{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T16:03:54Z","timestamp":1753891434005,"version":"3.41.2"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,3,2]],"date-time":"2023-03-02T00:00:00Z","timestamp":1677715200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002367","name":"Chinese Academy of Sciences","doi-asserted-by":"publisher","award":["XDA26040304 and XDA26050102"],"award-info":[{"award-number":["XDA26040304 and XDA26050102"]}],"id":[{"id":"10.13039\/501100002367","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32072760"],"award-info":[{"award-number":["32072760"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Silybum marianum meal is a by-product that remains silymarin complex and is perceived as a potential-protein source. The potential and its mechanism of silybum marianum meal as a protein supplement in ruminants were evaluated by testing the growth performance, biochemical parameters, cytokine levels, gut transcriptome and microbial community profiles. Forty-two male Hulunbeier growing lambs (aged about 3-month-old; averaged body weight of 21.55\u2009kg) were randomly divided into the CON (with 10% soybean meal) and SIL groups (with 10% silybum marianum meal). There was no significant difference in growth performance, feed intakes, or serum biochemical parameters between CON and SIL. The serum levels of IL-1\u03b2, TNF-\u03b1, TGF-\u03b2, HGF, and VEGF were all increased (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05) in the SIL group as compared with the CON group. Transcriptome gene set enrichment analysis (GSEA) revealed that the core genes in the rumen from SIL group were enriched with fructose and mannose metabolism, while the core genes in the ileum were enriched for three biological process, including digestive tract development, positive regulation of MAPK cascade, and regulation of I-kappaB kinase\/NF-kappaB signaling. The 16S rDNA results showed that the relative abundance of <jats:italic>Bacteroidetes<\/jats:italic>, <jats:italic>Firmicutes<\/jats:italic>, <jats:italic>Synergistetes<\/jats:italic>, and <jats:italic>Verrucomicrobia<\/jats:italic> in the rumen from SIL group was significantly higher than that in CON group (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05), whereas <jats:italic>Proteobacteria<\/jats:italic> was significantly lower than that in CON group (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05). The LEfSe analysis showed that the genera <jats:italic>Pyramidobacter<\/jats:italic>, <jats:italic>Saccharofermentans<\/jats:italic>, <jats:italic>Anaerovibrio<\/jats:italic>, <jats:italic>Oscillibacter<\/jats:italic> and <jats:italic>Barnesiella<\/jats:italic> were enriched in the rumen from SIL group, whereas <jats:italic>Sharpea<\/jats:italic> was enriched in the CON group (LDA\u2009&amp;gt;\u20092). In the ileum, there were no significant differences in the phylum-level classification of microbes observed. At the genus level, the relative abundances of <jats:italic>Bifidobacterium<\/jats:italic> and <jats:italic>Ruminococcus<\/jats:italic> in the ileum from SIL group were significantly higher than that in the CON group (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05), whereas the relative abundance of <jats:italic>Clostridium_XI<\/jats:italic> was lower (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05). Correlation analysis showed that <jats:italic>Clostridium_XI<\/jats:italic> was negatively correlated with VEGF, TGF-\u03b2, TNF-\u03b1 and HGF (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05). Core genes <jats:italic>BMP4<\/jats:italic> and <jats:italic>CD4<\/jats:italic> were negatively correlated with <jats:italic>Clostridium_XI<\/jats:italic> (<jats:italic>p<\/jats:italic> &amp;lt;\u20090.05). Our results indicated that supplementing silybum marianum meal as a replacement for soybean meal resulted in increased cytokines production without affecting growth performance in growing lambs, and the enrichment of immune-related genes and altered microbial community in the ileum were contributed to the increased immune responses.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1093129","type":"journal-article","created":{"date-parts":[[2023,3,2]],"date-time":"2023-03-02T07:09:34Z","timestamp":1677740974000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs"],"prefix":"10.3389","volume":"14","author":[{"given":"Tianxi","family":"Zhang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yanbo","family":"Ren","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chao","family":"Yang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kefyalew","family":"Gebeyew","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Min","family":"Gao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhixiong","family":"He","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhiliang","family":"Tan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,3,2]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.applanim.2016.03.008","article-title":"Targeted