Differential Effects of Oral and Intravenous Lipid Administration on Key Molecules Related to Energy Homeostasis

J Clin Endocrinol Metab. 2016 May;101(5):1989-97. doi: 10.1210/jc.2015-4141. Epub 2016 Mar 10.

Abstract

Context: The spectrum of lipid-induced changes in the secretion of hormones important in energy homeostasis has not yet been fully elucidated.

Objective: To identify potential incretin-like effects in response to lipid administration, we examined the short-term effect of iv vs oral lipids on key molecules regulating energy homeostasis. Design, Intervention, and Participants: After a 10-hour overnight fast, 26 subjects were randomized to receive an oral lipid load, a 10% iv lipid emulsion, a 20% iv lipid emulsion, or an iv saline infusion. We obtained blood samples at 30-minute intervals for the first 2 hours and hourly thereafter for a total of 6 hours.

Main outcome measures: Circulating levels of insulin, glucose, c-peptide, free fatty acids, incretins (glucagon-like peptide-1, gastric inhibitory polypeptide), glucagon, peptide YY, ghrelin, fibroblast growth factor 21, fetuin A, irisin, omentin, and adiponectin were measured.

Results: Oral lipid ingestion resulted in higher glucagon-like peptide-1, gastric inhibitory polypeptide, glucagon, and peptide YY levels, compared with the other three groups (incremental area under the curve P = .003, P < .001, P < .001, P < .001, respectively). The 20% lipid emulsion, leading to higher free fatty acid levels, resulted in greater insulin, c-peptide, and fibroblast growth factor 21 responses compared with placebo and the other two groups (incremental area under the curve P = .002, P = .005, P < .001, P < .001, respectively). Omentin, adiponectin, fetuin A, and irisin levels were not affected by either mode of lipid administration.

Conclusions: Metabolic responses to lipids depend on the route of administration. Only iv lipids trigger a dose-dependent fibroblast growth factor 21 secretion, which is nonglucagon mediated. Intravenous lipids also induce hyperinsulinemia without concurrent decreases in glucose, a phenomenon observed in insulin-resistant states. Orally administered lipids mostly affect gastrointestinal tract-secreted molecules important in glucose and energy homeostasis such as glucagon, incretins, and peptide YY.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adiponectin / blood
  • Administration, Oral
  • Adult
  • Blood Glucose
  • C-Peptide / blood
  • Cytokines / blood
  • Energy Metabolism / drug effects*
  • Fatty Acids, Nonesterified / blood
  • Female
  • Fibroblast Growth Factors / blood
  • Fibronectins / blood
  • GPI-Linked Proteins / blood
  • Ghrelin / blood
  • Glucagon / blood
  • Homeostasis / drug effects*
  • Humans
  • Incretins / blood
  • Infusions, Intravenous
  • Insulin / blood
  • Lectins / blood
  • Lipids / administration & dosage*
  • Male
  • Middle Aged
  • Peptide YY / blood
  • Young Adult
  • alpha-2-HS-Glycoprotein / metabolism

Substances

  • Adiponectin
  • Blood Glucose
  • C-Peptide
  • Cytokines
  • FNDC5 protein, human
  • Fatty Acids, Nonesterified
  • Fibronectins
  • GPI-Linked Proteins
  • Ghrelin
  • ITLN1 protein, human
  • Incretins
  • Insulin
  • Lectins
  • Lipids
  • alpha-2-HS-Glycoprotein
  • fibroblast growth factor 21
  • Peptide YY
  • Fibroblast Growth Factors
  • Glucagon