Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging

Purpose To compare regional oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen consumption (CMRO2) quantified from the microvascular quantitative susceptibility mapping (QSM) using a hypercapnic gas challenge with those measured by the dual‐gas calibrated BOLD imaging (DGC‐BOLD)...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Magnetic resonance in medicine 2020-01, Vol.83 (1), p.68-82
Hauptverfasser: Ma, Yuhan, Sun, Hongfu, Cho, Junghun, Mazerolle, Erin L., Wang, Yi, Pike, G. Bruce
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 82
container_issue 1
container_start_page 68
container_title Magnetic resonance in medicine
container_volume 83
creator Ma, Yuhan
Sun, Hongfu
Cho, Junghun
Mazerolle, Erin L.
Wang, Yi
Pike, G. Bruce
description Purpose To compare regional oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen consumption (CMRO2) quantified from the microvascular quantitative susceptibility mapping (QSM) using a hypercapnic gas challenge with those measured by the dual‐gas calibrated BOLD imaging (DGC‐BOLD) in healthy subjects. Methods Ten healthy subjects were scanned using a 3T MR system. The QSM data were acquired with a multi‐echo gradient‐echo sequence at baseline and hypercapnia. Cerebral blood flow data were acquired using the pseudo‐continuous arterial spin labeling technique. Baseline OEF and CMRO2 were calculated using QSM and cerebral blood flow measurements. The DGC‐BOLD data were also collected under a hypercapnic and a hyperoxic condition to yield baseline OEF and CMRO2. The QSM‐OEF and CMRO2 maps were compared with DGC‐BOLD OEF and CMRO2 maps using region of interest (vascular territories) analysis and Bland‐Altman plots. Results Hypercapnia is a robust stimulus for mapping OEF in combination with QSM. Average OEF in 16 vascular territory regions of interest across 10 subjects was 0.40 ± 0.04 by QSM‐OEF and 0.38 ± 0.09 by DGC‐BOLD. The average CMRO2 was 176 ± 35 and 167 ± 53 μmol O2/min/100g by QSM‐OEF and DGC‐BOLD, respectively. A Bland‐Altman plot of regional OEF and CMRO2 in regions of interest revealed a statistically significant but small difference (OEF difference = 0.02, CMRO2 difference = 9 μmol O2/min/100g, p < .05) between the 2 methods for the 10 healthy subjects. Conclusion Hypercapnic challenge–assisted QSM‐OEF is a feasible approach to quantify regional brain OEF and CMRO2. Compared with DGC‐BOLD, hypercapnia QSM‐OEF results in smaller intersubject variability and requires only 1 gas challenge.
doi_str_mv 10.1002/mrm.27907
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2268310678</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2268310678</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3887-5f2235125938cfd9e4fde1336bb17f359b95b17a2f1a829c0df4a8acac7660753</originalsourceid><addsrcrecordid>eNp10btuFDEUBmALgcgSKHgBZIkGikl8GY9turAkgLTRSghq64zHXjmaW2xPou0QT8Az8iQYdqFAorKLT_85Rz9Czyk5o4Sw8yEOZ0xqIh-gFRWMVUzo-iFaEVmTilNdn6AnKd0QQrSW9WN0wimXnCi1Qt_WLro2Qo-3l1f4doExBx8s5DCNb_AFttMwQwxpGnHKS7fHrcv3zo1Hmgu8czgtybo5hzb0Ie_xAPMcxh2GscPdAv2Pr993kLCFPpRR2XX47XbzDocBdoU9RY889Mk9O76n6MvV5ef1h2qzff9xfbGpLFdKVsIzxgUtp3Flfadd7TtHOW_alkrPhW61KD9gnoJi2pLO16DAgpVNQ6Tgp-jVIXeO0-3iUjZDKGv3PYxuWpJhrFGckkaqQl_-Q2-mJY5lO8M4oUTUjZBFvT4oG6eUovNmjuWmuDeUmF_FmFKM-V1MsS-OiUs7uO6v_NNEAecHcB96t_9_krn-dH2I_AklAJmi</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2301054657</pqid></control><display><type>article</type><title>Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging</title><source>MEDLINE</source><source>Wiley Free Content</source><source>Wiley Online Library All Journals</source><creator>Ma, Yuhan ; Sun, Hongfu ; Cho, Junghun ; Mazerolle, Erin