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Cell-based therapies might be considered as an alternative approach to growth factors for wound management. Cells so far studied for cutaneous wound healing effect include stem cells, keratinocytes, fibroblasts and platelets. The latter ones have been discussed under the previous section because of the growth factor secretion. An overview of the most frequently reported cell-based therapies for skin wound management in animals models is presented in Table 2.
The FDA has implemented a regulatory outline that controls cell-based products based on three topics: i prevention of using contaminated cells, ii prevention of handling that may cause contamination and iii clinical safety of cells used [ ]. There is a substantial gap between optimistic laboratory-based research and approved stem cell based products SCBPs in this fast emerging field [ ]. In order to translate SCBPs from bench to bedside and ensure patient safety, compliance with existing regulations and guidelines is required to ensure that the product is safe, pure and potent. Stem cells.
Stem cells are defined as unspecialized cells that have two defined properties: the ability to differentiate into other cells and the ability to self-regenerate [ ]. Stem cells may be categorized according to their potency: totipotent, pluripotent, multipotent or progenitor cells [ ] or conferring to the sources they originate from: embryonic stem cells ESCs , fetal stem cells, neonatal or umbilical cord stem cells and adult stem cells [ ]. Since adult, post-natal stem cells escape the ethical and safety issues associated with ESCs, adult stem cells are an important aspect for cell-based therapies [ ] and hence reviewed in this article.
To date, the role of stem cells in wound healing is progressively being valued. For this reason, an increasing number of regenerative therapies for wound healing are being developed and encouraged by promising findings from both animal and human studies. It has been suggested that stem cell application has more advantages than the use of single biological factors for several reasons [ ].
Indeed, stem cells have the capacity to differentiate into multiple cell lineages, influence environmental elements and produce healing enhancing factors indicating a great potential as a therapeutic tool [ , ]. Mesenchymal stem cells.
Adult mesenchymal stem cells MSCs are multipotent cells found in mesodermal tissues [ , ]. These cells represent a unique tool for tissue engineering. Indeed, it has been reported that MSCs can differentiate into multiple lineages such as osteoblasts, chondroblasts, adipocytes, tenocytes and myocytes [ ]. In this regard, it has been demonstrated that MSCs have important potential immunomodulatory effects. Therefore, the anti-inflammatory properties of MSCs increase their importance for chronic wound treatment.
In addition, MSCs are recognized to have antibacterial activities [ ], either by secretion of antimicrobial factors or indirectly by secretion of immunomodulative factors which up-regulate phagocytosis and bacterial killing [ , ]. A number of parameters can assess experimental and clinical wound healing upon MSC therapy. For clinical wound assessment, parameters like histology, tensiometry and tracing of the transplanted cells in the wound tissue over time are currently used. Histology evaluates the status of infiltration of inflammatory cells, vascular proliferation, fibroplasia, presence and depth of scar tissue, epithelialization rate and absence of adnexa including hair follicles, apocrine glands and smooth muscle.
Recent reports consider that both allogenic and autologous MSCs may positively impact all phases of wound repair in humans as well as animals [ 23 ]. Shumakov et al. It was also suggested that the cells produce bioactive substances that would enhance the regeneration process. Moreover, Nakagawa et al. Furthermore, a study by McFarlin et al.
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The latter study reported that MSCs may also facilitate wound healing by trans-differentiating into myoblasts and keratinocytes after migration to the wound site. Transplantation of human MSCs also resulted in promotion of incisional wound repair in rabbits and resulted in increased tensile strength, granulation tissue formation and decreased evidence of scar formation [ ]. Experiments by Wu et al. Recently, Kim et al [ ] applied allogenic MSCs on skin wounds in a canine experimental wound model and demonstrated that MSC treatment caused accelerated wound closure and enhanced collagen production, cellular proliferation and angiogenesis.
