Colten W Dornbach, James E Wells, Elaine D Berry, Samodha C Fernando, Paul R Broadway, Kristin E Hales
The aim was to longitudinally evaluate the association between antimicrobial exposure and resistance occurrence within generic Escherichia coli and Enterococcus spp. populations in feedlot beef cattle raised conventionally or raised without antimicrobials. Angus steers (n = 180) were sorted into 1 of 2 treatments over 2 consecutive years (108 in yr 1 and 72 in yr 2): steers raised without antimicrobials (NAT) and conventionally raised steers exposed to antimicrobials (CONV). Pens within treatment were adjacent and separated by five empty pens from the other treatment. Monensin and tylosin were included in CONV steer diets. On d 123, CONV steers received a metaphylactic antimicrobial. Longitudinal diet (n = 6/year) and fecal (n = 5/year) sampling timepoints were collected to determine E. coli and Enterococcus spp. concentration, prevalence, and resistance patterns. Dietary Enterococcus spp. concentrations, and erythromycin (8ERYR; 128ERYR), tetracycline (TETR), trimethoprim-sulfamethoxazole (COTR), and cefotaxime (CTXR) resistant E. coli concentrations and prevalence were greater in NAT diets than CONV diets (p < 0.02). Fecal E. coli concentrations tended to be greater in NAT steers than CON steers (p = 0.07). Fecal TETRE. coli concentrations were greater in CONV steers than NAT steers (p = 0.03). Fecal COTR and CTXRE. coli prevalence was greater for CONV steers at the beginning of the finishing phase while greater for NAT steers at the end of the finishing phase (p < 0.01). Fecal Enterococcus spp. concentrations did not differ between treatments (p = 0.11). Concentrations of 8ERYR and 128ERYREnterococcus spp. were greater in CONV steers on d 64, 130, and 168 than NAT steers (p < 0.05). Overall, antimicrobial resistant Enterococcus spp. and E. coli were detected regardless of antimicrobial exposure.
{"title":"Assessment of Antimicrobial Exposure on Generic <i>Escherichia coli</i> and <i>Enterococcus</i> spp. Concentration, Prevalence, and Resistance to Antimicrobials in Beef Cattle Raised with or Without Antimicrobials.","authors":"Colten W Dornbach, James E Wells, Elaine D Berry, Samodha C Fernando, Paul R Broadway, Kristin E Hales","doi":"10.1089/fpd.2024.0145","DOIUrl":"https://doi.org/10.1089/fpd.2024.0145","url":null,"abstract":"<p><p>The aim was to longitudinally evaluate the association between antimicrobial exposure and resistance occurrence within generic <i>Escherichia coli</i> and <i>Enterococcus</i> spp. populations in feedlot beef cattle raised conventionally or raised without antimicrobials. Angus steers (<i>n</i> = 180) were sorted into 1 of 2 treatments over 2 consecutive years (108 in yr 1 and 72 in yr 2): steers raised without antimicrobials (NAT) and conventionally raised steers exposed to antimicrobials (CONV). Pens within treatment were adjacent and separated by five empty pens from the other treatment. Monensin and tylosin were included in CONV steer diets. On d 123, CONV steers received a metaphylactic antimicrobial. Longitudinal diet (<i>n</i> = 6/year) and fecal (<i>n</i> = 5/year) sampling timepoints were collected to determine <i>E. coli</i> and <i>Enterococcus</i> spp. concentration, prevalence, and resistance patterns. Dietary <i>Enterococcus</i> spp. concentrations, and erythromycin (8ERY<sup>R</sup>; 128ERY<sup>R</sup>), tetracycline (TET<sup>R</sup>), trimethoprim-sulfamethoxazole (COT<sup>R</sup>), and cefotaxime (CTX<sup>R</sup>) resistant <i>E. coli</i> concentrations and prevalence were greater in NAT diets than CONV diets (<i>p</i> < 0.02). Fecal <i>E. coli</i> concentrations tended to be greater in NAT steers than CON steers (<i>p</i> = 0.07). Fecal TET<sup>R</sup> <i>E. coli</i> concentrations were greater in CONV steers than NAT steers (<i>p</i> = 0.03). Fecal COT<sup>R</sup> and CTX<sup>R</sup> <i>E. coli</i> prevalence was greater for CONV steers at the beginning of the finishing phase while greater for NAT steers at the end of the finishing phase (<i>p</i> < 0.01). Fecal <i>Enterococcus</i> spp. concentrations did not differ between treatments (<i>p</i> = 0.11). Concentrations of 8ERY<sup>R</sup> and 128ERY<sup>R</sup> <i>Enterococcus</i> spp. were greater in CONV steers on d 64, 130, and 168 than NAT steers (<i>p</i> < 0.05). Overall, antimicrobial resistant <i>Enterococcus</i> spp. and <i>E. coli</i> were detected regardless of antimicrobial exposure.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":""},"PeriodicalIF":1.9,"publicationDate":"2025-02-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143370586","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lin Wang, Zhen Xiao, Juan Wang, Na Liu, Wen Jiang, Yaopeng Liu, Fangyuan Hu, Huanqi Liu, Junhui Liu, Zhina Qu, Junwei Wang
Objective: The emergence of antibiotic-resistant Staphylococcus aureus, especially methicillin-resistant S. aureus (MRSA), poses a great challenge for animal and public health. This study aimed to isolate a broad-spectrum and high-efficiency MRSA phage and explore the phage-antibiotic synergistic effect on MRSA. Results: Phage STPX-6 belongs to Caudovirales, Podoviridae. It has a hexahedral head and a short tail. Its genome length was 17,007 bp, and it did not contain resistance genes and virulence genes. STPX-6 lysed 79.6% (133/167) of 167 S. aureus and 87.96% (95/108) of MRSA from different sources. The titer of phage was 1.18 × 1010 PFU/mL, the optimal multiplicity of infection was 1, the latent period and lysis period were about 10 min and 60 min, respectively, and the burst amount was 68 PFU/cell. At 50°C and 70-90°C, the titer of STPX-6 was maintained at about 1010 PFU/mL and at least 103 PFU/mL, respectively. In the range of pH 4-12, the titer of phage remained above 108 PFU/mL, and it remained above 104 PFU/mL at pH 2, 3, 13, and 14. The combined application of phage STPX-6 and enrofloxacin, doxycycline, ampicillin could reduce the minimum inhibitory concentration (MIC) of the three antibiotics to 1/4 MIC, 1/16 MIC, and 1/2 MIC, respectively. Conclusion: This study found that for the host MRSA, lytic phage STPX-6 had the characteristics of a broad lytic spectrum, a short latent period, strong adaptability and strong tolerance to high temperature, a strong acid and strong alkali environment, and might maintain certain activity under extreme environment. More importantly, the combination of phage STPX-6 with enrofloxacin, doxycycline, and ampicillin could reduce the antibiotic concentration used for MRSA. In other words, phages as new antibacterial agents have received increasing attention. The combined application of phages and antibiotics provides a new method for controlling multidrug resistant bacteria and reduce the use of antibiotics.