grazing of milk thistle (Silybum marianum) and Syrian thistle (Notobasis syriaca) by goats: preference following preconditioning, generational transfer, and toxicity","volume":"179","author":"Arviv","year":"2016","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.cell.2014.03.011","article-title":"Role of the microbiota in immunity and inflammation","volume":"157","author":"Belkaid","year":"2014","journal-title":"Cells"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"2333","DOI":"10.1111\/1462-2920.14614","article-title":"Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs","volume":"21","author":"Bi","year":"2019","journal-title":"Environ. Microbiol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1007\/s00251-017-1037-z","article-title":"Impact of a CD4 gene haplotype on the immune response in minipigs","volume":"70","author":"Blanc","year":"2018","journal-title":"Immunogenetics"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"2735","DOI":"10.1099\/ijs.0.017590-0","article-title":"Saccharofermentans acetigenes gen. Nov., sp. nov., an anaerobic bacterium isolated from sludge treating brewery wastewater","volume":"60","author":"Chen","year":"2010","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"23801","DOI":"10.1038\/s41598-021-03207-w","article-title":"Influence of selected factors on the Firmicutes, Bacteroidetes phyla and the Lactobacillaceae family in the digestive tract of sheep","volume":"11","author":"Cholewi\u0144ska","year":"2021","journal-title":"Sci. Rep."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1007\/s00580-010-0984-7","article-title":"Hepatoprotective effect of silymarin during negative energy balance in sheep","volume":"20","author":"Dehghan","year":"2011","journal-title":"Comp. Clin. Pathol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2020\/8884583","article-title":"The protective role of probiotics against colorectal cancer","volume":"2020","author":"Ding","year":"2020","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1687","DOI":"10.3390\/ani11061687","article-title":"Dose effect of milk thistle (Silybum marianum) seed cakes on the digestibility of nutrients, flavonolignans and the individual components of the silymarin complex in horses","volume":"11","author":"Dockalova","year":"2021","journal-title":"Animals"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"2460","DOI":"10.1093\/bioinformatics\/btq461","article-title":"Search and clustering orders of magnitude faster than BLAST","volume":"26","author":"Edgar","year":"2010","journal-title":"Bioinforma. Oxf. Engl."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1038\/nmeth.2604","article-title":"UPARSE: highly accurate OTU sequences from microbial amplicon reads","volume":"10","author":"Edgar","year":"2013","journal-title":"Nat. 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Biotechnol."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"104180","DOI":"10.1016\/j.livsci.2020.104180","article-title":"Impact of milk thistle (Silybum marianum L.) seeds in fattener diets on pig performance and carcass traits and fatty acid profile and cholesterol of meat, backfat and liver","volume":"239","author":"Grela","year":"2020","journal-title":"Livest. Sci."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/S0308-8146(01)00152-2","article-title":"High pressure extraction of vitamin E-rich oil from Silybum marianum","volume":"74","author":"Hadolin","year":"2001","journal-title":"Food Chem."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"410","DOI":"10.1111\/jpn.12747","article-title":"Effects of milk thistle meal on performance, ileal bacterial enumeration, jejunal morphology and blood lipid peroxidation in laying hens fed diets with different levels of metabolizable energy","volume":"102","author":"Hashemi Jabali","year":"2018","journal-title":"J. Anim. Physiol. Anim. Nutr."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1002\/JLB.4VMR0720-201R","article-title":"The adaptive immune response to Clostridioides difficile: a tricky balance between immunoprotection and immunopathogenesis","volume":"109","author":"Hern\u00e1ndez Del Pino","year":"2021","journal-title":"J. Leukoc. Biol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1210\/en.2009-0914","article-title":"Inhibitor of differentiation (id) genes are expressed in the steroidogenic cells of the ovine ovary and are differentially regulated by members of the transforming growth factor-\u03b2 family","volume":"151","author":"Hogg","year":"2010","journal-title":"Endocrinology"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1028","DOI":"10.1099\/ijs.0.006718-0","article-title":"Description of \u201cSynergistetes\u201d phyl. Nov. and emended description of the phylum \u201cDeferribacteres\u201d and of the family Syntrophomonadaceae, phylum \u201cFirmicutes.