Oxygen Penetration Through Full-Thickness Skin by Oxygen-Releasing Sutures for Skin Graft Transplantation

Wenjing Zai; Yunong Yuan; Lin Kang; Jialong Xu; Yiqiao Hu; Lifeng Kang; Jinhui Wu

doi:10.1016/j.eng.2023.05.006

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Engineering ›› 2023, Vol. 29 ›› Issue (10) : 83-94. DOI: 10.1016/j.eng.2023.05.006

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Article

Oxygen Penetration Through Full-Thickness Skin by Oxygen-Releasing Sutures for Skin Graft Transplantation

Wenjing Zai^a^,^c^,^# ,
Yunong Yuan^b^,^# ,
Lin Kang^a^,^f^,^# ,
Jialong Xu^a ,
Yiqiao Hu^a ,
Lifeng Kang^b ,
Jinhui Wu^a^,^d^,^e^,^*

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Abstract

The transplantation of full-thickness skin grafts (FTSGs) is important for reconstructing skin barrier and promoting wound healing. Sufficient oxygen supply is closely related to the success of skin grafting. However, full-thickness oxygen delivery is limited by the poor oxygen permeability of skin. Oxygen-releasing sutures (O₂ sutures) were developed to facilitate oxygen penetration through full-thickness skin. The O₂ sutures delivered 100 times more oxygen than topical gaseous oxygen therapy at a 15 mm depth in the skin model. Under extreme hypoxia (< 0.5% O₂, v/v), O₂ sutures could also promote endothelial cell proliferation. After the transplantation of FTSGs in mice, O₂ sutures accelerated blood re-perfusion and increased the survival area of the skin graft. It is expected that O₂ sutures will be adopted in clinical applications to increase the success rate of full-thickness skin transplantation.

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Keywords

Wound / Skin graft transplantation / Oxygen-releasing sutures / Full-thickness oxygen delivery

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Wenjing Zai, Yunong Yuan, Lin Kang, Jialong Xu, Yiqiao Hu, Lifeng Kang, Jinhui Wu. Oxygen Penetration Through Full-Thickness Skin by Oxygen-Releasing Sutures for Skin Graft Transplantation. Engineering, 2023, 29(10): 83‒94 https://doi.org/10.1016/j.eng.2023.05.006

References

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[1]	B.K. Sun, Z. Siprashvili, P.A. Khavari. Advances in skin grafting and treatment of cutaneous wounds. Science, 346 (6212) ( 2014), pp. 941-945. DOI: 10.1126/science.1253836

[2]	C.K. Sen, G.M. Gordillo, S. Roy, R. Kirsner, L. Lambert, T.K. Hunt, et al.. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen, 17 (6) ( 2009), pp. 763-771

[3]	L. Clay, B. Stark, U. Gunnarsson, K. Strigård.Full-thickness skin graft vs. synthetic mesh in the repair of giant incisional hernia: a randomized controlled multicenter study. Hernia, 22 (2) ( 2018), pp. 325-332. DOI: 10.1007/s10029-017-1712-x

[4]	A. Winsnes, P. Falk, U. Gunnarsson, K. Strigård. Full-thickness skin grafts to reinforce the abdominal wall: a cross-sectional histological study comparing intra- and extraperitoneal onlay positions in mice. J Wound Care, 31 (1) ( 2022), pp. 48-55. DOI: 10.12968/jowc.2022.31.1.48

[5]	M.D. Peck. Epidemiology of burns throughout the world. Part I: distribution and risk factors. Burns, 37 (7) ( 2011), pp. 1087-1100

[6]	K.L. Butler, J. Goverman, H. Ma, A. Fischman, Y.M. Yu, M. Bilodeau, et al.. Stem cells and burns: review and therapeutic implications. J Burn Care Res, 31 (6) ( 2010), pp. 874-881

[7]	A. Andreassi, R. Bilenchi, M. Biagioli, C. D’Aniello. Classification and pathophysiology of skin grafts. Clin Dermatol, 23 (4) ( 2005), pp. 332-337

[8]	Silva ITS, Menezes HF, Souza Neto VL, Sales JRP, Sousa PAF, et al. Terminological subset of the international classification for nursing practice for patients hospitalized due to burns. Rev Esc Enferm. In press.

