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Graphene oxide/polyethylene glycol aerogel reinforced with grape seed extracts as wound dressing

Journal of Materials Science volume 56, pages 16082–16096 (2021)Cite this article

Abstract

In this study, graphene oxide (GO) and polyethylene glycol (PEG) composite aerogels were developed by non-covalent interactions, and then, grape seed extracts (Ex), high in proanthocyanidins (PAs), were incorporated into these materials to evaluate their hemostatic performance. The morphology, chemical features, surface charge, aerogel/blood cell interactions, absorption and blood coagulation capacity, cytotoxicity and extract release from the aerogels were investigated. The aerogels showed heterogeneous porous structures capable of absorbing more than 20 times their weight when in contact with fresh human blood and water. No significant differences were observed in the physical properties of the aerogels with the inclusion of grape seed extracts. However, the effects of this natural compound were favorable to blood coagulation clotting, increasing the coagulated blood content from 77% to 84% for GO-PEG and GO-PEG/Ex aerogels after 30 s of reaction, respectively. The aerogel/blood cell interactions demonstrated the adhesion of red blood cells (RBCs) and leukocytes on the aerogel’s surface, these interactions being favored by the inclusion of grape extracts on GO-PEG matrices. The aerogels showed proliferative effects on human dermal fibroblast cells, which could be associated with the presence of PEG and PAs in their matrices. Finally, the PAs release studies from the GO-PEG/Ex aerogel matrix showed that a combined mechanism of Fickian and non-Fickian diffusion governed these release processes. This study provides a new material whose hemocompatibility properties and phytodrug release ability support its application as a hemostatic device.

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References

  1. Neuffer MC, McDivitt J, Rose D et al (2004) Hemostatic dressings for the first responder: a review. Mil Med 169:716–720. https://doi.org/10.7205/MILMED.169.9.716

    Article  Google Scholar 

  2. Shukla A, Fang JC, Puranam S et al (2012) Hemostatic multilayer coatings. Adv Mater 24:492–496. https://doi.org/10.1002/adma.201103794

    Article  CAS  Google Scholar 

  3. Quan K, Li G, Luan D et al (2015) Black hemostatic sponge based on facile prepared cross-linked graphene. Colloids Surf, B 132:27–33. https://doi.org/10.1016/j.colsurfb.2015.04.067

    Article  CAS  Google Scholar 

  4. Li G, Quan K, Xu C et al (2018) Synergy in thrombin-graphene sponge for improved hemostatic efficacy and facile utilization. Colloids Surf, B 161:27–34. https://doi.org/10.1016/j.colsurfb.2017.10.021

    Article  CAS  Google Scholar 

  5. Kozen BG, Kircher SJ, Henao J et al (2008) An alternative hemostatic dressing: comparison of CELOX, HemCon, and QuikClot. Acad Emerg Med 15:74–81. https://doi.org/10.1111/j.1553-2712.2007.00009.x

    Article  Google Scholar 

  6. Mellado C, Figueroa T, Baez R et al (2018) Development of graphene oxide composite aerogel with proanthocyanidins with hemostatic properties as a delivery system. ACS Appl Mater Interfaces 10:7717–7729. https://doi.org/10.1021/acsami.7b16084

    Article  CAS  Google Scholar 

  7. Cai J, Tian J, Gu H, Guo Z (2019) Amino carbon nanotube modified reduced graphene oxide aerogel for oil/water separation. ES Materials & Manufacturing 6:68–74

    Google Scholar 

  8. Kordjazi S, Kamyab K, Hemmatinejad N (2020) Super-hydrophilic/oleophobic chitosan/acrylamide hydrogel: an efficient water/oil separation filter. Adv Compos Hybrid Mater 3:167–176. https://doi.org/10.1007/s42114-020-00150-8

    Article  CAS  Google Scholar 

  9. Ul-Islam M, Ali J, Khan W et al (2019) Fast 4-nitrophenol reduction using gelatin hydrogel containing silver nanoparticles. Engineered Science 8:19–24

