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Plasma lipid profiling of tissue-specific insulin resistance in human obesity
Obesity-associated insulin resistance (IR) may develop in multiple organs, representing different aetiologies towards cardiometabolic diseases. This study aimed to identify distinct plasma lipid profiles in overweight/obese individuals who show muscle-IR and/or liver-IR. Baseline data of the Europea...
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Published in: | International Journal of Obesity 2019-05, Vol.43 (5), p.989-998 |
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container_end_page | 998 |
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container_title | International Journal of Obesity |
container_volume | 43 |
creator | van der Kolk, Birgitta W Vogelzangs, Nicole Jocken, Johan W E Valsesia, Armand Hankemeier, Thomas Astrup, Arne Saris, Wim H M Arts, Ilja C W van Greevenbroek, Marleen M J Blaak, Ellen E |
description | Obesity-associated insulin resistance (IR) may develop in multiple organs, representing different aetiologies towards cardiometabolic diseases. This study aimed to identify distinct plasma lipid profiles in overweight/obese individuals who show muscle-IR and/or liver-IR.
Baseline data of the European multicenter DiOGenes project were used (n = 640; 401 women, nondiabetic BMI: 27-45 kg/m
). Muscle insulin sensitivity index (MISI) and hepatic insulin resistance index (HIRI) were derived from a 5-point oral glucose tolerance test. The 140 plasma lipids were quantified by liquid chromatography-mass spectrometry. Linear mixed models were used to evaluate associations between MISI, HIRI and plasma lipids.
MISI was comparable between sexes while HIRI and triacylglycerol (TAG) levels were lower in women than in men. MISI was associated with higher lysophosphatidylcholine (LPC) levels (standardized (std)β = 0.126; FDR-p = 0.032). Sex interactions were observed for associations between HIRI, TAG and diacylglycerol (DAG) lipid classes. In women, but not in men, HIRI was associated with higher levels of TAG (44 out of 55 species) and both DAG species (stdβ: 0.139-0.313; FDR-p |
doi_str_mv | 10.1038/s41366-018-0189-8 |
format | article |
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Baseline data of the European multicenter DiOGenes project were used (n = 640; 401 women, nondiabetic BMI: 27-45 kg/m
). Muscle insulin sensitivity index (MISI) and hepatic insulin resistance index (HIRI) were derived from a 5-point oral glucose tolerance test. The 140 plasma lipids were quantified by liquid chromatography-mass spectrometry. Linear mixed models were used to evaluate associations between MISI, HIRI and plasma lipids.
MISI was comparable between sexes while HIRI and triacylglycerol (TAG) levels were lower in women than in men. MISI was associated with higher lysophosphatidylcholine (LPC) levels (standardized (std)β = 0.126; FDR-p = 0.032). Sex interactions were observed for associations between HIRI, TAG and diacylglycerol (DAG) lipid classes. In women, but not in men, HIRI was associated with higher levels of TAG (44 out of 55 species) and both DAG species (stdβ: 0.139-0.313; FDR-p < 0.05), a lower odd-chain/even-chain TAG ratio (stdβ = -0.182; FDR-p = 0.005) and a lower very-long-chain/long-chain TAG ratio (stdβ = -0.156; FDR-p = 0.037).
In overweight/obese individuals, muscle insulin sensitivity is associated with higher plasma LPC concentrations. Women have less hepatic IR and lower TAG than men. Nevertheless, hepatic IR is associated with higher plasma TAG and DAG concentrations and a lower abundance of odd-chain and very-long-chain TAG in women, but not in men. This suggests a more pronounced worsening of plasma lipid profile in women with the progression of hepatic IR.