Actigraphy-Derived Sleep Is Associated with Eating Behavior Characteristics

Rocío Barragán, Faris M Zuraikat, Victoria Tam, Samantha Scaccia, Justin Cochran, Si Li, Bin Cheng, Marie-Pierre St-Onge, Rocío Barragán, Faris M Zuraikat, Victoria Tam, Samantha Scaccia, Justin Cochran, Si Li, Bin Cheng, Marie-Pierre St-Onge

Abstract

Poor sleep is a determinant of obesity, with overconsumption of energy contributing to this relationship. Eating behavior characteristics are predictive of energy intake and weight change and may underlie observed associations of sleep with weight status and obesity risk factors. However, relationships between sleep and dimensions of eating behavior, as well as possible individual differences in these relations, are not well characterized. Therefore, the aim of this study was to evaluate whether sleep behaviors, including duration, timing, quality, and regularity relate to dietary restraint, disinhibition, and tendency towards hunger and to explore whether these associations differ by sex. This cross-sectional study included 179 adults aged 20-73 years (68.7% women, 64.8% with BMI ≥ 25 kg/m2). Sleep was evaluated by accelerometry over 2 weeks. Eating behavior dimensions were measured with the Three-Factor Eating Questionnaire. Prolonged wake after sleep onset (WASO) (0.029 ± 0.011, p = 0.007), greater sleep fragmentation index (0.074 ± 0.036, p = 0.041), and lower sleep efficiency (-0.133 ± 0.051, p = 0.010) were associated with higher dietary restraint. However, higher restraint attenuated associations of higher WASO and sleep fragmentation with higher BMI (p-interactions < 0.10). In terms of individual differences, sex influenced associations of sleep quality measures with tendency towards hunger (p-interactions < 0.10). Stratified analyses showed that, in men only, higher sleep fragmentation index, longer sleep onset latency, and lower sleep efficiency were associated with greater tendency towards hunger (β = 0.115 ± 0.037, p = 0.003, β = 0.169 ± 0.072, p = 0.023, β = -0.150 ± 0.055, p = 0.009, respectively). Results of this analysis suggest that the association of poor sleep on food intake could be exacerbated in those with eating behavior traits that predispose to overeating, and this sleep-eating behavior relation may be sex-dependent. Strategies to counter overconsumption in the context of poor quality sleep should be evaluated in light of eating behavior traits.

Keywords: BMI; disinhibition; eating behavior; hunger; restraint; sex; sleep.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Flow chart of participant inclusion and exclusion criteria for the different measures included in the study. BMI: body mass index; PSQI: Pittsburgh Sleep Quality Index; BQ: Berlin Questionnaire.

References

    1. Bayon V., Leger D., Gomez-Merino D., Vecchierini M.F., Chennaoui M. Sleep debt and obesity. Ann. Med. 2014;46:264–272. doi: 10.3109/07853890.2014.931103.
    1. Itani O., Jike M., Watanabe N., Kaneita Y. Short sleep duration and health outcomes: A systematic review, meta-analysis, and meta-regression. Sleep Med. 2017;32:246–256. doi: 10.1016/j.sleep.2016.08.006.
    1. Ogilvie R.P., Patel S.R. The epidemiology of sleep and obesity. Sleep Health. 2017;3:383–388. doi: 10.1016/j.sleh.2017.07.013.
    1. Reutrakul S., Van Cauter E. Sleep influences on obesity, insulin resistance, and risk of type 2 diabetes. Metabolism. 2018;84:56–66. doi: 10.1016/j.metabol.2018.02.010.
    1. St-Onge M.P. Sleep-obesity relation: Underlying mechanisms and consequences for treatment. Obes. Rev. 2017;18(Suppl. 1):34–39. doi: 10.1111/obr.12499.
    1. Wu Y., Zhai L., Zhang D. Sleep duration and obesity among adults: A meta-analysis of prospective studies. Sleep Med. 2014;15:1456–1462. doi: 10.1016/j.sleep.2014.07.018.
    1. Zuraikat F.M., Makarem N., Redline S., Aggarwal B., Jelic S., St-Onge M.P. Sleep Regularity and Cardiometabolic Heath: Is Variability in Sleep Patterns a Risk Factor for Excess Adiposity and Glycemic Dysregulation? Curr. Diabetes Rep. 2020;20:38. doi: 10.1007/s11892-020-01324-w.
