Protein status elicits compensatory changes in food intake and food preferences

Sanne Griffioen-Roose, Monica Mars, Els Siebelink, Graham Finlayson, Daniel Tomé, Cees de Graaf, Sanne Griffioen-Roose, Monica Mars, Els Siebelink, Graham Finlayson, Daniel Tomé, Cees de Graaf

Abstract

Background: Protein is an indispensable component within the human diet. It is unclear, however, whether behavioral strategies exist to avoid shortages.

Objective: The objective was to investigate the effect of a low protein status compared with a high protein status on food intake and food preferences.

Design: We used a randomized crossover design that consisted of a 14-d fully controlled dietary intervention involving 37 subjects [mean ± SD age: 21 ± 2 y; BMI (in kg/m(2)): 21.9 ± 1.5] who consumed individualized, isoenergetic diets that were either low in protein [0.5 g protein · kg body weight (BW)(-1) · d(-1)] or high in protein (2.0 g protein · kg BW(-1) · d(-1)). The diets were followed by an ad libitum phase of 2.5 d, during which a large array of food items was available, and protein and energy intakes were measured.

Results: We showed that in the ad libitum phase protein intake was 13% higher after the low-protein diet than after the high-protein diet (253 ± 70 compared with 225 ± 63 g, P < 0.001), whereas total energy intake was not different. The higher intake of protein was evident throughout the ad libitum phase of 2.5 d. In addition, after the low-protein diet, food preferences for savory high-protein foods were enhanced.

Conclusions: After a protein deficit, food intake and food preferences show adaptive changes that suggest that compensatory mechanisms are induced to restore adequate protein status. This indicates that there are human behavioral strategies present to avoid protein shortage and that these involve selection of savory high-protein foods. This trial was registered with the Dutch Trial register at http://www.trialregister.nl as NTR2491.

Figures

FIGURE 1.
FIGURE 1.
Design of the study. Subjects received a normal-protein diet for 2 d. Afterward, they were divided into 2 groups: one group received a low-protein diet for 14 d and one group received a high-protein diet for 14 d. The diets were followed by an ad libitum phase of 2.5 d during which a large array of food items was available, and intake was measured. Appetite was measured during 3 single 24-h periods: on day 2 of the normal-protein diet and on days 1 and 14 of the low- and high-protein diets (24-h appetite ratings). On day 14, the LFPQ was completed. After a 2-wk washout, the intervention was repeated and subjects switched groups. BW, body weight; LFPQ, Leeds Food Preference Questionnaire; lib, libitum.
FIGURE 2.
FIGURE 2.
Mean (±SEM) hourly rated feelings of hunger during waking hours from 1400 until 1200 the next day on days 1 and 14 during the low-protein diet (○) and the high-protein diet (•) assessed on a 10-point Likert scale. Subjects reported more hunger during the low-protein diet than during the high-protein diet on both days (P < 0.0001). The magnitude of this difference did not change (diet × day interaction: P = 0.52). Analyses were performed on AUCs by means of ANOVA (mixed-model procedure).
FIGURE 3.
FIGURE 3.
A: Total protein intake (g) of the lunch meals and of the home meal packages during the 3 d in the ad libitum phase after the low-protein diet (open bars) and high-protein diet (solid bars). Total protein intake (g) was higher after the low-protein diet than after the high-protein diet (P < 0.001). B: Total intake (MJ) of the lunch meals and home packages during the 3 d in the ad libitum phase after the low-protein diet (open bars) and after the high-protein diet (solid bars). Total energy intake (MJ) did not differ after the low-protein diet compared with after the high-protein diet (P = 0.14). Values are means ± SEMs (n = 37). The intake of protein (g) and energy (MJ) were compared by means of ANOVA (mixed-model procedure). home, home meal packages; meal, hot lunch meals.
FIGURE 4.
FIGURE 4.
A: Explicit wanting for the LP and HP sweet and savory products after the LP and HP diets assessed on a visual analog scale (100 mm). After the LP diet, there was greater explicit wanting for savory foods than for sweet foods (P < 0.001). No preference was evident after the HP diet. Also, no preference was evident for HP or LP products after either of the diets. B: Implicit wanting for the LP and HP sweet and savory products after the LP and HP diets expressed as a standardized d score, which is a validated algorithm to transform reaction time (24). A smaller d score means a greater implicit wanting for that food category relative to other categories in the task. After the LP diet, there was a greater implicit wanting for savory foods than for sweet foods (P < 0.05) and a greater implicit wanting for HP foods than for LP foods (P < 0.05). No preference was evident after the HP diet. Values are means ± SEMs (n = 37). Results of the Leeds Food Preference Questionnaire were analyzed by using ANOVA (General Linear Model procedure). HP, high-protein; LP, low-protein.

References

    1. Tome D. Protein, amino acids and the control of food intake. Br J Nutr 2004;92:S27–30
    1. Bensaïd A, Tomé D, Gietzen D, Even P, Morens C, Gausseres N, Fromentin G. Protein is more potent than carbohydrate for reducing appetite in rats. Physiol Behav 2002;75:577–82
    1. Apolzan JW, Carnell NS, Mattes RD, Campbell WW. Inadequate dietary protein increases hunger and desire to eat in younger and older men. J Nutr 2007;137:1478–82
    1. de Castro JM. Prior day's intake has macronutrient-specific delayed negative feedback effects on the spontaneous food intake of free-living humans. J Nutr 1998;128:61–7
    1. Simpson SJ, Raubenheimer D. Obesity: the protein leverage hypothesis. Obes Rev 2005;6:133–42
    1. Metcalf PA, Scragg RRK, Schaaf D, Dyall L, Black PN, Jackson R. Dietary intakes of European, Māori, Pacific and Asian adults living in Auckland: the Diabetes, Heart and Health Study. Aust N Z J Public Health 2008;32:454–60
    1. Simpson SJ, Batley R, Raubenheimer D. Geometric analysis of macronutrient intake in humans: the power of protein? Appetite 2003;41:123–40
    1. Long SJ, Jeffcoat AR, Millward DJ. Effect of habitual dietary-protein intake on appetite and satiety. Appetite 2000;35:79–88
    1. Booth DA, Simson PC. Food preferences acquired by association with variations in amino acid nutrition. Q J Exp Psychol 1971;23:135–45
    1. Booth DA. Food intake compensation for increase or decrease in the protein content of the diet. Behav Biol 1974;12:31–40
    1. Gibson EL, Booth DA. Acquired protein appetite in rats: dependence on a protein-specific need state. Experientia 1986;42:1003–4
    1. Simpson SJ, White PR. Associative learning and locust feeding: evidence for a `learned hunger’ for protein. Anim Behav 1990;40:506–13
    1. Gietzen DW, Hao S, Anthony TG. Mechanisms of Food Intake Repression in Indispensable Amino Acid Deficiency. Annu Rev Nutr 2007;27:63–78
    1. Barkeling B, Rossner S, Bjorvell H. Effect of a high-protein meal (meat) and a high-carbohydrate meal (vegetarian) on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int J Obes (Lond) 1990;14:743–51
    1. Hill AJ, Blundell JE. Macronutrient and Satiety: The effects of a high-protein or high-carbohydrate meal on subjective motivation to eat and food preferences. Nutr Behav 1986;3:133–44
    1. Vazquez M, Pearson PB, Beauchamp GK. Flavor preferences in malnourished mexican infants. Physiol Behav 1982;28:513–9
    1. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA) Scientific Opinion on the substantiation of health claims related to protein and increase in satiety leading to a reduction in energy intake (ID 414, 616, 730), contribution to the maintenance or achievement of a normal body weight (ID 414, 616, 730), maintenance of normal bone (ID 416) and growth or maintenance of muscle mass (ID 415, 417, 593, 594, 595, 715) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA J 2010;8:1811
    1. Blatt AD, Roe LS, Rolls BJ. Increasing the protein content of meals and its effect on daily energy intake. J Am Diet Assoc 2011;111:290–4
    1. de Graaf C, Hulshof T, Weststrate JA, Jas P. Short-term effects of different amounts of protein, fats, and carbohydrates on satiety. Am J Clin Nutr 1992;55:33–8
    1. Halton TL, Hu FB. The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr 2004;23:373–85
