Characterization of Bacterial and Fungal Microbiome in Children with Hirschsprung Disease with and without a History of Enterocolitis: A Multicenter Study
Development of potentially life-threatening enterocolitis is the most frequent complication in children with Hirschsprung disease (HSCR), even after definitive corrective surgery. Intestinal microbiota likely contribute to the etiology of enterocolitis, so the aim of this study was to compare the fe...
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| Veröffentlicht in: | PloS one 2015-04, Vol.10 (4), p.e0124172-e0124172 |
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| creator | Frykman, Philip K Nordenskjöld, Agneta Kawaguchi, Akemi Hui, Thomas T Granström, Anna L Cheng, Zhi Tang, Jie Underhill, David M Iliev, Iliyan Funari, Vince A Wester, Tomas |
| description | Development of potentially life-threatening enterocolitis is the most frequent complication in children with Hirschsprung disease (HSCR), even after definitive corrective surgery. Intestinal microbiota likely contribute to the etiology of enterocolitis, so the aim of this study was to compare the fecal bacterial and fungal communities of children who developed Hirschsprung-associated enterocolitis (HAEC) with HSCR patients who had never had enterocolitis. Eighteen Hirschsprung patients who had completed definitive surgery were enrolled: 9 had a history of HAEC and 9 did not. Fecal DNA was isolated and 16S and ITS-1 regions sequenced using Next Generation Sequencing and data analysis for species identification. The HAEC group bacterial composition showed a modest reduction in Firmicutes and Verrucomicrobia with increased Bacteroidetes and Proteobacteria compared with the HSCR group. In contrast, the fecal fungi composition of the HAEC group showed marked reduction in diversity with increased Candida sp., and reduced Malassezia and Saccharomyces sp. compared with the HSCR group. The most striking finding within the HAEC group is that the Candida genus segregated into "high burden" patients with 97.8% C. albicans and 2.2% C. tropicalis compared with "low burden" patients 26.8% C. albicans and 73% C. tropicalis. Interestingly even the low burden HAEC group had altered Candida community structure with just two species compared to more diverse Candida populations in the HSCR patients. This is the first study to identify Candida sp. as potentially playing a role in HAEC either as expanded commensal species as a consequence of enterocolitis (or treatment), or possibly as pathobioants contributing to the pathogenesis of HAEC. These findings suggest a dysbiosis in the gut microbial ecosystem of HAEC patients, such that there may be dominance of fungi and bacteria predisposing patients to development of HAEC. |
| doi_str_mv | 10.1371/journal.pone.0124172 |
| format | Article |
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Intestinal microbiota likely contribute to the etiology of enterocolitis, so the aim of this study was to compare the fecal bacterial and fungal communities of children who developed Hirschsprung-associated enterocolitis (HAEC) with HSCR patients who had never had enterocolitis. Eighteen Hirschsprung patients who had completed definitive surgery were enrolled: 9 had a history of HAEC and 9 did not. Fecal DNA was isolated and 16S and ITS-1 regions sequenced using Next Generation Sequencing and data analysis for species identification. The HAEC group bacterial composition showed a modest reduction in Firmicutes and Verrucomicrobia with increased Bacteroidetes and Proteobacteria compared with the HSCR group. In contrast, the fecal fungi composition of the HAEC group showed marked reduction in diversity with increased Candida sp., and reduced Malassezia and Saccharomyces sp. compared with the HSCR group. The most striking finding within the HAEC group is that the Candida genus segregated into "high burden" patients with 97.8% C. albicans and 2.2% C. tropicalis compared with "low burden" patients 26.8% C. albicans and 73% C. tropicalis. Interestingly even the low burden HAEC group had altered Candida community structure with just two species compared to more diverse Candida populations in the HSCR patients. This is the first study to identify Candida sp. as potentially playing a role in HAEC either as expanded commensal species as a consequence of enterocolitis (or treatment), or possibly as pathobioants contributing to the pathogenesis of HAEC. These findings suggest a dysbiosis in the gut microbial ecosystem of HAEC patients, such that there may be dominance of fungi and bacteria predisposing patients to development of HAEC.