The effects of short-term overfeeding on energy expenditure and nutrient oxidation in obesity-prone and obesity-resistant individuals

S L Schmidt, E H Kealey, T J Horton, S VonKaenel, D H Bessesen, S L Schmidt, E H Kealey, T J Horton, S VonKaenel, D H Bessesen

Abstract

Objective: The roles that energy expenditure (EE) and nutrient oxidation play in a predisposition for weight gain in humans remains unclear.

Subjects: We measured EE and respiratory exchange ratio (RER) in non-obese obesity-prone (OP; n=22) and obesity-resistant (OR; n=30) men and women following a eucaloric (EU) diet and after 3 days of overfeeding (1.4 × basal energy).

Results: Twenty-four hour EE, adjusted for fat-free mass and sex, measured while consuming a EU diet was not different between OP and OR subjects (2367±80 vs 2285±98 kcals; P=0.53). Following overfeeding, EE increased in both OP and OR (OP: 2506±63.7, P<0.01; OR: 2386±99 kcals, P<0.05). Overfeeding resulted in an increase in 24-hour RER (OP: 0.857±0.01 to 0.893±0.01, P=0.01; OR: 0.852±0.01 to 0.886±0.01, P=0.005), with no difference between groups in either the EU or overfeeding conditions (P>0.05). Nighttime RER (∼10pm-6:30am) did not change with overfeeding in OR (0.823±0.02 vs 0.837±0.01, P=0.29), but increased significantly in OP subjects (0.798±0.15 to 0.839±0.15, P<0.05), suggesting that fat oxidation during the night was downregulated to a greater extent in OP subjects following a brief period of overfeeding, as compared with OR subjects who appeared to maintain their usual rate of fat oxidation. Protein oxidation increased significantly in both OP (P<0.001) and OR (P<0.01) with overfeeding, with no differences between OP and OR.

Conclusion: These results support the idea that overfeeding a mixed diet results in increases in EE and RER, but these increases in EE and RER are likely not responsible for obesity resistance. Adaptive responses to overfeeding that occur during the night may have a role in opposing weight gain.

Figures

Figure 1
Figure 1
Frequency Distribution for change in 24h EE (24h EE in OF-EU study phases) in Obese Prone (OP) and Obese Resistant (OR) subjects.
Figure 2
Figure 2
Macronutrient Oxidation over 24h in Obese Prone (OP) and Obese Resistant (OR) subjects in the Eucaloric (EU) and Overfed (OF) study periods. $ p

