A randomized, controlled, crossover trial to assess the acute appetitive and metabolic effects of sausage and egg-based convenience breakfast meals in overweight premenopausal women

Tia M Rains, Heather J Leidy, Kristen D Sanoshy, Andrea L Lawless, Kevin C Maki, Tia M Rains, Heather J Leidy, Kristen D Sanoshy, Andrea L Lawless, Kevin C Maki

Abstract

Background: Dietary protein at breakfast has been shown to enhance satiety and reduce subsequent energy intake more so than carbohydrate or fat. However, relatively few studies have assessed substitution of protein for carbohydrate on indicators of appetite and glucose homeostasis simultaneously.

Methods: The acute appetitive and metabolic effects of commercially-prepared sausage and egg-based breakfast meals at two different protein levels (30 g and 39 g/serving), vs. a low-protein pancake breakfast (3 g protein) and no breakfast (water), were examined in premenopausal women (N = 35; age 32.5 ± 1.6 yr; BMI 24.8 ± 0.5 kg/m(2)). Test products provided ~280 kcal/serving and similar fat (12-14 g) and fiber contents (0-1 g). Visual Analog Scale ratings for appetite (hunger, fullness, prospective consumption, desire to eat) and repeated blood sampling for plasma glucose and insulin concentrations were assessed throughout each test day. Energy intake was recorded at an ad libitum lunch meal at 240 min.

Results: Results showed increased satiety ratings for both the 30 and 39 g protein meals vs. the low-protein and no breakfast conditions (p < 0.001 for all). Postprandial glucose and insulin excursions were lower following the 30 g and 39 g protein conditions vs. the low-protein condition, with smaller responses following the 39 g vs. 30 g protein condition (p < 0.05 for all). Energy intake at lunch was significantly less (p < 0.001) following the 39 g protein meal (692 kcal) vs. the low-protein and no breakfast conditions (789 and 810 kcal, respectively). Total energy intake from the test condition + lunch was higher (p < 0.01) for the 30 and 39 g meals (982 and 983 kcal, respectively) vs. no breakfast (810 kcal), and less than the low protein breakfast (1064 kcal; p < 0.01 vs. 39 g condition only).

Conclusions: Results suggest that convenience meals providing 30 or 39 g protein/serving produce greater appetite control, lower postprandial glycemia and insulinemia, and reduced subsequent intake at lunch relative to a low-protein control, or no breakfast.

Trial registration: NCT01713114.

Figures

Figure 1
Figure 1
Test visit flow diagram.
Figure 2
Figure 2
Appetite VAS ratings (hunger and fullness) at each timepoint and niAUC values for each condition. Data are presented as mean ± SEM. Different letters indicate differences between conditions (p < 0.0001). Pairwise comparisons between conditions were conducted using Tukey’s adjustment for multiple comparisons.
Figure 3
Figure 3
Appetite VAS ratings at each timepoint (left) and niAUC values (right) for each condition. Data are for desire to eat and prospective food consumption. Data are presented as mean ± SEM. Different letters indicate differences between conditions (p < 0.0001). Pairwise comparisons between conditions were conducted using Tukey’s adjustment for multiple comparisons.
Figure 4
Figure 4
Plasma glucose and insulin at each timepoint (left) and AUC values (right) for each condition. Data are presented as mean ± SEM. Different letters indicate differences between conditions (p < 0.0001). Pairwise comparisons between conditions were conducted using Tukey’s adjustment for multiple comparisons.
Figure 5
Figure 5
Lunch (left) and total (preload + lunch; right) energy intake following each condition (t = 240 min). Data are presented as median (75th percentile). Different letters indicate differences between conditions (p < 0.05, note - energy intake at lunch for the 30 g Pro breakfast vs. LP breakfast p = 0.053). Pairwise comparisons between conditions were conducted using Tukey’s adjustment for multiple comparisons.

