Psychiatry Research 215 (2014) 444–447
Contents lists available at ScienceDirect
Psychiatry Research journal homepage: www.elsevier.com/locate/psychres
The relationship between taste sensitivity to phenylthiocarbamide and anhedonia Justin Thomas n, Wahda Al-Mesaabi, Eman Bahusain, Meera Mutawa Department of Natural Science and Public Health, Zayed University, PO Box 144534, Abu Dhabi, United Arab Emirates
art ic l e i nf o
a b s t r a c t
Article history: Received 24 January 2013 Received in revised form 10 August 2013 Accepted 22 November 2013 Available online 4 December 2013
It has been proposed that taste sensitivity to bitter compounds such as, phenylthiocarbamide (PTC) and 6-n-propylthiouracil (PROP), represents a genetic marker for an increased vulnerability to depressive illness. Previous explorations of this idea have proven equivocal. This study refines and further explores this idea by focusing specifically on anhedonia (diminished hedonic capacity), a key symptom in some depressive illness, linked also with sensory pleasure. It is hypothesized that diminished PTC taste sensitivity will be associated with more general decrements in hedonic capacity (anhedonia). An opportunity sample of 198 university students were assessed using paper strips impregnated with PTC, the same participants also completed a widely used assessment of hedonic capacity, the SnaithHamilton Pleasure Scale (SHAPS). Hedonic capacity scores positively correlated with PTC taste sensitivity; specifically, heightened hedonic capacity was associated with heightened sensitivity to the bitter taste of PTC. Furthermore, modest differences were observed between those least (non-tasters) and most (supertasters) sensitive to PTC, with non-tasters reporting significantly lower hedonic capacity scores than supertasters. PTC taste sensitivity may represent a peripheral risk factor for anhedonia. & 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hedonic capacity PTC Genetic Depression
1. Introduction Genetic differences in taste sensitivity to bitter compounds were first reported in the 1930's (Fast et al., 2002; Blakeslee and Fox, 1932). Physiologically, these genetic differences manifest as varying densities of taste buds on the tongue, more specifically, varying densities of the fungiform papillae (Fast et al., 2002). Within the taste sensitivity literature individuals with the highest densities of fungiform papillae are generally referred to as “supertasters”, distinguishing them from “tasters” (an intermediate group) and “non-tasters”, those individuals with the lowest densities of fungiform papillae (Bartoshuk, 1993). Rather than examining fungiform papillae densities, taste status (whether one is supertaster, taster or non-taster) can also be reliably established by exploring individual taste sensitivity to bitter compounds such as phenylthiocarbamide (PTC) and 6-n-propylthiouracil (PROP). A typical testing protocol involves impregnating a strip of paper with a 3–5 micrograms of PTC, which individuals then place on their tongues. Supertasters have the highest sensitivity and lowest detection thresholds for PROP/PTC, and generally report the taste – even at low doses – as extremely bitter. Tasters and non-tasters have respectively higher detection thresholds and lower taste sensitivities, with non-tasters n
Corresponding author. E-mail address: [email protected] (J. Thomas).
