Delivery systems for growth factors and cytokines in the treatment of chronic skin wounds

Abstract

Chronic wounds are characterized by a wide prevalence, high mortality rate, complex and expensive treatment. Characteristic features of non-healing wounds are prolonged inflammation, dysfunction of immune cell regulation, and imbalance in the secretion of growth factors and cytokines. All this leads to impaired healing processes and restoration of skin functions. Current research demonstrates the importance of studying the influence of growth factors and cytokines on the process of repair of chronic skin wounds, and the importance of developing ways to use integrated therapies to deliver bioactive substances to injury site. Different types of encapsulating forms represent a promising and effective system for the delivery of drugs that have a stimulating effect on the wound healing process. Hydrogels provide controlled release and protect bioactive molecules from protease degradation. This review examines the role of immune cells in the pathogenesis of chronic skin wounds and their interactions with cytokines and growth factors in the reparative process of chronic skin injuries. The review article evaluates modern approaches to the use of various biomaterials for the delivery of cytokines, which, on the one hand, ensures their retention, stabilization and protection from degradation, and on the other hand, promotes the closure and healing of the wound surface.

Keywords

chronic injury / immunomodulatory therapy / skin injuries / cytokines / delivery systems

References

[1] Gain J, Gerasimenko M, Shakhrai S, et al. Modern sights at the reasons of occurrence and chronic wound pathogenesis. Innovatsionnye tekhnologii v meditsine. 2017;4:208–222. EDN: ZWJFYT

[2] Гаин Ю.М., Герасименко М.А., Шахрай С.В., и др. Современные взгляды на причины возникновения и патогенез хронической раны // Инновационные технологии в медицине. 2017. Т. 4. С. 208–222. EDN: ZWJFYT

[3] Kapp S, Miller C, Santamaria N. The quality of life of people who have chronic wounds and who self-treat. Journal of Clinical Nursing. 2018;27(1-2):182–192. doi: 10.1111/jocn.13870

[4] Kapp S., Miller C., Santamaria N. The quality of life of people who have chronic wounds and who self-treat // Journal of Clinical Nursing. 2018. Vol. 27, N 1-2. P. 182–192. doi: 10.1111/jocn.13870

[5] Heras KL, Igartua M, Santos-Vizcaino E, Hernandez RM. Chronic wounds: current status, available strategies and emerging therapeutic solutions. Journal of Controlled Release. 2020;328:532–550. doi: 10.1016/j.jconrel.2020.09.039

[6] Heras K.L., Igartua M., Santos-Vizcaino E., Hernandez R.M. Chronic wounds: current status, available strategies and emerging therapeutic solutions // Journal of Сontrolled Release. 2020. Vol. 328. P. 532–550. doi: 10.1016/j.jconrel.2020.09.039

[7] Slavnikov IA, Dundarov ZA, Yarets YI. Clinical and morphological features of acute and chronic wounds. Journal of the Grodno State Medical University. 2021;19(1):55–63. doi: 10.25298/2221-8785-2021-19-1-55-63

[8] Славников И.А., Дундаров З.А., Ярец Ю.И. Клинико-морфологические особенности острых и хронических ран // Журнал Гродненского государственного медицинского университета. 2021. Т. 19, № 1. С. 55–63. doi: 10.25298/2221-8785-2021-19-1-55-63

[9] Bowers S, Franco E. Chronic wounds: evaluation and management. American Family Physician. 2020;101(3):159–166.

[10] Bowers S., Franco E. Chronic wounds: evaluation and management // American Family Physician. 2020. Vol. 101, N 3. P. 159–166.