L. ; Wang, Yi ; Pike, G. Bruce</creator><creatorcontrib>Ma, Yuhan ; Sun, Hongfu ; Cho, Junghun ; Mazerolle, Erin L. ; Wang, Yi ; Pike, G. Bruce</creatorcontrib><description>Purpose To compare regional oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen consumption (CMRO2) quantified from the microvascular quantitative susceptibility mapping (QSM) using a hypercapnic gas challenge with those measured by the dual‐gas calibrated BOLD imaging (DGC‐BOLD) in healthy subjects. Methods Ten healthy subjects were scanned using a 3T MR system. The QSM data were acquired with a multi‐echo gradient‐echo sequence at baseline and hypercapnia. Cerebral blood flow data were acquired using the pseudo‐continuous arterial spin labeling technique. Baseline OEF and CMRO2 were calculated using QSM and cerebral blood flow measurements. The DGC‐BOLD data were also collected under a hypercapnic and a hyperoxic condition to yield baseline OEF and CMRO2. The QSM‐OEF and CMRO2 maps were compared with DGC‐BOLD OEF and CMRO2 maps using region of interest (vascular territories) analysis and Bland‐Altman plots. Results Hypercapnia is a robust stimulus for mapping OEF in combination with QSM. Average OEF in 16 vascular territory regions of interest across 10 subjects was 0.40 ± 0.04 by QSM‐OEF and 0.38 ± 0.09 by DGC‐BOLD. The average CMRO2 was 176 ± 35 and 167 ± 53 μmol O2/min/100g by QSM‐OEF and DGC‐BOLD, respectively. A Bland‐Altman plot of regional OEF and CMRO2 in regions of interest revealed a statistically significant but small difference (OEF difference = 0.02, CMRO2 difference = 9 μmol O2/min/100g, p &lt; .05) between the 2 methods for the 10 healthy subjects. Conclusion Hypercapnic challenge–assisted QSM‐OEF is a feasible approach to quantify regional brain OEF and CMRO2. Compared with DGC‐BOLD, hypercapnia QSM‐OEF results in smaller intersubject variability and requires only 1 gas challenge.</description><identifier>ISSN: 0740-3194</identifier><identifier>EISSN: 1522-2594</identifier><identifier>DOI: 10.1002/mrm.27907</identifier><identifier>PMID: 31373088</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Adult ; Algorithms ; Blood flow ; Brain - diagnostic imaging ; Brain Mapping ; calibrated BOLD ; Calibration ; Cerebral blood flow ; Cerebrovascular Circulation ; Computer Simulation ; Data acquisition ; Echo-Planar Imaging ; Female ; Functional magnetic resonance imaging ; Gray Matter - diagnostic imaging ; Healthy Volunteers ; Humans ; Hypercapnia ; Hypercapnia - metabolism ; Hyperoxia - metabolism ; Image processing ; Image Processing, Computer-Assisted - methods ; Magnetic Resonance Imaging ; Male ; Mapping ; Metabolic rate ; Microvasculature ; Neuroimaging ; Oxygen - blood ; Oxygen Consumption ; oxygen extraction fraction ; quantitative susceptibility mapping ; Reproducibility of Results ; Spin labeling ; Spin Labels ; Statistical analysis ; Territory</subject><ispartof>Magnetic resonance in medicine, 2020-01, Vol.83 (1), p.68-82</ispartof><rights>2019 International Society for Magnetic Resonance in Medicine</rights><rights>2019 International Society for Magnetic Resonance in Medicine.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3887-5f2235125938cfd9e4fde1336bb17f359b95b17a2f1a829c0df4a8acac7660753</citedby><cites>FETCH-LOGICAL-c3887-5f2235125938cfd9e4fde1336bb17f359b95b17a2f1a829c0df4a8acac7660753</cites><orcidid>0000-0002-0826-5463 ; 0000-0003-1404-8526 ; 0000-0001-7025-7539 ; 0000-0003-3436-7831</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmrm.27907$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmrm.27907$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,1432,27923,27924,45573,45574,46408,46832</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31373088$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, Yuhan</creatorcontrib><creatorcontrib>Sun, Hongfu</creatorcontrib><creatorcontrib>Cho, Junghun</creatorcontrib><creatorcontrib>Mazerolle, Erin L.