0165-1781/$ - see front matter & 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2013.11.026
being the least sensitive of all (Reed et al., 1995; Tepper, 1998). Occasionally within the PTC/PROP taste-sensitivity literature a simpler bimodal, or dichotomous classification is used: taster vs. non-taster. In such cases no distinction is made between supertasters and tasters, both are simply categorized and referred to as tasters. Variations in PTC taste sensitivity are thought to influence dietary habits, and have therefore been associated an increased risk of developing health problems such as, cardiovascular diseases, obesity and some forms of cancer (Goldstein et al., 2005). A small number of studies have also attempted to explore the relationship between PTC taste sensitivity and psychological health. One of the earliest studies exploring this relationship used PTC sensitivity to establish taste status, and also administered a self-report inventory (Cattell′s 16PF) to assess personality traits amongst university students (Mascie-Taylor et al., 1983). The results suggested that tasters tended to be significantly more “tense” and “apprehensive”, compared with their non-taster counterparts. Based on this finding Whittemore (1986) hypothesized that tasters might be more vulnerable to depression. Exploring this idea in subsequent studies, using family history data and a small group of depressed patients, Whittemore reports longer and more severe depressive episodes for those with heightened taste sensitivity (tasters/supertasters), as well as higher rates of familial depressive illness (Whittemore, 1986, 1990). It should be noted,
J. Thomas et al. / Psychiatry Research 215 (2014) 444–447
that Whittemore′s study with depressed participants, relied on only 23 patients, all of them female. In a more recent examination of the relationship between depression and PTC/PROP taste sensitivity, Joiner and Perez (2004) proposed that supertaster status might actually provide a protective factor. They argue that heightened PTC/PROP taste sensitivity has been associated with greater aversion to alcohol (DiCarlo and Powers, 1998), and that heavy alcohol use is associated with depression (see Graham et al., 2007 for review). Based on this reasoning Joiner and Perez suggest that the supertaster′s greater aversion to the taste of alcohol might represent a protective factor against heavy alcohol use, thereby, indirectly reducing the risk of depression. Joiner and Perez also suggest that the heightened PTC/PROP taste sensitivity of supertasters may lead to them experiencing more intense pleasure in regards to taste, and perhaps by extension, in other sensory modalities too. This proposed heightened pleasure sensitivity – “hyper-hedonia” – is viewed as conferring protection against depressive illness. This is based on the observation that a diminished ability to experience pleasure – anhedonia – is a cardinal symptom of major depressive disorder (American Psychiatric Association, 2000) and has also been identified as a vulnerability marker for the disorder′s onset (Loas, 1996; Schrader, 1997; Shankman et al., 2010). Joiner and Perez (2004) explored these ideas using a family history methodology similar to those employed by Whittemore (1986). Healthy adults (N ¼ 42) were assessed and assigned to three taste-status groups (Whittmore′s studies had only two groups tasters and non-tasters). Participants were asked about depressive illness within their families, as hypothesized supertasters reported significantly lower rates of depressive illness amongst their 1st degree relatives, than tasters and non-tasters. The results support the idea of heightened PTC/PROP taste sensitivity representing some kind of protective factor in the context of depression. However, the study used a relatively small sample, and was reliant on retrospective self-reports of familial depressive illness. One explanation for the previously equivocal findings in relation to PTC/PROP taste sensitivity and depression (Whittemore, 1986, 1990; Joiner and Perez, 2004) is that depression (MDD) is a heterogeneous syndrome characterized by a wide variety of symptoms some of which are mutually exclusive, for example, weight loss/weight gain; hypersomnia/insomnia. If we suspect the link with depression is related to the symptom of diminished hedonic capacity (anhedonia), then it may prove more fruitful to focus specifically on this symptom. This would directly explore the idea that PTC/PROP taste sensitivity is associated with hedonic capacity, and as such, may reflect some kind of a vulnerability/ protective marker for depression. The present study follows-up on the idea of a link between PTC/PROP taste-sensitivity and hedonic capacity/anhedonia first proposed by Joiner and Perez (2004). However, rather than have participants retrospect about familial depressive illness, this study directly explores the relationship, assessing the hedonic capacity and PTC/PROP taste sensitivity of all participants. If such taste sensitivity reflects some kind of a vulnerability marker for anhedonia, then we might expect hedonic capacity scores to vary as a function of taste-status. To the best of our knowledge, this is the first study to explore the following hypotheses: H1. There will be a positive correlation between PTC taste sensitivity and hedonic capacity. H2. Individuals identified as non-tasters, will report significantly lower hedonic capacity scores than tasters and supertasters.
