Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage
Different biotic stresses yield specific symptoms, owing to their distinct influence on a plant's physiological status. To monitor early changes in a plant's physiological status upon pathogen attack, chlorophyll fluorescence imaging (Cnl-FI) and thermography, which respectively visualize...
Gespeichert in:
Veröffentlicht in: | Plant and cell physiology 2004-07, Vol.45 (7), p.887-896 |
---|---|
Hauptverfasser: | , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 896 |
---|---|
container_issue | 7 |
container_start_page | 887 |
container_title | Plant and cell physiology |
container_volume | 45 |
creator | Chaerle, L. (Ghent Univ. (Belgium)) Hagenbeek, D De Bruyne, E Valcke, R Van Der Straeten, D |
description | Different biotic stresses yield specific symptoms, owing to their distinct influence on a plant's physiological status. To monitor early changes in a plant's physiological status upon pathogen attack, chlorophyll fluorescence imaging (Cnl-FI) and thermography, which respectively visualize photosynthetic efficiency and transpiration, were carried out in parallel Tor two fundamentally different plant-pathogen interactions. These non-destructive imaging techniques were able to visualize infections at an early stage, before damage appeared. Under growth-room conditions, a robotized set-up captured time series of visual, thermal and chlorophyll fluorescence images from infected regions on attached leaves. As a first symptom of the plant-virus interaction between resistant tobacco and tobacco mosaic virus (TMV), thermal imaging detected a local rise in temperature while Chl-FI monitored a co-localized increase in fluorescence intensity. Chl-FI also revealed pre-symptomatic high-intensity spots for the plant-fungus system sugar beet-Cercospora beticola. Concomitantly, spots of lower temperature were monitored with thermography, in marked contrast with our observations on TMV-infection in tobacco. Knowledge of disease signatures for different plant-pathogen interactions could allow early identification of emerging biotic stresses in crops, facilitating the containment of disease outbreaks. Presymptomatic monitoring clearly opens perspectives for quantitative screening for disease resistance, either on excised leaf pieces or attached leaves. |
doi_str_mv | 10.1093/pcp/pch097 |
format | Article |
fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_19815318</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>19815318</sourcerecordid><originalsourceid>FETCH-LOGICAL-c528t-8a3af3f1f9cad3c0be5857955c63281e32f45f5583bae5824375c3d345ac244a3</originalsourceid><addsrcrecordid>eNpdkc9rFTEQx4NY7Gv14l0JHjwIW_Nj8zZ7bIv12RYsWFF6CfOyye7WfZs1yYLvv3dkHwoewgTmw5eZzxDykrMzzmr5frITvo7V1ROy4mXFi5op-ZSsGJOiYJXmx-QkpUfG8C_ZM3LMlagVq8SK-PvOxR0MFMaG2m4IMUzdfhgKP8whumTdaB3td9D2Y0ubPmWsc586Og0w5mKC3IXWjbQfs4tgcx_GRCFjHnUQhz1NGVr3nBx5GJJ7cain5OvVh_vLTXH7-eOny_Pbwiqhc6FBgpee-9pCIy3bOqVVVStl11Jo7qTwpfJKabkFbIlSVsrKRpYKrChLkKfk7ZI7xfBzdimbXY87DDirC3MyvNZcSa4RfPMf-BjmOOJsRjC-5uuyrhB6t0A2hpSi82aKqCLuDWfmj3qD6s2iHuHXh8R5u3PNP_TgGoFiAVCi-_W3D_GHWVe4iNl8fzD8YXNz9-XiwnxD_tXCewgG2tgnc30nGFN4Vl5q-Ruoa5ks</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>201616497</pqid></control><display><type>article</type><title>Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage</title><source>MEDLINE</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Chaerle, L. (Ghent Univ. (Belgium)) ; Hagenbeek, D ; De Bruyne, E ; Valcke, R ; Van Der Straeten, D</creator><creatorcontrib>Chaerle, L. (Ghent Univ. (Belgium)) ; Hagenbeek, D ; De Bruyne, E ; Valcke, R ; Van Der Straeten, D</creatorcontrib><description>Different biotic stresses yield specific symptoms, owing to their distinct influence on a plant's physiological status. To monitor early changes in a plant's physiological status upon