    1. Al Khatib H.K., Harding S.V., Darzi J., Pot G.K. The effects of partial sleep deprivation on energy balance: A systematic review and meta-analysis. Eur. J. Clin. Nutr. 2017;71:614–624. doi: 10.1038/ejcn.2016.201.
    1. Capers P.L., Fobian A.D., Kaiser K.A., Borah R., Allison D.B. A systematic review and meta-analysis of randomized controlled trials of the impact of sleep duration on adiposity and components of energy balance. Obes. Rev. 2015;16:771–782. doi: 10.1111/obr.12296.
    1. St-Onge M.P., Roberts A.L., Chen J., Kelleman M., O’Keeffe M., RoyChoudhury A., Jones P.J. Short sleep duration increases energy intakes but does not change energy expenditure in normal-weight individuals. Am. J. Clin. Nutr. 2011;94:410–416. doi: 10.3945/ajcn.111.013904.
    1. Chaput J.P., St-Onge M.P. Increased food intake by insufficient sleep in humans: Are we jumping the gun on the hormonal explanation? Front. Endocrinol. 2014;5:116. doi: 10.3389/fendo.2014.00116.
    1. Benedict C., Brooks S.J., O’Daly O.G., Almen M.S., Morell A., Aberg K., Gingnell M., Schultes B., Hallschmid M., Broman J.E., et al. Acute sleep deprivation enhances the brain’s response to hedonic food stimuli: An fMRI study. J. Clin. Endocrinol. Metab. 2012;97:E443–E447. doi: 10.1210/jc.2011-2759.
    1. Demos K.E., Sweet L.H., Hart C.N., McCaffery J.M., Williams S.E., Mailloux K.A., Trautvetter J., Owens M.M., Wing R.R. The Effects of Experimental Manipulation of Sleep Duration on Neural Response to Food Cues. Sleep. 2017;40 doi: 10.1093/sleep/zsx125.
    1. Nechifor R.E., Ciobanu D., Vonica C.L., Popita C., Roman G., Bala C., Mocan A., Inceu G., Craciun A., Rusu A. Social jetlag and sleep deprivation are associated with altered activity in the reward-related brain areas: An exploratory resting-state fMRI study. Sleep Med. 2020;72:12–19. doi: 10.1016/j.sleep.2020.03.018.
    1. Rihm J.S., Menz M.M., Schultz H., Bruder L., Schilbach L., Schmid S.M., Peters J. Sleep Deprivation Selectively Upregulates an Amygdala-Hypothalamic Circuit Involved in Food Reward. J. Neurosci. 2019;39:888–899. doi: 10.1523/JNEUROSCI.0250-18.2018.
    1. St-Onge M.P., McReynolds A., Trivedi Z.B., Roberts A.L., Sy M., Hirsch J. Sleep restriction leads to increased activation of brain regions sensitive to food stimuli. Am. J. Clin. Nutr. 2012;95:818–824. doi: 10.3945/ajcn.111.027383.
    1. Hansen T.T., Hjorth M.F., Sandby K., Andersen S.V., Astrup A., Ritz C., Bullo M., Camacho-Barcia M.L., Garcia-Gavilan J.F., Salas-Salvado J., et al. Predictors of successful weight loss with relative maintenance of fat-free mass in individuals with overweight and obesity on an 8-week low-energy diet. Br. J. Nutr. 2019;122:468–479. doi: 10.1017/S0007114519001296.
    1. Quick V., Byrd-Bredbenner C., White A.A., Brown O., Colby S., Shoff S., Lohse B., Horacek T., Kidd T., Greene G. Eat, sleep, work, play: Associations of weight status and health-related behaviors among young adult college students. Am. J. Health Promot. 2014;29:e64–e72. doi: 10.4278/ajhp.130327-QUAN-130.
    1. Blumfield M.L., Bei B., Zimberg I.Z., Cain S.W. Dietary disinhibition mediates the relationship between poor sleep quality and body weight. Appetite. 2018;120:602–608. doi: 10.1016/j.appet.2017.10.022.
    1. Stunkard A.J., 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. Bryant E.J., King N.A., Blundell J.E. Disinhibition: Its effects on appetite and weight regulation. Obes. Rev. 2008;9:409–419. doi: 10.1111/j.1467-789X.2007.00426.x.