Apart from bone marrow, transplanted MSCs isolated from Wharton's jelly of caprine umbilical cord to full-thickness skin incision of goats Azari et al. In addition, peripheral blood-derived stem cells PBSCs have been reported to enhance different wound healing parameters of chronic naturally occurring wounds in horses, such as granulation tissue and scar tissue formation [ ]. However, the latter study contained no control groups with untreated wounds, so further research is definitely warranted.
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The wound was treated again on day 7 and 17 with cultured MSC and this resulted in wound size decrease and increase in dermal vascularization and thickness. Falanga et al [ ] suggested that bone marrow-derived MSCs accelerated skin resurfacing of defects from surgically excised non-melanoma skin cancers when combined with topically applied fibrin spray. Dash et al [ ] indicated that simultaneous intramuscular and topical administration of autologous bone marrow-derived MSCs for the treatment of non-healing ulcers of low extremities, enhanced the healing process and clinical parameters.
A similar result was also observed when Jain et al. The study conducted by Lu et al [ ], also demonstrated the clinical benefits of intramuscular administration of bone marrow-derived MSCs for treatment of diabetic critical limb ischemia and foot ulcers. Hematopoietic stem cells. The HSCs are a well-characterized population of self-renewing cells [ ], which are currently mainly being used for treating acquired and inherited bone marrow and hematologic disorders in man [ ]. Krause et al. They suggested that HSCs could possibly contribute to the clinical treatment of skin wounds. In this regard, it has also been reported that topical application of full thickness excisional wounds in diabetic mice with a side population of HSCs resulted in a high percentage of wound closure [ ].
Nevertheless, more research is warranted in order to determine whether HSCs alone have similar wound healing enhancing effects as other adult stem cell types reported so far.
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Epithelial stem cells. Epithelial stem cells EpSCs are adult stem cells which are quiescent yet have the capacity to self-renew and differentiate into at least one cell type [ ]. A clear distinction should be made between dermal papillae stem cells that contribute to multiple skin appendage formation and epidermal stem cells which are mainly designed to reconstitute epidermis.
There are different types of EpSCs which have been identified in the hair follicle [ ] or the basal layer of the epidermis [ 65 ]. In haired skin, progeny of bulge stem cells migrate towards new epidermis for re-epithelialization [ 37 ]. Yang et al. Their results showed that EpiASCs were able to rebuild the skin with hair formation.
Indeed, the dermis was thinner and displayed less granulation tissue than the control wounds, which was a desired feature in equine skin, since horses tend to form hypergranulation tissue. Moreover, the latter study reported a considerable increase in vascularization, elastin content and follicle-like structures in the EpSC-treated group. Since these cells are lineage committed and preliminary experiments demonstrated similar healing enhancing capacities as MSCs, EpSCs might be considered as a valuable alternative. Adipose-derived stem cells.
Adipose-derived stem cells ASCs represent alternative sources of multipotent cells with characteristics similar to bone marrow-derived MSCs [ , ]. Compared to BM-MSCs, ASCs are more abundant which makes them easier to isolate, and hence they are considered as an attractive source for wound regeneration [ ]. An in vitro study by Lee et al. Moreover, the latter study reported an increased contraction of the collagen matrix where the fibroblasts reside, indicating the importance of paracrine effects on surrounding cells. Lee et al. Moreover, it has been demonstrated that ASCs possess anti-inflammatory, vasculogenic and angiogenic properties, which are lacking in other cell types, such as dermal fibroblasts.
Due to these paracrine advantages, ASCs can be used as a substitute for fibroblasts in grafting engineered skin [ ]. Nevertheless, more protracted studies are necessary to demonstrate the working mechanism of these cells. Differentiated cells. Adult terminally differentiated cells are also used for skin wound treatment. To date, keratinocytes, fibroblasts and adipose-derived stromal vascular fraction SVF cells are being applied in a clinical setting of human skin wounds.
They are mainly combined with artificial dermis to optimize wound healing [ ].