Whole-body MRI in oncology: can a single anatomic T2 Dixon sequence replace the combination of T1 and STIR sequences to detect skeletal metastasis and myeloma?

Objectives To compare the diagnostic accuracy of a single T2 Dixon sequence to the combination T1+STIR as anatomical sequences used for detecting tumoral bone marrow lesions in whole-body MRI (WB-MRI) examinations. Methods Between January 2019 and January 2020, seventy-two consecutive patients (55 m...

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Veröffentlicht in:European radiology 2023-01, Vol.33 (1), p.244-257
Hauptverfasser: Chiabai, Ophelye, Van Nieuwenhove, Sandy, Vekemans, Marie-Christiane, Tombal, Bertrand, Peeters, Frank, Wuts, Joris, Triqueneaux, Perrine, Omoumi, Patrick, Kirchgesner, Thomas, Michoux, Nicolas, Lecouvet, Frédéric E.
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container_end_page 257
container_issue 1
container_start_page 244
container_title European radiology
container_volume 33
creator Chiabai, Ophelye
Van Nieuwenhove, Sandy
Vekemans, Marie-Christiane
Tombal, Bertrand
Peeters, Frank
Wuts, Joris
Triqueneaux, Perrine
Omoumi, Patrick
Kirchgesner, Thomas
Michoux, Nicolas
Lecouvet, Frédéric E.
description Objectives To compare the diagnostic accuracy of a single T2 Dixon sequence to the combination T1+STIR as anatomical sequences used for detecting tumoral bone marrow lesions in whole-body MRI (WB-MRI) examinations. Methods Between January 2019 and January 2020, seventy-two consecutive patients (55 men, 17 women, median age = 66 years) with solid (prostate, breast, neuroendocrine) cancers at high risk of metastasis or proven multiple myeloma (MM) prospectively underwent a WB-MRI examination including coronal T1, STIR, T2 Dixon and axial diffusion-weighted imaging sequences. Two radiologists independently assessed the combination of T1+STIR sequences and the fat+water reconstructions from the T2 Dixon sequence. The reference standard was established by consensus reading of WB-MRI and concurrent imaging available at baseline and at 6 months. Repeatability and reproducibility of MRI scores (presence and semi-quantitative count of lesions), image quality (SNR: signal-to-noise, CNR: contrast-to-noise, CRR: contrast-to-reference ratios), and diagnostic characteristics (Se: sensitivity, Sp: specificity, Acc: accuracy) were assessed per -skeletal region and per -patient. Results Repeatability and reproducibility were at least good regardless of the score, region, and protocol (0.67 ≤ AC1 ≤ 0.98). CRR was higher on T2 Dixon fat compared to T1 ( p < 0.0001) and on T2 Dixon water compared to STIR ( p = 0.0128). In the per -patient analysis, Acc of the T2 Dixon fat+water was higher than that of T1+STIR for the senior reader (Acc = +0.027 [+0.025; +0.029], p < 0.0001) and lower for the junior reader (Acc = −0.029 [−0.031; −0.027], p < 0.0001). Conclusions A single T2 Dixon sequence with fat+water reconstructions offers similar reproducibility and diagnostic accuracy as the recommended combination of T1+STIR sequences and can be used for skeletal screening in oncology, allowing significant time-saving. Key Points • Replacement of the standard anatomic T1 + STIR WB-MRI protocol by a single T2 Dixon sequence drastically shortens the examination time without loss of diagnostic accuracy. • A protocol based on fat + water reconstructions from a single T2 Dixon sequence offers similar inter-reader agreement and a higher contrast-to-reference ratio for detecting lesions compared to the standard T1 + STIR protocol. • Differences in the accuracy between the two protocols are marginal (+ 3% in favor of the T2 Dixon with the senior reader; −3% against the T2 Dixon with the junior r