    1. French S.A., Mitchell N.R., Wolfson J., Finlayson G., Blundell J.E., Jeffery R.W. Questionnaire and laboratory measures of eating behavior. Associations with energy intake and BMI in a community sample of working adults. Appetite. 2014;72:50–58. doi: 10.1016/j.appet.2013.09.020.
    1. Hays N.P., Roberts S.B. Aspects of eating behaviors “disinhibition” and “restraint” are related to weight gain and BMI in women. Obesity. 2008;16:52–58. doi: 10.1038/oby.2007.12.
    1. Borg P., Fogelholm M., Kukkonen-Harjula K. Food selection and eating behaviour during weight maintenance intervention and 2-y follow-up in obese men. Int. J. Obes. 2004;28:1548–1554. doi: 10.1038/sj.ijo.0802790.
    1. Bryant E.J., Caudwell P., Hopkins M.E., King N.A., Blundell J.E. Psycho-markers of weight loss. The roles of TFEQ Disinhibition and Restraint in exercise-induced weight management. Appetite. 2012;58:234–241. doi: 10.1016/j.appet.2011.09.006.
    1. Chambers L., Yeomans M.R. Individual differences in satiety response to carbohydrate and fat. Predictions from the Three Factor Eating Questionnaire (TFEQ) Appetite. 2011;56:316–323. doi: 10.1016/j.appet.2011.01.003.
    1. Chaput J.P., Tremblay A. Acute effects of knowledge-based work on feeding behavior and energy intake. Physiol. Behav. 2007;90:66–72. doi: 10.1016/j.physbeh.2006.08.030.
    1. de Lauzon B., Romon M., Deschamps V., Lafay L., Borys J.M., Karlsson J., Ducimetiere P., Charles M.A., Fleurbaix Laventie Ville Sante Study Group The Three-Factor Eating Questionnaire-R18 is able to distinguish among different eating patterns in a general population. J. Nutr. 2004;134:2372–2380. doi: 10.1093/jn/134.9.2372.
    1. Lindroos A.K., Lissner L., Mathiassen M.E., Karlsson J., Sullivan M., Bengtsson C., Sjostrom L. Dietary intake in relation to restrained eating, disinhibition, and hunger in obese and nonobese Swedish women. Obes. Res. 1997;5:175–182. doi: 10.1002/j.1550-8528.1997.tb00290.x.
    1. Ouwens M.A., van Strien T., van der Staak C.P. Tendency toward overeating and restraint as predictors of food consumption. Appetite. 2003;40:291–298. doi: 10.1016/S0195-6663(03)00006-0.
    1. Keranen A.M., Strengell K., Savolainen M.J., Laitinen J.H. Effect of weight loss intervention on the association between eating behaviour measured by TFEQ-18 and dietary intake in adults. Appetite. 2011;56:156–162. doi: 10.1016/j.appet.2010.10.004.
    1. Zambrowicz R., Schebendach J., Sysko R., Mayer L.E.S., Walsh B.T., Steinglass J.E. Relationship between three factor eating questionnaire-restraint subscale and food intake. Int. J. Eat. Disord. 2019;52:255–260. doi: 10.1002/eat.23014.
    1. Singh A., Bains K., Kaur H. Relationship of Eating Behaviors with Age, Anthropometric Measurements, and Body Composition Parameters among Professional Indian Women. Ecol. Food Nutr. 2017;56:411–423. doi: 10.1080/03670244.2017.1366317.
    1. Polivy J., Herman C.P. Restrained Eating and Food Cues: Recent Findings and Conclusions. Curr. Obes. Rep. 2017;6:79–85. doi: 10.1007/s13679-017-0243-1.
    1. James B.L., Loken E., Roe L.S., Rolls B.J. The Weight-Related Eating Questionnaire offers a concise alternative to the Three-Factor Eating Questionnaire for measuring eating behaviors related to weight loss. Appetite. 2017;116:108–114. doi: 10.1016/j.appet.2017.04.023.
    1. Bas M., Donmez S. Self-efficacy and restrained eating in relation to weight loss among overweight men and women in Turkey. Appetite. 2009;52:209–216. doi: 10.1016/j.appet.2008.09.017.
    1. Batra P., Das S.K., Salinardi T., Robinson L., Saltzman E., Scott T., Pittas A.G., Roberts S.B. Eating behaviors as predictors of weight loss in a 6 month weight loss intervention. Obesity. 2013;21:2256–2263. doi: 10.1002/oby.20404.
    1. Provencher V., Drapeau V., Tremblay A., Despres J.P., Lemieux S. Eating behaviors and indexes of body composition in men and women from the Quebec family study. Obes. Res. 2003;11:783–792. doi: 10.1038/oby.2003.109.
    1. Kilkus J.M., Booth J.N., Bromley L.E., Darukhanavala A.P., Imperial J.G., Penev P.D. Sleep and eating behavior in adults at risk for type 2 diabetes. Obesity. 2012;20:112–117. doi: 10.1038/oby.2011.319.
    1. Perez-Fuentes M.D.C., Molero Jurado M.D.M., Barragan Martin A.B., Martos Martinez A., Gazquez Linares J.J. Association with the Quality of Sleep and the Mediating Role of Eating on Self-Esteem in Healthcare Personnel. Nutrients. 2019;11:321. doi: 10.3390/nu11020321.
    1. Goel N., Kim H., Lao R.P. Gender differences in polysomnographic sleep in young healthy sleepers. Chronobiol. Int. 2005;22:905–915. doi: 10.1080/07420520500263235.
    1. van den Berg J.F., Miedema H.M., Tulen J.H., Hofman A., Neven A.K., Tiemeier H. Sex differences in subjective and actigraphic sleep measures: A population-based study of elderly persons. Sleep. 2009;32:1367–1375. doi: 10.1093/sleep/32.10.1367.
    1. Whinnery J., Jackson N., Rattanaumpawan P., Grandner M.A. Short and long sleep duration associated with race/ethnicity, sociodemographics, and socioeconomic position. Sleep. 2014;37:601–611. doi: 10.5665/sleep.3508.
    1. St-Onge M.P., O’Keeffe M., Roberts A.L., RoyChoudhury A., Laferrere B. Short sleep duration, glucose dysregulation and hormonal regulation of appetite in men and women. Sleep. 2012;35:1503–1510. doi: 10.5665/sleep.2198.
    1. Spaeth A.M., Dinges D.F., Goel N. Phenotypic vulnerability of energy balance responses to sleep loss in healthy adults. Sci. Rep. 2015;5:14920. doi: 10.1038/srep14920.
    1. Netzer N.C., Stoohs R.A., Netzer C.M., Clark K., Strohl K.P. Using the Berlin Questionnaire to identify patients at risk for the sleep apnea syndrome. Ann. Intern. Med. 1999;131:485–491. doi: 10.7326/0003-4819-131-7-199910050-00002.
    1. Buysse D.J., Reynolds C.F., 3rd, Monk T.H., Berman S.R., Kupfer D.J. The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Res. 1989;28:193–213. doi: 10.1016/0165-1781(89)90047-4.
    1. Horne J.A., Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 1976;4:97–110.
    1. Fatima Y., Doi S.A., Mamun A.A. Sleep quality and obesity in young subjects: A meta-analysis. Obes. Rev. 2016;17:1154–1166. doi: 10.1111/obr.12444.
    1. Zhou Q., Zhang M., Hu D. Dose-response association between sleep duration and obesity risk: A systematic review and meta-analysis of prospective cohort studies. Sleep Breath. 2019;23:1035–1045. doi: 10.1007/s11325-019-01824-4.
    1. Gazquez Linares J.J., Perez-Fuentes M.D.C., Molero Jurado M.M.D., Oropesa Ruiz N.F., Simon Marquez M.D.M., Saracostti M. Sleep Quality and the Mediating Role of Stress Management on Eating by Nursing Personnel. Nutrients. 2019;11:1731. doi: 10.3390/nu11081731.
    1. Zhu B., Chen X., Park C.G., Zhu D., Izci-Balserak B. Fatigue and Sleep Quality Predict Eating Behavior Among People with Type 2 Diabetes. Nurs. Res. 2020;69:419–426. doi: 10.1097/NNR.0000000000000447.
