Bioactive Medications for the Delivery of Platelet Derivatives to Skin Wounds

Page: [472 - 483] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Chronic wounds are the result of alterations in the complex series of events of physiological wound healing. In particular, the prolonged inflammation results in increased protease activity, in the degradation of extracellular matrix (ECM) and of growth factors (GFs). The relevance of platelet GFs in maintaining and restoring the complex equilibrium of different moments in wound healing is well recognized. Moreover, the observed decrease of their levels in chronic wounds suggested a possible therapeutic role of the external application to the wounds. It has been also pointed out that tissue regeneration can be more efficiently obtained by the synergic use of different GFs. Platelet derivatives such as platelet- rich plasma (PRP) and platelet lysate (PL) are able to release GFs in a balanced pool. Their therapeutic use in regenerative medicine and wound healing has been therefore more and more frequently proposed in clinical trials and in the literature. The development of a suitable formulation able to control the GFs release rate, to protect the GFs, and to assure their prolonged contact with the wound site, is of paramount importance for the therapeutic success. The present review considers some formulation approaches for PRP and PL application to wounds.

Keywords: Platelet-rich plasma, platelet lysate, drug delivery systems, skin regeneration, wound healing, extracellular matrix (ECM).

Graphical Abstract

[1]
Singh, S.; Young, A.; McNaught, C.E. The physiology of wound healing. Surgery, 2017, 35, 473-477.
[2]
Stolzenburg-Veeser, L.; Golubnitschaja, O. Mini-encyclopaedia of the wound healing - Opportunities for integrating multi-omic approaches into medical practice. J. Proteomics, 2018, 188, 71-84.
[3]
Ruthenborg, R.J.; Ban, J.J.; Wazir, A.; Takeda, N.; Kim, J.W. Regulation of wound healing and fibrosis by hypoxia and hypoxia-inducible factor-1. Mol. Cells, 2014, 37, 637-643.
[4]
Hong, W.X.; Hu, M.S.; Esquivel, M.; Liang, G.Y.; Rennert, R.C.; McArdle, A.; Paik, K.J.; Duscher, D.; Gurtner, G.C.; Lorenz, H.P.; Longaker, M.T. The role of hypoxia-inducible factor in wound healing. Adv. Wound Care, 2014, 3, 390-399.
[5]
Sen, C.K.; Gordillo, G.M.; Roy, S.; Kirsner, R.; Lambert, L.; Hunt, T.K.; Gottrup, F.; Gurtner, G.C.; Longaker, M.T. Human skin wounds: A major and snowballing threat to public health and the economy. Wound Repair Regen., 2009, 17, 763-771.
[6]
Nauta, T.D.; van Hinsbergh, V.W.; Koolwijk, P. Hypoxic signaling during tissue repair and regenerative medicine. Int. J. Mol. Sci., 2014, 15, 19791-19815.
[7]
Johnson, K.E.; Wilgus, T.A. Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv. Wound Care, 2014, 3, 647-661.
[8]
Bao, P.; Kodra, A.; Tomic-Canic, M.; Golinko, M.S.; Ehrlich, H.P.; Brem, H. The role of vascular endothelial growth factor in wound healing. J. Surg. Res., 2009, 153, 347-358.
[9]
Nissen, N.N.; Polverini, P.J.; Koch, A.E.; Volin, M.V.; Gamelli, R.L.; Di Pietro, L.A. Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am. J. Pathol., 1998, 152, 1445-1452.
[10]
Shah, J.M.; Omar, E.; Pai, D.R.; Sood, S. Cellular events and biomarkers of wound healing. Indian J. Plast. Surg., 2012, 45, 220-228.
[11]
Werner, S.; Grose, R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev., 2003, 83, 835-870.
[12]
Velnar, T.; Bailey, T.; Smrkolj, V. The wound healing process: An overview of the cellular and molecular mechanisms. J. Int. Med. Res., 2009, 37, 1528-1542.
[13]
Rousselle, P.; Braye, F.; Dayan, G. Re-epithelialization of adult skin wounds: Cellular mechanisms and therapeutic strategies. Adv. Drug Deliv. Rev., 2018. S0169-409X(18)30158-3.
