AnaerobePub Date : 2025-08-01Epub Date: 2025-06-25DOI: 10.1016/j.anaerobe.2025.102980
Anne Lecoutour , Victoria Mesa , Jeanne Couturier , Johanne Delannoy , Bénédicte Pigneur , Frédéric Barbut
{"title":"Phenotypic and genomic characterization of Clostridioides difficile strains involved in multiple recurrences","authors":"Anne Lecoutour , Victoria Mesa , Jeanne Couturier , Johanne Delannoy , Bénédicte Pigneur , Frédéric Barbut","doi":"10.1016/j.anaerobe.2025.102980","DOIUrl":"10.1016/j.anaerobe.2025.102980","url":null,"abstract":"<div><h3>Background</h3><div>Multiple relapses of <em>Clostridioides difficile</em> infections (CDI) are frequent, impact patients' quality of life, and are challenging to treat. These relapses are either linked to the patient's conditions (immunity, intestinal dysbiosis) or potentially to strain-specific characteristics.</div></div><div><h3>Objectives</h3><div>This study aims to determine the genomic and phenotypic characteristics of <em>C. difficile</em> (CD) strains associated with multiple relapses of CDIs (rCDI).</div></div><div><h3>Material and methods</h3><div>Between 2019 and 2022, 10 CD strains responsible for multiple (≥2) relapses were matched on PCR ribotype to 10 CD control strains isolated from patients with a single episode. Genomic (resistome, virulome, mobile genetic elements) and phenotypic (motility, sporulation, germination, biofilm production, stress resistance) characteristics of relapse and control strains were compared.</div></div><div><h3>Results</h3><div>No significant genomic or phenotypic differences were identified between strains involved in multiple relapses and control strains. Our analyses revealed significant genomic and phenotypic variability among strains.</div></div><div><h3>Conclusion</h3><div>The origin of rCDI does not seem to be directly related to the <em>C. difficile</em> strain, suggesting that these relapses are more likely associated with other factors, such as intestinal dysbiosis or the patient's immune status.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102980"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144511412","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Fulminant clostridioides (costridium) difficile infection caused by a rare strain of PCR-ribotype 153 in Japan: A case report","authors":"Daichi Yomogida , Suguru Hasegawa , Shiori Mizuta , Shinjiro Horikawa , Yoshinao Koshida , Koichiro Matsuda , Masahiko Nakamura , Hiroyasu Kaya , Akio Uchiyama , Mitsutoshi Senoh","doi":"10.1016/j.anaerobe.2024.102936","DOIUrl":"10.1016/j.anaerobe.2024.102936","url":null,"abstract":"<div><div><em>Clostridioides (Clostridium) difficile (C. difficile)</em> infection (CDI), often severe when producing toxin A, toxin B, and CDT, can cause life-threatening fulminant infections, especially in vulnerable patients. This case report discusses a 39-year-old woman with no medical history who developed severe CDI after antibiotic treatment, leading to fatal hypovolemic shock. A rare <em>C. difficile</em> PCR-ribotype 153 strain, which is positive for toxin A, toxin B, and CDT was identified. This case emphasizes the need for early CDI diagnosis, cautious antibiotic use, and prompt treatment to prevent severe outcomes like shock and multiorgan failure.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102936"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142881141","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-06-06DOI: 10.1016/j.anaerobe.2025.102978
Anastasia Karatzia , Danai Aristeridou , Wawi Kantz , A. Carmine Colavecchia , Harish Madhava , Mohammad Ateya , Carole Czudek , Patrick H. Kelly , Kate Halsby
{"title":"AI4CDI: Introducing a novel machine learning approach to demonstrate feasibility of timely and early identification of at-risk populations for Clostridioides difficile infections","authors":"Anastasia Karatzia , Danai Aristeridou , Wawi Kantz , A. Carmine Colavecchia , Harish Madhava , Mohammad Ateya , Carole Czudek , Patrick H. Kelly , Kate Halsby","doi":"10.1016/j.anaerobe.2025.102978","DOIUrl":"10.1016/j.anaerobe.2025.102978","url":null,"abstract":"<div><h3>Objective</h3><div>We evaluated machine learning (ML) model feasibility to predict <em>Clostridioides difficile</em> infection (CDI) six months prior to onset and to identify early predictors over a longer period.</div></div><div><h3>Methods</h3><div>A retrospective analysis was performed using electronic health records data from US adults (Optum Market Clarity). Cases with CDI and non-CDI controls were identified. A 1:1 coarsened exact matching algorithm was applied, with final analysis cohorts of 4736 cases and 4732 controls. CDI-relevant features were identified from the published literature, and information was extracted for >900 features. The final model was trained on 597 mostly binary features. Feature information during the 6 months prior to date of first CDI diagnosis was hidden to the model to identify patients at risk for CDI with a longer time horizon. Sensitivity analysis was conducted on cases aged 65–80 years.