have played a role in the acceleration of granulation tissue formation and maturation on the initial stages of wound healing. AgNPs have been demonstrated to reduce the production of the inflammatory cytokines, such as nitric oxide and prostaglandin E2, in lipopolysaccharide-induced RAW264.7 cells [56]. Hence, the silver nanoparticles-induced reduction of the inflammatory cytokines release might have also played a role in the improvement of granulation tissue formation. The dermal connective tissue of the GHP group showed earlier formation of mature hypovascular primary scars, but no pathological signs of hypercollagenization was observed. It has been previously reported that silver nanoparticles can reduce the levels of transforming growth factor β (TGF-β) expression while increasing interferon (IFN)-γ levels until full wound closure [57]. IFN-γ has been demonstrated to inhibit fibroblast proliferation and matrix production [58] and induce myofibroblasts apoptosis [59], whereas enhanced expression of TGF-β1 mRNA was found in both keloids and hypertrophic scars [60]. Hence, the modulation of TGF-β/ IFN-γ production may play a role in the positive effects of silver on wound healing. At the final stages of wound healing, healed skin treated with sodium alginate/gelatin hydrogels containing AgNPs presented a well-stratified epidermis, complete with basal, spinous, granular, and cornified layers, with epithelial buddings interpreted as rudimentary cutaneous appendages. Also, collagen tissue was well-formed, with long thick gross collagen fibers parallel-arranged. These results suggest that the silver-containing hydrogels improved both dermal and epidermal re-establishment. The precise mechanisms underlying such biological effects are not fully clarified yet. It has been demonstrated that silver nanoparticles can induce contraction of the wounds in mice as a result of increased keratinocyte migration and proliferation [61]. However, further studies are needed to find out whether the formation of rudimentary cutaneous appendages in the GHP group, but not in the others, result from AgNPs-induced stimulation of keratinocyte proliferation and differentiation or would be an indirect response secondary to the improvement of the early phases of wound healing. Our study suggests that hydrogels containing AgNPs provide significant benefits on wound healing in a rodent model; herein, we provide the evidence that AgNPs can accelerate granulation tissue formation and maturation and earlier development of the primary collagen scar and rudimentary cutaneous appendages. 4. Conclusions This study aimed to produce a safe, biocompatible formulation based on AgNPs for wound healing, for easy application and of low environmental impact. No inorganic solvents have been used nor any complex methodology that needs high energy. The use of natural polymers as sodium alginate and gelatin is a cost-effective approach for the production of a biocompatible hydrogel that can be easily loaded with antimicrobial AgNPs with healing properties. Compared to synthetic ones, natural polymers are of lower cost, non-toxic, less abrasive, and are environmentally friendly. The developed hydrogels demonstrated to be non-cytotoxic against fibroblasts, and their antimicrobial activity was confirmed in vitro using Gram-positive (Staphylococcus aureus) and Gram-negative (Pseudomonas aeruginosa) bacteria. The wound healing capacity of AgNPs hydrogels was studied over 14 days inPDF Image | Wound Healing Silver Nanoparticles-Composing Hydrogel
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