[14]
Boateng, J.; Catanzano, O. Advanced therapeutic dressings for effective wound healing-a review. J. Pharm. Sci., 2015, 104, 3653-3680.
[15]
Frykberg, R.G.; Banks, J. Challenges in the treatment of chronic wounds. Adv. Wound Care (New Rochelle), 2015, 4, 560-582.
[16]
Rafail, S.; Kourtzelis, I.; Foukas, P.G.; Markiewski, M.M.; DeAngelis, R.A.; Guariento, M.; Ricklin, D.; Grice, E.A.; Lambris, J.D. Complement deficiency promotes cutaneous woundhealing in mice. J. Immunol., 2015, 194, 1285-1291.
[17]
Tecilazich, F.; Dinh, T.; Pradhan-Nabzdyk, L.; Leal, E.; Tellechea, A.; Kafanas, A.; Gnardellis, C.; Magargee, M.L.; Dejam, A.; Toxavidis, V.; Tigges, J.C.; Carvalho, E.; Lyons, T.E.; Veves, A. Role of endothelial progenitor cells and inflammatory cytokines in healing of diabetic foot ulcers. PLoS One, 2013, 8, e83314.
[18]
Kurokawa, T.; Ohkohchi, N. Platelets in liver disease, cancer and regeneration. World J. Gastroenterol., 2017, 23, 3228-3239.
[19]
MacLeod, A.S.; Mansbridge, J.N. The innate immune system in acute and chronic wounds. Adv. Wound Care (New Rochelle), 2016, 5, 65-78.
[20]
Menke, N.B.; Ward, K.R.; Witten, T.M.; Bonchev, D.G.; Diegelmann, R.F. Impaired wound healing. Clin. Dermatol., 2007, 25, 19-25.
[21]
Lynch, S.E.; Nixon, J.C.; Colvin, R.B.; Antoniades, H.N. Role of platelet-derived growth factor in wound healing: Synergistic effects with other growth factors. Proc. Natl. Acad. Sci. USA, 1987, 84, 7696-7700.
[22]
Barrientos, S.; Stojadinovic, O.; Golinko, M.S.; Brem, H. TomicCanic, M. Growth factors and cytokines in wound healing. Wound Repair Regen., 2008, 16, 585-601.
[23]
Yu, D.H.; Mace, K.A.; Hansen, S.L.; Boudreau, N.; Young, D.M. Effects of decreased insulin-like growth factor-1 stimulation on hypoxia inducible factor 1-alpha protein synthesis and function during cutaneous repair in diabetic mice. Wound Repair Regen., 2007, 15, 628-635.
[24]
Mazzucco, L.; Borzini, P.; Gope, R. Platelet-derived factors involved in tissue repair-from signal to function. Transfus. Med. Rev., 2010, 3, 218-234.
[25]
Wilgus, T.A.; Ferreira, A.M.; Oberyszyn, T.O.; Bergdall, V.K.; Di Pietro, L.A. Regulation of scar formation by vascular endothelial growth factor. Lab. Invest., 2008, 88, 579-590.
[26]
Gainza, G.; Villullas, S.; Pedraz, J.L.; Hernandez, R.M.; Igartua, M. Advances in drug delivery systems (DDSs) to release growth factors for wound healing and skin regeneration. Nanomedicine, 2015, 11, 1551-1573.
[27]
Rossi, S.; Ferrari, F.; Sandri, G.; Bonferoni, M.C.; Del Fante, C.; Perotti, C.; Caramella, C. Wound healing: Biopolymers and hemoderivatives. In: Encyclopedia of Biomedical Polymers and Polymeric Biomaterials, 1st ed; Mishra, M., Ed.; Taylor & Francis: New York, 2015; Vol. 11, pp. 8280-8298.
[28]
Anitua, E.; Sánchez, M.; Nurden, A.T.; Nurden, P.; Orive, G.; Andía, I. New insights into and novel applications for platelet-rich fibrin therapies. Trends Biotechnol., 2006, 24, 227-234.
[29]
Hao, X.; Silva, E.A.; Månsson-Broberg, A.; Grinnemo, K.H.; Siddiqui, A.J.; Dellgren, G.; Wärdell, E.; Brodin, L.A.; Mooney, D.J.; Sylvén, C. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc. Res., 2007, 75, 178-185.
