REVIEW URRENT C OPINION
Disordered eating in obese individuals Marsha D. Marcus and Jennifer E. Wildes
Purpose of review This article provides an overview of current thinking about the association between disordered eating and obesity, emphasizing binge eating, binge eating disorder and food addiction as useful conceptual models. Recent findings Binge eating, recurrent and persistent episodes of overeating coupled with a lack of control over eating, and binge eating disorder, the Diagnostic and Statistical Manual-5 mental disorder, have been a major focus of work to clarify the relationship between disordered eating and obesity. A second focus has been the addiction model of aberrant eating, which posits that recurrent overeating of palatable food is similar to addictive behavior and characterized by dysregulation of the dopaminergic reward system. We describe efforts to integrate these models by focusing on binge eating phenotypes as the subgroup of obese individuals characterized by disordered eating. Examples of empirical work based on these models are provided, as well as selected studies that reflect the burgeoning literature focusing on addictive and feeding behaviors across multiple domains and levels of analysis. Summary Research evidence to explain similarities and differences across levels of BMI and varying aspects of feeding behavior may promote the identification of novel interventions that address weight and eating problems. Keywords binge eating disorder, binge eating, food addiction, obesity
INTRODUCTION The prevalence of obesity has increased dramatically over the last several decades with corresponding increases in obesity-related morbidities and associated health costs. Unsurprisingly, scientific investigation to explicate the causes of obesity has proliferated, with parallel increases in public discourse. Obesity or excess adiposity, commonly defined as a BMI greater than or equal to 30 [calculated as weight (kg)/height (m)2] is a heterogeneous condition that is caused by a complex interplay of host and environmental factors. Although there are many pathways to obesity, there is substantial evidence that disordered eating can be a significant factor in its development and maintenance. Indeed, the Diagnostic and Statistical Manual-5 (DSM-5) Eating Disorders Work Group was asked to consider whether obesity should be included in the DSM as a mental disorder. Ultimately, the group concluded that there was insufficient evidence to include obesity [1], but research to elucidate the relationship between disordered eating and obesity has been ongoing. In this manuscript, we will discuss two prominent models that have been focal points of ongoing investigations: first, binge eating and binge
eating disorder (BED) and second, ‘food addiction.’ Next, current efforts to integrate data regarding binge eating and food addiction, and to incorporate information from the rapidly expanding literature on the neurobiology of feeding behavior, addiction, and obesity will be discussed. Finally, we close with suggestions for future research and implications for the treatment of obesity and disordered eating.
BINGE EATING AND BINGE EATING DISORDER Binge eating is defined as the episodic intake of a large amount of food in association with a sense of loss of control (LOC) over eating during the episode. There are two required elements to a binge eating episode, namely, eating a larger amount of food than most other individuals would eat in a similar Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA Correspondence to Marsha D. Marcus, PhD, Professor of Psychiatry and Psychology, Western Psychiatric Institute and Clinic, 3811 O’Hara Street, Pittsburgh, PA 15213, USA. Tel: +1 412 246 6371; e-mail: [email protected] Curr Opin Psychiatry 2014, 27:443–447 DOI:10.1097/YCO.0000000000000103
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Eating disorders
KEY POINTS
&
There is substantial evidence that recurrent binge eating and BED are associated with psychiatric comorbidity and obesity. The relation between food addiction, or vulnerability to overeating highly palatable foods due to dysregulation in the neurocircuits associated with reward, and obesity is supported by research using animal models, but there have been mixed findings from human research. Studies that integrate the binge eating and food addiction models, as well as ongoing work to elucidate mechanisms associated with addiction and obesity, ultimately may lead to novel interventions.
