Abstract
Background
Studies have reported that impulsivity predicts childhood BMI and that the association is mediated by eating behaviors. One aspect of impulsivity—potentially crucial in the obesity context—is reward responsiveness, which may predispose to responsiveness to palatable food cues. The behavioral susceptibility theory hypothesizes that genetic susceptibility to obesity operates partly via genetically determined differences in appetite regulation. Reward responsiveness may therefore be one of the neuro-endophenotypes that mediates genetic susceptibility to obesity.
Objective
To test whether reward responsiveness, eating behaviors, and child BMI share common genetic architecture.
Methods
We examined reward responsiveness, eating behaviors, and BMI in 5-year-old children from Gemini, a UK birth cohort of 2402 twin pairs born in 2007. All measures were collected by parent report. Reward responsiveness was derived from the Behavioral Approach System. Compulsion to eat and eating for pleasure was measured with the “food responsiveness” scale of the Child Eating Behavior Questionnaire. Wanting to eat in response to environmental food cues was measured with the “external eating” scale of the Dutch Eating Behavior Questionnaire. Maximum-likelihood structural equation modeling was used to establish underlying common genetic and environmental influences.
Results
There were significant positive phenotypic correlations between all traits except for reward responsiveness and BMI. Genetic factors explained the majority of the association between food responsiveness and external eating (74%, 95% CI: 61, 87), whereas common shared environmental factors explained the majority of the associations between reward responsiveness with both food responsiveness (55%, 95% CI: 20, 90) and external eating (70%, 95% CI: 39, 100).
Conclusions
Our study demonstrates the importance of common environmental factors in the shared etiology between reward responsiveness and childhood eating behaviors. However, the common etiology underlying both reward responsiveness and BMI is unclear, as there was no phenotypic correlation between reward responsiveness and BMI at this age. Further longitudinal research needs to detangle this complex relationship throughout development.
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References
Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9·1 million participants. Lancet. 2011;377:557–67. http://www.ncbi.nlm.nih.gov/pubmed/21295846.
Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA. 2014;311:806. http://www.ncbi.nlm.nih.gov/pubmed/24570244.
Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK, et al. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA. 2016;315:2292. http://www.ncbi.nlm.nih.gov/pubmed/27272581.
Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML, et al. The global obesity pandemic: shaped by global drivers and local environments. Lancet. 2011;378:804–14. http://www.ncbi.nlm.nih.gov/pubmed/21872749.
Young LR, Nestle M. The contribution of expanding portion sizes to the US obesity epidemic. Am J Public Health. 2002;92:246–9. http://www.ncbi.nlm.nih.gov/pubmed/11818300.
Rodgers A, Woodward A, Swinburn B, Dietz WH. Prevalence trends tell us what did not precipitate the US obesity epidemic. Lancet Public Heal. 2018;3:e162–3. https://linkinghub.elsevier.com/retrieve/pii/S2468266718300215.
Elks CE, den Hoed M, Zhao JH, Sharp SJ, Wareham NJ, Loos RJF, et al. Variability in the heritability of body mass index: a systematic review and meta-regression. Front Endocrinol. 2012;3. http://journal.frontiersin.org/article/10.3389/fendo.2012.00029/abstract.
Yengo L, Sidorenko J, Kemper KE, Zheng Z, Wood AR, Weedon MN, et al. Meta-analysis of genome-wide association studies for height and body mass index in ∼700000 individuals of European ancestry. Hum Mol Genet. 2018;27:3641–9. https://academic.oup.com/hmg/article/27/20/3641/5067845.
Llewellyn C, Wardle J. Behavioral susceptibility to obesity: gene-environment interplay in the development of weight. Physiol Behav. 2015;152:494–501. http://www.ncbi.nlm.nih.gov/pubmed/26166156.
Llewellyn CH, Trzaskowski M, van Jaarsveld CHM, Plomin R, Wardle J. Satiety mechanisms in genetic risk of obesity. JAMA Pediatr. 2014;168:338. http://archpedi.jamanetwork.com/article.aspx?doi=10.1001/jamapediatrics.2013.4944.
Cornelis MC, Rimm EB, Curhan GC, Kraft P, Hunter DJ, Hu FB, et al. Obesity susceptibility loci and uncontrolled eating, emotional eating and cognitive restraint behaviors in men and women. Obesity. 2014;22:E135–41. http://doi.wiley.com/10.1002/oby.20592.
Konttinen H, Llewellyn C, Wardle J, Silventoinen K, Joensuu A, Mannisto S, et al. Appetitive traits as behavioural pathways in genetic susceptibility to obesity: a population-based cross-sectional study. Sci Rep. 2015;5:14726.
