Environmental Epigenetics最新文献

{"title":"EV-miRNA associated with environmental air pollution exposures in the MADRES cohort.","authors":"Helen Bermudez Foley, Sandrah P Eckel, Tingyu Yang, Mario Vigil, Xinci Chen, Carmen Marsit, Shohreh F Farzan, Theresa M Bastain, Rima Habre, Carrie V Breton","doi":"10.1093/eep/dvae019","DOIUrl":"https://doi.org/10.1093/eep/dvae019","url":null,"abstract":"<p><p>Air pollution is a hazardous contaminant, exposure to which has substantial consequences for health during critical periods, such as pregnancy. MicroRNA (miRNA) is an epigenetic mechanism that modulates transcriptome responses to the environment and has been found to change in reaction to air pollution exposure. The data are limited regarding extracellular-vesicle (EV) miRNA variation associated with air pollution exposure during pregnancy and in susceptible populations who may be disproportionately exposed. This study aimed to identify EV-miRNA expression associated with ambient, residential exposure to PM_2.5, PM₁₀, NO₂, O₃ and with traffic-related NO_x in 461 participants of the MADRES cohort, a low income, predominantly Hispanic pregnancy cohort based in Los Angeles, CA. This study used residence-based modeled air pollution data as well as Nanostring panels for EVmiRNA extracted with Qiagen exoRNeasy kits to evaluate 483 miRNA in plasma in early and late pregnancy. Average air pollution exposures were considered separately for 1-day, 1-week, and 8-week windows before blood collection in both early and late pregnancy. This study identified 63 and 66 EV-miRNA significantly associated with PM_2.5 and PM₁₀, respectively, and 2 miRNA associated with traffic-related NO_X (False Discovery Rate-adjusted <i>P</i>-value < .05). Of 103 unique EV-miRNA associated with PM, 92% were associated with lung conditions according to HMDD (Human miRNA Disease Database) evidence. In particular, EV-miRNA previously identified with air pollution exposure also associated with PM_2.5 and PM₁₀ in this study were: miR-126, miR-16-5p, miR-187-3p, miR200b-3p, miR486-3p, and miR-582-3p. There were no significant differences in average exposures in early vs late pregnancy. Significant EV-miRNAs were only identified in late pregnancy with an 8-week exposure window, suggesting a vulnerable timeframe of exposure, rather than an acute response. These results describe a wide array of EV-miRNA for which expression is affected by PM exposure and may be in part mediating the biological response to ambient air pollution, with potential for health implications in pregnant women and their children.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae019"},"PeriodicalIF":4.8,"publicationDate":"2024-10-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11552520/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142617194","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":"Correction to: To live or let die? Epigenetic adaptations to climate change-a review.","authors":"","doi":"10.1093/eep/dvae016","DOIUrl":"https://doi.org/10.1093/eep/dvae016","url":null,"abstract":"<p><p>[This corrects the article DOI: 10.1093/eep/dvae009.].</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae016"},"PeriodicalIF":4.8,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11444065/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142361287","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":"DNA methylation correlates with transcriptional noise in response to elevated pCO₂ in the eastern oyster (<i>Crassostrea virginica</i>).","authors":"Yaamini R Venkataraman, Ariana S Huffmyer, Samuel J White, Alan Downey-Wall, Jill Ashey, Danielle M Becker, Zachary Bengtsson, Hollie M Putnam, Emma Strand, Javier A Rodríguez-Casariego, Shelly A Wanamaker, Katie E Lotterhos, Steven B Roberts","doi":"10.1093/eep/dvae018","DOIUrl":"https://doi.org/10.1093/eep/dvae018","url":null,"abstract":"<p><p>Ocean acidification significantly affects marine calcifiers like oysters, warranting the study of molecular mechanisms like DNA methylation that contribute to adaptive plasticity in response to environmental change. However, a consensus has not been reached on the extent to which methylation modules gene expression, and in turn plasticity, in marine invertebrates. In this study, we investigated the impact of pCO₂ on gene expression and DNA methylation in the eastern oyster, <i>Crassostrea virginica</i>. After a 30-day exposure to control (572 ppm) or elevated pCO₂ (2827 ppm), whole-genome bisulfite sequencing (WGBS) and RNA-seq data were generated from adult female gonad tissue and male sperm samples. Although differentially methylated loci (DMLs) were identified in females (89) and males (2916), there were no differentially expressed genes and only one differentially expressed transcript in females. However, gene body methylation impacted other forms of gene activity in sperm, such as the maximum number of transcripts expressed per gene and changes in the predominant transcript expressed. Elevated pCO₂ exposure increased gene expression variability (transcriptional noise) in males but decreased noise in females, suggesting a sex-specific role of methylation in gene expression regulation. Functional annotation of genes with changes in transcript-level expression or containing DMLs revealed several enriched biological processes potentially involved in elevated pCO₂ response, including apoptotic pathways and signal transduction, as well as reproductive functions. Taken together, these results suggest that DNA methylation may regulate gene expression variability to maintain homeostasis in elevated pCO₂ conditions and could play a key role in environmental resilience in marine invertebrates.