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Argon Atmospheric Plasma Treatment Promotes Burn Healing by Stimulating Inflammation and Controlling the Redox State

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Abstract

Burns are a public health problem, with second-degree burns as one of the most common types. Although intense inflammation worsens burn healing, effective therapies are scarce. Thus, infections and hypertrophic scars may occur, which compromise patient quality of life and may delay healing. Argon atmospheric plasma (AP) has been shown to positively influence wound healing. In the context of identifying effective and alternative therapies for the treatment of second-degree burns, the present study evaluated AP in the treatment of second-degree burns in rats compared to that for sham treatment on the 2nd, 7th, 14th, and 21st days post-injury. Our results revealed proinflammatory effect for AP by recruiting predominantly neutrophils on the 7th day and macrophages on the 21st day compared to sham treatment, allowing a greater production of interleukin (IL)-1β, tumor necrosis factor (TNF)-α, and IL-17, and also controlled the inflammation by IL-10 and transforming growth factor (TGF)-β1. AP also showed antioxidant activity important for controlling oxidative damage on the 2nd day. This favored the induction of angiogenesis from the 2nd day and induction fibroplasia and fibrillogenesis after the 14th day, which enhanced burn healing with the formation of a thinner burn eschar before the 21st day post-burn. Thus, AP effectively modulated the inflammatory phase of second-degree burn healing through the control of oxidative damage that favored the following phases. Therefore, AP is a relevant alternative in the treatment of second-degree burns.

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References

  1. Heinlin, J., G. Isbary, W. Stolz, G. Morfill, M. Landthaler, T. Shimizu, B. Steffes, T. Nosenko, J. Zimmermann, and S. Karrer. 2011. Plasma applications in medicine with a special focus on dermatology. Journal of the European Academy of Dermatology and Venereology. 25: 1–11. https://doi.org/10.1111/j.1468-3083.2010.03702.x.

    Article  CAS  PubMed  Google Scholar 

  2. Lu, Gan, Song Zhang, Devesh Poorun, Dawei Liu, Xinpei Lu, Mengwen He, Xiaoru Duan, and Hongxiang Chen. 2018. Medical applica tions of nonthermal atmospheric pressure plasma in dermatology. Journal der Deutschen Dermatologischen Gesellschaft. 16: 7–13. https://doi.org/10.1111/ddg.13373.

    Article  PubMed  Google Scholar 

  3. Lee, Ok Joo, Ju Hyung Woo, Gilson Khang, Peter P. Sun, Jose Rivera, Jin Hoon Cho, Park Sung-Jin, J. Gary Eden, and Chan Hum Park. 2016. An experimental burn wound-healing study of non-thermal atmospheric pressure microplasma jet arrays. Journal of Tissue Engineering and Regenerative Medicine. 10: 348–357. https://doi.org/10.1002/term.2074.

    Article  CAS  PubMed  Google Scholar 

  4. Fathollah, Sara, Shahriar Mirpour, Parvin Mansouri, Ahmad Reza Dehpour, Mahmood Ghoranneviss, Nastaran Rahimi, Zahra Safaie Naraghi, Reza Chalangari, and Katalin Martits Chalangari. 2016. Investigation on the effects of the atmospheric pressure plasma on wound healing in diabetic rats. Scientific Reports 6. https://doi.org/10.1038/srep19144.

  5. Nomura, Yudai, Toshihiro Takamatsu, Hiroaki Kawano, Akitoshi Okino, Masaru Yoshida, and Takeshi Azuma. 2017. Investigation of blood coagulation effect of nonthermal multigas plasma jet in vitro and in vivo. Journal of Surgical Research. 219: 302–309. https://doi.org/10.1016/j.jss.2017.06.055.

    Article  PubMed  Google Scholar 

  6. Kang, S.U., J.H. Cho, J.W. Chang, Y.S. Shin, K.I. Kim, J.K. Park, S.S. Yang, J.S. Lee, E. Moon, K. Lee, and C.H. Kim. 2014. Nonthermal plasma induces head and neck cancer cell death: The potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species. Cell Death & Disease. 5: e1056. https://doi.org/10.1038/cddis.2014.33.