    1. Bathalon G.P., Tucker K.L., Hays N.P., Vinken A.G., Greenberg A.S., McCrory M.A., Roberts S.B. Psychological measures of eating behavior and the accuracy of 3 common dietary assessment methods in healthy postmenopausal women. Am. J. Clin. Nutr. 2000;71:739–745. doi: 10.1093/ajcn/71.3.739.
    1. Chen E.Y., Zeffiro T.A. Hunger and BMI modulate neural responses to sweet stimuli: fMRI meta-analysis. Int. J. Obes. 2020;44:1636–1652. doi: 10.1038/s41366-020-0608-5.
    1. Frank S., Laharnar N., Kullmann S., Veit R., Canova C., Hegner Y.L., Fritsche A., Preissl H. Processing of food pictures: Influence of hunger, gender and calorie content. Brain Res. 2010;1350:159–166. doi: 10.1016/j.brainres.2010.04.030.
    1. Siep N., Roefs A., Roebroeck A., Havermans R., Bonte M.L., Jansen A. Hunger is the best spice: An fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex. Behav. Brain Res. 2009;198:149–158. doi: 10.1016/j.bbr.2008.10.035.
    1. Chaput J.P., Despres J.P., Bouchard C., Tremblay A. The association between short sleep duration and weight gain is dependent on disinhibited eating behavior in adults. Sleep. 2011;34:1291–1297. doi: 10.5665/SLEEP.1264.
    1. Filiatrault M.L., Chaput J.P., Drapeau V., Tremblay A. Eating behavior traits and sleep as determinants of weight loss in overweight and obese adults. Nutr. Diabetes. 2014;4:e140. doi: 10.1038/nutd.2014.37.
    1. de Castro J.M. The relationship of cognitive restraint to the spontaneous food and fluid intake of free-living humans. Physiol. Behav. 1995;57:287–295. doi: 10.1016/0031-9384(94)00229-X.
    1. Rideout C.A., McLean J.A., Barr S.I. Women with high scores for cognitive dietary restraint choose foods lower in fat and energy. J. Am. Diet. Assoc. 2004;104:1154–1157. doi: 10.1016/j.jada.2004.04.024.
    1. van Strien T., Engels R.C., van Staveren W., Herman C.P. The validity of dietary restraint scales: Comment on Stice et al. (2004) Psychol. Assess. 2006;18:89–94; discussion 95–99. doi: 10.1037/1040-3590.18.1.89.
    1. Greenwood J., Broadbent J., Fuller-Tyszkiewicz M. Restrained eaters consume more food only if they are impulsive and male. Eat. Behav. 2014;15:582–585. doi: 10.1016/j.eatbeh.2014.08.017.
    1. Jansen A., Nederkoorn C., van Baak L., Keirse C., Guerrieri R., Havermans R. High-restrained eaters only overeat when they are also impulsive. Behav. Res. Ther. 2009;47:105–110. doi: 10.1016/j.brat.2008.10.016.
    1. Giudici K.V., Baudry J., Mejean C., Lairon D., Benard M., Hercberg S., Bellisle F., Kesse-Guyot E., Peneau S. Cognitive Restraint and History of Dieting Are Negatively Associated with Organic Food Consumption in a Large Population-Based Sample of Organic Food Consumers. Nutrients. 2019;11:2468. doi: 10.3390/nu11102468.
    1. Martin C.K., Williamson D.A., Geiselman P.J., Walden H., Smeets M., Morales S., Redmann S., Jr. Consistency of food intake over four eating sessions in the laboratory. Eat. Behav. 2005;6:365–372. doi: 10.1016/j.eatbeh.2005.03.002.
    1. Burger K.S., Stice E. Relation of dietary restraint scores to activation of reward-related brain regions in response to food intake, anticipated intake, and food pictures. NeuroImage. 2011;55:233–239. doi: 10.1016/j.neuroimage.2010.12.009.
    1. Coletta M., Platek S., Mohamed F.B., van Steenburgh J.J., Green D., Lowe M.R. Brain activation in restrained and unrestrained eaters: An fMRI study. J. Abnorm. Psychol. 2009;118:598–609. doi: 10.1037/a0016201.
    1. McNeil J., St-Onge M.P. Increased energy intake following sleep restriction in men and women: A one-size-fits-all conclusion? Obesity. 2017;25:989–992. doi: 10.1002/oby.21831.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi