{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T12:04:41Z","timestamp":1787313881208,"version":"build-2736575974"},"reference-count":59,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,7,10]],"date-time":"2025-07-10T00:00:00Z","timestamp":1752105600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Stenotrophomonas maltophilia<\/jats:italic>\n                      , an important opportunistic pathogen resistant to multiple antibiotics, necessitates alternative therapies. Phages, with their high specificity and bacteriolytic ability, are emerging as promising antibiotic alternatives. This study aimed to isolate and characterize a novel lytic phage targeting\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      and to evaluate its antibacterial potential.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      A novel lytic phage, vB_SmaS_QH16, was isolated from hospital sewage using\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      no.981 as the host. Phage morphology was analyzed using transmission electron microscopy (TEM), and genome sequencing and annotation were performed. Host range, efficiency of lysis (EOP), optimal multiplicity of infection (MOI), one-step growth curves, and physicochemical stability were also determined. Biofilm inhibition and eradication were assessed using crystal violet staining, MTT assays, and acridine orange fluorescence microscopy. Using\n                      <jats:italic>Galleria mellonella<\/jats:italic>\n                      and mouse infection models, the\n                      <jats:italic>in vivo<\/jats:italic>\n                      anti-infective effects of phages were evaluated.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Phage vB_SmaS_QH16, a member of the class Caudoviricetes, has a 43,500 bp genome with 64 open reading frames (ORFs) and no virulence, antibiotic resistance, or lysogeny-related genes. It exhibits a broad host range, lysing 47.95% (35\/73) of tested\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      strains. The optimal MOI was 0.01, with an average burst size of 37.69 PFU\/cell. The phage is stable at 4\u201350 \u00b0C and pH 3.0\u201311.0 but is highly sensitive to UV light. It effectively inhibits biofilm formation and eradicates mature biofilms in a concentration-dependent manner.\n                      <jats:italic>In vitro<\/jats:italic>\n                      , the phage significantly suppresses bacterial growth, though resistant mutants emerge over time.\n                      <jats:italic>In vivo<\/jats:italic>\n                      , vB_SmaS_QH16 increases the survival rates of larvae and mice, with a higher MOI offering better protection.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>\n                      Phage vB_SmaS_QH16 shows therapeutic potential against\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      infections, characterized by a broad host range, efficient lytic capability, and biofilm-disrupting activity. Its stability and safety further support its clinical application potential. Future research should explore its biofilm disruption mechanisms and monitor resistance development. Additionally, since its efficacy has been validated in mammalian models, further studies can focus on advancing its clinical translation.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fcimb.2025.1610857","type":"journal-article","created":{"date-parts":[[2025,7,10]],"date-time":"2025-07-10T05:31:22Z","timestamp":1752125482000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Characterization and antimicrobial activity of a novel lytic phage vB_SmaS_QH16 against Stenotrophomonas maltophilia: in vitro, in vivo, and biofilm studies"],"prefix":"10.3389","volume":"15","author":[{"given":"Peng","family":"Cheng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zian","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lanmin","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruizhe","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianwu","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqin","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoming","family":"Mu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingwei","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jideng","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangren","family":"A","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,7,10]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1207","DOI":"10.1007\/s10096-023-04649-y","article-title":"A novel lytic phage exhibiting a remarkable in vivo therapeutic potential and higher antibiofilm activity against Pseudomonas aeruginosa","volume":"42","author":"Abdelghafar","year":"2023","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2017.00981","article-title":"Editorial: phage therapy: past, present and future","volume":"8","author":"Abedon","year":"2017","journal-title":"Front. Microbiol."