Social stress interacts with diet history to promote emotional feeding in females

Summary

Stress-induced eating disorders cause significant health problems and are often co-morbid with mood disorders. Emotional feeding, particularly in women, may be important for the development of obesity and failed attempts to lose weight. However, prospective studies assessing the effect of chronic psychosocial stress on appetite in different dietary environments in females are lacking. The present study tested the hypothesis that chronic psychosocial stress would increase consumption of high caloric diet and this emotional feeding would persist even when a healthier diet was available. Socially housed female rhesus monkeys were studied to address whether subordination increases caloric intake when a high fat and sugar diet (HFSD) was available concurrently with a low fat, high fiber diet (LCD). Cortisol responsivity and food intake were quantified during this choice phase and when only the LCD was available. The order of diet condition was counterbalanced to assess whether a history of HFSD would affect appetite. All females preferred the HFSD but subordinates consumed significantly more calories during the choice phase. The increased calorie intake was maintained in subordinate monkeys even after withdrawal of the HFSD. Subordinate females demonstrated reduced glucocorticoid negative feedback, with post dexamethasone serum cortisol levels significantly predicting intake of the HFSD but not the LCD during the choice condition. The cortisol response to an acute stressor significantly predicted subsequent intake of a HFSD in all females. Continual exposure to the psychosocial stress of subordination in female monkeys results in excess caloric intake of foods that mimic a western dietary environment. In addition, this social stressor interacts with a history of HFSD intake to promote increased feeding even in a healthy dietary environment.

Introduction

In 2009, nearly 73 million adults in the US were obese, representing 28% of the population and an increase of 7% over 2001 rates (CDC, 2010). Additionally, 34% of adults in the US are overweight (Flegal, 2005). Because the health (Hill, 2006) and economic burden (Withrow and Alter, 2010) imposed by obesity is enormous, effective programs to prevent or alleviate obesity are a high priority. While gene variants regulating satiety or metabolism are known to influence appetite and body weight control (Hinney et al., 2010), environmental triggers are likely key determinants of this phenotype (Font et al., 2010). Indeed, emotional feeding resulting from the chronic exposure to psychosocial stressors is a probable contributing factor for excess food intake (Bjorntorp, 2001, Dallman et al., 2005, Rosmond, 2004, Scott et al., 2008). Importantly, attempts to lose weight often fail (Kassirer and Angell, 1998), as eating behaviors become disinhibited and people overeat in response to emotional states (Hays and Roberts, 2008).

Emotional feeding is coincident with both periods of acute and chronic exposure to psychosocial stressors (Adam and Epel, 2007). Psychopathologies with etiologies related to chronic exposure to psychosocial stressors, such as depression and anxiety disorders, are highly comorbid with obesity (Simon and Arterburn, 2009, Werrij et al., 2006). It is uncertain which factors increase an individual's vulnerability to augment caloric intake under stressful circumstances. While intake of highly palatable foods is rewarding via activation of the dopaminergic reward system (Bassareo and Di Chiara, 1999, Blackburn et al., 1986, Johnson and Kenny, 2010, Small et al., 2003), it remains unclear how consumption of a calorically dense diet or one that is high fat and sugar diet (HFSD) alters physiological responses to both chronic and acute stressors.

There is a great deal of uncertainty surrounding the effects of HFSD consumption on the activity of the limbic–hypothalamic–pituitary–adrenal (LHPA) axis in the literature. This could be due to a number of factors including the specific animal model employed and whether a dietary choice was available as a part of the stress paradigm (Adam and Epel, 2007, Warne, 2009). Another important consideration for the study of stress-induced emotional feeding that is often neglected in animal models is gender. Indeed, emotional eating (Zellner et al., 2006, Zellner et al., 2007) and an obese phenotype (Barry et al., 2008, Jones and Carney, 2006, Weissman and Olfson, 1995, Wurtman, 1993, Wurtman and Wurtman, 1995) occur significantly more often in women. The discrepancies in the current animal models available, and the alarming rate at which obesity epidemic is rising, necessitates that an appropriate animal model of stress-induced eating is developed so that the mechanisms responsible for stress-induced caloric intake can be elucidated.

Social subordination in female rhesus monkeys (Macaca Mulatta) is a well-characterized ethologically relevant, translational animal model used to study the adverse health effects of chronic psychosocial stress exposure in women (Adams et al., 1985, Cohen, 1999, Gust et al., 1991, Jarrell et al., 2008, Kaplan et al., 1996, Michopoulos et al., 2009, Morgan et al., 2002, Paiardini et al., 2009, Sapolsky, 2005, Shively, 1998, Wilson et al., 2008). We tested the hypothesis that socially subordinate females would increase overall caloric intake in a dietary environment mimicking a typical western situation wherein both low fat, high fiber diet and a HFSD were made available. In addition, we tested the hypothesis that a history of HFSD consumption would interact psychosocial stress promote excess calorie consumption even in a healthier dietary environment.