{"title":"Controlling Multidrug-Resistant <i>Staphylococcus aureus</i> by Combined Use of Antimicrobials and Phage STPX-6 with Broad Spectrum and High Efficiency.","authors":"Lin Wang, Zhen Xiao, Juan Wang, Na Liu, Wen Jiang, Yaopeng Liu, Fangyuan Hu, Huanqi Liu, Junhui Liu, Zhina Qu, Junwei Wang","doi":"10.1089/fpd.2024.0130","DOIUrl":"https://doi.org/10.1089/fpd.2024.0130","url":null,"abstract":"<p><p><b><i>Objective:</i></b> The emergence of antibiotic-resistant <i>Staphylococcus aureus</i>, especially methicillin-resistant <i>S. aureus</i> (MRSA), poses a great challenge for animal and public health. This study aimed to isolate a broad-spectrum and high-efficiency MRSA phage and explore the phage-antibiotic synergistic effect on MRSA. <b><i>Results:</i></b> Phage STPX-6 belongs to <i>Caudovirales</i>, <i>Podoviridae</i>. It has a hexahedral head and a short tail. Its genome length was 17,007 bp, and it did not contain resistance genes and virulence genes. STPX-6 lysed 79.6% (133/167) of 167 <i>S. aureu</i>s and 87.96% (95/108) of MRSA from different sources. The titer of phage was 1.18 × 10<sup>10</sup> PFU/mL, the optimal multiplicity of infection was 1, the latent period and lysis period were about 10 min and 60 min, respectively, and the burst amount was 68 PFU/cell. At 50°C and 70-90°C, the titer of STPX-6 was maintained at about 10<sup>10</sup> PFU/mL and at least 10<sup>3</sup> PFU/mL, respectively. In the range of pH 4-12, the titer of phage remained above 10<sup>8</sup> PFU/mL, and it remained above 10<sup>4</sup> PFU/mL at pH 2, 3, 13, and 14. The combined application of phage STPX-6 and enrofloxacin, doxycycline, ampicillin could reduce the minimum inhibitory concentration (MIC) of the three antibiotics to 1/4 MIC, 1/16 MIC, and 1/2 MIC, respectively. <b><i>Conclusion:</i></b> This study found that for the host MRSA, lytic phage STPX-6 had the characteristics of a broad lytic spectrum, a short latent period, strong adaptability and strong tolerance to high temperature, a strong acid and strong alkali environment, and might maintain certain activity under extreme environment. More importantly, the combination of phage STPX-6 with enrofloxacin, doxycycline, and ampicillin could reduce the antibiotic concentration used for MRSA. In other words, phages as new antibacterial agents have received increasing attention. The combined application of phages and antibiotics provides a new method for controlling multidrug resistant bacteria and reduce the use of antibiotics.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":""},"PeriodicalIF":1.9,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143254323","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-01Epub Date: 2024-09-04DOI: 10.1089/fpd.2024.0025
Miaorong Xiao, Ao Shen, Xiaodi Chen, Tongtong Lu, Jin Zhang, Shuzhen Li, Weiwei Yang
In this study, sea buckthorn polysaccharides (SBP) were added as functional substances to chitosan (CS), and chitosan/sea buckthorn polysaccharide (SCS) composite films were prepared using the casting method. The effects of SBP addition on the optical properties, physical properties, mechanical properties, structure, antioxidant activity, and antibacterial activity of the SCS composite films were studied, and the prepared SCS composite films were used to preserve yellow cherry tomatoes. The results showed that SCS composite films exhibited good UV resistance, water solubility, and antioxidant activity, but its apparent structure, hydrophobicity, and mechanical properties needed further improvement. Meanwhile, SBP has inhibitory effects on all 8 experimental strains. In addition, the SCS composite film with the addition of 200 mg/L SBP could reduce the weight loss rate of yellow cherry tomatoes, maintain hardness, delay the decrease of total soluble solids, titratable acid, and Vitamin C content, and inhibit the accumulation of malondialdehyde. SCS composite films are beneficial for enhancing the quality of yellow cherry tomatoes during storage, and their application in fruit and vegetable preservation has development prospects.