\u201d","volume":"59","author":"Jumas-Bilak","year":"2009","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1186\/s40168-016-0201-2","article-title":"Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation","volume":"4","author":"Kamke","year":"2016","journal-title":"Microbiome"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"fiaa077","DOI":"10.1093\/femsec\/fiaa077","article-title":"Characterization and survey in cattle of a rumen Pyrimadobacter sp. which degrades the plant toxin fluoroacetate","volume":"96","author":"Kang","year":"2020","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.5713\/ajas.2009.r.11","article-title":"Dietary transformation of lipid in the rumen microbial ecosystem","volume":"22","author":"Kim","year":"2009","journal-title":"Asian-Aust. J. Anim. Sci."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat. Methods"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"117157","DOI":"10.1016\/j.lfs.2019.117157","article-title":"MAP kinase phosphatase-1, a gatekeeper of the acute innate immune response","volume":"241","author":"Kirk","year":"2020","journal-title":"Life Sci."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"1332","DOI":"10.1016\/j.cell.2016.05.041","article-title":"From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites","volume":"165","author":"Koh","year":"2016","journal-title":"Cells"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/s10456-012-9255-3","article-title":"Soluble HSPB1 regulates VEGF-mediated angiogenesis through their direct interaction","volume":"15","author":"Lee","year":"2012","journal-title":"Angiogenesis"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1186\/1471-2105-12-323","article-title":"RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome","volume":"12","author":"Li","year":"2011","journal-title":"BMC Bioinform."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1093\/bioinformatics\/btn025","article-title":"SOAP: short oligonucleotide alignment program","volume":"24","author":"Li","year":"2008","journal-title":"Bioinforma. Oxf. Engl."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"479","DOI":"10.3390\/metabo11080479","article-title":"Fructose and mannose in inborn errors of metabolism and cancer","volume":"11","author":"Lieu","year":"2021","journal-title":"Meta"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1007\/s10482-015-0459-6","article-title":"Exploring the sheep rumen microbiome for carbohydrate-active enzymes","volume":"108","author":"Lopes","year":"2015","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"2957","DOI":"10.1093\/bioinformatics\/btr507","article-title":"FLASH: fast length adjustment of short reads to improve genome assemblies","volume":"27","author":"Magoc","year":"2011","journal-title":"Bioinformatics"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1016\/j.chom.2019.08.011","article-title":"Regional diversity of the gastrointestinal microbiome","volume":"26","author":"Martinez-Guryn","year":"2019","journal-title":"Cell Host Microbe"},{"key":"ref36","doi-asserted-by":"crossref","DOI":"10.1385\/1-59259-171-X:117","article-title":"Cytokines, cytokine antagonists, and growth factors for treating infections","volume-title":"Immunotherapy for Infectious Diseases","author":"Matthews","year":"2002"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1038\/nri3738","article-title":"Regional specialization within the intestinal immune system","volume":"14","author":"Mowat","year":"2014","journal-title":"Nat. Rev. Immunol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.aninu.2022.04.002","article-title":"Understanding the role of rumen epithelial host-microbe interactions in cattle feed efficiency","volume":"10","author":"Na","year":"2022","journal-title":"Anim. Nutr."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"e1000661","DOI":"10.1371\/journal.ppat.1000661","article-title":"IL-1\u03b2 processing in host defense: beyond the inflammasomes","volume":"6","author":"Netea","year":"2010","journal-title":"PLoS Pathog."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"804949","DOI":"10.3389\/fmicb.2021.804949","article-title":"Host immune responses to clostridioides difficile: toxins and beyond","volume":"12","author":"Nibbering","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref41","first-page":"401","article-title":"Effect of different levels of milk thistle (Silybum Marianum) in diets containing cereal grains with different ruminal degradation rate on rumen bacteria of Khuzestan buffalo","volume":"7","author":"Nikzad","year":"2017","journal-title":"Iran. J. Appl. Anim. Sci."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"419","DOI":"10.5958\/2231-6744.2019.00068.9","article-title":"Successful management of nitrite poisoning in crossbred dairy calves","volume":"36","author":"Niyas","year":"2019","journal-title":"Indian J. Anim. Nutr."