ANOREXIA NERVOSA (AN) is a complex psychiatric

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1 Psychiatry and Clinical Neurosciences 21; 64: doi:1.1111/j x Regular Article Taste reactivity deficit in anorexia nervosapcn_216 Csaba Szalay, MD, 1 * Ildikó Ábrahám, MD, 2 Szilárd Papp, MD, PhD, 1 Gábor Takács, PharmD, 1 Balázs Lukáts, MD, PhD, 1 Ágnes Gáti, MD, PhD 2 and Zoltán Karádi, MD, PhD 1 1 Institute of Physiology and Neurophysiology Research Group of the Hungarian Academy of Sciences and 2 Department of Psychiatry and Psychotherapy, Pécs University Medical School, Pécs, Hungary Aim: Anorexia nervosa is a complex psychiatric disorder posing a rapidly increasing burden on modern societies. Our purpose was to clarify perceptualmotivational aspects of gustatory disturbances in the disease. Methods: A taste reactivity test, with the use of all five primary qualities in two concentrations, was performed in restrictive-type anorexic patients, and their hedonic evaluations were compared to those of agematched healthy control subjects. Results: The patients gave significantly lower pleasantness scores for pleasant taste stimuli compared with controls. The differences were the greatest for the lower concentration sucrose, umami and sodium chloride. given for the aversive taste stimuli were similar in both experimental groups. Conclusion: Our findings contribute to a better understanding of complex symptoms of anorexia nervosa, and may also help to develop more effective cognitive-behavioral therapies. Key words: anorexia nervosa, gustatory disturbances, hedonic ratings, taste reactivity test. ANOREXIA NERVOSA (AN) is a complex psychiatric disorder posing a rapidly increasing burden on modern societies. It has an increasing frequency all over the world, 1 and it has the highest death rate of any psychiatric disease. 2 AN has two main types: restrictive and purgative. It develops overwhelmingly in adolescent women. 3 AN is characterized by extreme dietary restriction, a relentless pursuit of thinness, an obsessive fear of becoming fat, loss of body weight, and a variety of metabolic and endocrine alterations, including primary or secondary amenorrhea. 4 6 Persons suffering from AN exhibit a disturbed perception of their own body shape and size as well. Several studies have tried to elucidate the underlying pathophysiological and psychological mechanisms of the disease. Although its cause is so far unknown, it is obvious that the feeding behavior of *Correspondence: Csaba Szalay, MD, Institute of Physiology, Pécs University Medical School, H-7624 PÉCS, Szigeti str. 12., Hungary. csaba.szalay@aok.pte.hu Received 4 September 29; revised 3 May 21; accepted 5 May 21. AN patients is substantially disturbed compared to healthy subjects. As gustation plays an important role in the guidance of feeding, numerous studies have addressed the issue of taste in AN. When sugar/fat mixtures were used, anorexics disliked the foods rich in fat but there was no difference in the perception and preference for the sweet taste. 7 Gustometry studies utilizing various techniques revealed hypogeusia and dysgeusia in patients with eating disorders, 8,9 and Nozoe and co-workers also demonstrated that taste responsiveness improved significantly during behavior therapy, and such early improvement resulted in better progression of treatment. 1 The hedonic aspect of human gustation was thoroughly examined by the taste reactivity method (originally used in animal experiments 11 ), invented by Steiner and his co-workers This method is easy to perform, and it poses little burden on the subjects. Eiber and her co-workers, using a different technique, showed that patients with eating disorders had a decreased hedonic response to various concentration sucrose solutions when they were swallowed compared to when these solutions were spat out. 15 Despite this relative abundance of taste studies in 43