pathogen attack, chlorophyll fluorescence imaging (Cnl-FI) and thermography, which respectively visualize photosynthetic efficiency and transpiration, were carried out in parallel Tor two fundamentally different plant-pathogen interactions. These non-destructive imaging techniques were able to visualize infections at an early stage, before damage appeared. Under growth-room conditions, a robotized set-up captured time series of visual, thermal and chlorophyll fluorescence images from infected regions on attached leaves. As a first symptom of the plant-virus interaction between resistant tobacco and tobacco mosaic virus (TMV), thermal imaging detected a local rise in temperature while Chl-FI monitored a co-localized increase in fluorescence intensity. Chl-FI also revealed pre-symptomatic high-intensity spots for the plant-fungus system sugar beet-Cercospora beticola. Concomitantly, spots of lower temperature were monitored with thermography, in marked contrast with our observations on TMV-infection in tobacco. Knowledge of disease signatures for different plant-pathogen interactions could allow early identification of emerging biotic stresses in crops, facilitating the containment of disease outbreaks. Presymptomatic monitoring clearly opens perspectives for quantitative screening for disease resistance, either on excised leaf pieces or attached leaves.</description><identifier>ISSN: 0032-0781</identifier><identifier>EISSN: 1471-9053</identifier><identifier>DOI: 10.1093/pcp/pch097</identifier><identifier>PMID: 15295072</identifier><language>eng</language><publisher>Japan: Oxford University Press</publisher><subject>Ascomycota - pathogenicity ; Ascomycota - physiology ; BETA VULGARIS ; Beta vulgaris - microbiology ; Beta vulgaris - physiology ; CERCOSPORA BETICOLA ; Chl-FI ; Chlorophyll - analysis ; Chlorophyll - metabolism ; chlorophyll fluorescence image captured after high intensity excitation ; chlorophyll fluorescence image captured after low intensity excitation ; chlorophyll fluorescence imaging ; days post infection ; Disease Progression ; DPI ; EARLY DIAGNOSIS ; FIS ; FLUORESCENCE ; fluorescence imaging system ; Host-Parasite Interactions - drug effects ; Host-Parasite Interactions - physiology ; hypersensitive response ; IMAGERY ; Keywords: Cercospora beticola Sacc. — Chlorophyll fluorescence imaging — Hypersensitive response — Plant–pathogen interaction — Thermography — Tobacco mosaic virus ; Nicotiana - physiology ; Nicotiana - virology ; NICOTIANA TABACUM ; NONDESTRUCTIVE TESTING ; PATHOGENS ; PEA ; Photosynthesis - physiology ; Plant Diseases - microbiology ; Plant Diseases - virology ; plant efficiency analyzer ; PLANT RESPONSE ; salicylic acid ; Salicylic Acid - pharmacology ; Spectrometry, Fluorescence - methods ; Temperature ; Thermography - methods ; Time Factors ; TMV ; TOBACCO MOSAIC TOBAMOVIRUS ; Tobacco mosaic virus ; Tobacco Mosaic Virus - pathogenicity ; Tobacco Mosaic Virus - physiology</subject><ispartof>Plant and cell physiology, 2004-07, Vol.45 (7), p.887-896</ispartof><rights>Copyright Oxford University Press(England) Jul 15, 2004</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c528t-8a3af3f1f9cad3c0be5857955c63281e32f45f5583bae5824375c3d345ac244a3</citedby><cites>FETCH-LOGICAL-c528t-8a3af3f1f9cad3c0be5857955c63281e32f45f5583bae5824375c3d345ac244a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15295072$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chaerle, L. (Ghent Univ. (Belgium))</creatorcontrib><creatorcontrib>Hagenbeek, D</creatorcontrib><creatorcontrib>De Bruyne, E</creatorcontrib><creatorcontrib>Valcke, R</creatorcontrib><creatorcontrib>Van Der Straeten, D</creatorcontrib><title>Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage</title><title>Plant and cell physiology</title><addtitle>Plant Cell Physiol</addtitle><description>Different biotic stresses