[9]	M.K. Smith, D.J. Mooney. Hypoxia leads to necrotic hepatocyte death. J Biomed Mater Res A, 80 (3) ( 2007), pp. 520-529. DOI: 10.1002/jbm.a.30930

[10]	J. Malda, J. Rouwkema, D.E. Martens, E.P. Le Comte, F.K. Kooy, J. Tramper, et al.. Oxygen gradients in tissue-engineered PEGT/PBT cartilaginous constructs: measurement and modeling. Biotechnol Bioeng, 86 (1) ( 2004), pp. 9-18

[11]	G.L. Semenza. Life with oxygen. Science, 318 (5847) ( 2007), pp. 62-64. DOI: 10.1126/science.1147949

[12]	H. Marks, A. Bucknor, E. Roussakis, N. Nowell, P. Kamali, J.P. Cascales, et al.. A paintable phosphorescent bandage for postoperative tissue oxygen assessment in DIEP flap reconstruction. Sci Adv, 6 (51) ( 2020), p. eabd1061

[13]	S.J. Lin, M.D. Nguyen, C. Chen, S. Colakoglu, M.S. Curtis, A.M. Tobias, et al.. Tissue oximetry monitoring in microsurgical breast reconstruction decreases flap loss and improves rate of flap salvage. Plast Reconstr Surg, 127 (3) ( 2011), pp. 1080-1085

[14]	N.S. Al-Waili, G.J. Butler. Effects of hyperbaric oxygen on inflammatory response to wound and trauma: possible mechanism of action. Sci World J, 6 ( 2006), pp. 425-441. DOI: 10.1100/tsw.2006.78

[15]	S.A. Reading, M. Yeomans, C. Levesque. Skin oxygen tension is improved by immersion in oxygen-enriched water. Int J Cosmet Sci, 35 (6) ( 2013), pp. 600-607. DOI: 10.1111/ics.12083

[16]	M.Heyboer 3rd, D. Sharma, W. Santiago, N. McCulloch. Hyperbaric oxygen therapy: side effects defined and quantified. Adv Wound Care, 6 (6) ( 2017), pp. 210-224. DOI: 10.1089/wound.2016.0718

[17]	C.Y. Chen, P.W. Wu, M.C. Hsu, C.J. Hsieh, M.C. Chou. Adjunctive hyperbaric oxygen therapy for healing of chronic diabetic foot ulcers. J Wound Ostomy Cont, 44 (6) ( 2017), pp. 536-545

[18]	J. Dissemond, K. Kröger, M. Storck, A. Risse, P. Engels. Topical oxygen wound therapies for chronic wounds: a review. J Wound Care, 24 (2) ( 2015) 53-4,56-60,62-3

[19]	G.M. Gordillo, C.K. Sen. Evidence-based recommendations for the use of topical oxygen therapy in the treatment of lower extremity wounds. Int J Low Extrem Wounds, 8 (2) ( 2009), pp. 105-111. DOI: 10.1177/1534734609335149

[20]	W.A. Tawfick, S. Sultan. Technical and clinical outcome of topical wound oxygen in comparison to conventional compression dressings in the management of refractory nonhealing venous ulcers. Vasc Endovascular Surg, 47 (1) ( 2013), pp. 30-37. DOI: 10.1177/1538574412467684

[21]	H. Chen, Y. Cheng, J. Tian, P. Yang, X. Zhang, Y. Chen, et al.. Dissolved oxygen from microalgae-gel patch promotes chronic wound healing in diabetes. Sci Adv, 6 (20) ( 2020), Article eaba4311

[22]	M. Ochoa, R. Rahimi, J. Zhou, H. Jiang, C.K. Yoon, D. Maddipatla, et al.. Integrated sensing and delivery of oxygen for next-generation smart wound dressings. Microsyst Nanoeng, 6 (1) ( 2020), p. 46

[23]	A.S. Lewis. Eliminating oxygen supply limitations for transplanted microencapsulated islets in the treatment of type 1 diabetes[dissertation]. Cambridge: Massachusetts Institute of Technology ( 2008)

[24]	S.C. Davis, A.L. Cazzaniga, C. Ricotti, P. Zalesky, L.C. Hsu, J. Creech, et al.. Topical oxygen emulsion: a novel wound therapy. Arch Dermatol, 143 (10) ( 2007), pp. 1252-1256

[25]	J. Li, Y.P. Zhang, M. Zarei, L. Zhu, J.O. Sierra, P.M. Mertz, et al.. A topical aqueous oxygen emulsion stimulates granulation tissue formation in a porcine second-degree burn wound. Burns, 41 (5) ( 2015), pp. 1049-1057

[26]	V. Kalidasan, X. Yang, Z. Xiong, R.R. Li, H. Yao, H. Godaba, et al.. Wirelessly operated bioelectronic sutures for the monitoring of deep surgical wounds. Nat Biomed Eng, 5 (10) ( 2021), pp. 1217-1227. DOI: 10.1038/s41551-021-00802-0

