Reduced perception of bodily signals in anorexia nervosa

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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Available online at www.sciencedirect.com Eating Behaviors 9 (2008) 381 – 388 Reduced perception of bodily signals in anorexia nervosa Olga Pollatos a,b,c,⁎, Anne-Lene Kurz a,d , Jessica Albrecht b , Tatjana Schreder b , Anna Maria Kleemann b , Veronika Schöpf b , Rainer Kopietz b , Martin Wiesmann b , Rainer Schandry a a b Department of Psychology, Ludwig-Maximilians-University of Munich, Germany Department of Neuroradiology, Ludwig-Maximilians-University of Munich, Germany c Clinic of Neurology, Ludwig-Maximilians-University of Munich, Germany d Klinikum Freyung, Germany Received 16 August 2007; accepted 7 February 2008 Abstract Objective: Interoceptive awareness is known to be impaired in eating disorders. To date, it has remained unclear whether this variable is related to the construct of interoceptive sensitivity. Interoceptive sensitivity is considered to be an essential variable in emotional processes. The objective of the study was to elucidate this potential relationship and to clarify whether general interoceptive sensitivity is reduced in anorexia nervosa. Methods: Using a heartbeat perception task, interoceptive sensitivity was assessed in 28 female patients with anorexia nervosa and 28 matched healthy controls. Questionnaires assessing interoceptive awareness (EDI) and several other variables were also administered. Results: Patients with anorexia nervosa displayed significantly decreased interoceptive sensitivity. They also had more difficulties in interoceptive awareness. Conclusions: In addition to a decreased ability to recognize certain visceral sensations related to hunger, there is a generally reduced capacity to accurately perceive bodily signals in anorexia nervosa. This highlights the potential importance of interoceptive sensitivity in the pathogenesis of eating disorders. © 2008 Elsevier Ltd. All rights reserved. Keywords: Anorexia nervosa; Heartbeat perception; Interoceptive awareness 1. Introduction Eating disorders (EDs) are the most prevalent psychiatric disorders in females aged between 14 and 26 years and are associated with considerable physical and psychological morbidity (Zipfel, Lowe, Reas, Deter, & Herzog, 2000). In the last decades, the frequency of these illnesses has greatly increased (Fassino, Pierò, Gramaglia, & Abbate-Daga, 2004; KeskiRahkonen et al., 2007; Friedrich et al., 2006; Klein & Walsh, 2003), representing a great challenge for physicians of various specialties and significantly impacting health care in the female population (Mitchell & Bulik, 2006). Several authors have ⁎ Corresponding author. Leopoldstr. 13 80802 Munich, Germany. Tel.: +49 89 2180 6356; fax: +49 89 2180 5233. E-mail address: pollatos@psy.uni-muenchen.de (O. Pollatos). 1471-0153/$ - see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.eatbeh.2008.02.001 Author's personal copy 382 O. Pollatos et al. / Eating Behaviors 9 (2008) 381–388 contributed to a description of the psychological features of patients with EDs. A fundamental role has been played by Garner (Garner, Olmstead, & Polivy, 1983) who developed the Eating Disorder Inventory (EDI), a questionnaire which has become a standard tool in studies investigating EDs. The EDI (EDI-2) (Garner, 1984) assesses behavioral and psychological traits, such as the drive for thinness, bulimia, body dissatisfaction, and interoceptive awareness, the latter of which measures the ability to discriminate between individual sensations and to accurately respond to emotional states (Garner et al., 1983). This subscale also taps uncertainty in the identification of specific visceral sensations relating to hunger and satiety (Garner, 1984). Poor interoceptive awareness characterized by uncertainty in the recognition of emotional states and difficulties to discriminate sensations related to hunger and satiety is often a core psychopathological element which plays an important role in the onset and maintenance of EDs (Fassino et al., 2004). Recent research has provided evidence that interoceptive awareness, as measured by the EDI, is impaired in patients with eating disorders (Fassino et al., 2004; Garner et al., 1983; Lilenfeld, Wonderlich, Riso, Crosby, & Mitchell, 2006; Matsumoto et al., 2006): Fassino and coworkers found poorer interoceptive awareness in patients with various types of eating disturbances including anorexia nervosa, bulimia and obesity (Fassino et al., 2004). Matsumoto et al. (2006) also report poorer interoceptive awareness in patients with anorexia nervosa. This deficit significantly improved following treatment. Despite its great importance, interoceptive awareness has so far only been measured by means of self-report questionnaires. It can be