Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism

Abstract Background We sought to characterize the effects of dietary macronutrient composition on various hormones implicated in the regulation of insulin sensitivity (IS) and energy expenditure (EE). Methods Following 10–15% weight loss, 21 overweight subjects consumed 3 weight-loss maintenance die...

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Main Authors: Bridget M. Hron, Cara B. Ebbeling, Henry A. Feldman, David S. Ludwig
Format: Article
Language:English
Published: BMC 2017-07-01
Series:Nutrition & Metabolism
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12986-017-0198-y
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author Bridget M. Hron
Cara B. Ebbeling
Henry A. Feldman
David S. Ludwig
author_facet Bridget M. Hron
Cara B. Ebbeling
Henry A. Feldman
David S. Ludwig
author_sort Bridget M. Hron
collection DOAJ
description Abstract Background We sought to characterize the effects of dietary macronutrient composition on various hormones implicated in the regulation of insulin sensitivity (IS) and energy expenditure (EE). Methods Following 10–15% weight loss, 21 overweight subjects consumed 3 weight-loss maintenance diets [low fat (LF), low glycemic index (LGI) and very low carbohydrate (VLC)] in random order, each for 4 weeks. At baseline and at the end of each treatment period, fasting samples for fibroblast growth factor (FGF)-21, heme-oxygenase-1 (HO-1), chemerin, irisin, secreted frizzle-related protein (SFRP-4), total bile acids, ghrelin, gastrin inhibitory peptide (GIP), peptide-Y, and amylin; hepatic and peripheral IS; and EE were obtained. Analyses were controlled for age, gender, baseline body mass index, and diet sequence. Results FGF-21 decreased (P < 0.0001), with differential effect by macronutrient composition (mean change from baseline ± SEM: LF −49.4 ± 16.6, LGI -58.6 ± 16.3, VLC -76.7 ± 18.2 pg/mL, P = 0.0002). Change in FGF-21 was inversely associated with change in hepatic IS [Beta = −0.565 units/log(ng/mL), P = 0.02], but not with peripheral IS or EE. Heme-oxygenase-1 (HO-1) increased (P = 0.003), without differential effect by macronutrient composition (LF 0.40 ± 0.26, LGI 0.98 ± 0.63, VLC 0.49 ± 0.29 ng/mL, P = 0.07). Ghrelin increased (P = 0.0003), while chemerin decreased (P = 0.001) without macronutrient effect. Total bile acid, irisin, SFRP-4, GIP, peptide-Y and amylin levels did not change. Conclusions FGF-21 levels decreased with dietary intervention in proportion to carbohydrate content, and correlated with hepatic insulin sensitivity, suggesting a pattern of improving FGF-21 resistance. HO-1 increased in response to dietary intervention, a tendency to greater increase in response to the LGI diet. Dietary intervention affected ghrelin and chemerin, independent of macronutrient composition. These findings may elucidate relationships between dietary composition, insulin sensitivity and metabolism. Trial registration NCT00315354 .
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spelling doaj.art-5cb7183794cc43af9d98039e2cc751872022-12-21T20:03:03ZengBMCNutrition & Metabolism1743-70752017-07-011411710.1186/s12986-017-0198-yHepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolismBridget M. Hron0Cara B. Ebbeling1Henry A. Feldman2David S. Ludwig3Division of Gastroenterology, Hepatology and Nutrition, Boston Children’s HospitalNew Balance Foundation Obesity Prevention Center and Division of Endocrinology, Boston Children’s HospitalClinical Research Center, Boston Children’s HospitalNew Balance Foundation Obesity Prevention Center and Division of Endocrinology, Boston Children’s HospitalAbstract Background We sought to characterize the effects of dietary macronutrient composition on various hormones implicated in the regulation of insulin sensitivity (IS) and energy expenditure (EE). Methods Following 10–15% weight loss, 21 overweight subjects consumed 3 weight-loss maintenance diets [low fat (LF), low glycemic index (LGI) and very low carbohydrate (VLC)] in random order, each for 4 weeks. At baseline and at the end of each treatment period, fasting samples for fibroblast growth factor (FGF)-21, heme-oxygenase-1 (HO-1), chemerin, irisin, secreted frizzle-related protein (SFRP-4), total bile acids, ghrelin, gastrin inhibitory peptide (GIP), peptide-Y, and amylin; hepatic and peripheral IS; and EE were obtained. Analyses were controlled for age, gender, baseline body mass index, and diet sequence. Results FGF-21 decreased (P < 0.0001), with differential effect by macronutrient composition (mean change from baseline ± SEM: LF −49.4 ± 16.6, LGI -58.6 ± 16.3, VLC -76.7 ± 18.2 pg/mL, P = 0.0002). Change in FGF-21 was inversely associated with change in hepatic IS [Beta = −0.565 units/log(ng/mL), P = 0.02], but not with peripheral IS or EE. Heme-oxygenase-1 (HO-1) increased (P = 0.003), without differential effect by macronutrient composition (LF 0.40 ± 0.26, LGI 0.98 ± 0.63, VLC 0.49 ± 0.29 ng/mL, P = 0.07). Ghrelin increased (P = 0.0003), while chemerin decreased (P = 0.001) without macronutrient effect. Total bile acid, irisin, SFRP-4, GIP, peptide-Y and amylin levels did not change. Conclusions FGF-21 levels decreased with dietary intervention in proportion to carbohydrate content, and correlated with hepatic insulin sensitivity, suggesting a pattern of improving FGF-21 resistance. HO-1 increased in response to dietary intervention, a tendency to greater increase in response to the LGI diet. Dietary intervention affected ghrelin and chemerin, independent of macronutrient composition. These findings may elucidate relationships between dietary composition, insulin sensitivity and metabolism. Trial registration NCT00315354 .http://link.springer.com/article/10.1186/s12986-017-0198-yInsulin sensitivityEnergy expenditureFGF-21Metabolic hormonesDietary composition
spellingShingle Bridget M. Hron
Cara B. Ebbeling
Henry A. Feldman
David S. Ludwig
Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
Nutrition & Metabolism
Insulin sensitivity
Energy expenditure
FGF-21
Metabolic hormones
Dietary composition
title Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
title_full Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
title_fullStr Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
title_full_unstemmed Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
title_short Hepatic, adipocyte, enteric and pancreatic hormones: response to dietary macronutrient composition and relationship with metabolism
title_sort hepatic adipocyte enteric and pancreatic hormones response to dietary macronutrient composition and relationship with metabolism
topic Insulin sensitivity
Energy expenditure
FGF-21
Metabolic hormones
Dietary composition
url http://link.springer.com/article/10.1186/s12986-017-0198-y
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AT henryafeldman hepaticadipocyteentericandpancreatichormonesresponsetodietarymacronutrientcompositionandrelationshipwithmetabolism
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