situation and feeling a sense of lack of control during the episode. There has been ongoing discussion in the literature about the respective roles that the amount of food ingested during an episode (i.e., unusually large) and the sense of LOC have in explaining the clinical significance of binge eating [2]. There is considerable variability in the size of binge eating episodes, and many individuals report eating episodes characterized by LOC that do not involve an unusually large amount of food. These are referred to as ‘subjective’ binge episodes or LOC eating. Increasing evidence suggests that LOC is the hallmark of binge eating as neither size nor frequency of episodes are associated with impairment or psychiatric comorbidity [3 ]. In any event, prospective longitudinal studies of subjective binge eating (or LOC) and objective binge eating have documented that LOC in children predicts adiposity and psychiatric symptomatology [4], and objective binge eating in adolescents and young adults predicts incident depressive symptoms and obesity [5 ]. Thus, eating episodes characterized by LOC whether or not the food intake is objectively large have been linked to psychiatric morbidity and excess adiposity. BED is a psychiatric syndrome characterized by recurrent and persistent binge eating with marked distress and associated correlates, such as rapid eating, eating until uncomfortably full, eating when not hungry, eating alone because of embarrassment, and feeling disgusted, depressed or guilty after binge eating episodes. BED was included in an appendix of the DSM of Mental Disorders, 4th edition [6] as criteria set provided for further study. This led to a proliferation of investigation documenting the clinical utility of BED, its distinctiveness from other disorders including bulimia nervosa and obesity, and clear implications for treatment [7 ]. &
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Consequently, BED has been included in DSM-5 [8] as a new feeding and eating disorder [9 ,10]. Although BED occurs in healthy-weight individuals, it is strongly associated with obesity. Indeed, much of the research documenting the substantial clinical morbidity associated with BED has focused on obese individuals. Consequently, most work investigating the relation between eating disorders and obesity has centered on BED. Recent work, however, suggests that bulimia nervosa, which also is characterized by recurrent binge eating that is paired with regular compensatory behaviors (e.g., self-induced vomiting) to mitigate the effects of binge episodes, may be associated with adiposity. In a recent population-based study of more than 24 000 men and women in 14 countries, the prevalence and correlates of BED were examined using bulimia nervosa as a comparator [11 ]. The results of this investigation documented the significance of BED and bulimia nervosa as mental health problems with substantial psychiatric comorbidity and role impairment. Interestingly, individuals with bulimia nervosa and BED both had higher BMIs than those without a history of eating disorders, a finding that has been documented in some, but not most previous studies. Specifically, 32.8% of individuals with bulimia nervosa and 41.7% of individuals with BED were obese. Further, there were no significant differences between bulimia nervosa and BED in proportions of underweight, healthy-weight, overweight or obese individuals. These data suggest the importance of including individuals with binge eating irrespective of DSM-5 diagnosis in future research examining the relationship between disordered eating and obesity. &&
THE ADDICTION MODEL OF ABERRANT EATING The addiction model of obesity is based on observations that substance use disorders and continual overeating of palatable foods share common behavioral manifestations, including escalation of use over time, LOC, ongoing misuse despite negative consequences and significant distress. The behavioral similarities between addictive and overeating behaviors have face validity, and the concept of food addiction quickly gained traction in the scientific literature and lay press. Importantly, behavioral observations have been stimulated and bolstered by a significant body of animal research documenting that repeated consumption of palatable foods results in behavioral and neurochemical changes similar to those seen in chronic drug use. Further, scientists have studied changes in the dopaminergic reward system in response to food in people that are Volume 27 Number 6 November 2014
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Disordered eating in obese individuals Marcus and Wildes
obese to test the notion that powerful reinforcers in the form of palatable food can override homeostatic control of eating in a manner similar to that observed in individuals with addiction. There is evidence that addiction and obesity share neurobiological processes; in particular, impairments in dopaminergic circuitry associated with reward sensitivity and incentive motivation [12 ]. Nevertheless, the addiction model of obesity has attracted prominent critics [13 ,14] who have argued that research evidence is limited, findings are inconsistent and reductionist [15] and that the addiction model fails to take into account the remarkable complexity of human obesity. Recent work has been more nuanced, and there have been substantive efforts to refine and narrow the putative food addiction obesity phenotype by focusing on individuals with binge eating and incorporating information from multiple additional domains and levels of analysis. &&
&&
BINGE EATING AS THE OBESITY PHENOTYPE CHARACTERIZED BY FOOD ADDICTION Given mixed findings from studies comparing obese and lean individuals on facets of the addiction model, recognition of the heterogeneity of obesity, and interest in identifying neurobehavioral obesity phenotypes, it is not surprising that recent work has focused on commonalities between binge eating and addiction. First, as detailed by Smith and Robins [16] the pattern of symptoms associated with binge eating and addiction as outlined in the DSM are very similar. There also is recent experimental evidence supporting the notion of binge eating as the obesity phenotype characterized by food addiction. For example, Dalton et al. [17 ] administered a laboratory feeding paradigm to groups of lean and overweight women characterized as ‘binge-type’ and ‘nonbinge-type’ on the basis of scores on a selfreport measure of binge eating. In comparison with nonbinge-types, binge-types ate more palatable food and reported increased wanting for this foods even when satiated. Another group of investigators [18 ] examined reward responding to monetary cues in an functional MRI (fMRI) paradigm among obese individuals with and without BED and lean controls; results documented that in comparison with obese individuals without BED, obese individuals with BED exhibited reduced recruitment of networks involved in reward processing and self-regulation. Finally, recent work [19] suggests that there is variability among individuals with BED in activation of reward processing in frontostriatal circuits, and that individuals who continue binge eating after BED &
&
treatment show less recruitment of reward circuitry than those who do not continue binge eating.