yield specific symptoms, owing to their distinct influence on a plant's physiological status. To monitor early changes in a plant's physiological status upon pathogen attack, chlorophyll fluorescence imaging (Cnl-FI) and thermography, which respectively visualize photosynthetic efficiency and transpiration, were carried out in parallel Tor two fundamentally different plant-pathogen interactions. These non-destructive imaging techniques were able to visualize infections at an early stage, before damage appeared. Under growth-room conditions, a robotized set-up captured time series of visual, thermal and chlorophyll fluorescence images from infected regions on attached leaves. As a first symptom of the plant-virus interaction between resistant tobacco and tobacco mosaic virus (TMV), thermal imaging detected a local rise in temperature while Chl-FI monitored a co-localized increase in fluorescence intensity. Chl-FI also revealed pre-symptomatic high-intensity spots for the plant-fungus system sugar beet-Cercospora beticola. Concomitantly, spots of lower temperature were monitored with thermography, in marked contrast with our observations on TMV-infection in tobacco. Knowledge of disease signatures for different plant-pathogen interactions could allow early identification of emerging biotic stresses in crops, facilitating the containment of disease outbreaks. Presymptomatic monitoring clearly opens perspectives for quantitative screening for disease resistance, either on excised leaf pieces or attached leaves.</description><subject>Ascomycota - pathogenicity</subject><subject>Ascomycota - physiology</subject><subject>BETA VULGARIS</subject><subject>Beta vulgaris - microbiology</subject><subject>Beta vulgaris - physiology</subject><subject>CERCOSPORA BETICOLA</subject><subject>Chl-FI</subject><subject>Chlorophyll - analysis</subject><subject>Chlorophyll - metabolism</subject><subject>chlorophyll fluorescence image captured after high intensity excitation</subject><subject>chlorophyll fluorescence image captured after low intensity excitation</subject><subject>chlorophyll fluorescence imaging</subject><subject>days post infection</subject><subject>Disease Progression</subject><subject>DPI</subject><subject>EARLY DIAGNOSIS</subject><subject>FIS</subject><subject>FLUORESCENCE</subject><subject>fluorescence imaging system</subject><subject>Host-Parasite Interactions - drug effects</subject><subject>Host-Parasite Interactions - physiology</subject><subject>hypersensitive response</subject><subject>IMAGERY</subject><subject>Keywords: Cercospora beticola Sacc. — Chlorophyll fluorescence imaging — Hypersensitive response — Plant–pathogen interaction — Thermography — Tobacco mosaic virus</subject><subject>Nicotiana - physiology</subject><subject>Nicotiana - virology</subject><subject>NICOTIANA TABACUM</subject><subject>NONDESTRUCTIVE TESTING</subject><subject>PATHOGENS</subject><subject>PEA</subject><subject>Photosynthesis - physiology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - virology</subject><subject>plant efficiency analyzer</subject><subject>PLANT RESPONSE</subject><subject>salicylic acid</subject><subject>Salicylic Acid - pharmacology</subject><subject>Spectrometry, Fluorescence - methods</subject><subject>Temperature</subject><subject>Thermography - methods</subject><subject>Time Factors</subject><subject>TMV</subject><subject>TOBACCO MOSAIC TOBAMOVIRUS</subject><subject>Tobacco mosaic virus</subject><subject>Tobacco Mosaic Virus - pathogenicity</subject><subject>Tobacco Mosaic Virus - physiology</subject><issn>0032-0781</issn><issn>1471-9053</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc9rFTEQx4NY7Gv14l0JHjwIW_Nj8zZ7bIv12RYsWFF6CfOyye7WfZs1yYLvv3dkHwoewgTmw5eZzxDykrMzzmr5frITvo7V1ROy4mXFi5op-ZSsGJOiYJXmx-QkpUfG8C_ZM3LMlagVq8SK-PvOxR0MFMaG2m4IMUzdfhgKP8whumTdaB3td9D2Y0ubPmWsc586Og0w5mKC3IXWjbQfs4tgcx_GRCFjHnUQhz1NGVr3nBx5GJJ7cain5OvVh_vLTXH7-eOny_Pbwiqhc6FBgpee-9pCIy3bOqVVVStl11Jo7qTwpfJKabkFbIlSVsrKRpYKrChLkKfk7ZI7xfBzdimbXY87DDirC3MyvNZcSa4RfPMf-BjmOOJsRjC-5uuyrhB6t0A2hpSi82aKqCLuDWfmj3qD6s2iHuHXh8R5u3PNP_TgGoFiAVCi-_W3D_GHWVe4iNl8fzD8YXNz9-XiwnxD_tXCewgG2tgnc30nGFN4Vl5q-Ruoa5ks</recordid><startdate>20040701</startdate><enddate>20040701</enddate><creator>Chaerle, L. (Ghent Univ. (Belgium))</creator><creator>Hagenbeek, D</creator><creator>De Bruyne, E</creator><creator>Valcke, R</creator><creator>Van Der Straeten, D</creator><general>Oxford University Press</general><general>Oxford Publishing Limited (England)</general><scope>FBQ</scope><scope>BSCLL</scope><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>7QL</scope><scope>7QO</scope><scope>7QP</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>20040701</creationdate><title>Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage</title><author>Chaerle, L. (Ghent Univ. (Belgium)) ; Hagenbeek, D ; De Bruyne, E ; Valcke, R ; Van Der Straeten, D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c528t-8a3af3f1f9cad3c0be5857955c63281e32f45f5583bae5824375c3d345ac244a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Ascomycota - pathogenicity</topic><topic>Ascomycota - physiology</topic><topic>BETA VULGARIS</topic><topic>Beta vulgaris - microbiology</topic><topic>Beta vulgaris - physiology</topic><topic>CERCOSPORA BETICOLA</topic><topic>Chl-FI</topic><topic>Chlorophyll - analysis</topic><topic>Chlorophyll - metabolism</topic><topic>chlorophyll fluorescence image captured after high intensity excitation</topic><topic>chlorophyll fluorescence image captured after low intensity excitation</topic><topic>chlorophyll fluorescence imaging</topic><topic>days post infection</topic><topic>Disease Progression</topic><topic>DPI</topic><topic>EARLY DIAGNOSIS</topic><topic>FIS</topic><topic>FLUORESCENCE</topic><topic>fluorescence imaging system</topic><topic>Host-Parasite Interactions - drug effects</topic><topic>Host-Parasite Interactions - physiology</topic><topic>hypersensitive response</topic><topic>IMAGERY</topic><topic>Keywords: Cercospora beticola Sacc. — Chlorophyll fluorescence imaging — Hypersensitive response — Plant–pathogen interaction — Thermography — Tobacco mosaic virus</topic><topic>Nicotiana - physiology</topic><topic>Nicotiana - virology</topic><topic>NICOTIANA TABACUM</topic><topic>NONDESTRUCTIVE TESTING</topic><topic>PATHOGENS</topic><topic>PEA</topic><topic>Photosynthesis - physiology</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Diseases - virology</topic><topic>plant efficiency analyzer</topic><topic>PLANT RESPONSE</topic><topic>salicylic acid</topic><topic>Salicylic Acid - pharmacology</topic><topic>Spectrometry, Fluorescence - methods</topic><topic>Temperature</topic><topic>Thermography - methods</topic><topic>Time Factors</topic><topic>TMV</topic><topic>TOBACCO MOSAIC TOBAMOVIRUS</topic><topic>Tobacco mosaic virus</topic><topic>Tobacco Mosaic Virus - pathogenicity</topic><topic>Tobacco Mosaic Virus - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chaerle, L. (Ghent Univ. (Belgium))</creatorcontrib><creatorcontrib>Hagenbeek, D</creatorcontrib><creatorcontrib>De Bruyne, E</creatorcontrib><creatorcontrib>Valcke, R</creatorcontrib><creatorcontrib>Van Der Straeten, D</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Plant and cell physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chaerle, L. (Ghent Univ. (Belgium))</au><au>Hagenbeek, D</au><au>De Bruyne, E</au><au>Valcke, R</au><au>Van Der Straeten, D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage</atitle><jtitle>Plant and cell physiology</jtitle><addtitle>Plant Cell Physiol</addtitle><date>2004-07-01</date><risdate>2004</risdate><volume>45</volume><issue>7</issue><spage>887</spage><epage>896</epage><pages>887-896</pages><issn>0032-0781</issn><eissn>1471-9053</eissn><abstract>Different