1 Department of Pharmacology, Institute of Psychiatry and Neurology, Warsaw, 2 Department of Psychiatry Nursing, The Ludwik Rydygier Medical University, Bydgoszcz, 3 Department of Prevention and Treatment of Addictions, Institute of Psychiatry and Neurology, Warsaw and 4 Department of Otolaryngology, Warsaw Medical Academy, Warsaw, Poland
* Author to whom correspondence should be addressed at: Department of Pharmacology, Institute of Psychiatry and Neurology, Sobieskiego 9 St., PL-02957 Warsaw, Poland. Tel.: +48 22 32 13 376; Fax: +48 22 84 27 644; E-mail: scinska{at}yahoo.com
(Received 26 August 2004; first review notified 1 September 2004; in revised form 21 October 2004; accepted 8 November 2004)
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ABSTRACT |
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INTRODUCTION |
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Umami taste is now recognized to be the fifth basic taste category in mammals. It has been suggested that this taste category evolved to enhance detection of amino acids (e.g. glutamate and aspartate) and oligopeptides in foods (for review, see Bellisle, 1999; Brand, 2000
; Doty, 2003
). Monosodium glutamate (MSG) is a prototypic umami substance that is widely used as a research tool and flavour enhancer (Yamaguchi, 1991
; Yamaguchi and Ninomiya, 2000
; Kobayashi and Kennedy, 2002
; Nelson et al., 2002
). Preclinical studies have indicated that MSG solutions may evoke umami taste through interactions with both metabotropic (mGluR) and ionotropic (iGluR) glutamate receptors expressed by taste receptor cells in a taste bud (Brand, 2000
). Two subtypes of mGluRs, i.e. mGluR1 (Toyono et al., 2003
) and mGluR4 (Chaudhari et al., 2000
; Nakashima et al., 2001
), as well as the N-methyl-d-aspartate (NMDA) subtype of iGluRs (Brand, 2000
; Nakashima et al., 2001
), are candidate receptors involved in MSG detection by taste receptor cells.
It has been shown repeatedly that the glutamatergic system in the brain is involved in the mediation of the neurobehavioural effects of ethanol. For example, a large body of evidence indicates that NMDA receptors are particularly sensitive to clinically relevant ethanol concentrations (for review, see Lovinger, 1997; Spanagel and Bienkowski, 2002
). While acute ethanol inhibits NMDA receptors, chronic ethanol administration leads to enhancement of the NMDA receptor function (Danysz et al., 1992
; Hoffman, 1995
). Another line of research has also indicated that mGluRs, including mGluR1 and mGluR5, are modulated by both acute and chronic alcohol administration (Minami et al., 1998
; Spanagel and Bienkowski, 2002
). Given the role played by peripheral iGluRs and mGluRs in detection of umami substances, one may hypothesize that acute and/or chronic alcohol exposure alters sensitivity to MSG taste. Thus, in the present study, we decided to evaluate taste responses to MSG in chronic alcoholics and non-alcoholic controls. In order to evaluate the basic taste sensitivity of the two groups, detection thresholds were assessed by means of electrogustometry (Experiment 1). The effects of acute exposure of the oral mucosa to ethanol solutions on reactivity to MSG taste were assessed in social drinkers (Experiment 2).
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MATERIALS AND METHODS |
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Twenty-five male volunteers without a history of psychiatric disorder and consuming 1 standard drink/day served as controls. Only subjects with Alcohol Use Disorders Identification Test (AUDIT; Babor and Grant, 1989
) scores <8 were included in the study. The controls were recruited from families of staff members, through the institutions involved in the study.
The subjects in both groups were Caucasians, aged 1959 years (see Table 1 for details), in good medical health and had no recent history of acute conditions known to alter gustatory or olfactory function (Cullen and Leopold, 1999). Blood alcohol levels were not assessed before a taste test.
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Preparation of MSG samples. Six MSG solutions (0.03, 0.1, 0.3, 1.0, 3.0, 10.0% w/w; Sigma, Poznan, Poland) were prepared using sterile deionized water (Polfa, Lublin, Poland). The range of MSG concentrations was selected on the basis of previous reports (Yamaguchi, 1991; Kobayashi and Kennedy, 2002
). Deionized water served as a control stimulus and thus each participant received and rated seven different gustatory stimuli. Rows of 1-ml single-use syringes were filled with the MSG solutions (syringe 1 = water, syringe 2 = 0.03% MSG, syringe 3 = 0.1% MSG, syringe 4 = 0.3% MSG, etc.) and stored at 4°C until use.