{"title":"Preparation and Keep-Refreshing Effect of Chitosan/Sea Buckthorn Polysaccharide Composite Film on the Preservation of Yellow Cherry Tomatoes.","authors":"Miaorong Xiao, Ao Shen, Xiaodi Chen, Tongtong Lu, Jin Zhang, Shuzhen Li, Weiwei Yang","doi":"10.1089/fpd.2024.0025","DOIUrl":"10.1089/fpd.2024.0025","url":null,"abstract":"<p><p>In this study, sea buckthorn polysaccharides (SBP) were added as functional substances to chitosan (CS), and chitosan/sea buckthorn polysaccharide (SCS) composite films were prepared using the casting method. The effects of SBP addition on the optical properties, physical properties, mechanical properties, structure, antioxidant activity, and antibacterial activity of the SCS composite films were studied, and the prepared SCS composite films were used to preserve yellow cherry tomatoes. The results showed that SCS composite films exhibited good UV resistance, water solubility, and antioxidant activity, but its apparent structure, hydrophobicity, and mechanical properties needed further improvement. Meanwhile, SBP has inhibitory effects on all 8 experimental strains. In addition, the SCS composite film with the addition of 200 mg/L SBP could reduce the weight loss rate of yellow cherry tomatoes, maintain hardness, delay the decrease of total soluble solids, titratable acid, and Vitamin C content, and inhibit the accumulation of malondialdehyde. SCS composite films are beneficial for enhancing the quality of yellow cherry tomatoes during storage, and their application in fruit and vegetable preservation has development prospects.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"131-139"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142125267","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-01Epub Date: 2024-02-23DOI: 10.1089/fpd.2023.0104
Kashaf Yaseen, Sultan Ali, Sajjad-Ur Rahman, Muhammad Sohail Sajid
This study holds significant importance due to its focus on Campylobacter, the leading bacterial cause of gastroenteritis worldwide, responsible for ∼96 million cases each year. By investigating the prevalence of both Campylobacter jejuni and Campylobacter coli in humans, animals, and the environment, this research sheds light on the broader impact of these pathogens, which can harm both human and animal populations. Traditional microbiological methods were implemented followed by optimized multiplex polymerase chain reaction targeting 16S rDNA and virulence gene markers by using specific primers. The findings revealed that a total of 219 Campylobacter isolates were recovered from 528 collected specimens from human, animal, and environmental sources. Campylobacter species showed a prevalence of 41.5%, with C. jejuni accounting for 53% and C. coli for 47%. Antimicrobial resistance rates were high, with tetracycline at 89%, ceftriaxone at 75%, cefotaxime at 70%, erythromycin at 69%, nalidixic acid at 54%, ciprofloxacin at 39%, and gentamicin at 23%. Commonly prevalent virulence-associated genes observed in the Campylobacter were cadF at 93%, flaA at 91%, cdtB at 88%, cheY at 86%, sodB at 78%, and iamA at 32%. The study confirmed multidrug-resistant Campylobacter prevalence at the human-animal-environment interface, harboring virulence-associated genes with potential harm to humans. Data analysis showed a nonsignificant (p ≥ 0.05) correlation between virulence genes and antibiotic susceptibility. To effectively manage Campylobacter infections, a multifaceted strategy incorporating preventative interventions at different levels is required. This strategy should take into account practicability, effectiveness, and sustainability while strengthening surveillance systems and addressing the economics of disease prevention.
{"title":"Comparative Molecular Virulence Typing and Antibiotic Resistance of <i>Campylobacter</i> Species at the Human-Animal-Environment Interface.","authors":"Kashaf Yaseen, Sultan Ali, Sajjad-Ur Rahman, Muhammad Sohail Sajid","doi":"10.1089/fpd.2023.0104","DOIUrl":"10.1089/fpd.2023.0104","url":null,"abstract":"<p><p>This study holds significant importance due to its focus on <i>Campylobacter</i>, the leading bacterial cause of gastroenteritis worldwide, responsible for ∼96 million cases each year. By investigating the prevalence of both <i>Campylobacter jejuni</i> and <i>Campylobacter coli</i> in humans, animals, and the environment, this research sheds light on the broader impact of these pathogens, which can harm both human and animal populations. Traditional microbiological methods were implemented followed by optimized multiplex polymerase chain reaction targeting 16S rDNA and virulence gene markers by using specific primers. The findings revealed that a total of 219 <i>Campylobacter</i> isolates were recovered from 528 collected specimens from human, animal, and environmental sources. <i>Campylobacter</i> species showed a prevalence of 41.5%, with <i>C. jejuni</i> accounting for 53% and <i>C. coli</i> for 47%. Antimicrobial resistance rates were high, with tetracycline at 89%, ceftriaxone at 75%, cefotaxime at 70%, erythromycin at 69%, nalidixic acid at 54%, ciprofloxacin at 39%, and gentamicin at 23%. Commonly prevalent virulence-associated genes observed in the <i>Campylobacter</i> were <i>cad</i>F at 93%, <i>fla</i>A at 91%, <i>cdt</i>B at 88%, <i>che</i>Y at 86%, <i>sod</i>B at 78%, and <i>iam</i>A at 32%. The study confirmed multidrug-resistant <i>Campylobacter</i> prevalence at the human-animal-environment interface, harboring virulence-associated genes with potential harm to humans. Data analysis showed a nonsignificant (<i>p</i> ≥ 0.05) correlation between virulence genes and antibiotic susceptibility. To effectively manage <i>Campylobacter</i> infections, a multifaceted strategy incorporating preventative interventions at different levels is required. This strategy should take into account practicability, effectiveness, and sustainability while strengthening surveillance systems and addressing the economics of disease prevention.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"109-117"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139939900","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-01Epub Date: 2024-09-18DOI: 10.1089/fpd.2023.0169
Cui Xinhua, Wang Yang, Shi Jinyang, Xu Hongyue, Yu Wanlu, Zhu Mingmei, Qiu Jiazhang, Yu Lu