[30]
De Pascale, M.R.; Sommese, L.; Casamassimi, A.; Napoli, C. Platelet derivatives in regenerative medicine: an update. Transfus. Med. Rev., 2015, 29, 52-61.
[31]
Mendes, B.B.; Gómez-Florit, M.; Babo, P.S.; Domingues, R.M.; Reis, R.L.; Gomes, M.E. Blood derivatives awaken in regenerative medicine strategies to modulate wound healing. Adv. Drug Deliv. Rev., 2018, 129, 376-393.
[32]
Pallua, N.; Wolter, T.; Markowicz, M. Platelet-rich plasma in burns. Burns, 2010, 36, 4-8.
[33]
Venter, N.G.; Marques, R.G.; Santos, J.S.; Monte-Alto-Costa, A. Use of platelet-rich plasma in deep second- and third-degree burns. Burns, 2016, 42, 807-814.
[34]
Fernandez-Moure, J.S.; Van Eps, J.L.; Cabrera, F.J.; Barbosa, Z.; Medrano Del Rosal, G.; Weiner, B.K.; Ellsworth, W.A., 4th; Tasciotti, E. Platelet-rich plasma: A biomimetic approach to enhancement of surgical wound healing. J. Surg. Res., 2017, 207, 33-44.
[35]
Suthar, M.; Gupta, S.; Bukhari, S.; Ponemone, V. Treatment of chronic non-healing ulcers using autologous platelet rich plasma: A case series. J. Biomed. Sci., 2017, 24, 16.
[36]
Law, J.X.; Chowdhury, S.R.; Saim, A.B.; Idrus, R.B.H. Platelet-rich plasma with keratinocytes and fibroblasts enhance healing of full-thickness wounds. J. Tissue Viability, 2017, 26, 208-215.
[37]
Chicharro-Alcántara, D.; Rubio-Zaragoza, M.; Damiá-Giménez, E.; Carrillo-Poveda, J.M.; Cuervo-Serrato, B.; Peláez-Gorrea, P.; Sopena-Juncosa, J.J. Platelet rich plasma: New insights for cutaneous wound healing management. J. Funct. Biomater., 2018, 9, E10.
[38]
Crovetti, G.; Martinelli, G.; Issi, M.; Barone, M.; Guizzardi, M.; Campanati, B.; Moroni, M.; Carabelli, A. Platelet gel for healing cutaneous chronic wounds. Transfus. Apher Sci., 2004, 30, 145-151.
[39]
Mazzucco, L.; Medici, D.; Serra, M.; Panizza, R.; Rivara, G.; Orecchia, S.; Libener, R.; Cattana, E.; Levis, A.; Betta, P.G.; Borzini, P. The use of autologous platelet gel to treat difficult-to-heal wounds: A pilot study. Transfusion, 2004, 44, 1013-1018.
[40]
Borzini, P.; Mazzucco, L. Platelet gels and releasates. Curr. Opin. Hematol., 2005, 12, 473-479.
[41]
Piccin, A.; Di Pierro, A.M.; Canzian, L.; Primerano, M.; Corvetta, D.; Negri, G.; Mazzoleni, G.; Gastl, G.; Steurer, M.; Gentilini, I.; Eisendle, K.; Fontanella, F. Platelet gel: A new therapeutic tool with great potential. Blood Transfus., 2017, 15, 333-340.
[42]
Ranzato, E.; Patrone, M.; Mazzucco, L.; Burlando, B. Platelet lysate stimulates wound repair of HaCaT Keratinocytes. Br. J. Dermatol., 2008, 159, 537-545.
[43]
Fekete, N.; Gadelorge, M.; Fürst, D.; Maurer, C.; Dausend, J.; Fleury-Cappellesso, S.; Mailänder, V.; Lotfi, R.; Ignatius, A.; Sensebé, L.; Bourin, P.; Schrezenmeier, H.; Rojewski, M.T. Platelet lysate from whole blood-derived pooled platelet concentrates and apheresis-derived platelet concentrates for the isolation and expansion of human bone marrow mesenchymal stromal cells: Production process, content and identification of active components. Cytotherapy, 2012, 14, 540-554.
