Circulating bile acids in healthy adults respond differently to a dietary pattern characterized by whole grains, legumes and fruits and vegetables compared to a diet high in refined grains and added sugars: A randomized, controlled, crossover feeding study
The effects of diets high in refined grains on biliary and colonic bile acids have been investigated extensively. However, the effects of diets high in whole versus refined grains on circulating bile acids, which can influence glucose homeostasis and inflammation through activation of farnesoid X re...
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| creator | Ginos, Bigina N.R. Navarro, Sandi L. Schwarz, Yvonne Gu, Haiwei Wang, Dongfang Randolph, Timothy W. Shojaie, Ali Hullar, Meredith A.J. Lampe, Paul D. Kratz, Mario Neuhouser, Marian L. Raftery, Daniel Lampe, Johanna W. |
| description | The effects of diets high in refined grains on biliary and colonic bile acids have been investigated extensively. However, the effects of diets high in whole versus refined grains on circulating bile acids, which can influence glucose homeostasis and inflammation through activation of farnesoid X receptor (FXR) and G protein-coupled bile acid receptor 1 (TGR5), have not been studied.
We conducted a secondary analysis from a randomized controlled crossover feeding trial (NCT00622661) in 80 healthy adults (40 women/40 men, age 18–45 years) from the greater Seattle Area, half of which were normal weight (BMI 18.5–25.0 kg/m2) and half overweight to obese (BMI 28.0–39.9 kg/m2). Participants consumed two four-week controlled diets in randomized order: 1) a whole grain diet (WG diet), designed to be low in glycemic load (GL), high in whole grains, legumes, and fruits and vegetables, and 2) a refined grain diet (RG diet), designed to be high GL, high in refined grains and added sugars, separated by a four-week washout period. Quantitative targeted analysis of 55 bile acid species in fasting plasma was performed using liquid chromatography tandem mass spectrometry. Concentrations of glucose, insulin, and CRP were measured in fasting serum. Linear mixed models were used to test the effects of diet on bile acid concentrations, and determine the association between plasma bile acid concentrations and HOMA-IR and CRP. Benjamini-Hochberg false discovery rate (FDR) |
| doi_str_mv | 10.1016/j.metabol.2018.02.006 |
| format | Article |
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We conducted a secondary analysis from a randomized controlled crossover feeding trial (NCT00622661) in 80 healthy adults (40 women/40 men, age 18–45 years) from the greater Seattle Area, half of which were normal weight (BMI 18.5–25.0 kg/m2) and half overweight to obese (BMI 28.0–39.9 kg/m2). Participants consumed two four-week controlled diets in randomized order: 1) a whole grain diet (WG diet), designed to be low in glycemic load (GL), high in whole grains, legumes, and fruits and vegetables, and 2) a refined grain diet (RG diet), designed to be high GL, high in refined grains and added sugars, separated by a four-week washout period. Quantitative targeted analysis of 55 bile acid species in fasting plasma was performed using liquid chromatography tandem mass spectrometry. Concentrations of glucose, insulin, and CRP were measured in fasting serum. Linear mixed models were used to test the effects of diet on bile acid concentrations, and determine the association between plasma bile acid concentrations and HOMA-IR and CRP. Benjamini-Hochberg false discovery rate (FDR) < 0.05 was used to control for multiple testing.
A total of 29 plasma bile acids were reliably detected and retained for analysis. Taurolithocholic acid (TLCA), taurocholic acid (TCA) and glycocholic acid (GCA) were statistically significantly higher after the WG compared to the RG diet (FDR < 0.05). There were no significant differences by BMI or sex. When evaluating the association of bile acids and HOMA-IR, GCA, taurochenodeoxycholic acid, ursodeoxycholic acid (UDCA), 5β‑cholanic acid‑3β,12α‑diol, 5‑cholanic acid‑3β‑ol, and glycodeoxycholic acid (GDCA) were statistically significantly positively associated with HOMA-IR individually, and as a group, total, 12α‑hydroxylated, primary and secondary bile acids were also significant (FDR < 0.05). When stratifying by BMI, chenodeoxycholic acid (CDCA), cholic acid (CA), UDCA, 5β-cholanic acid-3β, deoxycholic acid, and total, 12α-hydroxylated, primary and secondary bile acid groups were significantly positively associated with HOMA-IR among overweight to obese individuals (FDR < 0.05). When stratifying by sex, GCA, CDCA, TCA, CA, UDCA, GDCA, glycolithocholic acid (GLCA), total, primary, 12α‑hydroxylated, and glycine-conjugated bile acids were significantly associated with HOMA-IR among women, and CDCA, GDCA, and GLCA were significantly associated among men (FDR < 0.05). There were no significant associations between bile acids and CRP.