</div></div><div><h3>Results</h3><div>Median age was 65 years (19–88) in case and control cohorts. The Gradient Boosted Trees ML model had an Area Under the Curve Receiver Operating Characteristic (AUC-ROC) of 0.79. Post-model bias evaluation revealed disparities in sensitivity (race). Long-term predictors included hospitalization days. While some predictors were exclusive to the 65–80 years model, others were more strongly associated with CDI in the overall model.</div></div><div><h3>Conclusions</h3><div>We developed a ML model that can identify patient groups at increased risk for primary CDI. While the predictive capability of this ML model is promising, validation is needed before exploring its readiness for use in healthcare settings to inform preventive measures for CDI.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102978"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144246088","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-07-19DOI: 10.1016/j.anaerobe.2025.102986
Paige McGraw , Su-Chen Lim , Deirdre A. Collins , Thomas V. Riley
{"title":"Toxigenic, atypical strains of Clostridioides difficile isolated from soils of Western Australian public parks","authors":"Paige McGraw , Su-Chen Lim , Deirdre A. Collins , Thomas V. Riley","doi":"10.1016/j.anaerobe.2025.102986","DOIUrl":"10.1016/j.anaerobe.2025.102986","url":null,"abstract":"<div><div>Public park soils in Perth, Western Australia were investigated for <em>Clostridioides difficile. C. difficile</em> was found at a high prevalence of 73 %. Over 19 % of the <em>C. difficile</em> isolates were toxigenic, including clinically relevant <em>C. difficile</em> ribotypes 014/020 and 106. Additionally, an esculin-hydrolysis negative, A<sup>+</sup>B<sup>−</sup>CDT<sup>-</sup> isolate was recovered.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102986"},"PeriodicalIF":2.6,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144681904","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-06-16DOI: 10.1016/j.anaerobe.2025.102979
Samuel C. Eziuzor , Carsten Vogt
{"title":"Exploring benzene mineralization by anaerobes isolated from denitrifying enrichment cultures","authors":"Samuel C. Eziuzor , Carsten Vogt","doi":"10.1016/j.anaerobe.2025.102979","DOIUrl":"10.1016/j.anaerobe.2025.102979","url":null,"abstract":"<div><h3>Objectives</h3><div>The study aimed to isolate and characterize benzene-mineralizing anaerobes from a nitrate-reducing community. The goal was to evaluate their potential for benzene degradation under anoxic conditions and to compare composition and metabolic activity in media with and without ammonium.</div></div><div><h3>Methods</h3><div>Two putative isolates (Bz4 and Bz7) were obtained using classical isolation techniques under nitrate-reducing conditions with either acetate or benzene as the sole carbon and energy source. Enrichment media differed by the presence (Bz4) or absence (Bz7) of ammonium. The ability of the isolates to mineralize [<sup>13</sup>C]-labeled acetate and [<sup>13</sup>C<sub>6</sub>]-labeled benzene was assessed by monitoring <sup>13</sup>CO<sub>2</sub> production under anoxic conditions over 184 days. Nitrite production was also measured. Community composition was determined via 16S rRNA gene amplicon sequencing.</div></div><div><h3>Results</h3><div>Both Bz4 and Bz7 consortia mineralized [<sup>13</sup>C]-acetate anoxically, with mineralization rates of 3.3 μM day<sup>−1</sup> and 2.7 μM day<sup>−1</sup>, respectively. Benzene mineralization was observed only in Bz4, which degraded [<sup>13</sup>C<sub>6</sub>]-benzene at a rate of 0.298 μM day<sup>−1</sup>, resulting in <sup>13</sup>CO<sub>2</sub> production with δ<sup>13</sup>C values reaching 960.2 ± 0.3 ‰. Bz4 also produced nitrite (4.60 ± 0.004 μM), while Bz7 showed no benzene mineralization with a smaller quantity of nitrite production. Microbial community analysis revealed that Bz4 was dominated by <em>Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium</em> (51.4 %), <em>Rhizobiaceae</em> (21.0 %), <em>Pseudomonas</em> (18.2 %), and <em>Nocardioides</em> (8.9 %). In contrast, Bz7 was almost exclusively composed of <em>Simplicispira</em> (96.7 %).</div></div><div><h3>Conclusions</h3><div>The Bz4 consortium demonstrated effective anaerobic benzene mineralization under nitrate-reducing conditions, highlighting its potential for further purification and study in the context of anaerobic benzene biodegradation.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102979"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144324337","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-06-07DOI: 10.1016/j.anaerobe.2025.102977
