Abundance and prevalence of ESBL coding genes in patients undergoing first line eradication therapy for Helicobacter pylori
The spread of extended-spectrum beta-lactamases (ESBLs) in nosocomial and community-acquired enterobacteria is an important challenge for clinicians due to the limited therapeutic options for infections that are caused by these organisms. Here, we developed a panel of ESBL coding genes, evaluated th...
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| creator | Gudra, Dita Silamikelis, Ivars Pjalkovskis, Janis Danenberga, Ilva Pupola, Darta Skenders, Girts Ustinova, Maija Megnis, Kaspars Leja, Marcis Vangravs, Reinis Fridmanis, Davids |
| description | The spread of extended-spectrum beta-lactamases (ESBLs) in nosocomial and community-acquired enterobacteria is an important challenge for clinicians due to the limited therapeutic options for infections that are caused by these organisms. Here, we developed a panel of ESBL coding genes, evaluated the abundance and prevalence of ESBL encoding genes in patients undergoing H. pylori eradication therapy, and summarized the effects of eradication therapy on functional profiles of the gut microbiome. To assess the repertoire of known beta lactamase (BL) genes, they were divided into clusters according to their evolutionary relation. Primers were designed for amplification of cluster marker regions, and the efficiency of this amplification panel was assessed in 120 fecal samples acquired from 60 patients undergoing H. pylori eradication therapy. In addition, fecal samples from an additional 30 patients were used to validate the detection efficiency of the developed ESBL panel. The presence for majority of targeted clusters was confirmed by NGS of amplification products. Metagenomic sequencing revealed that the abundance of ESBL genes within the pool of microorganisms was very low. The global relative abundances of the ESBL-coding gene clusters did not differ significantly among treatment states. However, at the level of each cluster, classical ESBL producers such as Klebsiella sp. for blaOXY (p = 0.0076), Acinetobacter sp. for blaADC (p = 0.02297) and others, differed significantly with a tendency to decrease compared to the pre- and post-eradication states. Only 13 clusters were common across all three datasets, suggesting a patient-specific distribution profile of ESBL-coding genes. The number of AMR genes detected in the post-eradication state was higher than that in the pre-eradication state, which could be attributed, at least in part, to the therapy. This study demonstrated that the ESBL screening panel was effective in targeting ESBL-coding gene clusters from bacterial DNA and that minor differences exist in the abundance and prevalence of ESBL-coding gene levels before and after eradication therapy. |
| doi_str_mv | 10.1371/journal.pone.0289879 |
| format | Article |
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Here, we developed a panel of ESBL coding genes, evaluated the abundance and prevalence of ESBL encoding genes in patients undergoing H. pylori eradication therapy, and summarized the effects of eradication therapy on functional profiles of the gut microbiome. To assess the repertoire of known beta lactamase (BL) genes, they were divided into clusters according to their evolutionary relation. Primers were designed for amplification of cluster marker regions, and the efficiency of this amplification panel was assessed in 120 fecal samples acquired from 60 patients undergoing H. pylori eradication therapy. In addition, fecal samples from an additional 30 patients were used to validate the detection efficiency of the developed ESBL panel. The presence for majority of targeted clusters was confirmed by NGS of amplification products. Metagenomic sequencing revealed that the abundance of ESBL genes within the pool of microorganisms was very low. The global relative abundances of the ESBL-coding gene clusters did not differ significantly among treatment states. However, at the level of each cluster, classical ESBL producers such as Klebsiella sp. for blaOXY (p = 0.0076), Acinetobacter sp. for blaADC (p = 0.02297) and others, differed significantly with a tendency to decrease compared to the pre- and post-eradication states. Only 13 clusters were common across all three datasets, suggesting a patient-specific distribution profile of ESBL-coding genes. The number of AMR genes detected in the post-eradication state was higher than that in the pre-eradication state, which could be attributed, at least in part, to the therapy. This study demonstrated that the ESBL screening panel was effective in targeting ESBL-coding gene clusters from bacterial DNA and that minor differences exist in the abundance and prevalence of ESBL-coding gene levels before and after eradication therapy.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0289879</identifier><identifier>PMID: 37561723</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abundance ; Amplification ; Anti-infective agents ; Antibiotics ; Antimicrobial agents ; Bacteria ; Bacterial infections ; Beta lactamases ; Biology and Life Sciences ; Complications and side effects ; Deoxyribonucleic acid ; Developing countries ; Diagnosis ; Disease prevention ; DNA ; Drug resistance ; Enzymes ; Eradication ; Feces ; Gene clusters ; Genes ; Genetic aspects ; Health aspects ; Helicobacter infections ; Helicobacter pylori ; Infection ; Infections ; Intestinal microflora ; Klebsiella ; LDCs ; Medicine and Health Sciences ; Metagenomics ; Metronidazole ; Microbiomes ; Microorganisms ; Nosocomial infection ; Patient outcomes ; Patients ; Research and analysis methods ; Sensors ; Therapy ; Type 2 diabetes ; Urogenital system ; Viral infections ; β Lactamase</subject><ispartof>PloS one, 2023-08, Vol.18 (8), p.e0289879-e0289879</ispartof><rights>Copyright: © 2023 Gudra et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Gudra et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Gudra et al 2023 Gudra et al</rights><rights>2023 Gudra et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c576t-bc66e329b52390e6cffe24b419216c8248792bb19b5142e484c36dd341a8f8ef3</cites><orcidid>0000-0002-8514-5991 ; 0000-0002-2587-9272 ; 0000-0002-9446-4521</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414638/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414638/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37561723$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gudra, Dita</creatorcontrib><creatorcontrib>Silamikelis, Ivars</creatorcontrib><creatorcontrib>Pjalkovskis, Janis</creatorcontrib><creatorcontrib>Danenberga, Ilva</creatorcontrib><creatorcontrib>Pupola, Darta</creatorcontrib><creatorcontrib>Skenders, Girts</creatorcontrib><creatorcontrib>Ustinova, Maija</creatorcontrib><creatorcontrib>Megnis, Kaspars</creatorcontrib><creatorcontrib>Leja, Marcis</creatorcontrib><creatorcontrib>Vangravs, Reinis</creatorcontrib><creatorcontrib>Fridmanis, Davids</creatorcontrib><title>Abundance and prevalence of ESBL coding genes in patients undergoing first line eradication therapy for Helicobacter pylori</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The spread of extended-spectrum beta-lactamases (ESBLs) in nosocomial and community-acquired enterobacteria is an important challenge for clinicians due to the limited therapeutic options for infections that are caused by these organisms. 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The global relative abundances of the ESBL-coding gene clusters did not differ significantly among treatment states. However, at the level of each cluster, classical ESBL producers such as Klebsiella sp. for blaOXY (p = 0.0076), Acinetobacter sp. for blaADC (p = 0.02297) and others, differed significantly with a tendency to decrease compared to the pre- and post-eradication states. Only 13 clusters were common across all three datasets, suggesting a patient-specific distribution profile of ESBL-coding genes. The number of AMR genes detected in the post-eradication state was higher than that in the pre-eradication state, which could be attributed, at least in part, to the therapy. This study demonstrated that the ESBL screening panel was effective in targeting ESBL-coding gene clusters from bacterial DNA and that minor differences exist in the abundance and prevalence of ESBL-coding gene levels before and after eradication therapy.</description><subject>Abundance</subject><subject>Amplification</subject><subject>Anti-infective agents</subject><subject>Antibiotics</subject><subject>Antimicrobial agents</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Beta lactamases</subject><subject>Biology and Life Sciences</subject><subject>Complications and side effects</subject><subject>Deoxyribonucleic acid</subject><subject>Developing countries</subject><subject>Diagnosis</subject><subject>Disease prevention</subject><subject>DNA</subject><subject>Drug resistance</subject><subject>Enzymes</subject><subject>Eradication</subject><subject>Feces</subject><subject>Gene clusters</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Helicobacter infections</subject><subject>Helicobacter pylori</subject><subject>Infection</subject><subject>Infections</subject><subject>Intestinal microflora</subject><subject>Klebsiella</subject><subject>LDCs</subject><subject>Medicine and Health Sciences</subject><subject>Metagenomics</subject><subject>Metronidazole</subject><subject>Microbiomes</subject><subject>Microorganisms</subject><subject>Nosocomial infection</subject><subject>Patient outcomes</subject><subject>Patients</subject><subject>Research and analysis methods</subject><subject>Sensors</subject><subject>Therapy</subject><subject>Type 2 diabetes</subject><subject>Urogenital system</subject><subject>Viral infections</subject><subject>β 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and prevalence of ESBL coding genes in patients undergoing first line eradication therapy for Helicobacter pylori</title><author>Gudra, Dita ; Silamikelis, Ivars ; Pjalkovskis, Janis ; Danenberga, Ilva ; Pupola, Darta ; Skenders, Girts ; Ustinova, Maija ; Megnis, Kaspars ; Leja, Marcis ; Vangravs, Reinis ; Fridmanis, Davids</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c576t-bc66e329b52390e6cffe24b419216c8248792bb19b5142e484c36dd341a8f8ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Abundance</topic><topic>Amplification</topic><topic>Anti-infective agents</topic><topic>Antibiotics</topic><topic>Antimicrobial agents</topic><topic>Bacteria</topic><topic>Bacterial infections</topic><topic>Beta lactamases</topic><topic>Biology and Life Sciences</topic><topic>Complications and side effects</topic><topic>Deoxyribonucleic acid</topic><topic>Developing 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challenge for clinicians due to the limited therapeutic options for infections that are caused by these organisms. Here, we developed a panel of ESBL coding genes, evaluated the abundance and prevalence of ESBL encoding genes in patients undergoing H. pylori eradication therapy, and summarized the effects of eradication therapy on functional profiles of the gut microbiome. To assess the repertoire of known beta lactamase (BL) genes, they were divided into clusters according to their evolutionary relation. Primers were designed for amplification of cluster marker regions, and the efficiency of this amplification panel was assessed in 120 fecal samples acquired from 60 patients undergoing H. pylori eradication therapy. In addition, fecal samples from an additional 30 patients were used to validate the detection efficiency of the developed ESBL panel. The presence for majority of targeted clusters was confirmed by NGS of amplification products. Metagenomic sequencing revealed that the abundance of ESBL genes within the pool of microorganisms was very low. The global relative abundances of the ESBL-coding gene clusters did not differ significantly among treatment states. However, at the level of each cluster, classical ESBL producers such as Klebsiella sp. for blaOXY (p = 0.0076), Acinetobacter sp. for blaADC (p = 0.02297) and others, differed significantly with a tendency to decrease compared to the pre- and post-eradication states. Only 13 clusters were common across all three datasets, suggesting a patient-specific distribution profile of ESBL-coding genes. The number of AMR genes detected in the post-eradication state was higher than that in the pre-eradication state, which could be attributed, at least in part, to the therapy. This study demonstrated that the ESBL screening panel was effective in targeting ESBL-coding gene clusters from bacterial DNA and that minor differences exist in the abundance and prevalence of ESBL-coding gene levels before and after eradication therapy.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37561723</pmid><doi>10.1371/journal.pone.0289879</doi><tpages>e0289879</tpages><orcidid>https://orcid.org/0000-0002-8514-5991</orcidid><orcidid>https://orcid.org/0000-0002-2587-9272</orcidid><orcidid>https://orcid.org/0000-0002-9446-4521</orcidid><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2848827180 |
| source | DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Abundance Amplification Anti-infective agents Antibiotics Antimicrobial agents Bacteria Bacterial infections Beta lactamases Biology and Life Sciences Complications and side effects Deoxyribonucleic acid Developing countries Diagnosis Disease prevention DNA Drug resistance Enzymes Eradication Feces Gene clusters Genes Genetic aspects Health aspects Helicobacter infections Helicobacter pylori Infection Infections Intestinal microflora Klebsiella LDCs Medicine and Health Sciences Metagenomics Metronidazole Microbiomes Microorganisms Nosocomial infection Patient outcomes Patients Research and analysis methods Sensors Therapy Type 2 diabetes Urogenital system Viral infections β Lactamase |
| title | Abundance and prevalence of ESBL coding genes in patients undergoing first line eradication therapy for Helicobacter pylori |
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