{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T19:22:57Z","timestamp":1767900177769,"version":"3.49.0"},"reference-count":50,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2023,5,29]],"date-time":"2023-05-29T00:00:00Z","timestamp":1685318400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/QUI-QFI\/2870\/2020"],"award-info":[{"award-number":["PTDC\/QUI-QFI\/2870\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/000081\/2020"],"award-info":[{"award-number":["UIDB\/000081\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDP\/00081\/2020"],"award-info":[{"award-number":["UIDP\/00081\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/05748\/2020"],"award-info":[{"award-number":["UIDB\/05748\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDP\/05748\/2020"],"award-info":[{"award-number":["UIDP\/05748\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["LA\/P\/0056\/2020"],"award-info":[{"award-number":["LA\/P\/0056\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["CEECINST\/00069\/2021"],"award-info":[{"award-number":["CEECINST\/00069\/2021"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Applied Sciences"],"abstract":"<jats:p>Reactive oxygen species (ROS), including superoxide anion, are involved in regulating various signaling pathways and are also responsible for oxidative stress. Sensing superoxide anion is of particular importance due to its biological significance. One potential approach is to use Coelenterazine as a chemiluminescent probe for the dynamic sensing of this ROS. In this study, we investigated the superoxide anion-triggered chemiluminescence of native Coelenterazine and two halogenated analogs and found that they showed a ~100-fold enhancement of light emission in aqueous solution, which was significantly reduced in methanol and nonexistent in aprotic solvents. In fact, Coelenterazine showed more intense light emission in aprotic solvents and, interestingly, although the light emission of the analogs seemed relatively unaffected by the solvents, their chemiluminescence was significantly quenched in water compared to methanol and, especially, to aprotic media. This suggests that the quenching effect observed for Coelenterazine is responsible for the differences in aqueous media, rather than an intrinsic enhanced emission by the analogs. In summary, we present Coelenterazine analogs that could serve as a basis for enhanced sensing of superoxide anion, providing information that could further our understanding of this chemiluminescent system.<\/jats:p>","DOI":"10.3390\/app13116617","type":"journal-article","created":{"date-parts":[[2023,5,30]],"date-time":"2023-05-30T02:33:27Z","timestamp":1685414007000},"page":"6617","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Investigation of the Superoxide Anion-Triggered Chemiluminescence of Coelenterazine Analogs"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5142-9278","authenticated-orcid":false,"given":"El Hadi","family":"Erbiai","sequence":"first","affiliation":[{"name":"Chemistry Research Unit (CIQUP), Institute of Molecular Sciences (IMS), Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0138-4929","authenticated-orcid":false,"given":"Patricia","family":"Gonz\u00e1lez-Berdullas","sequence":"additional","affiliation":[{"name":"Chemistry Research Unit (CIQUP), Institute of Molecular Sciences (IMS), Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8478-3441","authenticated-orcid":false,"given":"Joaquim C. G.","family":"Esteves da Silva","sequence":"additional","affiliation":[{"name":"Chemistry Research Unit (CIQUP), Institute of Molecular Sciences (IMS), Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"},{"name":"LACOMEPHI, GreenUPorto, Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5647-8455","authenticated-orcid":false,"given":"Lu\u00eds","family":"Pinto da Silva","sequence":"additional","affiliation":[{"name":"Chemistry Research Unit (CIQUP), Institute of Molecular Sciences (IMS), Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"},{"name":"LACOMEPHI, GreenUPorto, Department of Geosciences, Environment and Territorial Planning, Faculty of Sciences, University of Porto (FCUP), Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"122892","DOI":"10.1016\/j.talanta.2021.122892","article-title":"Detection strategies for superoxide anion: A review","volume":"236","author":"Jie","year":"2022","journal-title":"Talanta"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3390\/oxygen1010002","article-title":"Oxygen is Instrumental for Biological Signaling: An Overview","volume":"1","author":"Hancock","year":"2021","journal-title":"Oxygen"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Andr\u00e9s, C.M.C., Lastra, J.M.P., Juan, C.A., Plou, F.J., and P\u00e9rez-Lebena, E. (2023). Superoxide Anion Chemistry\u2014Its Role at the Core of the Innate Immunity. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24031841"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1186\/s12943-017-0648-1","article-title":"ROS signaling under metabolic stress: Cross-talk between AMPK and AKT pathway","volume":"16","author":"Zhao","year":"2017","journal-title":"Mol. Cancer"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2543","DOI":"10.1007\/s12325-017-0636-2","article-title":"A review of chronic granulomatous disease","volume":"34","author":"Arnold","year":"2017","journal-title":"Adv. Ther."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1038\/nchembio.607","article-title":"Chemistry and biology of reactive oxygen species in signaling or stress responses","volume":"7","author":"Dickinson","year":"2011","journal-title":"Nat. Chem. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/1477-3163-5-14","article-title":"Reactive oxygen species: Role in the development of cancer and various chronic conditions","volume":"6","author":"Waris","year":"2006","journal-title":"J. Carcinog."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e202100641","DOI":"10.1002\/cbic.202100641","article-title":"Oxidative Stress in Cancer Therapy: Friend or Enemy?","volume":"23","author":"Azmanova","year":"2022","journal-title":"ChemBioChem"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"7432797","DOI":"10.1155\/2016\/7432797","article-title":"Oxidative Stress and Inflammation: What Polyphenols can do for us?","volume":"2016","author":"Hussain","year":"2016","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Albano, G.D., Gagliardo, R.P., Montalbano, A.M., and Profita, M. (2022). Overview of the Mechanisms of Oxidative Stress: Impact in Inflammation of the Airway Diseases. Antioxidants, 11.","DOI":"10.3390\/antiox11112237"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"8559","DOI":"10.1021\/es201309c","article-title":"Environmentally persistent free radicals (EPFRs). 1. Generation of reactive oxygen species in aqueous solutions","volume":"45","author":"Khachatryan","year":"2011","journal-title":"Environ. Sci. Technol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"12036","DOI":"10.1021\/jp206540c","article-title":"First direct in situ EPR spectroelectrochemical evidence of the superoxide anion radical","volume":"115","author":"Petr","year":"2011","journal-title":"J. Phys. Chem. B"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"338827","DOI":"10.1016\/j.aca.2021.338827","article-title":"Non-invasive and accurate readout of superoxide anion in biological systems by near-infrared light","volume":"1179","author":"Teranishi","year":"2021","journal-title":"Anal. Chim. Acta"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1007\/s11307-015-0896-7","article-title":"Multimodality Imaging of Cancer Superoxide Anion Using the Small Molecule Coelenterazine","volume":"18","author":"Bronsart","year":"2016","journal-title":"Mol. Imaging Biol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Bronsart, L.L., Stokes, C., and Contag, C.H. (2016). Chemiluminescence Imaging of Superoxide Anion Detects Beta-Cell Function and Mass. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0146601"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"6927","DOI":"10.1021\/acs.chemrev.7b00649","article-title":"Chemi- and bioluminescence of cyclic peroxides","volume":"118","author":"Vacher","year":"2018","journal-title":"Chem. Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2286","DOI":"10.1002\/cphc.201600270","article-title":"Chemiluminescence and bioluminescence as an excitation source in the photodynamic therapy of cancer: A critical review","volume":"17","year":"2016","journal-title":"Chem. Phys. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"6800","DOI":"10.1039\/D0CS00348D","article-title":"Chemiluminescence for bioimaging and therapeutics: Recent advances and challenges","volume":"49","author":"Yang","year":"2020","journal-title":"Chem. Soc. Rev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"10002","DOI":"10.1021\/jacs.7b04804","article-title":"Self-Immolative Chemiluminescence Polymers: Innate Assimilation of Chemiexcitation in a Domino-Like Depolymerization","volume":"139","author":"Gnain","year":"2017","journal-title":"J. Am. Chem. Soc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4047","DOI":"10.7150\/thno.33228","article-title":"Chemiluminescence and Bioluminescence Imaging for Biosensing and Therapy: In Vitro and In Vivo Perspectives","volume":"9","author":"Yan","year":"2019","journal-title":"Theranostics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.microc.2018.12.056","article-title":"Recent advances in chemiluminescence for reactive oxygen species sensing and imaging analysis","volume":"146","author":"Su","year":"2019","journal-title":"Microchem. J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.jlumin.2017.10.025","article-title":"Combined experimental and theoretical study of Coelenterazine chemiluminescence in aqueous solution","volume":"194","year":"2018","journal-title":"J. Lumin."