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0124172</identifier><identifier>PMID: 25909773</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject><![CDATA[Analysis ; Antibiotics ; Bacteria ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteroidetes - genetics ; Bacteroidetes - isolation & purification ; Candida - classification ; Candida - genetics ; Candida - isolation & purification ; Candida albicans ; Child ; Child, Preschool ; Children ; Children & youth ; Childrens health ; Collaboration ; Colon ; Community structure ; Composition ; Data analysis ; Data processing ; Deoxyribonucleic acid ; Development and progression ; Disease Susceptibility ; DNA ; DNA, Bacterial - genetics ; DNA, Bacterial - isolation & purification ; DNA, Fungal - genetics ; DNA, Fungal - isolation & purification ; Dysbacteriosis ; Ecosystems ; Enterocolitis ; Enterocolitis - complications ; Enterocolitis - etiology ; Enterocolitis - microbiology ; Etiology ; Family medical history ; Feces ; Female ; Firmicutes - genetics ; Firmicutes - isolation & purification ; Fungi ; Fungi - genetics ; Fungi - isolation & purification ; Gastroenterology ; Gastrointestinal Microbiome - genetics ; Genomics ; High-Throughput Nucleotide Sequencing ; Hirschsprung Disease - complications ; Hirschsprung Disease - microbiology ; Hirschsprung's disease ; Hospitals ; Humans ; Infant ; Inflammatory bowel disease ; Intestinal microflora ; Intestine ; Laboratories ; Lindgren, Astrid (1907-2002) ; Male ; Medical research ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Next-generation sequencing ; Nucleotide sequence ; Ostomy ; Pathogenesis ; Patients ; Pediatrics ; Reduction ; Sequence Analysis, DNA ; Species ; Surgery ; Womens health]]></subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0124172-e0124172</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Frykman 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 Frykman et al 2015 Frykman et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c623t-3dd4a598d79f3f72e14047e031b9b3005c4c1c8c9b1cdaddf6d0b128fa057c543</citedby><cites>FETCH-LOGICAL-c623t-3dd4a598d79f3f72e14047e031b9b3005c4c1c8c9b1cdaddf6d0b128fa057c543</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/PMC4409062/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4409062/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25909773$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:131245011$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Frykman, Philip K</creatorcontrib><creatorcontrib>Nordenskjöld, Agneta</creatorcontrib><creatorcontrib>Kawaguchi, Akemi</creatorcontrib><creatorcontrib>Hui, Thomas T</creatorcontrib><creatorcontrib>Granström, Anna L</creatorcontrib><creatorcontrib>Cheng, Zhi</creatorcontrib><creatorcontrib>Tang, Jie</creatorcontrib><creatorcontrib>Underhill, David M</creatorcontrib><creatorcontrib>Iliev, Iliyan</creatorcontrib><creatorcontrib>Funari, Vince A</creatorcontrib><creatorcontrib>Wester, Tomas</creatorcontrib><creatorcontrib>HAEC Collaborative Research Group (HCRG)</creatorcontrib><title>Characterization of Bacterial and Fungal Microbiome in Children with Hirschsprung Disease with and without a History of Enterocolitis: A Multicenter Study</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Development of potentially life-threatening enterocolitis is the most frequent complication in children with Hirschsprung disease (HSCR), even after definitive corrective surgery. Intestinal microbiota likely contribute to the etiology of enterocolitis, so the aim of this study was to compare the fecal bacterial and fungal communities of children who developed Hirschsprung-associated enterocolitis (HAEC) with HSCR patients who had never had enterocolitis. Eighteen Hirschsprung patients who had completed definitive surgery were enrolled: 9 had a history of HAEC and 9 did not. Fecal DNA was isolated and 16S and ITS-1 regions sequenced using Next Generation Sequencing and data analysis for species identification. The HAEC group bacterial composition showed a modest reduction in Firmicutes