    Article  CAS  Google Scholar 

  7. Ye, Fuxiang, Hiroki Kaneko, Yosuke Nagasaka, Ryo Ijima, Kae Nakamura, Masatoshi Nagaya, Kei Takayama, Hiroaki Kajiyama, Takeshi Senga, Hiromasa Tanaka, Masaaki Mizuno, Fumitaka Kikkawa, Masaru Hori, and Hiroko Terasaki. 2015. Plasma-activated medium suppresses choroidal neovascularization in mice: A new therapeutic concept for age-related macular degeneration. Scientific Reports 5. https://doi.org/10.1038/srep07705.

  8. Matthes, Rutger, Claudia Bender, Rabea Schlüter, Ina Koban, René Bussiahn, Stephan Reuter, Jürgen Lademann, Klaus-Dieter Weltmann, and Axel Kramer. 2013. Antimicrobial efficacy of two surface barrier discharges with air plasma against in vitro biofilms. PLoS One 8: e70462. https://doi.org/10.1371/journal.pone.0070462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chutsirimongkol, Chanchai, Dheerawan Boonyawan, Niwat Polnikorn, Wasini Techawatthanawisan, Treenuch Kundilokchai, Chayanid Bunsaisup, Paisal Rummaneethorn, Wicharn Kirdwichai, Apirag Chuangsuwanich, and Pannapa Powthong. 2016. Non-thermal atmospheric dielectric barrier discharge plasma, medical application studies in Thailand. Plasma Medicine 6: 429–446. https://doi.org/10.1615/PlasmaMed.2017019317.

    Article  Google Scholar 

  10. Tiede, R., J. Hirschberg, G. Daeschlein, T. von Woedtke, W. Vioel, and S. Emmert. 2014. Plasma applications: A dermatological view. Contributions to Plasma Physics. 54: 118–130. https://doi.org/10.1002/ctpp.201310061.

    Article  CAS  Google Scholar 

  11. Brehmer, F., H.A. Haenssle, G. Daeschlein, R. Ahmed, S. Pfeiffer, A. Görlitz, D. Simon, M.P. Schön, D. Wandke, and S. Emmert. 2015. Alleviation of chronic venous leg ulcers with a hand-held dielectric barrier discharge plasma generator (PlasmaDerm(®) VU-2010): Results of a monocentric, two-armed, open, prospective, randomized and controlled trial (NCT01415622). Journal of the European Academy of Dermatology and Venereology 29: 148–155. https://doi.org/10.1111/jdv.12490.

    Article  CAS  PubMed  Google Scholar 

  12. Isbary, G., J. Heinlin, T. Shimizu, J.L. Zimmermann, G. Morfill, H.U. Schmidt, R. Monetti, B. Steffes, W. Bunk, Y. Li, T. Klaempfl, S. Karrer, M. Landthaler, and W. Stolz. 2012. Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: Results of a randomized controlled trial. British Journal of Dermatology 167: 404–410. https://doi.org/10.1111/j.1365-2133.2012.10923.x.

    Article  CAS  PubMed  Google Scholar 

  13. Kim, Yun-Jung, Sewhan Jin, Gook-Hee Han, Gi C. Kwon, Jin J. Choi, Eun H. Choi, Han S. Uhm, and Guangsup Cho. 2015. Plasma apparatuses for biomedical applications. IEEE Transactions on Plasma Science. 43: 944–950. https://doi.org/10.1109/TPS.2015.2388775.

    Article  CAS  Google Scholar 

  14. Suber, Freeman, Michael C. Carroll, and Francis D. Moore Jr. 2007. Innate response to self-antigen significantly exacerbates burn wound depth. Proceedings of the National Academy of Sciences of the United States of America. 104: 3973–3977. https://doi.org/10.1073/pnas.0609026104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Stevens, Richard, and Roberto Adachi. 2007. Protease-proteoglycan complexes of mouse and human mast cells and importance of their beta-tryptase-heparin complexes in inflammation and innate immunity. Immunological Reviews 217: 155–167. https://doi.org/10.1111/j.1600-065X.2007.00525.x.

    Article  CAS  PubMed  Google Scholar 

  16. Youn, Yeo-Kyu, Cheryl LaLonde, and Robert Demling. 1992. The role of mediators in the response to thermal injury. World Journal of Surgery. 16: 30–36. https://doi.org/10.1007/bf02067111.