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"7862","DOI":"10.1021\/acs.jpcb.7b06295","article-title":"Mechanistic Insight into Cypridina Bioluminescence with a Combined Experimental and Theoretical Chemiluminescent Approach","volume":"121","author":"Pereira","year":"2017","journal-title":"J. Phys. Chem. B"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1039\/c5pp00456j","article-title":"Lighting up bioluminescence with coelenterazine: Strategies and applications","volume":"15","author":"Jiang","year":"2016","journal-title":"Photochem. Photobiol. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Krasistkaya, V.V., Bashmakova, E.E., and Frank, L.A. (2020). Coelenterazine-Dependent Luciferases as a Powerful Analytical Tool for Research and Biomedical Applications. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21207465"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1146\/annurev-marine-120308-081028","article-title":"Bioluminescence in the sea","volume":"2","author":"Haddock","year":"2010","journal-title":"Annu. Rev. Mar. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1006\/abio.1997.2150","article-title":"Coelenterazine analogues as chemiluminescent probe for superoxide anion","volume":"249","author":"Teranishi","year":"1997","journal-title":"Anal. Biochem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.bioorg.2006.08.003","article-title":"Luminescence of imidazo(1,2-a)pyrazin-3(7H)-one compounds","volume":"35","author":"Teranishi","year":"2007","journal-title":"Bioorg. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/0009-8981(89)90164-2","article-title":"A sensitive and specific chemiluminescence method for estimating the ability of human granulocytes and monocytes to generate O2\u2212","volume":"179","author":"Nishida","year":"1989","journal-title":"Clin. Chim. Acta"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Kazumura, K., Takeuchi, K., Hara, A., Miwa, T., Hattori, M., Wu, Y., Morishita, N., Tsuchiya, H., and Osawa, T. (2018). Rapid on-site dual optical system to measure specific reactive oxygen species (O2\u2212\u00b7and OCl\u2212) in a tiny droplet of whole blood. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0200573"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1161\/01.RES.84.10.1203","article-title":"Chemiluminescent detection of oxidants in vascular tissue. Lucigenin but not coelenterazine enhances superoxide formation","volume":"84","author":"Tarpey","year":"1999","journal-title":"Circ. Res."},{"key":"ref_32","first-page":"11683","article-title":"Single-molecule chemiluminescent photosensitizer for a self-activating and tumor-selective photodynamic therapy of cancer","volume":"183","author":"Ferreira","year":"2019","journal-title":"Eur. J. Med. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Magalh\u00e3es, C.M., Gonz\u00e1lez-Berdullas, P., Duarte, D., Correia, A.S., Rodr\u00edguez-Borges, J.E., Vale, N., Esteves da Silva, J.C.G., and Pinto da Silva, L. (2021). Target-Oriented Syntheis of Marine Coelenterazine Derivatives with Anticancer Activity by Applying the Heavy-Atom Effect. Biomedicines, 9.","DOI":"10.3390\/biomedicines9091199"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Gonz\u00e1lez-Berdullas, P., Pereira, R.B., Teixeira, C., Silva, J.P., Magalh\u00e3es, C.M., Rodr\u00edguez-Borges, J.E., Pereira, D.M., Esteves da Silva, J.C.G., and Pinto da Silva, L. (2022). Discovery of the Anticancer Activity for Lung and Gastric Cancer of a Brominated Coelenteramine Analog. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158271"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Silva, J.P., Gonz\u00e1lez-Berdullas, P., Esteves da Silva, J.C.G., and Pinto da Silva, L. (2022). Development of a Coelenterazine Derivative with Enhanced Superoxide Anion-Triggered Chemiluminescence in Aqueous Solution. Chemosensors, 10.","DOI":"10.3390\/chemosensors10050174"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"114228","DOI":"10.1016\/j.jphotochem.2022.114228","article-title":"Evaluation of the anticancer activity and chemiluminescence of a halogenated coelenterazine analog","volume":"434","author":"Silva","year":"2023","journal-title":"J. Photochem. Photobiol. A"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Sousa, J., Magalh\u00e3es, C.M., Gonz\u00e1lez-Berdullas, P., Esteves da Silva, J.C.G., and Pinto da Silva, L. (2022). Comparative Investigation of the Chemiluminescent Properties of a Dibrominated Coelenterazine Analog. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158490"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Afonso, A.C.P., Gonz\u00e1lez-Berdullas, P., Esteves da Silva, J.C.G., and Pinto da Silva, L. (2022). Combined Experimental and Theoretical Investigation into the Photophysical Properties of Halogenated Coelenteramide Analogs. Molecules, 27.","DOI":"10.3390\/molecules27248875"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1016\/j.freeradbiomed.2003.09.005","article-title":"Reaction rate constants of superoxide scavenging by plant antioxidants","volume":"35","author":"Taubert","year":"2003","journal-title":"Free Radic. Biol. Med."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Misak, A., Brezova, V., Chovanec, M., Luspai, K., Nasim, M.J., Grman, M., Tomasova, L., Jacob, C., and Ondrias, K. (2021). EPR study of KO2 as a source of superoxide and BMPO-OH\/OOH Radical that cleaves Plasmid DNA and Detects Radical Interaction and H2S and Se-Derivatives. Antioxidants, 10.","DOI":"10.3390\/antiox10081286"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1039\/C8CC00428E","article-title":"The emergence of aqueous chemiluminescence: New promising class of phenoxy 1,2-dioxetane luminophores","volume":"54","author":"Gnaim","year":"2018","journal-title":"Chem. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1021\/acscentsci.7b00058","article-title":"Opening a Gateway for Chemiluminescence Cell Imaging: Distinctive Methodology for Design of Bright Chemiluminescence Dioxetane Probes","volume":"3","author":"Green","year":"2017","journal-title":"ACS Cent. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/j.jlumin.2018.03.069","article-title":"Study of coelenterazine luminescence: Electrostatic interactions as the controlling factor for efficient chemiexcitation","volume":"199","year":"2018","journal-title":"J. Lumin."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1039\/c3pp50197c","article-title":"Chemiluminescent 2,6-diphenylimidazo[1,2-a]pyrazin-3(7 H)-ones: A new entry to Cypridina luciferin analogues","volume":"13","author":"Ishii","year":"2014","journal-title":"Photochem. Photobiol. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1039\/b713374j","article-title":"The reaction mechanism for the high quantum yield of Cypridina (Vargula) bioluminescence supported by the chemiluminescence of 6-aryl-2-methylimidazo[1,2-a]pyrazin-3(7H)-ones (Cypridina luciferin analogues)","volume":"7","author":"Hirano","year":"2008","journal-title":"Photochem. Photobiol. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"6057","DOI":"10.1016\/j.tetlet.2006.06.101","article-title":"Chemiluminescence of 6-aryl-2-methylimidazo[1,2-a]pyrazin-3(7H)-ones in DMSO\/TMG and in diglyme\/acetate buffer: Support for the chemiexcitation process to generate the singlet-excited state of neutral oxyluciferin in a high quantum yield in the Cypridina (Vargula) bioluminescence mechanism","volume":"47","author":"Takahashi","year":"2006","journal-title":"Tetrahedron Lett."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3029","DOI":"10.1021\/acs.chemrev.5b00407","article-title":"Superoxide ion: Generation and chemical implications","volume":"116","author":"Hayyan","year":"2016","journal-title":"Chem. Rev."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1021\/ar00072a005","article-title":"How super is superoxide?","volume":"14","author":"Sawyer","year":"1981","journal-title":"Acc. Chem. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.jphotobiol.2018.11.006","article-title":"Comparative study of the chemiluminescence of coelenterazine, coelenterazine-e and Cypridina luciferin with an experimental and theoretical approach","volume":"190","year":"2019","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2646","DOI":"10.7150\/thno.32219","article-title":"Highly bright and stable NIR-BRET with blue-shifted coelenterazine derivatives for deep-tissue imaging of molecular events in vivo","volume":"9","author":"Nishihara","year":"2019","journal-title":"Theranostics"}],"container-title":["Applied Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3417\/13\/11\/6617\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:44:46Z","timestamp":1760125486000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3417\/13\/11\/6617"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,29]]},"references-count":50,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["app13116617"],"URL":"https:\/\/doi.org\/10.3390\/app13116617","relation":{},"ISSN":["2076-3417"],"issn-type":[{"value":"2076-3417","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,29]]}}}