References

    1. Bouchard C. Current understanding of the etiology of obesity: genetic and nongenetic factors. Am J Clin Nutr. 1991;53:1561S–1565S.
    1. Thorp AA, Owen N, Neuhaus M, Dunstan DW. Sedentary behaviors and subsequent health outcomes in adults a systematic review of longitudinal studies, 1996-2011. Am J Prev Med. 2011;41:207–215.
    1. Heitmann BL, Lissner L, Sorensen TI, Bengtsson C. Dietary fat intake and weight gain in women genetically predisposed for obesity. Am J Clin Nutr. 1995;61:1213–1217.
    1. Ravussin E, Lillioja S, Knowler WC, Christin L, Freymond D, Abbott WG, et al. Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med. 1988;318:467–472.
    1. Luke A, Dugas LR, Ebersole K, Durazo-Arvizu RA, Cao G, Schoeller DA, et al. Energy expenditure does not predict weight change in either Nigerian or African American women. Am J Clin Nutr. 2009;89:169–176.
    1. Weinsier RL, Nelson KM, Hensrud DD, Darnell BE, Hunter GR, Schutz Y. Metabolic predictors of obesity. Contribution of resting energy expenditure, thermic effect of food, and fuel utilization to four-year weight gain of post-obese and never-obese women. J Clin Invest. 1995;95:980–985.
    1. Westerterp KR. Dietary fat oxidation as a function of body fat. Curr Opin Lipidol. 2009;20:45–49.
    1. Astrup A. The relevance of increased fat oxidation for body-weight management: metabolic inflexibility in the predisposition to weight gain. Obes Rev
    1. Deriaz O, Tremblay A, Bouchard C. Non linear weight gain with long term overfeeding in man. Obes Res. 1993;1:179–185.
    1. Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G, et al. The response to long-term overfeeding in identical twins. N Engl J Med. 1990;322:1477–1482.
    1. Schmidt SL, Harmon KA, Sharp TA, Kealey EH, Bessesen DH. The Effects of Overfeeding on Spontaneous Physical Activity in Obesity Prone and Obesity Resistant Humans. Obesity (Silver Spring)
    1. Lowe MR, Butryn ML, Didie ER, Annunziato RA, Thomas JG, Crerand CE, et al. The Power of Food Scale. A new measure of the psychological influence of the food environment. Appetite. 2009;53:114–118.
    1. Stunkard AJ, Messick S. The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res. 1985;29:71–83.
    1. Garner DM, Olmsted MP, Bohr Y, Garfinkel PE. The eating attitudes test: psychometric features and clinical correlates. Psychol Med. 1982;12:871–878.
    1. Collins ME. Body figure perceptions and preferences among preadolescent children. International Journal of Eating Disorders. 1991;10:199–208.
    1. Radloff LS. The CES-D Scale: A Self-Report Depression Scale for Research in the General Population. Applied Psychological Measurement. 1977;1:385–401.
    1. Sun M, Reed GW, Hill JO. Modification of a whole room indirect calorimeter for measurement of rapid changes in energy expenditure. J Appl Physiol. 1994;76:2686–2691.
    1. Grunwald GK, Melanson EL, Forster JE, Seagle HM, Sharp TA, Hill JO. Comparison of methods for achieving 24-hour energy balance in a whole-room indirect calorimeter. Obes Res. 2003;11:752–759.
    1. Melanson EL, Gozansky WS, Barry DW, Maclean PS, Grunwald GK, Hill JO. When energy balance is maintained, exercise does not induce negative fat balance in lean sedentary, obese sedentary, or lean endurance-trained individuals. J Appl Physiol. 2009;107:1847–1856.
    1. Jequier E, Acheson K, Schutz Y. Assessment of energy expenditure and fuel utilization in man. Annu Rev Nutr. 1987;7:187–208.
    1. Elia M, Livesey G. Theory and validity of indirect calorimetry during net lipid synthesis. Am J Clin Nutr. 1988;47:591–607.
    1. Weyer C, Vozarova B, Ravussin E, Tataranni PA. Changes in energy metabolism in response to 48 h of overfeeding and fasting in Caucasians and Pima Indians. Int J Obes Relat Metab Disord. 2001;25:593–600.
    1. Freymond D, Larson K, Bogardus C, Ravussin E. Energy expenditure during normo- and overfeeding in peripubertal children of lean and obese Pima Indians. Am J Physiol. 1989;257:E647–653.
    1. Jebb SA, Prentice AM, Goldberg GR, Murgatroyd PR, Black AE, Coward WA. Changes in macronutrient balance during over- and underfeeding assessed by 12-d continuous whole-body calorimetry. Am J Clin Nutr. 1996;64:259–266.
    1. Diaz EO, Prentice AM, Goldberg GR, Murgatroyd PR, Coward WA. Metabolic response to experimental overfeeding in lean and overweight healthy volunteers. Am J Clin Nutr. 1992;56:641–655.
    1. Kaiyala KJ, Schwartz MW. Toward a more complete (and less controversial) understanding of energy expenditure and its role in obesity pathogenesis. Diabetes. 60:17–23.
    1. Howard BV, Bogardus C, Ravussin E, Foley JE, Lillioja S, Mott DM, et al. Studies of the etiology of obesity in Pima Indians. Am J Clin Nutr. 1991;53:1577S–1585S.
    1. Ravussin E. Energy metabolism in obesity. Studies in the Pima Indians. Diabetes Care. 1993;16:232–238.
    1. Krakoff J, Ma L, Kobes S, Knowler WC, Hanson RL, Bogardus C, et al. Lower metabolic rate in individuals heterozygous for either a frameshift or a functional missense MC4R variant. Diabetes. 2008;57:3267–3272.
    1. Avons P, James WP. Energy expenditure of young men from obese and non-obese families. Hum Nutr Clin Nutr. 1986;40:259–270.
    1. Treuth MS, Butte NF, Sorkin JD. Predictors of body fat gain in nonobese girls with a familial predisposition to obesity. Am J Clin Nutr. 2003;78:1212–1218.
    1. Amatruda JM, Statt MC, Welle SL. Total and resting energy expenditure in obese women reduced to ideal body weight. J Clin Invest. 1993;92:1236–1242.
    1. Wyatt HR, Grunwald GK, Seagle HM, Klem ML, McGuire MT, Wing RR, et al. Resting energy expenditure in reduced-obese subjects in the National Weight Control Registry. Am J Clin Nutr. 1999;69:1189–1193.
    1. Butte NF, Christiansen E, Sorensen TI. Energy imbalance underlying the development of childhood obesity. Obesity (Silver Spring) 2007;15:3056–3066.
    1. Astrup A. The relevance of increased fat oxidation for body-weight management: metabolic inflexibility in the predisposition to weight gain. Obesity Reviews. 2011;12:859–865.
    1. Ellis AC, Hyatt TC, Hunter GR, Gower BA. Respiratory Quotient Predicts Fat Mass Gain in Premenopausal Women. Obesity. 2010;18:2255–2259.
    1. Zurlo F, Lillioja S, Esposito-Del Puente A, Nyomba BL, Raz I, Saad MF, et al. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am J Physiol. 1990;259:E650–657.
    1. Hainer V, Kunesova M, Parizkova J, Stich V, Mikulova R, Slaba S. Respiratory quotient in obesity: its association with an ability to retain weight loss and with parental obesity. Sb Lek. 2000;101:99–104.
    1. Weinsier RL, Hunter GR, Zuckerman PA, Darnell BE. Low resting and sleeping energy expenditure and fat use do not contribute to obesity in women. Obesity Research. 2003;11:937–944.
    1. Bessesen DH, Rupp CL, Eckel RH. Dietary fat is shunted away from oxidation, toward storage in obese Zucker rats. Obes Res. 1995;3:179–189.
    1. Jackman MR, Kramer RE, MacLean PS, Bessesen DH. Trafficking of dietary fat in obesity-prone and obesity-resistant rats. Am J Physiol Endocrinol Metab. 2006;291:E1083–1091.
    1. Bessesen DH. Regulation of body weight: what is the regulated parameter? Physiol Behav. 104:599–607.
    1. Esquirol Y, Perret B, Ruidavets JB, Marquie JC, Dienne E, Niezborala M, et al. Shift work and cardiovascular risk factors: new knowledge from the past decade. Arch Cardiovasc Dis. 104:636–668.
    1. Huang W, Ramsey KM, Marcheva B, Bass J. Circadian rhythms, sleep, and metabolism. J Clin Invest. 121:2133–2141.

Source: PubMed

Подписаться