Hypoxic environment of wounds and photosynthesis-based oxygen therapy

Shuning Tian , Shenyu Tan , Mingjie Fan , Wenlin Gong , Tianchang Yang , Fangwen Jiao , Hongzhi Qiao

Burns & Trauma ›› 2024, Vol. 12 ›› Issue (1) : tkae012

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Burns & Trauma ›› 2024, Vol. 12 ›› Issue (1) :tkae012 DOI: 10.1093/burnst/tkae012
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Hypoxic environment of wounds and photosynthesis-based oxygen therapy
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Abstract

The hypoxic environment is among the most important factors that complicates the healing of chronic wounds, such as venous leg ulcers, pressure injuries and diabetic foot ulcers, which seriously affects the quality of life of patients. Various oxygen supply treatments are used in clinical practice to improve the hypoxic environment at the wound site. However, problems still occur, such as insufficient oxygen supply, short oxygen infusion time and potential biosafety risks. In recent years, artificial photosynthetic systems have become a research hotspot in the fields of materials and energy. Photosynthesis is expected to improve the oxygen level at wound sites and promote wound healing because the method provides a continuous oxygen supply and has good biosafety. In this paper, oxygen treatment methods for wounds are reviewed, and the oxygen supply principle and construction of artificial photosynthesis systems are described. Finally, research progress on the photosynthetic oxygen production system to promote wound healing is summarized.

Keywords

Photosynthesis / Oxygen therapy / Hypoxia / Wound healing / Chronic wounds / Hypoxia environment

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Shuning Tian, Shenyu Tan, Mingjie Fan, Wenlin Gong, Tianchang Yang, Fangwen Jiao, Hongzhi Qiao. Hypoxic environment of wounds and photosynthesis-based oxygen therapy. Burns & Trauma, 2024, 12 (1) : tkae012 DOI:10.1093/burnst/tkae012

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References

[1]

Haalboom M. Chronic wounds: innovations in diagnostics and therapeutics. Curr Med Chem. 2018; 25: 5772-81.

[2]

Olsson M, Järbrink K, Divakar U, Bajpai R, Upton Z, Schmidtchen A, et al. The humanistic and economic burden of chronic wounds: a systematic review. Wound Repair Regen. 2019; 27: 114-25.

[3]

Ouyang J, Ji X, Zhang X, Feng C, Tao W. In situ sprayed NIR-responsive, analgesic black phosphorus-based gel for diabetic ulcer treatment. Proc Natl Acad Sci USA. 2020; 117: 28667-77.

[4]

Tang N, Zhang R, Zheng Y, Wang J, Khatib M, Jiang X, et al. Highly efficient self-healing multifunctional dressing with antibacterial activity for Sutureless wound closure and infected wound monitoring. Adv Mater. 2022; 34:e2106842. https://doi.org/10.1002/adma.202106842.

[5]

Schreml S, Szeimies RM, Prantl L, Karrer S, Landthaler M, Babilas P. Oxygen in acute and chronic wound healing. Br J Dermatol. 2010; 163: 257-68.

[6]

Gottrup F, Dissemond J, Baines C, Frykberg R, Jensen P, Kot J, et al. Use of oxygen therapies in wound healing. J Wound Care. 2017; 26: S1-43.

[7]

Hayes PD, Alzuhir N, Curran G, Loftus IM. Topical oxygen therapy promotes the healing of chronic diabetic foot ulcers: a pilot study. J Wound Care. 2017; 26: 652-60.

[8]

Dissemond J, Kröger K, Storck M, Risse A, Engels P. Topical oxygen wound therapies for chronic wounds: a review. J Wound Care. 2015; 24: 53-63.

[9]

Tandara AA, Mustoe TA. Oxygen in wound healing-more than a nutrient. World J Surg. 2004; 28: 294-300.

[10]

Thangarajah H, Yao D, Chang EI, Shi Y, Jazayeri L, Vial IN, et al. The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues. Proc Natl Acad Sci. 2009; 106: 13505-10.

[11]

Thangarajah H, Vial IN, Grogan RH, Yao D, Shi Y, Januszyk M, et al. HIF-1α dysfunction in diabetes. Cell Cycle. 2010; 9: 75-9.

[12]

Kimmel HM, Grant A, Ditata J. The presence of oxygen in wound healing. Wounds. 2016; 28: 264-70.

[13]

Howard MA, Asmis R, Evans KK, Mustoe TA. Oxygen and wound care: a review of current therapeutic modalities and future direction. Wound Repair Regen. 2013; 21: 503-11.