Llewellyn CH, Fildes A. Behavioural susceptibility theory: Professor Jane Wardle and the role of appetite in genetic risk of obesity. Curr Obes Rep. 2017;6:38–45. http://www.ncbi.nlm.nih.gov/pubmed/28236287.
de Lauzon-Guillain B, Clifton EA, Day FR, Clément K, Brage S, Forouhi NG, et al. Mediation and modification of genetic susceptibility to obesity by eating behaviors. Am J Clin Nutr. 2017;106:996–1004. https://academic.oup.com/ajcn/article/106/4/996-1004/4652047.
Llewellyn CH, van Jaarsveld CH, Johnson L, Carnell S, Wardle J. Nature and nurture in infant appetite: analysis of the Gemini twin birth cohort. Am J Clin Nutr. 2010;91:1172–9. http://www.ncbi.nlm.nih.gov/pubmed/20335548.
Carnell S, Haworth CMA, Plomin R, Wardle J. Genetic influence on appetite in children. Int J Obes. 2008;32:1468–73. http://www.nature.com/articles/ijo2008127.
Dubois L, Diasparra M, Bédard B, Kaprio J, Fontaine-Bisson B, Tremblay R. et al. Genetic and environmental influences on eating behaviors in 2.5- and 9-year-old children: a longitudinal twin study. Int J Behav Nutr Phys Act. 2013;10:134. http://ijbnpa.biomedcentral.com/articles/10.1186/1479-5868-10-134.
Tholin S, Rasmussen F, Tynelius P, Karlsson J. Genetic and environmental influences on eating behavior: the Swedish Young Male Twins Study. Am J Clin Nutr. 2005;81:564–9. https://academic.oup.com/ajcn/article/81/3/564/4648900.
Sung J, Lee K, Song Y-M, Lee MK, Lee D-H. Heritability of eating behavior assessed using the DEBQ (Dutch Eating Behavior Questionnaire) and weight-related traits: the Healthy Twin Study. Obesity. 2010;18:1000–5. http://doi.wiley.com/10.1038/oby.2009.389.
Keskitalo K, Tuorila H, Spector TD, Cherkas LF, Knaapila A, Kaprio J, et al. The Three-Factor Eating Questionnaire, body mass index, and responses to sweet and salty fatty foods: a twin study of genetic and environmental associations. Am J Clin Nutr. 2008;88:263–71. https://academic.oup.com/ajcn/article/88/2/263/4649876.
van Jaarsveld CHM, Boniface D, Llewellyn CH, Wardle J. Appetite and growth. JAMA Pediatr. 2014;168:345. http://archpedi.jamanetwork.com/article.aspx?doi=10.1001/jamapediatrics.2013.4951.
van Jaarsveld CH, Llewellyn CH, Johnson L, Wardle J. Prospective associations between appetitive traits and weight gain in infancy. Am J Clin Nutr. 2011;94:1562–7. http://www.ncbi.nlm.nih.gov/pubmed/22071702.
Quah PL, Chan YH, Aris IM, Pang WW, Toh JY, Tint MT, et al. Prospective associations of appetitive traits at 3 and 12 months of age with body mass index and weight gain in the first 2 years of life. BMC Pediatr. 2015;15:153. http://bmcpediatr.biomedcentral.com/articles/10.1186/s12887-015-0467-8.
Emery RL, Levine MD. Questionnaire and behavioral task measures of impulsivity are differentially associated with body mass index: A comprehensive meta-analysis. Psychol Bull. 2017;143:868–902. http://www.ncbi.nlm.nih.gov/pubmed/28493725.
Evenden JL. Varieties of impulsivity. Psychopharmacology. 1999;146:348–61. http://www.ncbi.nlm.nih.gov/pubmed/10550486.
Leshem R, Yefet M. Does impulsivity converge distinctively with inhibitory control? Disentangling the cold and hot aspects of inhibitory control. Pers Individ Dif. 2019;145:44–51. https://www.sciencedirect.com/science/article/abs/pii/S0191886919301527.
van den Berg L, Pieterse K, Malik JA, Luman M, Willems van Dijk K, Oosterlaan J, et al. Association between impulsivity, reward responsiveness and body mass index in children. Int J Obes. 2011;35:1301–7. http://www.ncbi.nlm.nih.gov/pubmed/21694699.
Epstein LH, Dearing KK, Temple JL, Cavanaugh MD. Food reinforcement and impulsivity in overweight children and their parents. Eat Behav. 2008;9:319–27. http://www.ncbi.nlm.nih.gov/pubmed/18549991.
Steinsbekk S, Belsky J, Wichstrøm L. Parental Feeding and child eating: an investigation of reciprocal effects. Child Dev. 2016;87:1538–49. https://www.ncbi.nlm.nih.gov/pubmed/?term=Parental+Feeding+and+Child+Eating%3A+An+Investigation+of+Reciprocal+Effects.
