Table Info

Table 1.

Surface chemical composition obtained from XPS survey spectra and WCA of dECMf surface before and after plasma treatment

Sample	C (%)	O (%)	N (%)	N/C	O/C	WCA (°)
dECMfs	74.3 ± 0.7	15.5 ± 0.8	7.8 ± 0.6	0.11 ± 0.01	0.21 ± 0.01	92.4 ± 1.5
dECMf*	64.5 ± 1.9	20.3 ± 1.1	13.07 ± 1.1	0.20 ± 0.02	0.31 ± 0.03	86.1 ± 0.5

A statistically significant variation in the relative surface concentration of C (P = 0.0108), O (P = 0.0111) and N (P = 0.0225) was observed. The WCA showed a significant decrease after plasma treatment (P < 0.0001). Statistical analysis: unpaired t test with Welch correction

Declarations

Author contributions

MEL: Conceptualization, Data curation, Formal analysis, Investigation, Writing—original draft, Writing—review & editing. VM: Conceptualization, Data curation, Investigation. PC and FC: Conceptualization, Supervision, Validation, Writing—review & editing. FB and AS: Conceptualization, Project administration, Resources, Validation, Writing—review & editing. DM: Conceptualization, Funding acquisition, Project administration, Resources, Validation, Writing—review & editing. All authors have read and agreed to the published version of the manuscript.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This study was approved by the CHU de Quebec ethic (SCH11-09-091). This study complies with the WMA Declaration of Helsinki.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

The data supporting the conclusions of this study will be made available by the corresponding author on request.

Funding

This work was partially supported by the Natural Science and Engineering Research Council of Canada, the Ministry of Economy and Innovation of Quebec (PRIMA Quebec), and the Research Center of the CHU de Quebec. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright

References

Hernandez MJ, Yakutis GE, Zelus EI, Hill RC, Dzieciatkowska M, Hansen KC, et al. Manufacturing considerations for producing and assessing decellularized extracellular matrix hydrogels. Methods. 2020;171:20–7. [DOI] [PubMed]

McInnes AD, Moser MAJ, Chen X. Preparation and use of decellularized extracellular matrix for tissue engineering. J Funct Biomater. 2022;13:240. [DOI] [PubMed] [PMC]

Yao Q, Zheng YW, Lan QH, Kou L, Xu HL, Zhao YZ. Recent development and biomedical applications of decellularized extracellular matrix biomaterials. Mater Sci Eng C. 2019;104:109942. [DOI] [PubMed]

Amirazad H, Dadashpour M, Zarghami N. Application of decellularized bone matrix as a bioscaffold in bone tissue engineering. J Biol Eng. 2022;16:1. [DOI] [PubMed] [PMC]

Koo MA, Jeong H, Hong SH, Seon GM, Lee MH, Park JC. Preconditioning process for dermal tissue decellularization using electroporation with sonication. Regen Biomater. 2022;9:rbab071. [DOI] [PubMed] [PMC]

Kim YS, Majid M, Melchiorri AJ, Mikos AG. Applications of decellularized extracellular matrix in bone and cartilage tissue engineering. Bioeng Transl Med. 2018;4:83–95. [DOI] [PubMed] [PMC]

Bejleri D, Davis ME. Decellularized extracellular matrix materials for cardiac repair and regeneration. Adv Healthc Mater. 2019;8:e1801217. [DOI] [PubMed] [PMC]

Saldin LT, Cramer MC, Velankar SS, White LJ, Badylak SF. Extracellular matrix hydrogels from decellularized tissues: structure and function. Acta Bioma. 2017;49:1–15. [DOI] [PubMed] [PMC]

Arslan YE, Galata YF, Sezgin Arslan T, Derkus B. Trans-differentiation of human adipose-derived mesenchymal stem cells into cardiomyocyte-like cells on decellularized bovine myocardial extracellular matrix-based films. J Mater Sci Mater Med. 2018;29:127. [DOI] [PubMed]

10.