biotic stresses yield specific symptoms, owing to their distinct influence on a plant's physiological status. To monitor early changes in a plant's physiological status upon pathogen attack, chlorophyll fluorescence imaging (Cnl-FI) and thermography, which respectively visualize photosynthetic efficiency and transpiration, were carried out in parallel Tor two fundamentally different plant-pathogen interactions. These non-destructive imaging techniques were able to visualize infections at an early stage, before damage appeared. Under growth-room conditions, a robotized set-up captured time series of visual, thermal and chlorophyll fluorescence images from infected regions on attached leaves. As a first symptom of the plant-virus interaction between resistant tobacco and tobacco mosaic virus (TMV), thermal imaging detected a local rise in temperature while Chl-FI monitored a co-localized increase in fluorescence intensity. Chl-FI also revealed pre-symptomatic high-intensity spots for the plant-fungus system sugar beet-Cercospora beticola. Concomitantly, spots of lower temperature were monitored with thermography, in marked contrast with our observations on TMV-infection in tobacco. Knowledge of disease signatures for different plant-pathogen interactions could allow early identification of emerging biotic stresses in crops, facilitating the containment of disease outbreaks. Presymptomatic monitoring clearly opens perspectives for quantitative screening for disease resistance, either on excised leaf pieces or attached leaves.</abstract><cop>Japan</cop><pub>Oxford University Press</pub><pmid>15295072</pmid><doi>10.1093/pcp/pch097</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0032-0781 |
ispartof | Plant and cell physiology, 2004-07, Vol.45 (7), p.887-896 |
issn | 0032-0781 1471-9053 |
language | eng |
recordid | cdi_proquest_miscellaneous_19815318 |
source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals |
subjects | Ascomycota - pathogenicity Ascomycota - physiology BETA VULGARIS Beta vulgaris - microbiology Beta vulgaris - physiology CERCOSPORA BETICOLA Chl-FI Chlorophyll - analysis Chlorophyll - metabolism chlorophyll fluorescence image captured after high intensity excitation chlorophyll fluorescence image captured after low intensity excitation chlorophyll fluorescence imaging days post infection Disease Progression DPI EARLY DIAGNOSIS FIS FLUORESCENCE fluorescence imaging system Host-Parasite Interactions - drug effects Host-Parasite Interactions - physiology hypersensitive response IMAGERY Keywords: Cercospora beticola Sacc. — Chlorophyll fluorescence imaging — Hypersensitive response — Plant–pathogen interaction — Thermography — Tobacco mosaic virus Nicotiana - physiology Nicotiana - virology NICOTIANA TABACUM NONDESTRUCTIVE TESTING PATHOGENS PEA Photosynthesis - physiology Plant Diseases - microbiology Plant Diseases - virology plant efficiency analyzer PLANT RESPONSE salicylic acid Salicylic Acid - pharmacology Spectrometry, Fluorescence - methods Temperature Thermography - methods Time Factors TMV TOBACCO MOSAIC TOBAMOVIRUS Tobacco mosaic virus Tobacco Mosaic Virus - pathogenicity Tobacco Mosaic Virus - physiology |
title | Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T10%3A08%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Thermal%20and%20chlorophyll-fluorescence%20imaging%20distinguish%20plant-pathogen%20interactions%20at%20an%20early%20stage&rft.jtitle=Plant%20and%20cell%20physiology&rft.au=Chaerle,%20L.%20(Ghent%20Univ.%20(Belgium))&rft.date=2004-07-01&rft.volume=45&rft.issue=7&rft.spage=887&rft.epage=896&rft.pages=887-896&rft.issn=0032-0781&rft.eissn=1471-9053&rft_id=info:doi/10.1093/pcp/pch097&rft_dat=%3Cproquest_cross%3E19815318%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=201616497&rft_id=info:pmid/15295072&rfr_iscdi=true |