Anokhin AP, Grant JD, Mulligan RC, Heath AC. The genetics of impulsivity: evidence for the heritability of delay discounting. Biol Psychiatry. 2015;77:887–94. http://www.ncbi.nlm.nih.gov/pubmed/25555481.
Niv S, Tuvblad C, Raine A, Wang P, Baker LA. Heritability and longitudinal stability of impulsivity in adolescence. Behav Genet. 2012;42:378–92. http://link.springer.com/10.1007/s10519-011-9518-6.
Isen JD, Sparks JC, Iacono WG. Predictive validity of delay discounting behavior in adolescence: a longitudinal twin study. Exp Clin Psychopharmacol. 2014;22:434–43. http://www.ncbi.nlm.nih.gov/pubmed/24999868.
van Jaarsveld CHM, Johnson L, Llewellyn C, Wardle J. Gemini: A UK Twin Birth Cohort with a focus on early childhood weight trajectories, appetite and the family environment. Twin Res Hum Genet. 2010;13:72–8. http://www.ncbi.nlm.nih.gov/pubmed/20158309.
Dunn TJ, Baguley T, Brunsden V. From alpha to omega: a practical solution to the pervasive problem of internal consistency estimation. Br J Psychol. 2014;105:399–412. http://www.ncbi.nlm.nih.gov/pubmed/24844115.
Colder CR, O’Connor RM. Gray’s reinforcement sensitivity model and child psychopathology: laboratory and questionnaire assessment of the BAS and BIS. J Abnorm Child Psychol. 2004;32:435–51.
Wardle J, Guthrie CA, Sanderson S, Rapoport L. Development of the Children’s Eating Behaviour Questionnaire. J Child Psychol Psychiatry Allied Discipl. 2001;47:963–70. https://www.ncbi.nlm.nih.gov/pubmed/11693591.
Braet C, Van Strien T. Assessment of emotional, externally induced and restrained eating behaviour in nine to twelve-year-old obese and non-obese children. Behav Res Ther. 1997;35:863–73. http://www.ncbi.nlm.nih.gov/pubmed/9299807.
van Strien T, Oosterveld P. The children’s DEBQ for assessment of restrained, emotional, and external eating in 7- to 12-year-old children. Int J Eat Disord. 2008;41:72–81. http://doi.wiley.com/10.1002/eat.20424.
Cole TJ. Growth monitoring with the British 1990 growth reference. Arch Dis Child. 1997;76:47–9. http://www.ncbi.nlm.nih.gov/pubmed/9059161.
Pan H, Cole T. LMSGrowth Excel add in version 2.77. 2012. https://www.healthforallchildren.com/lmsgrowth-terms-of-copyright/.
Goldsmith HH. A zygosity questionnaire for young twins: a research note. Behav Genet. 2011;21:257–69.
Herle M, Fildes A, van Jaarsveld C, Rijsdijk F, Llewellyn CH. Parental reports of infant and child eating behaviors are not affected by their beliefs about their twins’ zygosity. Behav Genet. 2016;46:763–71. http://www.ncbi.nlm.nih.gov/pubmed/27406596.
Boker S, Neale M, Maes H, Wilde M, Spiegel M, Brick T, et al. OpenMx: an open source extended structural equation modeling framework. Psychometrika. 2011;76:306–17.
Posada D, Buckley TR. Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol. 2004;53:793–808. https://academic.oup.com/sysbio/article/53/5/793/2842928.
Rodenburg G, Kremers SP, Oenema A, van de Mheen D. Associations of parental feeding styles with child snacking behaviour and weight in the context of general parenting. Public Health Nutr. 2014;17:960–9. http://www.ncbi.nlm.nih.gov/pubmed/23527513.
Selzam S, McAdams TA, Coleman JRI, Carnell S, O’Reilly PF, Plomin R, et al. Evidence for gene-environment correlation in child feeding: links between common genetic variation for BMI in children and parental feeding practices. PLoS Genet. 2018;14:e1007757. http://dx.plos.org/10.1371/journal.pgen.1007757.
Giel KE, Teufel M, Junne F, Zipfel S, Schag K. Food-related impulsivity in obesity and binge eating disorder—a systematic update of the evidence. Nutrients. 2017;9. http://www.ncbi.nlm.nih.gov/pubmed/29077027.
Zheng H, Berthoud H-R. Neural systems controlling the drive to eat: mind versus metabolism. Physiology. 2008;23:75–83. http://www.ncbi.nlm.nih.gov/pubmed/18400690.
Spence JC, Carson V, Casey L, Boule N. Examining behavioural susceptibility to obesity among Canadian pre-school children: the role of eating behaviours. Int J Pediatr Obes. 2011;6:e501–7. http://informahealthcare.com/doi/abs/10.3109/17477166.2010.512087.