},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms12061202","article-title":"Biological traits and comprehensive genomic analysis of novel enterococcus faecalis bacteriophage EFP6","volume":"12","author":"Ahmad","year":"2024","journal-title":"Microorganisms"},{"key":"B4","doi-asserted-by":"publisher","first-page":"1222","DOI":"10.15537\/smj.2023.44.12.20230366","article-title":"Bacteriophage treatment as an alternative therapy for multidrug-resistant bacteria","volume":"44","author":"Alqahtani","year":"2023","journal-title":"SMJ"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2022.897531","article-title":"Isolation and Characterization of vB_kpnM_17-11, a Novel Phage Efficient Against Carbapenem-Resistant Klebsiella pneumoniae","volume":"12","author":"Bai","year":"2022","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1089\/phage.2024.0005","article-title":"Beyond antibiotics: exploring the potential of bacteriophages and phage therapy","volume":"5","author":"Biswas","year":"2024","journal-title":"Phage Ther. Appl. Res"},{"key":"B7","doi-asserted-by":"publisher","first-page":"3491","DOI":"10.1093\/jac\/dkaa345","article-title":"ResFinder 4.0 for predictions of phenotypes from genotypes","volume":"75","author":"Bortolaia","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"B8","doi-asserted-by":"publisher","first-page":"S384","DOI":"10.1093\/cid\/ciad497","article-title":"Therapeutic phage monitoring: A review","volume":"77","author":"Bosco","year":"2023","journal-title":"Clin. Infect. Dis."},{"key":"B9","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1128\/cmr.00019-11","article-title":"Stenotrophomonas maltophilia: an emerging global opportunistic pathogen","volume":"25","author":"Brooke","year":"2012","journal-title":"Clin. Microbiol. Rev."},{"key":"B10","first-page":"33","article-title":"Phage lysis: multiple genes for multiple barriers","volume-title":"Advances in virus research","author":"Cahill","year":"2019"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1186\/s12941-020-00389-5","article-title":"Bacteriophage therapy against Pseudomonas aeruginosa biofilms: a review","volume":"19","author":"Chegini","year":"2020","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1186\/s12985-023-02036-9","article-title":"Isolation and characterization of a novel phage belonging to a new genus against Vibrio parahaemolyticus","volume":"20","author":"Chen","year":"2023","journal-title":"Virol. J."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2025.1570665","article-title":"Characterization of the novel cross-genus phage vB_SmaS_QH3 and evaluation of its antibacterial efficacy against Stenotrophomonas maltophilia","volume":"16","author":"Cheng","year":"2025","journal-title":"Front. Microbiol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1038\/s41579-019-0311-5","article-title":"Phage diversity, genomics and phylogeny","volume":"18","author":"Dion","year":"2020","journal-title":"Nat. Rev. Microbiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1007\/bf03189322","article-title":"Gastric juice as a dissolution medium: surface tension and pH","volume":"23","author":"Efentakis","year":"1998","journal-title":"Eur. J. Drug Metab. Pharmacokinet."},{"key":"B16","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1080\/14787210.2018.1425139","article-title":"Therapies for multidrug resistant and extensively drug-resistant non-fermenting gram-negative bacteria causing nosocomial infections: a perilous journey toward \u2018molecularly targeted\u2019 therapy","volume":"16","author":"El Chakhtoura","year":"2018","journal-title":"Expert. Rev. Anti Infect. Ther."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1186\/s12985-023-02034-x","article-title":"Morphological, biological, and genomic characterization of Klebsiella pneumoniae phage vB_Kpn_ZC2","volume":"20","author":"Fayez","year":"2023","journal-title":"Virol. J."},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.3390\/ijms222312827","article-title":"The MTT assay: utility, limitations, pitfalls, and interpretation in bulk and single-cell analysis","volume":"22","author":"Ghasemi","year":"2021","journal-title":"IJMS"},{"key":"B19","doi-asserted-by":"publisher","first-page":"W484","DOI":"10.1093\/nar\/gkad326","article-title":"Proksee: in-depth characterization and visualization of bacterial genomes","volume":"51","author":"Grant","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1016\/j.heliyon.2024.e34849","article-title":"Mini review advantages and limitations of lytic phages compared with chemical antibiotics to combat bacterial infections","volume":"10","author":"Guo","year":"2024","journal-title":"Heliyon"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00203-015-1148-6","article-title":"Biofilm, pathogenesis and prevention\u2014a journey to break the wall: a review","volume":"198","author":"Gupta","year":"2015","journal-title":"Arch. Microbiol."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1016\/j.virusres.2021.198465","article-title":"Biochemical and genomic characterization of a novel bacteriophage BUCT555 lysing Stenotrophomonas maltophilia","volume":"301","author":"Han","year":"2021","journal-title":"Virus Res."},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.906961","article-title":"Characterization of the bacteriophage BUCT603 and therapeutic potential evaluation against drug-resistant stenotrophomonas maltophilia in a mouse model","volume":"13","author":"Han","year":"2022","journal-title":"Front. Microbiol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"236ed10","DOI":"10.1126\/scitranslmed.3009315","article-title":"Antimicrobial resistance: A global challenge","volume":"6","author":"Howard","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"B25","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ijantimicag.2010.10.025","article-title":"Stenotrophomonas maltophilia resistance to trimethoprim\/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron","volume":"37","author":"Hu","year":"2011","journal-title":"Int. J. Antimicrob. Agents"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1128\/jb.00398-21","article-title":"Evaluating metabolic pathways and biofilm formation in stenotrophomonas maltophilia","volume":"204","author":"Isom","year":"2021","journal-title":"J. Bacteriol"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.3390\/v15122455","article-title":"StM171, a stenotrophomonas maltophilia bacteriophage that affects sensitivity to antibiotics in host bacteria and their biofilm formation","volume":"15","author":"Jdeed","year":"2023","journal-title":"Viruses"},{"key":"B28","doi-asserted-by":"publisher","first-page":"2934","DOI":"10.1128\/jb.00892-08","article-title":"A stenotrophomonas maltophilia multilocus sequence typing scheme for inferring population structure","volume":"191","author":"Kaiser","year":"2009","journal-title":"J. Bacteriol"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1802","DOI":"10.3390\/v14081802","article-title":"Isolation and characterization of a newly discovered phage, V-YDF132, for lysing vibrio harveyi","volume":"14","author":"Kang","year":"2022","journal-title":"Viruses"},{"key":"B30","doi-asserted-by":"publisher","first-page":"D708","DOI":"10.1093\/nar\/gkx932","article-title":"Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV)","volume":"46","author":"Lefkowitz","year":"2017","journal-title":"Nucl. Acids Res."},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2024.1400700","article-title":"Characterization and genomic analysis of a lytic Stenotrophomonas maltophilia short-tailed phage A1432 revealed a new genus of the family Mesyanzhinovviridae","volume":"15","author":"Li","year":"2024","journal-title":"Front. Microbiol."},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1128\/spectrum.04030-22","article-title":"Efficacy in Galleria mellonella Larvae and Application Potential Assessment of a New Bacteriophage BUCT700 Extensively Lyse Stenotrophomonas maltophilia","volume":"11","author":"Li","year":"2023","journal-title":"Microbiol. Spectr."},{"key":"B33","doi-asserted-by":"publisher","first-page":"D912","DOI":"10.1093\/nar\/gkab1107","article-title":"VFDB 2022: a general classification scheme for bacterial virulence factors","volume":"50","author":"Liu","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.02146","article-title":"Insights into cystic fibrosis polymicrobial consortia: the role of species interactions in biofilm development, phenotype, and response to in-use antibiotics","volume":"7","author":"Magalh\u00e3es","year":"2017","journal-title":"Front. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"329","DOI":"10.2174\/1872208316666220512121205","article-title":"Review on Stenotrophomonas maltophilia: An Emerging Multidrug- resistant Opportunistic Pathogen","volume":"16","author":"Majumdar","year":"2022","journal-title":"BIOT"},{"key":"B36","doi-asserted-by":"publisher","first-page":"76","DOI":"10.3390\/v11010076","article-title":"Half a century of research on membrane-containing bacteriophages: bringing new concepts to modern virology","volume":"11","author":"M\u00e4ntynen","year":"2019","journal-title":"Viruses"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2024.1428637","article-title":"Bacteriophage-mediated approaches for biofilm control","volume":"14","author":"Mayorga-Ramos","year":"2024","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"3396","DOI":"10.1093\/bioinformatics\/btx440","article-title":"VICTOR: genome-based phylogeny and classification of prokaryotic viruses","volume":"33","author":"Meier-Kolthoff","year":"2017","journal-title":"Bioinformatics"},{"key":"B39","doi-asserted-by":"publisher","first-page":"1268","DOI":"10.1101\/2020.07.05.188268","article-title":"VIRIDIC \u2013 a novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses","volume":"12","author":"Moraru","year":"2020","journal-title":"Viruses"},{"key":"B40","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/s10096-007-0279-3","article-title":"Antimicrobial therapy for Stenotrophomonas maltophilia infections","volume":"26","author":"Nicodemo","year":"2007","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"B41","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1101\/gr.213959.116","article-title":"metaSPAdes: a new versatile metagenomic assembler","volume":"27","author":"Nurk","year":"2017","journal-title":"Genome Res."