[14]

Botusan IR, Sunkari VG, Savu O, Catrina AI, Grünler J, Lindberg S, et al. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci USA. 2008; 105: 19426-31.

[15]

Guan Y, Niu H, Liu Z, Dang Y, Shen J, Zayed M, et al. Sustained oxygenation accelerates diabetic wound healing by promoting epithelialization and angiogenesis and decreasing inflammation. Sci Adv. 2021; 7: eabj0153. https://doi.org/10.1126/sciadv.abj0153.

[16]

Heyboer M, Sharma D, Santiago W, Mcculloch N. Hyperbaric oxygen therapy: side effects defined and quantified. Adv Wound Care. 2017; 6: 210-24.

[17]

Kranke P, Bennett MH, Martyn-St James M, Schnabel A, Debus SE, Weibel S. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev. 2015; 2015: Cd004123.

[18]

Chandra PK, Ross CL, Smith LC, Jeong SS, Kim J, Yoo JJ, et al. Peroxide-based oxygen generating topical wound dressing for enhancing healing of dermal wounds. Wound Repair Regen. 2015; 23: 830-41.

[19]

Wang Q, Qiu W, Li M, Li N, Li X, Qin X, et al. Multifunctional hydrogel platform for biofilm scavenging and O(2) generating with photothermal effect on diabetic chronic wound healing. J Colloid Interface Sci. 2022; 617: 542-56.

[20]

Ward KR, Huvard GS, McHugh M, Mallepally RR, Imbruce R. Chemical oxygen generation. Respir Care. 2013; 58: 184-95.

[21]

Wang Y, Li S, Liu L, Lv F, Wang S. Conjugated polymer nanoparticles to augment photosynthesis of chloroplasts. Angew Chem Int Ed Engl. 2017; 56: 5308-11.

[22]

Duzgun AP, Satir HZ, Ozozan O, Saylam B, Kulah B, Coskun F. Effect of hyperbaric oxygen therapy on healing of diabetic foot ulcers. J Foot Ankle Surg. 2008; 47: 515-9.

[23]

Lam G, Fontaine R, Ross FL, Chiu ES. Hyperbaric oxygen therapy: exploring the clinical evidence. Adv Skin Wound Care. 2017; 30: 181-90.

[24]

Johnston BR, Ha AY, Brea B, Liu PY. The mechanism of hyperbaric oxygen therapy in the treatment of chronic wounds and diabetic foot ulcers. R I Med J. 2013; 2016: 26-9.

[25]

Gurdol F, Cimsit M, Oner-Iyidogan Y, Kocak H, Sengun S, Yalcinkaya-Demirsoz S. Collagen synthesis, nitric oxide and asymmetric dimethylarginine in diabetic subjects undergoing hyperbaric oxygen therapy. Physiol Res. 2010; 59: 423-9.

[26]

Moreira DACDL, Oliveira-Pinto J, Mansilha A. The role of hyperbaric oxygen therapy in the treatment of diabetic foot ulcers: a systematic review with meta-analysis of randomized controlled trials on limb amputation and ulcer healing. Int Angiol. 2022; 41: 63-73.

[27]

Nik Hisamuddin NAR, Wan Mohd Zahiruddin WN, Mohd Yazid B, Rahmah S. Use of hyperbaric oxygen therapy (HBOT) in chronic diabetic wound-a randomised trial. Med J Malaysia. 2019; 74: 418-24.

[28]

Plafki C, Peters P, Almeling M, Welslau W, Busch R. Complications and side effects of hyperbaric oxygen therapy. Aviat Space Environ Med. 2000; 71: 119-24.

[29]

Frykberg RG.Topical wound oxygen therapy in the treatment of chronic diabetic foot ulcers. Medicina (Kaunas). 2021; 57: 917.

[30]

Sayadi LR, Banyard DA, Ziegler ME, Obagi Z, Prussak J, Klopfer MJ, et al. Topical oxygen therapy & micro/nanobubbles: a new modality for tissue oxygen delivery. Int Wound J. 2018; 15: 363-74.

[31]

Heng MC, Kloss SG. Endothelial cell toxicity in leg ulcers treated with topical hyperbaric oxygen. Am J Dermatopathol. 1986; 8: 403-10.

[32]

Woo KY, Coutts PM, Sibbald RG. Continuous topical oxygen for the treatment of chronic wounds: a pilot study. Adv Skin Wound Care. 2012; 25: 543-7.

[33]

Driver VR, Reyzelman A, Kawalec J, French M. A prospective, randomized, blinded, controlled trial comparing transdermal continuous oxygen delivery to moist wound therapy for the treatment of diabetic foot ulcers. Ostomy Wound Manage. 2017; 63: 12-28.