INCORPORATING ADDITIONAL INFORMATION The proliferation of research findings in both the addiction and obesity fields has posed a challenge to the adoption of a simple binge eating/food addiction model in understanding the link between disordered eating and obesity. Conceptualizations of addiction have developed beyond the initial dopamine hypothesis of reward to encompass interacting circuits, including reward, memory, inhibitory control, motivation, interoception and stress reactivity, and the integration of genetic and epigenetic factors [20]. For example, the development of addiction increasingly has been conceptualized as a shift from impulsive to compulsive processes, which involves a change from ventral to dorsal striatal regulation and a transition from prefrontal executive control to striatal habit-related control. These concepts have not yet been examined fully in relation to food addiction [13 ,15], although there are recent studies that document that obese individuals with BED, when compared with control individuals without BED, demonstrate more impulsive responding to nonfood [21] and food cues [21,22 ] as assessed by behavioral laboratory tasks. Similarly, a recent investigation using fMRI to examine neural correlates of response to nonfood cues on a laboratory task among obese individuals with BED and weight matched and lean control individuals showed that individuals with BED were characterized by hypoactivity in brain areas involved with self-regulation and impulse control [23]. Future work is needed to examine whether individuals with BED demonstrate aspects of compulsivity, which would be expected to appear over time in individuals who demonstrate disordered eating. Simultaneously, research expanding the understanding of human feeding behavior also has burgeoned. In addition to reward neurocircuitry, the hypothalamic system, gastrointestinal and adipocyte hormones, inflammatory mediators, and microbiota and gut–brain axis are involved in the regulation of feeding behavior and have been implicated in the causes and maintenance of obesity. For example, previous distinctions between homeostatic eating, which is designed to preserve energy balance, and nonhomeostatic or hedonic eating, which involves food intake in the absence of any energy depletion signals, are no longer clear. As summarized by Volkow et al. [20], it now is apparent that homeostatic and hedonic eating do not occur in isolation, but rather that endocrine hormones
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Eating disorders
implicated in the regulation of homeostatic eating (e.g., insulin, leptin, and ghrelin) also modulate the effects of drugs. Conversely, neurotransmitters involved in drug-seeking (e.g., cannabinoids, serotonin, and glutamate) also affect food intake. The examples of an expanding literature provided above do not do justice to the manifold levels of analysis ranging from genes to psychosocial factors and the current food environment that are the targets of ongoing research on the regulation of feeding behavior and the pathogenesis of disordered eating and obesity. Narrowly focused research on a particular neural circuit or a particular aspect of feeding behavior is necessary, but not sufficient to understand the relation between disordered eating and obesity. For example, because the hypothalamic– pituitary–adrenal axis is involved in human response to stress as well as homeostatic feeding behavior, there is a substantial body of evidence examining the relationship between life stress and obesity. This work suggests that there is a subgroup of stressresponsive obese individuals who have a vulnerability to overeating palatable food and gaining weight over time. Stress also is a risk factor for addiction and relapse to addictive behavior. Thus, both obesity and addiction share multiple overlapping pathways [24 ]. Unsurprisingly, recent epidemiologic and laboratory studies have examined the relation between stress and disordered eating. One investigation studied the relationship between childhood abuse, a form of chronic stress, and food addiction among participants in the Nurses’ Health Study II [25] and documented that women with a history of childhood sexual or physical abuse were 2.5 times more likely to self-report food addiction in adulthood. Approximately two-thirds of food-addicted individuals also were obese, and the authors conclude that uncontrolled eating in response to stress may be one important factor affecting obesity risk in women. Gluck et at. [26] studied obese women with and without BED using a cold pressor stress test to examine changes in ghrelin, a peptide hormone known to increase hunger levels. Results documented increases in ghrelin levels in individuals with and without BED, but no between-group differences. These studies examining the role of stress in disordered eating exemplify the proliferation of salient research, but also the difficulties in evaluating findings from investigations utilizing widely varying methodology at very different levels of analysis. &
THE WAY FORWARD Given the accelerated rate of inquiry related to obesity, disordered eating, and addiction and 446
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evolving understanding of the complex interrelationships among these overlapping, but distinct phenomena, what are the questions that will lead to enhanced understanding and ultimately, to more effective treatments? We offer several suggestions that are not meant to be inclusive, but which grow directly from studies reviewed herein. First, available findings suggest the importance of including a range of binge eating phenotypes in future work (i.e., individuals with bulimia nervosa, BED and those with subjective or LOC episodes). Second, consistent with the current emphasis on incorporating dimensions in psychiatric research, additional studies should include validated dimensional measures of binge eating and traits such as disinhibition and food addiction that are related to obesity, weight gain, and binge eating. Third, it will be important to examine aberrant eating across the full spectrum of BMI to disentangle the relative roles of adiposity and eating behavior traits and phenotypes. Mixed findings in extant research also may result, in part, from the use of varying food cues (sight, smell, or taste of food) and/or neutral, nonfood related cues to elicit task-based responses in experimental individuals; thus, it is desirable to include food and nonfood cues in future research. Finally, longitudinal studies are needed to confirm the relationship between disordered eating and unwanted weight gain. For example, in an fMRI study of 162 male and female adolescents, Stice et al. [27 ] examined neural activation in response to anticipated and actual receipt of palatable food and monetary rewards in a group of healthy-weight adolescents, and evaluated weight changes 1 year after initial assessment. There was evidence that aberrant reward responsivity predicted future substance abuse, but not unhealthy weight gain in this yearlong study. However, binge eating was not assessed, and obese youth were not included. &&
IMPLICATIONS FOR TREATMENT There is a compelling need for additional treatments for obesity and disordered eating, and efforts to identify new treatment targets on the basis of new research findings are underway. For example, on the basis of the findings documenting dysregulation of the dopaminergic reward system in binge eating, an animal study found that deep brain stimulation of the nucleus accumbens shell, which has been implicated in reward-seeking behaviors, reduced binge eating of highly palatable food in a mouse model [28]. Similarly, on the basis of findings that opioid antagonists affect motivational and hedonic processes in the brain, an initial laboratory investigation with human [29] showed that treatment with a Volume 27 Number 6 November 2014
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Disordered eating in obese individuals Marcus and Wildes
novel mu-opioid receptor antagonist reduced brain responses to images of high-calorie foods among obese binge eaters. Although these studies are preliminary, the identification and testing of novel treatments will continue as the science evolves and ultimately, there is the promise of more effective interventions for those that suffer from disordered eating and weight problems.
