Fuel Selection in Skeletal Muscle Exercising at Low Intensity; Reliance on Carbohydrate in Very Sedentary Individuals

Background: Resting skeletal muscle in insulin resistance prefers to oxidize carbohydrate rather than lipid, exhibiting metabolic inflexibility. Although this is established in resting muscle, complexities involved in directly measuring fuel oxidation using indirect calorimetry across a muscle bed h...

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Veröffentlicht in:Metabolic syndrome and related disorders 2023-02, Vol.21 (1), p.16-24
Hauptverfasser: Barakati, Neusha, Bustos, Rocio Zapata, Coletta, Dawn K, Langlais, Paul R, Kohler, Lindsay N, Luo, Moulun, Funk, Janet L, Willis, Wayne T, Mandarino, Lawrence J
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container_end_page 24
container_issue 1
container_start_page 16
container_title Metabolic syndrome and related disorders
container_volume 21
creator Barakati, Neusha
Bustos, Rocio Zapata
Coletta, Dawn K
Langlais, Paul R
Kohler, Lindsay N
Luo, Moulun
Funk, Janet L
Willis, Wayne T
Mandarino, Lawrence J
description Background: Resting skeletal muscle in insulin resistance prefers to oxidize carbohydrate rather than lipid, exhibiting metabolic inflexibility. Although this is established in resting muscle, complexities involved in directly measuring fuel oxidation using indirect calorimetry across a muscle bed have limited studies of this phenomenon in working skeletal muscle. During mild exercise and at rest, whole-body indirect calorimetry imperfectly estimates muscle fuel oxidation. We provide evidence that a method termed “ΔRER” can reasonably estimate fuel oxidation in skeletal muscle activated by exercise. Methods: Completely sedentary volunteers ( n  = 20, age 31 ± 2 years, V̇O 2peak 24.4 ± 1.5 mL O 2 per min/kg) underwent glucose clamps to determine insulin sensitivity and graded exercise consisting of three periods of mild steady-state cycle ergometry (15, 30, 45 watts, or 10%, 20%, and 30% of maximum power) with measurements of whole-body gas exchange. ΔRER, the RER in working muscle, was calculated as (V̇CO2 exercise –V̇CO 2rest )/(V̇O 2exercise – V̇O 2rest ), from which the fraction of fuel accounted for by lipid was estimated. Results: Lactate levels were low and stable during steady-state exercise. Muscle biopsies were used to estimate mitochondrial content. The rise of V̇O 2 at onset of exercise followed a monoexponential function, with a time constant of 51 ± 7 sec, typical of skeletal muscle; the average O 2 cost of work was about 12 mL O 2 /watt/min, representing a mechanical efficiency of about 24%. At work rates of 30 or 45 watts, active muscle relied predominantly on carbohydrate, independent of insulin sensitivity within this group of very sedentary volunteers. Conclusions: The fraction of muscle fuel oxidation from fat was predicted by power output ( P  
doi_str_mv 10.1089/met.2022.0062
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Although this is established in resting muscle, complexities involved in directly measuring fuel oxidation using indirect calorimetry across a muscle bed have limited studies of this phenomenon in working skeletal muscle. During mild exercise and at rest, whole-body indirect calorimetry imperfectly estimates muscle fuel oxidation. We provide evidence that a method termed “ΔRER” can reasonably estimate fuel oxidation in skeletal muscle activated by exercise. Methods: Completely sedentary volunteers ( n  = 20, age 31 ± 2 years, V̇O 2peak 24.4 ± 1.5 mL O 2 per min/kg) underwent glucose clamps to determine insulin sensitivity and graded exercise consisting of three periods of mild steady-state