2 44 C. Szalay et al. Psychiatry and Clinical Neurosciences 21; 64: eating disorder patients, a par excellence taste reactivity study in AN, with the use of all five primary taste qualities, has not been performed yet. In the present experiments, therefore, a taste reactivity study was conducted in restrictive-type AN patients, and their hedonic evaluations were compared to those of agematched healthy control subjects. METHOD Altogether, 25 subjects volunteered initially in this study. Restrictive-type AN subjects were diagnosed based on the criteria of the DSM-IV Text Revision. Finally, after excluding three volunteers because of their uncertain diagnosis or unfitting morphometric or other examination data, 11 AN patients, ten women and one man (body mass index [BMI], ; mean age, 23.3 years) and 11 agematched healthy control subjects, nine women and two men (BMI, ; mean age, 24 years) participated in these experiments. All the volunteers were screened with the Eating Attitudes Test (EAT)-4 (patients, ; controls, ), and the Eating Disorder Inventory (EDI) test was also carried out ( drive for thinness [DFT] subscale: patients, ; controls, ; bulimia subscale: patients, ; controls, ; body dissatisfaction [BD] subscale: patients, ; controls, ; ineffectiveness [IE] subscale: patients, ; controls, ; perfectionism subscale: patients, ; controls, ; interpersonal distrust subscale: patients, ; controls, ; interoceptive awareness [IA] subscale: patients, ; controls, ; maturity fears [MF] subscale: patients, ; controls, ). All subjects were free of salivary dysfunction, and histories of gastrointestinal or other diseases, and their serum zinc and amylase concentrations were in the physiological range (12 24 mmol/l and 28 1 IU/L, respectively). The sessions took place in a quiet, well-separated room in the Psychiatry and Psychotherapy Clinic of Pécs University, Medical School. Written informed consent was obtained from all testees. The protocol fully conformed to the provisions of the Declaration of Helsinki (1995; rev. Edinburgh, 2). The project was approved by the Ethics Committee of Pécs University, Medical School. Gustatory functions were tested by presenting 5-mL liquid taste stimuli at room temperature in disposable plastic cups. Subjects, fasting for at least 6 h before the examination, were instructed to perform inter-stimulus distilled water rinses ad libitum. Two concentrations of each tastant were used:.1 M and.5 M sucrose as sweet,.1 M and.5 M NaCl as salty,.1 M and.5 M monosodium glutamate (MSG) as umami,.3 M and.3 M HCl as sour,.3 mm and 3 mm quinine HCl (QHCl) as bitter, and 5 and 25% orange juice (OJ) as complex (pleasant) taste. The sip and spit method was employed. 12 The testee had to swirl the solution around in the mouth and then spit it out. Between two taste solutions, distilled water rinses were performed to eliminate the taste from the subject s oral cavity. After each taste solution, the subject had to put a single pencil mark on a 2 mm visual analogue scale (VAS) where the left side (-1 mm) meant the hedonically negative taste, whereas the right side (+1 mm) meant the hedonically positive taste. The middle point of the scale, the, meant that the solution was neutral for the participant. For the VAS data, the distance between the and any given pencil mark was measured to the accuracy of 1 mm. Both concentrations of sucrose, the lower concentration salt (.1 M NaCl) and umami (.1 M MSG), and both concentrations of orange juice were considered as the hedonically positive tastes, whereas the hedonically negative tastes were the stronger salt (.5 M NaCl) and umami (.5 M MSG), and both concentrations of the acid (.3 M,.3 M HCl) and quinine solutions (.3 mm, 3 mm QHCl). 16,17 The sessions were videotaped for further analysis of the facial expressions regarding innate, discriminative motor reactions of the facial muscles to adequate stimulation of the peripheral gustatory receptors. 11,13 Verbal commentaries of the subjects were also recorded. For statistical analysis of data, the SPSS software package was used. Both individual and group VASscore averages were calculated, and independent samples t-tests were employed for averaged and normalized scores. Group comparisons were made using the Mann Whitney U-test, and Spearman s rank correlation coefficients (Spearman s rho [Srho]) were calculated as well. Statistical differences were considered to be significant at P <.5 or less. RESULTS In the present study, characteristic taste perception abnormalities were found in the AN patients. On the

3 Psychiatry and Clinical Neurosciences 21; 64: Taste reactivity and anorexia nervosa 45 (b) (a) General reactivity for pleasant tastes General reactivity for unpleasant tastes * The analysis of reactivity data of the individual stimuli also revealed a characteristic gustatory perception deficit of the patients (Fig. 2). Pleasantness ratings in the AN group, compared to controls, significantly decreased for the lower concentration of sucrose (t 1,2 = 2.561; P <.2), salt (t 1,2 = 2.61; P <.2), and umami (t 1,2 = 3.812; P <.2). Reactivity scores to the strong and either pleasant or (a) S1 S2 OJ1 Pleasant tastes * * ** OJ2 N1 U1 4 5 (b) Unpleasant tastes Figure 1. General reactivity for (a) pleasant and (b) unpleasant tastes. The ratings given for the pleasant tastes were significantly lower in the ( ) anorexia nervosa group compared to the ( ) controls. No significant difference was found in the ratings given for the aversive tastants. Ordinate, hedonic ratings; abscissa, groups of subjects. *Significant difference (P <.8) one hand, their general taste reactivity tended to be weaker compared to that of individuals in the control group (t 2,262 = 1.945; P =.53). On the other hand, and most characteristically, pronounced deficits were seen in the hedonic evaluation of gustatory stimuli. As demonstrated in Fig. 1a, the hedonic ratings of the anorexic patients given for the pleasant tastes, in comparison to the controls, proved to be significantly lower (t 2,13 = 2.714; P <.8), whereas the ratings given for the unpleasant, aversive tastes were similar (t 2,13 =.564; not significant; Fig. 1b). N2 U2 H1 H2 Q1 Q2 Figure 2. Taste reactivity ratings for the individual (a) pleasant and (b) unpleasant taste stimuli. A significant difference was found between the ( ) anorexia nervosa group and the ( ) controls in the ratings of milder sweet, salty, and umami solutions. Ordinate, hedonic ratings; abscissa, groups of subjects. *Significant difference (P <.5). **Significant difference (P <.2). S1, sucrose.1 M; S2, sucrose.5 M; OJ1, orange juice 5%; OJ2, orange juice 25%; N1, NaCl.1 M; N2, NaCl.5 M; U1, monosodium glutamate.1 M; U2, monosodium glutamate.5 M; H1, HCl.3 M; H2, HCl.3 M; Q1, quinine HCl.3 mm; Q2, quinine HCl 3 mm.

4 46 C. Szalay et al. Psychiatry and Clinical Neurosciences 21; 64: unpleasant, robust taste-sensation-eliciting test solutions (higher concentration of sucrose, both concentrations of orange juice, as well as the stronger salt and umami, and both concentrations of HCl and QHCl) did not differ significantly between the AN patients and the control subjects. The group comparisons of BMI, EAT-4, and several of the EDI subscales (DFT, BD, IE, IA and MF) revealed remarkable differences between the anorexic and control subjects (for both BMI and EAT-4, P <.1; for DFT, P <.1, for BD, P <.1, and for IE, IA, and MF, P <.1, respectively). In addition, a clear relationship among these parameters and the taste reactivity scores was also clearly demonstrated (lower concentration umami vs BMI: Srho,.529, P <.1; lower concentration sucrose vs EAT- 4: Srho,.448, P <.5; lower concentration salt vs EAT-4: Srho,.434, P <.5; lower concentration umami vs EAT-4: Srho,.557, P <.1). Of the EDI subscales, correlation of these data with taste reactivity scores was found to be especially high in the DFT (lower concentration sucrose vs DFT: Srho,.432, P <.5; lower concentration salt vs DFT: Srho,.429, P <.5; lower concentration umami vs DFT: Srho,.467, P <.5) and body dissatisfaction (lower concentration sucrose vs BD: Srho,.435, P <.5; lower concentration salt vs BD: Srho,.421, P <.5; lower concentration umami vs BD: Srho,.479, P <.5). DISCUSSION A full-scale taste reactivity study, including all five primary gustatory qualities and a complex taste (orange juice), with immediate hedonic evaluation of the stimulus solutions has not been performed yet for AN. Our experiments elucidated a relative weakness in general taste reactivity of AN patients. As the most characteristic finding of the present study, however, the hedonic ratings of the restrictive-type anorexic patients for the pleasant, but not for the aversive tastes proved to be significantly lower compared to those of control subjects. Furthermore, the correlation analysis substantiated the clear relationship of these results with the cognitive disturbances characterizing AN. Hypogeusia and dysgeusia, mainly involving the sour, bitter and salty tastes, have already been demonstrated in AN; 8 1,18,19 nevertheless, perceptualmotivational aspects of the findings so far received diverse interpretations. Earlier studies have emphasized that a characteristic carbohydrate phobia exists in anorexic patients. 4,6 Later reports, however, suggested no alteration of sweet taste preference but a definite dislike of foods rich in fat in anorexicrestrictors. 7,2,21 Sunday and Halmi also pointed out that the patients (and healthy subjects) liked the sweeter solution more. 2 Our findings only partly agree with the above data because in the present examinations hedonic ratings of the higher concentration sucrose solution in the AN patients did not differ from those in the control subjects. The virtual contradiction between our results no difference in sour and bitter responsiveness, and decreased hedonic ratings for the lower concentration sucrose solution and data of the literature can be resolved by taking into consideration the obvious heterogeneity of the methodologies employed. In fact, all the other studies used either food items (e.g. sucrose-sweetened cheese, milk or cream) or pure gustatory stimuli but in different volume, concentration or delivery method, whereas, to date, our investigation appears to be the first to use in eating disorder patients a par excellence human taste reactivity test with immediate hedonic evaluation of the stimulus solutions. Restrictive-type anorexics displayed significantly lower hedonic ratings for the mild pleasant taste stimuli, indicating that these patients may experience a reduced pleasure in eating. It has been suggested previously that a hedonic monitor exists, biased by body weight and caloric intake, and also that pleasure plays a physiological role in regulating body weight in lean and obese subjects. 22 More specifically, taste preference profiles for sweet solutions were shown to be a sensitive index of nutritional status of the organism. 23 Eiber and her co-workers observed a decrease in hedonic response of patients when sucrose solutions were swallowed compared to when they were spat out. 15 This reflects the fact that AN patients, in addition to their decreased ability to experience pleasure, do have excessive fear of gaining weight. Modern neuroimaging studies have revealed that there are taste-information-processing deficits in the insula, ventral and dorsal striatum present even in recovered restrictive-type anorexics. 24 Disturbance of the relevant perceptual-motivational mechanisms in AN is also substantiated by the EEG findings of Tóth and her co-workers, who reported a lower omega complexity during taste exposure, 25 and found a significantly higher proportion of theta and lower percentage of alpha1 activity in anorexic patients. 26

5 Psychiatry and Clinical Neurosciences 21; 64: Taste reactivity and anorexia nervosa 47 In conclusion, our results showed evidence for the existence of taste-associated complex perceptualmotivational disturbance in restrictive-type AN patients. To achieve a better understanding of the background of symptoms of this complex disease may also contribute to developing well-targeted and more effective therapeutic approaches. ACKNOWLEDGMENTS The authors wish to thank Ms Ildikó Fuchs for her valuable technical assistance. This work was supported by the Health Science Council of Hungary (ETT 315/26), and the Hungarian Academy of Sciences. REFERENCES 1. Makino M, Tsuboi K, Dennerstein L. Prevalence of eating disorders: a comparison of Western and non-western countries. Med. Gen. Med. 24; 6: Sullivan PF. Mortality in anorexia nervosa. Am. J. Psychiatry 1995; 152: American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association, Washington, DC, Crisp AH. The possible significance of some behavioral correlates of weight and carbohydrate intake. Psychosom. Res. 1967; 11: Johnson C, Lewis C, Hagman J. The syndrome of bulimia. Review and synthesis. Psychiatr. Clin. North Am. 1984; 7: Russell GFM. The nutritional deficit of anorexia nervosa. J. Psychosom. Res. 1967; 11: Simon Y, Bellisle F, Monneuse MO, Samuel-Lajeunesse B, Drewnowski A. Taste responsiveness in anorexia nervosa. Br. J. Psychiatry 1993; 162: Jirik-Babb P, Katz JL. Impairment of taste perception in anorexia nervosa and bulimia. Int. J. Eating Disord. 1988; 7: Nakai Y, Kinoshita T, Koh S, Tsuji S, Tsukada T. Taste function in patients with anorexia nervosa and bulimia nervosa. Int. J. Eating Disord. 1987; 6: Nozoe S, Masuda A, Naruo T, Soejima Y, Nagai N, Tanaka H. Changes in taste responsiveness in patients with anorexia nervosa during behavior therapy. Physiol. Behav. 1996; 59: Grill HJ, Norgren R. The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res. 1978; 143: Perl E, Hamburger R, Steiner JE. Taste- and odor-reactivity in elderly demented patients. Chem. Senses 1992; 17: Steiner JE. Discussion paper: innate, discriminative human facial expressions to taste and smell stimulation. Ann. N. Y. Acad. Sci. 1974; 237: Steiner JE, Lidar-Lifschitz D, Perl E. Taste and odor: reactivity in depressive disorders, a multidisciplinary approach. Percept. Mot. Skills 1993; 77: Eiber R, Berlin I, de Brettes B, Foulon C, Guelfi JD. Hedonic response to sucrose solutions and the fear of weight gain in patients with eating disorders. Psychiatry Res. 22; 113: Moskowitz HKV, Sharma KN, Jacobs HL, Sharma SD. Effects of hunger, satiety and glucose load upon taste intensity and taste hedonics. Physiol. Behav. 1976; 16: Yamaguchi S. Basic properties of umami and its effects on food flavour. Food Rev. Int. 1998; 14: Lacey JH, Stanley PA, Crutchfield M, Crisp AH. Sucrose sensitivity in anorexia nervosa. J. Psychosom. Res. 1977; 21: Casper RC, Kirschner B, Sandstead HH, Jacob RA, Davis JM. An evaluation of trace metals, vitamins, and taste function in anorexia nervosa. Am. J. Clin. Nutr. 198; 33: Sunday SR, Halmi KA. Taste perceptions and hedonics in eating disorders. Physiol. Behav. 199; 48: Drewnowski A, Halmi KA, Pierce B, Gibbs J, Smith GP. Taste and eating disorders. Am. J. Clin. Nutr. 1987; 46: Thompson DA, Moskowitz HR, Campbell RG. Effects of body weight and food intake on pleasantness ratings for a sweet stimulus. J. Appl. Physiol. 1976; 41: Cabanac M. Physiological role of pleasure. Science 1971; 173: Wagner A, Aizenstein H, Mazurkewicz L et al. Altered insula response to taste stimuli in individuals recovered from restricting-type anorexia nervosa. Neuropsychopharmacology 28; 33: Toth E, Kondakor I, Tury F, Gati A, Weisz J, Molnar M. Nonlinear and linear EEG complexity changes caused by gustatory stimuli in anorexia nervosa. Int. J. Psychophysiol. 24; 51: Toth E, Tury F, Gati A, Weisz J, Kondakor I, Molnar M. Effects of sweet and bitter gustatory stimuli in anorexia nervosa on EEG frequency spectra. Int. J. Psychophysiol. 24; 52: