Carbohydrate-rich breakfast attenuates glycaemic, insulinaemic and ghrelin response to ad libitum lunch relative to morning fasting in lean adults

Enhad A Chowdhury, Judith D Richardson, Kostas Tsintzas, Dylan Thompson, James A Betts, Enhad A Chowdhury, Judith D Richardson, Kostas Tsintzas, Dylan Thompson, James A Betts

Abstract

Breakfast omission is associated with obesity and CVD/diabetes, but the acute effects of extended morning fasting upon subsequent energy intake and metabolic/hormonal responses have received less attention. In a randomised cross-over design, thirty-five lean men (n 14) and women (n 21) extended their overnight fast or ingested a typical carbohydrate-rich breakfast in quantities relative to RMR (i.e. 1963 (sd 238) kJ), before an ad libitum lunch 3 h later. Blood samples were obtained hourly throughout the day until 3 h post-lunch, with subjective appetite measures assessed. Lunch intake was greater following extended fasting (640 (sd 1042) kJ, P< 0.01) but incompletely compensated for the omitted breakfast, with total intake lower than the breakfast trial (3887 (sd 1326) v. 5213 (sd 1590) kJ, P< 0.001). Systemic concentrations of peptide tyrosine-tyrosine and leptin were greater during the afternoon following breakfast (both P< 0.05) but neither acylated/total ghrelin concentrations were suppressed by the ad libitum lunch in the breakfast trial, remaining greater than the morning fasting trial throughout the afternoon (all P< 0.05). Insulin concentrations were greater during the afternoon in the morning fasting trial (all P< 0.01). There were no differences between trials in subjective appetite during the afternoon. In conclusion, morning fasting caused incomplete energy compensation at an ad libitum lunch. Breakfast increased some anorectic hormones during the afternoon but paradoxically abolished ghrelin suppression by the second meal. Extending morning fasting until lunch altered subsequent metabolic and hormonal responses but without greater appetite during the afternoon. The present study clarifies the impact of acute breakfast omission and adds novel insights into second-meal metabolism.

Keywords: Appetite hormones; Breakfast skipping; Energy intake; Insulin sensitivity; Second-meal effect.

Figures

Fig. 1
Fig. 1
Energy intake during trials. In the morning fasting trial, an asymmetric normalised CI is plotted, the negative portion of which reflects the comparison between lunches and the positive portion reflects the comparison against total intake (i.e. lunch plus breakfast). An asterisk above a bar represents the comparison between the sum of the components of the bar, an asterisk between the bars represents the comparison between the specific component (P< 0·01). n 34, as one individual felt nauseous prior to lunch provision on one visit.
Fig. 2
Fig. 2
Metabolic responses during trials. (a) Plasma glucose (n 32), (b) serum insulin (n 32), (c) plasma NEFA (n 31), where missing data are due to insufficient blood for analysis. Values are means with their normalised CI represented by vertical bars. * Mean value was significantly different from the corresponding time point in other trial (P< 0·03). B, breakfast period, in which participants ate a prescribed breakfast during the breakfast trial and rested during the morning fasting trial. L, ad libitum pasta lunch. –▲–, Breakfast; –○–, fasting.
Fig. 3
Fig. 3
Hormonal responses during trials. (a) Plasma acylated and total ghrelin (n 32), (b) plasma peptide tyrosine–tyrosine (PYY, n 32), (c) plasma glucagon-like peptide-1 (GLP-1, n 32), (d) serum leptin (n 32), where missing data are due to insufficient blood for analysis. Values are means with their normalised CI represented by vertical bars. * Mean value was significantly different from the corresponding time point in other trial (P< 0·05). B, breakfast period, in which participants ate a prescribed breakfast during the breakfast trial and rested during the morning fasting trial. L, ad libitum pasta lunch. –▲–, Breakfast; –○–, fasting.
Fig. 4
Fig. 4
Appetite score during trials. B, breakfast period, in which participants ate a prescribed breakfast during the breakfast trial and rested during the morning fasting trial. L, ad libitum pasta lunch. n 34, as one individual was not provided with hedonic scales on one of their trials. Values are means with their normalised CI represented by vertical bars. * Mean value was significantly different from the corresponding time point in other trial (P< 0·01). –▲–, Breakfast; –○–, fasting.