[11] Kathawala MH, Ng WL, Liu D, et al. Healing of chronic wounds: an update of recent developments and future possibilities. Tissue Engineering. Part B, Reviews. 2019;25(5):429–444. doi: 10.1089/ten.teb.2019.0019

[12] Kathawala M.H., Ng W.L., Liu D., et al. Healing of chronic wounds: an update of recent developments and future possibilities // Tissue Engineering. Part B, Reviews. 2019. Vol. 25, N 5. P. 429–444. doi: 10.1089/ten.teb.2019.0019

[13] Cañedo-Dorantes L, Cañedo-Ayala M. Skin acute wound healing: a comprehensive review. International Journal of Inflammation. 2019;2019:3706315. doi: 10.1155/2019/3706315

[14] Cañedo-Dorantes L., Cañedo-Ayala M. Skin acute wound healing: a comprehensive review // International Journal of Inflammation. 2019. Vol. 2019. P. 3706315. doi: 10.1155/2019/3706315

[15] Cutolo M, Campitiello R, Gotelli E, et al. The role of M1/M2 macrophage polarization in rheumatoid arthritis synovitis. Frontiers in Immunology. 2022;13:867260. doi: 10.3389/fimmu.2022.867260

[16] Cutolo M., Campitiello R., Gotelli E., et al. The role of M1/M2 macrophage polarization in rheumatoid arthritis synovitis // Frontiers in Immunology. 2022. Vol. 13. P. 867260. doi: 10.3389/fimmu.2022.867260

[17] Karppinen SM, Heljasvaara R, Gullberg D, Tasanen K, Pihlajaniemi T. Toward understanding scarless skin wound healing and pathological scarring. F1000Research. 2019;8:787. doi: 10.12688/f1000research.18293.1

[18] Karppinen S.-M., Heljasvaara R., Gullberg D., Tasanen K., Pihlajaniemi T. Toward understanding scarless skin wound healing and pathological scarring // F1000Research. 2019. Vol. 8. P. 787. doi: 10.12688/f1000research.18293.1

[19] Sorg H, Sorg CGG. Skin wound healing: of players, patterns, and processes. European Surgical Research. 2023;64(2):141–157. doi: 10.1159/000528271

[20] Sorg H., Sorg C.G.G. Skin wound healing: of players, patterns, and processes // European Surgical Research. 2023. Vol. 64, N 2. P. 141–157. doi: 10.1159/000528271

[21] Melkonyan KI, Alekseenko SN, Bykov IM. Comparative evaluation of efficiency of burn wound healing with derma-based hydrogel: a preclinical experimental study. Kuban Scientific Medical Bulletin. 2023;30(6):15–27. doi: 10.25207/1608-6228-2023-30-6-15-27

[22] Мелконян К.И., Алексеенко С.Н., Быков И.М. Сравнительная оценка эффективности репарации ожоговых ран при применении гидрогелевого материала на основе дермы: доклиническое экспериментальное исследование // Кубанский научный медицинский вестник. 2023. Т. 30, № 6. С. 15–27. doi: 10.25207/1608-6228-2023-30-6-15-27

[23] Aitcheson SM, Frentiu FD, Hurn SE, Edwards K, Murray RZ. Skin wound healing: normal macrophage function and macrophage dysfunction in diabetic wounds. Molecules. 2021;26(16):4917. doi: 10.3390/molecules26164917

[24] Aitcheson S.M., Frentiu F.D., Hurn S.E., Edwards K., Murray R.Z. Skin wound healing: normal macrophage function and macrophage dysfunction in diabetic wounds // Molecules. 2021. Vol. 26, N 16. P. 4917. doi: 10.3390/molecules26164917

[25] Short WD, Wang X, Keswani SG. The role of T lymphocytes in cutaneous scarring. Advances in Wound Care. 2022;11(3):121–131. doi: 10.1089/wound.2021.0059

[26] Short W.D., Wang X., Keswani S.G. The role of T lymphocytes in cutaneous scarring // Advances in Wound Care. 2022. Vol. 11, N 3. P. 121–131. doi: 10.1089/wound.2021.0059

[27] Papadopoulou M, Sanchez Sanchez G, Vermijlen D. Innate and adaptive γδ T cells: How, when, and why. Immunological Reviews. 2020;298(1):99–116. doi: 10.1111/imr.12926

