Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery

The obesity pandemic in the obstetrical population plus increased frequency of Cesarean delivery (CD) has increased vulnerability to surgical site infection (SSI). Here we characterized the microbiome at the site of skin incision before and after CD. Skin and relevant surgical sites were sampled bef...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Scientific reports 2018-06, Vol.8 (1), p.8756-8, Article 8756
Hauptverfasser: Rood, Kara M., Buhimschi, Irina A., Jurcisek, Joseph A., Summerfield, Taryn L., Zhao, Guomao, Ackerman, William E., Wang, Weiwei, Rumpf, R. Wolfgang, Thung, Stephen F., Bakaletz, Lauren O., Buhimschi, Catalin S.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 8
container_issue 1
container_start_page 8756
container_title Scientific reports
container_volume 8
creator Rood, Kara M.
Buhimschi, Irina A.
Jurcisek, Joseph A.
Summerfield, Taryn L.
Zhao, Guomao
Ackerman, William E.
Wang, Weiwei
Rumpf, R. Wolfgang
Thung, Stephen F.
Bakaletz, Lauren O.
Buhimschi, Catalin S.
description The obesity pandemic in the obstetrical population plus increased frequency of Cesarean delivery (CD) has increased vulnerability to surgical site infection (SSI). Here we characterized the microbiome at the site of skin incision before and after CD. Skin and relevant surgical sites were sampled before and after surgical antisepsis from obese (n = 31) and non-obese (n = 27) pregnant women. We quantified bacterial biomass by qPCR, microbial community composition by 16sRNA sequencing, assigned operational taxonomic units, and stained skin biopsies from incision for bacteria and biofilms. In obese women, incision site harbors significantly higher bacterial biomass of lower diversity. Phylum Firmicutes predominated over Actinobacteria , with phylotypes Clostridales and Bacteroidales over commensal Staphylococcus and Propionbacterium spp. Skin dysbiosis increased post-surgical prep and at end of surgery. Biofilms were identified post-prep in the majority (73%) of skin biopsies. At end of surgery, incision had significant gains in bacterial DNA and diversity, and obese women shared more genera with vagina and surgeon’s glove in CD. Our findings suggest microbiota at incision differs between obese and non-obese pregnant women, and changes throughout CD. An interaction between vaginal and cutaneous dysbiosis at the incision site may explain the a priori increased risk for SSI among obese pregnant women.
doi_str_mv 10.1038/s41598-018-27134-5
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5993816</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2052589296</sourcerecordid><originalsourceid>FETCH-LOGICAL-c513t-c520b85f3ee7d3d2ba5d9e9cf8462be6d9dfb3d4fd83bde9e4dd5c4c28d029393</originalsourceid><addsrcrecordid>eNp9kU1PVDEUhhsjEYL8ARemiRs3F_s5025MyKhIgiFxNCRsmt72dCzcaaG9l4R_b4dBBBd20Y-c57yn57wIvaHkkBKuPlRBpVYdoapjc8pFJ1-gPUaE7Bhn7OWT-y46qPWStCWZFlS_QrtMKyXmmu-hi-VVTPhbdCX3MY8Wt9dZDxXweV5DwnbE32O9wiEXvJzKKjo74GUcAZ-kAG6MOeGjMELBC6i2gE34EwzxFsrda7QT7FDh4OHcRz-_fP6x-Nqdnh2fLI5OOycpH9vOSK9k4ABzzz3rrfQatAtKzFgPM6996LkXwSvee9AgvJdOOKY8YZprvo8-bnWvp34N3kEaix3MdYlrW-5MttE8j6T4y6zyrZFac0VnTeD9g0DJNxPU0axjdTAMNkGeqmFtcIrwudjUevcPepmnklp795RUmumNINtSbaq1FgiPn6HEbNwzW_dMc8_cu2dkS3r7tI3HlD9eNYBvgdpCaQXlb-3_yP4GCWmmXA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2052589296</pqid></control><display><type>article</type><title>Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery</title><source>Nature Free</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><source>Springer Nature OA Free Journals</source><creator>Rood, Kara M. ; Buhimschi, Irina A. ; Jurcisek, Joseph A. ; Summerfield, Taryn L. ; Zhao, Guomao ; Ackerman, William E. ; Wang, Weiwei ; Rumpf, R. Wolfgang ; Thung, Stephen F. ; Bakaletz, Lauren O. ; Buhimschi, Catalin S.</creator><creatorcontrib>Rood, Kara M. ; Buhimschi, Irina A. ; Jurcisek, Joseph A. ; Summerfield, Taryn L. ; Zhao, Guomao ; Ackerman, William E. ; Wang, Weiwei ; Rumpf, R. Wolfgang ; Thung, Stephen F. ; Bakaletz, Lauren O. ; Buhimschi, Catalin S.