[34]

Roe DF, Gibbins BL, Ladizinsky DA. Topical dissolved oxygen penetrates skin: model and method. J Surg Res. 2010; 159: e29-36.

[35]

Davis P, Wood L, Wood Z, Eaton A, Wilkins J. Clinical experience with a glucose oxidase-containing dressing on recalcitrant wounds. J Wound Care. 2009; 18: 114-21.

[36]

Xie CW, Wang ZZ, Zhang YN, Chen YL, Li RP, Zhang JD. Effect of interaction between adenosine and nitric oxide on central nervous system oxygen toxicity. Neurotox Res. 2019; 36: 193-203.

[37]

Davis SC, Cazzaniga AL, Ricotti C, Zalesky P, Hsu LC, Creech J, et al. Topical oxygen emulsion: a novel wound therapy. Arch Dermatol. 2007; 143: 1252-6.

[38]

Martin WF, Bryant DA, Beatty JT. A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol Rev. 2018; 42: 205-31.

[39]

Dogutan DK, Nocera DG. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis. Acc Chem Res. 2019; 52: 3143-8.

[40]

Garg V, Kodis G, Liddell PA, Terazono Y, Moore TA, Moore AL, et al. Artificial photosynthetic reaction center with a coumarin-based antenna system. J Phys Chem B. 2013; 117: 11299-308.

[41]

Chávez MN, Moellhoff N, Schenck TL, Egaña JT, Nickelsen J. Photosymbiosis for biomedical applications. Front Bioeng Biotechnol. 2020; 8: 577204. https://doi.org/10.3389/fbioe.2020.577204.

[42]

Qiao Y, Yang F, Xie T, Du Z, Zhong D, Qi Y, et al. Engineered algae: a novel oxygen-generating system for effective treatment of hypoxic cancer. Sci Adv. 2020; 6: eaba5996.

[43]

Huo M, Wang L, Zhang L, Wei C, Chen Y, Shi J. Photosynthetic tumor oxygenation by photosensitizer-containing cyanobacteria for enhanced photodynamic therapy. Angew Chem Int Ed Engl. 2020; 59: 1906-13.

[44]

Wang H, Liu H, Guo Y, Zai W, Li X, Xiong W, et al. Photosynthetic microorganisms coupled photodynamic therapy for enhanced antitumor immune effect. Bioact Mater. 2022; 12: 97-106.

[45]

Chang M, Feng W, Ding L, Zhang H, Dong C, Chen Y, et al. Persistent luminescence phosphor as in-vivo light source for tumoral cyanobacterial photosynthetic oxygenation and photodynamic therapy. Bioact Mater. 2022; 10: 131-44.

[46]

Wang J, Su Q, Lv Q, Cai B, Xiaohalati X, Wang G, et al. Oxygen-generating cyanobacteria powered by Upconversion-nanoparticles-converted near-infrared light for ischemic stroke treatment. Nano Lett. 2021; 21: 4654-65.

[47]

Voss LJ, Plouviez M, Whittle N. Microalgae-based photosynthetic strategy for oxygenating avascularised mouse brain tissue-an in vitro proof of concept study. Brain Res. 2021; 1768: 147585. https://doi.org/10.1016/j.brainres.2021.147585.

[48]

Özugur S, Chávez MN, Sanchez-Gonzalez R, Kunz L, Nickelsen J, Straka H. Green oxygen power plants in the brain rescue neuronal activity. iScience. 2021; 24: 103158. https://doi.org/10.1016/j.isci.2021.103158.

[49]

Cohen JE, Goldstone AB, Paulsen MJ, Shudo Y, Steele AN, Edwards BB, et al. An innovative biologic system for photon-powered myocardium in the ischemic heart. Sci Adv. 2017; 3: e1603078. https://doi.org/10.1126/sciadv.1603078.

[50]

Veloso-Giménez V, Escamilla R, Necuñir D, Corrales-Orovio R, Riveros S, Marino C, et al. Development of a novel Perfusable solution for ex vivo preservation: towards photosynthetic oxygenation for organ transplantation. Front Bioeng Biotechnol. 2021; 9: 796157. https://doi.org/10.3389/fbioe.2021.796157.

[51]

Yamaoka I, Kikuchi T, Arata T, Kobayashi E. Organ preservation using a photosynthetic solution. Transplant Res. 2012; 1: 2.

[52]

Centeno-Cerdas C, Jarquín-Cordero M, Chávez MN, Hopfner U, Holmes C, Schmauss D, et al. Development of photosynthetic sutures for the local delivery of oxygen and recombinant growth factors in wounds. Acta Biomater. 2018; 81: 184-94.

