Biofilm最新文献

{"title":"Cystic fibrosis and the clinical biofilm revolution A survey of the Danish CF Center's contribution","authors":"Niels Høiby","doi":"10.1016/j.bioflm.2024.100246","DOIUrl":"10.1016/j.bioflm.2024.100246","url":null,"abstract":"<div><h3>Background</h3><div>Biofilm infections are chronic infections which are difficult to diagnose. Biofilm infections are tolerant to antibiotics and the defense mechanisms of the host. Patients with the genetic disease cystic fibrosis (CF) produce viscid mucus in the respiratory tract and therefore suffer from chronic biofilm infections in their lungs and paranasal sinuses.</div><div>The most important microorganism is the mucoid phenotype of <em>Pseudomonas aeruginosa</em> which causes chronic biofilm infections in the lungs of CF patients and untreated patients succumb as children if they contact this biofilm infection.</div><div>Since CF patients are treated in CF Centers all over the world, it is possible to do longitudinal studies on epidemiology, pathophysiology, diagnosis, prevention and treatment of <em>P. aeruginosa</em> biofilm infection which is not possible if such patients are not followed in specialized centers.</div><div>This survey describes the research through several decades in the Danish CF Center in Copenhagen which have changed the epidemiology, treatment, prophylaxis and prognosis of CF patients worldwide. Based on these results ESCMID Guidelines for diagnosis and treatment of biofilm infections were published which have influenced biofilm research and treatment in other areas.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100246"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11732244/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142985525","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Protecting bacteriophages under UV irradiation with brilliant blue FCF for targeted bacterial control","authors":"Mateusz Wdowiak ,&nbsp;Aneta Magiera ,&nbsp;Magdalena Tomczyńska ,&nbsp;Witold Adamkiewicz ,&nbsp;Francesco Stellacci ,&nbsp;Jan Paczesny","doi":"10.1016/j.bioflm.2025.100286","DOIUrl":"10.1016/j.bioflm.2025.100286","url":null,"abstract":"<div><div>Compared to the standard methods for treating bacterial diseases, bacteriophages are eco-friendly and chemical-free. Exposure to ultraviolet (UV) light or sunlight hampers the efficacy of phage-based approaches. This is crucial when phages are <em>i)</em> exposed to sunlight (e.g., in agriculture) or <em>ii</em>) are to be used simultaneously with UV for sterilization. Here, we develop a method utilizing a food dye, brilliant blue FCF (BB), that selectively stabilizes bacteriophages against exposure to UV irradiation. In the absence of BB, all tested phages and bacteria are completely inactivated by UV exposure. However, with the addition of BB, all tested non-enveloped phages are effectively protected, while gram-negative bacteria remain vulnerable to UV inactivation. The mechanism of protection requires selective binding of BB to the virion. The simultaneous action of BB-stabilized bacteriophages and UV allows for the removal of up to 99.99 % of bacteria within only 30–60 min. We demonstrate the method's applicability in combating biofouling of membranes and food sterilization. We envision using the developed approach against biofouling in industrial processes, agriculture, and the food industry.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100286"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143948733","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Key bacterial vaginosis-associated bacteria influence each other's growth in biofilms in rich media and media simulating vaginal tract secretions","authors":"Lúcia G.V. Sousa ,&nbsp;Christina A. Muzny ,&nbsp;Nuno Cerca","doi":"10.1016/j.bioflm.2024.100247","DOIUrl":"10.1016/j.bioflm.2024.100247","url":null,"abstract":"<div><div>Bacterial vaginosis (BV) is a very common gynaecologic condition affecting women of reproductive age worldwide. BV is characterized by a depletion of lactic acid-producing <em>Lactobacillus</em> species and an increase in strict and facultative anaerobic bacteria that develop a polymicrobial biofilm on the vaginal epithelium. Despite multiple decades of research, the etiology of this infection is still not clear. However, some BV-associated bacteria (BVAB) may play a key role in the development of this infection, namely <em>Gardnerella</em> species, <em>Prevotella bivia</em>, and <em>Fannyhessea vaginae</em>. In this work, we aimed to characterize the growth of these three species in a rich medium and in a medium simulating vaginal tract secretions (mGTS). We first assessed planktonic growth in New York City (NYCIII) medium and mGTS and observed that the three species showed distinct capacities to grow in the two media. Surprisingly, despite the ability of all three species to grow in single-species in NYCIII, in a triple-species consortium <em>P. bivia</em> was not able to increase its concentration after 48 h, as assessed by qPCR. Furthermore, when using the more restrictive mGTS media, <em>G. vaginalis</em> was the only BVAB able to grow in the triple-species consortia. Interestingly, we found that <em>P. bivia</em> growth in NYCIII was influenced by the cell-free supernatant (CFS) of <em>F. vaginae</em> and by the CFS of <em>G. vaginalis</em> in mGTS. This antimicrobial activity appears to happen due to the acidification of the media. Single- and triple-species biofilms were then formed, and the growth of each species was further quantified by qPCR. While <em>G. vaginalis</em> had a high capacity to form biofilms in both media, <em>F. vaginae</em> and <em>P. bivia</em> biofilm growth was favored when cultured in rich media. Differences were also found in the structure of triple-species biofilms formed in both media, as assessed by confocal laser scanning microscopy. In conclusion, while all three species were able to grow in single-species biofilms in rich media, in mGTS the growth of <em>G. vaginalis</em> was essential for incorporation of the other species in the biofilm.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100247"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11773214/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143061677","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Multipronged impact of environmental temperature on Staphylococcus aureus infection by phage Kayvirus rodi: Implications for biofilm control","authors":"Lucía Fernández ,&nbsp;Ana Catarina Duarte ,&nbsp;Andrea Jurado ,&nbsp;Laura Bueres ,&nbsp;Ana Rodríguez ,&nbsp;Pilar García","doi":"10.1016/j.bioflm.2024.100248","DOIUrl":"10.1016/j.bioflm.2024.100248","url":null,"abstract":"<div><div>Environmental cues sometimes have a direct impact on phage particle stability, as well as bacterial physiology and metabolism, having a profound effect on phage infection outcome. Here, we explore the impact of temperature on the interplay between phage <em>Kayvirus rodi</em> (phiIPLA-RODI) and its host, <em>Staphylococcus aureus</em>. Our results show that phiIPLA-RODI is a more effective predator at room (25 °C) compared to body temperature (37 °C) against planktonic cultures of several strains with varying degrees of phage susceptibility. This result differs from most known examples of temperature-dependent phage infection, in which optimum infection is correlated with the host growth rate. Further characterization of this phenomenon was carried out with strains IPLA15 and IPLA16, whose respective MICs were 7 log units and a 1-log unit higher at 37 °C than at 25 °C. Our results demonstrated that the phage also had a greater impact at room temperature during biofilm development and for the treatment of preformed biofilms. There was no difference in phage adsorption between the two temperatures for strain IPLA16. Conversely, adsorption of phiIPLA-RODI to IPLA15 was reduced at 37 °C compared to 25 °C. Moreover, confocal microscopy analysis indicated that the biofilm matrix of both strains has a greater content of PIA/PNAG at 37 °C than at 25 °C. Regarding infection parameters, we observed longer duration of the lytic cycle at 25 °C for both strains, and infection of IPLA15 by phiIPLA-RODI resulted in a smaller burst size at 37 °C than at 25 °C. Finally, we also found that the rate of phage resistant mutant selection was higher at 37 °C for both strains. Altogether, this information highlights the impact that bacterial responses to environmental factors have on phage-host interactions. Moreover, phage phiIPLA-RODI appears to be a highly effective candidate for biofilm disinfection at room temperature, while its efficacy in biofilm-related infections will require combination with other antimicrobials.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100248"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11751508/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143025710","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Immune-based strategies for the treatment of biofilm infections","authors":"Zachary Van Roy,&nbsp;Tammy Kielian","doi":"10.1016/j.bioflm.2025.100264","DOIUrl":"10.1016/j.bioflm.2025.100264","url":null,"abstract":"<div><div>Biofilms are bacterial communities surrounded by a polymeric matrix that can form on implanted materials and biotic surfaces, resulting in chronic infection that is recalcitrant to immune- and antibiotic-mediated clearance. Therefore, biofilm infections present a substantial clinical challenge, as treatment often involves additional surgical interventions to remove the biofilm nidus, prolonged antimicrobial therapy to clear residual bacteria, and considerable risk of treatment failure or infection recurrence. These factors, combined with progressive increases in antimicrobial resistance, highlight the need for alternative therapeutic strategies to circumvent undue morbidity, mortality, and resource strain on the healthcare system resulting from biofilm infections. One promising option is reprogramming dysfunctional immune responses elicited by biofilm. Here, we review the literature describing immune responses to biofilm infection with a focus on targets or strategies ripe for clinical translation. This represents a complex and dynamic challenge, with context-dependent host-pathogen interactions that differ across infection models, microenvironments, and individuals. Nevertheless, consistencies among these variables exist, which could facilitate the development of immune-based strategies for the future treatment of biofilm infections.