</description><identifier>ISSN: 0307-0565</identifier><identifier>EISSN: 1476-5497</identifier><identifier>DOI: 10.1038/s41366-018-0189-8</identifier><identifier>PMID: 30242234</identifier><language>eng</language><publisher>England: Nature Publishing Group</publisher><subject>Adult ; Biomarkers - metabolism ; Blood lipids ; Body mass ; Body weight ; Care and treatment ; Chains ; Chromatography ; Chromatography, Liquid ; Diglycerides ; Female ; Glucose ; Glucose tolerance ; Glucose Tolerance Test ; Humans ; Insulin ; Insulin resistance ; Insulin Resistance - physiology ; Lipid Metabolism - physiology ; Lipids ; Lipids - blood ; Liquid chromatography ; Liver ; Lysophosphatidylcholine ; Male ; Mass spectrometry ; Mass spectroscopy ; Medical research ; Men ; Middle Aged ; Muscle, Skeletal - metabolism ; Muscles ; Obesity ; Obesity - metabolism ; Obesity - physiopathology ; Organs ; Overweight ; Phospholipids ; Sensitivity ; Sexually transmitted diseases ; Signal Transduction ; Spectroscopy ; STD ; Triglycerides ; Type 2 diabetes ; Women ; Young Adult</subject><ispartof>International Journal of Obesity, 2019-05, Vol.43 (5), p.989-998</ispartof><rights>COPYRIGHT 2019 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group May 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-c457079fdd8cf851bda0456540352431e64c0ec4e9ecbe3dcb6e3c730a3ca5b33</citedby><cites>FETCH-LOGICAL-c470t-c457079fdd8cf851bda0456540352431e64c0ec4e9ecbe3dcb6e3c730a3ca5b33</cites><orcidid>0000-0001-8968-8996 ; 0000-0002-2496-3464 ; 0000-0001-6462-6692 ; 0000-0003-0746-9664 ; 0000-0001-8608-541X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30242234$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van der Kolk, Birgitta W</creatorcontrib><creatorcontrib>Vogelzangs, Nicole</creatorcontrib><creatorcontrib>Jocken, Johan W E</creatorcontrib><creatorcontrib>Valsesia, Armand</creatorcontrib><creatorcontrib>Hankemeier, Thomas</creatorcontrib><creatorcontrib>Astrup, Arne</creatorcontrib><creatorcontrib>Saris, Wim H M</creatorcontrib><creatorcontrib>Arts, Ilja C W</creatorcontrib><creatorcontrib>van Greevenbroek, Marleen M J</creatorcontrib><creatorcontrib>Blaak, Ellen E</creatorcontrib><creatorcontrib>DiOGenes consortium</creatorcontrib><creatorcontrib>the DiOGenes consortium</creatorcontrib><title>Plasma lipid profiling of tissue-specific insulin resistance in human obesity</title><title>International Journal of Obesity</title><addtitle>Int J Obes (Lond)</addtitle><description>Obesity-associated insulin resistance (IR) may develop in multiple organs, representing different aetiologies towards cardiometabolic diseases. This study aimed to identify distinct plasma lipid profiles in overweight/obese individuals who show muscle-IR and/or liver-IR.
Baseline data of the European multicenter DiOGenes project were used (n = 640; 401 women, nondiabetic BMI: 27-45 kg/m
). Muscle insulin sensitivity index (MISI) and hepatic insulin resistance index (HIRI) were derived from a 5-point oral glucose tolerance test. The 140 plasma lipids were quantified by liquid chromatography-mass spectrometry. Linear mixed models were used to evaluate associations between MISI, HIRI and plasma lipids.
MISI was comparable between sexes while HIRI and triacylglycerol (TAG) levels were lower in women than in men. MISI was associated with higher lysophosphatidylcholine (LPC) levels (standardized (std)β = 0.126; FDR-p = 0.032). Sex interactions were observed for associations between HIRI, TAG and diacylglycerol (DAG) lipid classes. In women, but not in men, HIRI was associated with higher levels of TAG (44 out of 55 species) and both DAG species (stdβ: 0.139-0.313; FDR-p < 0.05), a lower odd-chain/even-chain TAG ratio (stdβ = -0.182; FDR-p = 0.005) and a lower very-long-chain/long-chain TAG ratio (stdβ = -0.156; FDR-p = 0.037).
In overweight/obese individuals, muscle insulin sensitivity is associated with higher plasma LPC concentrations. Women have less hepatic IR and lower TAG than men. Nevertheless, hepatic IR is associated with higher plasma TAG and DAG concentrations and a lower abundance of odd-chain and very-long-chain TAG in women, but not in men. This suggests a more pronounced worsening of plasma lipid profile in women with the progression of hepatic IR.</description><subject>Adult</subject><subject>Biomarkers - metabolism</subject><subject>Blood lipids</subject><subject>Body mass</subject><subject>Body weight</subject><subject>Care and treatment</subject><subject>Chains</subject><subject>Chromatography</subject><subject>Chromatography, Liquid</subject><subject>Diglycerides</subject><subject>Female</subject><subject>Glucose</subject><subject>Glucose tolerance</subject><subject>Glucose Tolerance Test</subject><subject>Humans</subject><subject>Insulin</subject><subject>Insulin resistance</subject><subject>Insulin Resistance - physiology</subject><subject>Lipid Metabolism - physiology</subject><subject>Lipids</subject><subject>Lipids - blood</subject><subject>Liquid chromatography</subject><subject>Liver</subject><subject>Lysophosphatidylcholine</subject><subject>Male</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Medical