CONCLUSION Research on the association between disordered eating and obesity is advancing rapidly and multiple lines of inquiry may lead to a fuller understanding of and treatments for disordered eating and obesity. Acknowledgements Dr Marcus acknowledges NIH grant support (DK61254, DK066585, HL096770, MH085921, HD068802, and DK096405). Dr Wildes acknowledges NIH grant support (MH085921). Conflicts of interest The authors report no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Marcus MD, Wildes JE. Obesity: is it a mental disorder? Int J Eat Disord 2009; 42:739–753. 2. Wolfe BE, Baker CW, Smith AT, Kelly-Weeder S. Validity and utility of the current definition of binge eating. Int J Eat Disord 2009; 42:674–686. 3. Vannucci A, Theim KR, Kass AE, et al. What constitutes clinically significant & binge eating? Association between binge features and clinical validators in college-age women. Int J Eat Disord 2013; 46:226–232. This study provides evidence that LOC, rather than the size or frequency of binge eating episodes, is most strongly associated with clinically significant impairments. 4. Kelly NR, Shank LM, Bakalar JL, Tanofsky-Kraff M. Pediatric feeding and eating disorders: current state of diagnosis and treatment. Curr Psychiatry Rep 2014; 16:446. 5. Sonneville KR, Horton NJ, Micali N, et al. Longitudinal associations between && binge eating and overeating and adverse outcomes among adolescents and young adults: does loss of control matter? JAMA Pediatr 2013; 167:149– 155. This is a prospective, longitudinal study of a large cohort of the United States youth that documents that binge eating was associated with incident weight problems and depressive symptoms. 6. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 1994. 7. Tanofsky-Kraff M, Bulik CM, Marcus MD, et al. BED: the next generation of & research. Int J Eat Disord 2013; 46:193–207. This study summarizes recommendations generated by attendees at a meeting sponsored by the National Institute of Mental Health for future research on BED. 8. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Washington, DC: American Psychiatric Association; 2013.
9. Attia E, Becker AE, Bryant-Waugh R, et al. Feeding and eating disorders in & DSM-5. Am J Psychiatry 2013; 170:1237–1239. This commentary provides a succinct overview of changes in feeding and eating disorders from DSM-IV to DSM-5. 10. Call C, Walsh BT, Attia E. From DSM-IV to DSM-5: changes to eating disorder diagnoses. Curr Opin Psychiatry 2013; 26:532–536. 11. Kessler RC, Berglund PA, Chiu WT, et al. The prevalence and correlates of && binge eating disorder in the World Health Organization World Mental Health Surveys. Biol Psychiatry 2013; 73:904–914. This investigation provides data collected from more than 24 000 individuals in 14 countries who participated in the World Health Organization World Mental Health Survey. Findings document the clinical importance of BED, and also confirm a relation between bulimia nervosa and obesity. 12. Volkow ND, Wang GJ, Tomasi D, Baler RD. Obesity and addiction: neuro&& biological overlaps. Obes Rev 2013; 14:2–18. This review article provides an excellent overview of the experimental evidence documenting shared neurobiological features of obesity and addiction. 13. Ziauddeen H, Fletcher PC. Is food addiction a valid and useful concept? Obes && Rev 2013; 14:19–28. This review summarizes the limitations of the food addiction concept and suggests directions for future research. 14. Meule A. Are certain foods addictive? Front Psychiatry 2014; 5:38. 15. Salamone JD, Correa M. Dopamine and food addiction: lexicon badly needed. Biol Psychiatry 2013; 73:e15–e24. 16. Smith DG, Robbins TW. The neurobiological underpinnings of obesity and binge eating: a rationale for adopting the food addiction model. Biol Psychiatry 2013; 73:804–810. 17. Dalton M, Blundell J, Finlayson G. Effect of BMI and binge eating on food & reward and energy intake: further evidence for a binge eating subtype of obesity. Obes Facts 2013; 6:348–359. This study compared overweight or obese individuals with and without trait binge eating on food reward and food intake when fasted and fed. Findings provide support for trait binge eating as a distinct subtype of obesity. 18. Balodis IM, Kober H, Worhunsky PD, et al. Monetary reward processing in & obese individuals with and without binge eating disorder. Biol Psychiatry 2013; 73:877–886. This investigation shows differences between obese individuals with and without BED and lean controls on neural responses to nonfood cues in an fMRI paradigm. 19. Balodis IM, Grilo CM, Kober H, et al. A pilot study linking reduced frontostriatal recruitment during reward processing to persistent bingeing following treatment for binge-eating disorder. Int J Eat Disord 2014; 47:376–384. 20. Volkow ND, Baler RD. Addiction science: uncovering neurobiological complexity. Neuropharmacology 2014; 76 (Pt B):235–249. 21. Svaldi J, Naumann E, Trentowska M, Schmitz F. General and food-specific inhibitory deficits in BED. Int J Eat Disord 2014; 47:534–542. 