[44]
Barsotti, M.C.; Losi, P.; Briganti, E.; Sanguinetti, E.; Magera, A.; Al Kayal, T.; Feriani, R.; Di Stefano, R.; Soldani, G. Effect of platelet lysate on human cells involved in different phases of wound healing. PLoS One, 2013, 8, e84753.
[45]
Sergeeva, N.S.; Shanskii, Y.D.; Sviridova, I.K.; Karalkin, P.A.; Kirsanova, V.A.; Akhmedova, S.A.; Kaprin, A.D. Analysis of reparative activity of platelet lysate: Effect on cell monolayer recovery in vitro and skin wound healing in vivo. Bull. Exp. Biol. Med., 2016, 162, 138-145.
[46]
Pezzotta, S.; Del Fante, C.; Scudeller, L.; Rossi, G.C.; Perotti, C.; Bianchi, P.E.; Antoniazzi, E. Long-term safety and efficacy of autologous platelet lysate drops for treatment of ocular GvHD. Bone Marrow Transplant., 2017, 52, 101-106.
[47]
Amable, P.R.; Carias, R.B.; Teixeira, M.V.; da Cruz Pacheco, I.; Correa do Amaral, R.J.; Granjeiro, J.M.; Borojevic, R. Platelet-rich plasma preparation for regenerative medicine: Optimization and quantification of cytokines and growth factors. Stem Cell Res. Ther., 2013, 4, 67.
[48]
Martineau, I.; Lacoste, E.; Gagnon, G. Effects of calcium and thrombin on growth factor release from platelet concentrates: Kinetics and regulation of endothelial cell proliferation. Biomaterials, 2004, 25, 4489-4502.
[49]
Messora, M.R.; Nagata, M.J.; Dornelles, R.C.; Bomfim, S.R.; Furlaneto, F.A.; de Melo, L.G.; Deliberador, T.M.; Bosco, A.F.; Garcia, V.G.; Fucini, S.E. Bone healing in critical-size defects treated with platelet-rich plasma activated by two different methods. A histologic and histometric study in rat calvaria. J. Periodontal Res., 2008, 43, 723-729.
[50]
Matsui, M.; Tabata, Y. Enhanced angiogenesis by multiple release of platelet-rich plasma contents and basic fibroblast growth factor from gelatin hydrogels. Acta Biomater., 2012, 8, 1792-1801.
[51]
Bari, E.; Perteghella, S.; Faragò, S.; Torre, M.L. Association of silk sericin and platelet lysate: Premises for the formulation of wound healing active medications. Int. J. Biol. Macromol., 2018, 119, 37-47.
[52]
Sandri, G.; Bonferoni, M.C.; Rossi, S.; Ferrari, F.; Mori, M.; Del Fante, C.; Perotti, C.; Scudeller, L.; Caramella, C. Platelet lysate formulations based on mucoadhesive polymers for the treatment of corneal lesions. J. Pharm. Pharmacol., 2011, 63, 189-198.
[53]
Sandri, G.; Bonferoni, M.C.; Rossi, S.; Ferrari, F.; Mori, M.; Del Fante, C.; Perotti, C.; Caramella, C. Thermosensitive eyedrops containing platelet lysate for the treatment of corneal ulcers. Int. J. Pharm., 2012, 426, 1-6.
[54]
Bonferoni, M.C.; Sandri, G.; Rossi, S.; Dellera, E.; Invernizzi, A.; Boselli, C.; Icaro Cornaglia, A.; Del Fante, C.; Perotti, C.; Vigani, B.; Riva, F.; Caramella, C.; Ferrari, F. Association of alpha tocopherol and Ag sulfadiazine chitosan oleate nanocarriers in bioactive dressings supporting platelet lysate application to skin wounds. Mar. Drugs, 2018, 16, E56.
[55]
Caccavo, D.; Cascone, S.; Lamberti, G.; Barba, A.A.; Larsson, A. Drug delivery from hydrogels: A general framework for the release modeling. Curr. Drug Deliv., 2017, 14, 179-189.