References

    1. Holt SH, Miller JC, Petocz P, Farmakalidis E. A satiety index of common foods. Eur J Clin Nutr. 1995;49:675–90.
    1. Stubbs J, Ferres S, Horgan G. Energy density of foods: effects on energy intake. Crit Rev Food Sci Nutr. 2000;40:481–515. doi: 10.1080/10408690091189248.
    1. Porrini M, Santangelo A, Crovetti R, Riso P, Testolin G, Blundell JE. Weight, protein, fat, and timing of preloads affect food intake. Physiol Behav. 1997;62:563–70. doi: 10.1016/S0031-9384(97)00162-5.
    1. Johnstone AM, Stubbs RJ, Harbron CG. Effect of overfeeding macronutrients on day-to-day food intake in man. Eur J Clin Nutr. 1996;50:418–30.
    1. Leidy HJ, Bossingham MJ, Mattes RD, Campbell WW. Increased dietary protein consumed at breakfast leads to an initial and sustained feeling of fullness during energy restriction compared to other meal times. Br J Nutr. 2009;101:798–803. doi: 10.1017/S0007114508051532.
    1. Fallaize R, Wilson L, Gray J, Morgan LM, Griffin BA. Variation in the effects of three different breakfast meals on subjective satiety and subsequent intake of energy at lunch and evening meal. Eur J Nutr. 2013;52:1353–9. doi: 10.1007/s00394-012-0444-z.
    1. Vander Wal JS, Marth JM, Khosla P, Jen KL, Dhurandhar NV. Short-term effect of eggs on satiety in overweight and obese subjects. J Am Coll Nutr. 2005;24:510–5. doi: 10.1080/07315724.2005.10719497.
    1. Leidy HJ, Carnell NS, Mattes RD, Campbell WW. Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women. Obesity. 2007;15:421–9. doi: 10.1038/oby.2007.531.
    1. Leidy HJ, Racki EM. 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) 2010;34:1125–33. doi: 10.1038/ijo.2010.3.
    1. Ratliff J, Leite JO, de Ogburn R, Puglisi MJ, VanHeest J, Fernandez ML. Consuming eggs for breakfast influences plasma glucose and ghrelin, while reducing energy intake during the next 24 hours in adult men. Nutr Res. 2010;30:96–103. doi: 10.1016/j.nutres.2010.01.002.
    1. Clegg M, Shafat A. Energy and macronutrient composition of breakfast affect gastric emptying of lunch and subsequent food intake, satiety and satiation. Appetite. 2010;54:517–23. doi: 10.1016/j.appet.2010.02.005.
    1. Leidy HJ, Ortinau LC, Douglas SM, Hoertel HA. 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. 2013;97:677–88. doi: 10.3945/ajcn.112.053116.
    1. Alfenas Rde C, Bressan J, Paiva AC. Effects of protein quality on appetite and energy metabolism in normal weight subjects. Arq Bras Endocrinol Metabol. 2010;54:45–51. doi: 10.1590/S0004-27302010000100008.
    1. Dong JY, Zhang ZL, Wang PY, Qin LQ. Effects of high-protein diets on body weight, glycaemic control, blood lipids and blood pressure in type 2 diabetes: meta-analysis of randomised controlled trials. Br J Nutr. 2013;110:781–9. doi: 10.1017/S0007114513002055.
    1. Clifton PM, Condo D, Keogh JB. Long term weight maintenance after advice to consume low carbohydrate, higher protein diets–a systematic review and meta analysis. Nutr Metab Cardiovasc Dis. 2014;24:224–35. doi: 10.1016/j.numecd.2013.11.006.
    1. Lorenzo C, Okoloise M, Williams K, Stern MP, Haffner SM. The metabolic syndrome as predictor of type 2 diabetes: the San Antonio heart study. Diabetes Care. 2003;26:3153. doi: 10.2337/diacare.26.11.3153.
    1. Brunner EJ, Shipley MJ, Witte DR, Fuller JH, Marmot MG. Relation between blood glucose and coronary mortality over 33 years in the Whitehall Study. Diabetes Care. 2006;29:26–31. doi: 10.2337/diacare.29.01.06.dc05-1405.