22. Schag K, Teufel M, Junne F, et al. Impulsivity in BED: food cues elicit increased & reward responses and disinhibition. PLoS One 2013; 8:e76542. This study provides evidence that obese individuals with BED, when compared to non-BED obese individuals and lean controls, show increases in two aspects of impulsivity, reward sensitivity and rash responding to food and nonfood cues, in a laboratory investigation. 23. Balodis IM, Molina ND, Kober H, et al. Divergent neural substrates of inhibitory control in BED relative to other manifestations of obesity. Obesity (Silver Spring) 2013; 21:367–377. 24. Sinha R, Jastreboff AM. Stress as a common risk factor for obesity and & addiction. Biol Psychiatry 2013; 73:827–835. This review article summarizes evidence that stress plays an integral role in the neurobiology of addiction and obesity. 25. Mason SM, Flint AJ, Field AE, et al. Abuse victimization in childhood or adolescence and risk of food addiction in adult women. Obesity (Silver Spring) 2013; 21:E775–E881. 26. Gluck ME, Yahav E, Hashim SA, Geliebter A. Ghrelin levels after a cold pressor stress test in obese women with BED. Psychosom Med 2014; 76:74–79. 27. Stice E, Yokum S, Burger KS. Elevated reward region responsivity predicts && future substance use onset but not overweight/obesity onset. Biol Psychiatry 2013; 73:869–876. This longitudinal investigation provides evidence that aberrant responding in the reward system is prospectively associated with the onset of substance abuse, but not obesity in adolescents, demonstrating the critical importance of extending findings from basic clinical work to free-living situations. 28. Halpern CH, Tekriwal A, Santollo J, et al. Amelioration of binge eating by nucleus accumbens shell deep brain stimulation in mice involves D2 receptor modulation. J Neurosci 2013; 33:7122–7129. 29. Cambridge VC, Ziauddeen H, Nathan PJ, et al. Neural and behavioral effects of a novel mu opioid receptor antagonist in binge-eating obese people. Biol Psychiatry 2013; 73:887–894.
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Disordered eating in obese individuals Marsha D. Marcus and Jennifer E. Wildes
Purpose of review This article provides an overview of current thinking about the association between disordered eating and obesity, emphasizing binge eating, binge eating disorder and food addiction as useful conceptual models. Recent findings Binge eating, recurrent and persistent episodes of overeating coupled with a lack of control over eating, and binge eating disorder, the Diagnostic and Statistical Manual-5 mental disorder, have been a major focus of work to clarify the relationship between disordered eating and obesity. A second focus has been the addiction model of aberrant eating, which posits that recurrent overeating of palatable food is similar to addictive behavior and characterized by dysregulation of the dopaminergic reward system. We describe efforts to integrate these models by focusing on binge eating phenotypes as the subgroup of obese individuals characterized by disordered eating. Examples of empirical work based on these models are provided, as well as selected studies that reflect the burgeoning literature focusing on addictive and feeding behaviors across multiple domains and levels of analysis. Summary Research evidence to explain similarities and differences across levels of BMI and varying aspects of feeding behavior may promote the identification of novel interventions that address weight and eating problems. Keywords binge eating disorder, binge eating, food addiction, obesity
INTRODUCTION The prevalence of obesity has increased dramatically over the last several decades with corresponding increases in obesity-related morbidities and associated health costs. Unsurprisingly, scientific investigation to explicate the causes of obesity has proliferated, with parallel increases in public discourse. Obesity or excess adiposity, commonly defined as a BMI greater than or equal to 30 [calculated as weight (kg)/height (m)2] is a heterogeneous condition that is caused by a complex interplay of host and environmental factors. Although there are many pathways to obesity, there is substantial evidence that disordered eating can be a significant factor in its development and maintenance. Indeed, the Diagnostic and Statistical Manual-5 (DSM-5) Eating Disorders Work Group was asked to consider whether obesity should be included in the DSM as a mental disorder. Ultimately, the group concluded that there was insufficient evidence to include obesity [1], but research to elucidate the relationship between disordered eating and obesity has been ongoing. In this manuscript, we will discuss two prominent models that have been focal points of ongoing investigations: first, binge eating and binge
eating disorder (BED) and second, ‘food addiction.’ Next, current efforts to integrate data regarding binge eating and food addiction, and to incorporate information from the rapidly expanding literature on the neurobiology of feeding behavior, addiction, and obesity will be discussed. Finally, we close with suggestions for future research and implications for the treatment of obesity and disordered eating.
BINGE EATING AND BINGE EATING DISORDER Binge eating is defined as the episodic intake of a large amount of food in association with a sense of loss of control (LOC) over eating during the episode. There are two required elements to a binge eating episode, namely, eating a larger amount of food than most other individuals would eat in a similar Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA Correspondence to Marsha D. Marcus, PhD, Professor of Psychiatry and Psychology, Western Psychiatric Institute and Clinic, 3811 O’Hara Street, Pittsburgh, PA 15213, USA. Tel: +1 412 246 6371; e-mail: [email protected] Curr Opin Psychiatry 2014, 27:443–447 DOI:10.1097/YCO.0000000000000103
0951-7367 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-psychiatry.com
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Eating disorders
KEY POINTS
&
There is substantial evidence that recurrent binge eating and BED are associated with psychiatric comorbidity and obesity. The relation between food addiction, or vulnerability to overeating highly palatable foods due to dysregulation in the neurocircuits associated with reward, and obesity is supported by research using animal models, but there have been mixed findings from human research. Studies that integrate the binge eating and food addiction models, as well as ongoing work to elucidate mechanisms associated with addiction and obesity, ultimately may lead to novel interventions.
situation and feeling a sense of lack of control during the episode. There has been ongoing discussion in the literature about the respective roles that the amount of food ingested during an episode (i.e., unusually large) and the sense of LOC have in explaining the clinical significance of binge eating [2]. There is considerable variability in the size of binge eating episodes, and many individuals report eating episodes characterized by LOC that do not involve an unusually large amount of food. These are referred to as ‘subjective’ binge episodes or LOC eating. Increasing evidence suggests that LOC is the hallmark of binge eating as neither size nor frequency of episodes are associated with impairment or psychiatric comorbidity [3 ]. In any event, prospective longitudinal studies of subjective binge eating (or LOC) and objective binge eating have documented that LOC in children predicts adiposity and psychiatric symptomatology [4], and objective binge eating in adolescents and young adults predicts incident depressive symptoms and obesity [5 ]. Thus, eating episodes characterized by LOC whether or not the food intake is objectively large have been linked to psychiatric morbidity and excess adiposity. BED is a psychiatric syndrome characterized by recurrent and persistent binge eating with marked distress and associated correlates, such as rapid eating, eating until uncomfortably full, eating when not hungry, eating alone because of embarrassment, and feeling disgusted, depressed or guilty after binge eating episodes. BED was included in an appendix of the DSM of Mental Disorders, 4th edition [6] as criteria set provided for further study. This led to a proliferation of investigation documenting the clinical utility of BED, its distinctiveness from other disorders including bulimia nervosa and obesity, and clear implications for treatment [7 ]. &
&&
&
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Consequently, BED has been included in DSM-5 [8] as a new feeding and eating disorder [9 ,10]. Although BED occurs in healthy-weight individuals, it is strongly associated with obesity. Indeed, much of the research documenting the substantial clinical morbidity associated with BED has focused on obese individuals. Consequently, most work investigating the relation between eating disorders and obesity has centered on BED. Recent work, however, suggests that bulimia nervosa, which also is characterized by recurrent binge eating that is paired with regular compensatory behaviors (e.g., self-induced vomiting) to mitigate the effects of binge episodes, may be associated with adiposity. In a recent population-based study of more than 24 000 men and women in 14 countries, the prevalence and correlates of BED were examined using bulimia nervosa as a comparator [11 ]. The results of this investigation documented the significance of BED and bulimia nervosa as mental health problems with substantial psychiatric comorbidity and role impairment. Interestingly, individuals with bulimia nervosa and BED both had higher BMIs than those without a history of eating disorders, a finding that has been documented in some, but not most previous studies. Specifically, 32.8% of individuals with bulimia nervosa and 41.7% of individuals with BED were obese. Further, there were no significant differences between bulimia nervosa and BED in proportions of underweight, healthy-weight, overweight or obese individuals. These data suggest the importance of including individuals with binge eating irrespective of DSM-5 diagnosis in future research examining the relationship between disordered eating and obesity. &&
THE ADDICTION MODEL OF ABERRANT EATING The addiction model of obesity is based on observations that substance use disorders and continual overeating of palatable foods share common behavioral manifestations, including escalation of use over time, LOC, ongoing misuse despite negative consequences and significant distress. The behavioral similarities between addictive and overeating behaviors have face validity, and the concept of food addiction quickly gained traction in the scientific literature and lay press. Importantly, behavioral observations have been stimulated and bolstered by a significant body of animal research documenting that repeated consumption of palatable foods results in behavioral and neurochemical changes similar to those seen in chronic drug use. Further, scientists have studied changes in the dopaminergic reward system in response to food in people that are Volume 27 Number 6 November 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Disordered eating in obese individuals Marcus and Wildes