Salmonella Typhimurium is a foodborne pathogen threatening livestock and human health. It is highly resistant to commonly used clinical antibiotics, and it is urgently needed to explore new anti-Salmonella treatment schemes. In this study, first, our in vivo mouse experiments showed that Baitouweng decoction (BTW), a classical Traditional Chinese Medicine (TCM) prescription, had good efficacy against Salmonella Typhimurium infection: mitigating weight loss of mice; lowering the bacterial load of liver, spleen, and colon; reducing the production of serum inflammatory factors (interleukin-1β and tumor necrosis factor-α); and decreasing histological index scores than that in the Salmonella Typhimurium infection group. Furthermore, we explored the potential active components and molecular mechanism of BTW in the treatment of Salmonella Typhimurium infection. A total of 465 compounds of BTW were retrieved from herb website and 227 bioactive compounds were identified, 911 potential BTW-related targets and 1,602 disease targets of Salmonella Typhimurium infection were acquired by ten public analytical databases, among them, 188 genes were overlay targets of BTW-Salmonella Typhimurium; String, Metascape, and Cytoscape plug-in Molecular Complex Detection and ClueGo analysis pointed that BTW exerted an anti-Salmonella effect through a multicomponent, multitarget, and multipathway manner, including 10 hub targets (TNF, AKT CASP3, ALB, EGFR, JUN, MAPK, STAT3, VEGFA, and TP53) and 94 pathways such as cell apoptosis, inflammation, and metabolism. Finally, AutoDock Vina showed that the hub target AKT1 with menispermine and quercetin had good binding energy, which was confirmed by the in vitro cellular thermal shift assay and drug affinity responsive target stability assay. This study laid the foundation for further study of BTW mechanism and for further development of BTW anti-Salmonella.
{"title":"The Effects of Baitouweng Decoction on <i>Salmonella</i> Typhimurium Infection and Its Underlying Mechanisms Evaluated by <i>In Vivo</i> and <i>In Vitro</i> Experiments, Network Pharmacology Analysis, and Molecular Docking Technology.","authors":"Cui Xinhua, Wang Yang, Shi Jinyang, Xu Hongyue, Yu Wanlu, Zhu Mingmei, Qiu Jiazhang, Yu Lu","doi":"10.1089/fpd.2023.0169","DOIUrl":"10.1089/fpd.2023.0169","url":null,"abstract":"<p><p><i>Salmonella</i> Typhimurium is a foodborne pathogen threatening livestock and human health. It is highly resistant to commonly used clinical antibiotics, and it is urgently needed to explore new anti-<i>Salmonella</i> treatment schemes. In this study, first, our <i>in vivo</i> mouse experiments showed that Baitouweng decoction (BTW), a classical Traditional Chinese Medicine (TCM) prescription, had good efficacy against <i>Salmonella</i> Typhimurium infection: mitigating weight loss of mice; lowering the bacterial load of liver, spleen, and colon; reducing the production of serum inflammatory factors (interleukin-1β and tumor necrosis factor-α); and decreasing histological index scores than that in the <i>Salmonella</i> Typhimurium infection group. Furthermore, we explored the potential active components and molecular mechanism of BTW in the treatment of <i>Salmonella</i> Typhimurium infection. A total of 465 compounds of BTW were retrieved from herb website and 227 bioactive compounds were identified, 911 potential BTW-related targets and 1,602 disease targets of <i>Salmonella</i> Typhimurium infection were acquired by ten public analytical databases, among them, 188 genes were overlay targets of BTW-<i>Salmonella</i> Typhimurium; String, Metascape, and Cytoscape plug-in Molecular Complex Detection and ClueGo analysis pointed that BTW exerted an anti-<i>Salmonella</i> effect through a multicomponent, multitarget, and multipathway manner, including 10 hub targets (TNF, AKT CASP3, ALB, EGFR, JUN, MAPK, STAT3, VEGFA, and TP53) and 94 pathways such as cell apoptosis, inflammation, and metabolism. Finally, AutoDock Vina showed that the hub target AKT1 with menispermine and quercetin had good binding energy, which was confirmed by the <i>in vitro</i> cellular thermal shift assay and drug affinity responsive target stability assay. This study laid the foundation for further study of BTW mechanism and for further development of BTW anti-<i>Salmonella</i>.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"140-158"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142282796","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Salmonella enterica serovar Typhimurium and its variants are the most common serotypes of human salmonellosis cases. Serotyping Salmonella Typhimurium and its variants has always been challenging. Our previous work found that among 14 Salmonella Typhimurium and variant strains, some different antigenic formulas had 100% pulsed-field gel electrophoresis (PFGE) similarity. The 14 strains were sorted into 3 groups; in each group, the different antigenic formulas had the same PFGE patterns. This phenomenon suggested that different antigenic formula identification might originate from a common ancestor subtyped by PFGE. To assess whether the serotyping method on Salmonella Typhimurium and variant strains reflected the genetic relationship, we improved the discrimination for the phylogenetic relationship among the 14 Salmonella Typhimurium and variant strains using Fourier-transform infrared spectroscopy (FTIR) and whole-genome multilocus sequence typing (wgMLST). We compared the wgMLST assay of 14 Salmonella Typhimurium and variant strains from this study with 50 public ST34 strain data of Salmonella Typhimurium and variant strains. We also compared flagella (H antigen)-related genes based on the whole genome of 14 strains and the other 293 ST34 public database for further understanding of this question. The phylogenetic results (PFGE) showed no regularity between the antigenic formulas and genotypes. The results of the higher discrimination power assays (FTIR and whole-genome multilocus sequence typing) also showed no regularity between the antigenic formulas and genotypes (or phenotypes). The 58 flagella encoding genes of different antigenic formulas were sorted into 13 patterns. However, a similar phenomenon was found: the same flagella encoding gene patterns could express different antigenic formulas. In conclusion, there is no consistency between the antigenic formulas and phylogenetic relationships among ST34 Salmonella Typhimurium and variant strains, even in flagella antigenic formula and flagella encoding genes.
{"title":"Flagella Phenotypic Variations of ST34 Type <i>Salmonella</i> Typhimurium and Variants.","authors":"Xin Wu, Fanan Suksawat, Patchara Phuektes, Supatcharee Siriwong, Hongmei Liu, Wengui Li, Sunpetch Angkititrakul","doi":"10.1089/fpd.2023.0091","DOIUrl":"10.1089/fpd.2023.0091","url":null,"abstract":"<p><p><i>Salmonella enterica</i> serovar Typhimurium and its variants are the most common serotypes of human salmonellosis cases. Serotyping <i>Salmonella</i> Typhimurium and its variants has always been challenging. Our previous work found that among 14 <i>Salmonella</i> Typhimurium and variant strains, some different antigenic formulas had 100% pulsed-field gel electrophoresis (PFGE) similarity. The 14 strains were sorted into 3 groups; in each group, the different antigenic formulas had the same PFGE patterns. This phenomenon suggested that different antigenic formula identification might originate from a common ancestor subtyped by PFGE. To assess whether the serotyping method on <i>Salmonella</i> Typhimurium and variant strains reflected the genetic relationship, we improved the discrimination for the phylogenetic relationship among the 14 <i>Salmonella</i> Typhimurium and variant strains using Fourier-transform infrared spectroscopy (FTIR) and whole-genome multilocus sequence typing (wgMLST). We compared the wgMLST assay of 14 <i>Salmonella</i> Typhimurium and variant strains from this study with 50 public ST34 strain data of <i>Salmonella</i> Typhimurium and variant strains. We also compared flagella (H antigen)-related genes based on the whole genome of 14 strains and the other 293 ST34 public database for further understanding of this question. The phylogenetic results (PFGE) showed no regularity between the antigenic formulas and genotypes. The results of the higher discrimination power assays (FTIR and whole-genome multilocus sequence typing) also showed no regularity between the antigenic formulas and genotypes (or phenotypes). The 58 flagella encoding genes of different antigenic formulas were sorted into 13 patterns. However, a similar phenomenon was found: the same flagella encoding gene patterns could express different antigenic formulas. In conclusion, there is no consistency between the antigenic formulas and phylogenetic relationships among ST34 <i>Salmonella</i> Typhimurium and variant strains, even in flagella antigenic formula and flagella encoding genes.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"159-166"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140101405","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-01Epub Date: 2024-04-02DOI: 10.1089/fpd.2023.0079
Mehedi Hasan, Sudipta Talukder, Amit Kumar Mandal, Syeda Tanjina Tasmim, Sonia Parvin, Yamin Ali, Mahmudul Hasan Sikder, Thomas J Callaghan, Ricardo J Soares Magalhães, Taohidul Islam
The rapid emergence of antimicrobial resistance (AMR) in Campylobacter has reinforced its status as a foodborne pathogen of significant public health concern. Resistant Campylobacter is typically transferred to humans via the consumption of contaminated animal products, particularly poultry. The genes associated with antimicrobial resistance in Campylobacter spp. are poorly understood. To address this knowledge gap, we conducted a prevalence survey of AMR Campylobacter across 84 chicken farms in two districts of Bangladesh. Pooled cloacal swabs were collected from chickens and underwent bacteriological testing for Campylobacter spp. with PCR confirmation. Antimicrobial susceptibility was tested against 14 antibiotics by disk diffusion method, and 12 resistance genes were screened in Campylobacter-positive isolates using multiplex PCR. A total of 34 (40.5%) farms were Campylobacter-positive of which 73.5% of isolates were resistant to at least 10 antibiotics. The antimicrobial susceptibility results indicate a high level of resistance against streptomycin (97.1%), clindamycin (97.1%), ampicillin (94.1%), tetracycline (94.1%), erythromycin (91.2%), ciprofloxacin (88.2%), nalidixic acid (85.3%), and imipenem (82.4%), and comparatively a low frequency of resistance to chloramphenicol (47.1%), ceftazidime (44.1%), and colistin (35.3%). Multidrug-resistant (MDR) and extensively drug-resistant Campylobacter were identified in 97.1%, and 50% of isolates, respectively. Ten resistance genes were identified including blaTEM (in 97.1% of isolates), strA-strB (85.9%), tetA (70.6%), tetB (32.4%), qnrS (23.5%), blaCTX-M-1 (20.6%), qnrB (20.6%), blaSHV (8.8%), aadB (5.9%), and qnrA (2.9%). Our findings demonstrate that resistance to ampicillin, tetracycline, and ceftazidime in Campylobacter isolates was significantly (p ≤ 0.05) associated with the presence of blaTEM, tetA, and blaSHV genes, respectively. The high rates of AMR in Campylobacter isolates from our study are not surprising given the liberal use of antimicrobials and incomplete biosecurity provisions on farms. Of particular concern are resistance rates to those classes of antibiotics that should be reserved for human use (azithromycin, ciprofloxacin, and colistin). AMR was more prevalent in chicken farms that used multiple antibiotics, engaged in prophylactic treatment of the birds, and improperly disposed of antibiotic packages. The high prevalence of MDR in chicken-derived Campylobacter isolates from the different regions of our study reinforces the need for more prudent use of antimicrobial compounds in Bangladeshi chicken farms.