</creatorcontrib><creatorcontrib>Wang, Yi</creatorcontrib><creatorcontrib>Pike, G. Bruce</creatorcontrib><title>Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging</title><title>Magnetic resonance in medicine</title><addtitle>Magn Reson Med</addtitle><description>Purpose To compare regional oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen consumption (CMRO2) quantified from the microvascular quantitative susceptibility mapping (QSM) using a hypercapnic gas challenge with those measured by the dual‐gas calibrated BOLD imaging (DGC‐BOLD) in healthy subjects. Methods Ten healthy subjects were scanned using a 3T MR system. The QSM data were acquired with a multi‐echo gradient‐echo sequence at baseline and hypercapnia. Cerebral blood flow data were acquired using the pseudo‐continuous arterial spin labeling technique. Baseline OEF and CMRO2 were calculated using QSM and cerebral blood flow measurements. The DGC‐BOLD data were also collected under a hypercapnic and a hyperoxic condition to yield baseline OEF and CMRO2. The QSM‐OEF and CMRO2 maps were compared with DGC‐BOLD OEF and CMRO2 maps using region of interest (vascular territories) analysis and Bland‐Altman plots. Results Hypercapnia is a robust stimulus for mapping OEF in combination with QSM. Average OEF in 16 vascular territory regions of interest across 10 subjects was 0.40 ± 0.04 by QSM‐OEF and 0.38 ± 0.09 by DGC‐BOLD. The average CMRO2 was 176 ± 35 and 167 ± 53 μmol O2/min/100g by QSM‐OEF and DGC‐BOLD, respectively. A Bland‐Altman plot of regional OEF and CMRO2 in regions of interest revealed a statistically significant but small difference (OEF difference = 0.02, CMRO2 difference = 9 μmol O2/min/100g, p &lt; .05) between the 2 methods for the 10 healthy subjects. Conclusion Hypercapnic challenge–assisted QSM‐OEF is a feasible approach to quantify regional brain OEF and CMRO2. Compared with DGC‐BOLD, hypercapnia QSM‐OEF results in smaller intersubject variability and requires only 1 gas challenge.</description><subject>Adult</subject><subject>Algorithms</subject><subject>Blood flow</subject><subject>Brain - diagnostic imaging</subject><subject>Brain Mapping</subject><subject>calibrated BOLD</subject><subject>Calibration</subject><subject>Cerebral blood flow</subject><subject>Cerebrovascular Circulation</subject><subject>Computer Simulation</subject><subject>Data acquisition</subject><subject>Echo-Planar Imaging</subject><subject>Female</subject><subject>Functional magnetic resonance imaging</subject><subject>Gray Matter - diagnostic imaging</subject><subject>Healthy Volunteers</subject><subject>Humans</subject><subject>Hypercapnia</subject><subject>Hypercapnia - metabolism</subject><subject>Hyperoxia - metabolism</subject><subject>Image processing</subject><subject>Image Processing, Computer-Assisted - methods</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Mapping</subject><subject>Metabolic rate</subject><subject>Microvasculature</subject><subject>Neuroimaging</subject><subject>Oxygen - blood</subject><subject>Oxygen Consumption</subject><subject>oxygen extraction fraction</subject><subject>quantitative susceptibility mapping</subject><subject>Reproducibility of Results</subject><subject>Spin labeling</subject><subject>Spin Labels</subject><subject>Statistical