    Article  CAS  PubMed  Google Scholar 

  17. Schafer, Freya Q., and Garry R. Buettner. 2001. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology & Medicine. 30: 1191–1212. https://doi.org/10.1016/s0891-5849(01)00480-4.

    Article  CAS  Google Scholar 

  18. Andrade, T.A., A. Iyer, P.K. Das, N.T. Foss, S.B. Garcia, J. Coutinho-Netto, A.A. Jordão Jr., and M.A. Frade. 2011. The inflammatory stimulus of a natural latex biomembrane improves healing in mice. Brazilian Journal of Medical and Biological Research. 44: 1036–1047. https://doi.org/10.1590/s0100-879x2011007500116.

    Article  CAS  PubMed  Google Scholar 

  19. Moscardi, Leandro C., Talita P. Espíndola, Amanda A. Ferreira, Naiara Alves, Maria Esméria C. Amaral, Andréa A. Aro, Rodrigo A. Dalia, Marcelo A.M. Esquisatto, Fernanda A.S. Mendonça, Gláucia M.T. Santos, and Thiago A.M. Andrade. 2018. Lasertherapy as a strategy for treatment healing under caloric restriction – Study in rats. Journal of Pharmacy and Pharmacology. https://doi.org/10.17265/2328-2150/2018.07.002.

  20. Hall, Caroline, Carolyn Hardin, Christopher J. Corkins, Alisha Z. Jiwani, John Fletcher, Anders Carlsson, and Rodney Chan. 2017. Pathophysiologic mechanisms and current treatments for cutaneous sequelae of burn wounds. Comprehensive Physiology. https://doi.org/10.1002/cphy.c170016.

  21. Chiarotto, G. Bortolança, Lia M. Neves, Marcelo A. Esquisatto, Maria E. Amaral, Gláucia M. Santos, and Fernanda A. Mendonça. 2014. Effects of laser irradiation (670-nm InGaP and 830-nm GaAlAs) on burn of second-degree in rats. Lasers in Medical Science. 29: 1685–1693. https://doi.org/10.1007/s10103-014-1573-9.

    Article  PubMed  Google Scholar 

  22. Lopes, B. Bellotti, Maria B. Kraft, Jussara Rehder, Fabiana R. Batista, and Maria B. Puzzi. 2013. The interactions between non-thermal atmospheric pressure plasma and ex-vivo dermal fibroblasts. Procedia Engineering 59: 92–100. https://doi.org/10.1016/j.proeng.2013.05.098.

    Article  Google Scholar 

  23. Silvestrini, Ana V., Luana H. Macedo, Thiago A. Andrade, Maíra F. Mendes, Acácio A. Pigoso, and Maurício V. Mazzi. 2019. Intradermal application of crotamine induces inflammatory and immunological changes in vivo. Toxins. https://doi.org/10.3390/toxins11010039.

  24. Buege, John A., and Steven D. Aust. 1978. Microsomal lipid peroxidation. Methods in Enzymology. https://doi.org/10.1016/s0076-6879(78)52032-6.

  25. Sedlak, Jozef, and H. Raymond. 1968. Lindsay. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Analytical Biochemistry. https://doi.org/10.1016/0003-2697(68)90092-4.

  26. Amaral, Maria E., Mirian Ueno, Camila A. Oliveira, Natália C. Borsonello, Emerielle C. Vanzela, Rosane A. Ribeiro, Patricia L. Alves, Helena C. Barbosa, Everardo M. Carneiro, and Antonio C. Boschero. 2011. Reduced expression of SIRT1 is associated with diminished glucose-induced insulin secretion in islets from calorie-restricted rats. The Journal of Nutritional Biochemistry. 22: 554–559. https://doi.org/10.1016/j.jnutbio.2010.04.010.

    Article  CAS  PubMed  Google Scholar 

  27. Stegemann, Hermann, and Karlheinz Stalder. 1967. Determination of hydroxyproline. Clinica Chimica Acta. 18: 267–273. https://doi.org/10.1016/0009-8981(67)90167-2.

    Article  CAS  Google Scholar 

  28. Jorge, Michelle P., Cristiana Madjarof, Ana L. Ruiza, Alik T. Fernandes, Rodney A. Rodrigues, Ilza M. Sousa, Mary A. Foglio, and João E. Carvalho. 2008. Evaluation of wound healing properties of Arrabidaea chica Verlot extract. Journal of Ethnopharmacology 118: 361–366. https://doi.org/10.1016/j.jep.2008.04.024.