[53]

Chen H, Cheng Y, Tian J, Yang P, Zhang X, Chen Y, et al. Dissolved oxygen from microalgae-gel patch promotes chronic wound healing in diabetes. Sci Adv. 2020; 6: eaba4311.

[54]

Wang X, Yang C, Yu Y, Zhao Y. In situ 3D bioprinting living photosynthetic scaffolds for autotrophic wound healing. Research (Wash D C). 2022; 2022: 9794745.

[55]

Obaíd ML, Camacho JP, Brenet M, Corrales-Orovio R, Carvajal F, Martorell X, et al. A first in human trial implanting microalgae shows safety of photosynthetic therapy for the effective treatment of full thickness skin wounds. Front Med (Lausanne). 2021; 8: 772324. https://doi.org/10.3389/fmed.2021.772324.

[56]

Chávez MN, Schenck TL, Hopfner U, Centeno-Cerdas C, Somlai-Schweiger I, Schwarz C, et al. Towards autotrophic tissue engineering: photosynthetic gene therapy for regeneration. Biomaterials. 2016; 75: 25-36.

[57]

Shchelik IS, Sieber S, Gademann K. Green algae as a drug delivery system for the controlled release of antibiotics. Chemistry. 2020; 26: 16644-8.

[58]

Hopfner U, Schenck TL, Chávez MN, Machens HG, Bohne AV, Nickelsen J, et al. Development of photosynthetic biomaterials for in vitro tissue engineering. Acta Biomater. 2014; 10: 2712-7.

[59]

Schenck TL, Hopfner U, Chávez MN, Machens HG, Somlai-Schweiger I, Giunta RE, et al. Photosynthetic biomaterials: a pathway towards autotrophic tissue engineering. Acta Biomater. 2015; 15: 39-47.

[60]

Lindberg P, Kenkel A, Bühler K. Introduction to cyanobacteria. Adv Biochem Eng Biotechnol. 2023; 183: 1-24.

[61]

Li W, Wang S, Zhong D, Du Z, Zhou M. A bioactive living hydrogel: photosynthetic bacteria mediated hypoxia elimination and bacteriakgilling to promote infected wound healing. Adv Therap. 2020; 4: 2000107.

[62]

Stapleton LM, Farry JM, Zhu Y, Lucian HJ, Wang H, Paulsen MJ, et al. Microfluidic encapsulation of photosynthetic cyanobacteria in hydrogel microparticles augments oxygen delivery to rescue ischemic myocardium. J Biosci Bioeng. 2023; 135: 493-9.

[63]

He Y, Chang Q, Lu F. Oxygen-releasing biomaterials for chronic wounds breathing: from theoretical mechanism to application prospect. Mater Today Bio. 2023; 20: 100687. https://doi.org/10.1016/j.mtbio.2023.100687.

[64]

Song R, Zheng J, Liu Y, Tan Y, Yang Z, Song X, et al. A natural cordycepin/chitosan complex hydrogel with outstanding self-healable and wound healing properties. Int J Biol Macromol. 2019; 134: 91-9.

[65]

Wang X, Jia J, Niu M, Li W, Zhao Y. Living Chinese herbal scaffolds from microfluidic bioprinting for wound healing. Research (Wash D C). 2023; 6: 0138.

[66]

Chen G, Yu J, Gu Z. Glucose-responsive microneedle patches for diabetes treatment. J Diabetes Sci Technol. 2019; 13: 41-8.

[67]

Jinqiang W, Zejun W, Yu J, Kahkoska AR, Buse JB, Gu Z. Glucose-responsive insulin and delivery systems: innovation and translation. Adv Mater. 2020; 32: e1902004.

[68]

Ye Y, Yu J, Wen D, Kahkoska AR, Gu Z. Polymeric microneedles for transdermal protein delivery. Adv Drug Deliv Rev. 2018; 127: 106-18.

[69]

Zhao E, Xiao T, Tan Y, Zhou X, Li Y, Wang X, et al. Separable microneedles with photosynthesis-driven oxygen manufactory for diabetic wound healing. ACS Appl Mater Interfaces. 2023; 15: 7725-34.

[70]

Choi H, Kim B, Jeong SH, Kim TY, Kim DP, Oh YK, et al. Microalgae-based biohybrid microrobot for accelerated diabetic wound healing. Small. 2023; 19: e2204617. https://doi.org/10.1002/smll.202204617.

[71]

Foster AA, Marquardt LM, Heilshorn SC. The diverse roles of hydrogel mechanics in injectable stem cell transplantation. Curr Opin Chem Eng. 2017; 15: 15-23.