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100264"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143509191","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"From adhesion to biofilms formation and resilience: Exploring the impact of silver nanoparticles-based biomaterials on Pseudomonas aeruginosa","authors":"Maya Rima ,&nbsp;Christina Villeneuve-Faure ,&nbsp;Ludovic Pilloux ,&nbsp;Christine Roques ,&nbsp;Fatima El Garah ,&nbsp;Kremena Makasheva","doi":"10.1016/j.bioflm.2025.100267","DOIUrl":"10.1016/j.bioflm.2025.100267","url":null,"abstract":"<div><div>Colonization of medical devices by microorganisms, often progressing to the formation of resilient biofilms, presents a common clinical issue. To address this challenge, there is growing interest in developing novel biomaterials with antimicrobial/antibiofilm properties as a promising preventive measure. This study explores nanocomposite biomaterials based on silver nanoparticles (AgNPs) deposited on thin silica (SiO₂) layers for their potential effect on the adhesion, detachment, viability and biofilm formation of the opportunistic <em>Pseudomonas aeruginosa</em>. The AgNPs-based biointerface effect on biofilm development is investigated on the PAO1-Tn<em>7</em>-<em>gfp</em> strain by combining experiments under static and dynamic conditions. For the latter, a shear-stress flow chamber is used to mimic conditions encountered around certain medical devices. The findings reveal a rapid bactericidal effect of the AgNPs, noticeable within 30 min of exposure. Moreover, a delay in surface colonization is observed with a thin and unstructured biofilm, even after 72h of dynamic culture. A considerable fragility and sensitivity to hydrodynamic stresses is noticed for this loosely attached bacterial monolayer when compared with the thick and resilient biofilm formed on SiO₂ surface. This study underlines the potential of AgNPs-based biomaterials in the conception of novel antimicrobial/antibiofilm surfaces with controlled release of the biocidal agent.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100267"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143577741","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"A guide to publishing in Biofilm: how to avoid a desk rejection","authors":"Tom Coenye ,&nbsp;Darla M. Goeres ,&nbsp;Birthe Veno Kjellerup ,&nbsp;Ákos T. Kovács","doi":"10.1016/j.bioflm.2025.100282","DOIUrl":"10.1016/j.bioflm.2025.100282","url":null,"abstract":"","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100282"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144279998","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Aqueous extracts of Moringa oleifera and Cinnamomum cassia as promising sources of antibiofilm compounds against mucoid and small colony variants of Pseudomonas aeruginosa and Staphylococcus aureus","authors":"Eduarda Silva ,&nbsp;Pedro Ferreira-Santos ,&nbsp;José A. Teixeira ,&nbsp;Maria Olivia Pereira ,&nbsp;Cristina M.R. Rocha ,&nbsp;Ana Margarida Sousa","doi":"10.1016/j.bioflm.2024.100250","DOIUrl":"10.1016/j.bioflm.2024.100250","url":null,"abstract":"<div><div>Bacterial biofilms formed by <em>Staphylococcus aureus</em> and <em>Pseudomonas aeruginosa</em> pose significant challenges in treating cystic fibrosis (CF) airway infections due to their resistance to antibiotics. New therapeutic approaches are urgently needed to treat these chronic infections. This study aimed to investigate the antibiofilm potential of various plant extracts, specifically targeting mucoid and small colony variants of <em>P. aeruginosa</em> and <em>S. aureus</em> and strains. Moreover, it aimed to gain insights into the mechanisms of action and the potential phytochemicals responsible for antibiofilm activity. Solid-liquid extractions were performed on seven biomasses using water and ethanol (70 and 96 %) under controlled conditions, resulting in 21 distinct plant extracts. These extracts were evaluated for extraction yield, antioxidant activity, phenolic content, chemical composition by HPLC-TOF-MS, and antibiofilm activity using a 96-well plate assay, followed by crystal violet staining, bacterial adhesion assessment, and brightfield microscopy. Our findings revealed that aqueous extracts exhibited the highest inhibition of biofilm formation, with cinnamon bark and moringa seeds showing strong antibiofilm activity against both bacterial species. Brightfield microscopy confirmed that these extracts effectively inhibited biofilm formation. Chemical analysis identified key bioactive compounds, including moringin, benzaldehyde, coumarin, and quinic acid, which likely contribute to the observed antibiofilm effects. Recognizing that the antibiofilm properties of moringin, a common compound in both moringa seed and cinnamon bark extracts, remain underexplored, we conducted potential target identification via PharmMapper and molecular docking analyses to provide a foundation for future research. Computational analyses indicated that moringin might inhibit aspartate-semialdehyde dehydrogenase in <em>P. aeruginosa</em> and potentially interact with an unknown target in <em>S. aureus</em>. In conclusion, moringa seed and cinnamon bark extracts demonstrated significant potential for developing new therapies targeting biofilm-associated infections in CF. Further studies are needed to validate the computational predictions, identify the bacterial targets, and elucidate the precise mechanisms behind moringin's antibiofilm activity, which is likely the potential key contributor to the observed activity of the moringa and cinnamon bark extracts.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100250"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11772965/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143061676","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Machine learning assisted classification of staphylococcal biofilm maturity","authors":"S.C.J. van Dun ,&nbsp;R. Knol ,&nbsp;A.S. Silva-Herdade ,&nbsp;A.S. Veiga ,&nbsp;M.A.R.B. Castanho ,&nbsp;P.H. Nibbering ,&nbsp;B.G.C.W. Pijls ,&nbsp;A.M. van der Does ,&nbsp;J. Dijkstra ,&nbsp;M.G.J. de Boer","doi":"10.1016/j.bioflm.2025.100283","DOIUrl":"10.1016/j.bioflm.2025.100283","url":null,"abstract":"<div><div>An increasing incidence of device-related, biofilm-associated infections has been observed in clinical practice worldwide. <em>In vitro</em> biofilm models are essential to study these burdensome infections and to design and test potential new treatment approaches. However, there is considerable variation in <em>in vitro</em> biofilm models, and a generally accepted systematic description of biofilm maturity – apart from incubation time – is lacking.</div><div>Therefore, we proposed a scheme comprised of 6 different classes based on common topographic characteristics, <em>i.e.</em>, the substrate, bacterial cells and extracellular matrix, identified by atomic force microscopy (AFM), to describe biofilm maturity independent of incubation time. Evaluation of a test set of staphylococcal biofilm images by a group of independent researchers showed that human observers were capable of classifying images with a mean accuracy of 0.77 ± 0.18. However, manual evaluation of AFM biofilm images is time-consuming, and subject to observer bias. To circumvent these disadvantages, a machine learning algorithm was designed and developed to aid in classification of biofilm images.</div><div>The designed algorithm was capable of identifying pre-set characteristics of biofilms and able to discriminate between the six different classes in the proposed framework. Compared to the established ground truth, the mean accuracy of the developed algorithm amounted to 0.66 ± 0.06 with comparable recall, and off-by-one accuracy of 0.91 ± 0.05. This algorithm, which classifies AFM images of biofilms, has been made available as an open access desktop tool.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100283"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143907642","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Investigations into the growth and formation of biofilm by Leptospira biflexa at temperatures encountered during infection","authors":"Priscyla dos Santos Ribeiro ,&nbsp;Judith Stasko ,&nbsp;Adrienne Shircliff ,&nbsp;Luis Guilherme Fernandes ,&nbsp;Ellie J. Putz ,&nbsp;Claire Andreasen ,&nbsp;Vasco Azevedo ,&nbsp;Paula Ristow ,&nbsp;Jarlath E. Nally","doi":"10.1016/j.bioflm.2024.100243","DOIUrl":"10.1016/j.bioflm.2024.100243","url":null,"abstract":"<div><div>The genus <em>Leptospira</em> comprises unique atypical spirochete bacteria that includes the etiological agent of leptospirosis, a globally important zoonosis. Biofilms are microecosystems composed of microorganisms embedded in a self-produced matrix that offers protection against hostile factors. Leptospires form biofilms <em>in vitro, in situ</em> in rice fields and unsanitary urban areas, and <em>in vivo</em> while colonizing rodent kidneys. The complex three-dimensional biofilm matrix includes secreted polymeric substances such as proteins, extracellular DNA (eDNA), and saccharides. The genus <em>Leptospira</em> comprises pathogenic and saprophytic species with the saprophytic <em>L. biflexa</em> being commonly used as a model organism for the genus. In this study, the growth and formation of biofilms by <em>L. biflexa</em> was investigated not just at 29 °C, but at 37 °C/5 % CO₂, a temperature similar to that encountered during host infection. Planktonic free-living <em>L. biflexa</em> grow in HAN media at both 29 °C and 37 °C/5 % CO_2, but cells grown at 37 °C/5 % CO₂ are longer (18.52 μm ± 3.39) compared to those at 29 °C (13.93 μm ± 2.84). Biofilms formed at 37 °C/5 % CO₂ had more biomass compared to 29 °C, as determined by crystal violet staining. Confocal microscopy determined that the protein content within the biofilm matrix was more prominent than double-stranded DNA, and featured a distinct layer attached to the solid substrate. Additionally, the model enabled effective protein extraction for proteomic comparison across different biofilm phenotypes. Results highlight an important role for proteins in biofilm matrix structure by leptospires and the identification of their specific protein components holds promise for strategies to mitigate biofilm formation.</div></div>","PeriodicalId":55844,"journal":{"name":"Biofilm","volume":"9 ","pages":"Article 100243"},"PeriodicalIF":5.9,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11697785/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142933665","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}