    Article  CAS  PubMed  Google Scholar 

  29. Farndale, Richard W., David J. Buttle, and Alan J. Barrett. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochimica et Biophysica Acta (BBA) - General Subjects. 883: 173–177. https://doi.org/10.1016/0304-4165(86)90306-5.

    Article  CAS  Google Scholar 

  30. Stanojcic, Mile, Abdikarim Abdullahi, Sarah Rehou, Alexandra Parousis, and Marc G. Jeschke. 2018. Pathophysiological response to burn injury in adults. Annals of Surgery. 267: 576–584. https://doi.org/10.1097/SLA.0000000000002097.

    Article  PubMed  Google Scholar 

  31. Yuan, Lin, Chen Minghua, Ding Feifei, Runxiu Wang, Ziqiang Liang, Meng Chengyue, and Jia Wenbo. 2015. Study of the use of recombinant human granulocyte-macrophage colony-stimulating factor hydrogel externally to treat residual wounds of extensive deep partial-thickness burn. Burns. 41: 1086–1091. https://doi.org/10.1016/j.burns.2014.12.004.

    Article  PubMed  Google Scholar 

  32. Shi, Yuhua, Li Ligen, Chai Jiake, and Sun Tongzhu. 2012. Effect of Poloxamer 188 on deepening of deep second-degree burn wounds in the early stage. Burns. 38: 95–101. https://doi.org/10.1016/j.burns.2010.06.002.

    Article  Google Scholar 

  33. Palumbo, A. Accardo, G.I. Forte, D. Pileri, L. Vaccarino, F. Conte, L. D'Amelio, M. Palmeri, A. Triolo, N. D'Arpa, L. Scola, G. Misiano, S. Milano, and D. Lio. 2012. Analysis of IL-6, IL-10 and IL-17 genetic polymorphisms as risk factors for sepsis development in burned patients. Burns. 38: 208–213. https://doi.org/10.1016/j.burns.2011.07.022.

    Article  Google Scholar 

  34. Shabgah, Arezoo G., Ebrahim Fattahi, and Fatemeh Z. Shahneh. 2014. Interleukin-17 in human inflammatory diseases. Advances in Dermatology and Allergology. 4: 256–261. https://doi.org/10.5114/pdia.2014.40954.

    Article  Google Scholar 

  35. Ma, Tengxiao, Xiao Wang, Ya Jiao, Haitao Wang, Yongjun Qi, Hongmin Gong, Longxiao Zhang, and Duyin Jiang. 2018. Interleukin 17 (IL-17)-induced mesenchymal stem cells prolong the survival of allogeneic skin grafts. Annals of Transplantation. 23: 615–621. https://doi.org/10.12659/AOT.909381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sasaki, Jennifer R., Qiong Zhang, and Martin G. Schwacha. 2011. Burn induces a Th-17 inflammatory response at the injury site. Burns. 37: 646–651. https://doi.org/10.1016/j.burns.2011.01.028.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Zhang, Julei, Qiao Qiao, Mengdong Liu, Ting He, Jihong Shi, Xiaozhi Bai, Yijie Zhang, Yan Li, Weixia Cai, Shichao Han, and Hao Guan. 2018. IL-17 promotes scar formation by inducing macrophage infiltration. The American Journal of Pathology. 188: 1693–1702. https://doi.org/10.1016/j.ajpath.2018.04.005.

    Article  CAS  PubMed  Google Scholar 

  38. Souza, H. Ribeiro, Lucas R. Azevedo, Lucas Possebon, Sara S. Costa, Melina M. Pilon, Sonia M. Oliani, and Ana P. Girol. 2017. Heterogeneity of mast cells and expression of Annexin A1 protein in a second degree burn model with silver sulfadiazine treatment. PLoS One 12: e0173417. https://doi.org/10.1371/journal.pone.0173417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Demling, Robert, Keiichi Ikegami, and B.S. Cheryl Lalonde. 1995. Increased lipid peroxidation and decreased antioxidant activity correspond with death after smoke exposure in the rat. The Journal of Burn Care & Rehabilitation. 16: 104–110. https://doi.org/10.1097/00004630-199503000-00003.