[28] Papadopoulou M., Sanchez Sanchez G., Vermijlen D. Innate and adaptive γδ T cells: How, when, and why // Immunological Reviews. 2020. Vol. 298, N. 1. P. 99–116. doi: 10.1111/imr.12926

[29] Morton LM, Phillips TJ. Wound healing and treating wounds: Differential diagnosis and evaluation of chronic wounds. Journal of the American Academy of Dermatology. 2016;74(4):589–605. doi: 10.1016/j.jaad.2015.08.068

[30] Morton L.M., Phillips T.J. Wound healing and treating wounds: Differential diagnosis and evaluation of chronic wounds // Journal of the American Academy of Dermatology. 2016. Vol. 74, N 4. P. 589–605. doi: 10.1016/j.jaad.2015.08.068

[31] Raziyeva K, Kim Y, Zharkinbekov Z, et al. Immunology of acute and chronic wound healing. Biomolecules. 2021;11(5):700. doi: 10.3390/biom11050700

[32] Raziyeva K., Kim Y., Zharkinbekov Z., et al. Immunology of acute and chronic wound healing // Biomolecules. 2021. Vol. 11, N 5. P. 700. doi: 10.3390/biom11050700

[33] Song J, Hu L, Liu B, et al. The emerging role of immune cells and targeted therapeutic strategies in diabetic wounds healing. Journal of Inflammation Research. 2022;15:4119–4138. doi: 10.2147/JIR.S371939

[34] Song J., Hu L., Liu B., et al. The emerging role of immune cells and targeted therapeutic strategies in diabetic wounds healing // Journal of Inflammation Research. 2022. Vol. 15. P. 4119–4138. doi: 10.2147/JIR.S371939

[35] Galkowska H, Wojewodzka U, Olszewski WL. Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair and Regeneration. 2006;14(5):558–565. doi: 10.1111/j.1743-6109.2006.00155.x

[36] Galkowska H., Wojewodzka U., Olszewski W.L. Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers // Wound Repair and Regeneration. 2006. Vol. 14, N 5. P. 558–565. doi: 10.1111/j.1743-6109.2006.00155.x

[37] Cruz MS, Diamond A, Russell A, et al. Human αβ and γδ T cells in skin immunity and disease. Frontiers in Immunology. 2018;9:1304. doi: 10.3389/fimmu.2018.01304

[38] Cruz M.S., Diamond A., Russell A., et al. Human αβ and γδ T cells in skin immunity and disease // Frontiers in Immunology. 2018. Vol. 9. P. 1304. doi: 10.3389/fimmu.2018.01304

[39] Las Heras K, Igartua M, Santos-Vizcaino E, Hernandez RM. Chronic wounds: Current status, available strategies and emerging therapeutic solutions. Journal of Controlled Release. 2020;328:532–550. doi: 10.1016/j.jconrel.2020.09.039

[40] Las Heras K., Igartua M., Santos-Vizcaino E., Hernandez R.M. Chronic wounds: Current status, available strategies and emerging therapeutic solutions // Journal of Controlled Release. 2020. Vol. 328. P. 532–550. doi: 10.1016/j.jconrel.2020.09.039

[41] Eriksson E, Liu PY, Schultzet GS, et al. Chronic wounds: Treatment consensus. Wound Repair and Regeneration. 2022;30(2):156–171. doi: 10.1111/wrr.12994

[42] Eriksson E., Liu P.Y., Schultzet G.S., et al. Chronic wounds: Treatment consensus // Wound Repair and Regeneration. 2022. Vol. 30, N 2. P. 156–171. doi: 10.1111/wrr.12994

[43] Nakkala JR, Li Z, Ahmad W, Wang K, Gao C. Immunomodulatory biomaterials and their application in therapies for chronic inflammation-related diseases. Acta biomaterialia. 2021;123:1–30. doi: 10.1016/j.actbio.2021.01.025