Diets with comparable macronutrient and energy composition, but differing in carbohydrate source, affected fasting plasma bile acids differently. Specifically, a diet characterized by whole grains, legumes, and fruits and vegetables compared to a diet high in refined grains and added sugars led to modest increases in concentrations of TLCA, TCA and GCA, ligands for FXR and TGR5, which may have beneficial effects on glucose homeostasis.
•Three plasma bile acids increased after a whole versus refined grain diet pattern.•There were significant positive associations between bile acids and HOMA-IR.•Diet patterns varying in carbohydrate type affect plasma bile acids differently.</description><identifier>ISSN: 0026-0495</identifier><identifier>EISSN: 1532-8600</identifier><identifier>DOI: 10.1016/j.metabol.2018.02.006</identifier><identifier>PMID: 29458053</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adolescent ; Adult ; Bile acid ; Bile Acids and Salts - blood ; Cross-Over Studies ; Diet ; Dietary Carbohydrates - pharmacology ; Dietary patterns ; Edible Grain - physiology ; Fabaceae - physiology ; Feeding Behavior - physiology ; Feeding study ; Female ; Fruit - physiology ; FXR ; Healthy Volunteers ; Humans ; Insulin resistance ; Male ; Middle Aged ; Sugars ; Vegetables - physiology ; Whole grains ; Whole Grains - physiology ; Young Adult</subject><ispartof>Metabolism, clinical and experimental, 2018-06, Vol.83, p.197-204</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c467t-a57a1b7ef6baf4121201feae1e72caa65d50215b46dae74a4a78e73a5282d5353</citedby><cites>FETCH-LOGICAL-c467t-a57a1b7ef6baf4121201feae1e72caa65d50215b46dae74a4a78e73a5282d5353</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0026049518300453$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29458053$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ginos, Bigina N.R.</creatorcontrib><creatorcontrib>Navarro, Sandi L.</creatorcontrib><creatorcontrib>Schwarz, Yvonne</creatorcontrib><creatorcontrib>Gu, Haiwei</creatorcontrib><creatorcontrib>Wang, Dongfang</creatorcontrib><creatorcontrib>Randolph, Timothy W.</creatorcontrib><creatorcontrib>Shojaie, Ali</creatorcontrib><creatorcontrib>Hullar, Meredith A.J.</creatorcontrib><creatorcontrib>Lampe, Paul D.</creatorcontrib><creatorcontrib>Kratz, Mario</creatorcontrib><creatorcontrib>Neuhouser, Marian L.</creatorcontrib><creatorcontrib>Raftery, Daniel</creatorcontrib><creatorcontrib>Lampe, Johanna W.</creatorcontrib><title>Circulating bile acids in healthy adults respond differently to a dietary pattern characterized by whole grains, legumes and fruits and vegetables compared to a diet high in refined grains and added sugars: A randomized, controlled, crossover feeding study</title><title>Metabolism, clinical and experimental</title><addtitle>Metabolism</addtitle><description>The effects of diets high in refined grains on biliary and colonic bile acids have been investigated extensively. However, the effects of diets high in whole versus refined grains on circulating bile acids, which can influence glucose homeostasis and inflammation through activation of farnesoid X receptor (FXR) and G protein-coupled bile acid receptor 1 (TGR5), have not been studied.
We conducted a secondary analysis from a randomized controlled crossover feeding trial (NCT00622661) in 80 healthy adults (40 women/40 men, age 18–45 years) from the greater Seattle Area, half of which were normal weight (BMI 18.5–25.0 kg/m2) and half overweight to obese (BMI 28.0–39.9 kg/m2). Participants consumed two four-week controlled diets in randomized order: 1) a whole grain diet (WG diet), designed to be low in glycemic load (GL), high in whole grains, legumes, and fruits and vegetables, and 2) a refined grain diet (RG diet), designed to be high GL, high in refined grains and added sugars, separated by a four-week washout period. Quantitative targeted analysis of 55 bile acid species in fasting plasma was performed using liquid chromatography tandem mass spectrometry. Concentrations of glucose, insulin, and CRP were measured in fasting serum. Linear mixed models were used to test the effects of diet on bile acid concentrations, and determine the association between plasma bile acid concentrations and HOMA-IR and CRP. Benjamini-Hochberg false discovery rate (FDR) < 0.05 was used to control for multiple testing.