{"title":"Antimicrobial Resistance Profiles of <i>Campylobacter</i> spp. Recovered from Chicken Farms in Two Districts of Bangladesh.","authors":"Mehedi Hasan, Sudipta Talukder, Amit Kumar Mandal, Syeda Tanjina Tasmim, Sonia Parvin, Yamin Ali, Mahmudul Hasan Sikder, Thomas J Callaghan, Ricardo J Soares Magalhães, Taohidul Islam","doi":"10.1089/fpd.2023.0079","DOIUrl":"10.1089/fpd.2023.0079","url":null,"abstract":"<p><p>The rapid emergence of antimicrobial resistance (AMR) in <i>Campylobacter</i> has reinforced its status as a foodborne pathogen of significant public health concern. Resistant <i>Campylobacter</i> is typically transferred to humans via the consumption of contaminated animal products, particularly poultry. The genes associated with antimicrobial resistance in <i>Campylobacter</i> spp. are poorly understood. To address this knowledge gap, we conducted a prevalence survey of AMR <i>Campylobacter</i> across 84 chicken farms in two districts of Bangladesh. Pooled cloacal swabs were collected from chickens and underwent bacteriological testing for <i>Campylobacter</i> spp. with PCR confirmation. Antimicrobial susceptibility was tested against 14 antibiotics by disk diffusion method, and 12 resistance genes were screened in <i>Campylobacter</i>-positive isolates using multiplex PCR. A total of 34 (40.5%) farms were <i>Campylobacter</i>-positive of which 73.5% of isolates were resistant to at least 10 antibiotics. The antimicrobial susceptibility results indicate a high level of resistance against streptomycin (97.1%), clindamycin (97.1%), ampicillin (94.1%), tetracycline (94.1%), erythromycin (91.2%), ciprofloxacin (88.2%), nalidixic acid (85.3%), and imipenem (82.4%), and comparatively a low frequency of resistance to chloramphenicol (47.1%), ceftazidime (44.1%), and colistin (35.3%). Multidrug-resistant (MDR) and extensively drug-resistant <i>Campylobacter</i> were identified in 97.1%, and 50% of isolates, respectively. Ten resistance genes were identified including <i>bla</i><sub>TEM</sub> (in 97.1% of isolates), <i>strA</i>-<i>strB</i> (85.9%), <i>tetA</i> (70.6%), <i>tetB</i> (32.4%), <i>qnrS</i> (23.5%), <i>bla</i><sub>CTX-M-1</sub> (20.6%), <i>qnrB</i> (20.6%), <i>bla</i><sub>SHV</sub> (8.8%), <i>aadB</i> (5.9%), and <i>qnrA</i> (2.9%). Our findings demonstrate that resistance to ampicillin, tetracycline, and ceftazidime in <i>Campylobacter</i> isolates was significantly (<i>p</i> ≤ 0.05) associated with the presence of <i>bla</i><sub>TEM</sub>, <i>tetA</i>, and <i>bla</i><sub>SHV</sub> genes, respectively. The high rates of AMR in <i>Campylobacter</i> isolates from our study are not surprising given the liberal use of antimicrobials and incomplete biosecurity provisions on farms. Of particular concern are resistance rates to those classes of antibiotics that should be reserved for human use (azithromycin, ciprofloxacin, and colistin). AMR was more prevalent in chicken farms that used multiple antibiotics, engaged in prophylactic treatment of the birds, and improperly disposed of antibiotic packages. The high prevalence of MDR in chicken-derived <i>Campylobacter</i> isolates from the different regions of our study reinforces the need for more prudent use of antimicrobial compounds in Bangladeshi chicken farms.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"118-130"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140335255","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Brucellosis, a significant zoonotic disease, threatens food safety substantially, particularly in developing nations such as the Middle East. This study aimed to comprehensively assess the prevalence of Brucella spp. in Iranian milk and dairy products through a systematic review and meta-analysis. A thorough search of international and domestic databases from January 2008 to October 2023 identified 38 relevant studies encompassing 11,130 samples for meta-analysis. The overall prevalence of Brucella spp. in Iranian dairy products was 22% (95% CI: 16-28%). The highest and lowest overall prevalence of Brucella spp. in milk were found in raw goat milk 27% (95% CI: 11-42%) and raw camel milk 15% (95% CI: -0.42 to 72%), respectively. The overall prevalence of traditional cheese, ice cream, and cream is estimated to be 9% (95% CI: -16 to 35%), 2% (95% CI: -2.78 to 2.82%), and 9% (95% CI: -0.94 to 1.12%). Geographical disparities were evident, with Zanjan province reporting the highest contamination rate, 53%, while Razavi Khorasan province had the lowest, 1%. However, the prevalence of Brucella spp. in Iranian dairy products has fluctuated over time, with a significant association between the study year and sample size. Comprehensive planning, robust policy implementation, and rigorous monitoring are imperative to mitigate and ultimately eliminate Brucella contamination in dairy products effectively. Further research is essential to refine prevalence estimates and develop targeted prevention strategies to safeguard public health.