    Article  CAS  Google Scholar 

  40. Şener, Göksel, A. Özer Şehirli, Handan Şatıroğlu, Meral K. Uysal, and Berrak Ç. Yeğen. 2002. Melatonin improves oxidative organ damage in a rat model of thermal injury. Burns. 28: 419–425. https://doi.org/10.1016/s0305-4179(02)00053-0.

    Article  PubMed  Google Scholar 

  41. Brun, Paola, Surajit Pathak, Ignazio Castagliuolo, Giorgio Palù, Paola Brun, Matteo Zuin, Roberto Cavazzana, and Emilio Martines. 2014. Helium generated cold plasma finely regulates activation of human fibroblast-like primary cells. PLoS One 9: e104397. https://doi.org/10.1371/journal.pone.0104397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Liu, Jin-Ren, Gui-Min Xu, Xing-Min Shi, and Guan-Jun Zhang. 2017. Low temperature plasma promoting fibroblast proliferation by activating the NF-κB pathway and increasing cyclinD1 expression. Scientific Reports 7: 11698. https://doi.org/10.1038/s41598-017-12043-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Sysolyatina, E., M. Vasiliev, M. Kurnaeva, I. Kornienko, O. Petrov, V. Fortov, A. Gintsburg, E. Petersen, and S. Ermolaeva. 2016. Frequency of cell treatment with cold microwave argon plasma is important for the final outcome. Journal of Physics D: Applied Physics. 49: 294002. https://doi.org/10.1088/0022-3727/49/29/294002.

    Article  CAS  Google Scholar 

  44. Gabryšová, Leona, Ashleigh Howes, Margarida Saraiva, and Anne O’Garra. 2014. The regulation of IL-10 expression. Current Topics in Microbiology and Immunology. https://doi.org/10.1007/978-3-662-43492-5_8.

  45. Guo, S., and L.A. Dipietro. 2010. Factors affecting wound healing. Journal of Dental Research. 89: 219–229. https://doi.org/10.1177/0022034509359125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Maligieri, Luis A., Lia M. Neves, Driele T. Morais, Rayane F. Domingues, Andrea A. Aro, Edson R. Pimentel, Maria E. Amaral, Marcelo A. Esquisatto, Gláucia M. Santos, and Fernanda A. Mendonça. 2017. Differing energy densities with laser 670nm InGaP controls inflammation and collagen reorganization in burns. Burns. 43: 1524–1531. https://doi.org/10.1016/j.burns.2017.04.008.

    Article  PubMed  Google Scholar 

  47. Andrade, Thiago A., Daniela S. Meyers, Guilherme F. Caetano, Vânia A. Terra, Paula P. Ovidio, Alceu A. Jordão-Jr, and Marco A. Frade. 2017. Skin changes in streptozotocin-induced diabetic rats. Biochemical and Biophysical Research Communications. 490: 1154–1161. https://doi.org/10.1016/j.bbrc.2017.06.166.

    Article  CAS  PubMed  Google Scholar 

  48. Busuioc, C.J., G.D. Mogoşanu, F.C. Popescu, I. Lascăr, H. Pârvănescu, and L. Mogoantă. 2013. Phases of the cutaneous angiogenesis process in experimental third-degree skin burns: Histological and immunohistochemical study. Romanian Journal of Morphology and Embryology.

  49. Cui, H. Song, So Y. Joo, Dae H. Lee, Joo H. Yu, Je H. Jeong, June B. Kim, and Cheong H. Seo. 2017. Low temperature plasma induces angiogenic growth factor via up-regulating hypoxia-inducible factor 1α in human dermal fibroblasts. Archives of Biochemistry and Biophysics. 630: 9–17. https://doi.org/10.1016/j.abb.2017.07.012.

    Article  CAS  PubMed  Google Scholar 

  50. D'Arpa, Peter, and P. Kai. 2017. Leung. Toll-like receptor signaling in burn wound healing and scarring. Advances in Wound Care. https://doi.org/10.1089/wound.2017.0733.

  51. Baum, Christian L., and Christopher J. Arpey. 2005. Normal cutaneous wound healing: Clinical correlation with cellular and molecular events. Dermatologic Surgery. 31: 674–686. https://doi.org/10.1111/j.1524-4725.2005.31612.

