Abstract
Background:
Previous patterns of energy intake influence gastrointestinal function and appetite, probably reflecting changes in small-intestinal nutrient-mediated feedback. Obese individuals consume more fat and may be less sensitive to its gastrointestinal and appetite-suppressant effects than lean individuals.
Objective:
To evaluate the hypothesis that, in obese individuals, the effects of duodenal fat on gastrointestinal motor and hormone function, and appetite would be enhanced by a short period on a very-low-calorie diet (VLCD).
Methods:
Eight obese men (body mass index 34±0.6 kg m−2) were studied on two occasions, before (V1), and immediately after (V2), a 4-day VLCD. On both occasions, antropyloroduodenal motility, plasma cholecystokinin (CCK), peptide-YY (PYY) and ghrelin concentrations, and appetite perceptions were measured during a 120-min intraduodenal fat infusion (2.86 kcal min−1). Immediately afterwards, energy intake was quantified.
Results:
During V2, basal pyloric pressure and the number and amplitude of isolated pyloric pressure waves (PWs) were greater, whereas the number of antral and duodenal PWs was less, compared with V1 (all P<0.05). Moreover, during V2, baseline ghrelin concentration was higher; the stimulation of PYY and suppression of ghrelin by lipid were greater, with no difference in CCK concentration; and hunger and energy intake (kJ; V1: 4378±691, V2: 3634±700) were less (all P<0.05), compared with V1.
Conclusions:
In obese males, the effects of small-intestinal lipid on gastrointestinal motility and some hormone responses and appetite are enhanced after a 4-day VLCD.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
WHO. WHO Fact Sheet No. 311: Obesity and overweight 2006, http://www.who.int/mediacentre/factsheets/fs311/en/print.html. (accessed in May 2010).
Kaplan LM . Pharmacological therapies for obesity. Gastroenterol Clin North Am 2005; 34: 91–104.
Brennan IM, Feltrin KL, Horowitz M, Smout AJ, Meyer JH, Wishart J et al. Evaluation of interactions between CCK and GLP-1 in their effects on appetite, energy intake, and antropyloroduodenal motility in healthy men. Am J Physiol Regul Integr Comp Physiol 2005; 288: R1477–R1485.
Sturm K, Parker B, Wishart J, Feinle-Bisset C, Jones KL, Chapman I et al. Energy intake and appetite are related to antral area in healthy young and older subjects. Am J Clin Nutr 2004; 80: 656–667.
Cunningham KM, Daly J, Horowitz M, Read NW . Gastrointestinal adaptation to diets of differing fat composition in human volunteers. Gut 1991; 32: 483–486.
Little TJ, Russo A, Meyer JH, Horowitz M, Smyth DR, Bellon M et al. Free fatty acids have more potent effects on gastric emptying, gut hormones, and appetite than triacylglycerides. Gastroenterology 2007; 133: 1124–1131.
Pilichiewicz AN, Papadopoulos P, Brennan IM, Little TJ, Meyer JH, Wishart JM et al. Load-dependent effects of duodenal lipid on antropyloroduodenal motility, plasma CCK and PYY, and energy intake in healthy men. Am J Physiol Regul Integr Comp Physiol 2007; 293: R2170–R2178.
Feinle C, O'Donovan D, Doran S, Andrews JM, Wishart J, Chapman I et al. Effects of fat digestion on appetite, APD motility, and gut hormones in response to duodenal fat infusion in humans. Am J Physiol Gastrointest Liver Physiol 2003; 284: G798–G807.
Feltrin KL, Little TJ, Meyer JH, Horowitz M, Rades T, Wishart J et al. Effects of lauric acid on upper gut motility, plasma cholecystokinin and peptide YY, and energy intake are load, but not concentration, dependent in humans. J Physiol 2007; 581: 767–777.
Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL et al. Gut hormone PYY(3–36) physiologically inhibits food intake. Nature 2002; 418: 650–654.
Beglinger C, Degen L, Matzinger D, D'Amato M, Drewe J . Loxiglumide, a CCK-A receptor antagonist, stimulates calorie intake and hunger feelings in humans. Am J Physiol Regul Integr Comp Physiol 2001; 280: R1149–R1154.
Schirra J, Nicolaus M, Roggel R, Katschinski M, Storr M, Woerle HJ et al. Endogenous glucagon-like peptide-1 controls endocrine pancreatic secretion and antro-pyloro-duodenal motility in humans. Gut 2006; 55: 243–251.
Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG et al. Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 2001; 86: 5992–5996.
Seimon RV, Lange K, Little TJ, Brennan IM, Pilichiewicz AN, Feltrin KL et al. Pooled-data analysis identifies pyloric pressures and plasma CCK concentrations as major determinants of acute energy intake in healthy lean males. Am J Clin Nutr 2010; 92: 61–68.
Vazquez Roque MI, Camilleri M, Stephens DA, Jensen MD, Burton DD, Baxter KL et al. Gastric sensorimotor functions and hormone profile in normal weight, overweight, and obese people. Gastroenterology 2006; 131: 1717–1724.
French SJ, Murray B, Rumsey RD, Sepple CP, Read NW . Preliminary studies on the gastrointestinal responses to fatty meals in obese people. Int J Obes Relat Metab Disord 1993; 17: 295–300.
Maddox A, Horowitz M, Wishart J, Collins P . Gastric and oesophageal emptying in obesity. Scand J Gastroenterol 1989; 24: 593–598.
Baranowska B, Radzikowska M, Wasilewska-Dziubinska E, Roguski K, Borowiec M . Disturbed release of gastrointestinal peptides in anorexia nervosa and in obesity. Diabetes Obes Metab 2000; 2: 99–103.
le Roux CW, Batterham RL, Aylwin SJ, Patterson M, Borg CM, Wynne KJ et al. Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology 2006; 147: 3–8.
Verdich C, Toubro S, Buemann B, Lysgard Madsen J, Juul Holst J, Astrup A . The role of postprandial releases of insulin and incretin hormones in meal-induced satiety—effect of obesity and weight reduction. Int J Obes Relat Metab Disord 2001; 25: 1206–1214.
Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS . A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 2001; 50: 1714–1719.
Corvilain B, Abramowicz M, Fery F, Schoutens A, Verlinden M, Balasse E et al. Effect of short-term starvation on gastric emptying in humans: relationship to oral glucose tolerance. Am J Physiol Gastrointest Liver Physiol 1995; 269: G512–G517.
Nguyen NQ, Fraser RJ, Chapman MJ, Bryant LK, Holloway RH, Vozzo R et al. Feed intolerance in critical illness is associated with increased basal and nutrient-stimulated plasma cholecystokinin concentrations. Crit Care Med 2007; 35: 82–88.
Chapman M, Fraser R, Vozzo R, Bryant L, Tam W, Nguyen N et al. Antro-pyloro-duodenal motor responses to gastric and duodenal nutrient in critically ill patients. Gut 2005; 54: 1384–1390.
Stunkard AJ, Messick S . The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res 1985; 29: 71–83.
Harris JA, Benedict FG . A biometric study of human basal metabolism. Proc Natl Acad Sci USA 1918; 4: 370–373.
Heddle R, Collins PJ, Dent J, Horowitz M, Read NW, Chatterton B et al. Motor mechanisms associated with slowing of the gastric emptying of a solid meal by an intraduodenal lipid infusion. J Gastroenterol Hepatol 1989; 4: 437–447.
Parker BA, Sturm K, MacIntosh CG, Feinle C, Horowitz M, Chapman IM . Relation between food intake and visual analogue scale ratings of appetite and other sensations in healthy older and young subjects. Eur J Clin Nutr 2004; 58: 212–218.
Feltrin KL, Little TJ, Meyer JH, Horowitz M, Smout AJ, Wishart J et al. Effects of intraduodenal fatty acids on appetite, antropyloroduodenal motility, and plasma CCK and GLP-1 in humans vary with their chain length. Am J Physiol Regul Integr Comp Physiol 2004; 287: R524–R533.
Brennan IM, Otto B, Feltrin KL, Meyer JH, Horowitz M, Feinle-Bisset C . Intravenous CCK-8, but not GLP-1, suppresses ghrelin and stimulates PYY release in healthy men. Peptides 2007; 28: 607–611.
Riepl RL, Fiedler F, Ernstberger M, Teufel J, Lehnert P . Effect of intraduodenal taurodeoxycholate and L-phenylalanine on pancreatic secretion and on gastroenteropancreatic peptide release in man. Eur J Med Res 1996; 1: 499–505.
Seimon RV, Wooster T, Otto B, Golding M, Day L, Little TJ et al. The droplet size of intraduodenal fat emulsions influences antropyloroduodenal motility, hormone release, and appetite in healthy males. Am J Clin Nutr 2009; 89: 1729–1736.