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Methods Between January 2019 and January 2020, seventy-two consecutive patients (55 men, 17 women, median age = 66 years) with solid (prostate, breast, neuroendocrine) cancers at high risk of metastasis or proven multiple myeloma (MM) prospectively underwent a WB-MRI examination including coronal T1, STIR, T2 Dixon and axial diffusion-weighted imaging sequences. Two radiologists independently assessed the combination of T1+STIR sequences and the fat+water reconstructions from the T2 Dixon sequence. The reference standard was established by consensus reading of WB-MRI and concurrent imaging available at baseline and at 6 months. Repeatability and reproducibility of MRI scores (presence and semi-quantitative count of lesions), image quality (SNR: signal-to-noise, CNR: contrast-to-noise, CRR: contrast-to-reference ratios), and diagnostic characteristics (Se: sensitivity, Sp: specificity, Acc: accuracy) were assessed per -skeletal region and per -patient. Results Repeatability and reproducibility were at least good regardless of the score, region, and protocol (0.67 ≤ AC1 ≤ 0.98). CRR was higher on T2 Dixon fat compared to T1 ( p &lt; 0.0001) and on T2 Dixon water compared to STIR ( p = 0.0128). In the per -patient analysis, Acc of the T2 Dixon fat+water was higher than that of T1+STIR for the senior reader (Acc = +0.027 [+0.025; +0.029], p &lt; 0.0001) and lower for the junior reader (Acc = −0.029 [−0.031; −0.027], p &lt; 0.0001). Conclusions A single T2 Dixon sequence with fat+water reconstructions offers similar reproducibility and diagnostic accuracy as the recommended combination of T1+STIR sequences and can be used for skeletal screening in oncology, allowing significant time-saving. Key Points • Replacement of the standard anatomic T1 + STIR WB-MRI protocol by a single T2 Dixon sequence drastically shortens the examination time without loss of diagnostic accuracy. • A protocol based on fat + water reconstructions from a single T2 Dixon sequence offers similar inter-reader agreement and a higher contrast-to-reference ratio for detecting lesions compared to the standard T1 + STIR protocol. • Differences in the accuracy between the two protocols are marginal (+ 3% in favor of the T2 Dixon with the senior reader; −3% against the T2 Dixon with the junior reader).</description><identifier>ISSN: 1432-1084</identifier><identifier>ISSN: 0938-7994</identifier><identifier>EISSN: 1432-1084</identifier><identifier>DOI: 10.1007/s00330-022-09007-8</identifier><identifier>PMID: 35925384</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Accuracy ; Aged ; Axial diffusion ; Bone marrow ; Conserved sequence ; Diagnostic Radiology ; Diagnostic systems ; Female ; Humans ; Image contrast ; Image quality ; Imaging ; Internal Medicine ; Interventional Radiology ; Lesions ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Male ; Medical imaging ; Medicine ; Medicine &amp; Public Health ; Metastases ; Metastasis ; Multiple myeloma ; Multiple Myeloma - diagnostic imaging ; Neuroendocrine tumors ; Neuroradiology ; Oncology ; Prostate ; Radiology ; Reproducibility ; Reproducibility of Results ; Signal quality ; Signal to noise ratio ; Ultrasound ; Water ; Whole Body Imaging - methods</subject><ispartof>European radiology, 2023-01, Vol.33 (1), p.244-257</ispartof><rights>The Author(s) 2022</rights><rights>2022. The Author(s).</rights><rights>The Author(s) 2022. 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-c474t-923acdbb0e4d7c891cb92ad0c5247dac86abd4784a1fd868fe0566d441f75f713</citedby><cites>FETCH-LOGICAL-c474t-923acdbb0e4d7c891cb92ad0c5247dac86abd4784a1fd868fe0566d441f75f713</cites><orcidid>0000-0003-3568-3254</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00330-022-09007-8$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00330-022-09007-8$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35925384$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chiabai, Ophelye</creatorcontrib><creatorcontrib>Van Nieuwenhove, Sandy</creatorcontrib><creatorcontrib>Vekemans, Marie-Christiane</creatorcontrib><creatorcontrib>Tombal, Bertrand</creatorcontrib><creatorcontrib>Peeters, Frank</creatorcontrib><creatorcontrib>Wuts, Joris</creatorcontrib><creatorcontrib>Triqueneaux, Perrine</creatorcontrib><creatorcontrib>Omoumi, Patrick</creatorcontrib><creatorcontrib>Kirchgesner, Thomas</creatorcontrib><creatorcontrib>Michoux, Nicolas</creatorcontrib><creatorcontrib>Lecouvet, Frédéric E.