[72]

Ravanbakhsh H, Karamzadeh V, Bao G, Mongeau L, Juncker D, Zhang YS. Emerging Technologies in Multi-Material Bioprinting. Adv Mater. 2021; 33: e2104730. https://doi.org/10.1002/adma.202104730.

[73]

Gong J, Schuurmans CCL, Genderen AMV, Cao X, Li W, Cheng F, et al. Complexation-induced resolution enhancement of 3D-printed hydrogel constructs. Nat Commun. 2020; 11: 1267.

[74]

Alizadehgiashi M, Nemr CR, Chekini M, Pinto Ramos D, Mittal N, Ahmed SU, et al. Multifunctional 3D-printed wound dressings. ACS Nano. 2021; 15: 12375-87.

[75]

Siebert L, Luna-Cerón E, García-Rivera LE, Oh J, Jang J, Rosas-Gómez DA, et al. Light-controlled growth factors release on tetrapodal ZnO-incorporated 3D-printed hydrogels for developing smart wound scaffold. Adv Funct Mater. 2021; 31: 2007555.

[76]

Lode A, Krujatz F, Brüggemeier S, Quade M, Schütz K, Knaack S, et al. Green bioprinting: fabrication of photosynthetic algae-laden hydrogel scaffolds for biotechnological and medical applications. Engineering in Life Sciences. 2015; 15: 177-83.

[77]

Seidel J, Ahlfeld T, Adolph M, Kümmritz S, Steingroewer J, Krujatz F, et al. Green bioprinting: extrusion-based fabrication of plant cell-laden biopolymer hydrogel scaffolds. Biofabrication. 2017; 9: 045011. https://doi.org/10.1088/1758-5090/aa8854.

[78]

da Silva FV, Sant’Anna C. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J Microbiol Biotechnol. 2017; 33: 20.

[79]

Li L, Wang Y, Gao L, Zhou W, Chen L, Zhang Z, et al. Experiments and cellular automata simulation reveal light/carbon transportation and growth mechanism of Chlorella vulgaris biofilm in attached cultivation. Chem Eng J. 2023; 457: 141177. https://doi.org/10.1016/j.cej.2022.141177.

[80]

Wang J, Soto F, Liu S, Yin Q, Purcell E, Zeng Y, et al. Volbots: Volvox microalgae-based robots for multimode precision imaging and therapy. Adv Funct Mater. 2022; 32: 2201800.

[81]

Jeong JW, McCall JG, Shin G, Zhang Y, Al-Hasani R, Kim M, et al. Wireless Optofluidic Systems for Programmable in vivo pharmacology and Optogenetics. Cell. 2015; 162: 662-74.

[82]

Wang S, Li B, Zhang F. Molecular fluorophores for deep-tissue bioimaging. ACS Cent Sci. 2020; 6: 1302-16.

[83]

Gutruf P, Yin RT, Lee KB, Ausra J, Brennan JA, Qiao Y, et al. Wireless, battery-free, fully implantable multimodal and multisite pacemakers for applications in small animal models. Nat Commun. 2019; 10: 5742.

[84]

Yamagishi K, Kirino I, Takahashi I, Amano H, Takeoka S, Morimoto Y, et al. Tissue-adhesive wirelessly powered optoelectronic device for metronomic photodynamic cancer therapy. Nat Biomed Eng. 2019; 3: 27-36.

[85]

Zhou H, Zeng X, Li A, Zhou W, Tang L, Hu W, et al. Upconversion NIR-II fluorophores for mitochondria-targeted cancer imaging and photothermal therapy. Nat Commun. 2020; 11: 6183.

[86]

Deng K, Tang Y, Xiao Y, Zhong D, Zhang H, Fang W, et al. A biodegradable, flexible photonic patch for in vivo phototherapy. Nat Commun. 2023; 14: 3069.

[87]

Chen G, Wang F, Zhang X, Shang Y, Zhao Y. Living microecological hydrogels for wound healing. Sci Adv. 2023; 9: eadg3478.

[88]

Corrales-Orovio R, Carvajal F, Holmes C, Miranda M, González-Itier S, Cárdenas C, et al. Development of a photosynthetic hydrogel as potential wound dressing for the local delivery of oxygen and bioactive molecules. Acta Biomater. 2023; 155: 154-66.

[89]

Chávez MN, Fuchs B, Moellhoff N, Hofmann D, Zhang L, Selão TT, et al. Use of photosynthetic transgenic cyanobacteria to promote lymphangiogenesis in scaffolds for dermal regeneration. Acta Biomater. 2021; 126: 132-43.

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