[27]	M. Liu, Y. Zhang, K. Liu, G. Zhang, Y. Mao, L. Chen, et al.. Biomimicking antibacterial opto-electro sensing sutures made of regenerated silk proteins. Adv Mater, 33 (1) ( 2021), Article e2004733

[28]	J. Zhu, Q. Jin, H. Zhao, W. Zhu, Z. Liu, et al.. Reactive oxygen species scavenging sutures for enhanced wound sealing and repair. Small struct, 2 (7) ( 2021), Article 2100002

[29]	W. Zai, L. Kang, T. Dong, H. Wang, L. Yin, S. Gan, et al.. E. coli membrane vesicles as a catalase carrier for long-term tumor hypoxia relief to enhance radiotherapy. ACS Nano, 15 (9) ( 2021), pp. 15381-15394. DOI: 10.1021/acsnano.1c07621

[30]	Z. Ma, Z. Yang, Q. Gao, G. Bao, A. Valiei, F. Yang, et al.. Bioinspired tough gel sheath for robust and versatile surface functionalization. Sci Adv, 7 (15) ( 2021), Article eabc3012

[31]	L.H. Wang, A.U. Ernst, D. An, A.K. Datta, B. Epel, M. Kotecha, et al.. A bioinspired scaffold for rapid oxygenation of cell encapsulation systems. Nat Commun, 12 (1) ( 2021), Article 5846

[32]	A. Farzin, S. Hassan, L.S.M. Teixeira, M. Gurian, J.F. Crispim, V. Manhas, et al.. Self-oxygenation of tissues orchestrates full-thickness vascularization of living implants. Adv Funct Mater, 31 (42) ( 2021), Article 2100850

[33]	J. Ishihara, A. Ishihara, R.D. Starke, C.R. Peghaire, K.E. Smith, T.A.J. McKinnon, et al.. The heparin binding domain of von Willebrand factor binds to growth factors and promotes angiogenesis in wound healing. Blood, 133 (24) ( 2019), pp. 2559-2569. DOI: 10.1182/blood.2019000510

[34]	A.M. Randi, M.A. Laffan. von Willebrand factor and angiogenesis: basic and applied issues. J Thromb Haemost, 15 (1) ( 2017), pp. 13-20. DOI: 10.1111/jth.13551

[35]	K.T. Chen, S. Mardini, D.C.C. Chuang, C.H. Lin, M.H. Cheng, Y.T. Lin, et al.. Timing of presentation of the first signs of vascular compromise dictates the salvage outcome of free flap transfers. Plast Reconstr Surg, 120 (1) ( 2007), pp. 187-195. DOI: 10.1097/01.prs.0000264077.07779.50

[36]	J.S. Davis. Address of the president: the story of plastic surgery. Ann Surg, 113 (5) ( 1941), pp. 641-656. DOI: 10.1097/00000658-194105000-00001

[37]	V. Holmdahl, B. Stark, L. Clay, U. Gunnarsson, K. Strigård. Long-term follow-up of full-thickness skin grafting in giant incisional hernia repair: a randomised controlled trial. Hernia, 26 (2) ( 2022), pp. 473-479. DOI: 10.1007/s10029-021-02544-z

[38]	N.G.A. Willemen, S. Hassan, M. Gurian, M.F. Jasso-Salazar, K. Fan, H. Wang, et al.. Enzyme-mediated alleviation of peroxide toxicity in self-oxygenating biomaterials. Adv Healthc Mater, 11 (13) ( 2022), Article e2102697

[39]	Y. Yuan, Y. Han, C.W. Yap, J.S. Kochhar, H. Li, X. Xiang, et al.. Prediction of drug permeation through microneedled skin by machine learning. Bioeng Transl Med, 10512 ( 2023), p. e10512

[40]	M.H. Kudur, S.B. Pai, H. Sripathi, S. Prabhu. Sutures and suturing techniques in skin closure. Indian J Dermatol Ve, 75 (4) ( 2009), pp. 425-434. DOI: 10.4103/0378-6323.53155

This paper was supported by the National Key Research and Development Program of China (2022YFC3401600), the National Natural Science Foundation of China (32171372), the Program A for Outstanding PhD Candidate of Nanjing University (202102A004), the Logistics Research Projects (BWS20J017), and the University of Sydney-China Scholarship Council (USYD-CSC) scholarship (202008320366). We would like to thank Editage (www.editage.cn) for English language editing.

Funding

the National Key Research and Development Program of China(2022YFC3401600); the National Natural Science Foundation of China(32171372); the Program A for Outstanding PhD Candidate of Nanjing University(202102A004); the Logistics Research Projects(BWS20J017); the University of Sydney-China Scholarship Council (USYD-CSC) scholarship(202008320366)