</creatorcontrib><description>The obesity pandemic in the obstetrical population plus increased frequency of Cesarean delivery (CD) has increased vulnerability to surgical site infection (SSI). Here we characterized the microbiome at the site of skin incision before and after CD. Skin and relevant surgical sites were sampled before and after surgical antisepsis from obese (n = 31) and non-obese (n = 27) pregnant women. We quantified bacterial biomass by qPCR, microbial community composition by 16sRNA sequencing, assigned operational taxonomic units, and stained skin biopsies from incision for bacteria and biofilms. In obese women, incision site harbors significantly higher bacterial biomass of lower diversity. Phylum Firmicutes predominated over Actinobacteria , with phylotypes Clostridales and Bacteroidales over commensal Staphylococcus and Propionbacterium spp. Skin dysbiosis increased post-surgical prep and at end of surgery. Biofilms were identified post-prep in the majority (73%) of skin biopsies. At end of surgery, incision had significant gains in bacterial DNA and diversity, and obese women shared more genera with vagina and surgeon’s glove in CD. Our findings suggest microbiota at incision differs between obese and non-obese pregnant women, and changes throughout CD. An interaction between vaginal and cutaneous dysbiosis at the incision site may explain the a priori increased risk for SSI among obese pregnant women.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-018-27134-5</identifier><identifier>PMID: 29884793</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/22 ; 38/23 ; 38/77 ; 45/41 ; 692/308/575 ; 692/420/254 ; 692/499 ; Bacteria ; Biofilms ; Biomass ; Biopsy ; Cesarean section ; Community composition ; Deoxyribonucleic acid ; DNA ; Dysbacteriosis ; Genera ; Humanities and Social Sciences ; Microbiomes ; Microbiota ; multidisciplinary ; Obesity ; Pandemics ; Pregnancy ; Science ; Science (multidisciplinary) ; Skin ; Surgery ; Surgical site infections ; Vagina</subject><ispartof>Scientific reports, 2018-06, Vol.8 (1), p.8756-8, Article 8756</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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><citedby>FETCH-LOGICAL-c513t-c520b85f3ee7d3d2ba5d9e9cf8462be6d9dfb3d4fd83bde9e4dd5c4c28d029393</citedby><cites>FETCH-LOGICAL-c513t-c520b85f3ee7d3d2ba5d9e9cf8462be6d9dfb3d4fd83bde9e4dd5c4c28d029393</cites><orcidid>0000-0002-8504-6715</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/PMC5993816/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5993816/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27903,27904,41099,42168,51554,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29884793$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rood, Kara M.</creatorcontrib><creatorcontrib>Buhimschi, Irina A.</creatorcontrib><creatorcontrib>Jurcisek, Joseph A.</creatorcontrib><creatorcontrib>Summerfield, Taryn L.</creatorcontrib><creatorcontrib>Zhao, Guomao</creatorcontrib><creatorcontrib>Ackerman, William E.</creatorcontrib><creatorcontrib>Wang, Weiwei</creatorcontrib><creatorcontrib>Rumpf, R. Wolfgang</creatorcontrib><creatorcontrib>Thung, Stephen F.</creatorcontrib><creatorcontrib>Bakaletz, Lauren O.</creatorcontrib><creatorcontrib>Buhimschi, Catalin S.</creatorcontrib><title>Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>The obesity pandemic in the obstetrical population plus increased frequency of Cesarean delivery (CD) has increased vulnerability to surgical site infection (SSI). Here we characterized the microbiome at the site of skin incision before and after CD. Skin and relevant surgical sites were sampled before and after surgical antisepsis from obese (n = 31) and non-obese (n = 27) pregnant women. We quantified bacterial biomass by qPCR, microbial community composition by 16sRNA sequencing, assigned operational taxonomic units, and stained skin biopsies from incision for bacteria and biofilms. In obese women, incision site harbors