{"title":"The Prevalence of <i>Brucella</i> spp. in Dairy Products in Iran: A Systematic Review and Meta-Analysis.","authors":"Narges Shahbazpour, Elahesadat Hosseini, Seyed Ehsan Beladian Behbahan, Fatemeh Esfarjani, Seyed Amir Mohamad Mortazavian, Abdol-Samad Abedi, Slim Smaoui","doi":"10.1089/fpd.2024.0093","DOIUrl":"10.1089/fpd.2024.0093","url":null,"abstract":"<p><p>Brucellosis, a significant zoonotic disease, threatens food safety substantially, particularly in developing nations such as the Middle East. This study aimed to comprehensively assess the prevalence of <i>Brucella</i> spp. in Iranian milk and dairy products through a systematic review and meta-analysis. A thorough search of international and domestic databases from January 2008 to October 2023 identified 38 relevant studies encompassing 11,130 samples for meta-analysis. The overall prevalence of <i>Brucella</i> spp. in Iranian dairy products was 22% (95% CI: 16-28%). The highest and lowest overall prevalence of <i>Brucella</i> spp. in milk were found in raw goat milk 27% (95% CI: 11-42%) and raw camel milk 15% (95% CI: -0.42 to 72%), respectively. The overall prevalence of traditional cheese, ice cream, and cream is estimated to be 9% (95% CI: -16 to 35%), 2% (95% CI: -2.78 to 2.82%), and 9% (95% CI: -0.94 to 1.12%). Geographical disparities were evident, with Zanjan province reporting the highest contamination rate, 53%, while Razavi Khorasan province had the lowest, 1%. However, the prevalence of <i>Brucella</i> spp. in Iranian dairy products has fluctuated over time, with a significant association between the study year and sample size. Comprehensive planning, robust policy implementation, and rigorous monitoring are imperative to mitigate and ultimately eliminate <i>Brucella</i> contamination in dairy products effectively. Further research is essential to refine prevalence estimates and develop targeted prevention strategies to safeguard public health.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"71-85"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142105981","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-01Epub Date: 2024-03-18DOI: 10.1089/fpd.2023.0089
Catherine A Gensler, Stephanie C Hempstead, Shivaramu Keelara, Paula J Fedorka-Cray, Natalie J Urie, Alyson M Wiedenheft, Keira Stuart, Katherine L Marshall, Megan E Jacob
Escherichia coli and Enterococcus species are normal bacteria of the gastrointestinal tract and serve as indicator organisms for the epidemiology and emergence of antimicrobial resistance in their hosts and the environment. Some E. coli serovars, including E. coli O157:H7, are important human pathogens, although reservoir species such as goats remain asymptomatic. We describe the prevalence and antimicrobial resistance of generic E. coli, E. coli O157:H7, and Enterococcus species collected from a national surveillance study of goat feces as part of the National Animal Health Monitoring System (NAHMS) Goat 2019 study. Fecal samples were collected from 4918 goats on 332 operations across the United States. Expectedly, a high prevalence of E. coli (98.7%, 4850/4915) and Enterococcus species (94.8%, 4662/4918) was found. E. coli O157:H7 prevalence was low (0.2%; 10/4918). E. coli isolates, up to three per operation, were evaluated for antimicrobial susceptibility and 84.7% (571/674) were pansusceptible. Multidrug resistance (MDR; ≥3 classes) was uncommon among E. coli, occurring in 8.2% of isolates (55/674). Resistance toward seven antimicrobial classes was observed in a single isolate. Resistance to tetracycline alone (13.6%, 92/674) or to tetracycline, streptomycin, and sulfisoxazole (7.0% 47/674) was the most common pattern. All E. coli O157:H7 isolates were pansusceptible. Enterococcus isolates, up to four per operation, were prioritized by public health importance, including Enterococcus faecium and Enterococcus faecalis and evaluated. Resistance to lincomycin (93.8%, 1232/1313) was most common, with MDR detected in 29.5% (388/1313) of isolates. The combination of ciprofloxacin, lincomycin, and quinupristin resistance (27.1%, 105/388) was the most common pattern detected. Distribution and characteristics of antimicrobial resistance in E. coli and Enterococcus in the U.S. goat population from this study can inform stewardship considerations and public health efforts surrounding goats and their products.