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae018"},"PeriodicalIF":4.8,"publicationDate":"2024-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11556341/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142617187","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":"Bronchial cell epigenetic aging in a human experimental study of short-term diesel and ozone exposures.","authors":"Jamaji C Nwanaji-Enwerem, Anne K Bozack, Cavin Ward-Caviness, David Diaz-Sanchez, Robert B Devlin, Marie-Abèle C Bind, Andres Cardenas","doi":"10.1093/eep/dvae017","DOIUrl":"https://doi.org/10.1093/eep/dvae017","url":null,"abstract":"<p><p>Blood-based, observational, and cross-sectional epidemiological studies suggest that air pollutant exposures alter biological aging. In a single-blinded randomized crossover human experiment of 17 volunteers, we examined the effect of randomized 2-h controlled air pollution exposures on respiratory tissue epigenetic aging. Bronchial epithelial cell DNA methylation 24 h post-exposure was measured using the HumanMethylation450K BeadChip, and there was a minimum 2-week washout period between exposures. All 17 volunteers were exposed to ozone, but only 13 were exposed to diesel exhaust. Horvath DNAmAge [Pearson coefficient (r) = 0.64; median absolute error (MAE) = 2.7 years], GrimAge (r = 0.81; MAE = 13 years), and DNAm Telomere Length (DNAmTL) (r = -0.65) were strongly correlated with chronological age in this tissue. Compared to clean air, ozone exposure was associated with longer DNAmTL (median difference 0.11 kb, Fisher's exact <i>P</i>-value = .036). This randomized trial suggests a weak relationship of ozone exposure with DNAmTL in target respiratory cells. Still, causal relationships with long-term exposures need to be evaluated.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae017"},"PeriodicalIF":4.8,"publicationDate":"2024-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11482248/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142485604","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":"Prenatal exposure to maternal smoking and adult lung cancer risk: a nested case-control study using peripheral blood leukocyte DNA methylation prediction of exposure.","authors":"Meng Ru, Dominique S Michaud, Naisi Zhao, Karl T Kelsey, Devin C Koestler, Jiayun Lu, Elizabeth A Platz, Christine M Ladd-Acosta","doi":"10.1093/eep/dvae015","DOIUrl":"10.1093/eep/dvae015","url":null,"abstract":"<p><p>A prior study reported no association between prenatal smoking methylation scores and adult lung cancer risk adjusting for methylation-predicted adult smoking, without considering maternal smoking trends by birth cohort. To address this gap, we examined the association between prenatal smoking methylation scores and adult lung cancer, independent of methylation-predicted adult packyears and by birth cohort, in a study nested in CLUE II. Included were 208 incident lung cancer cases ascertained by cancer registry linkage and 208 controls matched on age, sex, and smoking. DNA methylation was measured in prediagnostic blood. We calculated two prenatal smoking scores, using 19 (Score-19) and 15 (Score-15) previously identified CpGs and a methylation-predicted adult packyears score. Conditional logistic regression was used to estimate odds ratios (ORs) and 95% confidence intervals (CIs) adjusting for adult packyears score and batch effects. Score-15 was positively associated with lung cancer (per standard deviation, OR = 1.40, 95% CI = 1.10-1.79, <i>P</i>-trend = .006), especially in the 1930-1938 birth cohort (OR = 3.43, 95% CI = 1.55-7.60, <i>P</i>-trend = .002). Score-19 was associated only in the 1930-1938 birth cohort (OR = 2.12, 95% CI = 1.15-3.91). Participants with both prenatal scores below the median (vs all other combinations) had lower risk (OR = 0.44, 95% CI = 0.27-0.72), especially in the 1930-1938 birth cohort (OR = 0.16, 95% CI = 0.04-0.62). Among ever smokers, participants with higher prenatal smoking scores had higher risk, irrespective of adult packyears (low: OR = 2.81, 95% CI = 1.38-5.72, high: OR = 2.67, 95% CI = 1.03-6.95). This prospective study suggests a positive association between prenatal smoking exposure and adult lung cancer risk, especially in the 1930-1938 birth cohort, independent of active smoking. Future studies with multiple birth cohorts are needed.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae015"},"PeriodicalIF":4.8,"publicationDate":"2024-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11562842/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142617209","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":"Epigenetic transgenerational inheritance of toxicant exposure-specific non-coding RNA in sperm.","authors":"Hayden McSwiggin, Rubens Magalhães, Eric E Nilsson, Wei Yan, Michael K Skinner","doi":"10.1093/eep/dvae014","DOIUrl":"10.1093/eep/dvae014","url":null,"abstract":"<p><p>Environmentally induced epigenetic transgenerational inheritance of phenotypic variation and disease susceptibility requires the germ cell (sperm or egg) transmission of integrated epigenetic mechanisms involving DNA methylation, histone modifications, and non-coding RNA (ncRNA) actions. Previous studies have demonstrated that transgenerational exposure and disease-specific differential DNA methylation regions (DMRs) in sperm are observed and that ncRNA-mediated DNA methylation occurs. The current study was designed to determine if transgenerational exposure-specific ncRNAs exist in sperm. Specifically, toxicants with distinct mechanisms of action including the fungicide vinclozolin (anti-androgenic), pesticide dichlorodiphenyltrichloroethane (estrogenic), herbicide atrazine (endocrine disruptor at cyclic adenosine monophosphate level), and hydrocarbon mixture jet fuel (JP8) (aryl hydrocarbon receptor disruptor) were used to promote transgenerational disease phenotypes in F3 generation outbred rats. New aliquots of sperm, previously collected and used for DNA methylation analyses, were used in the current study for ncRNA sequencing analyses of nuclear RNA. Significant changes in transgenerational sperm ncRNA were observed for each transgenerational exposure lineage. The majority of ncRNA was small noncoding RNAs including piwi-interacting RNA, tRNA-derived small RNAs, microRNAs, rRNA-derived small RNA, as well as long ncRNAs. Although there was some overlap among the different classes of ncRNA across the different exposures, the majority of differentially expressed ncRNAs were exposure-specific with no overlapping ncRNA between the four different exposure lineages in the transgenerational F3 generation sperm nuclear ncRNAs. The ncRNA chromosomal locations and gene associations were identified for a small number of differential expressed ncRNA. Interestingly, an overlap analysis between the transgenerational sperm DMRs and ncRNA chromosomal locations demonstrated small populations of overlapping ncRNA, but a large population of non-overlapping ncRNAs. Observations suggest that transgenerational sperm ncRNAs have both exposure-specific populations within the different classes of ncRNA, as well as some common populations of ncRNAs among the different exposures. The lack of co-localization of many of the ncRNAs with previously identified transgenerational DMRs suggests a distal integration of the different epigenetic mechanisms. The potential use of ncRNA analyses for transgenerational toxicant exposure assessment appears feasible.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae014"},"PeriodicalIF":4.8,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11529619/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142567124","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":"Environmental conditions elicit a slow but enduring response of histone post-translational modifications in Mozambique tilapia.","authors":"Elizabeth A Mojica, Kathleen A Petcu, Dietmar Kültz","doi":"10.1093/eep/dvae013","DOIUrl":"10.1093/eep/dvae013","url":null,"abstract":"<p><p>This study sheds new light on the timescale through which histone post-translational modifications (PTMs) respond to environmental stimuli, demonstrating that the histone PTM response does not necessarily precede the proteomic response or acclimation. After a variety of salinity treatments were administered to Mozambique tilapia (<i>Oreochromis mossambicus</i>) throughout their lifetimes, we quantified 343 histone PTMs in the gills of each fish. We show here that histone PTMs differ dramatically between fish exposed to distinct environmental conditions for 18 months, and that the majority of these histone PTM alterations persist for at least 4 weeks, irrespective of further salinity changes. However, histone PTMs respond minimally to 4-week-long periods of salinity acclimation during adulthood. The results of this study altogether signify that patterns of histone PTMs in individuals reflect their prolonged exposure to environmental conditions.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae013"},"PeriodicalIF":4.8,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11452309/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142380314","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":"Impaired energy expenditure following exposure to either DDT or DDE in mice may be mediated by DNA methylation changes in brown adipose.","authors":"Juliann A Jugan, Kyle B Jackson, Sarah E Elmore, Michele A La Merrill","doi":"10.1093/eep/dvae011","DOIUrl":"https://doi.org/10.1093/eep/dvae011","url":null,"abstract":"<p><p>The insecticide dichlorodiphenyltrichloroethane (DDT) and its persistent metabolite, dichlorodiphenyldichloroethylene (DDE), have been associated with increased adiposity and obesity in multiple generations of rodents and humans. These lipophilic pollutants accumulate in adipose tissue and appear to decrease energy expenditure through the impairment of thermogenesis in brown adipose tissue (BAT). We hypothesized that impaired thermogenesis is due to persistent epigenetic modifications of BAT. To address this, we exposed C57BL/6 J mice to DDT or DDE from gestational day (GD) 11.5 to postnatal day (PND) 5, evaluated longitudinal body temperature, and performed reduced representation bisulfite sequencing and RNA sequencing of BAT from infant and adult offspring. Exposure to DDT or DDE reduced core body temperature in adult mice, and differential methylation at the pathway and gene level was persistent from infancy to adulthood. Furthermore, thermogenesis and biological pathways essential for thermogenic function, such as oxidative phosphorylation and mechanistic target of rapamycin kinase (mTOR) signaling, were enriched with differential methylation and RNA transcription in adult mice exposed to DDT or DDE. PAZ6 human brown preadipocytes were differentiated in the presence of DDT or DDE to understand the brown adipocyte-autonomous effect of these pollutants. <i>In vitro</i> exposure led to limited changes in RNA expression; however, mitochondrial membrane potential was decreased <i>in vitro</i> with 0.1 µM and 1 µM doses of DDT or DDE. These results demonstrate that concentrations of DDT and DDE relevant to human exposure have a significant effect on thermogenesis, the transcriptome, and DNA methylome of mouse BAT and the mitochondrial function of human brown adipocytes.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae011"},"PeriodicalIF":4.8,"publicationDate":"2024-08-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472829/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142460873","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":"To live or let die? Epigenetic adaptations to climate change-a review.","authors":"Jonas Zetzsche, Manon Fallet","doi":"10.1093/eep/dvae009","DOIUrl":"10.1093/eep/dvae009","url":null,"abstract":"<p><p>Anthropogenic activities are responsible for a wide array of environmental disturbances that threaten biodiversity. Climate change, encompassing temperature increases, ocean acidification, increased salinity, droughts, and floods caused by frequent extreme weather events, represents one of the most significant environmental alterations. These drastic challenges pose ecological constraints, with over a million species expected to disappear in the coming years. Therefore, organisms must adapt or face potential extinctions. Adaptations can occur not only through genetic changes but also through non-genetic mechanisms, which often confer faster acclimatization and wider variability ranges than their genetic counterparts. Among these non-genetic mechanisms are epigenetics defined as the study of molecules and mechanisms that can perpetuate alternative gene activity states in the context of the same DNA sequence. Epigenetics has received increased attention in the past decades, as epigenetic mechanisms are sensitive to a wide array of environmental cues, and epimutations spread faster through populations than genetic mutations. Epimutations can be neutral, deleterious, or adaptative and can be transmitted to subsequent generations, making them crucial factors in both long- and short-term responses to environmental fluctuations, such as climate change. In this review, we compile existing evidence of epigenetic involvement in acclimatization and adaptation to climate change and discuss derived perspectives and remaining challenges in the field of environmental epigenetics. <b>Graphical Abstract</b>.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae009"},"PeriodicalIF":4.8,"publicationDate":"2024-07-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11321362/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141975419","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":"DNA methylation is associated with hair trace elements in female adolescents from two vulnerable populations in the Colombian Caribbean.","authors":"Alejandra Manjarres-Suarez, Anne Bozack, Andres Cardenas, Jesus Olivero-Verbel","doi":"10.1093/eep/dvae008","DOIUrl":"https://doi.org/10.1093/eep/dvae008","url":null,"abstract":"<p><p>Exposure to trace elements (TEs) influences DNA methylation patterns, which may be associated with disease development. Vulnerable populations, such as adolescents undergoing maturity, are susceptible to the effects of TE exposure. The aim of this study was to analyze the association of hair TE concentration with DNA methylation in a sample from female adolescents living in two communities in the Colombian Caribbean coast. Hair and blood samples were obtained from 45 females, between 13 and 16 years of age. Seventeen TEs were quantified in hair samples. DNA methylation was measured in leukocytes using the Infinium MethylationEPIC BeadChip. Linear models were employed to identify differentially methylated positions (DMPs) adjusting for age, body mass index, mother's education, and cell type composition. Among the tested elements, vanadium, chromium, nickel, copper, zinc, yttrium, tin, and barium were significantly associated with DMPs (false discovery rate < 0.05), registering 225, 1, 2, 184, 1, 209 189, and 104 hits, respectively. Most of the DMPs were positively associated with TEs and located in open sea regions. The greatest number of DMPs was annotated to the <i>HOXA3</i> and <i>FOXO3</i> genes, related to regulation of gene expression and oxidative stress, respectively. These findings suggest that DNA methylation may be involved in linking exposure to TEs among female adolescents to downstream health risks.</p>","PeriodicalId":11774,"journal":{"name":"Environmental Epigenetics","volume":"10 1","pages":"dvae008"},"PeriodicalIF":4.8,"publicationDate":"2024-06-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11548963/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142617190","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}