    Google Scholar 

  10. Li S, Jasim A, Zhao W et al (2018) Fabrication of pH-electroactive bacterial cellulose/polyaniline hydrogel for the development of a controlled drug release system. ES Materials & Manufacturing 1:41–49

    Google Scholar 

  11. Ma Y, Chen Y (2015) Three-dimensional graphene networks: synthesis, properties and applications. Natl Sci Rev 2:40–53. https://doi.org/10.1093/nsr/nwu072

    Article  CAS  Google Scholar 

  12. Quan K, Li G, Tao L et al (2016) Diaminopropionic acid reinforced graphene sponge and its use for hemostasis. ACS Appl Mater Interfaces 8:7666–7673. https://doi.org/10.1021/acsami.5b12715

    Article  CAS  Google Scholar 

  13. Jadhav UU, Sawant J, Jagtap S, Pathan HM (2021) Decontamination of fresh-cut produce using photo-active carbon nanoparticles: current status and challenges. ES Food & Agroforestry 3:23–26

    Google Scholar 

  14. Chen Y, Guo Z, Das R, Jiang Q (2020) Starch-based carbon nanotubes and graphene: preparation, properties and applications. ES Food & Agroforestry 2:13–21

    Google Scholar 

  15. Gu R, Sun W, Zhou H et al (2010) The performance of a fly-larva shell-derived chitosan sponge as an absorbable surgical hemostatic agent. Biomaterials 31:1270–1277. https://doi.org/10.1016/j.biomaterials.2009.10.023

    Article  CAS  Google Scholar 

  16. Layek RK, Nandi AK (2013) A review on synthesis and properties of polymer functionalized graphene. Polymer 54:5087–5103. https://doi.org/10.1016/j.polymer.2013.06.027

    Article  CAS  Google Scholar 

  17. Wang H, Yuan X, Wu Y et al (2013) Graphene-based materials: Fabrication, characterization and application for the decontamination of wastewater and wastegas and hydrogen storage/generation. Adv Colloid Interface Sci 195:19–40. https://doi.org/10.1016/j.cis.2013.03.009

    Article  CAS  Google Scholar 

  18. Dreyer DR, Park S, Bielawski CW, Ruoff RS (2010) The chemistry of graphene oxide. Chem Soc Rev 39:228–240. https://doi.org/10.1039/b917103g

    Article  CAS  Google Scholar 

  19. Casero E, Parra-Alfambra AM, Petit-Domínguez MD et al (2012) Differentiation between graphene oxide and reduced graphene by electrochemical impedance spectroscopy (EIS). Electrochem Commun 20:63–66. https://doi.org/10.1016/j.elecom.2012.04.002

    Article  CAS  Google Scholar 

  20. Kołodziej A, Długoń E, Świętek M et al (2021) A raman spectroscopic analysis of polymer membranes with graphene oxide and reduced graphene oxide. Journal of Composites Science 5:20. https://doi.org/10.3390/jcs5010020

    Article  CAS  Google Scholar 

  21. Li G, Liang Y, Xu C et al (2019) Polydopamine reinforced hemostasis of a graphene oxide sponge via enhanced platelet stimulation. Colloids Surf, B 174:35–41. https://doi.org/10.1016/j.colsurfb.2018.10.074

    Article  CAS  Google Scholar 

  22. Scaffaro R, Maio A, Lopresti F et al (2016) Synthesis and self-assembly of a PEGylated-graphene aerogel. Compos Sci Technol 128:193–200. https://doi.org/10.1016/j.compscitech.2016.03.030

    Article  CAS  Google Scholar 

  23. Nie C, Ma L, Li S et al (2019) Recent progresses in graphene based bio-functional nanostructures for advanced biological and cellular interfaces. Nano Today 26:57–97. https://doi.org/10.1016/j.nantod.2019.03.003

    Article  CAS  Google Scholar 

  24. Locilento DA, Mercante LA, Andre RS et al (2019) Biocompatible and biodegradable electrospun nanofibrous membranes loaded with grape seed extract for wound dressing application. J Nanomater. https://www.hindawi.com/journals/jnm/2019/2472964/. 

  25. Fraga CG, Galleano M, Verstraeten SV, Oteiza PI (2010) Basic biochemical mechanisms behind the health benefits of polyphenols. Mol Aspects Med 31:435–445. https://doi.org/10.1016/j.mam.2010.09.006

    Article  CAS  Google Scholar 

  26. Figueroa T, Carmona S, Guajardo S et al (2021) Synthesis and characterization of graphene oxide chitosan aerogels reinforced with flavan-3-ols as hemostatic agents. Colloids Surf, B 197:111398. https://doi.org/10.1016/j.colsurfb.2020.111398

    Article  CAS  Google Scholar 

  27. Morales C, Roeckel M, Fernández K (2014) Microscopic modeling of país grape seed extract absorption in the small intestine. AAPS PharmSciTech 15:103–110. https://doi.org/10.1208/s12249-013-0045-z

    Article  Google Scholar 

  28. Jerez M, Selga A, Sineiro J et al (2007) A comparison between bark extracts from Pinus pinaster and Pinus radiata: Antioxidant activity and procyanidin composition. Food Chem 100:439–444. https://doi.org/10.1016/j.foodchem.2005.09.064

    Article  CAS  Google Scholar 

  29. Kennedy JA, Jones GP (2001) Analysis of proanthocyanidin cleavage products following acid-catalysis in the presence of excess phloroglucinol. J Agric Food Chem 49:1740–1746. https://doi.org/10.1021/jf001030o

    Article  CAS  Google Scholar 

  30. Bai H, Li C, Wang X, Shi G (2011) On the gelation of graphene oxide. J Phys Chem C 115:5545–5551. https://doi.org/10.1021/jp1120299

    Article  CAS  Google Scholar 

  31. Mustapa AN, Martin A, Sanz-Moral LM et al (2016) Impregnation of medicinal plant phytochemical compounds into silica and alginate aerogels. The Journal of Supercritical Fluids 116:251–263. https://doi.org/10.1016/j.supflu.2016.06.002

    Article  CAS  Google Scholar 

  32. Chen G, Qiao C, Wang Y, Yao J (2014) Synthesis of biocompatible gelatin-functionalised graphene nanosheets for drug delivery applications. Aust J Chem 67:1532–1537. https://doi.org/10.1071/CH13678

    Article  CAS  Google Scholar 

  33. Piao Y, Chen B (2016) One-pot synthesis and characterization of reduced graphene oxide-gelatin nanocomposite hydrogels. RSC Adv 6:6171–6181. https://doi.org/10.1039/c5ra20674j

    Article  CAS  Google Scholar 

  34. Piao Y, Chen B (2015) Self-assembled graphene oxide–gelatin nanocomposite hydrogels: characterization, formation mechanisms, and pH-sensitive drug release behavior. J Polym Sci, Part B: Polym Phys 53:356–367. https://doi.org/10.1002/polb.23636

    Article  CAS  Google Scholar 

  35. Ferreira FV, Brito FS, Franceschi W et al (2018) Functionalized graphene oxide as reinforcement in epoxy based nanocomposites. Surfaces and Interfaces 10:100–109. https://doi.org/10.1016/j.surfin.2017.12.004

    Article  CAS  Google Scholar 

  36. He L, Wang H, Yang F, Zhu H (2018) Preparation and properties of polyethylene glycol/unsaturated polyester resin/graphene nanoplates composites as form-stable phase change materials. Thermochim Acta 665:43–52. https://doi.org/10.1016/j.tca.2018.04.012

    Article  CAS  Google Scholar 

  37. Ma ZF, Zhang H (2017) Phytochemical constituents, health benefits, and industrial applications of grape seeds: a mini-review. Antioxidants 6:71. https://doi.org/10.3390/antiox6030071

    Article  CAS  Google Scholar 

  38. Georgiev V, Ananga A, Tsolova V (2014) Recent advances and uses of grape flavonoids as nutraceuticals. Nutrients 6:391–415. https://doi.org/10.3390/nu6010391

