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...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Plant and cell physiology 2004-07, Vol.45 (7), p.887-896
Hauptverfasser: Chaerle, L. (Ghent Univ. (Belgium)), Hagenbeek, D, De Bruyne, E, Valcke, R, Van Der Straeten, D
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 &amp; 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 &amp; 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