</creatorcontrib><title>Whole-body MRI in oncology: can a single anatomic T2 Dixon sequence replace the combination of T1 and STIR sequences to detect skeletal metastasis and myeloma?</title><title>European radiology</title><addtitle>Eur Radiol</addtitle><addtitle>Eur Radiol</addtitle><description>Objectives To compare the diagnostic accuracy of a single T2 Dixon sequence to the combination T1+STIR as anatomical sequences used for detecting tumoral bone marrow lesions in whole-body MRI (WB-MRI) examinations. Methods Between January 2019 and January 2020, seventy-two consecutive patients (55 men, 17 women, median age = 66 years) with solid (prostate, breast, neuroendocrine) cancers at high risk of metastasis or proven multiple myeloma (MM) prospectively underwent a WB-MRI examination including coronal T1, STIR, T2 Dixon and axial diffusion-weighted imaging sequences. Two radiologists independently assessed the combination of T1+STIR sequences and the fat+water reconstructions from the T2 Dixon sequence. The reference standard was established by consensus reading of WB-MRI and concurrent imaging available at baseline and at 6 months. Repeatability and reproducibility of MRI scores (presence and semi-quantitative count of lesions), image quality (SNR: signal-to-noise, CNR: contrast-to-noise, CRR: contrast-to-reference ratios), and diagnostic characteristics (Se: sensitivity, Sp: specificity, Acc: accuracy) were assessed per -skeletal region and per -patient. Results Repeatability and reproducibility were at least good regardless of the score, region, and protocol (0.67 ≤ AC1 ≤ 0.98). CRR was higher on T2 Dixon fat compared to T1 ( p &lt; 0.0001) and on T2 Dixon water compared to STIR ( p = 0.0128). In the per -patient analysis, Acc of the T2 Dixon fat+water was higher than that of T1+STIR for the senior reader (Acc = +0.027 [+0.025; +0.029], p &lt; 0.0001) and lower for the junior reader (Acc = −0.029 [−0.031; −0.027], p &lt; 0.0001). Conclusions A single T2 Dixon sequence with fat+water reconstructions offers similar reproducibility and diagnostic accuracy as the recommended combination of T1+STIR sequences and can be used for skeletal screening in oncology, allowing significant time-saving. Key Points • Replacement of the standard anatomic T1 + STIR WB-MRI protocol by a single T2 Dixon sequence drastically shortens the examination time without loss of diagnostic accuracy. • A protocol based on fat + water reconstructions from a single T2 Dixon sequence offers similar inter-reader agreement and a higher contrast-to-reference ratio for detecting lesions compared to the standard T1 + STIR protocol. • Differences in the accuracy between the two protocols are marginal (+ 3% in favor of the T2 Dixon with the senior reader; −3% against the T2 Dixon with the junior reader).</description><subject>Accuracy</subject><subject>Aged</subject><subject>Axial diffusion</subject><subject>Bone marrow</subject><subject>Conserved sequence</subject><subject>Diagnostic Radiology</subject><subject>Diagnostic systems</subject><subject>Female</subject><subject>Humans</subject><subject>Image contrast</subject><subject>Image quality</subject><subject>Imaging</subject><subject>Internal Medicine</subject><subject>Interventional Radiology</subject><subject>Lesions</subject><subject>Magnetic resonance imaging</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Medicine</subject><subject>Medicine &amp; Public Health</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Multiple myeloma</subject><subject>Multiple Myeloma - diagnostic imaging</subject><subject>Neuroendocrine tumors</subject><subject>Neuroradiology</subject><subject>Oncology</subject><subject>Prostate</subject><subject>Radiology</subject><subject>Reproducibility</subject><subject>Reproducibility