research</subject><subject>Men</subject><subject>Middle Aged</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Muscles</subject><subject>Obesity</subject><subject>Obesity - metabolism</subject><subject>Obesity - physiopathology</subject><subject>Organs</subject><subject>Overweight</subject><subject>Phospholipids</subject><subject>Sensitivity</subject><subject>Sexually transmitted diseases</subject><subject>Signal Transduction</subject><subject>Spectroscopy</subject><subject>STD</subject><subject>Triglycerides</subject><subject>Type 2 diabetes</subject><subject>Women</subject><subject>Young Adult</subject><issn>0307-0565</issn><issn>1476-5497</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNptkctu1TAQhi0EoqeFB2CDIiEhNinjWxwvq6pQpCJYwNpynEmPq8Q-ZJJF3x5Hp1yKsDVjafzN6Ld_xl5xOOcg2_ekuGyaGni7ha3bJ2zHlWlqrax5ynYgwdSgG33CTonuAEBrEM_ZiQShhJBqxz5_HT1NvhrjIfbVYc5DHGO6rfJQLZFoxZoOGOIQQxUTreWumpEiLT4FLKVqv04-VbkrxeX-BXs2-JHw5cN5xr5_uPp2eV3ffPn46fLipg7KwFKyNmDs0PdtGFrNu96DKjIVSC2U5NioABgUWgwdyj50DcpgJHgZvO6kPGPvjnOL4B8r0uKmSAHH0SfMKznBy9K85aagb_5B7_I6p6LOCSG44BZs-4e69SO6mIa8zD5sQ92FbpXRVlso1Pl_qLJ7nGLICcvn4eOGt3817NGPy57yuC4xJ3oM8iMY5kw04-AOc5z8fO84uM1rd_TaFZ-3sG7T_PrhZWs3Yf-745e58ieOPaHk</recordid><startdate>20190501</startdate><enddate>20190501</enddate><creator>van der Kolk, Birgitta W</creator><creator>Vogelzangs, Nicole</creator><creator>Jocken, Johan W E</creator><creator>Valsesia, Armand</creator><creator>Hankemeier, Thomas</creator><creator>Astrup, Arne</creator><creator>Saris, Wim H M</creator><creator>Arts, Ilja C W</creator><creator>van Greevenbroek, Marleen M J</creator><creator>Blaak, Ellen E</creator><general>Nature Publishing Group</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>3V.</scope><scope>7T2</scope><scope>7TK</scope><scope>7TS</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8C1</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8968-8996</orcidid><orcidid>https://orcid.org/0000-0002-2496-3464</orcidid><orcidid>https://orcid.org/0000-0001-6462-6692</orcidid><orcidid>https://orcid.org/0000-0003-0746-9664</orcidid><orcidid>https://orcid.org/0000-0001-8608-541X</orcidid></search><sort><creationdate>20190501</creationdate><title>Plasma lipid profiling of tissue-specific insulin resistance in human obesity</title><author>van der Kolk, Birgitta W ; Vogelzangs, Nicole ; Jocken, Johan W E ; Valsesia, Armand ; Hankemeier, Thomas ; Astrup, Arne ; Saris, Wim H M ; Arts, Ilja C W ; van Greevenbroek, Marleen M J ; Blaak, Ellen E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-c457079fdd8cf851bda0456540352431e64c0ec4e9ecbe3dcb6e3c730a3ca5b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Biomarkers - metabolism</topic><topic>Blood lipids</topic><topic>Body mass</topic><topic>Body weight</topic><topic>Care and treatment</topic><topic>Chains</topic><topic>Chromatography</topic><topic>Chromatography, Liquid</topic><topic>Diglycerides</topic><topic>Female</topic><topic>Glucose</topic><topic>Glucose tolerance</topic><topic>Glucose Tolerance Test</topic><topic>Humans</topic><topic>Insulin</topic><topic>Insulin resistance</topic><topic>Insulin Resistance - physiology</topic><topic>Lipid Metabolism - physiology</topic><topic>Lipids</topic><topic>Lipids - blood</topic><topic>Liquid chromatography</topic><topic>Liver</topic><topic>Lysophosphatidylcholine</topic><topic>Male</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Medical research</topic><topic>Men</topic><topic>Middle Aged</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Muscles</topic><topic>Obesity</topic><topic>Obesity - metabolism</topic><topic>Obesity - physiopathology</topic><topic>Organs</topic><topic>Overweight</topic><topic>Phospholipids</topic><topic>Sensitivity</topic><topic>Sexually transmitted diseases</topic><topic>Signal Transduction</topic><topic>Spectroscopy</topic><topic>STD</topic><topic>Triglycerides</topic><topic>Type 2 diabetes</topic><topic>Women</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van der Kolk, Birgitta W</creatorcontrib><creatorcontrib>Vogelzangs, Nicole</creatorcontrib><creatorcontrib>Jocken, Johan W E</creatorcontrib><creatorcontrib>Valsesia, Armand</creatorcontrib><creatorcontrib>Hankemeier, Thomas</creatorcontrib><creatorcontrib>Astrup, Arne</creatorcontrib><creatorcontrib>Saris, Wim H M</creatorcontrib><creatorcontrib>Arts, Ilja C W</creatorcontrib><creatorcontrib>van Greevenbroek, Marleen M J</creatorcontrib><creatorcontrib>Blaak, Ellen