English PJ, Ghatei MA, Malik IA, Bloom SR, Wilding JP . Food fails to suppress ghrelin levels in obese humans. J Clin Endocrinol Metab 2002; 87: 2984–2987.
Lin HC, Chey WY, Zhao X . Release of distal gut peptide YY (PYY) by fat in proximal gut depends on CCK. Peptides 2000; 21: 1561–1563.
Aponte GW, Fink AS, Meyer JH, Tatemoto K, Taylor IL . Regional distribution and release of peptide YY with fatty acids of different chain length. Am J Physiol Gastrointest Liver Physiol 1985; 249: G745–G750.
Spiller RC, Trotman IF, Adrian TE, Bloom SR, Misiewicz JJ, Silk DB . Further characterisation of the ‘ileal brake’ reflex in man—effect of ileal infusion of partial digests of fat, protein, and starch on jejunal motility and release of neurotensin, enteroglucagon, and peptide YY. Gut 1988; 29: 1042–1051.
Feinle-Bisset C, Patterson M, Ghatei MA, Bloom SR, Horowitz M . Fat digestion is required for suppression of ghrelin and stimulation of peptide YY and pancreatic polypeptide secretion by intraduodenal lipid. Am J Physiol Endocrinol Metab 2005; 289: E948–E953.
Cummings DE, Weigle DS, Frayo RS, Breen PA, Ma MK, Dellinger EP et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 2002; 346: 1623–1630.
Covasa M, Grahn J, Ritter RC . Reduced hindbrain and enteric neuronal response to intestinal oleate in rats maintained on high-fat diet. Auton Neurosci 2000; 84: 8–18.
Covasa M, Grahn J, Ritter RC . High fat maintenance diet attenuates hindbrain neuronal response to CCK. Regul Pept 2000; 86: 83–88.
Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE, Rood J et al. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 2006; 295: 1539–1548.
Nair NS, Brennan IM, Little TJ, Gentilcore D, Hausken T, Jones KL et al. Reproducibility of energy intake, gastric emptying, blood glucose, plasma insulin and cholecystokinin responses in healthy young males. Br J Nutr 2009; 101: 1094–1102.
Brennan IM, Feltrin KL, Nair NS, Hausken T, Little TJ, Gentilcore D et al. Effects of the phases of the menstrual cycle on gastric emptying, glycemia, plasma GLP-1 and insulin, and energy intake in healthy lean women. Am J Physiol Gastrointest Liver Physiol 2009; 297: G602–G610.
Acknowledgements
IM Brennan and RV Seimon were supported by Dawes Postgraduate Scholarships provided by the Royal Adelaide Hospital and the University of Adelaide, and C Feinle-Bisset by a Clinical Career Development Award (grant 299074, 2004–2009) from the National Health and Medical Research Council of Australia (NHMRC). The research was funded by an NHMRC project grant to C Feinle-Bisset (Grant 565312, 2009–2011).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Author contributions
IM Brennan was involved in study concept and design, data acquisition, data analysis and interpretation, statistical analysis and manuscript writing, RV Seimon in data acquisition and manuscript writing, ND Luscombe-Marsh in study concept and design and manuscript writing, B Otto performed the hormone assays and was involved in data analysis, M Horowitz was involved in study concept and design, data interpretation and manuscript writing, and C Feinle-Bisset was involved in study concept and design, data analysis and interpretation, statistical analysis and manuscript writing, obtained the funding and had overall responsibility for the study.
Rights and permissions
About this article
Cite this article
Brennan, I., Seimon, R., Luscombe-Marsh, N. et al. Effects of acute dietary restriction on gut motor, hormone and energy intake responses to duodenal fat in obese men. Int J Obes 35, 448–456 (2011). https://doi.org/10.1038/ijo.2010.153
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ijo.2010.153
Keywords
This article is cited by
-
Intermittent fasting two days versus one day per week, matched for total energy intake and expenditure, increases weight loss in overweight/obese men and women
Nutrition Journal (2022)
-
Bugs, guts and brains, and the regulation of food intake and body weight
International Journal of Obesity Supplements (2016)
-
Dietary Renaissance in IBS: Has Food Replaced Medications as a Primary Treatment Strategy?
Current Treatment Options in Gastroenterology (2014)
-
Dietary and lifestyle factors in functional dyspepsia
Nature Reviews Gastroenterology & Hepatology (2013)
-
Dietary Lipids and Functional Gastrointestinal Disorders
American Journal of Gastroenterology (2013)