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Bone Marrow Metabolism Is Impaired in Insulin Resistance and Improves After Exercise Training

Abstract Context Exercise training improves bone mineral density, but little is known about the effects of training on bone marrow (BM) metabolism. BM insulin sensitivity has been suggested to play an important role in bone health and whole-body insulin sensitivity. Objective To study the effects of...

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Published in:The journal of clinical endocrinology and metabolism 2020-12, Vol.105 (12), p.1-e4303
Main Authors: Ojala, Ronja, Motiani, Kumail K, Ivaska, Kaisa K, Arponen, Milja, Eskelinen, Jari-Joonas, Virtanen, Kirsi A, Löyttyniemi, Eliisa, Heiskanen, Marja A, U-Din, Mueez, Nuutila, Pirjo, Kalliokoski, Kari K, Hannukainen, Jarna C
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creator Ojala, Ronja
Motiani, Kumail K
Ivaska, Kaisa K
Arponen, Milja
Eskelinen, Jari-Joonas
Virtanen, Kirsi A
Löyttyniemi, Eliisa
Heiskanen, Marja A
U-Din, Mueez
Nuutila, Pirjo
Kalliokoski, Kari K
Hannukainen, Jarna C
description Abstract Context Exercise training improves bone mineral density, but little is known about the effects of training on bone marrow (BM) metabolism. BM insulin sensitivity has been suggested to play an important role in bone health and whole-body insulin sensitivity. Objective To study the effects of exercise training on BM metabolism. Design Randomized controlled trial. Setting Clinical research center. Participants Sedentary healthy (n = 28, 40–55 years, all males) and insulin resistant (IR) subjects (n = 26, 43–55 years, males/females 16/10) Intervention Two weeks of sprint interval training or moderate-intensity continuous training Main outcome measures We measured femoral, lumbar, and thoracic BM insulin-stimulated glucose uptake (GU) and fasting free fatty acid uptake (FFAU) using positron-emission tomography and bone turnover markers from plasma. Results At baseline, GU was highest in lumbar, followed by thoracic, and lowest in femoral BM (all Ps 
doi_str_mv 10.1210/clinem/dgaa516
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BM insulin sensitivity has been suggested to play an important role in bone health and whole-body insulin sensitivity. Objective To study the effects of exercise training on BM metabolism. Design Randomized controlled trial. Setting Clinical research center. Participants Sedentary healthy (n = 28, 40–55 years, all males) and insulin resistant (IR) subjects (n = 26, 43–55 years, males/females 16/10) Intervention Two weeks of sprint interval training or moderate-intensity continuous training Main outcome measures We measured femoral, lumbar, and thoracic BM insulin-stimulated glucose uptake (GU) and fasting free fatty acid uptake (FFAU) using positron-emission tomography and bone turnover markers from plasma. Results At baseline, GU was highest in lumbar, followed by thoracic, and lowest in femoral BM (all Ps &lt; 0.0001). FFAU was higher in lumbar and thoracic than femoral BM (both Ps &lt; 0.0001). BM FFAU and femoral BM GU were higher in healthy compared to IR men and in females compared to males (all Ps &lt; 0.05). Training increased femoral BM GU similarly in all groups and decreased lumbar BM FFAU in males (all Ps &lt; 0.05). Osteocalcin and PINP were lower in IR than healthy men and correlated positively with femoral BM GU and glycemic status (all Ps &lt; 0.05). Conclusions BM metabolism differs regarding anatomical location. Short-term training improves BM GU and FFAU in healthy and IR subjects. Bone turnover rate is decreased in insulin resistance and associates positively with BM metabolism and glycemic control. Clinical Trial Registration Number NCT01344928.</description><identifier>ISSN: 0021-972X</identifier><identifier>EISSN: 1945-7197</identifier><identifier>DOI: 10.1210/clinem/dgaa516</identifier><identifier>PMID: 32785654</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adult ; Bone marrow ; Bone Marrow - metabolism ; Bone mineral density ; Bone turnover ; Clinical s ; Exercise ; Exercise - physiology ; Female ; Femur ; Fitness training programs ; Health aspects ; Humans ; Insulin ; Insulin resistance ; Insulin Resistance - physiology ; Male ; Males ; Metabolism ; Middle Aged ; Osteocalcin ; Physical training ; Physiological aspects ; Positron emission tomography ; Sedentary Behavior ; Thorax</subject><ispartof>The journal of clinical endocrinology and metabolism, 2020-12, Vol.105 (12), p.1-e4303</ispartof><rights>Endocrine Society 2020. 2020</rights><rights>Endocrine Society 2020.