and Verrucomicrobia with increased Bacteroidetes and Proteobacteria compared with the HSCR group. In contrast, the fecal fungi composition of the HAEC group showed marked reduction in diversity with increased Candida sp., and reduced Malassezia and Saccharomyces sp. compared with the HSCR group. The most striking finding within the HAEC group is that the Candida genus segregated into "high burden" patients with 97.8% C. albicans and 2.2% C. tropicalis compared with "low burden" patients 26.8% C. albicans and 73% C. tropicalis. Interestingly even the low burden HAEC group had altered Candida community structure with just two species compared to more diverse Candida populations in the HSCR patients. This is the first study to identify Candida sp. as potentially playing a role in HAEC either as expanded commensal species as a consequence of enterocolitis (or treatment), or possibly as pathobioants contributing to the pathogenesis of HAEC. These findings suggest a dysbiosis in the gut microbial ecosystem of HAEC patients, such that there may be dominance of fungi and bacteria predisposing patients to development of HAEC.</description><subject>Analysis</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteroidetes - genetics</subject><subject>Bacteroidetes - isolation & purification</subject><subject>Candida - classification</subject><subject>Candida - genetics</subject><subject>Candida - isolation & purification</subject><subject>Candida albicans</subject><subject>Child</subject><subject>Child, Preschool</subject><subject>Children</subject><subject>Children & youth</subject><subject>Childrens health</subject><subject>Collaboration</subject><subject>Colon</subject><subject>Community structure</subject><subject>Composition</subject><subject>Data analysis</subject><subject>Data processing</subject><subject>Deoxyribonucleic acid</subject><subject>Development and progression</subject><subject>Disease Susceptibility</subject><subject>DNA</subject><subject>DNA, Bacterial - genetics</subject><subject>DNA, Bacterial - isolation & purification</subject><subject>DNA, Fungal - genetics</subject><subject>DNA, Fungal - isolation & purification</subject><subject>Dysbacteriosis</subject><subject>Ecosystems</subject><subject>Enterocolitis</subject><subject>Enterocolitis - complications</subject><subject>Enterocolitis - etiology</subject><subject>Enterocolitis - microbiology</subject><subject>Etiology</subject><subject>Family medical history</subject><subject>Feces</subject><subject>Female</subject><subject>Firmicutes - genetics</subject><subject>Firmicutes - isolation & purification</subject><subject>Fungi</subject><subject>Fungi - genetics</subject><subject>Fungi - isolation & purification</subject><subject>Gastroenterology</subject><subject>Gastrointestinal Microbiome - genetics</subject><subject>Genomics</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Hirschsprung Disease - complications</subject><subject>Hirschsprung Disease - microbiology</subject><subject>Hirschsprung's disease</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Infant</subject><subject>Inflammatory bowel disease</subject><subject>Intestinal microflora</subject><subject>Intestine</subject><subject>Laboratories</subject><subject>Lindgren, Astrid (1907-2002)</subject><subject>Male</subject><subject>Medical research</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Next-generation sequencing</subject><subject>Nucleotide sequence</subject><subject>Ostomy</subject><subject>Pathogenesis</subject><subject>Patients</subject><subject>Pediatrics</subject><subject>Reduction</subject><subject>Sequence Analysis, 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Medical Research Collection</collection><collection>ProQuest One Academic Middle East (New)</collection><collection>ProQuest One Health & Nursing</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Applied & Life Sciences</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</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>Frykman, Philip K</au><au>Nordenskjöld, Agneta</au><au>Kawaguchi, Akemi</au><au>Hui, Thomas T</au><au>Granström, Anna L</au><au>Cheng, Zhi</au><au>Tang, Jie</au><au>Underhill, David M</au><au>Iliev, Iliyan</au><au>Funari, Vince A</au><au>Wester, Tomas</au><aucorp>HAEC Collaborative Research Group (HCRG)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of