analysis</subject><subject>Territory</subject><issn>0740-3194</issn><issn>1522-2594</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10btuFDEUBmALgcgSKHgBZIkGikl8GY9turAkgLTRSghq64zHXjmaW2xPou0QT8Az8iQYdqFAorKLT_85Rz9Czyk5o4Sw8yEOZ0xqIh-gFRWMVUzo-iFaEVmTilNdn6AnKd0QQrSW9WN0wimXnCi1Qt_WLro2Qo-3l1f4doExBx8s5DCNb_AFttMwQwxpGnHKS7fHrcv3zo1Hmgu8czgtybo5hzb0Ie_xAPMcxh2GscPdAv2Pr993kLCFPpRR2XX47XbzDocBdoU9RY889Mk9O76n6MvV5ef1h2qzff9xfbGpLFdKVsIzxgUtp3Flfadd7TtHOW_alkrPhW61KD9gnoJi2pLO16DAgpVNQ6Tgp-jVIXeO0-3iUjZDKGv3PYxuWpJhrFGckkaqQl_-Q2-mJY5lO8M4oUTUjZBFvT4oG6eUovNmjuWmuDeUmF_FmFKM-V1MsS-OiUs7uO6v_NNEAecHcB96t_9_krn-dH2I_AklAJmi</recordid><startdate>202001</startdate><enddate>202001</enddate><creator>Ma, Yuhan</creator><creator>Sun, Hongfu</creator><creator>Cho, Junghun</creator><creator>Mazerolle, Erin L.</creator><creator>Wang, Yi</creator><creator>Pike, G. Bruce</creator><general>Wiley Subscription Services, Inc</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>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7Z</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0826-5463</orcidid><orcidid>https://orcid.org/0000-0003-1404-8526</orcidid><orcidid>https://orcid.org/0000-0001-7025-7539</orcidid><orcidid>https://orcid.org/0000-0003-3436-7831</orcidid></search><sort><creationdate>202001</creationdate><title>Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging</title><author>Ma, Yuhan ; Sun, Hongfu ; Cho, Junghun ; Mazerolle, Erin L. ; Wang, Yi ; Pike, G. Bruce</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3887-5f2235125938cfd9e4fde1336bb17f359b95b17a2f1a829c0df4a8acac7660753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Algorithms</topic><topic>Blood flow</topic><topic>Brain - diagnostic imaging</topic><topic>Brain Mapping</topic><topic>calibrated BOLD</topic><topic>Calibration</topic><topic>Cerebral blood flow</topic><topic>Cerebrovascular Circulation</topic><topic>Computer Simulation</topic><topic>Data acquisition</topic><topic>Echo-Planar Imaging</topic><topic>Female</topic><topic>Functional magnetic resonance imaging</topic><topic>Gray Matter - diagnostic imaging</topic><topic>Healthy Volunteers</topic><topic>Humans</topic><topic>Hypercapnia</topic><topic>Hypercapnia - metabolism</topic><topic>Hyperoxia - metabolism</topic><topic>Image processing</topic><topic>Image Processing, Computer-Assisted - methods</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Mapping</topic><topic>Metabolic rate</topic><topic>Microvasculature</topic><topic>Neuroimaging</topic><topic>Oxygen - blood</topic><topic>Oxygen Consumption</topic><topic>oxygen extraction fraction</topic><topic>quantitative susceptibility mapping</topic><topic>Reproducibility of Results</topic><topic>Spin labeling</topic><topic>Spin Labels</topic><topic>Statistical analysis</topic><topic>Territory</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, Yuhan</creatorcontrib><creatorcontrib>Sun, Hongfu</creatorcontrib><creatorcontrib>Cho, Junghun</creatorcontrib><creatorcontrib>Mazerolle, Erin L.</creatorcontrib><creatorcontrib>Wang, Yi</creatorcontrib><creatorcontrib>Pike, G. Bruce</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biochemistry Abstracts 1</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Magnetic resonance in medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Yuhan</au><au>Sun, Hongfu</au><au>Cho, Junghun</au><au>Mazerolle, Erin L.