Liao J, Xu B, Zhang R, Fan Y, Xie H, Li X. Applications of decellularized materials in tissue engineering: advantages, drawbacks and current improvements, and future perspectives. J Mater Chem B. 2020;8:10023–49. [DOI] [PubMed]

11.

Yao S, Cui J, Chen S, Zhou X, Li J, Zhang K. Extracellular matrix coatings on cardiovascular materials—a review. Coatings. 2022;12:1039. [DOI]

12.

Efraim Y, Schoen B, Zahran S, Davidov T, Vasilyev G, Baruch L, et al. 3D structure and processing methods direct the biological attributes of ECM-based cardiac scaffolds. Sci Rep. 2019;9:5578. [DOI] [PubMed] [PMC]

13.

Cai S, Xu H, Jiang Q, Yang Y. Novel 3D electrospun scaffolds with fibers oriented randomly and evenly in three dimensions to closely mimic the unique architectures of extracellular matrices in soft tissues: fabrication and mechanism study. Langmuir. 2013;29:2311–8. [DOI] [PubMed]

14.

Cai S, Wu C, Yang W, Liang W, Yu H, Liu L. Recent advance in surface modification for regulating cell adhesion and behaviors. Nanotechnol Rev. 2020;9:971–89. [DOI]

15.

Firoozi M, Entezam M, Masaeli E, Ejeian F, Nasr-Esfahani MH. Physical modification approaches to enhance cell supporting potential of poly (vinyl alcohol)-based hydrogels. J Appl Polym Sci. 2022;139:51485. [DOI]

16.

López-Pérez PM, Marques AP, da Silva RMP, Pashkuleva I, Reis RL. Effect of chitosan membrane surface modification via plasma induced polymerization on the adhesion of osteoblast-like cells. J Mater Chem. 2007;17:4064–71. [DOI]

17.

Klee D, Ademovic Z, Bosserhoff A, Hoecker H, Maziolis G, Erli HJ. Surface modification of poly(vinylidenefluoride) to improve the osteoblast adhesion. Biomaterials. 2003;24:3663–70. [DOI] [PubMed]

18.

Goddard JM, Hotchkiss JH. Polymer surface modification for the attachment of bioactive compounds. Prog Polym Sci. 2007;32:698–725. [DOI]

19.

Barish JA, Goddard JM. Topographical and chemical characterization of polymer surfaces modified by physical and chemical processes. J Appl Polym Sci. 2011;120:2863–71. [DOI]

20.

Yoshida S, Hagiwara K, Hasebe T, Hotta A. Surface modification of polymers by plasma treatments for the enhancement of biocompatibility and controlled drug release. Surf Coatings Technol. 2013;233:99–107. [DOI]

21.

Vaz JM, Taketa TB, Hernandez-Montelongo J, Chevallier P, Cotta MA, Mantovani D, et al. Antibacterial properties of chitosan-based coatings are affected by spacer-length and molecular weight. Appl Surf Sci. 2018;445:478–87. [DOI]

22.

Ma C, Nikiforov A, De Geyter N, Morent R, Ostrikov KK. Plasma for biomedical decontamination: from plasma-engineered to plasma-active antimicrobial surfaces. Curr Opin Chem Eng. 2022;36:100764. [DOI]

23.

Valence Sd, Tille JC, Chaabane C, Gurny R, Bochaton-Piallat ML, Walpoth BH, et al. Plasma treatment for improving cell biocompatibility of a biodegradable polymer scaffold for vascular graft applications. Eur J Pharm Biopharm. 2013;85:78–86. [DOI] [PubMed]

24.

Ino JM, Chevallier P, Letourneur D, Mantovani D, Le Visage C. Plasma functionalization of poly(vinyl alcohol) hydrogel for cell adhesion enhancement. Biomatter. 2013;3:e25414. [DOI] [PubMed] [PMC]

25.