[44] Nakkala J.R., Li Z., Ahmad W., Wang K., Gao C. Immunomodulatory biomaterials and their application in therapies for chronic inflammation-related diseases // Acta Biomaterialia. 2021. Vol. 123. P. 1–30. doi: 10.1016/j.actbio.2021.01.025

[45] Heydari P, Kharaziha M, Varshosaz J, Javanmard SH. Current knowledge of immunomodulation strategies for chronic skin wound repair. Journal of Biomedical Materials Research. Part B, Applied Biomaterials. 2022;110(2):265–288. doi: 10.1002/jbm.b.34921

[46] Heydari P., Kharaziha M., Varshosaz J., Javanmard S.H. Current knowledge of immunomodulation strategies for chronic skin wound repair // Journal of Biomedical Materials Research. Part B, Applied Biomaterials. 2022. Vol. 110, N 2. P. 265–288. doi: 10.1002/jbm.b.34921

[47] Catanzano O, Quaglia F, Boateng JS. Wound dressings as growth factor delivery platforms for chronic wound healing. Expert Opinion on Drug Delivery. 2021;18(6):737–759. doi: 10.1080/17425247.2021.1867096

[48] Catanzano O., Quaglia F., Boateng J.S. Wound dressings as growth factor delivery platforms for chronic wound healing // Expert Opinion on Drug Delivery. 2021. Vol. 18, N 6. P. 737–759. doi: 10.1080/17425247.2021.1867096

[49] Mazini L, Rochette L, Hamdan Y, Malka G. Skin immunomodulation during regeneration: emerging new targets. Journal of Personalized Medicine. 2021;11(2):85. doi: 10.3390/jpm11020085

[50] Mazini L., Rochette L., Hamdan Y., Malka G. Skin immunomodulation during regeneration: emerging new targets // Journal of Personalized Medicine. 2021. Vol. 11, N 2. P. 85. doi: 10.3390/jpm11020085

[51] Yamakawa S, Hayashida K. Advances in surgical applications of growth factors for wound healing. Burns & Trauma. 2019;7:10. doi: 10.1186/s41038-019-0148-1

[52] Yamakawa S., Hayashida K. Advances in surgical applications of growth factors for wound healing // Burns & Trauma. 2019. Vol. 7. P. 10. doi: 10.1186/s41038-019-0148-1

[53] Park JW, Hwang SR, Yoon IS. Advanced growth factor delivery systems in wound management and skin regeneration. Molecules. 2017;22(8):1259. doi: 10.3390/molecules22081259

[54] Park J.W., Hwang S.R., Yoon I.-S. Advanced growth factor delivery systems in wound management and skin regeneration // Molecules. 2017. Vol. 22, N 8. P. 1259. doi: 10.3390/molecules22081259

[55] Hachim D, Whittaker TE, Kim H, Stevens MM. Glycosaminoglycan-based biomaterials for growth factor and cytokine delivery: Making the right choices. Journal of Controlled Release. 2019;313:131–147. doi: 10.1016/j.jconrel.2019.10.018

[56] Hachim D., Whittaker T.E., Kim H., Stevens M.M. Glycosaminoglycan-based biomaterials for growth factor and cytokine delivery: Making the right choices // Journal of Controlled Release. 2019. Vol. 313. P. 131–147. doi: 10.1016/j.jconrel.2019.10.018

[57] Zhang X, Kang X, Jin L, et al. Stimulation of wound healing using bioinspired hydrogels with basic fibroblast growth factor (bFGF). International Journal of Nanomedicine. 2018;13:3897–3906. doi: 10.2147/ijn.s168998

[58] Zhang X., Kang X., Jin L., et al. Stimulation of wound healing using bioinspired hydrogels with basic fibroblast growth factor (bFGF) // International Journal of Nanomedicine. 2018. Vol. 13. P. 3897–3906. doi: 10.2147/ijn.s168998