Bacterial and Fungal Microbiome in Children with Hirschsprung Disease with and without a History of Enterocolitis: A Multicenter Study</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-24</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0124172</spage><epage>e0124172</epage><pages>e0124172-e0124172</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Development of potentially life-threatening enterocolitis is the most frequent complication in children with Hirschsprung disease (HSCR), even after definitive corrective surgery. Intestinal microbiota likely contribute to the etiology of enterocolitis, so the aim of this study was to compare the fecal bacterial and fungal communities of children who developed Hirschsprung-associated enterocolitis (HAEC) with HSCR patients who had never had enterocolitis. Eighteen Hirschsprung patients who had completed definitive surgery were enrolled: 9 had a history of HAEC and 9 did not. Fecal DNA was isolated and 16S and ITS-1 regions sequenced using Next Generation Sequencing and data analysis for species identification. The HAEC group bacterial composition showed a modest reduction in Firmicutes and Verrucomicrobia with increased Bacteroidetes and Proteobacteria compared with the HSCR group. In contrast, the fecal fungi composition of the HAEC group showed marked reduction in diversity with increased Candida sp., and reduced Malassezia and Saccharomyces sp. compared with the HSCR group. The most striking finding within the HAEC group is that the Candida genus segregated into "high burden" patients with 97.8% C. albicans and 2.2% C. tropicalis compared with "low burden" patients 26.8% C. albicans and 73% C. tropicalis. Interestingly even the low burden HAEC group had altered Candida community structure with just two species compared to more diverse Candida populations in the HSCR patients. This is the first study to identify Candida sp. as potentially playing a role in HAEC either as expanded commensal species as a consequence of enterocolitis (or treatment), or possibly as pathobioants contributing to the pathogenesis of HAEC. These findings suggest a dysbiosis in the gut microbial ecosystem of HAEC patients, such that there may be dominance of fungi and bacteria predisposing patients to development of HAEC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25909773</pmid><doi>10.1371/journal.pone.0124172</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-04, Vol.10 (4), p.e0124172-e0124172 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1676150142 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SWEPUB Freely available online; Free Full-Text Journals in Chemistry |
| subjects | Analysis Antibiotics Bacteria Bacteria - genetics Bacteria - isolation & purification Bacteroidetes - genetics Bacteroidetes - isolation & purification Candida - classification Candida - genetics Candida - isolation & purification Candida albicans Child Child, Preschool Children Children & youth Childrens health Collaboration Colon Community structure Composition Data analysis Data processing Deoxyribonucleic acid Development and progression Disease Susceptibility DNA DNA, Bacterial - genetics DNA, Bacterial - isolation & purification DNA, Fungal - genetics DNA, Fungal - isolation & purification Dysbacteriosis Ecosystems Enterocolitis Enterocolitis - complications Enterocolitis - etiology Enterocolitis - microbiology Etiology Family medical history Feces Female Firmicutes - genetics Firmicutes - isolation & purification Fungi Fungi - genetics Fungi - isolation & purification Gastroenterology Gastrointestinal Microbiome - genetics Genomics High-Throughput Nucleotide Sequencing Hirschsprung Disease - complications Hirschsprung Disease - microbiology Hirschsprung's disease Hospitals Humans Infant Inflammatory bowel disease Intestinal microflora Intestine Laboratories Lindgren, Astrid (1907-2002) Male Medical research Microbiota Microbiota (Symbiotic organisms) Microorganisms Next-generation sequencing Nucleotide sequence Ostomy Pathogenesis Patients Pediatrics Reduction Sequence Analysis, DNA Species Surgery Womens health |
| title | Characterization of Bacterial and Fungal Microbiome in Children with Hirschsprung Disease with and without a History of Enterocolitis: A Multicenter Study |
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