E</creatorcontrib><creatorcontrib>DiOGenes consortium</creatorcontrib><creatorcontrib>the DiOGenes consortium</creatorcontrib><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>Health and Safety Science Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest Public Health Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database (ProQuest)</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>International Journal of Obesity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van der Kolk, Birgitta W</au><au>Vogelzangs, Nicole</au><au>Jocken, Johan W E</au><au>Valsesia, Armand</au><au>Hankemeier, Thomas</au><au>Astrup, Arne</au><au>Saris, Wim H M</au><au>Arts, Ilja C W</au><au>van Greevenbroek, Marleen M J</au><au>Blaak, Ellen E</au><aucorp>DiOGenes consortium</aucorp><aucorp>the DiOGenes consortium</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plasma lipid profiling of tissue-specific insulin resistance in human obesity</atitle><jtitle>International Journal of Obesity</jtitle><addtitle>Int J Obes (Lond)</addtitle><date>2019-05-01</date><risdate>2019</risdate><volume>43</volume><issue>5</issue><spage>989</spage><epage>998</epage><pages>989-998</pages><issn>0307-0565</issn><eissn>1476-5497</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-News-2</notes><notes>ObjectType-Feature-3</notes><notes>content type line 23</notes><abstract>Obesity-associated insulin resistance (IR) may develop in multiple organs, representing different aetiologies towards cardiometabolic diseases. This study aimed to identify distinct plasma lipid profiles in overweight/obese individuals who show muscle-IR and/or liver-IR.
Baseline data of the European multicenter DiOGenes project were used (n = 640; 401 women, nondiabetic BMI: 27-45 kg/m
). Muscle insulin sensitivity index (MISI) and hepatic insulin resistance index (HIRI) were derived from a 5-point oral glucose tolerance test. The 140 plasma lipids were quantified by liquid chromatography-mass spectrometry. Linear mixed models were used to evaluate associations between MISI, HIRI and plasma lipids.
MISI was comparable between sexes while HIRI and triacylglycerol (TAG) levels were lower in women than in men. MISI was associated with higher lysophosphatidylcholine (LPC) levels (standardized (std)β = 0.126; FDR-p = 0.032). Sex interactions were observed for associations between HIRI, TAG and diacylglycerol (DAG) lipid classes. In women, but not in men, HIRI was associated with higher levels of TAG (44 out of 55 species) and both DAG species (stdβ: 0.139-0.313; FDR-p < 0.05), a lower odd-chain/even-chain TAG ratio (stdβ = -0.182; FDR-p = 0.005) and a lower very-long-chain/long-chain TAG ratio (stdβ = -0.156; FDR-p = 0.037).
In overweight/obese individuals, muscle insulin sensitivity is associated with higher plasma LPC concentrations. Women have less hepatic IR and lower TAG than men. Nevertheless, hepatic IR is associated with higher plasma TAG and DAG concentrations and a lower abundance of odd-chain and very-long-chain TAG in women, but not in men. This suggests a more pronounced worsening of plasma lipid profile in women with the progression of hepatic IR.</abstract><cop>England</cop><pub>Nature Publishing Group</pub><pmid>30242234</pmid><doi>10.1038/s41366-018-0189-8</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-8968-8996</orcidid><orcidid>https://orcid.org/0000-0002-2496-3464</orcidid><orcidid>https://orcid.org/0000-0001-6462-6692</orcidid><orcidid>https://orcid.org/0000-0003-0746-9664</orcidid><orcidid>https://orcid.org/0000-0001-8608-541X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Biomarkers - metabolism Blood lipids Body mass Body weight Care and treatment Chains Chromatography Chromatography, Liquid Diglycerides Female Glucose Glucose tolerance Glucose Tolerance Test Humans Insulin Insulin resistance Insulin Resistance - physiology Lipid Metabolism - physiology Lipids Lipids - blood Liquid chromatography Liver Lysophosphatidylcholine Male Mass spectrometry Mass spectroscopy Medical research Men Middle Aged Muscle, Skeletal - metabolism Muscles Obesity Obesity - metabolism Obesity - physiopathology Organs Overweight Phospholipids Sensitivity Sexually transmitted diseases Signal Transduction Spectroscopy STD Triglycerides Type 2 diabetes Women Young Adult |
title | Plasma lipid profiling of tissue-specific insulin resistance in human obesity |
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