Food Craving, Stress and Limbic Irritability

ACTIVITAS Activitas Nervosa Superior 2010;52:3-4,113-117 NERVOSA ORIGINAL SUPERIOR ARTICLE

FOOD CRAVING, STRESS AND LIMBIC IRRITABILITY

Miroslav Svetlak*

Department of Physiology, Faculty of Medicine, Masaryk University, Brno, Czech Republic Center for Neuropsychiatric Research of Traumatic Stress & Department of Psychiatry, 1st Faculty of Medicine, Charles University, Praha, Czech Republic Received August 23, 2010; accepted September 12, 2010

Abstract

Recent findings show that food craving is strongly related to emotional distress. Stress-induced feeding is a phenomenon related to sensitization associated with repeated stress stimuli and related increase in incentive salience attributed to known familiar foods and increased craving. Because stress sensitization may also produce seizure-like activity, aim of the present study was to test a hypothesis that food craving could be linked to heightened level of seizure-like symptoms that present cognitive and affective symptoms related to temporo-limbic hyperexcitability. In order to achieve this goal we have measured indices of food craving, traumatic stress and seizure-like symptoms using psychometric measures in 257 university students. The results indicate statistically significant correlations of food craving with traumatic stress symptoms (r=0.26, p<0.05), dissociative symptoms (r=0.37, p<0.01) and seizure-like symptoms (r=0.41, p<0.01). These results present first supportive evidence that food craving in healthy persons may be related to traumatic stress and seizure-like symptoms. The present results also support findings that traumatic stress may lead to kindling-like sensitization that could play a role in food craving mechanisms.

Key words: Food craving; Limbic irritability; Stress

INTRODUCTION Many researches show that normal healthy people There is growing evidence that palatable food, similarly sometimes experience a craving for certain food, fe- as addictive drugs, can activate the brain reward system males more often than males (Pelchat, 1997; Weingar- and produce powerful behavioral reinforcement (Cota et ten & Elston, 1991). Food craving presents irresistible al., 2006; Hernandez & Hoebel, 1988; Robinson & Ber- need for food intake that presents subjective experience ridge, 1993; Mercer & Holder, 1997; Rogers & Hen- motivating people to eat a particular food (Pelchat, drik, 2000). 2002; Mercer & Holder, 1997). Recent findings show Complex interactions of bio-psycho-social factors of that food craving is related to body weight and causes palatable food intake may lead to neurobiological adap- excessive eating patterns observed in obesity, binge tations that eventually increase food intake characte- eating and bulimia nervosa (Weingarten & Elston, rized by subjective feeling of food craving (Volkow & 1990; Sullivan & Bulik, 1998; Cepeda-Benito, Fernan- Wise, 2005; Robinson & Berridge, 1993). Pleasure re- dez, & Moreno, 2003; Sobik et al., 2005; Franken & lated to hedonic impact of food (”liking”) and the moti- Muris, 2005). Food craving is related to emotional dis- vational incentive value (“wanting”) frequently occur tress, anxiety, dysphoric mood and/or depression (Hill simultaneously (Berridge, 2004) but they may disso- et al., 1991; Christensen, 2001). ciate and “pathological wanting” (craving) may emerge Stress-induced feeding is a phenomenon that has been independently of liking and physiological nutritional reported in both animals and humans (Antelman & needs (Robinson & Berridge, 1993; Finlayson, King & Szechtman, 1975; Morley, Levine & Rowland, 1983) Blundell, 2007, 2008). and associations of an ability to cope with stress and *Correspondence to: Miloslav Svetlak, email: [email protected] 113