Marek Kwaśniewski , Tomasz M. Karpiński
{"title":"Identification and characterization of anaerobic bacteria in human semen: A retrospective study","authors":"Marek Kwaśniewski , Tomasz M. Karpiński","doi":"10.1016/j.anaerobe.2025.102977","DOIUrl":"10.1016/j.anaerobe.2025.102977","url":null,"abstract":"<div><div>This study analyzed retrospectively 291 semen samples, identifying diverse anaerobic bacteria, mainly <em>Prevotella</em> (49 % of all isolates), <em>Veillonella</em>, and <em>Peptoniphilus</em>. Most isolates were susceptible to amoxicillin/clavulanic acid, suggesting its therapeutic potential in male infertility. Resistance to metronidazole was observed in <em>Peptoniphilus, Veillonella</em>, and <em>Propionimicrobium</em>, while <em>Bacteroides</em> exhibited resistance to benzylpenicillin.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102977"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144257245","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-06-26DOI: 10.1016/j.anaerobe.2025.102981
Hrisi Bahar Tokman , Muhammed Yusuf Afacan , Arin Celayir , Ece Davutluoglu , Ayse Akgonul , Ayse Ceylan Kilincarslan , Edip Tokuc , Mahmut Kursat Ozsahin , Huseyin Botanlioglu
{"title":"The first case report of an intraosseous hemangioma complicated by Prevotella bivia infection","authors":"Hrisi Bahar Tokman , Muhammed Yusuf Afacan , Arin Celayir , Ece Davutluoglu , Ayse Akgonul , Ayse Ceylan Kilincarslan , Edip Tokuc , Mahmut Kursat Ozsahin , Huseyin Botanlioglu","doi":"10.1016/j.anaerobe.2025.102981","DOIUrl":"10.1016/j.anaerobe.2025.102981","url":null,"abstract":"<div><div>Intraosseous hemangiomas are rare benign vascular tumors that occur within the bone. <em>Prevotella bivia</em> is an anaerobic, gram-negative rod that is part of the normal microbiota of the gastrointestinal and urogenital tract as well as the oral cavity, but it rarely causes bone infections. This case report presents a patient with a history of dental infection who was initially diagnosed radiologically with non-ossifying fibroma (NOF) in the knee. Histopathology and anaerobic culture identified the lesion as an intraosseous hemangioma infected with <em>P</em>.<em>bivia</em>. The patient was treated with amoxicillin-clavulanic acid and metronidazole. This case report underscores the importance of considering rare pathogens in the differential diagnosis of bone lesions when clinical and radiological findings do not align.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102981"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144526215","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-07-08DOI: 10.1016/j.anaerobe.2025.102984
Yuliang Zhao, Haijuan Qin, Yuhua Lyu, Song Yan, Huali Yu
{"title":"Study on acute exposure of polyethylene terephthalate microplastics on the performance of anammox granular sludge","authors":"Yuliang Zhao, Haijuan Qin, Yuhua Lyu, Song Yan, Huali Yu","doi":"10.1016/j.anaerobe.2025.102984","DOIUrl":"10.1016/j.anaerobe.2025.102984","url":null,"abstract":"<div><h3>Background</h3><div>Anaerobic ammonia oxidation is a new and efficient biological denitrification process, which has been used in practice. Research on the effect of microplastics (MPs) on anaerobic ammonia oxidation (anammox) process is limited.</div></div><div><h3>Topic</h3><div>In this study, the effects of short-term exposure of polyethylene terephthalate (PET) with different particle sizes for 12 h on anammox granular sludge (AnGS) and the metabolic mechanism of anaerobic ammonia oxidizing bacteria (AnAOB) were studied.</div></div><div><h3>Results</h3><div>The results showed that the acute exposure of anammox reactor to PET-MPs could promote the denitrification rate of the reactor. The enzyme activity of hydrazine dehydrogenase (HDH), the key enzyme of anammox reaction, was increased under acute exposure of different particle sizes of PET-MPs. PET-MPs with larger particle size had a stronger promoting effect on the treatment efficiency and HDH activity of the reactor. PET-MPs could stimulate AnAOB to secrete a large amount of extracellular polymeric substances (EPS). Metabonomic analysis showed that after the addition of PET-MPs, the abundance of 3-methoxytyramine was down-regulated, and the abundance of L-serine decreased. In the 13 μm PET-MPs group, the abundance of L-asparagine was up-regulated, changes in these metabolites affected various amino acid metabolism, proteolytic enzymes, and AnAOB biosynthesis.</div></div><div><h3>Implication</h3><div>This study provides valuable insights into the response characteristics and mechanism of the anammox process exposed to MPs, which may be helpful for the application of MPs in wastewater treatment.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102984"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144599208","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-08-01Epub Date: 2025-07-08DOI: 10.1016/j.anaerobe.2025.102983