significantly higher bacterial biomass of lower diversity. Phylum Firmicutes predominated over Actinobacteria , with phylotypes Clostridales and Bacteroidales over commensal Staphylococcus and Propionbacterium spp. Skin dysbiosis increased post-surgical prep and at end of surgery. Biofilms were identified post-prep in the majority (73%) of skin biopsies. At end of surgery, incision had significant gains in bacterial DNA and diversity, and obese women shared more genera with vagina and surgeon’s glove in CD. Our findings suggest microbiota at incision differs between obese and non-obese pregnant women, and changes throughout CD. An interaction between vaginal and cutaneous dysbiosis at the incision site may explain the a priori increased risk for SSI among obese pregnant women.</description><subject>38/22</subject><subject>38/23</subject><subject>38/77</subject><subject>45/41</subject><subject>692/308/575</subject><subject>692/420/254</subject><subject>692/499</subject><subject>Bacteria</subject><subject>Biofilms</subject><subject>Biomass</subject><subject>Biopsy</subject><subject>Cesarean section</subject><subject>Community composition</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Dysbacteriosis</subject><subject>Genera</subject><subject>Humanities and Social Sciences</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>multidisciplinary</subject><subject>Obesity</subject><subject>Pandemics</subject><subject>Pregnancy</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Skin</subject><subject>Surgery</subject><subject>Surgical site infections</subject><subject>Vagina</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kU1PVDEUhhsjEYL8ARemiRs3F_s5025MyKhIgiFxNCRsmt72dCzcaaG9l4R_b4dBBBd20Y-c57yn57wIvaHkkBKuPlRBpVYdoapjc8pFJ1-gPUaE7Bhn7OWT-y46qPWStCWZFlS_QrtMKyXmmu-hi-VVTPhbdCX3MY8Wt9dZDxXweV5DwnbE32O9wiEXvJzKKjo74GUcAZ-kAG6MOeGjMELBC6i2gE34EwzxFsrda7QT7FDh4OHcRz-_fP6x-Nqdnh2fLI5OOycpH9vOSK9k4ABzzz3rrfQatAtKzFgPM6996LkXwSvee9AgvJdOOKY8YZprvo8-bnWvp34N3kEaix3MdYlrW-5MttE8j6T4y6zyrZFac0VnTeD9g0DJNxPU0axjdTAMNkGeqmFtcIrwudjUevcPepmnklp795RUmumNINtSbaq1FgiPn6HEbNwzW_dMc8_cu2dkS3r7tI3HlD9eNYBvgdpCaQXlb-3_yP4GCWmmXA</recordid><startdate>20180608</startdate><enddate>20180608</enddate><creator>Rood, Kara M.</creator><creator>Buhimschi, Irina A.</creator><creator>Jurcisek, Joseph A.</creator><creator>Summerfield, Taryn L.</creator><creator>Zhao, Guomao</creator><creator>Ackerman, William E.</creator><creator>Wang, Weiwei</creator><creator>Rumpf, R. Wolfgang</creator><creator>Thung, Stephen F.</creator><creator>Bakaletz, Lauren O.</creator><creator>Buhimschi, Catalin S.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8504-6715</orcidid></search><sort><creationdate>20180608</creationdate><title>Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery</title><author>Rood, Kara M. ; Buhimschi, Irina A. ; Jurcisek, Joseph A. ; Summerfield, Taryn L. ; Zhao, Guomao ; Ackerman, William E. ; Wang, Weiwei ; Rumpf, R. Wolfgang ; Thung, Stephen F. ; Bakaletz, Lauren O. ; Buhimschi, Catalin S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-c520b85f3ee7d3d2ba5d9e9cf8462be6d9dfb3d4fd83bde9e4dd5c4c28d029393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>38/22</topic><topic>38/23</topic><topic>38/77</topic><topic>45/41</topic><topic>692/308/575</topic><topic>692/420/254</topic><topic>692/499</topic><topic>Bacteria</topic><topic>Biofilms</topic><topic>Biomass</topic><topic>Biopsy</topic><topic>Cesarean section</topic><topic>Community composition</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Dysbacteriosis</topic><topic>Genera</topic><topic>Humanities and Social Sciences</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>multidisciplinary</topic><topic>Obesity</topic><topic>Pandemics</topic><topic>Pregnancy</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Skin</topic><topic>Surgery</topic><topic>Surgical site infections</topic><topic>Vagina</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rood, Kara M.</creatorcontrib><creatorcontrib>Buhimschi, Irina A.