hypothesized that patients with difficulties in discriminating visceral sensations with respect to hunger and satiety should also be less able to perceive bodily signals in general. This hypothesis draws upon a broader concept of interoception. Interoceptive processes and the ability to perceive these processes accurately are often quantified using various heartbeat perception tasks that measure the ability to perceive one's heartbeats (Cameron, 2001; Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004; Dunn, Dalgleish, Ogilvie, & Lawrence, 2007; Pollatos, Gramann, & Schandry, 2007; Pollatos, Herbert, Matthias, & Schandry, 2007; Pollatos, Schandry, Auer, & Kaufmann, 2007; Pollatos, Trautmattausch, Schroeder, & Schandry, 2006; Wiens, 2005). While different kinds of heartbeat perception tasks are in use it is a common observation that there are substantial, interindividual differences in this variable (Jones, 1994; Cameron, 2001; Schandry & Bestler, 1995). Empirical data suggest that heartbeat detection correlates with the ability to detect changes in other autonomically innervated organs (Whitehead & Drescher, 1980), thus this variable should reflect a general sensitivity for visceral processes. The extent of an individual's sensitivity to bodily signals (“interoceptive sensitivity”) is considered to be an essential variable in many theories of emotions such as that proposed by James or Damasio (James, 1884; Schachter & Singer, 1962; Damasio, 1994; Damasio, 1999). The idea that we feel emotions because we perceive our bodily reactions (Bennett & Hacker, 2005) is a core characteristic of these theories suggesting that participants who perceive bodily signals with a high degree of sensitivity should experience emotions more intensely and vice versa that reduced interoceptive awareness is accompanied with affected experience of emotions (Damasio, 1994; Damasio, 1999; James, 1884; Schachter & Singer, 1962). The question as to whether interoceptive sensitivity measured by a heartbeat perception task is reduced in eating disorders is still open. Concerning other psychiatric disorders significant differences in heartbeat perception ability have been observed in several clinical samples: Many studies (Ehlers, 1995; Ehlers, Mayou, Springings, & Birkhead, 2000; Eley, Stirling, Ehlers, Gregory, & Clark, 2004; Pineles & Mineka, 2005; Roth et al., 1992; Wald & Taylor, 2005; White, Brown, Somers, & Barlow, 2006; Van der Does, Antony, Ehlers, & Barsky, 2000; Zoellner & Craske, 1999) have shown that interoceptive sensitivity is closely associated with anxiety disorders. For example, Ehlers et al. (2000) report a higher accuracy of heartbeat perception in panic patients. In a similar study with children, increased panic symptoms were associated with an enhanced ability to perceive internal physiological cues as measured by a heartbeat perception task (Eley et al., 2004). Interestingly a recent study could show that interoceptive sensitivity is reduced in depressed patients (Dunn et al., 2007). Concerning a possible deficit of interoceptive processes and interoceptive sensitivity in EDs it can be assume that patients with attenuated interoceptive awareness experience many emotional situations less intensely (Bennett & Hacker, 2005) which might contribute to deficits in emotional and social functioning known to be associated both with depression (Lee, Harkness, Sabbagh, & Jacobson, 2005) and EDs (Zonnevijlle-Bender, van Goozen, Cohen-Kettenis, van Elburg, & van Engeland, 2002; Zonnevylle-Bender et al., 2005). Deficits in interoceptive sensitivity might therefore play an important role in the aetiology and maintenance of EDs. The main objective of the present study was to investigate the degree of interoceptive sensitivity in anorexia nervosa. Additionally the relationship between interoceptive sensitivity and the well-validated construct of interoceptive awareness (EDI subscale) should be examined. As former data indicated that interoceptive sensitivity is related to anxiety and depression these variables were also assessed and included as possible mediators for observed differences. Author's personal copy O. Pollatos et al. / Eating Behaviors 9 (2008) 381–388 383 2. Materials and methods 2.1. Participants Twenty-eight female patients with anorexia nervosa (ANs) were recruited from patient self-help groups (ANAD e.V., Pathways, Cinderella e.V., Max-Planck-Institute of Psychiatry) in Munich. All participants met DSM-IV criteria for anorexia nervosa as assessed by the self-report screening version (SIAB-S) of the Structured Interview for Anorexic and Bulimic Syndromes for DSM-IV and ICD-10 (Fichter & Quadflieg, 2000). DSM-IV (American Psychiatric Association, 1994) criteria for anorexia nervosa were also assessed using a semi-structured psychiatric interview. Exclusion criterion included past or present psychotic disorders. Mean age in the anorexia nervosa group was 21.4 years (SD 4.8). Mean body mass index was 16.6 kg/m2 (SD 1.2) and mean duration of illness 2.5 years (SD 3.2 years). Thirteen of the ANs (46%) received an additional Axis I diagnosis. Of these, nine had major depressive disorder (MDD; 32%) with no comorbid anxiety disorder, two had MDD with a comorbid anxiety disorder (social phobia, panic disorder) and a further two had an anxiety disorder (panic disorder, generalized anxiety disorder) without comorbid depression. Three patients were taking antidepressive medication from the class of selective serotonin reuptake inhibitors (two patients citalopram and one fluoxetin). 