</au><au>Wang, Yi</au><au>Pike, G. Bruce</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging</atitle><jtitle>Magnetic resonance in medicine</jtitle><addtitle>Magn Reson Med</addtitle><date>2020-01</date><risdate>2020</risdate><volume>83</volume><issue>1</issue><spage>68</spage><epage>82</epage><pages>68-82</pages><issn>0740-3194</issn><eissn>1522-2594</eissn><abstract>Purpose To compare regional oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen consumption (CMRO2) quantified from the microvascular quantitative susceptibility mapping (QSM) using a hypercapnic gas challenge with those measured by the dual‐gas calibrated BOLD imaging (DGC‐BOLD) in healthy subjects. Methods Ten healthy subjects were scanned using a 3T MR system. The QSM data were acquired with a multi‐echo gradient‐echo sequence at baseline and hypercapnia. Cerebral blood flow data were acquired using the pseudo‐continuous arterial spin labeling technique. Baseline OEF and CMRO2 were calculated using QSM and cerebral blood flow measurements. The DGC‐BOLD data were also collected under a hypercapnic and a hyperoxic condition to yield baseline OEF and CMRO2. The QSM‐OEF and CMRO2 maps were compared with DGC‐BOLD OEF and CMRO2 maps using region of interest (vascular territories) analysis and Bland‐Altman plots. Results Hypercapnia is a robust stimulus for mapping OEF in combination with QSM. Average OEF in 16 vascular territory regions of interest across 10 subjects was 0.40 ± 0.04 by QSM‐OEF and 0.38 ± 0.09 by DGC‐BOLD. The average CMRO2 was 176 ± 35 and 167 ± 53 μmol O2/min/100g by QSM‐OEF and DGC‐BOLD, respectively. A Bland‐Altman plot of regional OEF and CMRO2 in regions of interest revealed a statistically significant but small difference (OEF difference = 0.02, CMRO2 difference = 9 μmol O2/min/100g, p &lt; .05) between the 2 methods for the 10 healthy subjects. Conclusion Hypercapnic challenge–assisted QSM‐OEF is a feasible approach to quantify regional brain OEF and CMRO2. Compared with DGC‐BOLD, hypercapnia QSM‐OEF results in smaller intersubject variability and requires only 1 gas challenge.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>31373088</pmid><doi>10.1002/mrm.27907</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-0826-5463</orcidid><orcidid>https://orcid.org/0000-0003-1404-8526</orcidid><orcidid>https://orcid.org/0000-0001-7025-7539</orcidid><orcidid>https://orcid.org/0000-0003-3436-7831</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0740-3194
ispartof Magnetic resonance in medicine, 2020-01, Vol.83 (1), p.68-82
issn 0740-3194
1522-2594
language eng
recordid cdi_proquest_miscellaneous_2268310678
source MEDLINE; Wiley Free Content; Wiley Online Library All Journals
subjects Adult
Algorithms
Blood flow
Brain - diagnostic imaging
Brain Mapping
calibrated BOLD
Calibration
Cerebral blood flow
Cerebrovascular Circulation
Computer Simulation
Data acquisition
Echo-Planar Imaging
Female
Functional magnetic resonance imaging
Gray Matter - diagnostic imaging
Healthy Volunteers
Humans
Hypercapnia
Hypercapnia - metabolism
Hyperoxia - metabolism
Image processing
Image Processing, Computer-Assisted - methods
Magnetic Resonance Imaging
Male
Mapping
Metabolic rate
Microvasculature
Neuroimaging
Oxygen - blood
Oxygen Consumption
oxygen extraction fraction
quantitative susceptibility mapping
Reproducibility of Results
Spin labeling
Spin Labels
Statistical analysis
Territory
title Cerebral OEF quantification: A comparison study between quantitative susceptibility mapping and dual‐gas calibrated BOLD imaging
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-11T06%3A37%3A47IST&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=Cerebral%20OEF%20quantification:%20A%20comparison%20study%20between%20quantitative%20susceptibility%20mapping%20and%20dual%E2%80%90gas%20calibrated%20BOLD%20imaging&rft.jtitle=Magnetic%20resonance%20in%20medicine&rft.au=Ma,%20Yuhan&rft.date=2020-01&rft.volume=83&rft.issue=1&rft.spage=68&rft.epage=82&rft.pages=68-82&rft.issn=0740-3194&rft.eissn=1522-2594&rft_id=info:doi/10.1002/mrm.27907&rft_dat=%3Cproquest_cross%3E2268310678%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=2301054657&rft_id=info:pmid/31373088&rfr_iscdi=true