</creatorcontrib><creatorcontrib>Jurcisek, Joseph A.</creatorcontrib><creatorcontrib>Summerfield, Taryn L.</creatorcontrib><creatorcontrib>Zhao, Guomao</creatorcontrib><creatorcontrib>Ackerman, William E.</creatorcontrib><creatorcontrib>Wang, Weiwei</creatorcontrib><creatorcontrib>Rumpf, R. Wolfgang</creatorcontrib><creatorcontrib>Thung, Stephen F.</creatorcontrib><creatorcontrib>Bakaletz, Lauren O.</creatorcontrib><creatorcontrib>Buhimschi, Catalin S.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rood, Kara M.</au><au>Buhimschi, Irina A.</au><au>Jurcisek, Joseph A.</au><au>Summerfield, Taryn L.</au><au>Zhao, Guomao</au><au>Ackerman, William E.</au><au>Wang, Weiwei</au><au>Rumpf, R. Wolfgang</au><au>Thung, Stephen F.</au><au>Bakaletz, Lauren O.</au><au>Buhimschi, Catalin S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2018-06-08</date><risdate>2018</risdate><volume>8</volume><issue>1</issue><spage>8756</spage><epage>8</epage><pages>8756-8</pages><artnum>8756</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>The obesity pandemic in the obstetrical population plus increased frequency of Cesarean delivery (CD) has increased vulnerability to surgical site infection (SSI). Here we characterized the microbiome at the site of skin incision before and after CD. Skin and relevant surgical sites were sampled before and after surgical antisepsis from obese (n = 31) and non-obese (n = 27) pregnant women. We quantified bacterial biomass by qPCR, microbial community composition by 16sRNA sequencing, assigned operational taxonomic units, and stained skin biopsies from incision for bacteria and biofilms. In obese women, incision site harbors significantly higher bacterial biomass of lower diversity. Phylum Firmicutes predominated over Actinobacteria , with phylotypes Clostridales and Bacteroidales over commensal Staphylococcus and Propionbacterium spp. Skin dysbiosis increased post-surgical prep and at end of surgery. Biofilms were identified post-prep in the majority (73%) of skin biopsies. At end of surgery, incision had significant gains in bacterial DNA and diversity, and obese women shared more genera with vagina and surgeon’s glove in CD. Our findings suggest microbiota at incision differs between obese and non-obese pregnant women, and changes throughout CD. An interaction between vaginal and cutaneous dysbiosis at the incision site may explain the a priori increased risk for SSI among obese pregnant women.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29884793</pmid><doi>10.1038/s41598-018-27134-5</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-8504-6715</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2045-2322
ispartof Scientific reports, 2018-06, Vol.8 (1), p.8756-8, Article 8756
issn 2045-2322
2045-2322
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5993816
source Nature Free; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry; Springer Nature OA Free Journals
subjects 38/22
38/23
38/77
45/41
692/308/575
692/420/254
692/499
Bacteria
Biofilms
Biomass
Biopsy
Cesarean section
Community composition
Deoxyribonucleic acid
DNA
Dysbacteriosis
Genera
Humanities and Social Sciences
Microbiomes
Microbiota
multidisciplinary
Obesity
Pandemics
Pregnancy
Science
Science (multidisciplinary)
Skin
Surgery
Surgical site infections
Vagina
title Skin Microbiota in Obese Women at Risk for Surgical Site Infection After Cesarean Delivery
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-27T06%3A25%3A00IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Skin%20Microbiota%20in%20Obese%20Women%20at%20Risk%20for%20Surgical%20Site%20Infection%20After%20Cesarean%20Delivery&rft.jtitle=Scientific%20reports&rft.au=Rood,%20Kara%20M.&rft.date=2018-06-08&rft.volume=8&rft.issue=1&rft.spage=8756&rft.epage=8&rft.pages=8756-8&rft.artnum=8756&rft.issn=2045-2322&rft.eissn=2045-2322&rft_id=info:doi/10.1038/s41598-018-27134-5&rft_dat=%3Cproquest_pubme%3E2052589296%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2052589296&rft_id=info:pmid/29884793&rfr_iscdi=true