[59] Xu HL, Chen PP, Wang LF, et al. Skin-permeable liposome improved stability and permeability of bFGF against skin of mice with deep second degree scald to promote hair follicle neogenesis through inhibition of scar formation. Colloids and surfaces. B, Biointerfaces. 2018;172:573–585. doi: 10.1016/j.colsurfb.2018.09.006

[60] Xu H.L., Chen P.P., Wang L.-F., et al. Skin-permeable liposome improved stability and permeability of bFGF against skin of mice with deep second degree scald to promote hair follicle neogenesis through inhibition of scar formation // Colloids and surfaces. B, Biointerfaces. 2018. Vol. 172. P. 573–585. doi: 10.1016/j.colsurfb.2018.09.006

[61] Joshi A, Xu Z, Ikegami Y, et al. Exploiting synergistic effect of externally loaded bFGF and endogenous growth factors for accelerated wound healing using heparin functionalized PCL/gelatin co-spun nanofibrous patches. Chemical Engineering Journal. 2021;404:126518. doi: 10.1016/j.cej.2020.126518

[62] Joshi A., Xu Z., Ikegami Y., et al. Exploiting synergistic effect of externally loaded bFGF and endogenous growth factors for accelerated wound healing using heparin functionalized PCL/gelatin co-spun nanofibrous patches // Chemical Engineering Journal. 2021. Vol. 404. P. 126518. doi: 10.1016/j.cej.2020.126518

[63] Liu T, Dan W, Dan NA, et al. A novel grapheme oxide-modified collagen-chitosan bio-film for controlled growth factor release in wound healing applications. Materials Science & Engineering. C, Materials for Biological Applications. 2017;77:202–211. doi: 10.1016/j.msec.2017.03.256

[64] Liu T., Dan W., Dan N.A. et al. A novel grapheme oxide-modified collagen-chitosan bio-film for controlled growth factor release in wound healing applications // Materials Science & Engineering. C, Materials for Biological Applications. 2017. Vol. 77. P. 202–211. doi: 10.1016/j.msec.2017.03.256

[65] Wu J, Zhu J, He C. Comparative study of heparin-poloxamer hydrogel modified bFGF and aFGF for in vivo wound healing efficiency. ACS Applied Materials & Interfaces. 2016;8(29):18710–18721. doi: 10.1021/acsami.6b06047

[66] Wu J., Zhu J., He C., et al. Comparative study of heparin-poloxamer hydrogel modified bFGF and aFGF for in vivo wound healing efficiency // ACS Applied Materials & Interfaces. 2016. Vol. 8, N 29. P. 18710–18721. doi: 10.1021/acsami.6b06047

[67] Hui Q, Zhang L, Yang X, et al. Higher biostability of rh-aFGF-carbomer 940 hydrogel and its effect on wound healing in a diabetic rat model. ACS Biomaterials Science & Engineering. 2018;4(5):1661–1668. doi: 10.1021/acsbiomaterials.8b00011

[68] Hui Q., Zhang L., Yang X., et al. Higher biostability of rh-aFGF-carbomer 940 hydrogel and its effect on wound healing in a diabetic rat model // ACS Biomaterials Science & Engineering. 2018. Vol. 4, N 5. P. 1661–1668. doi: 10.1021/acsbiomaterials.8b00011

[69] Jeong S, Kim B, Park M, et al. Improved diabetic wound healing by EGF encapsulation in gelatin-alginate coacervates. Pharmaceutics. 2020;12(4):334. doi: 10.3390/pharmaceutics12040334

[70] Jeong S., Kim B., Park M., et al. Improved diabetic wound healing by EGF encapsulation in gelatin-alginate coacervates // Pharmaceutics. 2020. Vol. 12, N 4. P. 334. doi: 10.3390/pharmaceutics12040334