{"title":"Antimicrobial Resistance Characteristics of Fecal <i>Escherichia coli</i> and <i>Enterococcus</i> Species in U.S. Goats: 2019 National Animal Health Monitoring System Enteric Study.","authors":"Catherine A Gensler, Stephanie C Hempstead, Shivaramu Keelara, Paula J Fedorka-Cray, Natalie J Urie, Alyson M Wiedenheft, Keira Stuart, Katherine L Marshall, Megan E Jacob","doi":"10.1089/fpd.2023.0089","DOIUrl":"10.1089/fpd.2023.0089","url":null,"abstract":"<p><p><i>Escherichia coli</i> and <i>Enterococcus</i> species are normal bacteria of the gastrointestinal tract and serve as indicator organisms for the epidemiology and emergence of antimicrobial resistance in their hosts and the environment. Some <i>E. coli</i> serovars, including <i>E. coli</i> O157:H7, are important human pathogens, although reservoir species such as goats remain asymptomatic. We describe the prevalence and antimicrobial resistance of generic <i>E. coli</i>, <i>E. coli</i> O157:H7, and <i>Enterococcus</i> species collected from a national surveillance study of goat feces as part of the National Animal Health Monitoring System (NAHMS) Goat 2019 study. Fecal samples were collected from 4918 goats on 332 operations across the United States. Expectedly, a high prevalence of <i>E. coli</i> (98.7%, 4850/4915) and <i>Enterococcus</i> species (94.8%, 4662/4918) was found. <i>E. coli</i> O157:H7 prevalence was low (0.2%; 10/4918). <i>E. coli</i> isolates, up to three per operation, were evaluated for antimicrobial susceptibility and 84.7% (571/674) were pansusceptible. Multidrug resistance (MDR; ≥3 classes) was uncommon among <i>E. coli</i>, occurring in 8.2% of isolates (55/674). Resistance toward seven antimicrobial classes was observed in a single isolate. Resistance to tetracycline alone (13.6%, 92/674) or to tetracycline, streptomycin, and sulfisoxazole (7.0% 47/674) was the most common pattern. All <i>E. coli</i> O157:H7 isolates were pansusceptible. <i>Enterococcus</i> isolates, up to four per operation, were prioritized by public health importance, including <i>Enterococcus faecium</i> and <i>Enterococcus faecalis</i> and evaluated. Resistance to lincomycin (93.8%, 1232/1313) was most common, with MDR detected in 29.5% (388/1313) of isolates. The combination of ciprofloxacin, lincomycin, and quinupristin resistance (27.1%, 105/388) was the most common pattern detected. Distribution and characteristics of antimicrobial resistance in <i>E. coli</i> and <i>Enterococcus</i> in the U.S. goat population from this study can inform stewardship considerations and public health efforts surrounding goats and their products.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":"97-108"},"PeriodicalIF":1.9,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140174097","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yu-Jeong Hwang, Bo-Youn Moon, Ji-In Kim, Md Sekendar Ali, Hyun-Ju Song, Yeon-Hee Lee, Ji-Hyun Choi, Hee-Seung Kang, Hyeon-Jung Park, Jae-Myung Kim, Suk-Kyung Lim
Antimicrobial-resistant bacterial contamination of meat poses a significant global public health risk. We aimed to determine antimicrobial resistance profiles and trends of Escherichia coli recovered from carcasses of healthy food-producing animals in South Korea during 2010-2023. In total, 4748 E. coli isolates obtained from cattle (n = 1582), pigs (n = 1572), and chickens (n = 1594) were assessed for susceptibility to 12 antimicrobials. Antimicrobial resistance was different among samples. Overall, antimicrobial resistance was high in pigs and chicken carcasses. More than about 80% of isolates from pigs and chickens exhibited resistance to one or more antimicrobials. Among the tested antimicrobials, resistance to ampicillin, chloramphenicol, streptomycin, and tetracycline was significantly higher in pigs and chickens compared with cattle (p < 0.05). Moreover, chicken isolates showed much higher resistance to nalidixic acid and ciprofloxacin than other samples. Resistance to critically important antimicrobials, colistin, remained less than about 1%, while resistance to ceftiofur showed increased trends in pig and chicken samples. Higher multidrug-resistant (MDR) isolates were identified in chickens and pigs compared with cattle (p < 0.05). Furthermore, most MDR patterns include streptomycin and tetracycline resistance. MDR E. coli contaminating meat during slaughter can be transmitted to humans via the food chain. Thus, prudent use of antimicrobials and proper hygienic practices are urgently needed to reduce the risk of transmission.
{"title":"Antimicrobial Resistance Profiles of <i>Escherichia coli</i> Isolated from Food Animal Carcasses During 2010-2023 in South Korea.","authors":"Yu-Jeong Hwang, Bo-Youn Moon, Ji-In Kim, Md Sekendar Ali, Hyun-Ju Song, Yeon-Hee Lee, Ji-Hyun Choi, Hee-Seung Kang, Hyeon-Jung Park, Jae-Myung Kim, Suk-Kyung Lim","doi":"10.1089/fpd.2024.0168","DOIUrl":"10.1089/fpd.2024.0168","url":null,"abstract":"<p><p>Antimicrobial-resistant bacterial contamination of meat poses a significant global public health risk. We aimed to determine antimicrobial resistance profiles and trends of <i>Escherichia coli</i> recovered from carcasses of healthy food-producing animals in South Korea during 2010-2023. In total, 4748 <i>E. coli</i> isolates obtained from cattle (<i>n</i> = 1582), pigs (<i>n</i> = 1572), and chickens (<i>n</i> = 1594) were assessed for susceptibility to 12 antimicrobials. Antimicrobial resistance was different among samples. Overall, antimicrobial resistance was high in pigs and chicken carcasses. More than about 80% of isolates from pigs and chickens exhibited resistance to one or more antimicrobials. Among the tested antimicrobials, resistance to ampicillin, chloramphenicol, streptomycin, and tetracycline was significantly higher in pigs and chickens compared with cattle (<i>p</i> < 0.05). Moreover, chicken isolates showed much higher resistance to nalidixic acid and ciprofloxacin than other samples. Resistance to critically important antimicrobials, colistin, remained less than about 1%, while resistance to ceftiofur showed increased trends in pig and chicken samples. Higher multidrug-resistant (MDR) isolates were identified in chickens and pigs compared with cattle (<i>p</i> < 0.05). Furthermore, most MDR patterns include streptomycin and tetracycline resistance. MDR <i>E. coli</i> contaminating meat during slaughter can be transmitted to humans via the food chain. Thus, prudent use of antimicrobials and proper hygienic practices are urgently needed to reduce the risk of transmission.</p>","PeriodicalId":12333,"journal":{"name":"Foodborne pathogens and disease","volume":" ","pages":""},"PeriodicalIF":1.9,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143022791","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}