},{"key":"B42","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1179\/2047773215y.0000000030","article-title":"Antimicrobial resistance: a global multifaceted phenomenon","volume":"109","author":"Prestinaci","year":"2015","journal-title":"Pathog. Glob. Health"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.950737","article-title":"Genomic characterization of a new phage BUCT541 against Klebsiella pneumoniae K1-ST23 and efficacy assessment in mouse and Galleria mellonella larvae","volume":"13","author":"Pu","year":"2022","journal-title":"Front. Microbiol."},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1042\/ebc20240012","article-title":"Phage diversity in one health","volume":"68","author":"Pye","year":"2024","journal-title":"Essays Biochem"},{"key":"B45","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/nrmicro3564","article-title":"A century of the phage: past, present and future","volume":"13","author":"Salmond","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"B47","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1007\/s12223-016-0471-x","article-title":"Bacteriophages and its applications: an overview","volume":"62","author":"Sharma","year":"2016","journal-title":"Folia Microbiol. (Praha)"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.3390\/ph17020155","article-title":"Antibacterial and anti-biofilm efficacy of endolysin lysAB1245 against a panel of important pathogens","volume":"17","author":"Soontarach","year":"2024","journal-title":"Pharmaceuticals"},{"key":"B49","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: molecular evolutionary genetics analysis version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1101\/2020.07.11.198606","article-title":"PhageAI - bacteriophage life cycle recognition with machine learning and natural language processing","author":"Tynecki","year":"2020","journal-title":"bioRxiv."},{"key":"B51","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1038\/s41579-024-01035-z","article-title":"The wound microbiota: microbial mechanisms of impaired wound healing and infection","volume":"22","author":"Uberoi","year":"2024","journal-title":"Nat. Rev. Microbiol."},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.15252\/emmm.202012435","article-title":"Biological foundations of successful bacteriophage therapy","volume":"14","author":"Venturini","year":"2022","journal-title":"EMBO Mol. Med."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.3390\/v14051057","article-title":"Deconstructing the phage\u2013bacterial biofilm interaction as a basis to establish new antibiofilm strategies","volume":"14","author":"Visnapuu","year":"2022","journal-title":"Viruses"},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1186\/s12985-024-02556-y","article-title":"Characterization of phage HZY2308 against Acinetobacter baumannii and identification of phage-resistant bacteria","volume":"21","author":"Wang","year":"2024","journal-title":"Virol. J."},{"key":"B55","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1080\/1120009x.2016.1156892","article-title":"Galleria mellonella as a model system to assess the efficacy of antimicrobial agents against Klebsiella pneumoniae infection","volume":"29","author":"Wei","year":"2016","journal-title":"J. Chemother."},{"key":"B56","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.3390\/v14081709","article-title":"Isolation and characterization of the lytic pseudoxanthomonas kaohsiungensi phage PW916","volume":"14","author":"Wen","year":"2022","journal-title":"Viruses"},{"key":"B57","doi-asserted-by":"publisher","DOI":"10.3390\/v14020264","article-title":"Characterization of the Novel Phage vB_VpaP_FE11 and Its Potential Role in Controlling Vibrio parahaemolyticus Biofilms","volume":"14","author":"Yang","year":"2022","journal-title":"Viruses"},{"key":"B58","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1007\/s12275-014-4087-z","article-title":"Phage lysis: Three steps, three choices, one outcome","volume":"52","author":"Young","year":"2014","journal-title":"J. Microbiol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"137","DOI":"10.3760\/cma.j.cn501120-20211130-00400","article-title":"Analysis of genomic information and biological characteristics of a bacteriophage against methicillin-resistant","volume":"38","author":"Zhang","year":"2022","journal-title":"Zhonghua shao shang za zhi = Zhonghua shaoshang zazhi = Chin. J. burns"}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1610857\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,10]],"date-time":"2025-07-10T05:31:24Z","timestamp":1752125484000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1610857\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,10]]},"references-count":59,"alternative-id":["10.3389\/fcimb.2025.1610857"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2025.1610857","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,10]]},"article-number":"1610857"}}