[71] Mariia K, Arif M, Shi J, el al. Novel chitosan-ulvan hydrogel reinforcement by cellulose nanocrystals with epidermal growth factor for enhanced wound healing: In vitro and in vivo analysis. International Journal of Biological Macromolecules. 2021;183:435–446. doi: 10.1016/j.ijbiomac.2021.04.156

[72] Mariia K., Arif M., Shi J., et al. Novel chitosan-ulvan hydrogel reinforcement by cellulose nanocrystals with epidermal growth factor for enhanced wound healing: In vitro and in vivo analysis // International Journal of Biological Macromolecules. 2021. Vol. 183. P. 435–446. doi: 10.1016/j.ijbiomac.2021.04.156

[73] Mohanty C, Pradhan J. A human epidermal growth factor-curcumin bandage bioconjugate loaded with mesenchymal stem cell for in vivo diabetic wound healing. Materials Science and Engineering. C, Materials for Biological Applications. 2020;111;110751. doi: 10.1016/j.msec.2020.110751

[74] Mohanty C., Pradhan J. A human epidermal growth factor-curcumin bandage bioconjugate loaded with mesenchymal stem cell for in vivo diabetic wound healing // Materials Science and Engineering. C, Materials for Biological Applications. 2020. Vol. 111. P. 110751. doi: 10.1016/j.msec.2020.110751

[75] Rahman MM, Garcia N, Loh YS., et al. A platelet-derived hydrogel improves neovascularisation in full thickness wounds. Acta Biomaterialia. 2021;136:199–209. doi: 10.1016/j.actbio.2021.09.043

[76] Rahman M.M., Garcia N., Loh, Y.S., et al. A platelet-derived hydrogel improves neovascularisation in full thickness wounds // Acta Biomaterialia. 2021. Vol. 136. P. 199–209. doi: 10.1016/j.actbio.2021.09.043

[77] Li Q, Cui J, Huang H, et al. IGF-1C domain-modified chitosan hydrogel accelerates cutaneous wound healing by promoting angiogenesis. Future Medicinal Chemistry. 2020;12(13):1239–1251. doi: 10.4155/fmc-2020-0071

[78] Li Q., Cui J., Huang H., et al. IGF-1C domain-modified chitosan hydrogel accelerates cutaneous wound healing by promoting angiogenesis // Future Medicinal Chemistry. 2020. Vol. 12, N 13. P. 1239–1251. doi: 10.4155/fmc-2020-0071

[79] Lin MJ, Lu MC, Chang HY. Sustained release of insulin-like growth factor-1 from Bombyx mori L. silk fibroin delivery for diabetic wound therapy. International Journal of Molecular Sciences. 2021;22(12):6267. doi: 10.3390/ijms22126267

[80] Lin M.-J., Lu M.-C., Chang H.-Y. Sustained release of insulin-like growth factor-1 from Bombyx mori L. silk fibroin delivery for diabetic wound therapy // International Journal of Molecular Sciences. 2021. Vol. 22, N 12. P. 6267. doi: 10.3390/ijms22126267

[81] Achar RAN., Silva TC, Achar E, et al. Use of insulin-like growth factor in the healing of open wounds in diabetic and non-diabetic rats. Acta Cirurgica Brasileira. 2014.;29(2):125–131. doi: 10.1590/S0102-86502014000200009

[82] Achar R.A.N., Silva T.C., Achar E., Martines R.B., Machado J.L. Use of insulin-like growth factor in the healing of open wounds in diabetic and non-diabetic rats // Acta Cirurgica Brasileira. 2014. Vol. 29, N 2. P. 125–131. doi: 10.1590/S0102-86502014000200009

[83] Olekson MAP, Faulknor R, Bandekar A, et al. SDF-1 liposomes promote sustained cell proliferation in mouse diabetic wounds. Wound Repair and Regeneration. 2015;23(5):711–723. doi: 10.1111/wrr.12334