Electrogustometer. The electrogustometer (TR-06, Rion Co., Ltd, Tokyo, Japan) used in the study is a commercially available device that is used for assessing the human taste function (Kuga et al., 1999; Miller et al., 2002
; Sienkiewicz-Jarosz et al., 2005
). The apparatus allows the delivery of anodal currents of low intensity (from 6 to 34 dB, in 2-dB steps; 4400 µA) at known durations. In the present study, the stimulus duration was kept at 0.5 s (Ajdukovic, 1984
; Kuga et al., 1999
). The electrogustometer was equipped with a stainless steel, flat, circular stimulus rod (5 mm in diameter) and a larger indifferent electrode (a neck band). During the test, the stimulus probe was placed on the tongue tip (Miller et al., 2002
), while the indifferent electrode was attached to the subject's neck. The participant signalled any new taste sensation on the tongue with the help of a response button connected to a small buzzer.
Procedure. A single taste test was conducted between 10 am and 2 pm in quiet, well-ventilated rooms. The subjects were asked to refrain from eating, drinking and smoking for at least 1 h prior to the test session. Before the start of the session, each participant was familiarized with rating scales and questioned regarding drinking coffee and tea, and smoking cigarettes. The Fagerström Test for Nicotine Dependence (FTND) was used to assess nicotine dependence in current smokers (Fagerström et al., 1996).
A modified version of the initially ascending, single-staircase detection threshold procedure was used to assess electrogustometric thresholds (Sienkiewicz-Jarosz et al., 2005). The subject was asked to signal any new taste sensation on the tongue by pressing the response button. The current intensity was increased if no response occurred within 3 s. The current intensity was decreased (reversal) if the subject signalled detection of the stimulus. The reported threshold (in µA) was an average of the last four out of eight reversals. For technical reasons, only 19 alcoholics could be tested by electrogustometry. Baseline characteristics of these subjects did not differ from that reported for the whole alcoholic group.
The MSG samples were administered 5 min after completion of electrogustometry. The subjects received an additional 1 ml sample of deionized water on an unblinded basis as a neutral reference point. Then, increasing concentrations of MSG (0.010.0%) were administered in a volume of 1 ml on the anterior tongue from the single-use syringes. The participants were asked to thoroughly taste each sample within the entire oral cavity, and to rate intensity and pleasantness on 100-mm lines labelled at the ends for intensity not at all and extremely (scored 0100) and for pleasantness extremely unpleasant and extremely pleasant (scored 50 to 50) (Scinska et al., 2000, 2001
). The testing of each sample was separated by a duration of 60 s during which the subjects filled the response forms, rinsed their mouths with deionized water and waited for the next sample. The subjects were instructed to spit out the solutions. The test was performed by an experimenter who was blinded to the actual content of the syringes, and no feedback was given to the participant as to the correctness of his taste responses.
Experiment 2
Subjects. Ten social drinkers (six males and four non-pregnant females) were recruited from families of staff members, through the institutions involved in the study. Subjects with AUDIT scores <8 points and consuming 1 standard drink/day were included. Six participants were current smokers. The subjects were Caucasians, aged 1930 years, in good medical health and had no recent history of conditions known to alter gustatory function (Cullen and Leopold, 1999
). Their mean (±SEM) age, weight and height was 23.5 ± 1.0 years, 74.7 ± 5.7 kg and 177.0 ± 3.0 cm.
Preparation of MSG samples and ethanol rinses. Samples of MSG (0.0, 0.3, 1.0, 3.0% w/w) were prepared in the 1 ml syringes as described above (syringe 1 = water, syringe 2 = 0.3% MSG, syringe 3 = 1.0% MSG, syringe 4 = 3.0% MSG). The syringes were stored at 4°C until use.
Ethanol concentrations (0.5, 1.0, 2.0, 4.0% v/v) were prepared from commercially available rectified spirit (95% v/v; Polmos, Zielona Gora, Poland). Deionized water served as a control solution (0.0% ethanol). The solutions were stored at 4°C in tightly sealed sterilized bottles. The bottles were kept at room temperature for 23 h prior to use. Identical 25 ml samples of the five solutions were prepared immediately prior to use in small plastic cups.