    1. Fulgoni VL., 3rd Current protein intake in America: analysis of the National Health and Nutrition Examination Survey, 2003–2004. Am J Clin Nutr. 2008;87:1554S–7.
    1. Rains TM, Maki KC, Fulgoni VL, 3rd, Auestad N. Protein intake at breakfast is associated with reduced energy intake at lunch: an analysis of NHANES 2003–2006. FASEB J. 2013;27:349.7.
    1. Kant AK, Graubard BI. Secular trends in patterns of self-reported food consumption of adult Americans: NHANES 1971–1975 to NHANES 1999–2002. Am J Clin Nutr. 2006;84:1215–23.
    1. Stunkard AJ, Messick S. The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res. 1985;29:71–83. doi: 10.1016/0022-3999(85)90010-8.
    1. Flint A, Raben A, Blundell JE, Astrup A. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord. 2000;24:38–48. doi: 10.1038/sj.ijo.0801083.
    1. Šidák Z. On probabilities of rectangles in multivariate normal Student distributions: their dependence on correlations. Ann Math Statist. 1971;41:169–75.
    1. Brouns F, Bjorck I, Frayn KN, Gibbs AL, Lang V, Slama G, et al. Glycaemic index methodology. Nutr Res Rev. 2005;18:145–71. doi: 10.1079/NRR2005100.
    1. Meinert L, Kehlet U, Aaslyng MD. Consuming pork proteins at breakfast reduces the feeling of hunger before lunch. Appetite. 2012;59:201–3. doi: 10.1016/j.appet.2012.04.018.
    1. Belza A, Ritz C, Sorensen MQ, Holst JJ, Rehfeld JF, Astrup A. Contribution of gastroenteropancreatic appetite hormones to protein-induced satiety. Am J Clin Nutr. 2013;97:980–9. doi: 10.3945/ajcn.112.047563.
    1. International Food Information Council, IFIC. (2008, December 19). IFIC Review: Breakfast and Health. Retreived from . Accessed November 6, 2012.
    1. Sacks FM, Carey VJ, Anderson CAM, Miller ER, III, Copeland T, Charleston J, et al. Effects of high vs low glycemic index of dietary carbohydrate on cardiovascular disease risk factors and insulin sensitivity. JAMA. 2014;312:2531–41. doi: 10.1001/jama.2014.16658.
    1. Gannon MC, Nuttall JA, Damberg G, Gupta V, Nuttall FG. Effect of protein ingestion on the glucose appearance rate in people with type 2 diabetes. J Clin Endocrinol Metab. 2001;86:1040–7.
    1. Anderson HG, Catherine NLA, Woodend DM, Wolever TMS. Inverse association between the effect of carbohydrates on blood glucose and subsequent short-term food intake in young men. Am J Clin Nutr. 2002;76:1023–30.
    1. Karatsoreos IN, Thaler JP, Borgland SL, Champagne FA, Hurd YL, Hill MN. Food for thought: hormonal, experiential, and neural influences on feeding and obesity. J Neurosci. 2013;33:17610–6. doi: 10.1523/JNEUROSCI.3452-13.2013.
    1. Probst A, Humpeler S, Heinzl H, Blasche G, Ekmekcioglu C. Short-term effect of macronutrient composition and glycemic index of a yoghurt breakfast on satiety and mood in healthy young men. Forsch Komplementmed. 2012;19:247–51. doi: 10.1159/000343163.
    1. Bertenshaw EJ, Lluch A, Yeomans MR. Satiating effects of protein but not carbohydrate consumed in a between-meal beverage context. Physiol Behav. 2008;93:427–36. doi: 10.1016/j.physbeh.2007.09.014.
    1. Dove ER, Hodgson JM, Puddey IB, Beilin LJ, Lee YP, Mori TA. Skim milk compared with a fruit drink acutely reduces appetite and energy intake in overweight men and women. Am J Clin Nutr. 2009;90:70–5. doi: 10.3945/ajcn.2008.27411.
