Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study
Necrotizing enterocolitis (NEC) is an inflammatory disease of the newborn bowel, primarily affecting premature infants. Early intestinal colonization has been implicated in the pathogenesis of NEC. The objective of this prospective case-control study was to evaluate differences in the intestinal mic...
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| description | Necrotizing enterocolitis (NEC) is an inflammatory disease of the newborn bowel, primarily affecting premature infants. Early intestinal colonization has been implicated in the pathogenesis of NEC. The objective of this prospective case-control study was to evaluate differences in the intestinal microbiota between infants who developed NEC and unaffected controls prior to disease onset. We conducted longitudinal analysis of the 16S rRNA genes of 312 samples obtained from 12 NEC cases and 26 age-matched controls with a median frequency of 7 samples per subject and median sampling interval of 3 days. We found that the microbiome undergoes dynamic development during the first two months of life with day of life being the major factor contributing to the colonization process. Depending on when the infant was diagnosed with NEC (i.e. early vs. late onset), the pattern of microbial progression was different for cases and controls. The difference in the microbiota was most overt in early onset NEC cases and controls. In proximity to NEC onset, the abundances of Clostridium sensu stricto from Clostridia class were significantly higher in early onset NEC subjects comparing to controls. In late onset NEC, Escherichia/Shigella among Gammaproteobacteria, showed an increasing pattern prior to disease onset, and was significantly higher in cases than controls six days before NEC onset. Cronobacter from Gammaproteobacteria was also significantly higher in late onset NEC cases than controls 1-3 days prior to NEC onset. Thus, the specific infectious agent associated with NEC may vary by the age of infant at disease onset. We found that intravenously administered antibiotics may have an impact on the microbial diversity present in fecal material. Longitudinal analysis at multiple time points was an important strategy utilized in this study, allowing us to appreciate the dynamics of the premature infant intestinal microbiome while approaching NEC at various points. |
| doi_str_mv | 10.1371/journal.pone.0118632 |
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Early intestinal colonization has been implicated in the pathogenesis of NEC. The objective of this prospective case-control study was to evaluate differences in the intestinal microbiota between infants who developed NEC and unaffected controls prior to disease onset. We conducted longitudinal analysis of the 16S rRNA genes of 312 samples obtained from 12 NEC cases and 26 age-matched controls with a median frequency of 7 samples per subject and median sampling interval of 3 days. We found that the microbiome undergoes dynamic development during the first two months of life with day of life being the major factor contributing to the colonization process. Depending on when the infant was diagnosed with NEC (i.e. early vs. late onset), the pattern of microbial progression was different for cases and controls. The difference in the microbiota was most overt in early onset NEC cases and controls. In proximity to NEC onset, the abundances of Clostridium sensu stricto from Clostridia class were significantly higher in early onset NEC subjects comparing to controls. In late onset NEC, Escherichia/Shigella among Gammaproteobacteria, showed an increasing pattern prior to disease onset, and was significantly higher in cases than controls six days before NEC onset. Cronobacter from Gammaproteobacteria was also significantly higher in late onset NEC cases than controls 1-3 days prior to NEC onset. Thus, the specific infectious agent associated with NEC may vary by the age of infant at disease onset. We found that intravenously administered antibiotics may have an impact on the microbial diversity present in fecal material. Longitudinal analysis at multiple time points was an important strategy utilized in this study, allowing us to appreciate the dynamics of the premature infant intestinal microbiome while approaching NEC at various points.