Cámara-Torres M, Sinha R, Scopece P, Neubert T, Lachmann K, Patelli A, et al. Tuning cell behavior on 3D scaffolds fabricated by atmospheric plasma-assisted additive manufacturing. ACS Appl Mater Interfaces. 2021;13:3631–44. [DOI] [PubMed] [PMC]

26.

Turkoglu Sasmazel H, Alazzawi M, Kadim Abid Alsahib N. Atmospheric pressure plasma surface treatment of polymers and influence on cell cultivation. Molecules. 2021;26:1665. [DOI] [PubMed] [PMC]

27.

Maryin PV, Tran TH, Frolova AA, Buldakov MA, Choinzonov EL, Kozelskaya AI, et al. Electrospun poly-L-lactic acid scaffolds surface-modified via reactive magnetron sputtering using different mixing ratios of nitrogen and xenon. Polymers (Basel). 2023;15:2969. [DOI] [PubMed] [PMC]

28.

Eswaramoorthy N, McKenzie DR. Plasma treatments of dressings for wound healing: a review. Biophys Rev. 2017;9:895–917. [DOI] [PubMed] [PMC]

29.

García JL, Asadinezhad A, Pacherník J, Lehocký M, Junkar I, Humpolícek P, et al. Cell proliferation of HaCaT keratinocytes on collagen films modified by argon plasma treatment. Molecules. 2010;15:2845–56. [DOI] [PubMed] [PMC]

30.

Taraballi F, Zanini S, Lupo C, Panseri S, Cunha C, Riccardi C, et al. Amino and carboxyl plasma functionalization of collagen films for tissue engineering applications. J Colloid Interface Sci. 2013;394:590–7. [DOI] [PubMed]

31.

Chen R, Curran J, Pu F, Zhuola Z, Bayon Y, Hunt JA. In vitro response of human peripheral blood mononuclear cells (PBMC) to collagen films treated with cold plasma. Polymers (Basel). 2017;9:254. [DOI] [PubMed] [PMC]

32.

Demina TS, Bikmulina PY, Birdibekova AV, Kuryanova AS, Frolova AA, Koteneva PI, et al. Modification of the chemical structure, morphology, and cytocompatibility of chitosan films via low-frequency plasma treatment. Appl Biochem Microbiol. 2022;58:118–25. [DOI]

33.

Weber M, Steinle H, Golombek S, Hann L, Schlensak C, Wendel HP, et al. Blood-contacting biomaterials: in vitro evaluation of the hemocompatibility. Front Bioeng Biotechnol. 2018;6:99. [DOI] [PubMed] [PMC]

34.

Wilson DJ, Rhodes NP, Williams RL. Surface modification of a segmented polyetherurethane using a low-powered gas plasma and its influence on the activation of the coagulation system. Biomaterials. 2003;24:5069–81. [DOI] [PubMed]

35.

Recek N. Biocompatibility of plasma-treated polymeric implants. Materials (Basel). 2019;12:240. [DOI] [PubMed] [PMC]

36.

Lopez LC, Belviso MR, Gristina R, Nardulli M, d’Agostino R, Favia P. Plasma-treated nitrogen-containing surfaces for cell adhesion: the role of the polymeric substrate. Plasma Process Polym. 2007;4:S402–5. [DOI]

37.

Truica-Marasescu F, Wertheimer MR. Nitrogen-rich plasma-polymer films for biomedical applications. Plasma Process Polym. 2008;5:44–57. [DOI]

38.

Boccafoschi F, Calvo Catoira M, Fusaro L, inventors. Hydrogel from bovine pericardium for medical use. International application PCT/IB2021/052779. 2 April 2021.

39.

Hu Y, Liu L, Gu Z, Dan W, Dan N, Yu X. Modification of collagen with a natural derived cross-linker, alginate dialdehyde. Carbohydr Polym. 2014;102:324–32. [DOI] [PubMed]

40.