cycle ergometry (15, 30, 45 watts, or 10%, 20%, and 30% of maximum power) with measurements of whole-body gas exchange. ΔRER, the RER in working muscle, was calculated as (V̇CO2 exercise –V̇CO 2rest )/(V̇O 2exercise – V̇O 2rest ), from which the fraction of fuel accounted for by lipid was estimated. Results: Lactate levels were low and stable during steady-state exercise. Muscle biopsies were used to estimate mitochondrial content. The rise of V̇O 2 at onset of exercise followed a monoexponential function, with a time constant of 51 ± 7 sec, typical of skeletal muscle; the average O 2 cost of work was about 12 mL O 2 /watt/min, representing a mechanical efficiency of about 24%. At work rates of 30 or 45 watts, active muscle relied predominantly on carbohydrate, independent of insulin sensitivity within this group of very sedentary volunteers. Conclusions: The fraction of muscle fuel oxidation from fat was predicted by power output ( P  &lt; 0.001) and citrate synthase activity ( P  &lt; 0.05), indicating that low mitochondrial content may be the main driver of fuel choice in sedentary people, independent of insulin sensitivity.</description><identifier>ISSN: 1540-4196</identifier><identifier>EISSN: 1557-8518</identifier><identifier>DOI: 10.1089/met.2022.0062</identifier><identifier>PMID: 36318809</identifier><language>eng</language><publisher>United States: Mary Ann Liebert, Inc., publishers</publisher><subject>Adult ; Carbohydrates ; Exercise - physiology ; Humans ; Insulin Resistance ; Lipids ; Muscle, Skeletal - metabolism ; Original ; Original Articles ; Oxygen Consumption</subject><ispartof>Metabolic syndrome and related disorders, 2023-02, Vol.21 (1), p.16-24</ispartof><rights>2023, Mary Ann Liebert, Inc., publishers</rights><rights>Copyright 2023, Mary Ann Liebert, Inc., publishers 2023 Mary Ann Liebert, Inc., publishers</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c392t-3dac51af4824bedcfe58d6a082de29a35a3bfd1a4af2bfc21e708e5e18de66993</citedby><cites>FETCH-LOGICAL-c392t-3dac51af4824bedcfe58d6a082de29a35a3bfd1a4af2bfc21e708e5e18de66993</cites><orcidid>0000-0003-0982-8229</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36318809$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barakati, Neusha</creatorcontrib><creatorcontrib>Bustos, Rocio Zapata</creatorcontrib><creatorcontrib>Coletta, Dawn K</creatorcontrib><creatorcontrib>Langlais, Paul R</creatorcontrib><creatorcontrib>Kohler, Lindsay N</creatorcontrib><creatorcontrib>Luo, Moulun</creatorcontrib><creatorcontrib>Funk, Janet L</creatorcontrib><creatorcontrib>Willis, Wayne T</creatorcontrib><creatorcontrib>Mandarino, Lawrence J</creatorcontrib><title>Fuel Selection in Skeletal Muscle Exercising at Low Intensity; Reliance on Carbohydrate in Very Sedentary Individuals</title><title>Metabolic syndrome and related disorders</title><addtitle>Metab Syndr Relat Disord</addtitle><description>Background: Resting skeletal muscle in insulin resistance prefers to oxidize carbohydrate rather than lipid, exhibiting metabolic inflexibility. Although this is established in resting muscle, complexities involved in directly measuring fuel oxidation using indirect calorimetry across a muscle bed have limited studies of this phenomenon in working skeletal muscle. During mild exercise and at rest, whole-body indirect calorimetry imperfectly estimates muscle fuel oxidation. We provide evidence that a method termed “ΔRER” can reasonably estimate fuel oxidation in skeletal muscle activated by exercise. Methods: Completely sedentary volunteers ( n  = 20, age 31 ± 2 years, V̇O 2peak 24.4 ± 1.5 mL O 2 per min/kg) underwent glucose clamps to determine insulin