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eating behavior is well documented (Nieuwenhuizen & METHODS Rutters, 2008). Recent findings suggest that lasting stress exposure may lead to mesotelencephalic dopami- Participants nergic system sensitization associated with repeated The sample included 257 healthy university students stress stimuli and related increase in incentive salience (77 men and 180 women; mean age was 24.2±1.8). Ac- attributed to known familiar foods and increased crav- cording to the WHO standards, 16 (6.2%) of students ing (Robinson & Berridge, 1993; Antelman & Szech- could be classified as an underweight, 197 (76.7%) as a tman, 1975; Morley, Levine & Rowland, 1983). The normal weight, 38 (14.8%) as an overweight, and 6 stress related sensitization has also been proposed to (2.3%) as obese. Exclusion criteria were organic diseas- cause changes in GABA postsynaptic receptors that es of the CNS, any form of epilepsy, psychiatric disord- may lead to overstimulation of neurons mainly in the ers, alcohol dependence and drug abuse according to limbic system and these changes may increase sensitivi- criteria M.I.N.I. version 5.0.0 (Sheehan et al., 1998). ty and damaging potential of future stressors through The study was approved by the University ethical com- enhancement of responsiveness (Teicher et al., 2003, mittee and all the participants gave written informed 2006; Post et al., 1995). consent. Recent data suggest that influence of repeated stressors may result to kindling-like process leading to increased Psychometric measures limbic excitability and limbic irritability because of For the assessment of food craving the modified version deficits of inhibitory systems and executive functions of General Trait Food-Cravings Questionnaire (G-FCQ- (Teicher et al., 2003, 2006). T) was used (Nijs, Franken & Muris, 2007). The G- Clinically, these stress related neuro-functional changes FCQ-T is 21-item questionnaire (Cronbach’s alpha may lead to sudden transitions of subjective feeling, 0.91, test-retest reliability after week 0.86) that reflects mood and other signs of cognitive and emotional dysre- typical factors of craving, such as preoccupation with gulation observed as cognitive, memory and affective food (Cronbach’s alpha 0.86), loss of control (Cron- seizure-like symptoms, which usually occur in temporal bach’s alpha 0.90), positive outcome expectancy (Cron- lobe epilepsy but may occur also in nonepileptic condi- bach’s alpha 0.82) and emotional craving (Cronbach’s tions (Heath, 1976; Bear, 1979; Geschwind, 1979; Ro- alpha 0.82). Subjects indicate a degree of their expe- berts et al., 1993; Hines et al., 1995; Teicher et al., rience on a six-point Likert scale 1 (never or not appli- 2003, 2006; Schutter & van Honk, 2006). In this con- cable) to 6 (always). text, it was documented that limbic irritability symp- Limbic irritability was assessed using complex partial toms were significantly elevated in subjects with a self- seizure-like symptoms inventory– CPSI (Roberts et al., reported history of exposure to childhood sexual or 1993). CPSI was originally designed to measure somat- physical abuse (Teicher et al., 1993; 2006) but may oc- ic, sensory, and behavioral and memory symptoms as- cur also in normal population (Roberts et al., 1993; Bob, sociated with ictal temporal lobe epilepsy (brief halluci- 2008). nations, paroxysmal somatic disturbances, automatisms Consistently with these findings increased occurrence of and dissociative disturbances). The inventory has 35 EEG abnormalities, such as spikes, sharp waves, or pa- questions and subjects indicate degree of their expe- roxysmal slowing predominantly over left frontotem- rience on 6-point Likert scale (Cronbach’s alpha 0.95, poral region have been reported in significantly trauma- test-retest reliability after week 0.87). Total score higher tized patients (Teicher et al., 2003, 2006; Putnam, 1997; than 70 meets the criterion for the so-called epilepsy Ito et al., 1993). spectrum disorder but also lower values may indicate an Recent data also suggest that a certain decrease in cere- underlying electrophysiological dysfunction (Roberts et bellar vermis blood flow which occurs in traumatized al., 1993). patients may cause deficits in inhibitory control of lim- For screening traumatic stress symptoms the question- bic functioning, temporal-limbic seizure-like activity naire Trauma Symptom Checklist TSC-40 (Briere, and related cognitive and emotional dysregulation 1996) was used (Cronbach’s alpha 0.91, test-retest re- (Heath, 1976; Riklan et al., 1976; Anderson et al., 2002; liability after week 0.88). TSC-40 was developed to Teicher et al., 2003, 2006; Schutter & van Honk, 2006). assess the adult symptom patterns associated with a In the context of reported findings between stress and history of victimization, especially childhood sexual food craving, aim of the present study is to test a hypo- abuse. The inventory has 40 questions and subjects in- thesis that food craving could be linked to heightened dicate degree of their experience on 4-point Likert level of stress related psychopathology and seizure-like scale. Total scores higher than 70 are associated with symptoms. In order to achieve this goal we have meas- significant childhood traumas. ured indices of food craving, stress related psychopa- Symptoms of dissociation reflecting experienced trau- thology and limbic irritability using psychometric matic stress were measured using Dissociative Expe- measures in 257 university students. rience Scale (DES) (Bernstein & Putnam, 1986). The

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DES is a self-report scale asking respondents to indicate craving but did not show the difference for positive out- response on 100-mm scale to what extent they expe- come expectancy. rience 28 dissociative phenomena in daily life (Cron- bach’s alpha 0.92, test-retest reliability after week 0.91). Table 2. Mean scores and standard deviations of used Examples of such phenomena include feelings of deper- questionnaires and differences between men and wom- sonalization, derealization, and psychogenic amnesia. en.