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0118632</identifier><identifier>PMID: 25741698</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Antibiotics ; Babies ; Case studies ; Case-Control Studies ; Colonization ; Cronobacter sakazakii ; Disease control ; Enterocolitis ; Enterocolitis, Necrotizing - microbiology ; Feces ; Feces - microbiology ; Female ; Gastrointestinal diseases ; Gastrointestinal Microbiome ; Genomes ; Health aspects ; Hospitals ; Humans ; Infant ; Infant, Newborn ; Infant, Premature ; Infant, Premature, Diseases - microbiology ; Infants ; Inflammatory diseases ; Intestinal microflora ; Intestine ; Intestines - microbiology ; Laboratories ; Longitudinal Studies ; Male ; Medicine ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Mortality ; Necrosis ; Necrotizing enterocolitis ; Newborn babies ; Pathogenesis ; Pediatrics ; Premature infants ; Risk factors ; RNA, Ribosomal, 16S ; Rodents ; rRNA 16S</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0118632-e0118632</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Zhou 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>2015 Zhou et al 2015 Zhou et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-a7eaa5f93a4aaf9a68ddb9a87bef197577516bd9bd9f4d11b3bf4b7d7a31db133</citedby><cites>FETCH-LOGICAL-c692t-a7eaa5f93a4aaf9a68ddb9a87bef197577516bd9bd9f4d11b3bf4b7d7a31db133</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4351051/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4351051/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2106,2932,23875,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25741698$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Lightfoot, David A</contributor><creatorcontrib>Zhou, Yanjiao</creatorcontrib><creatorcontrib>Shan, Gururaj</creatorcontrib><creatorcontrib>Sodergren, Erica</creatorcontrib><creatorcontrib>Weinstock, George</creatorcontrib><creatorcontrib>Walker, W Allan</creatorcontrib><creatorcontrib>Gregory, Katherine E</creatorcontrib><title>Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Necrotizing enterocolitis (NEC) is an inflammatory disease of the newborn bowel, primarily affecting premature infants. Early intestinal colonization has been implicated in the pathogenesis of NEC. The objective of this prospective case-control study was to evaluate differences in the intestinal microbiota between infants who developed NEC and unaffected controls prior to disease onset. We conducted longitudinal analysis of the 16S rRNA genes of 312 samples obtained from 12 NEC cases and 26 age-matched controls with a median frequency of 7 samples per subject and median sampling interval of 3 days. We found that the microbiome undergoes dynamic development during the first two months of life with day of life being the major factor contributing to the colonization process. Depending on when the infant was diagnosed with NEC (i.e. early vs. late onset), the pattern of microbial progression was different for cases and controls. The difference in the microbiota was most overt in early onset NEC cases and controls. In proximity to NEC onset, the abundances of Clostridium sensu stricto from Clostridia class were significantly higher in early onset NEC subjects comparing to controls. In late onset NEC, Escherichia/Shigella among Gammaproteobacteria, showed an increasing pattern prior to disease onset, and was significantly higher in cases than controls six days before NEC onset. Cronobacter from Gammaproteobacteria was also significantly higher in late onset NEC cases than controls 1-3 days prior to NEC onset. Thus, the specific infectious agent associated with NEC may vary by the age of infant at disease onset. We found that intravenously administered antibiotics may have an impact on the microbial diversity present in fecal material. Longitudinal analysis at multiple time points was an important strategy utilized in this study, allowing us to appreciate the dynamics of the premature infant intestinal microbiome while approaching NEC at various points.</description><subject>Analysis</subject><subject>Antibiotics</subject><subject>Babies</subject><subject>Case studies</subject><subject>Case-Control Studies</subject><subject>Colonization</subject><subject>Cronobacter sakazakii</subject><subject>Disease control</subject><subject>Enterocolitis</subject><subject>Enterocolitis, Necrotizing - microbiology</subject><subject>Feces</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Gastrointestinal diseases</subject><subject>Gastrointestinal Microbiome</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Infant</subject><subject>Infant, Newborn</subject><subject>Infant, Premature</subject><subject>Infant, Premature, Diseases - microbiology</subject><subject>Infants</subject><subject>Inflammatory diseases</subject><subject>Intestinal microflora</subject><subject>Intestine</subject><subject>Intestines - microbiology</subject><subject>Laboratories</subject><subject>Longitudinal Studies</subject><subject>Male</subject><subject>Medicine</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Mortality</subject><subject>Necrosis</subject><subject>Necrotizing enterocolitis</subject><subject>Newborn babies</subject><subject>Pathogenesis</subject><subject>Pediatrics</subject><subject>Premature infants</subject><subject>Risk factors</subject><subject>RNA, Ribosomal, 16S</subject><subject>Rodents</subject><subject>rRNA 16S</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QLgujFjE3TJq0XwrL4MTCw4NdtOGmTToa2GZNUHPHHezrTXaayF9LSlNPnvKd5T04UPSXJklBO3mzt4Hpolzvbq2VCSMFoei86JyVNFyxN6P2T97PokffbJMlpwdjD6CzNeUZYWZxHf9a2b0wYaoNaMeBj742PrY7DRsU7pzoIg1Ox6TX0AZegfDiwnamclcZ2I2asi4ONe4WxYH6bvokVos5WtjXB-LcxxBV4tahsH5xtY48l94-jBxpar55M60X07cP7r1efFuvrj6ury_WiYmUaFsAVQK5LChmALoEVdS1LKLhUmpQ85zwnTNYl3jqrCZFU6kzymgMltSSUXkTPj7q71noxGecFYSwp04wVKRKrI1Fb2ArcTwduLywYcQhY1whwwVStEoxCRTgjteY00zSRTFaU1kUhKVqaSNR6N1UbZKfqCo1w0M5E5196sxGN_SkympMkJyjwahJw9seAfovO-Eq1LfTKDof_JjTNSzaiL_5B797dRDWAG8BWWqxbjaLiMkvLgvCUFEgt76DwqhX2Gk-ZNhifJbyeJYy9Vb9CA4P3YvXl8_-z19_n7MsTdqOgDRtv2yEY2_s5mB1BPHXeO6VvTSaJGIfkxg0xDomYhgTTnp026DbpZiroX34_EBE</recordid><startdate>20150305</startdate><enddate>20150305</enddate><creator>Zhou, Yanjiao</creator><creator>Shan, Gururaj</creator><creator>Sodergren, Erica</creator><creator>Weinstock, George</creator><creator>Walker, W Allan</creator><creator>Gregory, Katherine E</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150305</creationdate><title>Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study</title><author>Zhou, Yanjiao ; Shan, Gururaj ; Sodergren, Erica ; Weinstock, George ; Walker, W Allan ; Gregory, Katherine E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-a7eaa5f93a4aaf9a68ddb9a87bef197577516bd9bd9f4d11b3bf4b7d7a31db133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Analysis</topic><topic>Antibiotics</topic><topic>Babies</topic><topic>Case studies</topic><topic>Case-Control Studies</topic><topic>Colonization</topic><topic>Cronobacter sakazakii</topic><topic>Disease control</topic><topic>Enterocolitis</topic><topic>Enterocolitis, Necrotizing - microbiology</topic><topic>Feces</topic><topic>Feces - microbiology</topic><topic>Female</topic><topic>Gastrointestinal diseases</topic><topic>Gastrointestinal Microbiome</topic><topic>Genomes</topic><topic>Health aspects</topic><topic>Hospitals</topic><topic>Humans</topic><topic>Infant</topic><topic>Infant, Newborn</topic><topic>Infant, Premature</topic><topic>Infant, Premature, Diseases - microbiology</topic><topic>Infants</topic><topic>Inflammatory diseases</topic><topic>Intestinal microflora</topic><topic>Intestine</topic><topic>Intestines - microbiology</topic><topic>Laboratories</topic><topic>Longitudinal Studies</topic><topic>Male</topic><topic>Medicine</topic><topic>Microbiota</topic><topic>Microbiota (Symbiotic organisms)</topic><topic>Microorganisms</topic><topic>Mortality</topic><topic>Necrosis</topic><topic>Necrotizing enterocolitis</topic><topic>Newborn babies</topic><topic>Pathogenesis</topic><topic>Pediatrics</topic><topic>Premature infants</topic><topic>Risk factors</topic><topic>RNA, Ribosomal, 16S</topic><topic>Rodents</topic><topic>rRNA 