sensitivity and graded exercise consisting of three periods of mild steady-state cycle ergometry (15, 30, 45 watts, or 10%, 20%, and 30% of maximum power) with measurements of whole-body gas exchange. ΔRER, the RER in working muscle, was calculated as (V̇CO2 exercise –V̇CO 2rest )/(V̇O 2exercise – V̇O 2rest ), from which the fraction of fuel accounted for by lipid was estimated. Results: Lactate levels were low and stable during steady-state exercise. Muscle biopsies were used to estimate mitochondrial content. The rise of V̇O 2 at onset of exercise followed a monoexponential function, with a time constant of 51 ± 7 sec, typical of skeletal muscle; the average O 2 cost of work was about 12 mL O 2 /watt/min, representing a mechanical efficiency of about 24%. At work rates of 30 or 45 watts, active muscle relied predominantly on carbohydrate, independent of insulin sensitivity within this group of very sedentary volunteers. Conclusions: The fraction of muscle fuel oxidation from fat was predicted by power output ( P  &lt; 0.001) and citrate synthase activity ( P  &lt; 0.05), indicating that low mitochondrial content may be the main driver of fuel choice in sedentary people, independent of insulin sensitivity.</description><subject>Adult</subject><subject>Carbohydrates</subject><subject>Exercise - physiology</subject><subject>Humans</subject><subject>Insulin Resistance</subject><subject>Lipids</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Original</subject><subject>Original Articles</subject><subject>Oxygen Consumption</subject><issn>1540-4196</issn><issn>1557-8518</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc9rFDEUx4MotlaPXiVHL7Pmx8xsgiDI0urCimDVa3iTvGmj2UxNMtX9782wtejJ03tJPvm8B19CnnO24kzpV3ssK8GEWDHWiwfklHfdulEdVw-XvmVNy3V_Qp7k_I1VjLPuMTmRveRKMX1K5osZA73EgLb4KVIf6eX3eioQ6Ic524D0_Bcm67OPVxQK3U0_6TYWjNmXw2v6CYOHaJHWvxtIw3R9cAkKLqKvmA5V7TAWqN02On_r3QwhPyWPxlrw2V09I18uzj9v3je7j--2m7e7xkotSiMd2I7D2CrRDujsiJ1yPTAlHAoNsgM5jI5DC6MYRis4rpnCDrly2PdayzPy5ui9mYd9FdRNEgRzk_y-bmQm8Obfl-ivzdV0a7TutVJ9Fby8E6Tpx4y5mL3PFkOAiNOcjVhL3oq-bXlFmyNq05RzwvF-DGdmicrUqMwSlVmiqvyLv3e7p_9kUwF5BJZriDF4HDCV_2h_A9NmpGk</recordid><startdate>20230201</startdate><enddate>20230201</enddate><creator>Barakati, Neusha</creator><creator>Bustos, Rocio Zapata</creator><creator>Coletta, Dawn K</creator><creator>Langlais, Paul R</creator><creator>Kohler, Lindsay N</creator><creator>Luo, Moulun</creator><creator>Funk, Janet L</creator><creator>Willis, Wayne T</creator><creator>Mandarino, Lawrence J</creator><general>Mary Ann Liebert, Inc., publishers</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0982-8229</orcidid></search><sort><creationdate>20230201</creationdate><title>Fuel Selection in Skeletal Muscle Exercising at Low Intensity; Reliance on Carbohydrate in Very Sedentary Individuals</title><author>Barakati, Neusha ; Bustos, Rocio Zapata ; Coletta, Dawn K ; Langlais, Paul R ; Kohler, Lindsay N ; Luo, Moulun ; Funk, Janet L ; Willis, Wayne T ; Mandarino, Lawrence J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c392t-3dac51af4824bedcfe58d6a082de29a35a3bfd1a4af2bfc21e708e5e18de66993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Adult</topic><topic>Carbohydrates</topic><topic>Exercise - physiology</topic><topic>Humans</topic><topic>Insulin Resistance</topic><topic>Lipids</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Original</topic><topic>Original Articles</topic><topic>Oxygen Consumption</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barakati, Neusha</creatorcontrib><creatorcontrib>Bustos, Rocio Zapata</creatorcontrib><creatorcontrib>Coletta, Dawn K</creatorcontrib><creatorcontrib>Langlais, Paul R</creatorcontrib><creatorcontrib>Kohler, Lindsay N</creatorcontrib><creatorcontrib>Luo, Moulun</creatorcontrib><creatorcontrib>Funk, Janet L</creatorcontrib><creatorcontrib>Willis, Wayne T</creatorcontrib><creatorcontrib>Mandarino, Lawrence J</creatorcontrib><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>Metabolic syndrome and related disorders</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barakati, Neusha</au><au>Bustos, Rocio Zapata</au><au>Coletta, Dawn K</au><au>Langlais, Paul R</au><au>Kohler, Lindsay N</au><au>Luo, Moulun</au><au>Funk, Janet L</au><au>Willis, Wayne T</au><au>Mandarino, Lawrence J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fuel Selection in Skeletal Muscle Exercising at Low Intensity; Reliance on Carbohydrate in Very Sedentary Individuals</atitle><jtitle>Metabolic syndrome and related disorders</jtitle><addtitle>Metab Syndr Relat Disord</addtitle><date>2023-02-01</date><risdate>2023</risdate><volume>21</volume><issue>1</issue><spage>16</spage><epage>24</epage><pages>16-24</pages><issn>1540-4196</issn><eissn>1557-8518</eissn><abstract>Background: Resting skeletal muscle in insulin resistance prefers to oxidize carbohydrate rather than lipid, exhibiting metabolic inflexibility. Although this is established in resting muscle, complexities involved in directly measuring fuel oxidation using indirect calorimetry across a muscle bed have limited studies of this phenomenon in working skeletal muscle. During mild exercise and at rest, whole-body indirect calorimetry imperfectly estimates muscle fuel oxidation. We provide evidence that a method termed “ΔRER” can reasonably estimate fuel oxidation in skeletal muscle activated by exercise. Methods: Completely sedentary volunteers ( n  = 20, age 31 ± 2 years, V̇O 2peak 24.4 ± 1.5 mL O 2 per min/kg) underwent glucose clamps to determine insulin sensitivity and graded exercise consisting of three periods of mild steady-state cycle ergometry (15, 30, 45 watts, or 10%, 20%, and 30% of maximum power) with measurements of whole-body gas exchange. ΔRER, the RER in working muscle, was calculated as (V̇CO2 exercise –V̇CO 2rest )/(V̇O 2exercise – V̇O 2rest ), from which the fraction of fuel accounted for by lipid was estimated. Results: Lactate levels were low and stable during steady-state exercise. Muscle biopsies were used to estimate mitochondrial content. The rise of V̇O 2 at onset of exercise followed a monoexponential function, with a time constant of 51 ± 7 sec, typical of skeletal muscle; the average O 2 cost of work was about 12 mL O 2 /watt/min, representing a mechanical efficiency of about 24%. At work rates of 30 or 45 watts, active muscle relied predominantly on carbohydrate, independent of insulin sensitivity within this group of very sedentary volunteers. Conclusions: The fraction of muscle fuel oxidation from fat was predicted by power output ( P  &lt; 0.001) and citrate synthase activity ( P  &lt; 0.05), indicating that low mitochondrial content may be the main driver of fuel choice in sedentary people, independent of insulin sensitivity.</abstract><cop>United States</cop><pub>Mary Ann Liebert, Inc., publishers</pub><pmid>36318809</pmid><doi>10.1089/met.2022.0062</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0003-0982-8229</orcidid></addata></record>
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subjects Adult
Carbohydrates
Exercise - physiology
Humans
Insulin Resistance
Lipids
Muscle, Skeletal - metabolism
Original
Original Articles
Oxygen Consumption
title Fuel Selection in Skeletal Muscle Exercising at Low Intensity; Reliance on Carbohydrate in Very Sedentary Individuals
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