Data analysis Men Women Empirical data obtained in psychometric assessment Variables (N = 77) (N = 180) t p were processed in a statistical evaluation that included Mean ± SD Mean ± SD calculation of means, standard deviations (SD), Pearson product-moment correlation coefficients and t-test for BMI 23.4 ± 2.9 21.8 ± 3.2 4.820 0.0001 independent samples using software package Statistica CPSI 21.4 ± 14.6 23.5 ± 18.9 -0.386 0.69 version 8.0. TSC-40 23.4 ± 9.9 27.0 ± 14.5 -1.405 0.16 DES 8.2 ± 7.4 9.3 ± 9.9 -0.372 0.61 RESULTS G-FCQ-T 49.8 ± 15.4 57.0 ± 16.4 -2.845 0.001 The results of the present study are in agreement with the hypothesis that food craving could be linked to I. 12.5 ± 5.2 15.4 ± 6.1 -3.799 0.001 heightened level of stress related psychopathology and II. 13.9 ± 5.9 15.7 ± 6.6 -1.561 0.12 seizure-like symptoms (Table 1). These results indicate III. 16.6 ± 5.1 16.5 ± 4.6 0.623 0.53 statistically significant correlations of food craving in- IV. 7.2 ± 3.4 9.7 ± 4.4 -4.248 0.0001 dexed by G-FCQ-T with measures of seizure-like symptoms (CPSI), traumatic stress (TSC-40) and dissociation Note. G-FCQ-T -General Food Cravings Questionnaire-Trait; (DES). I. Preoccupation with food; II. Loss of control; III. Positive outcome expectancy; IV. Emotional craving. CPSI - Complex Table 1. Correlations of food craving indexed by G- Partial Seizure-like symptoms Inventory; TCS-40 – Trauma FCQ-T with measures of seizure-like symptoms (CPSI), Symptom Checklist. traumatic stress (TSC-40) and dissociation (DES). DISCUSSION Variables CPSI G-FCQ-T TSC-40 DES As a whole results of the present study support the hy- CPSI - 0.41** 0.69** 0.73** pothesis linking food craving with heightened level of stress related psychopathology and seizure-like symp- ** TSC-40 0.69** 0.33** - 0.63 toms. DES 0.73** 0.37** 0.63** - The results indicate statistically significant correlation G-FCQ-T 0.41** - 0.33** 0.37** of food craving indexed by G-FCQ-T with traumatic stress symptoms measured TSC-40 (r=0.33, p<0.01). ** I. 0.37** 0.87** 0.27** 0.36 More expressive correlation was found between food II. 0.39** 0.85** 0.30** 0.39** craving and dissociative symptoms measured by DES (r=0.37, p<0.01). These results are in agreement with III. 0.15* 0.56** 0.11 0.01 growing evidence that early life stressors and childhood ** IV. 0.31** 0.75** 0.31** 0.39 physical or psychological abuse are associated with obesity in adulthood (Felitti et al., 1998; Jonge et al., Note. G-FCQ-T -General Food Cravings Questionnaire-Trait; 2003; Gustafson & Sarwer, 2004; Alvarez et al., 2007), I. Preoccupation with food; II Loss of control; III Positive increased relative weight in children (Mellbin & Vuille, outcome expectancy; IV Emotional craving. CPSI - Complex 1989), a major risk factor for excessive weight gain and Partial Seizure-like symptoms Inventory; TCS-40 - Trauma (visceral) obesity (Nieuwenhuizen & Rutters, 2008) and Symptom Checklist; DES – Dissociative experience scale; * with etiology of eating disorders (Weingarten & Elston, p<0.05; ** p<0.01 1990; Sullivan & Bulik, 1998; Cepeda-Benito, Fernan- dez, & Moreno, 2003; Sobik et al., 2005; Gunstad et al., 2006; Alvarez et al., 2007). Statistical analysis (Table 2) did not show significant Important correlation was found between food craving differences between men and women in CPSI score and and seizure-like symptoms measured by CPSI (r=0.41, TSC-40 score. Conversely, the analysis indicates that p<0.01). Close relationships were also found for symp- women have higher scores of G-FCQ-T than men. toms of traumatic stress and dissociation with seizure- Women also had higher score than men for subscales: like symptoms, which support hypothesis that traumatic preoccupation with food, loss of control, emotional stress may lead to kindling-like sensitization in agree-

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