    Article  CAS  PubMed  Google Scholar 

  52. Aro, A.A., U. Nishan, M.O. Perez, R.A. Rodrigues, M.A. Foglio, J.E. Carvalho, L. Gomes, B.C. Vidal, and E.R. Pimentel. 2012. Structural and biochemical alterations during the healing process of tendons treated with Aloe vera. Life Sciences. 91: 885–893. https://doi.org/10.1016/j.lfs.2012.09.002.

    Article  CAS  PubMed  Google Scholar 

  53. Michael, Kjær. 2004. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiological Reviews 84: 649–698. https://doi.org/10.1152/physrev.00031.2003.

    Article  Google Scholar 

  54. Pandarinathan, Chithra, G.B. Sajithlal, and Gowri Chandrakasan. 1998. Influence of Aloe vera on collagen characteristics in healing dermal wounds in rats. Molecular and Cellular Biochemistry 181: 71–76. https://doi.org/10.1023/a:1006813510959.

    Article  Google Scholar 

  55. Aro, Andrea A., Danilo L. Ferrucci, Frederico P. Borges, Dagmar R. Stach-Machado, Denise V. Macedo, and Edson R. Pimentel. 2014. Exhaustive exercise with different rest periods changes the collagen content and MMP-2 activation on the calcaneal tendon. The Anatomical Record. 297: 281–288. https://doi.org/10.1002/ar.22842.

    Article  CAS  PubMed  Google Scholar 

  56. Chakravarti, Shukti. 2002. Functions of lumican and fibromodulin: Lessons from knockout mice. Glycoconjugate Journal. 19: 287–293. https://doi.org/10.1023/A:1025348417078.

    Article  CAS  PubMed  Google Scholar 

  57. Chen, Shixing, Ming-Zhong Sun, Bo Wang, Lihong Hao, Cuili Zhang, and Yi Xin. 2011. Wound healing effects of cactus extracts on second degree superficial burned mice. Journal of medicinal plant research.

  58. Aro, Andrea A., Giane D. Carneiro, Luis F. Teodoro, Fernanda C. Veiga, Danilo L. Ferrucci, Gustavo F. Simões, Priscyla W. Simões, Lúcia E. Alvares, Alexandre L. Oliveira, Cristina P. Vicente, Caio P. Gomes, João B. Pesquero, Marcelo A. Esquisatto, Benedicto D. Vidal, and Edson R. Pimentel. 2018. Injured Achilles tendons treated with adipose-derived stem cells transplantation and GDF-5. Cells. 7. https://doi.org/10.3390/cells7090127.

  59. Nakagaki, Wilson R., Tatiana C. Tomiosso, Edson R. Pimentel, and José A. Camilli. 2013. Mechanical and morphological aspects of the calcaneal tendon of mdx mice at 21 days of age. The Anatomical Record. 296: 1546–1551. https://doi.org/10.1002/ar.22759.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant number: 2017/00126-5) and Herminio Ometto Foundation - FHO. The authors also acknowledge the undergraduate students Kauan Alves and Aline Eugênio. We would like to thank Editage (https://www.editage.com) for English language editing.

Funding

This study was funded by FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant number: 2017/00126–5) and Herminio Ometto Foundation - FHO.

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Lucas Buzeli de Souza approved the version to be published, drafted the work, or revised it critically for important intellectual content; made substantial contributions to the analysis, or interpretation of data.

Jennyffer Ione de Souza Silva approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Leonardo Bagne approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Amanda Tavares Pereira approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Maraiara Aparecida de Oliveira approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Bruno Bellotti Lopes approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Maria Esméria Corezola do Amaral approved the version to be published, agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Andrea Aparecida de Aro approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Marcelo Augusto Marretto Esquisatto approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Gláucia Maria Tech dos Santos approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the analysis or interpretation of data.

Thiago Antônio Moretti de Andrade approved the version to be published, agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved, and made substantial contributions to the conception or design of the work, or the acquisition, analysis, or interpretation of data.

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Correspondence to Thiago Antônio Moretti de Andrade.

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Souza, L.B., Silva, J.I., Bagne, L. et al. Argon Atmospheric Plasma Treatment Promotes Burn Healing by Stimulating Inflammation and Controlling the Redox State. Inflammation 43, 2357–2371 (2020). https://doi.org/10.1007/s10753-020-01305-x

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