The causal role of breakfast in energy balance and health: a randomized controlled trial in lean adults

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

Abstract

Background: Popular beliefs that breakfast is the most important meal of the day are grounded in cross-sectional observations that link breakfast to health, the causal nature of which remains to be explored under real-life conditions.

Objective: The aim was to conduct a randomized controlled trial examining causal links between breakfast habits and all components of energy balance in free-living humans.

Design: The Bath Breakfast Project is a randomized controlled trial with repeated-measures at baseline and follow-up in a cohort in southwest England aged 21-60 y with dual-energy X-ray absorptiometry-derived fat mass indexes ≤11 kg/m² in women (n = 21) and ≤7.5 kg/m² in men (n = 12). Components of energy balance (resting metabolic rate, physical activity thermogenesis, energy intake) and 24-h glycemic responses were measured under free-living conditions with random allocation to daily breakfast (≥700 kcal before 1100) or extended fasting (0 kcal until 1200) for 6 wk, with baseline and follow-up measures of health markers (eg, hematology/biopsies).

Results: Contrary to popular belief, there was no metabolic adaptation to breakfast (eg, resting metabolic rate stable within 11 kcal/d), with limited subsequent suppression of appetite (energy intake remained 539 kcal/d greater than after fasting; 95% CI: 157, 920 kcal/d). Rather, physical activity thermogenesis was markedly higher with breakfast than with fasting (442 kcal/d; 95% CI: 34, 851 kcal/d). Body mass and adiposity did not differ between treatments at baseline or follow-up and neither did adipose tissue glucose uptake or systemic indexes of cardiovascular health. Continuously measured glycemia was more variable during the afternoon and evening with fasting than with breakfast by the final week of the intervention (CV: 3.9%; 95% CI: 0.1%, 7.8%).

Conclusions: Daily breakfast is causally linked to higher physical activity thermogenesis in lean adults, with greater overall dietary energy intake but no change in resting metabolism. Cardiovascular health indexes were unaffected by either of the treatments, but breakfast maintained more stable afternoon and evening glycemia than did fasting.

Figures

FIGURE 1.
FIGURE 1.
Components of energy balance under free-living conditions with either ingestion of ≥700 kcal before 1100 daily (breakfast group) or abstinence from all energy-providing nutrients until at least 1200 daily (fasting group). Values are means ± SEs. Estimated energy intake values for comparison of relative differences between groups are the average of the first [breakfast (n = 16) compared with fasting (n = 17): 2715 ± 565 compared with 2169 ± 490 kcal/d; P = 0.01] and last [breakfast (n = 16) compared with fasting (n = 17): 2745 ± 658 compared with 2214 ± 584 kcal/d; P = 0.02] week of intervention. Resting metabolic rate values (breakfast group, n = 16; fasting group, n = 16) were recorded at follow-up; diet-induced thermogenesis values (breakfast group, n = 16; fasting group, n = 17) were estimated from reported energy intake; physical activity values are the average of the first [breakfast (n = 15) compared with fasting (n = 15): 1455 ± 676 compared with 1015 ± 433 kcal/d; P = 0.04] and last [breakfast (n = 15) compared with fasting (n = 15): 1443 ± 705 compared with 998 ± 423 kcal/d; P = 0.05] week of intervention. The P value above the bar pertains to the overall comparison between groups; P values between the bars pertain to the specific comparison for the relevant component.
FIGURE 2.
FIGURE 2.
Physical activity thermogenesis under free-living conditions with either ingestion of ≥700 kcal before 1100 daily (breakfast group, n = 15) or abstinence from all energy-providing nutrients until at least 1200 daily (fasting group, n = 15). Values are means ± SEs partitioned by the time of day and intensity of energy expenditure. The P value above the bar pertains to the overall comparison between groups; P values between the bars pertain to the specific comparison for the relevant component. MET, metabolic equivalent.
FIGURE 3.
FIGURE 3.
Rates of [U-14C]-d-glucose uptake in adipocytes under basal, physiologic (50 pmol insulin/L), and supraphysiologic (20 nmol insulin/L) conditions, measured at baseline and after 6-wk ingestion of ≥700 kcal before 1100 daily (breakfast group; n = 13) or abstinence from all energy-providing nutrients until at least 1200 daily (fasting group; n = 16). Values are means ± SEs. Three-factor ANOVA (treatment × time × insulin) showed a significant effect of treatment (F = 4.2, P = 0.05) and insulin (F = 17.3, P < 0.001) with no significant effect of time nor any interaction of these factors. Ins, insulin.
FIGURE 4.
FIGURE 4.
Glucose variability before and after 1200 (expressed as CVs) derived from subcutaneous glucose concentrations continuously monitored during the first and last week of either ingesting ≥700 kcal before 1100 daily (breakfast group; n = 16) or abstaining from all energy-providing nutrients until at least 1200 daily (fasting group; n = 16). Values are means ± SEs. Two-factor ANOVA (treatment × time) showed a nonsignificant trend for treatment (F = 3.9, P = 0.06) with no significant effect of time nor any interaction of these factors during the morning (left side of panel) and a significant effect of treatment (F = 6.2, P = 0.02) with nonsignificant trends for time (F = 3.8, P = 0.06) and treatment × time (F = 3.6, P = 0.07) during the afternoon/evening (right side of panel).