    1. Van Strien T. Nederlandse Vragenlijst voor eetgedrag Handleiding. [Dutch Eating Behavior Questionnaire manual.]. Amsterdam, Netherlands: Boom Test Publishers, 2005
    1. WHO Protein and amino acid requirements in human nutrition. Report of a Joint WHO/FAO/UNU Expert Consultation. Geneva, Switzerland: World Health Organization, 2007
    1. Hulshof K, Ocké M, Van Rossum C, Buurma-Rethans E, Brants H, Drijvers J. Results of the National Food Consumption Survey 2003. Bilthoven, Netherlands: RIVM (National Institute for Public Health and the Environment), 2003
    1. Finlayson G, King N, Blundell JE. Is it possible to dissociate ‘liking’ and ‘wanting’ for foods in humans? A novel experimental procedure. Physiol Behav 2007;90:36–42
    1. Griffioen-Roose S, Finlayson G, Mars M, Blundell JE, de Graaf C. Measuring food reward and the transfer effect of sensory specific satiety. Appetite 2010;55:648–55
    1. Griffioen-Roose S, Mars M, Finlayson G, Blundell JE, de Graaf C. The effect of within-meal protein content and taste on subsequent food choice and satiety. Br J Nutr 2011;106:779–88
    1. Association of Official Analytical Chemists International Official methods of analysis of AOAC International. 16th ed Gaithersburg, MD: Association of Official Analytical Chemists International, 1997, revised 1999
    1. Siebelink E, Geelen A, de Vries JHM. Self-reported energy intake by FFQ compared with actual energy intake to maintain body weight in 516 adults. Br J Nutr 2011;106:274–81
    1. WHO Principles for the estimation of energy requirements. Energy and protein requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. 2nd ed Geneva, Switzerland: World Health Organization, 1985:34–52
    1. NEVO Tabel. Dutch Nutrient Database 2006. Den Haag, Netherlands: Voedingscentrum, 2006
    1. Greenwald AG, Nosek BA, Banaji MR. Understanding and using the Implicit Association Test: I. An improved scoring algorithm. J Pers Soc Psychol 2003;85:197–216
    1. Bingham S, Cummings JH. The use of 4-aminobenzoic acid as a marker to validate the completeness of 24 h urine collections in man. Clin Sci (Lond) 1983;64:629–35
    1. Luscombe-Marsh ND, Smeets AJPG, Westerterp-Plantenga MS. Taste sensitivity for monosodium glutamate and an increased liking of dietary protein. Br J Nutr 2008;99:904–8
    1. Yamaguchi S, Ninomiya K. Umami and food palatability. J Nutr 2000;130:921S–6S
    1. Booth DA. Conditioned satiety in the rat. J Comp Physiol Psychol 1972;81:457–71
    1. Booth DA. Food-conditioned eating preferences and aversions with interoceptive elements—conditioned appetites and satieties. Ann N Y Acad Sci 1985;443:22–41
    1. Baker BJ, Booth DA, Duggan JP, Gibson EL. Protein appetite demonstrated: Learned specificity of protein-cue preference to protein need in adult rats. Nutr Res 1987;7:481–7
    1. Gibson EL, Wainwright CJ, Booth DA. Disguised protein in lunch after low-protein breakfast conditions food-flavor preferences dependent on recent lack of protein intake. Physiol Behav 1995;58:363–71
    1. Rolls BJ, Rolls ET, Rowe EA, Sweeney K. Sensory specific satiety in man. Physiol Behav 1981;27:137–42
    1. Berridge KC, Robinson TE, Aldridge JW. Dissecting components of reward: `liking’, `wanting’, and learning. Curr Opin Pharmacol 2009;9:65–73
    1. Prestwich A, Hurling R, Baker S. Implicit shopping: attitudinal determinants of the purchasing of healthy and unhealthy foods. Psychol Health 2011;26:875–85

Source: PubMed

3
Abonnere