[56]
Kikuchi, I.S.; Cardoso Galante, R.S.; Dua, K.; Malipeddi, V.R.; Awasthi, R.; Ghisleni, D.D.M.; de Jesus Andreoli, P.T. Hydrogel based drug delivery systems: A review with special emphasis on challenges associated with decontamination of hydrogels and biomaterials. Curr. Drug Deliv., 2017, 14, 917-925.
[57]
Vedadghavami, A.; Minooei, F.; Mohammadi, M.H.; Khetani, S.; Rezaei Kolahchi, A.; Mashayekhan, S.; Sanati-Nezhad, A. Manufacturing of hydrogel biomaterials with controlled mechanical properties for tissue engineering applications. Acta Biomater., 2017, 62, 42-63.
[58]
Guan, X.; Avci-Adali, M.; Alarçin, E.; Cheng, H.; Kashaf, S.S.; Li, Y.; Chawla, A.; Jang, H.L.; Khademhosseini, A. Development of hydrogels for regenerative engineering. Biotechnol. J., 2017, 12(5)
[http://dx.doi.org/10.1002/biot.201600394]
[59]
Liu, Y.; He, W.; Zhang, Z.; Lee, B.P. Recent development in tough hydrogels for biomedical applications. Gels, 2018, 4, 46.
[60]
Kondo, S.; Kuroyanagi, Y. Development of a wound dressing composed of hyaluronic acid and collagen sponge with epidermal growth factor. J. Biomater. Sci. Polym. Ed., 2012, 23, 629-643.
[61]
Mori, M.; Rossi, S.; Ferrari, F.; Bonferoni, M.C.; Sandri, G.; Chlapanidas, T.; Torre, M.L.; Caramella, C. Sponge-like dressings based on the association of chitosan and sericin for the treatment of chronic skin ulcers. I. design of experiments-assisted development. J. Pharm. Sci., 2016, 105, 1180-1187.
[62]
Flores, C.; Lopez, M.; Tabary, N.; Neut, C.; Chai, F.; Betbeder, D.; Herkt, C.; Cazaux, F.; Gaucher, V.; Martel, B.; Blanchemain, N. Preparation and characterization of novel chitosan and β-cyclodextrin polymer sponges for wound dressing applications. Carbohydr. Polym., 2017, 173, 535-546.
[63]
Ranjan, S.; Fontana, F.; Ullah, H.; Hirvonen, J.; Santos, H.A. Microparticles to enhance delivery of drugs and growth factors into wound sites. Ther. Deliv., 2016, 7, 711-732.
[64]
Chakrabarti, S.; Chattopadhyay, P.; Islam, J.; Ray, S.; Raju, P.S.; Mazumder, B. Aspects of nanomaterials in wound healing. Curr. Drug Deliv., 2019, 16, 26-41.
[65]
Parani, M.; Lokhande, G.; Singh, A.; Gaharwar, A.K. Engineered nanomaterials for infection control and healing acute and chronic wounds. ACS Appl. Mater. Interfaces, 2016, 8, 10049-10069.
[66]
Vijayakumar, V.; Samal, S.K.; Mohanty, S.; Nayak, S.K. Recent advancements in biopolymer and metal nanoparticle-based materials in diabetic wound healing management. Int. J. Biol. Macromol., 2019, 122, 137-148.
[67]
Torres-Martinez, E.J.; Cornejo, B.J.M.; Serrano, M.A.; Pérez González, G.L.; Villarreal, G.L.J. A summary of electrospun nanofibers as drug delivery system: Drugs loaded and biopolymers used as matrices. Curr. Drug Deliv., 2018, 15, 1360-1374.
[68]
Singh, A.; Rath, G.; Singh, R.; Goyal, A.K. Nanofibers: An effective tool for controlled and sustained drug delivery. Curr. Drug Deliv., 2018, 15, 155-166.
[69]
Liu, M.; Duan, X.P.; Li, Y.M.; Yang, D.P.; Long, Y.Z. Electrospun nanofibers for wound healing. Mater. Sci. Eng. C Mater. Biol. Appl., 2017, 76, 1413-1423.
[70]
Nimal, T.R.; Baranwal, G.; Bavya, M.C.; Biswas, R.; Jayakumar, R. Anti-staphylococcal activity of injectable nano tigecycline/chitosan-PRP composite hydrogel using drosophila melanogaster model for infectious wounds. ACS Appl. Mater. Interfaces, 2016, 8, 22074-22083.