Riaz T, Zeeshan R, Zarif F, Ilyas K, Muhammad N, Safi SZ, et al. FTIR analysis of natural and synthetic collagen. Appl Spectrosc Rev. 2018;53:703–46. [DOI]

41.

Sanden KW, Kohler A, Afseth NK, Böcker U, Rønning SB, Liland KH, et al. The use of fourier-transform infrared spectroscopy to characterize connective tissue components in skeletal muscle of Atlantic cod (Gadus morhua L.). J Biophotonics. 2019;12:e201800436. [DOI] [PubMed] [PMC]

42.

Huang CC. Microporous scaffolds via a designed decellularization procedure combined with papain-containing reagent treatments after supercritical fluid of carbon dioxide. Mater Lett. 2021;304:130539. [DOI]

43.

Naomi R, Ridzuan PM, Bahari H. Current insights into collagen type I. Polymers (Basel). 2021;13:2642. [DOI] [PubMed] [PMC]

44.

Wang MJ, Chang YI, Poncin-Epaillard F. Effects of the addition of hydrogen in the nitrogen cold plasma: the surface modification of polystyrene. Langmuir. 2003;19:8325–30. [DOI]

45.

Loffredo S, Gambaro S, Copes F, Paternoster C, Giguère N, Vedani M, et al. Effect of silver in thermal treatments of Fe-Mn-C degradable metals: implications for stent processing. Bioact Mater. 2022;12:30–41. [DOI] [PubMed] [PMC]

46.

Di Francesco D, Bertani F, Fusaro L, Clemente N, Carton F, Talmon M, et al. Regenerative potential of a bovine ECM-derived hydrogel for biomedical applications. Biomolecules. 2022;12:1222. [DOI] [PubMed] [PMC]

47.

Kull KR, Steen ML, Fisher ER. Surface modification with nitrogen-containing plasmas to produce hydrophilic, low-fouling membranes. J Memb Sci. 2005;246:203–15. [DOI]

48.

López-Santos C, Yubero F, Cotrino J, González-Elipe AR. Nitrogen plasma functionalization of low density polyethylene. Surf Coatings Technol. 2011;205:3356–64. [DOI]

49.

Sanchis MR, Calvo O, Fenollar O, Garcia D, Balart R. Characterization of the surface changes and the aging effects of low-pressure nitrogen plasma treatment in a polyurethane film. Polym Test. 2008;27:75–83. [DOI]

50.

Kawano T, Wang MJ, Andou Y. Surface modification of a regenerated cellulose film using low-pressure plasma treatment with various reactive gases. ACS Omega. 2022;7:44085–92. [DOI] [PubMed] [PMC]

51.

Luna SM, Silva SS, Gomes ME, Mano JF, Reis RL. Cell adhesion and proliferation onto chitosan-based membranes treated by plasma surface modification. J Biomater Appl. 2011;26:101–16. [DOI] [PubMed]

52.

Arima Y, Iwata H. Effect of wettability and surface functional groups on protein adsorption and cell adhesion using well-defined mixed self-assembled monolayers. Biomaterials. 2007;28:3074–82. [DOI] [PubMed]

53.

Samanta A, Wang Q, Shaw SK, Ding H. Roles of chemistry modification for laser textured metal alloys to achieve extreme surface wetting behaviors. Mater Des. 2020;192:108744. [DOI]

54.

Majhy B, Priyadarshini P, Sen AK. Effect of surface energy and roughness on cell adhesion and growth – facile surface modification for enhanced cell cultur. RSC Adv. 2021;11:15467–76. [DOI] [PubMed] [PMC]

55.

Bismarck A, Brostow W, Chiu R, Hagg Lobland HE, Ho KKC. Effects of surface plasma treatment on tribology of thermoplastic polymers. Polym Eng Sci. 2008;48:1971–6. [DOI]

56.

