Superior sagittal sinus flow as a proxy for tracking global cerebral blood flow dynamics during wakefulness and sleep
Sleep, a state of reduced consciousness, affects brain oxygen metabolism and lowers cerebral metabolic rate of oxygen (CMRO2). Previously, we quantified CMRO2 during sleep via Fick’s Principle, with a single-band MRI sequence measuring both hemoglobin O2 saturation (SvO2) and superior sagittal sinus...
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Veröffentlicht in: | Journal of cerebral blood flow and metabolism 2023-08, Vol.43 (8), p.1340-1350 |
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creator | Caporale, Alessandra S Barclay, Alexander M Xu, Jing Rao, Hengyi Lee, Hyunyeol Langham, Michael C Detre, John A Wehrli, Felix W |
description | Sleep, a state of reduced consciousness, affects brain oxygen metabolism and lowers cerebral metabolic rate of oxygen (CMRO2). Previously, we quantified CMRO2 during sleep via Fick’s Principle, with a single-band MRI sequence measuring both hemoglobin O2 saturation (SvO2) and superior sagittal sinus (SSS) blood flow, which was upscaled to obtain total cerebral blood flow (tCBF). The procedure involves a brief initial calibration scan to determine the upscaling factor (fc), assumed state-invariant. Here, we used a dual-band sequence to simultaneously provide SvO2 in SSS and tCBF in the neck every 16 seconds, allowing quantification of fc dynamically. Ten healthy subjects were scanned by MRI with simultaneous EEG for 80 minutes, yielding 300 temporal image frames per subject. Four volunteers achieved slow-wave sleep (SWS), as evidenced by increased δ-wave activity (per American Academy of Sleep Medicine criteria). SWS was maintained for 13.5 ± 7.0 minutes, with CMRO2 28.6 ± 5.5% lower than pre-sleep wakefulness. Importantly, there was negligible bias between tCBF obtained by upscaling SSS-blood flow, and tCBF measured directly in the inflowing arteries of the neck (intra-class correlation 0.95 ± 0.04, averaged across all subjects), showing that the single-band approach is a valid substitute for quantifying tCBF, simplifying image data collection and analysis without sacrificing accuracy. |
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Previously, we quantified CMRO2 during sleep via Fick’s Principle, with a single-band MRI sequence measuring both hemoglobin O2 saturation (SvO2) and superior sagittal sinus (SSS) blood flow, which was upscaled to obtain total cerebral blood flow (tCBF). The procedure involves a brief initial calibration scan to determine the upscaling factor (fc), assumed state-invariant. Here, we used a dual-band sequence to simultaneously provide SvO2 in SSS and tCBF in the neck every 16 seconds, allowing quantification of fc dynamically. Ten healthy subjects were scanned by MRI with simultaneous EEG for 80 minutes, yielding 300 temporal image frames per subject. Four volunteers achieved slow-wave sleep (SWS), as evidenced by increased δ-wave activity (per American Academy of Sleep Medicine criteria). SWS was maintained for 13.5 ± 7.0 minutes, with CMRO2 28.6 ± 5.5% lower than pre-sleep wakefulness. Importantly, there was negligible bias between tCBF obtained by upscaling SSS-blood flow, and tCBF measured directly in the inflowing arteries of the neck (intra-class correlation 0.95 ± 0.04, averaged across all subjects), showing that the single-band approach is a valid substitute for quantifying tCBF, simplifying image data collection and analysis without sacrificing accuracy.