[84] Olekson M.A.P, Faulknor R., Bandekar A., et al. SDF-1 liposomes promote sustained cell proliferation in mouse diabetic wounds // Wound Repair and Regeneration. 2015. Vol. 23, N 5. P. 711–723. doi: 10.1111/wrr.12334

[85] Justine RY, Janssen M, Liang BJ, et al. A liposome/gelatin methacrylate nanocomposite hydrogel system for delivery of stromal cell-derived factor-1α and stimulation of cell migration. Acta Biomaterialia. 2020;108:67–76. doi: 10.1016/j.actbio.2020.03.015

[86] Justine R.Y., Janssen M., Liang B.J., Huang H.-C., Fisher J.P. A liposome/gelatin methacrylate nanocomposite hydrogel system for delivery of stromal cell-derived factor-1α and stimulation of cell migration // Acta Biomaterialia. 2020. Vol. 108. P. 67–76. doi: 10.1016/j.actbio.2020.03.015

[87] Yang X, Yang R, Chen M, et al. KGF-2 and FGF-21 poloxamer 407 hydrogel coordinates inflammation and proliferation homeostasis to enhance wound repair of scalded skin in diabetic rats. BMJ Open Diabetes Research and Care. 2020;8(1):e001009. doi: 10.1136/bmjdrc-2019-001009

[88] Yang X., Yang R., Chen M., et al. KGF-2 and FGF-21 poloxamer 407 hydrogel coordinates inflammation and proliferation homeostasis to enhance wound repair of scalded skin in diabetic rats // BMJ Open Diabetes Research and Care. 2020. Vol. 8, N 1. P. e001009. doi: 10.1136/bmjdrc-2019-001009

[89] Muhamed I, Sproul EP, Ligler FS, Brown AC. Fibrin nanoparticles coupled with keratinocyte growth factor enhance the dermal wound-healing rate. ACS Applied Materials & Interfaces. 2019;11(4):3771–3780. doi: 10.1021/acsami.8b21056

[90] Muhamed I., Sproul E.P., Ligler F.S., Brown A.C. Fibrin nanoparticles coupled with keratinocyte growth factor enhance the dermal wound-healing rate // ACS Applied Materials & Interfaces. 2019. Vol. 11, N 4. P. 3771–3780. doi: 10.1021/acsami.8b21056

[91] Smagul S, Kim Y, Smagulova A, et al. Biomaterials loaded with growth factors/cytokines and stem cells for cardiac tissue regeneration. International Journal of Molecular Sciences. 2020;21(17):5952. doi: 10.3390/ijms21175952

[92] Smagul S., Kim Y., Smagulova A., et al. Biomaterials loaded with growth factors/cytokines and stem cells for cardiac tissue regeneration // International Journal of Molecular Sciences. 2020. Vol. 21, N 17. P. 5952. doi: 10.3390/ijms21175952

[93] Vishwakarma A, Bhise NS, Evangelista MB, et al. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends in Biotechnology. 2016;34(6):470–482. doi: 10.1016/j.tibtech.2016.03.009

[94] Vishwakarma A., Bhise N.S., Evangelista M.B., et al. Engineering immunomodulatory biomaterials to tune the inflammatory response // Trends in Biotechnology. 2016. Vol. 34, N 6. P. 470–482. doi: 10.1016/j.tibtech.2016.03.009

[95] Kesharwani P, Bisht A, Alexander A, et al. Biomedical applications of hydrogels in drug delivery system: An update. Journal of Drug Delivery Science and Technology. 2021;66:102914. doi: 10.1016/j.jddst.2021.102914

[96] Kesharwani P., Bisht A., Alexander A., et al. Biomedical applications of hydrogels in drug delivery system: An update // Journal of Drug Delivery Science and Technology. 2021. Vol. 66. P. 102914. doi: 10.1016/j.jddst.2021.102914

[97] Zhang M, Yang M, Woo MW, et al. High-mechanical strength carboxymethyl chitosan-based hydrogel film for antibacterial wound dressing. Carbohydrate Polymers. 2021;256:117590. doi: 10.1016/j.carbpol.2020.117590