Sleddens EF, Kremers SP, Thijs C. The children’s eating behaviour questionnaire: factorial validity and association with Body Mass Index in Dutch children aged 6-7. Int J Behav Nutr Phys Act. 2008;5:49. http://ijbnpa.biomedcentral.com/articles/10.1186/1479-5868-5-49.
Webber L, Hill C, Saxton J, Van Jaarsveld CHM, Wardle J. Eating behaviour and weight in children. Int J Obes. 2009;33:21–8. http://www.ncbi.nlm.nih.gov/pubmed/19002146.
Bezdjian S, Baker LA, Tuvblad C. Genetic and environmental influences on impulsivity: a meta-analysis of twin, family and adoption studies. Clin Psychol Rev. 2011;31:1209–23. http://www.ncbi.nlm.nih.gov/pubmed/21889436.
Carnell S, Haworth CMA, Plomin R, Wardle J. Genetic influence on appetite in children. Int J Obes. 2008;32:1468–73. http://www.ncbi.nlm.nih.gov/pubmed/18679413.
Silventoinen K, Jelenkovic A, Sund R, Hur Y-M, Yokoyama Y, Honda C, et al. Genetic and environmental effects on body mass index from infancy to the onset of adulthood: an individual-based pooled analysis of 45 twin cohorts participating in the COllaborative project of Development of Anthropometrical measures in Twins (CODATwins) study. Am J Clin Nutr. 2016;104:371–9. http://www.ncbi.nlm.nih.gov/pubmed/27413137.
Min J, Chiu DT, Wang Y. Variation in the heritability of body mass index based on diverse twin studies: a systematic review. Obes Rev. 2013;14:871–82. http://doi.wiley.com/10.1111/obr.12065.
Collins CE, Watson J, Burrows T. Measuring dietary intake in children and adolescents in the context of overweight and obesity. Int J Obes. 2010;34:1103–15. http://www.ncbi.nlm.nih.gov/pubmed/19935750.
Magarey A, Watson J, Golley RK, Burrows T, Sutherland R, McNaughton SA, et al. Assessing dietary intake in children and adolescents: considerations and recommendations for obesity research. Int J Pediatr Obes. 2011;6:2–11. http://informahealthcare.com/doi/abs/10.3109/17477161003728469.
De BI, Van OP. Personal and family determinants of dietary behaviour in adolescents and their parents. Psychol Health. 2000;15:751–70. http://www.tandfonline.com/doi/abs/10.1080/08870440008405579.
Fisher JO, Birch LL. Restricting access to foods and children’s eating. Appetite. 1999;32:405–19. https://linkinghub.elsevier.com/retrieve/pii/S0195666399902313.
Sharma L, Markon KE, Clark LA. Toward a theory of distinct types of “impulsive” behaviors: a meta-analysis of self-report and behavioral measures. Psychol Bull. 2014;140:374–408. http://www.ncbi.nlm.nih.gov/pubmed/24099400.
Felson J. What can we learn from twin studies? A comprehensive evaluation of the equal environments assumption. Soc Sci Res. 2014;43:184–99. https://linkinghub.elsevier.com/retrieve/pii/S0049089X13001397.
Acknowledgements
We thank the Gemini families for participating in the study.
Funding
The Gemini 5-year data collection was supported by a Cancer Research UK program grant (C1418/A7974), awarded to Prof. Jane Wardle, who died in 2015. CL was employed on the grant during the time of the study. Gemini is currently funded by an MQ Fellows award to CL (MQ17-4 Llewellyn). CK and JT are part funded by the NIHR Mental Health Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London. CK is an NIHR clinical lecturer and has also previously received salary support from Novo Nordisk UK Research Foundation and Marie Curie Fellowship. MH is supported by a skills development fellowship from the Medical Research Council UK (MR/T027843/1). The views expressed are those of the authors and not necessarily those of the Wellcome Trust, the NHS, the NIHR, CRUK, MQ, MRC, or the Department of Health. The funders did not have a role in the study design, data collection/analysis/interpretation, or preparation of this manuscript.
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CK, MH, FR, JT, and CL designed the research; CK, MH, and FR performed the statistical analyses; and all authors wrote and revised the manuscript for important intellectual content. All authors read and approved the final manuscript.
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Kan, C., Herle, M., Treasure, J. et al. Common etiological architecture underlying reward responsiveness, externally driven eating behaviors, and BMI in childhood: findings from the Gemini twin cohort. Int J Obes 44, 2064–2074 (2020). https://doi.org/10.1038/s41366-020-0605-8
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DOI: https://doi.org/10.1038/s41366-020-0605-8
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