16S</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhou, Yanjiao</creatorcontrib><creatorcontrib>Shan, Gururaj</creatorcontrib><creatorcontrib>Sodergren, Erica</creatorcontrib><creatorcontrib>Weinstock, George</creatorcontrib><creatorcontrib>Walker, W Allan</creatorcontrib><creatorcontrib>Gregory, Katherine E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhou, Yanjiao</au><au>Shan, Gururaj</au><au>Sodergren, Erica</au><au>Weinstock, George</au><au>Walker, W Allan</au><au>Gregory, Katherine E</au><au>Lightfoot, David A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-05</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0118632</spage><epage>e0118632</epage><pages>e0118632-e0118632</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Necrotizing enterocolitis (NEC) is an inflammatory disease of the newborn bowel, primarily affecting premature infants. Early intestinal colonization has been implicated in the pathogenesis of NEC. The objective of this prospective case-control study was to evaluate differences in the intestinal microbiota between infants who developed NEC and unaffected controls prior to disease onset. We conducted longitudinal analysis of the 16S rRNA genes of 312 samples obtained from 12 NEC cases and 26 age-matched controls with a median frequency of 7 samples per subject and median sampling interval of 3 days. We found that the microbiome undergoes dynamic development during the first two months of life with day of life being the major factor contributing to the colonization process. Depending on when the infant was diagnosed with NEC (i.e. early vs. late onset), the pattern of microbial progression was different for cases and controls. The difference in the microbiota was most overt in early onset NEC cases and controls. In proximity to NEC onset, the abundances of Clostridium sensu stricto from Clostridia class were significantly higher in early onset NEC subjects comparing to controls. In late onset NEC, Escherichia/Shigella among Gammaproteobacteria, showed an increasing pattern prior to disease onset, and was significantly higher in cases than controls six days before NEC onset. Cronobacter from Gammaproteobacteria was also significantly higher in late onset NEC cases than controls 1-3 days prior to NEC onset. Thus, the specific infectious agent associated with NEC may vary by the age of infant at disease onset. We found that intravenously administered antibiotics may have an impact on the microbial diversity present in fecal material. Longitudinal analysis at multiple time points was an important strategy utilized in this study, allowing us to appreciate the dynamics of the premature infant intestinal microbiome while approaching NEC at various points.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25741698</pmid><doi>10.1371/journal.pone.0118632</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Antibiotics Babies Case studies Case-Control Studies Colonization Cronobacter sakazakii Disease control Enterocolitis Enterocolitis, Necrotizing - microbiology Feces Feces - microbiology Female Gastrointestinal diseases Gastrointestinal Microbiome Genomes Health aspects Hospitals Humans Infant Infant, Newborn Infant, Premature Infant, Premature, Diseases - microbiology Infants Inflammatory diseases Intestinal microflora Intestine Intestines - microbiology Laboratories Longitudinal Studies Male Medicine Microbiota Microbiota (Symbiotic organisms) Microorganisms Mortality Necrosis Necrotizing enterocolitis Newborn babies Pathogenesis Pediatrics Premature infants Risk factors RNA, Ribosomal, 16S Rodents rRNA 16S |
| title | Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-03T09%3A41%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Longitudinal%20analysis%20of%20the%20premature%20infant%20intestinal%20microbiome%20prior%20to%20necrotizing%20enterocolitis:%20a%20case-control%20study&rft.jtitle=PloS%20one&rft.au=Zhou,%20Yanjiao&rft.date=2015-03-05&rft.volume=10&rft.issue=3&rft.spage=e0118632&rft.epage=e0118632&rft.pages=e0118632-e0118632&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0118632&rft_dat=%3Cgale_plos_%3EA429817218%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1660924682&rft_id=info:pmid/25741698&rft_galeid=A429817218&rft_doaj_id=oai_doaj_org_article_63ac1761df734f30b6bc33d88b31690b&rfr_iscdi=true |