    Article  CAS  Google Scholar 

  39. Fernández K, Kennedy JA, Agosin E (2007) Characterization of vitis vinifera L. Cv. carménère grape and wine proanthocyanidins. J Agric Food Chem 55:3675–3680. https://doi.org/10.1021/jf063232b

    Article  CAS  Google Scholar 

  40. Fernández K, Agosin E (2007) Quantitative analysis of red wine tannins using fourier-transform mid-infrared spectrometry. J Agric Food Chem 55:7294–7300. https://doi.org/10.1021/jf071193d

    Article  CAS  Google Scholar 

  41. Zhang Y, Guan J, Wu J et al (2019) N-alkylated chitosan/graphene oxide porous sponge for rapid and effective hemostasis in emergency situations. Carbohyd Polym 219:405–413. https://doi.org/10.1016/j.carbpol.2019.05.028

    Article  CAS  Google Scholar 

  42. Guajardo S, Figueroa T, Borges J et al (2021) Graphene oxide-gelatin aerogels as wound dressings with improved hemostatic properties. Materials Today Chemistry 20:100418. https://doi.org/10.1016/j.mtchem.2020.100418

    Article  CAS  Google Scholar 

  43. Mohammadi S, Keshvari H, Eskandari M, Faghihi S (2016) Graphene oxide–enriched double network hydrogel with tunable physico-mechanical properties and performance. React Funct Polym 106:120–131. https://doi.org/10.1016/j.reactfunctpolym.2016.07.015

    Article  CAS  Google Scholar 

  44. Ji H, Li J, Zhang J, Yan Y (2019) Remarkable microwave absorption performance of ultralight graphene-polyethylene glycol composite aerogels with a very low loading ratio of graphene. Compos A Appl Sci Manuf 123:158–169. https://doi.org/10.1016/j.compositesa.2019.05.012

    Article  CAS  Google Scholar 

  45. Lu H, Li C, Zhang B et al (2016) Toward highly compressible graphene aerogels of enhanced mechanical performance with polymer. RSC Adv 6:43007–43015. https://doi.org/10.1039/C6RA04995H

    Article  CAS  Google Scholar 

  46. Chang Y-W, Lee K-S, Lee Y-W, Bang JH (2015) Poly(ethylene oxide)/graphene oxide nanocomposites: structure, properties and shape memory behavior. Polym Bull 72:1937–1948. https://doi.org/10.1007/s00289-015-1381-9

    Article  CAS  Google Scholar 

  47. Xu LQ, Neoh K-G, Kang E-T (2018) Natural polyphenols as versatile platforms for material engineering and surface functionalization. Prog Polym Sci 87:165–196. https://doi.org/10.1016/j.progpolymsci.2018.08.005

    Article  CAS  Google Scholar 

  48. Kaniyoor A, Ramaprabhu S (2012) A Raman spectroscopic investigation of graphite oxide derived graphene. AIP Adv 2:032183. https://doi.org/10.1063/1.4756995

    Article  CAS  Google Scholar 

  49. Mellado C, Figueroa T, Baez R et al (2019) Effects of probe and bath ultrasonic treatments on graphene oxide structure. Materials Today Chemistry 13:1–7. https://doi.org/10.1016/j.mtchem.2019.04.006

    Article  CAS  Google Scholar 

  50. Sagitova EA, Prokhorov KA, Nikolaeva GY et al (2018) Raman analysis of polyethylene glycols and polyethylene oxides. J Phys: Conf Ser 999:012002. https://doi.org/10.1088/1742-6596/999/1/012002

    Article  CAS  Google Scholar 

  51. Ramesha GK, Vijaya Kumara A, Muralidhara HB, Sampath S (2011) Graphene and graphene oxide as effective adsorbents toward anionic and cationic dyes. J Colloid Interface Sci 361:270–277. https://doi.org/10.1016/j.jcis.2011.05.050

    Article  CAS  Google Scholar 

  52. Li D, Müller MB, Gilje S et al (2008) Processable aqueous dispersions of graphene nanosheets. Nature Nanotech 3:101–105. https://doi.org/10.1038/nnano.2007.451