</description><identifier>ISSN: 0271-678X</identifier><identifier>EISSN: 1559-7016</identifier><identifier>DOI: 10.1177/0271678X231164423</identifier><identifier>PMID: 36927172</identifier><language>eng</language><publisher>London, England: SAGE Publications</publisher><subject>Brain - blood supply ; Cerebrovascular Circulation - physiology ; Humans ; Magnetic Resonance Imaging - methods ; Original ; Oxygen - metabolism ; Oxygen Consumption - physiology ; Sleep ; Superior Sagittal Sinus - diagnostic imaging ; Wakefulness - physiology</subject><ispartof>Journal of cerebral blood flow and metabolism, 2023-08, Vol.43 (8), p.1340-1350</ispartof><rights>The Author(s) 2023</rights><rights>The Author(s) 2023 2023 International Society for Cerebral Blood Flow and Metabolism</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c391t-6368399ca90faf3cc03f853564d5e98054307f80190f12d1e4952183057004833</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10369151/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10369151/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,21819,27924,27925,43621,43622,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36927172$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Caporale, Alessandra S</creatorcontrib><creatorcontrib>Barclay, Alexander M</creatorcontrib><creatorcontrib>Xu, Jing</creatorcontrib><creatorcontrib>Rao, Hengyi</creatorcontrib><creatorcontrib>Lee, Hyunyeol</creatorcontrib><creatorcontrib>Langham, Michael C</creatorcontrib><creatorcontrib>Detre, John A</creatorcontrib><creatorcontrib>Wehrli, Felix W</creatorcontrib><title>Superior sagittal sinus flow as a proxy for tracking global cerebral blood flow dynamics during wakefulness and sleep</title><title>Journal of cerebral blood flow and metabolism</title><addtitle>J Cereb Blood Flow Metab</addtitle><description>Sleep, a state of reduced consciousness, affects brain oxygen metabolism and lowers cerebral metabolic rate of oxygen (CMRO2). Previously, we quantified CMRO2 during sleep via Fick’s Principle, with a single-band MRI sequence measuring both hemoglobin O2 saturation (SvO2) and superior sagittal sinus (SSS) blood flow, which was upscaled to obtain total cerebral blood flow (tCBF). The procedure involves a brief initial calibration scan to determine the upscaling factor (fc), assumed state-invariant. Here, we used a dual-band sequence to simultaneously provide SvO2 in SSS and tCBF in the neck every 16 seconds, allowing quantification of fc dynamically. Ten healthy subjects were scanned by MRI with simultaneous EEG for 80 minutes, yielding 300 temporal image frames per subject. Four volunteers achieved slow-wave sleep (SWS), as evidenced by increased δ-wave activity (per American Academy of Sleep Medicine criteria). SWS was maintained for 13.5 ± 7.0 minutes, with CMRO2 28.6 ± 5.5% lower than pre-sleep wakefulness. Importantly, there was negligible bias between tCBF obtained by upscaling SSS-blood flow, and tCBF measured directly in the inflowing arteries of the neck (intra-class correlation 0.95 ± 0.04, averaged across all subjects), showing that the single-band approach is a valid substitute for quantifying tCBF, simplifying image data collection and analysis without sacrificing accuracy.</description><subject>Brain - blood supply</subject><subject>Cerebrovascular Circulation - physiology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Original</subject><subject>Oxygen - metabolism</subject><subject>Oxygen Consumption - physiology</subject><subject>Sleep</subject><subject>Superior Sagittal Sinus - diagnostic imaging</subject><subject>Wakefulness - physiology</subject><issn>0271-678X</issn><issn>1559-7016</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>AFRWT</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU9vFSEUxYnR2NfqB3BjWLqZyuXPDKyMadSaNHGhTbojPAae0_JghKH1ffvy8mqjaeIKkvM7h8s9CL0BcgowDO8JHaAf5BVlAD3nlD1DKxBCdQOB_jla7fVuDxyh41KuCSGSCfESHbFeNWmgK1S_19nlKWVczGZaFhNwmWIt2Id0h03BBs85_d5h35AlG3szxQ3ehLRupHXZrXO7rENK48Ey7qLZTrbgseY9emdunK8hutKy4ohLcG5-hV54E4p7_XCeoMvPn36cnXcX3758Pft40VmmYOl61kumlDWKeOOZtYR5KZjo-SickkRwRgYvCTQd6AiOK0FBMiIGQrhk7AR9OOTOdb11o3WxfSHoOU9bk3c6mUn_q8Tpp96kWw2krQgEtIR3Dwk5_aquLHo7FetCMNGlWjSVnFDOgaqGwgG1OZWSnX98B4je96Wf9NU8b_8e8NHxp6AGnB6AVo_T16nm2Bb2n8R7fQ6fCg</recordid><startdate>20230801</startdate><enddate>20230801</enddate><creator>Caporale, Alessandra S</creator><creator>Barclay, Alexander M</creator><creator>Xu, Jing</creator><creator>Rao, Hengyi</creator><creator>Lee, Hyunyeol</creator><creator>Langham, Michael C</creator><creator>Detre, John A</creator><creator>Wehrli, Felix W</creator><general>SAGE Publications</general><scope>AFRWT</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20230801</creationdate><title>Superior sagittal sinus flow as a proxy for tracking global cerebral blood flow dynamics during wakefulness and sleep</title><author>Caporale, Alessandra S ; Barclay, Alexander M ; Xu, Jing ; Rao, Hengyi ; Lee, Hyunyeol ; Langham, Michael C ; Detre, John A ; Wehrli, Felix W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c391t-6368399ca90faf3cc03f853564d5e98054307f80190f12d1e4952183057004833</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Brain - blood supply</topic><topic>Cerebrovascular Circulation - physiology</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Original</topic><topic>Oxygen - metabolism</topic><topic>Oxygen Consumption - physiology</topic><topic>Sleep</topic><topic>Superior Sagittal Sinus - diagnostic imaging</topic><topic>Wakefulness - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Caporale, Alessandra S</creatorcontrib><creatorcontrib>Barclay, Alexander M</creatorcontrib><creatorcontrib>Xu, Jing</creatorcontrib><creatorcontrib>Rao, Hengyi</creatorcontrib><creatorcontrib>Lee, Hyunyeol</creatorcontrib><creatorcontrib>Langham, Michael C</creatorcontrib><creatorcontrib>Detre, John A</creatorcontrib><creatorcontrib>Wehrli, Felix W</creatorcontrib><collection>Sage Journals GOLD Open Access 2024</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cerebral blood flow and metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Caporale, Alessandra S</au><au>Barclay, Alexander M</au><au>Xu, Jing</au><au>Rao, Hengyi</au><au>Lee, Hyunyeol</au><au>Langham, Michael C</au><au>Detre, John A</au><au>Wehrli, Felix W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Superior sagittal sinus flow as a proxy for tracking global cerebral blood flow dynamics during wakefulness and sleep</atitle><jtitle>Journal of cerebral blood flow and metabolism</jtitle><addtitle>J Cereb Blood Flow Metab</addtitle><date>2023-08-01</date><risdate>2023</risdate><volume>43</volume><issue>8</issue><spage>1340</spage><epage>1350</epage><pages>1340-1350</pages><issn>0271-678X</issn><eissn>1559-7016</eissn><abstract>Sleep, a state of reduced consciousness, affects brain oxygen metabolism and lowers cerebral metabolic rate of oxygen (CMRO2). Previously, we quantified CMRO2 during sleep via Fick’s Principle, with a single-band MRI sequence measuring both hemoglobin O2 saturation (SvO2) and superior sagittal sinus (SSS) blood flow, which was upscaled to obtain total cerebral blood flow (tCBF). The procedure involves a brief initial calibration scan to determine the upscaling factor (fc), assumed state-invariant. Here, we used a dual-band sequence to simultaneously provide SvO2 in SSS and tCBF in the neck every 16 seconds, allowing quantification of fc dynamically. Ten healthy subjects were scanned by MRI with simultaneous EEG for 80 minutes, yielding 300 temporal image frames per subject. Four volunteers achieved slow-wave sleep (SWS), as evidenced by increased δ-wave activity (per American Academy of Sleep Medicine criteria). SWS was maintained for 13.5 ± 7.0 minutes, with CMRO2 28.6 ± 5.5% lower than pre-sleep wakefulness. Importantly, there was negligible bias between tCBF obtained by upscaling SSS-blood flow, and tCBF measured directly in the inflowing arteries of the neck (intra-class correlation 0.95 ± 0.04, averaged across all subjects), showing that the single-band approach is a valid substitute for quantifying tCBF, simplifying image data collection and analysis without sacrificing accuracy.</abstract><cop>London, England</cop><pub>SAGE Publications</pub><pmid>36927172</pmid><doi>10.1177/0271678X231164423</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Brain - blood supply Cerebrovascular Circulation - physiology Humans Magnetic Resonance Imaging - methods Original Oxygen - metabolism Oxygen Consumption - physiology Sleep Superior Sagittal Sinus - diagnostic imaging Wakefulness - physiology |
title | Superior sagittal sinus flow as a proxy for tracking global cerebral blood flow dynamics during wakefulness and sleep |
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