References

    1. Ma Y, Bertone ER, Stanek EJ, et al. (2003) Association between eating patterns and obesity in a free-living US adult population. Am J Epidemiol 158, 85–92.
    1. Horikawa C, Kodama S, Yachi Y, et al. (2011) Skipping breakfast and prevalence of overweight and obesity in Asian and Pacific regions: a meta-analysis. Prev Med 53, 260–267.
    1. Purslow LR, Sandhu MS, Forouhi N, et al. (2008) Energy intake at breakfast and weight change: prospective study of 6,764 middle-aged men and women. Am J Epidemiol 167, 188–192.
    1. Mekary RA, Giovannucci E, Cahill L, et al. (2013) Eating patterns and type 2 diabetes risk in older women: breakfast consumption and eating frequency. Am J Clin Nutr 98, 436–443.
    1. Mekary RA, Giovannucci E, Willett WC, et al. (2012) Eating patterns and type 2 diabetes risk in men: breakfast omission, eating frequency, and snacking. Am J Clin Nutr 95, 1182–1189.
    1. Cahill LE, Chiuve SE, Mekary RA, et al. (2013) Prospective study of breakfast eating and incident coronary heart disease in a cohort of male US health professionals. Circulation 128, 337–343.
    1. Clegg M & Shafat A (2010) Energy and macronutrient composition of breakfast affect gastric emptying of lunch and subsequent food intake, satiety and satiation. Appetite 54, 517–523.
    1. Hamedani A, Akhavan T, Samra RA, et al. (2009) Reduced energy intake at breakfast is not compensated for at lunch if a high-insoluble-fiber cereal replaces a low-fiber cereal. Am J Clin Nutr 89, 1343–1349.
    1. Kim H, Stote KS, Behall KM, et al. (2009) Glucose and insulin responses to whole grain breakfasts varying in soluble fiber, β-glucan: a dose response study in obese women with increased risk for insulin resistance. Eur J Nutr 48, 170–175.
    1. Levine AS, Tallman JR, Grace MK, et al. (1989) Effect of breakfast cereals on short-term food intake. Am J Clin Nutr 50, 1303–1307.
    1. Liljeberg HG, Akerberg AK & Bjorck IM (1999) Effect of the glycemic index and content of indigestible carbohydrates of cereal-based breakfast meals on glucose tolerance at lunch in healthy subjects. Am J Clin Nutr 69, 647–655.
    1. Martin A, Normand S, Sothier M, et al. (2000) Is advice for breakfast consumption justified? Results from a short-term dietary and metabolic experiment in young healthy men. Br J Nutr 84, 337–344.
    1. Rosen LA, Ostman EM & Bjorck IM (2011) Effects of cereal breakfasts on postprandial glucose, appetite regulation and voluntary energy intake at a subsequent standardized lunch; focusing on rye products. Nutr J 10, 7.
    1. Nilsson AC, Ostman EM, Granfeldt Y, et al. (2008) Effect of cereal test breakfasts differing in glycemic index and content of indigestible carbohydrates on daylong glucose tolerance in healthy subjects. Am J Clin Nutr 87, 645–654.
    1. Gonzalez JT, Veasey RC, Rumbold PL, et al. (2013) Breakfast and exercise contingently affect postprandial metabolism and energy balance in physically active males. Br J Nutr 110, 721–732.
    1. Levitsky DA & Pacanowski CR (2013) Effect of skipping breakfast on subsequent energy intake. Physiol Behav 119, 9–16.
    1. Astbury NM, Taylor MA & Macdonald IA (2011) Breakfast consumption affects appetite, energy intake, and the metabolic and endocrine responses to foods consumed later in the day in male habitual breakfast eaters. J Nutr 141, 1381–1389.
    1. Cummings DE, Purnell JQ, Frayo RS, et al. (2001) A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50, 1714–1719.
    1. Leidy HJ, Ortinau LC, Douglas SM, et al. (2013) Beneficial effects of a higher-protein breakfast on the appetitive, hormonal, and neural signals controlling energy intake regulation in overweight/obese, “breakfast-skipping,” late-adolescent girls. Am J Clin Nutr 97, 677–688.
    1. Batterham RL, Cowley MA, Small CJ, et al. (2002) Gut hormone PYY(3–36) physiologically inhibits food intake. Nature 418, 650–654.
    1. Leidy HJ & Racki EM (2010) The addition of a protein-rich breakfast and its effects on acute appetite control and food intake in ‘breakfast-skipping’ adolescents. Int J Obes (Lond) 34, 1125–1133.
    1. Holst JJ (2013) Incretin hormones and the satiation signal. Int J Obes (Lond) 37, 1161–1168.
    1. Kant AK & Graubard BI (2014) 40-Year trends in meal and snack eating behaviors of American adults. J Acad Nutr Diet 115, 50–63.
    1. Reeves S, Halsey LG, McMeel Y, et al. (2013) Breakfast habits, beliefs and measures of health and wellbeing in a nationally representative UK sample. Appetite 60, 51–57.
    1. Betts JA, Richardson JD, Chowdhury EA, et al. (2014) The causal role of breakfast in energy balance and health: a randomized controlled trial in lean adults. Am J Clin Nutr 100, 539–547.
    1. Betts JA, Thompson D, Richardson JD, et al. (2011) Bath Breakfast Project (BBP) – examining the role of extended daily fasting in human energy balance and associated health outcomes: study protocol for a randomised controlled trial [ISRCTN31521726]. Trials 12, 172.
    1. Kelly TL, Wilson KE & Heymsfield SB (2009) Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS ONE 4, e7038.
    1. Buffenstein R, Poppitt SD, McDevitt RM, et al. (1995) Food intake and the menstrual cycle: a retrospective analysis, with implications for appetite research. Physiol Behav 58, 1067–1077.
    1. Lissner L, Stevens J, Levitsky DA, et al. (1988) Variation in energy intake during the menstrual cycle: implications for food-intake research. Am J Clin Nutr 48, 956–962.
    1. Chryssanthopoulos C, Williams C, Nowitz A, et al. (2004) Skeletal muscle glycogen concentration and metabolic responses following a high glycaemic carbohydrate breakfast. J Sports Sci 22, 1065–1071.
    1. Timlin MT & Pereira MA (2007) Breakfast frequency and quality in the etiology of adult obesity and chronic diseases. Nutr Rev 65, 268–281.
    1. Blundell JE, Caudwell P, Gibbons C, et al. (2012) Role of resting metabolic rate and energy expenditure in hunger and appetite control: a new formulation. Dis Model Mech 5, 608–613.
    1. Kokkinos A, le Roux CW, Alexiadou K, et al. (2010) Eating slowly increases the postprandial response of the anorexigenic gut hormones, peptide YY and glucagon-like peptide-1. J Clin Endocrinol Metab 95, 333–337.
    1. Betts JA & Thompson D (2012) Thinking outside the bag (not necessarily outside the lab). Med Sci Sports Exerc 44, 2040; author reply 2041.
    1. Compher C, Frankenfield D, Keim N, et al. (2006) Best practice methods to apply to measurement of resting metabolic rate in adults: a systematic review. J Am Diet Assoc 106, 881–903.
    1. Weir JB (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109, 1–9.
    1. Jequier E, Acheson K & Schutz Y (1987) Assessment of energy expenditure and fuel utilization in man. Ann Rev Nutr 7, 187–208.
    1. Chandarana K, Drew ME, Emmanuel J, et al. (2009) Subject standardization, acclimatization, and sample processing affect gut hormone levels and appetite in humans. Gastroenterology 136, 2115–2126.
    1. Anderson GH, Catherine NL, Woodend DM, et al. (2002) Inverse association between the effect of carbohydrates on blood glucose and subsequent short-term food intake in young men. Am J Clin Nutr 76, 1023–1030.
    1. Atkinson G (2002) Analysis of repeated measurements in physical therapy research: multiple comparisons amongst level means and multi-factorial designs. Phys Ther Sport 3, 191–203.
    1. Ludbrook J (1998) Multiple comparison procedures updated. Clin Exp Pharmacol Physiol 25, 1032–1037.
    1. Loftus GR & Masson ME (1994) Using confidence intervals in within-subject designs. Psychon Bull Rev 1, 476–490.
    1. Adrian TE, Ferri GL, Bacarese-Hamilton AJ, et al. (1985) Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 89, 1070–1077.
    1. Saad MF, Riad-Gabriel MG, Khan A, et al. (1998) Diurnal and ultradian rhythmicity of plasma leptin: effects of gender and adiposity. J Clin Endocrinol Metab 83, 453–459.
    1. Schoeller DA, Cella LK, Sinha MK, et al. (1997) Entrainment of the diurnal rhythm of plasma leptin to meal timing. J Clin Invest 100, 1882–1887.
    1. Blom WA, Stafleu A, de Graaf C, et al. (2005) Ghrelin response to carbohydrate-enriched breakfast is related to insulin. Am J Clin Nutr 81, 367–375.
    1. Foster-Schubert KE, Overduin J, Prudom CE, et al. (2008) Acyl and total ghrelin are suppressed strongly by ingested proteins, weakly by lipids, and biphasically by carbohydrates. J Clin Endocrinol Metab 93, 1971–1979.
    1. Flanagan DE, Evans ML, Monsod TP, et al. (2003) The influence of insulin on circulating ghrelin. Am J Physiol Endocrinol Metab 284, E313–E316.
    1. Murdolo G, Lucidi P, et al. (2003) Di Loreto C. Insulin is required for prandial ghrelin suppression in humans. Diabetes 52, 2923–2927.
    1. Saad MF, Bernaba B, Hwu CM, et al. (2002) Insulin regulates plasma ghrelin concentration. J Clin Endocrinol Metab 87, 3997–4000.
    1. Caixas A, Bashore C, Nash W, et al. (2002) Insulin, unlike food intake, does not suppress ghrelin in human subjects. J Clin Endocrinol Metab 87, 1902.
    1. Schaller G, Schmidt A, Pleiner J, et al. (2003) Plasma ghrelin concentrations are not regulated by glucose or insulin: a double-blind, placebo-controlled crossover clamp study. Diabetes 52, 16–20.
    1. Blom WA, de Graaf C, Lluch A, et al. (2009) Postprandial ghrelin responses are associated with the intermeal interval in time-blinded normal weight men, but not in obese men. Physiol Behav 96, 742–748.
    1. Hamman L & Hirschmann I (1919) Studies on blood sugar. IV. Effects upon the blood sugar of the repeated ingestion of glucose. Johns Hopkins Hosp Bull 30, 306–307.
    1. Bonuccelli S, Muscelli E, Gastaldelli A, et al. (2009) Improved tolerance to sequential glucose loading (Staub-Traugott effect): size and mechanisms. Am J Physiol Endocrinol Metab 297, E532–E537.
    1. Reeves S, Huber JW, Halsey LG, et al. (2014) Experimental manipulation of breakfast in normal and overweight/obese participants is associated with changes to nutrient and energy intake consumption patterns. Physiol Behav 133C 130–135.
    1. Robertson MD, Henderson RA, Vist GE, et al. (2002) Extended effects of evening meal carbohydrate-to-fat ratio on fasting and postprandial substrate metabolism. Am J Clin Nutr 75, 505–510.
    1. Hochstenbach-Waelen A, Veldhorst MA, Nieuwenhuizen AG, et al. (2009) Comparison of 2 diets with either 25 % or 10 % of energy as casein on energy expenditure, substrate balance, and appetite profile. Am J Clin Nutr 89, 831–838.

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