A total of 29 plasma bile acids were reliably detected and retained for analysis. Taurolithocholic acid (TLCA), taurocholic acid (TCA) and glycocholic acid (GCA) were statistically significantly higher after the WG compared to the RG diet (FDR < 0.05). There were no significant differences by BMI or sex. When evaluating the association of bile acids and HOMA-IR, GCA, taurochenodeoxycholic acid, ursodeoxycholic acid (UDCA), 5β‑cholanic acid‑3β,12α‑diol, 5‑cholanic acid‑3β‑ol, and glycodeoxycholic acid (GDCA) were statistically significantly positively associated with HOMA-IR individually, and as a group, total, 12α‑hydroxylated, primary and secondary bile acids were also significant (FDR < 0.05). When stratifying by BMI, chenodeoxycholic acid (CDCA), cholic acid (CA), UDCA, 5β-cholanic acid-3β, deoxycholic acid, and total, 12α-hydroxylated, primary and secondary bile acid groups were significantly positively associated with HOMA-IR among overweight to obese individuals (FDR < 0.05). When stratifying by sex, GCA, CDCA, TCA, CA, UDCA, GDCA, glycolithocholic acid (GLCA), total, primary, 12α‑hydroxylated, and glycine-conjugated bile acids were significantly associated with HOMA-IR among women, and CDCA, GDCA, and GLCA were significantly associated among men (FDR < 0.05). There were no significant associations between bile acids and CRP.
Diets with comparable macronutrient and energy composition, but differing in carbohydrate source, affected fasting plasma bile acids differently. Specifically, a diet characterized by whole grains, legumes, and fruits and vegetables compared to a diet high in refined grains and added sugars led to modest increases in concentrations of TLCA, TCA and GCA, ligands for FXR and TGR5, which may have beneficial effects on glucose homeostasis.
•Three plasma bile acids increased after a whole versus refined grain diet pattern.•There were significant positive associations between bile acids and HOMA-IR.•Diet patterns varying in carbohydrate type affect plasma bile acids differently.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Bile acid</subject><subject>Bile Acids and Salts - blood</subject><subject>Cross-Over Studies</subject><subject>Diet</subject><subject>Dietary Carbohydrates - pharmacology</subject><subject>Dietary patterns</subject><subject>Edible Grain - physiology</subject><subject>Fabaceae - physiology</subject><subject>Feeding Behavior - physiology</subject><subject>Feeding study</subject><subject>Female</subject><subject>Fruit - physiology</subject><subject>FXR</subject><subject>Healthy Volunteers</subject><subject>Humans</subject><subject>Insulin resistance</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Sugars</subject><subject>Vegetables - physiology</subject><subject>Whole grains</subject><subject>Whole Grains - physiology</subject><subject>Young Adult</subject><issn>0026-0495</issn><issn>1532-8600</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUk2P0zAQDQjEloWfAPKRw7bYbuykHBatKr6klbjA2ZrYk8SVExfbKSq_HqctKzhx8mjmzZuZ51cUrxhdMcrk291qwASNdytOWb2ifEWpfFwsmFjzZS0pfVIsKOVyScuNuCqex7ijlFZVLZ8VV3xTipqK9eJRsbVBTw6SHTvSWIcEtDWR2JH0CC71RwJmcimSgHHvR0OMbVsMOCZ3JMkTyIm8SDiSPaSEYSS6hwA6h_YXGtIcyc_eZ94ugB3jDXHYTQNGApmrDZNN5_CA3XyPyxXthz2E3PtAT3rb9fNOAVs75sqZ7NQIxuREnDoI8R25IyEn_TDPvslMYwreuVMcfIz-gIG0iGY-N6bJHF8UT1twEV9e3uvi-8cP37afl_dfP33Z3t0vdSmrtARRAWsqbGUDbck4y6q3CMiw4hpACiMoZ6IppQGsSiihqrFag-A1N2It1tfF7Zl3PzUDGp0FDODUPtghi6c8WPVvZbS96vxBiY2kks0Eby4Ewf-YMCY12KjRORjRT1Hx_LuM8Y2oMlScoaebs2YPYxhVs3vUTl3co2b3KMpVdk_ue_33jg9df-ySAe_PAMxKHSwGFbXFUWc9A-qkjLf_GfEbYlLghQ</recordid><startdate>20180601</startdate><enddate>20180601</enddate><creator>Ginos, Bigina N.R.</creator><creator>Navarro, Sandi L.</creator><creator>Schwarz, Yvonne</creator><creator>Gu, Haiwei</creator><creator>Wang, Dongfang</creator><creator>Randolph, Timothy W.</creator><creator>Shojaie, Ali</creator><creator>Hullar, Meredith A.J.</creator><creator>Lampe, Paul D.</creator><creator>Kratz, Mario</creator><creator>Neuhouser, Marian L.</creator><creator>Raftery, Daniel</creator><creator>Lampe, Johanna W.</creator><general>Elsevier Inc</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></search><sort><creationdate>20180601</creationdate><title>Circulating bile acids in healthy adults respond differently to a dietary pattern characterized by whole grains, legumes and fruits and vegetables compared to a diet high in refined grains and added sugars: A randomized, controlled, crossover feeding study</title><author>Ginos, Bigina N.R. ; Navarro, Sandi L. ; Schwarz, Yvonne ; Gu, Haiwei ; Wang, Dongfang ; Randolph, Timothy W. ; Shojaie, Ali ; Hullar, Meredith A.J. ; Lampe, Paul D. ; Kratz, Mario ; Neuhouser, Marian L. ; Raftery, Daniel ; Lampe, Johanna W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c467t-a57a1b7ef6baf4121201feae1e72caa65d50215b46dae74a4a78e73a5282d5353</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Bile acid</topic><topic>Bile Acids and Salts - blood</topic><topic>Cross-Over Studies</topic><topic>Diet</topic><topic>Dietary Carbohydrates - pharmacology</topic><topic>Dietary patterns</topic><topic>Edible Grain - physiology</topic><topic>Fabaceae - physiology</topic><topic>Feeding Behavior - physiology</topic><topic>Feeding study</topic><topic>Female</topic><topic>Fruit - physiology</topic><topic>FXR</topic><topic>Healthy Volunteers</topic><topic>Humans</topic><topic>Insulin resistance</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Sugars</topic><topic>Vegetables - physiology</topic><topic>Whole grains</topic><topic>Whole Grains - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ginos, Bigina N.R.</creatorcontrib><creatorcontrib>Navarro, Sandi L.</creatorcontrib><creatorcontrib>Schwarz, Yvonne</creatorcontrib><creatorcontrib>Gu, Haiwei</creatorcontrib><creatorcontrib>Wang, Dongfang</creatorcontrib><creatorcontrib>Randolph, Timothy W.</creatorcontrib><creatorcontrib>Shojaie, Ali</creatorcontrib><creatorcontrib>Hullar, Meredith A.J.</creatorcontrib><creatorcontrib>Lampe, Paul D.</creatorcontrib><creatorcontrib>Kratz, Mario</creatorcontrib><creatorcontrib>Neuhouser, Marian L.</creatorcontrib><creatorcontrib>Raftery, Daniel</creatorcontrib><creatorcontrib>Lampe, Johanna W.</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>Metabolism, clinical and experimental</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ginos, Bigina N.R.</au><au>Navarro, Sandi L.</au><au>Schwarz, Yvonne</au><au>Gu, Haiwei</au><au>Wang, Dongfang</au><au>Randolph, Timothy W.</au><au>Shojaie, Ali</au><au>Hullar, Meredith A.J.</au><au>Lampe, Paul D.</au><au>Kratz, Mario</au><au>Neuhouser, Marian L.</au><au>Raftery, Daniel</au><au>Lampe, Johanna W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Circulating bile acids in healthy adults respond differently to a dietary pattern characterized by whole grains, legumes and fruits and vegetables compared to a diet high in refined grains and added sugars: A randomized, controlled, crossover feeding study</atitle><jtitle>Metabolism, clinical and experimental</jtitle><addtitle>Metabolism</addtitle><date>2018-06-01</date><risdate>2018</risdate><volume>83</volume><spage>197</spage><epage>204</epage><pages>197-204</pages><issn>0026-0495</issn><eissn>1532-8600</eissn><abstract>The effects of diets high in refined grains on biliary and colonic bile acids have been investigated extensively. However, the effects of diets high in whole versus refined grains on circulating bile acids, which can influence glucose homeostasis and inflammation through activation of farnesoid X receptor (FXR) and G protein-coupled bile acid receptor 1 (TGR5), have not been studied.
We conducted a secondary analysis from a randomized controlled crossover feeding trial (NCT00622661) in 80 healthy adults (40 women/40 men, age 18–45 years) from the greater Seattle Area, half of which were normal weight (BMI 18.5–25.0 kg/m2) and half overweight to obese (BMI 28.0–39.9 kg/m2). Participants consumed two four-week controlled diets in randomized order: 1) a whole grain diet (WG diet), designed to be low in glycemic load (GL), high in whole grains, legumes, and fruits and vegetables, and 2) a refined grain diet (RG diet), designed to be high GL, high in refined grains and added sugars, separated by a four-week washout period. Quantitative targeted analysis of 55 bile acid species in fasting plasma was performed using liquid chromatography tandem mass spectrometry. Concentrations of glucose, insulin, and CRP were measured in fasting serum. Linear mixed models were used to test the effects of diet on bile acid concentrations, and determine the association between plasma bile acid concentrations and HOMA-IR and CRP. Benjamini-Hochberg false discovery rate (FDR) < 0.05 was used to control for multiple testing.
A total of 29 plasma bile acids were reliably detected and retained for analysis. Taurolithocholic acid (TLCA), taurocholic acid (TCA) and glycocholic acid (GCA) were statistically significantly higher after the WG compared to the RG diet (FDR < 0.05). There were no significant differences by BMI or sex. When evaluating the association of bile acids and HOMA-IR, GCA, taurochenodeoxycholic acid, ursodeoxycholic acid (UDCA), 5β‑cholanic acid‑3β,12α‑diol, 5‑cholanic acid‑3β‑ol, and glycodeoxycholic acid (GDCA) were statistically significantly positively associated with HOMA-IR individually, and as a group, total, 12α‑hydroxylated, primary and secondary bile acids were also significant (FDR < 0.05). When stratifying by BMI, chenodeoxycholic acid (CDCA), cholic acid (CA), UDCA, 5β-cholanic acid-3β, deoxycholic acid, and total, 12α-hydroxylated, primary and secondary bile acid groups were significantly positively associated with HOMA-IR among overweight to obese individuals (FDR < 0.05). When stratifying by sex, GCA, CDCA, TCA, CA, UDCA, GDCA, glycolithocholic acid (GLCA), total, primary, 12α‑hydroxylated, and glycine-conjugated bile acids were significantly associated with HOMA-IR among women, and CDCA, GDCA, and GLCA were significantly associated among men (FDR < 0.05). There were no significant associations between bile acids and CRP.
Diets with comparable macronutrient and energy composition, but differing in carbohydrate source, affected fasting plasma bile acids differently. Specifically, a diet characterized by whole grains, legumes, and fruits and vegetables compared to a diet high in refined grains and added sugars led to modest increases in concentrations of TLCA, TCA and GCA, ligands for FXR and TGR5, which may have beneficial effects on glucose homeostasis.
•Three plasma bile acids increased after a whole versus refined grain diet pattern.•There were significant positive associations between bile acids and HOMA-IR.•Diet patterns varying in carbohydrate type affect plasma bile acids differently.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>29458053</pmid><doi>10.1016/j.metabol.2018.02.006</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Metabolism, clinical and experimental, 2018-06, Vol.83, p.197-204 |
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| subjects | Adolescent Adult Bile acid Bile Acids and Salts - blood Cross-Over Studies Diet Dietary Carbohydrates - pharmacology Dietary patterns Edible Grain - physiology Fabaceae - physiology Feeding Behavior - physiology Feeding study Female Fruit - physiology FXR Healthy Volunteers Humans Insulin resistance Male Middle Aged Sugars Vegetables - physiology Whole grains Whole Grains - physiology Young Adult |
| title | Circulating bile acids in healthy adults respond differently to a dietary pattern characterized by whole grains, legumes and fruits and vegetables compared to a diet high in refined grains and added sugars: A randomized, controlled, crossover feeding study |
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