[98] Zhang M., Yang M., Woo M.W., et al. High-mechanical strength carboxymethyl chitosan-based hydrogel film for antibacterial wound dressing // Carbohydrate Polymers. 2021. Vol. 256. P. 117590. doi: 10.1016/j.carbpol.2020.117590

[99] Bogomolov MS. Comparative analysis of the efficacy of current dressings in the treatment of venous trophic ulcers. Wounds and Wound Infections. The prof. B.M. Kostyuchenok Journal. 2015;2(4):32–39. doi: 10.17650/2408-9613-2015-2-4-33-39

[100] Богомолов М.С. Сравнительный анализ эффективности современных перевязочных средств при лечении венозных трофических язв // Раны и раневые инфекции. Журнал имени проф. Б.М. Костючёнка. 2015. Т. 2, № 4. С. 32–39. doi: 10.17650/2408-9613-2015-2-4-33-39

[101] Morozov AM, Minakova YuE, Pichugova AN, et al. Experience of the application of local immunostimulating drugs in the treatment of trophic ulcers: a clinical case. Journal of New Medical Technologies, eEdition. 2020;14(1):60–65. doi: 10.24411/2075-4094-2020-16609

[102] Морозов А.М., Минакова Ю.Е., Пичугова А.Н., и др. Опыт применения местных иммуностимулирующих препаратов при лечении трофических язв (клинический случай) // Вестник новых медицинских технологий. Электронное издание. 2020. Т. 14, № 1. С. 60–65. doi: 10.24411/2075-4094-2020-16609

[103] Varyushina EA, Moskalenko EA, Lebedeva TP, et al.. Interleukin-1β application for local treatment of purulent and necrotic lesions of lower extremities. Medical Immunology. 2008;10(4-5):439–448. doi: 10.15789/1563-0625-2008-4-5-439-448

[104] Варюшина Е.А., Москаленко В.В., Лебедева Т.П., и др. Использование интерлейкина-1β для местного лечения гнойно-некротических поражений нижних конечностей // Медицинская иммунология. 2008. Т. 10, № 4-5. С. 439–448. doi: 10.15789/1563-0625-2008-4-5-439-448

[105] Xiong Y, Feng Q, Lu L, et al. Immunomodulatory hydrogels: advanced regenerative tools for diabetic foot ulcer. Advanced Functional Materials. 2023;33(10):2213066. doi: 10.1002/adfm.202213066

[106] Xiong Y., Feng Q., Lu L., et al. Immunomodulatory hydrogels: advanced regenerative tools for diabetic foot ulcer // Advanced Functional Materials. 2023. Vol. 33, N 10. P. 2213066. doi: 10.1002/adfm.202213066

[107] Li S, Dong Q, Peng X, et al. Self-healing hyaluronic acid nanocomposite hydrogels with platelet-rich plasma impregnated for skin regeneration. ACS Nano. 2022;16(7):11346–11359. doi: 10.1021/acsnano.2c05069

[108] Li S., Dong Q., Peng X., et al. Self-healing hyaluronic acid nanocomposite hydrogels with platelet-rich plasma impregnated for skin regeneration // ACS Nano. 2022. Vol. 16, N 7. P. 11346–11359. doi: 10.1021/acsnano.2c05069

[109] Heras KL, Igartua M, Santos-Vizcaino E, Hernandez RM. Chronic wounds: current status, available strategies and emerging therapeutic solutions. Journal of Controlled Release. 2020;328:532–550. doi: 10.1016/j.jconrel.2020.09.039

[110] Heras K.L., Igartua M., Santos-Vizcaino E., Hernandez R.M. Chronic wounds: current status, available strategies and emerging therapeutic solutions // Journal of Controlled Release. 2020. Vol. 328. P. 532–550. doi: 10.1016/j.jconrel.2020.09.039

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