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"4745","DOI":"10.4049\/jimmunol.175.7.4745","article-title":"A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function","volume":"175","author":"Okunishi","year":"2005","journal-title":"J. Immunol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"775","DOI":"10.1080\/1547691X.2016.1193574","article-title":"Is TGF\u03b2 as an anti-inflammatory cytokine required for differentiation of inflammatory T H 17 cells?","volume":"13","author":"Pourgholaminejad","year":"2016","journal-title":"J. Immunotoxicol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"838","DOI":"10.3390\/ani11030838","article-title":"Diet transition from high-forage to high-concentrate alters rumen bacterial community composition, epithelial transcriptomes and ruminal fermentation parameters in dairy cows","volume":"11","author":"Ramos","year":"2021","journal-title":"Animals"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"16180","DOI":"10.1038\/s41598-021-95691-3","article-title":"Dietary cardoon meal modulates rumen biohydrogenation and bacterial community in lambs","volume":"11","author":"Salami","year":"2021","journal-title":"Sci. Rep."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"993","DOI":"10.11118\/actaun201967040993","article-title":"Performance, biochemical profile and antioxidant activity of hens supplemented with addition of milk thistle (Silybum marianum) seed cakes in diet","volume":"67","author":"\u0160\u0165astn\u00edk","year":"2019","journal-title":"Acta Univ. Agric. Silvic. Mendel. Brun."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"1384","DOI":"10.3390\/ani10081384","article-title":"The milk thistle seed cakes and hempseed cakes are potential feed for poultry","volume":"10","author":"Stastnik","year":"2020","journal-title":"Animals"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"31","DOI":"10.2754\/avb200877010031","article-title":"Hepatoprotective effects of milk thistle (Silybum marianum) seed cakes during the chicken broiler fattening","volume":"77","author":"Such\u00fd","year":"2008","journal-title":"Acta Vet. Brno"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1038\/nri.2017.52","article-title":"The non-canonical NF-\u03baB pathway in immunity and inflammation","volume":"17","author":"Sun","year":"2017","journal-title":"Nat. Rev. Immunol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"600","DOI":"10.3109\/10799893.2015.1030412","article-title":"Signaling pathway of MAPK\/ERK in cell proliferation, differentiation, migration, senescence and apoptosis","volume":"35","author":"Sun","year":"2015","journal-title":"J. Recept. Signal Transduct."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1002\/ptr.6153","article-title":"Silybum marianum (milk thistle) and its main constituent, silymarin, as a potential therapeutic plant in metabolic syndrome: a review: silybum marianum and metabolic syndrome","volume":"32","author":"Tajmohammadi","year":"2018","journal-title":"Phytother. Res."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"4816","DOI":"10.1002\/jsfa.9115","article-title":"Effects of silymarin on metabolic syndrome: a review: silymarin and metabolic syndrome","volume":"98","author":"Vahabzadeh","year":"2018","journal-title":"J. Sci. Food Agric."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"802823","DOI":"10.3389\/fmicb.2022.802823","article-title":"Gut microbiota and metabolite changes in patients with ulcerative colitis and Clostridioides difficile infection","volume":"13","author":"Wan","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"895636","DOI":"10.3389\/fimmu.2022.895636","article-title":"NF-\u03baB inducing kinase regulates intestinal immunity and homeostasis","volume":"13","author":"Wang","year":"2022","journal-title":"Front. Immunol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"e20191130","DOI":"10.1084\/jem.20191130","article-title":"Single-cell transcriptome analysis reveals differential nutrient absorption functions in human intestine","volume":"217","author":"Wang","year":"2020","journal-title":"J. Exp. Med."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"e0205055","DOI":"10.1371\/journal.pone.0205055","article-title":"Dietary or supplemental fermentable fiber intake reduces the presence of clostridium XI in mouse intestinal microbiota: the importance of higher fecal bacterial load and density","volume":"13","author":"Zheng","year":"2018","journal-title":"PLoS One"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1093129\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,2]],"date-time":"2023-03-02T07:09:42Z","timestamp":1677740982000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1093129\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,2]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2023.1093129"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1093129","relation":{},"ISSN":["1664-302X"],"issn-type":[{"type":"electronic","value":"1664-302X"}],"subject":[],"published":{"date-parts":[[2023,3,2]]},"article-number":"1093129"}}