23 of the ANs were of the restricting subtype and five of the binge–purge subtype. ANs were matched for gender, age and educational level with twenty-eight healthy controls. Controls had a mean age of 22.4 (SD 2.4), a mean BMI of 21.5 (SD 4.3) and were recruited in universities, trade schools and technical colleges. They were also assessed using a semi-structured psychiatric interview. All control participants had no Axis I diagnosis. Participants were paid € 20 for taking part in the study. 2.2. Procedure Experiments were conducted in accordance with the Declaration of Helsinki. Ethical approval was obtained from an institutional review board. Participants were provided with written information about the experiment and informed consent was obtained. The heartbeat perception task was performed using four intervals of 25 s, 35 s, 45 s and 100 s duration in accordance with the Mental Tracking Method described by Schandry (1981). During all trials, participants were asked to silently count their own heartbeats. A start and stop cue signalled the beginning and end of the counting phases. During heartbeat counting, participants were not permitted to take their pulse or attempt to use other forms of manipulation in order to aid the counting of their heartbeats. Following the stop signal, participants were required to verbally report the number of counted heartbeats. Participants were not informed about the length of the counting phases or the quality of their performance. Height and weight were assessed and they filled in several questionnaires including the Beck's Depression Inventory BDI, the State Trait Anxiety Inventory STAI, the Toronto Alexithymia Scale TAS and a personal questionnaire assessing personal data like age and schooling. 2.3. ECG recording The ECG was measured using nonpolarizable Ag–AgCl electrodes attached to the right mid-clavicle and lower left rib cage. ECG activity was recorded with a DC amplifier and digitised at a sampling rate of 500 Hz. 2.4. Data analyses Heartbeat perception was calculated as the mean score of four heartbeat perception intervals according to the following transformation: 1=4 X ð1
ðjrecorded heartbeats
counted heartbeatsjÞ=recorded heartbeatsÞ According to this transformation, the heartbeat perception score can vary between 0 and 1 with higher scores indicating small differences between counted and recorded heartbeats. Mean heartbeat perception score and questionnaire scale scores were calculated for each participant group and analysed using ANOVAs. Spearman correlations were calculated between heartbeat perception score, the interoceptive awareness Author's personal copy 384 O. Pollatos et al. / Eating Behaviors 9 (2008) 381–388 scale of the EDI and the other personality (Beck's Depression Inventory BDI, State Trait Anxiety Inventory STAI, Toronto Alexithymia Scale TAS) and personal (BMI, age) variables. A linear regression analysis was conducted between the interoceptive awareness scale and the following variables: BMI, age, BDI total score, TAS subscales, STAI state and trait scales. 3. Results 3.1. Sample description and questionnaire data Sociodemographic features (age, BMI) and questionnaire data obtained for the two participant groups are presented in Table 1. Group comparisons performed with ANOVAs revealed a significantly lower BMI for patients with anorexia nervosa and no differences with respect to schooling or age. Patients with anorexia nervosa also scored significantly higher in problems in interoceptive awareness (EDI), depression (BDI), anxiety (STAI) and alexithymia (TAS, all subscores and total score). It is important to remember that higher interoceptive awareness scores are related to a poorer ability to discriminate between individual sensations and feelings, and between the sensations of hunger and satiety. Other EDI-2 subscale scores are not relevant for the aims of the present study and are not presented. 3.2. Heartbeat perception The mean heartbeat perception score was .77 (SD .14) for the control group. The patients with anorexia nervosa had a mean heartbeat perception score of .68 (SD .18). This difference was statistically significant (F (df = 1,54) = 4.61, p b .05, η2 = .08, ε = .56) indicating poorer interoceptive sensitivity in patients with anorexia nervosa. Since anxiety and depression have been found to be related to differences in interoceptive accuracy (Dunn et al., 2007; Ehlers et al., 2000; Eley et al., 2004; Pollatos, Traut-Mattausch, et al., 2006) and interoceptive awareness measured by the EDI is altered in eating disorders, a further ANOVA was conducted with these variables as covariates in order to control for possible mediating effects. This analysis confirmed poorer heartbeat perception in patients with anorexia nervosa as compared to healthy controls (F (df = 1,50) = 7.27, p b .01, η2 = .13, ε = .75) when controlling for possible confoundation. 3.3. Relation between interoceptive sensitivity, interoceptive awareness and other psychological variables Interoceptive awareness and interoceptive sensitivity were not related (r = .04, p = n.s.), whereas high interrelations were observed between interoceptive awareness and the BMI (r = − .37, p b .01), the BDI score (r = .77, p b .001), the STAI state score (r = .58, p b .001), the STAI trait score (r = .70, p b .001), the TAS scale “ability to identify feelings (TAS1)” (r = .70, p b .001) and the TAS scale “ ability to describe feelings (TAS 2)” (r = .65, p b .001). In order to test which of the assessed variables were independent variables linearly related to the interoceptive awareness scale of the EDI, a multiple linear regression (R = 0.85; R2 = 0.72; F (df = 8,45) = 14.65; p b .001) was Table 1 Comparison between the two groups with respect to sociodemographic and questionnaire data (p b .05 =*, p b .01 =**, p b .001 = ***) Age Schooling BMI EDI interoceptive awareness BDI STAI-State STAI-Trait TAS 1 TAS 2 TAS 3 TAS Total Anorexics mean (SD) Controls mean (SD) F (df = 1,54) p 21.43 (2.38) 4.12 (0.94) 16.59 (1.16) 8.89 (6.36) 17.61 (10.55) 42.21 (6.30) 51.07 (11.04) 24.24 (7.04) 22.00 (5.39) 20.81 (4.62) 67.05 (12.98) 22.39 (4.78) 3.78 (0.33) 21.49 (4.28) 1.61 (2.83) 2.92 (2.80) 36.14 (11.30) 37.04 (10.04) 15.79 (5.20) 13.75 (5.42) 17.23 (4.87) 46.76 (12.00) 0.92 1.01 34.03 31.05 50.64 6.24 24.84 25.62 32.50 7.66 35.88 n.s. n.s. *** *** *** * *** *** *** ** *** Author's personal copy O. Pollatos et al. / Eating Behaviors 9 (2008) 381–388 385 performed. While personal (age) and clinical (BMI) features of the participants were not correlated with interoceptive awareness, interoceptive awareness independently and positively correlated with assessed depression level (β = 0.50; p b 0.01) and the state anxiety score (β = 0.29; p b 0.01). 4. Discussion Our data suggest that interoceptive sensitivity is decreased in anorexia nervosa as compared to healthy controls. This result extends former research reporting a decreased ability to discriminate hunger and satiety sensations in eating disorders as measured by the interoceptive awareness score of the EDI (Fassino et al., 2004; Garner et al., 1983; Lilenfeld et al., 2006; Matsumoto et al., 2006). The present study suggests that patients with anorexia nervosa not only have problems in recognizing certain visceral sensations related to hunger and satiety, but also exhibit a generally reduced capacity to accurately perceive bodily signals. As heartbeat perception correlates with the ability to detect changes in other autonomically innervated organs (Whitehead & Drescher, 1980) a general reduced sensitivity to visceral processes in anorexia nervosa can be assumed. The observed deficit in interoceptive sensitivity in anorexia nervosa remained significant when controlling for differences in anxiety and depression between the two participant groups. This result is in accordance with data from depressive patients where reduced interoceptive sensitivity was demonstrated (Dunn et al., 2007). Following the somatic marker hypothesis of Damasio (Damasio, 1994, 1999), emotional situations are associated with bodily changes which are centrally processed and consolidate so called somatic markers. Such somatic markers are required for guiding individual behavior by signaling stimulus significance to the body. There is some empirical evidence suggesting that in addition to the observed deficits in interoceptive sensitivity there are also altered autonomic functioning in EDs: Murialdo et al. (2007) demonstrated alterations of sympathovagal control of heart rate variability in EDs. These changes were unrelated to body weight and BMI, subtype of ED (anorexia nervosa vs. bulimia) and leptin levels (Murialdo et al., 2007). Using a stress induction paradigm Zonneyville-Bender et al. (2005) demonstrated a significantly lower heart rate increase during the task in patients with anorexia nervosa who were characterized by a great discordance between self-reported emotional arousal and indices of neurophysiological arousal. The reported mismatch between “subjective” arousal and “objective” physiological response (Zonnevylle-Bender et al., 2005) is in accordance to the present study demonstrating a general deficit in interoceptive sensitivity in patients with anorexia nervosa. Confirming this assumption other studies could show that interoceptive sensitivity correlated positively to indices of neurophysiological arousal during the processing of emotional pictures (Pollatos, Gramann, et al., 2007; Pollatos, Herbert, et al., 2007; Pollatos, Traut-Mattausch, et al., 2006). Affected autonomic response patterns and blunted bodily reactions in anorexia nervosa would plausibly lead to an altered feedback from the body which could be an important contributing factor to the onset and maintenance of psychopathology. It can be followed that attenuated interoceptive sensitivity and assumed altered autonomic response patterns in EDs are accompanied with less intense emotional experiences in many everyday situations (Bennett & Hacker, 2005). It is interesting that although patients with anorexia nervosa had problems in both interoceptive sensitivity and interoceptive awareness as compared to healthy controls, the two variables were not correlated to one another, while the EDI score for interoceptive awareness was highly positively correlated with assessed levels of depression and anxiety. These results suggest that self-reported data on interoceptive awareness as measured by the EDI are confounded with anxiety and depression. The observed poorer ability to discriminate between individual sensations and feelings in anorexia nervosa might therefore reflect disorder-specific dysfunctional thoughts and feelings rather than actual differences in visceral sensitivity. This suggestion is confirmed by previous data reporting increased levels of alexithymia in eating disorders (Berthoz, Perdereau, Gadart, Corcos, & Haviland, 2007; Corcos et al., 2000; de Zwaan, Biener, Bach, Wiesnagrotzki, & Stacher, 1996; Taylor, Bagby, & Parker, 1999). Alexithymia, a syndrome involving a marked inability to identify, describe, regulate, and express one's emotions (Sifneos, 1976; Taylor & Doody, 1985), was originally described by Sifneos in patients with psychosomatic disorders and has been related to a broad range of physical and psychiatric disorders (e.g., alcoholism, drug addiction, post-traumatic stress disorders and eating disorders, see Taylor et al., 1999). Alexithymia is presently viewed in both clinical and non-clinical populations as a continuous personality variable, i.e., people differ in their ability to identify and describe their feelings (Jessimer & Markham, 1997). Problems in discriminating sensations relating to hunger and satiety in eating disorders, as characterized by the EDI interoceptive awareness score, might therefore be mediated by a general inability to regulate and describe one's emotions. Author's personal copy 386 O. Pollatos et al. / Eating Behaviors 9 (2008) 381–388 Concerning the heartbeat detection task used in the present study, potential weaknesses in the assessment of interoception must be taken into account. While this task is widely used (Ehlers & Breuer, 1996; Ehlers et al., 2000; Dunn et al., 2007; Pollatos, Gramann, et al., 2007; Pollatos, Traut-Mattausch, et al., 2006; Pollatos, Schandry, et al., 2007; Pollatos, Herbert, et al., 2007; Van der Does et al., 2000), several studies have reported that these kind of tracking tasks may be influenced by people's beliefs and expectancies with respect to their heart rates (Knapp, Ring, & Brener, 1997; Knapp-Kline & Kline, 2005; Wiens & Palmer, 2001; Windmann, Schonecke, Fröhlig, & Maldener, 1999). Besides such expectancies, other factors such as attention or motivation may also influence the outcome of heartbeat perception tasks. Nevertheless, a convincing body of evidence exists showing that results of different heartbeat perception tasks are congruent with effects of interoception on emotions (Katkin, Wiens, & Ohman, 2001; Pollatos, Kirsch, & Schandry, 2005b; Pollatos, Gramann, et al., 2007; Wiens, 2005) or localization of relevant brain structures activated during heartbeat perception (Critchley et al., 2004; Pollatos, Kirsch, & Schandry, 2005a; Pollatos, Schandry, et al., 2007). This lends support to the validity of heartbeat perception tasks in detecting processes involved in interoception (see Wiens, 2005). We conclude that in addition to a decreased ability to recognize certain visceral sensations related to hunger and satiety, there is a generally reduced capacity to accurately perceive bodily signals in eating disorders. To our knowledge, the present study is the first empirical work to show that interoceptive accuracy, as measured by a heartbeat perception task, is reduced in anorexia nervosa. 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