Chen L, Yan C, Zheng Z. Functional polymer surfaces for controlling cell behaviors. Mater Today. 2018;21:38–59. [DOI]

57.

Bharadwaj A. An overview on biomaterials and its applications in medical science. IOP Conf Ser Mater Sci Eng. 2021;1116:012178. [DOI]

58.

Ledari SA, Milani JM, Lanbar FS. Improving gelatin-based emulsion films with cold plasma using different gases. Food Sci Nutr. 2020;8:6487–96. [DOI] [PubMed] [PMC]

59.

Chichti E, Henrion G, Cleymand F, Jamshidian M, Linder M, Arab-Tehrany E. Effects of Ar–N₂–O₂ microwave plasma on poly-L-lactic acid thin films designed for tissue engineering. Plasma Process Polym. 2013;10:535–43. [DOI]

60.

Pohan G, Chevallier P, Anderson DEJ, Tse JW, Yao Y, Hagen MW, et al. Luminal plasma treatment for small diameter polyvinyl alcohol tubular scaffolds. Front Bioeng Biotechnol. 2019;7:117. [DOI] [PubMed] [PMC]

61.

Yang J, Bei J, Wang S. Improving cell affinity of poly(D,L-lactide) film modified by anhydrous ammonia plasma treatment. Polym Adv Technol. 2002;13:220–6. [DOI]

62.

Davoodi A, Zadeh HH, Joupari MD, Sahebalzamani MA, Khani MR, Shahabi S. Physicochemical- and biocompatibility of oxygen and nitrogen plasma treatment using a PLA scaffold. AIP Adv. 2020;10:125205. [DOI]

63.

Prasertsung I, Kanokpanont S, Mongkolnavin R, Wong CS, Panpranot J, Damrongsakkul S. Comparison of the behavior of fibroblast and bone marrow-derived mesenchymal stem cell on nitrogen plasma-treated gelatin films. Mater Sci Eng C. 2013;33:4475–9. [DOI] [PubMed]

64.

Jacobs T, Morent R, De Geyter N, Dubruel P, Leys C. Plasma surface modification of biomedical polymers: influence on cell-material interaction. Plasma Chem Plasma Process. 2012;32:1039–73. [DOI]

65.

Solouk A, Cousins BG, Mirzadeh H, Seifalian AM. Application of plasma surface modification techniques to improve hemocompatibility of vascular grafts: a review. Biotechnol Appl Biochem. 2011;58:311–27. [DOI] [PubMed]

66.

Farndale RW, Sixma JJ, Barnes MJ, de Groot PG. The role of collagen in thrombosis and hemostasis. J Thromb Haemost. 2004;2:561–73. [DOI] [PubMed]

67.

Keuren JF, Wielders SJ, Driessen A, Verhoeven M, Hendriks M, Lindhout T. Covalently-bound heparin makes collagen thromboresistant. Arterioscler Thromb Vasc Biol. 2004;24:613–7. [DOI] [PubMed]

68.

Niu Y, Galluzzi M. Hyaluronic acid/collagen nanofiber tubular scaffolds support endothelial cell proliferation, phenotypic shape and endothelialization. Nanomaterials. 2021;11:2334. [DOI]

69.

Brown M, Li J, Moraes C, Tabrizian M, Li-Jessen NYK. Decellularized extracellular matrix: new promising and challenging biomaterials for regenerative medicine. Biomaterials. 2022;289:121786. [DOI] [PubMed]

70.

Zhang X, Chen X, Hong H, Hu R, Liu J, Liu C. Decellularized extracellular matrix scaffolds: recent trends and emerging strategies in tissue engineering. Bioact Mater. 2022;10:15–31. [DOI] [PubMed] [PMC]

71.

Copes F, Pien N, Van Vlierberghe S, Boccafoschi F, Mantovani D. Collagen-based tissue engineering strategies for vascular medicine. Front Bioeng Biotechnol. 2019;7:166. [DOI]