{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T18:47:27Z","timestamp":1789238847324,"version":"build-2803163510"},"reference-count":53,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,3,15]],"date-time":"2024-03-15T00:00:00Z","timestamp":1710460800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"New Frontiers in Research Fund Exploration","award":["NFRFE-2019-01585"],"award-info":[{"award-number":["NFRFE-2019-01585"]}]},{"name":"Northern Cancer Foundation Grant","award":["NFRFE-2019-01585"],"award-info":[{"award-number":["NFRFE-2019-01585"]}]},{"name":"NOSM University Faculty Association Research Development Award","award":["NFRFE-2019-01585"],"award-info":[{"award-number":["NFRFE-2019-01585"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Radiation therapy for abdominopelvic malignancies often results in damage to the gastrointestinal tract (GIT) and permanent changes in bowel function. An overlooked component of the pathophysiology of radiation-induced bowel injury is the role of the gut microbiome. The goal of this research was to identify the impacts of acute radiation exposure on the GIT and gut microbiome. C57BL\/6 mice exposed to whole-body X-rays (0.1\u20133 Gy) were assessed for histological and microbiome changes 48 h post-radiation exposure. Within the ileum, a dose of 3 Gy significantly decreased crypt depth as well as the number of goblet cells, but increased overall goblet cell size. Overall, radiation altered the microbial distribution within each of the main phyla in a dose- and tissue-dependent manner. Within the Firmicutes phylum, high dose irradiation resulted in significant alterations in bacteria from the class Bacilli within the small bowels, and from the class Clostridia in the large bowels. The 3 Gy radiation also significantly increased the abundance of bacterial families from the Bacteroidetes phylum in the colon and feces. Overall, we identified various alterations in microbiome composition following acute radiation exposure, which could potentially lead to novel biomarkers for tracking patient toxicities or could be used as targets for mitigation strategies against radiation damage.<\/jats:p>","DOI":"10.3390\/ijms25063339","type":"journal-article","created":{"date-parts":[[2024,3,15]],"date-time":"2024-03-15T09:32:30Z","timestamp":1710495150000},"page":"3339","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["Acute Impacts of Ionizing Radiation Exposure on the Gastrointestinal Tract and Gut Microbiome in Mice"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9749-1461","authenticated-orcid":false,"given":"Alexandra","family":"Jameus","sequence":"first","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica","family":"Dougherty","sequence":"additional","affiliation":[{"name":"Medical Sciences Division, NOSM University, 935 Ramsey Lake Rd., Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramya","family":"Narendrula","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniela","family":"Levert","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manon","family":"Valiquette","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jake","family":"Pirkkanen","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7467-5575","authenticated-orcid":false,"given":"Christine","family":"Lalonde","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrice","family":"Bonin","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey D.","family":"Gagnon","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vasu D.","family":"Appanna","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sujeenthar","family":"Tharmalingam","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"},{"name":"Medical Sciences Division, NOSM University, 935 Ramsey Lake Rd., Sudbury, ON P3E 2C6, Canada"},{"name":"Health Sciences North Research Institute, 56 Walford Road, Sudbury, ON P3E 2H3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0160-9657","authenticated-orcid":false,"given":"Christopher","family":"Thome","sequence":"additional","affiliation":[{"name":"School of Natural Sciences, Laurentian University, Sudbury, ON P3E 2C6, Canada"},{"name":"Medical Sciences Division, NOSM University, 935 Ramsey Lake Rd., Sudbury, ON P3E 2C6, Canada"},{"name":"Health Sciences North Research Institute, 56 Walford Road, Sudbury, ON P3E 2H3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,15]]},"reference":[{"key":"ref_1","first-page":"142","article-title":"Radiation Therapy for Cancer","volume":"Volume 3","author":"Gelband","year":"2015","journal-title":"Cancer: Disease Control Priorities"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"400","DOI":"10.4251\/wjgo.v13.i5.400","article-title":"Update on the Management of the Gastrointestinal Effects of Radiation","volume":"13","author":"McCaughan","year":"2021","journal-title":"World J. Gastrointest. Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Kumagai, T., Rahman, F., and Smith, A.M. (2018). The Microbiome and Radiation Induced-Bowel Injury: Evidence for Potential Mechanistic Role in Disease Pathogenesis. Nutrients, 10.","DOI":"10.3390\/nu10101405"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"643283","DOI":"10.3389\/fphar.2021.643283","article-title":"Acute Radiation Syndrome and the Microbiome: Impact and Review","volume":"12","author":"Hollingsworth","year":"2021","journal-title":"Front. Pharmacol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1177\/2040622313510730","article-title":"Radiation-Induced Small Bowel Disease: Latest Developments and Clinical Guidance","volume":"5","author":"Stacey","year":"2014","journal-title":"Ther. Adv. Chronic Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"13803","DOI":"10.1038\/s41598-019-50023-4","article-title":"Long-Term Mucosal Injury and Repair in a Murine Model of Pelvic Radiotherapy","volume":"9","author":"Malipatlolla","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Appanna, V.D. (2018). Human Microbes-the Power within: Health, Healing and Beyond, Springer.","DOI":"10.1007\/978-981-10-7684-8"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Paquette, S., Thomas, S.C., Venkataraman, K., Appanna, V.D., and Tharmalingam, S. (2023). The Effects of Oral Probiotics on Type 2 Diabetes Mellitus (T2DM): A Clinical Trial Systematic Literature Review. Nutrients, 15.","DOI":"10.3390\/nu15214690"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Lkhagva, D.E., Chung, H.J., Hong, J., Tang, W.H.W., Lee, S.I., Hong, S.T., and Lee, S. (2021). The Regional Diversity of Gut Microbiome along the GI Tract of Male C57BL\/6 Mice. BMC Microbiol., 21.","DOI":"10.1186\/s12866-021-02099-0"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1002\/ame2.12257","article-title":"Characteristics of Gut Microbiota in Representative Mice Strains: Implications for Biological Research","volume":"5","author":"Guo","year":"2022","journal-title":"Anim. Model. Exp. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1264\/jsme2.ME17017","article-title":"Microbial Ecology along the Gastrointestinal Tract","volume":"32","author":"Hillman","year":"2017","journal-title":"Microbes Environ."},{"key":"ref_12","first-page":"3508","article-title":"The Protective Role of Short-Chain Fatty Acids Acting as Signal Molecules in Chemotherapy- or Radiation-Induced Intestinal Inflammation","volume":"10","author":"Tian","year":"2020","journal-title":"Am. J. Cancer Res."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Nam, Y.-D., Kim, H.J., Seo, J.-G., Kang, S.W., and Bae, J.-W. (2013). Impact of Pelvic Radiotherapy on Gut Microbiota of Gynecological Cancer Patients Revealed by Massive Pyrosequencing. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0082659"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Wang, A., Ling, Z., Yang, Z., Kiela, P.R., Wang, T., Wang, C., Cao, L., Geng, F., Shen, M., and Ran, X. (2015). Gut Microbial Dysbiosis May Predict Diarrhea and Fatigue in Patients Undergoing Pelvic Cancer Radiotherapy: A Pilot Study. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0126312"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Vill\u00e9ger, R., Lop\u00e8s, A., Carrier, G., Veziant, J., Billard, E., Barnich, N., Gagni\u00e8re, J., Vazeille, E., and Bonnet, M. (2019). Intestinal Microbiota: A Novel Target to Improve Anti-Tumor Treatment?. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20184584"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Kalkeri, R., Walters, K., Van Der Pol, W., McFarland, B.C., Fisher, N., Koide, F., Morrow, C.D., and Singh, V.K. (2021). Changes in the Gut Microbiome Community of Nonhuman Primates Following Radiation Injury. BMC Microbiol., 21.","DOI":"10.1186\/s12866-021-02146-w"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1667\/RR14975.1","article-title":"Specific Members of the Gut Microbiota Are Reliable Biomarkers of Irradiation Intensity and Lethality in Large Animal Models of Human Health","volume":"191","author":"Carbonero","year":"2018","journal-title":"Radiat. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1093\/toxsci\/kfz144","article-title":"Impact of Low-Dose Ionising Radiation on the Composition of the Gut Microbiota of Mice","volume":"171","author":"Liu","year":"2019","journal-title":"Toxicol. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e139","DOI":"10.1016\/S1470-2045(13)70504-7","article-title":"Microbiota and Radiation-Induced Bowel Toxicity: Lessons from Inflammatory Bowel Disease for the Radiation Oncologist","volume":"15","author":"Ferreira","year":"2014","journal-title":"Lancet Oncol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1111\/apt.12878","article-title":"Systematic Review: The Role of the Gut Microbiota in Chemotherapy- or Radiation-Induced Gastrointestinal Mucositis\u2014Current Evidence and Potential Clinical Applications","volume":"40","author":"Touchefeu","year":"2014","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Segers, C., Mastroleo, F., Verslegers, M., Baatout, S., Leys, N., and Lebeer, S. (2019). Food Supplements to Mitigate Detrimental Effects of Pelvic Radiotherapy. Microorganisms, 7.","DOI":"10.3390\/microorganisms7040097"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.rpor.2011.06.001","article-title":"Radiobiology of the Acute Radiation Syndrome","volume":"16","year":"2011","journal-title":"Rep. Pract. Oncol. Radiother."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/s43705-021-00024-0","article-title":"Intestinal Mucositis Precedes Dysbiosis in a Mouse Model for Pelvic Irradiation","volume":"11","author":"Segers","year":"2021","journal-title":"ISME Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1136\/gutjnl-2011-300367","article-title":"Lactobacillus Probiotic Protects Intestinal Epithelium from Radiation Injury in a TLR-2\/Cyclo-Oxygenase-2-Dependent Manner","volume":"61","author":"Ciorba","year":"2012","journal-title":"Gut"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1002\/jcp.30651","article-title":"Lactobacillus Plantarum Alleviates Irradiation-Induced Intestinal Injury by Activation of FXR-FGF15 Signaling in Intestinal Epithelia","volume":"237","author":"Jian","year":"2022","journal-title":"J. Cell. Physiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2967","DOI":"10.1021\/acsomega.9b03906","article-title":"Antibiotic Alleviates Radiation-Induced Intestinal Injury by Remodeling Microbiota, Reducing Inflammation, and Inhibiting Fibrosis","volume":"5","author":"Zhao","year":"2020","journal-title":"ACS Omega"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1080\/09553002.2020.1830317","article-title":"Gut Microbiota Response to Ionizing Radiation and Its Modulation by HDAC Inhibitor TSA","volume":"96","author":"Gupta","year":"2020","journal-title":"Int. J. Radiat. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Livanova, A.A., Fedorova, A.A., Zavirsky, A.V., Krivoi, I.I., and Markov, A.G. (2023). Dose- and Segment-Dependent Disturbance of Rat Gut by Ionizing Radiation: Impact of Tight Junction Proteins. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24021753"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1038\/s41467-022-28744-4","article-title":"Microalgae-Based Oral Microcarriers for Gut Microbiota Homeostasis and Intestinal Protection in Cancer Radiotherapy","volume":"13","author":"Zhang","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1177\/2050640616640443","article-title":"A PPAR-Gamma Agonist Protects from Radiation-Induced Intestinal Toxicity","volume":"5","author":"Mangoni","year":"2017","journal-title":"United Eur. Gastroenterol. J."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Jang, H., Kim, S., Kim, H., Oh, S.H., Kwak, S.Y., Joo, H.W., Lee, S.B., Jang, W.I., Park, S., and Shim, S. (2022). Metformin Protects the Intestinal Barrier by Activating Goblet Cell Maturation and Epithelial Proliferation in Radiation-Induced Enteropathy. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23115929"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1007\/s11894-010-0130-3","article-title":"Intestinal Stem Cells","volume":"12","author":"Umar","year":"2010","journal-title":"Curr. Gastroenterol. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1093\/femsre\/fuz013","article-title":"Experimental Models to Study Intestinal Microbes\u2013Mucus Interactions in Health and Disease","volume":"43","author":"Chassaing","year":"2019","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2232","DOI":"10.1136\/gutjnl-2020-322260","article-title":"Mucus Barrier, Mucins and Gut Microbiota: The Expected Slimy Partners?","volume":"69","author":"Paone","year":"2020","journal-title":"Gut"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"109473","DOI":"10.1016\/j.foodres.2020.109473","article-title":"Health Promoting Microbial Metabolites Produced by Gut Microbiota after Prebiotics Metabolism","volume":"136","year":"2020","journal-title":"Food Res. Int."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1007\/s11894-010-0131-2","article-title":"Intestinal Goblet Cells and Mucins in Health and Disease: Recent Insights and Progress","volume":"12","author":"Kim","year":"2010","journal-title":"Curr. Gastroenterol. Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1131S","DOI":"10.1093\/ajcn\/73.6.1131S","article-title":"Microbial Modulation of Innate Defense: Goblet Cells and the Intestinal Mucus Layer","volume":"73","author":"Deplancke","year":"2001","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1038\/s12276-020-0473-2","article-title":"Of Men in Mice: The Development and Application of a Humanized Gnotobiotic Mouse Model for Microbiome Therapeutics","volume":"52","author":"Park","year":"2020","journal-title":"Exp. Mol. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1111\/j.1445-2197.1980.tb04500.x","article-title":"Anaerobic Bacteria, the Colon and Colitis","volume":"50","author":"Roediger","year":"1980","journal-title":"Aust. N. Z. J. Surg."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/imm.12760","article-title":"The Immune Response to Prevotella Bacteria in Chronic Inflammatory Disease","volume":"151","author":"Larsen","year":"2017","journal-title":"Immunology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"840245","DOI":"10.3389\/fimmu.2022.840245","article-title":"Lactobacillus Spp. for Gastrointestinal Health: Current and Future Perspectives","volume":"13","author":"Dempsey","year":"2022","journal-title":"Front. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.jenvrad.2018.10.012","article-title":"Review of Microbial Resistance to Chronic Ionizing Radiation Exposure under Environmental Conditions","volume":"196","author":"Shuryak","year":"2019","journal-title":"J. Environ. Radioact."},{"key":"ref_43","first-page":"75","article-title":"Radioresistance: Implications for Astrobiological and Medical Research","volume":"4","author":"Lai","year":"2019","journal-title":"Health Sci. Isc."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.mrrev.2015.10.001","article-title":"Unraveling the Mechanisms of Extreme Radioresistance in Prokaryotes: Lessons from Nature","volume":"767","author":"Pavlopoulou","year":"2016","journal-title":"Mutat. Res.-Rev. Mutat. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1007\/s00125-015-3614-8","article-title":"A Model for the Role of Gut Bacteria in the Development of Autoimmunity for Type 1 Diabetes","volume":"58","author":"Triplett","year":"2015","journal-title":"Diabetologia"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.ijrobp.2019.12.040","article-title":"Microbial Diversity and Composition Is Associated with Patient-Reported Toxicity during Chemoradiation Therapy for Cervical Cancer","volume":"107","author":"Mitra","year":"2020","journal-title":"Int. J. Radiat. Oncol. Biol. Phys."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1981","DOI":"10.1016\/j.bbadis.2014.05.023","article-title":"Rapidly Expanding Knowledge on the Role of the Gut Microbiome in Health and Disease","volume":"1842","author":"Matzaraki","year":"2014","journal-title":"Biochim. Biophys. Acta-Mol. Basis Dis."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"4112","DOI":"10.1111\/jam.15504","article-title":"Balancing Reactive Oxygen Species Generation by Rebooting Gut Microbiota","volume":"132","author":"Singh","year":"2022","journal-title":"J. Appl. Microbiol."},{"key":"ref_49","unstructured":"Mohan, H., Soni, S., and Syed, S. (2022). Handbook of Oxidative Stress in Cancer: Therapeutic Aspects, Springer."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An Open-Source Platform for Biological-Image Analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1002\/cpmo.2","article-title":"Intestinal Preparation Techniques for Histological Analysis in the Mouse","volume":"6","author":"Williams","year":"2016","journal-title":"Curr. Protoc. Mouse Biol."},{"key":"ref_52","first-page":"e59980","article-title":"Microbiota Analysis Using Two-Step PCR and Next-Generation 16S RRNA Gene Sequencing","volume":"2019","author":"Shahi","year":"2019","journal-title":"J. Vis. Exp."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1002\/j.1538-7305.1948.tb01338.x","article-title":"A Mathematical Theory of Communication","volume":"27","author":"Shannon","year":"1948","journal-title":"Bell Syst. Technol. J."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/6\/3339\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:14:08Z","timestamp":1760105648000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/6\/3339"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,15]]},"references-count":53,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["ijms25063339"],"URL":"https:\/\/doi.org\/10.3390\/ijms25063339","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,15]]}}}