Su-Chen Lim , Jessica Chisholm , Deirdre A. Collins , Molly Lattin , Charlotte Bell , Linda Selvey , Simon Reid , Thomas V. Riley
{"title":"Clostridioides difficile in Australian dairy farms","authors":"Su-Chen Lim , Jessica Chisholm , Deirdre A. Collins , Molly Lattin , Charlotte Bell , Linda Selvey , Simon Reid , Thomas V. Riley","doi":"10.1016/j.anaerobe.2025.102983","DOIUrl":"10.1016/j.anaerobe.2025.102983","url":null,"abstract":"<div><h3>Objectives</h3><div>This study aimed to investigate the prevalence and diversity of <em>C. difficile</em> in Australian dairy farms.</div></div><div><h3>Methods</h3><div>A total of 320 samples, including faeces, rectal swabs, effluent, soil and water, were collected from seven dairy farms across two Australian states.</div></div><div><h3>Results</h3><div><em>C. difficile</em> was present in all seven farms (100 %) and 44.4 % of the samples tested, with the highest prevalence found in soil (94.3 %), effluent (73.7 %) and faeces (60.4 %). Forty-four distinct ribotypes were identified among 174 isolates, of which 17 have been found previously in humans. <em>C. difficile</em> ribotype (RT) 127 (A + B + CDT+) was the predominant strain, comprising 42.5 % of isolates. The findings also indicated that the environment of Australian dairy farms is persistently contaminated with <em>C. difficile</em>, especially RT 127 and may represent a potential source for zoonotic transmission.</div></div><div><h3>Conclusions</h3><div><em>C. difficile</em> may be widespread in Australian dairy farms, with notably high prevalence in both animals and environmental samples.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"94 ","pages":"Article 102983"},"PeriodicalIF":2.5,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144607222","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
AnaerobePub Date : 2025-06-01Epub Date: 2025-03-19DOI: 10.1016/j.anaerobe.2025.102953
Jon J. Vernon , David W. Eyre , Mark H. Wilcox , Jane Freeman
{"title":"Molecular clock complexities of Clostridioides difficile","authors":"Jon J. Vernon , David W. Eyre , Mark H. Wilcox , Jane Freeman","doi":"10.1016/j.anaerobe.2025.102953","DOIUrl":"10.1016/j.anaerobe.2025.102953","url":null,"abstract":"<div><h3>Objectives</h3><div>Reconstruct the phylogenetic status of a collection of historical <em>Clostridioides difficile</em> isolates and evaluate the congruence of their evolutionary trajectories with established molecular clock models.</div></div><div><h3>Methods</h3><div>Phylogenetic analysis was performed on Illumina sequence reads from previously analysed historic <em>C. difficile</em> isolates (1980–86; <em>n</em> = 75) demonstrating multiple antimicrobial resistances. Data was grouped by ribotype (RT), including comparators from European surveillance (2012–13) and phylogenetic studies (1985–2010). Reads were mapped to CD630/CD196 reference genomes and compared using recombination-adjusted maximum likelihood trees. Prediction intervals for expected SNP differences by age were calculated using a Poisson distribution and molecular clock estimates (0.74 SNPs per genome/per year). Root-to-tip analysis was performed to determine the date of most common recent ancestor of genomes sharing a ribotype.</div></div><div><h3>Results</h3><div>Moxifloxacin-resistant (>16 mg/L) RT027 isolate JV67 (1986) was two SNPs distinct from a 2006 genome, fewer than the expected lower estimate (4.4 SNPs) under current molecular clock calculations; (<em>p</em> = 3.93x10<sup>−5</sup>). For isolate JV02 (1981), the 13 SNP divergence from a 2008 isolate was consistent with expectations (5.9 SNPs; <em>p</em> = 0.07). JV73 (1983) demonstrated an 8 SNP difference, which although above the expected lower limit (5.5 SNPs), was outside the 95 % prediction interval; (<em>p</em> = 4.51x10<sup>−3</sup>). Only sixty-nine percent of historical genomes fit within the prediction interval for the number of SNPs expected compared to recent isolates, with fewer SNPs observed more frequently than expected. Root-to-tip analysis demonstrated a weak linear correlation.</div></div><div><h3>Conclusions</h3><div><em>C. difficile</em> molecular clock estimations may be more complex than previously considered, with periods of spore quiescence potentially complicating analyses.</div></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"93 ","pages":"Article 102953"},"PeriodicalIF":2.5,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143673198","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}