of Results</subject><subject>Signal quality</subject><subject>Signal to noise ratio</subject><subject>Ultrasound</subject><subject>Water</subject><subject>Whole Body Imaging - methods</subject><issn>1432-1084</issn><issn>0938-7994</issn><issn>1432-1084</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kc1u1DAUhSMEoqXwAiyQJTZsAtc_iR0WVKj8jVSEVAaxtBz7ZsbFsYc4g5in4VUxnTIUFkiWr-X7nWNfnap6SOEpBZDPMgDnUANjNXTlola3qmMqOKspKHH7xvmoupfzJQB0VMi71RFvOtZwJY6rH5_XKWDdJ7cj7y8WxEeSok0hrXbPiTWRGJJ9XAUkJpo5jd6SJSOv_PcUScavW4wWyYSbYEqd10hsGntfUF-ANJAlLUJHPi4XFwc-kzkRhzPameQvGHA2gYxlz2X5fCUYdxjSaE7vV3cGEzI-uK4n1ac3r5dn7-rzD28XZy_PayukmOuOcWNd3wMKJ63qqO07ZhzYhgnpjFWt6Z2QShg6ONWqAaFpWycEHWQzSMpPqhd73822H9FZjPNkgt5MfjTTTifj9d-d6Nd6lb7pTjYNKFYMnlwbTKmMmWc9-mwxBBMxbbNmbadazhjnBX38D3qZtlMs42kmG9E2AAwKxfaUnVLOEw6Hz1DQv_LX-_x1yV9f5a9VET26OcZB8jvwAvA9kEsrrnD68_Z_bH8CFvy9XQ</recordid><startdate>20230101</startdate><enddate>20230101</enddate><creator>Chiabai, Ophelye</creator><creator>Van Nieuwenhove, Sandy</creator><creator>Vekemans, Marie-Christiane</creator><creator>Tombal, Bertrand</creator><creator>Peeters, Frank</creator><creator>Wuts, Joris</creator><creator>Triqueneaux, Perrine</creator><creator>Omoumi, Patrick</creator><creator>Kirchgesner, Thomas</creator><creator>Michoux, Nicolas</creator><creator>Lecouvet, Frédéric E.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>C6C</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>3V.</scope><scope>7QO</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3568-3254</orcidid></search><sort><creationdate>20230101</creationdate><title>Whole-body MRI in oncology: can a single anatomic T2 Dixon sequence replace the combination of T1 and STIR sequences to detect skeletal metastasis and myeloma?</title><author>Chiabai, Ophelye ; Van Nieuwenhove, Sandy ; Vekemans, Marie-Christiane ; Tombal, Bertrand ; Peeters, Frank ; Wuts, Joris ; Triqueneaux, Perrine ; Omoumi, Patrick ; Kirchgesner, Thomas ; Michoux, Nicolas ; Lecouvet, Frédéric E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-923acdbb0e4d7c891cb92ad0c5247dac86abd4784a1fd868fe0566d441f75f713</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Accuracy</topic><topic>Aged</topic><topic>Axial diffusion</topic><topic>Bone marrow</topic><topic>Conserved sequence</topic><topic>Diagnostic Radiology</topic><topic>Diagnostic systems</topic><topic>Female</topic><topic>Humans</topic><topic>Image contrast</topic><topic>Image quality</topic><topic>Imaging</topic><topic>Internal Medicine</topic><topic>Interventional Radiology</topic><topic>Lesions</topic><topic>Magnetic resonance imaging</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Male</topic><topic>Medical imaging</topic><topic>Medicine</topic><topic>Medicine &amp; Public Health</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Multiple myeloma</topic><topic>Multiple Myeloma - diagnostic imaging</topic><topic>Neuroendocrine tumors</topic><topic>Neuroradiology</topic><topic>Oncology</topic><topic>Prostate</topic><topic>Radiology</topic><topic>Reproducibility</topic><topic>Reproducibility of Results</topic><topic>Signal quality</topic><topic>Signal to noise ratio</topic><topic>Ultrasound</topic><topic>Water</topic><topic>Whole Body Imaging - methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chiabai, Ophelye</creatorcontrib><creatorcontrib>Van Nieuwenhove, Sandy</creatorcontrib><creatorcontrib>Vekemans, Marie-Christiane</creatorcontrib><creatorcontrib>Tombal, Bertrand</creatorcontrib><creatorcontrib>Peeters, Frank</creatorcontrib><creatorcontrib>Wuts, Joris</creatorcontrib><creatorcontrib>Triqueneaux, Perrine</creatorcontrib><creatorcontrib>Omoumi, Patrick</creatorcontrib><creatorcontrib>Kirchgesner, Thomas</creatorcontrib><creatorcontrib>Michoux, Nicolas</creatorcontrib><creatorcontrib>Lecouvet, Frédéric E.