</rights><rights>COPYRIGHT 2020 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c519t-e5aca52ba248a9f4747ce4d5dc0cab79ceba2363d37f2c266c664528b0f3f16c3</citedby><cites>FETCH-LOGICAL-c519t-e5aca52ba248a9f4747ce4d5dc0cab79ceba2363d37f2c266c664528b0f3f16c3</cites><orcidid>0000-0002-8692-4049 ; 0000-0002-2393-0281 ; 0000-0001-9597-338X</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/32785654$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ojala, Ronja</creatorcontrib><creatorcontrib>Motiani, Kumail K</creatorcontrib><creatorcontrib>Ivaska, Kaisa K</creatorcontrib><creatorcontrib>Arponen, Milja</creatorcontrib><creatorcontrib>Eskelinen, Jari-Joonas</creatorcontrib><creatorcontrib>Virtanen, Kirsi A</creatorcontrib><creatorcontrib>Löyttyniemi, Eliisa</creatorcontrib><creatorcontrib>Heiskanen, Marja A</creatorcontrib><creatorcontrib>U-Din, Mueez</creatorcontrib><creatorcontrib>Nuutila, Pirjo</creatorcontrib><creatorcontrib>Kalliokoski, Kari K</creatorcontrib><creatorcontrib>Hannukainen, Jarna C</creatorcontrib><title>Bone Marrow Metabolism Is Impaired in Insulin Resistance and Improves After Exercise Training</title><title>The journal of clinical endocrinology and metabolism</title><addtitle>J Clin Endocrinol Metab</addtitle><description>Abstract Context Exercise training improves bone mineral density, but little is known about the effects of training on bone marrow (BM) metabolism. BM insulin sensitivity has been suggested to play an important role in bone health and whole-body insulin sensitivity. Objective To study the effects of exercise training on BM metabolism. Design Randomized controlled trial. Setting Clinical research center. Participants Sedentary healthy (n = 28, 40–55 years, all males) and insulin resistant (IR) subjects (n = 26, 43–55 years, males/females 16/10) Intervention Two weeks of sprint interval training or moderate-intensity continuous training Main outcome measures We measured femoral, lumbar, and thoracic BM insulin-stimulated glucose uptake (GU) and fasting free fatty acid uptake (FFAU) using positron-emission tomography and bone turnover markers from plasma. Results At baseline, GU was highest in lumbar, followed by thoracic, and lowest in femoral BM (all Ps &lt; 0.0001). FFAU was higher in lumbar and thoracic than femoral BM (both Ps &lt; 0.0001). BM FFAU and femoral BM GU were higher in healthy compared to IR men and in females compared to males (all Ps &lt; 0.05). Training increased femoral BM GU similarly in all groups and decreased lumbar BM FFAU in males (all Ps &lt; 0.05). Osteocalcin and PINP were lower in IR than healthy men and correlated positively with femoral BM GU and glycemic status (all Ps &lt; 0.05). Conclusions BM metabolism differs regarding anatomical location. Short-term training improves BM GU and FFAU in healthy and IR subjects. Bone turnover rate is decreased in insulin resistance and associates positively with BM metabolism and glycemic control. Clinical Trial Registration Number NCT01344928.</description><subject>Adult</subject><subject>Bone marrow</subject><subject>Bone Marrow - metabolism</subject><subject>Bone mineral density</subject><subject>Bone turnover</subject><subject>Clinical s</subject><subject>Exercise</subject><subject>Exercise - physiology</subject><subject>Female</subject><subject>Femur</subject><subject>Fitness training programs</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Insulin</subject><subject>Insulin resistance</subject><subject>Insulin Resistance - physiology</subject><subject>Male</subject><subject>Males</subject><subject>Metabolism</subject><subject>Middle Aged</subject><subject>Osteocalcin</subject><subject>Physical training</subject><subject>Physiological aspects</subject><subject>Positron emission tomography</subject><subject>Sedentary Behavior</subject><subject>Thorax</subject><issn>0021-972X</issn><issn>1945-7197</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqFkt9rFDEQx4Mo9nr66qMEfNGHbfM7uy_CWaoetAhSwRcJ2ezsmbKbnMlutf-9Oe6sPyjIPARmPvMdZvJF6BklJ5RRcuoGH2A87TbWSqoeoAVthKw0bfRDtCCE0arR7PMROs75mhAqhOSP0RFnupZKigX68iYGwJc2pfgdX8Jk2zj4POJ1xutxa32CDvuA1yHPZRL-CNnnyQYH2IZuh6R4Axmv-gkSPv8ByfkM-CpZH3zYPEGPejtkeHp4l-jT2_Ors_fVxYd367PVReUkbaYKpHVWstYyUdumF1poB6KTnSPOtrpxUEpc8Y7rnjmmlFNKSFa3pOc9VY4v0eu97nZuR-gchCnZwWyTH226NdF683cl-K9mE2-MlkzporxELw8CKX6bIU9m9NnBMNgAcc6GCS6ILDdrCvriH_Q6zimU9QqlKWENr_VvamMHMD70scx1O1GzUrKpuVBsR53cQ5XoYPSu_EzvS_6-Bpdizgn6ux0pMTtDmL0hzMEQpeH5n5e5w385oACv9kCct_8T-wnsnsGs</recordid><startdate>20201201</startdate><enddate>20201201</enddate><creator>Ojala, Ronja</creator><creator>Motiani, Kumail K</creator><creator>Ivaska, Kaisa K</creator><creator>Arponen, Milja</creator><creator>Eskelinen, Jari-Joonas</creator><creator>Virtanen, Kirsi A</creator><creator>Löyttyniemi, Eliisa</creator><creator>Heiskanen, Marja