    Article  CAS  Google Scholar 

  53. Li M, Liu C, Xie Y et al (2014) The evolution of surface charge on graphene oxide during the reduction and its application in electroanalysis. Carbon 66:302–311. https://doi.org/10.1016/j.carbon.2013.09.004

    Article  CAS  Google Scholar 

  54. Li G, Quan K, Liang Y et al (2016) Graphene-montmorillonite composite sponge for safe and effective hemostasis. ACS Appl Mater Interfaces 8:35071–35080. https://doi.org/10.1021/acsami.6b13302

    Article  CAS  Google Scholar 

  55. Zheng L, Zhang S, Ying Z et al (2020) Engineering of aerogel-based biomaterials for biomedical applications. Int J Nanomedicine 15:2363–2378. https://doi.org/10.2147/IJN.S238005

    Article  CAS  Google Scholar 

  56. Kenry LKP, Lim CT (2016) Selective concentration-dependent manipulation of intrinsic fluorescence of plasma proteins by graphene oxide nanosheets. RSC Adv 6:46558–46566. https://doi.org/10.1039/C6RA04978H

    Article  CAS  Google Scholar 

  57. Kenry LKP, Lim CT (2015) Molecular hemocompatibility of graphene oxide and its implication for antithrombotic applications. Small 11:5105–5117. https://doi.org/10.1002/smll.201500841

    Article  CAS  Google Scholar 

  58. Jaffer IH, Weitz JI (2019) The blood compatibility challenge. Part 1: Blood-contacting medical devices: the scope of the problem. Acta Biomater 94:2–10. https://doi.org/10.1016/j.actbio.2019.06.021

    Article  CAS  Google Scholar 

  59. Chen K, Zhang H (2019) Alginate/pectin aerogel microspheres for controlled release of proanthocyanidins. Int J Biol Macromol 136:936–943. https://doi.org/10.1016/j.ijbiomac.2019.06.138

    Article  CAS  Google Scholar 

  60. Grassi M, Grassi G (2014) Application of mathematical modeling in sustained release delivery systems. Expert Opin Drug Deliv 11:1299–1321. https://doi.org/10.1517/17425247.2014.924497

    Article  CAS  Google Scholar 

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Funding

We thank FONDECYT-Chile (Project No. 1170681) for the financial support for this investigation. Jessica Borges-Vilches thanks the National Research and Development Agency (ANID) for the Doctorate in Chemical Engineering (UdeC) scholarship ANID-PFCHA/National Doctorate 21180288.

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Authors and Affiliations

  1. Laboratory of Biomaterials, Department of Chemical Engineering, Faculty of Engineering, Universidad de Concepción, Concepción, Chile

    Jessica Borges-Vilches, Javiera Poblete, Fernando Gajardo & Katherina Fernández

  2. Department of Clinical Biochemistry and Immunology, Faculty of Pharmacy, Universidad de Concepción, Concepción, Chile

    Claudio Aguayo

Authors
  1. Jessica Borges-Vilches
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  2. Javiera Poblete
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  3. Fernando Gajardo
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  5. Katherina Fernández
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Contributions

JB-V and JP were involved in conceptualization, investigation, methodology, formal analysis of results and writing—original draft. FG helped in investigation and methodology. CA contributed to investigation, methodology and supervision. KF was involved in conceptualization, supervision, visualization and writing—review & editing, project administration.

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Correspondence to Katherina Fernández.

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Appendix 1: Supplementary information

The methodology and operation parameters used in the physicochemical characterization of all the materials are reported here. Scanning electron microscopy (SEM), X-ray diffraction (XRD), Fourier transform infrared (FTIR) spectroscopy, Raman analysis and surface charge measurements were performed. The total phenol content, degree of polymerization (mDP), structural composition and molecular weight distribution of the País grape seed extracts were determined.

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Borges-Vilches, J., Poblete, J., Gajardo, F. et al. Graphene oxide/polyethylene glycol aerogel reinforced with grape seed extracts as wound dressing. J Mater Sci 56, 16082–16096 (2021). https://doi.org/10.1007/s10853-021-06297-z

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