obese to test the notion that powerful reinforcers in the form of palatable food can override homeostatic control of eating in a manner similar to that observed in individuals with addiction. There is evidence that addiction and obesity share neurobiological processes; in particular, impairments in dopaminergic circuitry associated with reward sensitivity and incentive motivation [12 ]. Nevertheless, the addiction model of obesity has attracted prominent critics [13 ,14] who have argued that research evidence is limited, findings are inconsistent and reductionist [15] and that the addiction model fails to take into account the remarkable complexity of human obesity. Recent work has been more nuanced, and there have been substantive efforts to refine and narrow the putative food addiction obesity phenotype by focusing on individuals with binge eating and incorporating information from multiple additional domains and levels of analysis. &&
&&
BINGE EATING AS THE OBESITY PHENOTYPE CHARACTERIZED BY FOOD ADDICTION Given mixed findings from studies comparing obese and lean individuals on facets of the addiction model, recognition of the heterogeneity of obesity, and interest in identifying neurobehavioral obesity phenotypes, it is not surprising that recent work has focused on commonalities between binge eating and addiction. First, as detailed by Smith and Robins [16] the pattern of symptoms associated with binge eating and addiction as outlined in the DSM are very similar. There also is recent experimental evidence supporting the notion of binge eating as the obesity phenotype characterized by food addiction. For example, Dalton et al. [17 ] administered a laboratory feeding paradigm to groups of lean and overweight women characterized as ‘binge-type’ and ‘nonbinge-type’ on the basis of scores on a selfreport measure of binge eating. In comparison with nonbinge-types, binge-types ate more palatable food and reported increased wanting for this foods even when satiated. Another group of investigators [18 ] examined reward responding to monetary cues in an functional MRI (fMRI) paradigm among obese individuals with and without BED and lean controls; results documented that in comparison with obese individuals without BED, obese individuals with BED exhibited reduced recruitment of networks involved in reward processing and self-regulation. Finally, recent work [19] suggests that there is variability among individuals with BED in activation of reward processing in frontostriatal circuits, and that individuals who continue binge eating after BED &
&
treatment show less recruitment of reward circuitry than those who do not continue binge eating.
INCORPORATING ADDITIONAL INFORMATION The proliferation of research findings in both the addiction and obesity fields has posed a challenge to the adoption of a simple binge eating/food addiction model in understanding the link between disordered eating and obesity. Conceptualizations of addiction have developed beyond the initial dopamine hypothesis of reward to encompass interacting circuits, including reward, memory, inhibitory control, motivation, interoception and stress reactivity, and the integration of genetic and epigenetic factors [20]. For example, the development of addiction increasingly has been conceptualized as a shift from impulsive to compulsive processes, which involves a change from ventral to dorsal striatal regulation and a transition from prefrontal executive control to striatal habit-related control. These concepts have not yet been examined fully in relation to food addiction [13 ,15], although there are recent studies that document that obese individuals with BED, when compared with control individuals without BED, demonstrate more impulsive responding to nonfood [21] and food cues [21,22 ] as assessed by behavioral laboratory tasks. Similarly, a recent investigation using fMRI to examine neural correlates of response to nonfood cues on a laboratory task among obese individuals with BED and weight matched and lean control individuals showed that individuals with BED were characterized by hypoactivity in brain areas involved with self-regulation and impulse control [23]. Future work is needed to examine whether individuals with BED demonstrate aspects of compulsivity, which would be expected to appear over time in individuals who demonstrate disordered eating. Simultaneously, research expanding the understanding of human feeding behavior also has burgeoned. In addition to reward neurocircuitry, the hypothalamic system, gastrointestinal and adipocyte hormones, inflammatory mediators, and microbiota and gut–brain axis are involved in the regulation of feeding behavior and have been implicated in the causes and maintenance of obesity. For example, previous distinctions between homeostatic eating, which is designed to preserve energy balance, and nonhomeostatic or hedonic eating, which involves food intake in the absence of any energy depletion signals, are no longer clear. As summarized by Volkow et al. [20], it now is apparent that homeostatic and hedonic eating do not occur in isolation, but rather that endocrine hormones
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Eating disorders
implicated in the regulation of homeostatic eating (e.g., insulin, leptin, and ghrelin) also modulate the effects of drugs. Conversely, neurotransmitters involved in drug-seeking (e.g., cannabinoids, serotonin, and glutamate) also affect food intake. The examples of an expanding literature provided above do not do justice to the manifold levels of analysis ranging from genes to psychosocial factors and the current food environment that are the targets of ongoing research on the regulation of feeding behavior and the pathogenesis of disordered eating and obesity. Narrowly focused research on a particular neural circuit or a particular aspect of feeding behavior is necessary, but not sufficient to understand the relation between disordered eating and obesity. For example, because the hypothalamic– pituitary–adrenal axis is involved in human response to stress as well as homeostatic feeding behavior, there is a substantial body of evidence examining the relationship between life stress and obesity. This work suggests that there is a subgroup of stressresponsive obese individuals who have a vulnerability to overeating palatable food and gaining weight over time. Stress also is a risk factor for addiction and relapse to addictive behavior. Thus, both obesity and addiction share multiple overlapping pathways [24 ]. Unsurprisingly, recent epidemiologic and laboratory studies have examined the relation between stress and disordered eating. One investigation studied the relationship between childhood abuse, a form of chronic stress, and food addiction among participants in the Nurses’ Health Study II [25] and documented that women with a history of childhood sexual or physical abuse were 2.5 times more likely to self-report food addiction in adulthood. Approximately two-thirds of food-addicted individuals also were obese, and the authors conclude that uncontrolled eating in response to stress may be one important factor affecting obesity risk in women. Gluck et at. [26] studied obese women with and without BED using a cold pressor stress test to examine changes in ghrelin, a peptide hormone known to increase hunger levels. Results documented increases in ghrelin levels in individuals with and without BED, but no between-group differences. These studies examining the role of stress in disordered eating exemplify the proliferation of salient research, but also the difficulties in evaluating findings from investigations utilizing widely varying methodology at very different levels of analysis. &
THE WAY FORWARD Given the accelerated rate of inquiry related to obesity, disordered eating, and addiction and 446
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evolving understanding of the complex interrelationships among these overlapping, but distinct phenomena, what are the questions that will lead to enhanced understanding and ultimately, to more effective treatments? We offer several suggestions that are not meant to be inclusive, but which grow directly from studies reviewed herein. First, available findings suggest the importance of including a range of binge eating phenotypes in future work (i.e., individuals with bulimia nervosa, BED and those with subjective or LOC episodes). Second, consistent with the current emphasis on incorporating dimensions in psychiatric research, additional studies should include validated dimensional measures of binge eating and traits such as disinhibition and food addiction that are related to obesity, weight gain, and binge eating. Third, it will be important to examine aberrant eating across the full spectrum of BMI to disentangle the relative roles of adiposity and eating behavior traits and phenotypes. Mixed findings in extant research also may result, in part, from the use of varying food cues (sight, smell, or taste of food) and/or neutral, nonfood related cues to elicit task-based responses in experimental individuals; thus, it is desirable to include food and nonfood cues in future research. Finally, longitudinal studies are needed to confirm the relationship between disordered eating and unwanted weight gain. For example, in an fMRI study of 162 male and female adolescents, Stice et al. [27 ] examined neural activation in response to anticipated and actual receipt of palatable food and monetary rewards in a group of healthy-weight adolescents, and evaluated weight changes 1 year after initial assessment. There was evidence that aberrant reward responsivity predicted future substance abuse, but not unhealthy weight gain in this yearlong study. However, binge eating was not assessed, and obese youth were not included. &&
IMPLICATIONS FOR TREATMENT There is a compelling need for additional treatments for obesity and disordered eating, and efforts to identify new treatment targets on the basis of new research findings are underway. For example, on the basis of the findings documenting dysregulation of the dopaminergic reward system in binge eating, an animal study found that deep brain stimulation of the nucleus accumbens shell, which has been implicated in reward-seeking behaviors, reduced binge eating of highly palatable food in a mouse model [28]. Similarly, on the basis of findings that opioid antagonists affect motivational and hedonic processes in the brain, an initial laboratory investigation with human [29] showed that treatment with a Volume 27 Number 6 November 2014
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Disordered eating in obese individuals Marcus and Wildes
novel mu-opioid receptor antagonist reduced brain responses to images of high-calorie foods among obese binge eaters. Although these studies are preliminary, the identification and testing of novel treatments will continue as the science evolves and ultimately, there is the promise of more effective interventions for those that suffer from disordered eating and weight problems.
CONCLUSION Research on the association between disordered eating and obesity is advancing rapidly and multiple lines of inquiry may lead to a fuller understanding of and treatments for disordered eating and obesity. Acknowledgements Dr Marcus acknowledges NIH grant support (DK61254, DK066585, HL096770, MH085921, HD068802, and DK096405). Dr Wildes acknowledges NIH grant support (MH085921). Conflicts of interest The authors report no conflicts of interest.
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