    1. Hursel R, van der Zee L, Westerterp-Plantenga MS. Effects of a breakfast yoghurt, with additional total whey protein or caseinomacropeptide-depleted alpha-lactalbumin-enriched whey protein, on diet-induced thermogenesis and appetite suppression. Br J Nutr. 2010;103:775–80. doi: 10.1017/S0007114509992352.
    1. Tsuchiya A, Almiron-Roig E, Lluch A, Guyonnet D, Drewnowski A. Higher satiety ratings following yogurt consumption relative to fruit drink or dairy fruit drink. J Am Diet Assoc. 2006;106:550–7. doi: 10.1016/j.jada.2006.01.004.
    1. Bish CL, Blanck HM, Serdula MK, Marcus M, Kohl HW, 3rd, Khan LK. Diet and physical activity behaviors among Americans trying to lose weight: 2000 behavioral risk factor surveillance system. Obesity Res. 2005;13:596–607. doi: 10.1038/oby.2005.64.
    1. Maki KC, Rains TM, Kaden VN, Raneri KR, Davidson MH. Effects of a reduced-glycemic-load diet on body weight, body composition, and cardiovascular disease risk markers in overweight and obese adults. Am J Clin Nutr. 2007;85:724–34.
    1. Vander Wal JS, Gupta A, Khosla P, Dhurhandar NV. Egg breakfast enhances weight loss. Int J Obes (Lond) 2008;32:1545–51. doi: 10.1038/ijo.2008.130.
    1. Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, et al. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82:41–8.
    1. Bowen J, Noakes M, Trenerry C, Clifton PM. Energy intake, ghrelin, and cholecystokinin after different carbohydrate and protein preloads in overweight men. J Clin Endocrinol Metab. 2006;91:1477–83. doi: 10.1210/jc.2005-1856.
    1. Batterham RL, Heffron H, Kapoor S, Chivers JE, Chandarana K, Herzog H, et al. Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab. 2006;4:223–33. doi: 10.1016/j.cmet.2006.08.001.
    1. Blom WA, Lluch A, Stafleu A, Vinoy S, Holst JJ, Schaafsma G, et al. Effect of a high-protein breakfast on the postprandial ghrelin response. Am J Clin Nutr. 2006;83:211–20.
    1. Schloegl H, Percik R, Horstmann A, Villringer A, Stumvoll M. Peptide hormones regulating appetite–focus on neuroimaging studies in humans. Diabetes Metab Res Rev. 2011;27:104–12. doi: 10.1002/dmrr.1154.
    1. Holt SH, Miller JB. Increased insulin responses to ingested foods are associated with lessened satiety. Appetite. 1995;24:43–54. doi: 10.1016/S0195-6663(95)80005-0.
    1. Leidy HJ, Apolzan JW, Mattes RD, Campbell WW. Food form and portion size affect postprandial appetite sensations and hormonal responses in healthy, nonobese, older adults. Obesity. 2010;18:293–9. doi: 10.1038/oby.2009.217.
    1. Sobrino Crespo C, Perianes Cachero A, Puebla Jimenez L, Barrios V, Arilla Ferreiro E. Peptides and food intake. Front Endocrinol. 2014;5:58. doi: 10.3389/fendo.2014.00058.
    1. Crovetti R, Porrini M, Santangelo A, Testolin G. The influence of thermic effect of food on satiety. Eur J Clin Nutr. 1998;52:482–8. doi: 10.1038/sj.ejcn.1600578.
    1. Veldhorst M, Smeets A, Soenen S, Hochstenbach-Waelen A, Hursel R, Diepvens K, et al. Protein-induced satiety: effects and mechanisms of different proteins. Physiol Behav. 2008;94:300–7. doi: 10.1016/j.physbeh.2008.01.003.
    1. Blundell J, de Graaf C, Hulshof T, Jebb S, Livingstone B, Lluch A, et al. Appetite control: methodological aspects of the evaluation of foods. Obes Rev. 2010;11:251–70. doi: 10.1111/j.1467-789X.2010.00714.x.
    1. Williams RA, Roe LS, Rolls BJ. Assessment of satiety depends on the energy density and portion size of the test meal. Obesity. 2014;22:318–24. doi: 10.1002/oby.20589.

Source: PubMed

3
Abonneren