References

    1. Casazza K, Fontaine KR, Astrup A, Birch LL, Brown AW, Bohan Brown MM, Durant N, Dutton G, Foster EM, Heymsfield SB, et al. Myths, presumptions, and facts about obesity. N Engl J Med 2013;368:446–54.
    1. Brown AW, Bohan Brown MM, Allison DB. Belief beyon d the evidence: using the proposed effect of breakfast on obesity to show 2 practices that distort scientific evidence. Am J Clin Nutr 2013;98:1298–08.
    1. Fabry P, Hejl Z, Fodor J, Braun T, Zvolankova K. The frequency of meals. Its relation to overweight, hypercholesterolaemia, and decreased glucose-tolerance. Lancet 1964;2:614–5.
    1. Barton BA, Eldridge AL, Thompson D, Affenito SG, Striegel-Moore RH, Franko DL, Albertson AM, Crockett SJ. The relationship of breakfast and cereal consumption to nutrient intake and body mass index: the National Heart, Lung, and Blood Institute Growth and Health Study. J Am Diet Assoc 2005;105:1383–9.
    1. Kant AK, Schatzkin A, Graubard BI, Ballard-Barbash R. Frequency of eating occasions and weight change in the NHANES I Epidemiologic Follow-up Study. Int J Obes Relat Metab Disord 1995;19:468–74.
    1. Smith KJ, Gall SL, McNaughton SA, Blizzard L, Dwyer T, Venn AJ. Skipping breakfast: longitudinal associations with cardiometabolic risk factors in the Childhood Determinants of Adult Health Study. Am J Clin Nutr 2010;92:1316–25.
    1. Cahill LE, Chiuve SE, Mekary RA, Jensen MK, Flint AJ, Hu FB, Rimm EB. prospective study of breakfast eating and incident coronary heart disease in a cohort of male US health professionals. Circulation 2013;128:337–43.
    1. Duval K, Strychar I, Cyr MJ, Prud'homme D, Rabasa-Lhoret R, Doucet E. Physical activity is a confounding factor of the relation between eating frequency and body composition. Am J Clin Nutr 2008;88:1200–5.
    1. Keski-Rahkonen A, Kaprio J, Rissanen A, Virkkunen M, Rose RJ. Breakfast skipping and health-compromising behaviors in adolescents and adults. Eur J Clin Nutr 2003;57:842–53.
    1. Ruxton CH, Kirk TR. Breakfast: a review of associations with measures of dietary intake, physiology and biochemistry. Br J Nutr 1997;78:199–213.
    1. Astbury NM, Taylor MA, Macdonald IA. 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 2011;141:1381–9.
    1. Dallosso HM, Murgatroyd PR, James WP. Feeding frequency and energy balance in adult males. Hum Nutr Clin Nutr 1982;36C:25–39.
    1. Smeets AJ, Westerterp-Plantenga MS. Acute effects on metabolism and appetite profile of one meal difference in the lower range of meal frequency. Br J Nutr 2008;99:1316–21.
    1. Taylor MA, Garrow JS. Compared with nibbling, neither gorging nor a morning fast affect short-term energy balance in obese patients in a chamber calorimeter. Int J Obes Relat Metab Disord 2001;25:519–28.
    1. Verboeket-van de Venne WP, Westerterp KR, Kester AD. Effect of the pattern of food intake on human energy metabolism. Br J Nutr 1993;70:103–15.
    1. Martin A, Normand S, Sothier M, Peyrat J, Louche-Pelissier C, Laville M. Is advice for breakfast consumption justified? Results from a short-term dietary and metabolic experiment in young healthy men. Br J Nutr 2000;84:337–44.
    1. Tai MM, Castillo P, Pi-Sunyer FX. Meal size and frequency: effect on the thermic effect of food. Am J Clin Nutr 1991;54:783–7.
    1. Belko A, Barbieri T. Effect of meal size and frequency on the thermic effect of food. Nutr Res 1987;7:237–42.
    1. Arnold LM, Ball MJ, Duncan AW, Mann J. Effect of isoenergetic intake of three or nine meals on plasma lipoproteins and glucose metabolism. Am J Clin Nutr 1993;57:446–51.
    1. Farshchi HR, Taylor MA, Macdonald IA. Decreased thermic effect of food after an irregular compared with a regular meal pattern in healthy lean women. Int J Obes Relat Metab Disord 2004;28:653–60.
    1. Farshchi HR, Taylor MA, Macdonald IA. Regular meal frequency creates more appropriate insulin sensitivity and lipid profiles compared with irregular meal frequency in healthy lean women. Eur J Clin Nutr 2004;58:1071–7.
    1. Keim NL, Van Loan MD, Horn WF, Barbieri TF, Mayclin PL. Weight loss is greater with consumption of large morning meals and fat-free mass is preserved with large evening meals in women on a controlled weight reduction regimen. J Nutr 1997;127:75–82.
    1. Stote KS, Baer DJ, Spears K, Paul DR, Harris GK, Rumpler WV, Strycula P, Najjar SS, Ferrucci L, Ingram DK, et al. A controlled trial of reduced meal frequency without caloric restriction in healthy, normal-weight, middle-aged adults. Am J Clin Nutr 2007;85:981–8.
    1. Verboeket-van de Venne WP, Westerterp KR. Frequency of feeding, weight reduction and energy metabolism. Int J Obes Relat Metab Disord 1993;17:31–6.
    1. Farshchi HR, Taylor MA, Macdonald IA. Deleterious effects of omitting breakfast on insulin sensitivity and fasting lipid profiles in healthy lean women. Am J Clin Nutr 2005;81:388–96.
    1. Schlundt DG, Hill JO, Sbrocco T, Pope-Cordle J, Sharp T. The role of breakfast in the treatment of obesity: a randomized clinical trial. Am J Clin Nutr 1992;55:645–51.
    1. Halsey LG, Huber JW, Low T, Ibeawuchi C, Woodruff P, Reeves S. Does consuming breakfast influence activity levels? An experiment into the effect of breakfast consumption on eating habits and energy expenditure. Health Nutr 2012;15:238–45.
    1. Corder K, Brage S, Mattocks C, Ness A, Riddoch C, Wareham NJ, Ekelund U. Comparison of two methods to assess PAEE during six activities in children. Med Sci Sports Exerc 2007;39:2180–8.
    1. Thompson D, Batterham AM, Bock S, Robson C, Stokes K. Assessment of low-to-moderate intensity physical activity thermogenesis in young adults using synchronized heart rate and accelerometry with branched-equation modeling. J Nutr 2006;136:1037–42.
    1. Betts JA, Thompson D, Richardson JD, Chowdhury EA, Jeans M, Holman GD, Tsintzas K. 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. Trials 2011;12:172.
    1. Schulz KF, Altman DG, Moher D. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials 2010;11:32.
    1. Kelly TL, Wilson KE, Heymsfield SB. Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS ONE 2009;4:e7038.
    1. Ludbrook J. Multiple comparison procedures updated. Clin Exp Pharmacol Physiol 1998;25:1032–7.
    1. Westerterp KR. Diet induced thermogenesis. Nutr Metab (Lond) 2004;1:5.
    1. de Castro JM. Accommodation of particular foods or beverages into spontaneously ingested evening meals. Appetite 1994;23:57–66.
    1. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of the Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001;285:2486–97.
    1. Fryer LG, Holness MJ, Sugden MC. Selective modification of insulin action in adipose tissue by hyperthyroidism. J Endocrinol 1997;154:513–22.
    1. Siegelaar SE, Holleman F, Hoekstra JB, DeVries JH. Glucose variability; does it matter? Endocr Rev 2010;31:171–82.
    1. Wyatt HR, Grunwald GK, Mosca CL, Klem ML, Wing RR, Hill JO. Long-term weight loss and breakfast in subjects in the National Weight Control Registry. Obes Res 2002;10:78–82.
    1. Corder K, van Sluijs EM, Steele RM, Stephen AM, Dunn V, Bamber D, Goodyer I, Griffin SJ, Ekelund U. Breakfast consumption and physical activity in British adolescents. Br J Nutr 2011;105:316–21.
    1. Schembre SM, Wen CK, Davis JN, Shen E, Nguyen-Rodriguez ST, Belcher BR, Hsu YW, Weigensberg MJ, Goran MI, Spruijt-Metz D. Eating breakfast more frequently is cross-sectionally associated with greater physical activity and lower levels of adiposity in overweight Latina and African American girls. Am J Clin Nutr 2013;98:275–81.
    1. Levine JA, Eberhardt NL, Jensen MD. Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science 1999;283:212–4.
    1. Simpson EJ, Holdsworth M, Macdonald IA. Interstitial glucose profile associated with symptoms attributed to hypoglycemia by otherwise healthy women. Am J Clin Nutr 2008;87:354–61.
    1. Staub H. Examination of sugar metabolisms in humans. Z Klin Med 1921;91:44–8.

Source: PubMed

3
購読する