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; 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Methods Between January 2019 and January 2020, seventy-two consecutive patients (55 men, 17 women, median age = 66 years) with solid (prostate, breast, neuroendocrine) cancers at high risk of metastasis or proven multiple myeloma (MM) prospectively underwent a WB-MRI examination including coronal T1, STIR, T2 Dixon and axial diffusion-weighted imaging sequences. Two radiologists independently assessed the combination of T1+STIR sequences and the fat+water reconstructions from the T2 Dixon sequence. The reference standard was established by consensus reading of WB-MRI and concurrent imaging available at baseline and at 6 months. Repeatability and reproducibility of MRI scores (presence and semi-quantitative count of lesions), image quality (SNR: signal-to-noise, CNR: contrast-to-noise, CRR: contrast-to-reference ratios), and diagnostic characteristics (Se: sensitivity, Sp: specificity, Acc: accuracy) were assessed per -skeletal region and per -patient. Results Repeatability and reproducibility were at least good regardless of the score, region, and protocol (0.67 ≤ AC1 ≤ 0.98). CRR was higher on T2 Dixon fat compared to T1 ( p &lt; 0.0001) and on T2 Dixon water compared to STIR ( p = 0.0128). In the per -patient analysis, Acc of the T2 Dixon fat+water was higher than that of T1+STIR for the senior reader (Acc = +0.027 [+0.025; +0.029], p &lt; 0.0001) and lower for the junior reader (Acc = −0.029 [−0.031; −0.027], p &lt; 0.0001). Conclusions A single T2 Dixon sequence with fat+water reconstructions offers similar reproducibility and diagnostic accuracy as the recommended combination of T1+STIR sequences and can be used for skeletal screening in oncology, allowing significant time-saving. Key Points • Replacement of the standard anatomic T1 + STIR WB-MRI protocol by a single T2 Dixon sequence drastically shortens the examination time without loss of diagnostic accuracy. • A protocol based on fat + water reconstructions from a single T2 Dixon sequence offers similar inter-reader agreement and a higher contrast-to-reference ratio for detecting lesions compared to the standard T1 + STIR protocol. • Differences in the accuracy between the two protocols are marginal (+ 3% in favor of the T2 Dixon with the senior reader; −3% against the T2 Dixon with the junior reader).</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>35925384</pmid><doi>10.1007/s00330-022-09007-8</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3568-3254</orcidid><oa>free_for_read</oa></addata></record>
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subjects Accuracy
Aged
Axial diffusion
Bone marrow
Conserved sequence
Diagnostic Radiology
Diagnostic systems
Female
Humans
Image contrast
Image quality
Imaging
Internal Medicine
Interventional Radiology
Lesions
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Male
Medical imaging
Medicine
Medicine & Public Health
Metastases
Metastasis
Multiple myeloma
Multiple Myeloma - diagnostic imaging
Neuroendocrine tumors
Neuroradiology
Oncology
Prostate
Radiology
Reproducibility
Reproducibility of Results
Signal quality
Signal to noise ratio
Ultrasound
Water
Whole Body Imaging - methods
title Whole-body MRI in oncology: can a single anatomic T2 Dixon sequence replace the combination of T1 and STIR sequences to detect skeletal metastasis and myeloma?
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T02%3A16%3A35IST&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=Whole-body%20MRI%20in%20oncology:%20can%20a%20single%20anatomic%20T2%20Dixon%20sequence%20replace%20the%20combination%20of%20T1%20and%20STIR%20sequences%20to%20detect%20skeletal%20metastasis%20and%20myeloma?&rft.jtitle=European%20radiology&rft.au=Chiabai,%20Ophelye&rft.date=2023-01-01&rft.volume=33&rft.issue=1&rft.spage=244&rft.epage=257&rft.pages=244-257&rft.issn=1432-1084&rft.eissn=1432-1084&rft_id=info:doi/10.1007/s00330-022-09007-8&rft_dat=%3Cproquest_pubme%3E2698632233%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=2754650020&rft_id=info:pmid/35925384&rfr_iscdi=true