A</creator><creator>U-Din, Mueez</creator><creator>Nuutila, Pirjo</creator><creator>Kalliokoski, Kari K</creator><creator>Hannukainen, Jarna C</creator><general>Oxford University Press</general><scope>TOX</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>7QP</scope><scope>7T5</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8692-4049</orcidid><orcidid>https://orcid.org/0000-0002-2393-0281</orcidid><orcidid>https://orcid.org/0000-0001-9597-338X</orcidid></search><sort><creationdate>20201201</creationdate><title>Bone Marrow Metabolism Is Impaired in Insulin Resistance and Improves After Exercise Training</title><author>Ojala, Ronja ; Motiani, Kumail K ; Ivaska, Kaisa K ; Arponen, Milja ; Eskelinen, Jari-Joonas ; Virtanen, Kirsi A ; Löyttyniemi, Eliisa ; Heiskanen, Marja A ; U-Din, Mueez ; Nuutila, Pirjo ; Kalliokoski, Kari K ; Hannukainen, Jarna C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c519t-e5aca52ba248a9f4747ce4d5dc0cab79ceba2363d37f2c266c664528b0f3f16c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Bone marrow</topic><topic>Bone Marrow - metabolism</topic><topic>Bone mineral density</topic><topic>Bone turnover</topic><topic>Clinical s</topic><topic>Exercise</topic><topic>Exercise - physiology</topic><topic>Female</topic><topic>Femur</topic><topic>Fitness training programs</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Insulin</topic><topic>Insulin resistance</topic><topic>Insulin Resistance - physiology</topic><topic>Male</topic><topic>Males</topic><topic>Metabolism</topic><topic>Middle Aged</topic><topic>Osteocalcin</topic><topic>Physical training</topic><topic>Physiological aspects</topic><topic>Positron emission tomography</topic><topic>Sedentary Behavior</topic><topic>Thorax</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ojala, Ronja</creatorcontrib><creatorcontrib>Motiani, Kumail K</creatorcontrib><creatorcontrib>Ivaska, Kaisa K</creatorcontrib><creatorcontrib>Arponen, Milja</creatorcontrib><creatorcontrib>Eskelinen, Jari-Joonas</creatorcontrib><creatorcontrib>Virtanen, Kirsi A</creatorcontrib><creatorcontrib>Löyttyniemi, Eliisa</creatorcontrib><creatorcontrib>Heiskanen, Marja A</creatorcontrib><creatorcontrib>U-Din, Mueez</creatorcontrib><creatorcontrib>Nuutila, Pirjo</creatorcontrib><creatorcontrib>Kalliokoski, Kari K</creatorcontrib><creatorcontrib>Hannukainen, Jarna C</creatorcontrib><collection>Open Access: Oxford University Press Open 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>Calcium &amp; 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BM insulin sensitivity has been suggested to play an important role in bone health and whole-body insulin sensitivity. Objective To study the effects of exercise training on BM metabolism. Design Randomized controlled trial. Setting Clinical research center. Participants Sedentary healthy (n = 28, 40–55 years, all males) and insulin resistant (IR) subjects (n = 26, 43–55 years, males/females 16/10) Intervention Two weeks of sprint interval training or moderate-intensity continuous training Main outcome measures We measured femoral, lumbar, and thoracic BM insulin-stimulated glucose uptake (GU) and fasting free fatty acid uptake (FFAU) using positron-emission tomography and bone turnover markers from plasma. Results At baseline, GU was highest in lumbar, followed by thoracic, and lowest in femoral BM (all Ps &lt; 0.0001). FFAU was higher in lumbar and thoracic than femoral BM (both Ps &lt; 0.0001). BM FFAU and femoral BM GU were higher in healthy compared to IR men and in females compared to males (all Ps &lt; 0.05). Training increased femoral BM GU similarly in all groups and decreased lumbar BM FFAU in males (all Ps &lt; 0.05). Osteocalcin and PINP were lower in IR than healthy men and correlated positively with femoral BM GU and glycemic status (all Ps &lt; 0.05). Conclusions BM metabolism differs regarding anatomical location. Short-term training improves BM GU and FFAU in healthy and IR subjects. Bone turnover rate is decreased in insulin resistance and associates positively with BM metabolism and glycemic control. 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subjects Adult
Bone marrow
Bone Marrow - metabolism
Bone mineral density
Bone turnover
Clinical s
Exercise
Exercise - physiology
Female
Femur
Fitness training programs
Health aspects
Humans
Insulin
Insulin resistance
Insulin Resistance - physiology
Male
Males
Metabolism
Middle Aged
Osteocalcin
Physical training
Physiological aspects
Positron emission tomography
Sedentary Behavior
Thorax
title Bone Marrow Metabolism Is Impaired in Insulin Resistance and Improves After Exercise Training
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