[71]
Notodihardjo, P.V.; Morimoto, N.; Kakudo, N.; Matsui, M.; Sakamoto, M.; Liem, P.H.; Suzuki, K.; Tabata, Y.; Kusumoto, K. Gelatin hydrogel impregnated with platelet-rich plasma releasate promotes angiogenesis and wound healing in murine Model. J. Artif. Organs, 2015, 18, 64-71.
[72]
Santo, V.E.; Babo, P.; Amador, M.; Correia, C.; Cunha, B.; Coutinho, D.F.; Neves, N.M.; Mano, J.F.; Reis, R.L.; Gomes, M.E. Engineering enriched microenvironments with gradients of platelet lysate in hydrogel fibers. Biomacromolecules, 2016, 17, 1985-1997.
[73]
Rossi, S.; Faccendini, A.; Bonferoni, M.C.; Ferrari, F.; Sandri, G.; Del Fante, C.; Perotti, C.; Caramella, C.M. “Sponge-like” dressings based on biopolymers for the delivery of platelet lysate to skin chronic wounds. Int. J. Pharm., 2013, 440, 207-215.
[74]
Mori, M.; Rossi, S.; Ferrari, F.; Bonferoni, M.C.; Sandri, G.; Riva, F.; Tenci, M.; Del Fante, C.; Nicoletti, G.; Caramella, C. Sponge-like dressings based on the association of chitosan and sericin for the treatment of chronic skin ulcers. II. loading of the hemoderivative platelet lysate. J. Pharm. Sci., 2016, 105, 1188-1195.
[75]
Tenci, M.; Rossi, S.; Bonferoni, M.C.; Sandri, G.; Boselli, C.; Di Lorenzo, A.; Daglia, M.; Icaro Cornaglia, A.; Gioglio, L.; Perotti, C.; Caramella, C.M.; Ferrari, F. Particulate systems based on pectin/chitosan association for the delivery of manuka honey components and platelet lysate in chronic skin ulcers. Int. J. Pharm., 2016, 509, 59-70.
[76]
Lima, A.C.; Mano, J.F.; Concheiro, A.; Alvarez-Lorenzo, C. Fast and mild strategy, using superhydrophobic surfaces, to produce collagen/platelet lysate gel beads for skin regeneration. Stem Cell Rev., 2015, 11, 161-179.
[77]
Mori, M.; Rossi, S.; Bonferoni, M.C.; Ferrari, F.; Sandri, G.; Riva, F.; Del Fante, C.; Perotti, C.; Caramella, C. Calcium alginate particles for the combined delivery of platelet lysate and vancomycin hydrochloride in chronic skin ulcers. Int. J. Pharm., 2014, 461, 505-513.
[78]
Takabayashi, Y.; Ishihara, M.; Sumi, Y.; Takikawa, M.; Nakamura, S.; Kiyosawa, T. Platelet-rich plasma-containing fragmin-protamine micro-nanoparticles promote epithelialization and angiogenesis in split-thickness skin graft donor sites. J. Surg. Res., 2015, 193, 483-491.
[79]
Fontana, F.; Mori, M.; Riva, F.; Mäkilä, E.; Liu, D.; Salonen, J.; Nicoletti, G.; Hirvonen, J.; Caramella, C.; Santos, H.A. Platelet lysate-modified porous silicon microparticles for enhanced cell proliferation in wound healing applications. ACS Appl. Mater. Interfaces, 2016, 13, 988-996.
[80]
Sandri, G.; Bonferoni, M.C.; D’Autilia, F.; Rossi, S.; Ferrari, F.; Grisoli, P.; Sorrenti, M.; Catenacci, L.; Del Fante, C.; Perotti, C.; Caramella, C. Wound dressings based on silver sulfadiazine SLN for tissue repairing. Eur. J. Pharm. Biopharm., 2013, 84, 84-90.
[81]
Bonferoni, M.C.; Sandri, G.; Dellera, E.; Rossi, S.; Ferrari, F.; Mori, M.; Caramella, C. Ionic polymeric micelles based on chitosan and fatty acids and intended for wound healing. Comparison of linoleic and oleic acid. Eur. J. Pharm. Biopharm., 2014, 87, 101-106.
[82]
Bonferoni, M.C.; Riva, F.; Invernizzi, A.; Dellera, E.; Sandri, G.; Rossi, S.; Marrubini, G.; Bruni, G.; Vigani, B.; Caramella, C.; Ferrari, F. Alpha tocopherol loaded chitosan oleate nanoemulsions for wound healing. Evaluation on cell lines and ex vivo human biopsies, and stabilization in spray dried Trojan microparticles. Eur. J. Pharm. Biopharm., 2018, 123, 31-41.
[83]
Pignatelli, C.; Perotto, G.; Nardini, M.; Cancedda, R.; Mastrogiacomo, M.; Athanassiou, A. Electrospun silk fibroin fibers for storage and controlled release of human platelet lysate. Acta Biomater., 2018, 73, 365-376.
[84]
Bertoncelj, V.; Pelipenko, J.; Kristl, J.; Jeras, M.; Cukjati, M.; Kocbek, P. Development and bioevaluation of nanofibers with blood-derived growth factors for dermal wound healing. Eur. J. Pharm. Biopharm., 2014, 88, 64-74.
[85]
Chlapanidas, T.; Perteghella, S.; Faragò, S.; Boschi, A.; Tripodo, G.; Vigani, B.; Crivelli, B.; Renzi, S.; Dotti, S.; Preda, S.; Marazzi, M.; Torre, M.L.; Ferrari, M. Platelet lysate and adipose mesenchymal stromal cells on silk fibroin nonwoven mats for wound healing. J. Appl. Polym. Sci., 2016, 133, art 43371.
[86]
Kutlu, B.; Tigli, A.R.S.; Akman, A.C.; Gumusderelioglu, M.; Nohutcu, R.M. Platelet-rich plasma-loaded chitosan scaffolds: Preparation and growth factor release kinetics. J. Biomed. Mater. Res. Part B, 2013, 101, 28-35.
[87]
Ito, R.; Morimoto, N.; Pham, L.H.; Taira, T.; Kawai, K.; Suzuki, S. Efficacy of the controlled release of concentrated platelet lysate from a collagen/gelatin scaffold for dermis-like tissue regeneration. Tissue Eng. Part A, 2013, 19, 1398-1405.
[88]
Sandri, G.; Bonferoni, M.C.; Rossi, S.; Ferrari, F.; Mori, M.; Cervio, M.; Riva, F.; Liakos, I.; Athanassiou, A.; Saporito, F.; Marini, L.; Caramella, C. Platelet lysate embedded scaffolds for skin regeneration. Expert Opin. Drug Deliv., 2015, 12, 525-554.
[89]
Brown, B.N.; Valentin, J.E.; Stewart-Akers, A.M.; McCabe, G.P.; Badylak, S.F. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials, 2009, 30, 1482-1491.
[90]
Vats, A.; Tolley, N.S.; Polak, J.M.; Gough, J.E. Scaffolds and biomaterials for tissue engineering: A review of clinical applications. Clin. Otolaryngol. Allied Sci., 2003, 28, 165-172.
[91]
Lu, B.; Wang, T.; Li, Z.; Dai, F.; Lv, L.; Tang, F.; Yu, K.; Liu, J.; Lan, G. Healing of skin wounds with a chitosan-gelatin sponge loaded with tannins and platelet-rich plasma. Int. J. Biol. Macromol., 2016, 82, 884-891.
[92]
Jeon, O.; Kang, S.W.; Lim, H.W.; Hyung Chung, J.; Kim, B.S. Long-term and zero-order release of basic fibroblast growth factor from heparin-conjugated poly(L-lactide-co-glycolide) nanospheres and fibrin gel. Biomaterials, 2006, 27, 1598-1607.
[93]
Yang, H.S.; Bhang, S.H.; Hwang, J.W.; Kim, D.I.; Kim, B.S. Delivery of basic fibroblast growth factor using heparin-conjugated fibrin for therapeutic angiogenesis. Tissue Eng. Part A, 2010, 16, 2113-2119.
[94]
Schultz, G.S.; Wysocki, A. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen., 2009, 17, 153-162.
[95]
Yang, H.S.; Shin, J.; Bhang, S.H.; Shin, J.Y.; Park, J.; Im, G.I.; Kim, C.S.; Kim, B.S. Enhanced skin wound healing by a sustained release of growth factors contained in platelet-rich plasma. Exp. Mol. Med., 2011, 43, 622-629.
[96]
La, W.G.; Yang, H.S. Heparin-conjugated poly(lactic-co-glycolic acid) nanospheres enhance large-wound healing by delivering growth factors in platelet-rich plasma. Artif. Organs, 2015, 39, 388-394.
[97]
Takikawa, M.; Nakamura, S.; Nakamura, S.; Nambu, M.; Ishihara, M.; Fujita, M.; Kishimoto, S.; Doumoto, T.; Yanagibayashi, S.; Azuma, R.; Yamamoto, N.; Kiyosawa, T. Enhancement of vascularization and granulation tissue formation by growth factors in human platelet-rich plasma containing fragmin/protamine microparticles. J. Biomed. Mater. Res. B Appl. Biomater., 2011, 97, 373-380.
[98]
Diaz-Gomez, L.; Alvarez-Lorenzo, C.; Concheiro, A.; Silva, M.; Dominguez, F.; Sheikh, F.A.; Cantu, T.; Desai, R.; Garcia, V.L.; Macossay, J. Biodegradable electrospun nanofibers coated with platelet-rich plasma for cell adhesion and proliferation. Mater. Sci. Eng. C Mater. Biol. Appl., 2014, 40, 180-188.
[99]
Oliveira, J.T.; Gardel, L.S.; Rada, T.; Martins, L.; Gomes, M.E.; Reis, R.L. Injectable gellan gum hydrogels with autologous cells for the treatment of rabbit articular cartilage defects. J. Orthop. Res., 2010, 28, 1193-1199.
[100]
Silva-Correia, J.; Oliveira, J.M.; Caridade, S.G.; Oliveira, J.T.; Sousa, R.A.; Mano, J.F.; Reis, R.L. Gellan gum-based hydrogels for intervertebral disc tissue-engineering applications. J. Tissue Eng. Regener. Med., 2011, 5(6), e97-e107.
[101]
Esposito, E.; Pecorelli, A.; Sguizzato, M.; Drechsler, M.; Mariani, P.; Carducci, F.; Cervellati, F.; Nastruzzi, C.; Cortesi, R.; Valacchi, G. Production and characterization of nanoparticle based hyaluronate gel containing retinyl palmitate for wound healing. Curr. Drug Deliv., 2018, 15, 1172-1182.
[102]
Rossi, S.; Mori, M.; Vigani, B.; Bonferoni, M.C.; Sandri, G.; Riva, F.; Caramella, C.; Ferrari, F.; Del Fante, C.; Perotti, C.; Caramella, C.M. A novel dressing for the combined delivery of platelet lysate and vancomycin hydrochloride to chronic skin ulcers: Hyaluronic acid particles in alginate matrices. Eur. J. Pharm. Sci., 2018, 118, 87-95.
[103]
Dellera, E.; Bonferoni, M.C.; Sandri, G.; Rossi, S.; Ferrari, F.; Del Fante, C.; Perotti, C.; Grisoli, P.; Caramella, C. Development of chitosan oleate ionic micelles loaded with silver sulfadiazine to be associated with platelet lysate for application in wound healing. Eur. J. Pharm. Biopharm., 2014, 88, 643-650.
[104]
Bonferoni, M.C.; Sandri, G.; Rossi, S.; Usai, D.; Liakos, I.; Garzoni, A.; Fiamma, M.; Zanetti, S.; Athanassiou, A.; Caramella, C.; Ferrari, F. A novel ionic amphiphilic chitosan derivative as a stabilizer of nanoemulsions: Improvement of antimicrobial activity of Cymbopogon citratus essential oil. Colloids Surf. B Biointerfaces, 2017, 152, 385-392.
[105]
Shen, E.C.; Chou, T.C.; Gau, C.H.; Tu, H.P.; Chen, Y.T.; Fu, E. Releasing growth factors from activated human platelets after chitosan stimulation: A possible biomaterial for platelet-rich plasma preparation. Clin. Oral Implants Res., 2006, 17, 572-578.