The range of ethanol concentrations was selected based on our previous studies. Higher ethanol concentrations produced bitter taste sensation and local irritation (Scinska et al., 2000; Bienkowski et al., unpublished).
Procedure. A single test session was conducted between 10 am and 2 pm in a quiet, well-ventilated room. The subjects were asked to refrain from eating, drinking and smoking for at least 1 h prior to the test session. The basic aspects of the procedure used in Experiment 2 were identical to those described above for Experiment 1. However, the delivery of each MSG sample was preceded by two rinses. The standard deionized water rinse was followed by the ethanol rinse. The participants were instructed to sip the entire 25 ml sample of ethanol solution, to swish the solution in their mouth for 10 s and to spit it out. Afterwards, the MSG solution was administered in a volume of 1 ml on the anterior tongue. The participants were asked to thoroughly taste each sample within the entire oral cavity and to rate its intensity and pleasantness. The MSG samples (0.03.0%) were administered in six repetitions, i.e. after rinsing with 0.0, 0.5, 1.0, 2.0, 4.0 and 0.0% ethanol. The water (0.0% ethanol) rinse was repeated in order to control for effects of repeated rinsing on basic reactivity to MSG taste.
The testing of the MSG samples was separated by a duration of 60 s during which the subjects rated the taste stimuli and rinsed their mouths as described above.
Statistics
In Experiment 1, between-group differences in basic sociodemographic parameters were analysed with the aid of the Student's t-test, the MannWhitney U-test or the Fisher exact probability test (for quantal measures). Electrogustometric thresholds were analysed with the aid of a one-way analysis of variance (ANOVA). A two-way ANOVA (group x MSG concentration) with repeated measures on MSG concentration was used to assess between-group differences in taste responses to MSG. The Pearson productmoment correlation test was employed to search for correlations between taste reactivity and selected sociodemographic and clinical parameters.
In Experiment 2, the two-way ANOVA (ethanol concentration x MSG concentration) with two repeated measures was used to assess the effects of ethanol rinses on reactivity to MSG. All analyses were performed with the aid of the Statistica 5.0 software package for Windows (StatSoft, Inc., Tulsa, OK). A probability level P < 0.05 was considered significant. No correction for multiple comparisons was applied.
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RESULTS |
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Electrogustometric thresholds were significantly higher in the alcoholics (135.9 ± 28.8 µA) than in the controls [58.4 ± 11.2 µA; F(1,42) = 7.58, P < 0.01]. The difference remained significant (P < 0.05) when age, smoking status and coffee drinking were used as covariances, and when subjects with abnormal liver function tests (six alcoholics) were excluded from the analysis. Electrogustometric thresholds did not correlate with duration of alcohol abuse or dependence, alcohol consumption before admission and abstinence duration (Ps > 0.05).
Figure 1 shows intensity (Fig. 1A) and pleasantness (Fig. 1B) ratings of the MSG samples. The two-way ANOVA (group x MSG concentration) revealed that intensity ratings of MSG increased with concentration [F(6,348) = 58.63, P < 0.0001]. Neither a group effect [F(1,58) = 0.68, P = 0.41] nor a group x MSG concentration interaction [F(6,348) = 0.98, P = 0.43] was significant. The ANOVA revealed that pleasantness ratings of MSG varied with concentration [F(6,348) = 6.73, P < 0.001]. Neither a group effect [F(1.58) = 1.76, P = 0.18] nor a group x MSG concentration interaction [F(6,348) = 0.54, P = 0.77] was significant. Elimination of the subjects with abnormal liver tests did not change the results of the ANOVA (Ps > 0.3 for group effects and Group x MSG concentration interactions).
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Experiment 2
Repeated rinsing did not alter the basic taste reactivity to MSG. The ANOVA did not show any difference [F(1,36) = 0.62, P = 0.43 for intensity, F(1,36) = 0.40, P = 0.52 for pleasantness] between responses to the first and last series of the MSG samples (i.e. the samples administered after the control water rinses). Thus, the control data were averaged across the two series.
The two-way ANOVA (ethanol concentration x MSG concentration) revealed that intensity ratings increased with MSG concentration [F(3,36) = 18.13, P < 0.01]. However, neither an ethanol concentration effect [F(4,144) = 1.85, P = 0.12] nor an MSG concentration x ethanol concentration interaction [F(12,144) = 0.98, P = 0.46] was significant (Fig. 2A).
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DISCUSSION |
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In contrast, electrogustometric thresholds were significantly higher in the alcoholic group. Hence, it seems that alcohol dependence may be related to poorer detection of weak gustatory stimuli. Our findings support the results of Smith (1972) who found that alcoholics had higher taste thresholds to quinine than non-alcoholic controls. The two groups in the latter study did not differ in terms of their smoking habits. Jones et al. (1978)
have reported higher thresholds for sodium chloride in the group of long-term non-Korsakoff alcoholics when compared with normal controls. However, the difference between the alcoholics and controls was not much and did not reach significance (P > 0.1). The non-Korsakoff alcoholics in this latter study did not show any abnormalities in terms of reactivity to higher sodium chloride concentrations and thresholds or suprathreshold olfactory cues. On the other hand, both olfactory and gustatory responses were severely impaired in Korsakoff alcoholics (Jones et al., 1978
).
Higher taste thresholds in alcoholics may be a consequence of central and/or peripheral effects of chronic alcohol consumption. Notably, several brain structures (e.g. the striatum and orbitofrontal cortex) and neurotransmitter systems (e.g. dopaminergic and serotonergic transmission) are involved both in taste processing and development of alcohol dependence (Diamond and Gordon, 1997; Yamamoto et al., 1998
; Goldstein et al., 2001
; Small et al., 2003
; Kringelbach and Rolls, 2004
; Myrick et al., 2004
). It is also possible that the toxic effects of alcohol on the oral mucosa (Maier et al., 1994
; Maito et al., 2003
) lead to suppression of threshold electrogustometric responses while leaving whole-mouth responses to suprathreshold stimuli largely unaffected (Bogucka-Bonikowska et al., 2001
; this study).
Higher thresholds in alcohol-dependent subjects may be an indirect consequence of vitamin and/or mineral deficiencies characteristic of this population (Russell, 1980). However, the lack of correlations between the basic clinical parameters and the electrogustometric thresholds (this study) suggest that the elevated taste threshold is a trait rather than a state marker for alcoholism. This hypothesis needs validation in further studies on children of alcoholics and larger samples of alcohol-dependent subjects.
The groups recruited for Experiment 1 differed in their smoking behaviour and coffee intake. In line with previous reports (e.g. Gurling et al., 1985; Swan et al., 1997
), the alcoholics consumed more coffee and were more likely to be smokers. Moreover, the mean FTND score was significantly higher in the alcoholic group, indicating that the alcohol-dependent smokers smoked more heavily than the non-alcoholic smokers. Importantly, the above findings could not be solely responsible for the higher electrogustometric thresholds in the alcoholic group as this latter difference remained significant after controlling for cigarette smoking and coffee drinking.
Limitations of the present study include its relatively small sample size. In addition, it is possible that the alcoholics recruited for Experiment 1 did not represent the whole population of alcoholics. For example, men with more severe forms of alcohol dependence, like those with more antisocial behaviours, are less likely to seek professional help and to enter a treatment programme. One should also bear in mind that the method used in the study, including the concentrations and volumes of the MSG (Experiments 1 and 2) and ethanol solutions (Experiment 2), may not reflect all aspects of gustatory responses in real-life conditions. Given the well-known effects of alcohol on oral biology (Dutta et al., 1992; Maier et al., 1994
; Maito et al., 2003
), further studies will be necessary to fully evaluate the effects of chronic alcohol consumption on taste reactivity in humans.
In conclusion, the present results suggest that: (i) neither acute nor chronic alcohol exposure modifies taste responses to MSG in humans; (ii) alcohol dependence is associated with higher electrogustometric thresholds. Our results add to a growing body of evidence which indicates that the reactivity of alcohol-dependent subjects to suprathreshold taste stimuli remains largely unaffected. On the other hand, alcohol dependence may be associated with deficit(s) in detection of perithreshold gustatory stimuli.
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ACKNOWLEDGEMENTS |
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