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2. Method 2.1. Participants Participants were an opportunity sample of 198 Emirati students taking general education courses at Zayed University in the UAE. Females were 60.1% of the sample, reflecting the institution′s gender ratios. The mean age was 22.05 (S.D.¼ 5.9); there were no significant gender differences for age. All participants were bilingual and spoke Arabic as their first language. 2.2. Measures 2.2.1. Snaith–Hamilton Pleasure Scale (Snaith et al., 1995) The SHAPs was translated into Arabic and independently back translated by bilingual masters-level faculty within Zayed University. The psychometric properties of this dual-language instrument has been favorably reported elsewhere (Thomas et al., 2012). The14-item scale assess anhedonia across 4 domains: interest/pastimes, social interaction, sensory experience, and food/drink. The following is an example item: – “I would get pleasure from helping others”. Items are scored from 1 to 4, with 1 anchored to the response “Strongly Disagree”, while a score of 4 is anchored to “Strongly Agree” etc. (Snaith et al., 1995). This scoring method means lower scores are indicative of greater anhedonia (diminished hedonic capacity). Previous psychometric explorations have reported acceptable internal consistency, 0.91 (Franken and Muris, 2007) and 0.86 (Leventhal et al., 2006) for the scale. Similarly, its convergent and discriminant validity, and its test re-test reliability have all, also yielded acceptable correlations (Leventhal et al., 2006; Franken and Muris, 2007). 2.2.2. The PTC taste test strips The test strips were pre-prepared by a commercial supplier, Precision Laboratories. Each strip of blotting paper was 5 cm in length and 0.5 cm in width and had been impregnated with 3–5 micrograms of phenylthiourea-phenylthiocarbamide. This method has become increasingly popular in the field (Tepper et al., 2001) and has been widely used to good effect in previous studies of PTC/PROP taste sensitivity (Intranuovo and Powers, 1998; Dicarlo and Powers, 1998; Reed et al., 1999; Prescott and Swain-Campbell, 2000). 2.3. Procedure Zayed University human subjects ethics committee approved the study. All participants gave informed consent, and were tested in classrooms in groups of approximately 15, over a 2-week period. Participants were tested at the end of class and had not consumed food or beverages for at least 1 h prior to testing. Participants first completed the SHAPS and then were each given PTC impregnated taste-test strips and a taste-rating sheet. The taste-rating sheet was a nine-point scale anchored at 0 with the phrase (in English and Arabic) “no taste at all” through to 9, with the phrase “tastes extremely bad/bitter”. 2.4. Statistical analysis After log transforming the skewed SHAPS scores, all continuous data met the assumptions for parametric statistical analysis. Pearson's product moment was used to conduct the bivariate correlational analysis based on a one-tailed hypothesis. The comparison of mean SHAPS scores between the three taste-status groups was undertaken using a univariate general linear model (ANCOVA) and a post hoc test. All analyses were undertaken using SPSS version 20.
3. Results The mean score on the SHAPS was 48.08 (S.D. ¼4.87); for males alone the mean was, 48.34(S.D. ¼4.85), and for females, 47.89 (S.D. ¼5.26). These gender differences were not statistically significant. Similarly no gender differences were observed for PTC taste sensitivity scores between females (M ¼6.48, S.D. ¼3.01) and males (M¼ 5.42, S.D. ¼ 3.44). Using Cronbach′s alpha, the internal reliability of the Arabic translation of SHAPs was acceptable: α¼0.78. Participants were categorized according to the tripartite system. Supertaster status was assigned if the participant reported a PTC taste sensitivity score of 7, 8, or 9. Taster status was assigned for scores of 4, 5, and 6, whereas non-tasters were defined as those reporting scores 1, 2 or 3. This method of assigning taste status
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J. Thomas et al. / Psychiatry Research 215 (2014) 444–447
based on a nine-point category response set is identical to that used by DiCarlo and Powers (1998). In their study the agreement between the nine-point scale, and an alternative form of tastestatus assessment (magnitude matching), reached 84%. In the current study, this nine-point scale method of taste status assignment resulted in 58.8% supertasters, 15.5% tasters and 25.7% non-tasters. The mean SHAPS (Anhedonia) scores for these groups were M¼48.88 (S.D. ¼4.52), M¼ 47.92 (S.D. ¼ 4.25) and M¼ 46.97 (S.D. ¼4.50) respectively. A univariate general linear model (ANCOVA) using SHAPs scores as the dependent variable, taste status as a fixed factor and controlling for gender as a covariate, revealed significant group differences: F(2,185) ¼5.40, p o0.01. As hypothesized, post hoc tests confirmed that non-tasters reported significantly lower ( p o0.05) hedonic capacity (SHAPS) scores than supertasters. 3.1. Correlational analysis As hypothesized, higher SHAPS scores were associated with higher PTC taste sensitivity scores. This relationship was statistically significant with a small effect-size; r ¼0.26, p o0.001. Neither PTC taste sensitivity nor SHAPS scores were correlated with age
4. Discussion Heightened PTC taste sensitivity was associated with higher hedonic capacity scores. The effect size of this finding was small, suggesting there are numerous other factors accounting for the variance in hedonic capacity scores. The finding that non-tasters had significantly lower hedonic capacity scores than supertasters is also modestly supportive of a link between PTC taste sensitivity and anhedonia. These findings support those of Joiner and Perez (2004), who found supertasters reported lower rates of depression amongst their first-degree relatives, a finding they speculated might be explicable in terms of heightened hedonic capacity conferring a protective factor against depressive illness. This hedonic capacity hypothesis might explain the previous equivocal findings with regard to PTC/PROP taste sensitivity and depression. It is possible that it may only be depression typified by anhedonia that shows any relationship with PTC/PROP taste sensitivity. For a diagnosis of major depressive disorder (MDD) the DSM-IV (American Psychiatric Association, 2000) requires the presence of either (a) dysphoria/sadness or (b) anhedonia. A study exploring the MDD symptom profiles exclusively associated with anhedonia, found anhedonic MDD to be occasioned by significantly higher degrees of appetite and weight loss. This was not the case for MDD primarily characterized by dysphoria. Similarly, the absence of anhedonia in MDD was significantly correlated with increased appetite and weight gain (Buckner et al., 2008). It is important to note however that the present study was an analog study, and clinical levels of depression or anhedonia were not explored. As such the present findings, at best, represent an initial exploration of a hypothesis with potentially important implications for understanding individual differences in depressive vulnerability. In contrast to other PTC/PROP taste sensitivity studies undertaken in western industrialized nations, the percentage of supertasters amongst the present Emirati sample was relatively high. However, PROP/PTC taste sensitivity in non-western populations has previously been found to vary widely. A cross-national review of over 370 taste sensitivity studies worldwide, reports that Australian Aborigines, Central Americans, North American Indians and Eskimos all demonstrated very different patterns of responsiveness to PTC/PROP compared with predominantly European or European American populations (Guo and Reed, 2001).
Of particular note in this regard are Australian Aborigines, with a non-taster rate of 49.7%. One proposed explanation for the nontaster preponderance amongst the Australian Aborigines is consanguineous marriage. Consanguineous marriage is relatively common within this population (Houseman, 1997) and less genetic heterogeneity may lead to a particular taste status becoming increasingly prevalent. Consanguineous marriage is also a longstanding tradition in the Arab world, a practice that has become increasingly common in the UAE over the past few decades, with consanguinity rates reportedly increasing from 39% to 50.5% in one generation (Tadmouri et al., 2009). The UAE′s relatively high rate of consanguineous marriage may explain the present study′s relative preponderance of supertasters. Both the high rate of Emirati supertasters, and the modest correlational between taste sensitivity and hedonic capacity, are worthy of further exploration. However, the present study has several important limitations that future studies may avoid. Firstly, the reliance on a single – self-report – assessment of hedonic capacity (SHAPS) somewhat reduces confidence in the findings. Despite having good internal reliability in the present study, SHAPS is a self-report measure that asks the individual to respond based on a retrospection of how they have felt over the previous few days. Robinson and Clore (2002) propose that the timeframe within which respondents are asked to consider their emotional state will influence whether semantic, or episodic knowledge retrieval strategies are used. They suggest retrospective
Fig. A1. Transformed distribution of SHAPS scores and Scatter plot of Shaps data alongside taste test scores.
J. Thomas et al. / Psychiatry Research 215 (2014) 444–447
self-reports are more likely to draw on semantic knowledge, whereas online measures, those where participants are asked to report their feeling in the moment, or within the last few hours, are more likely to draw on episodic retrieval strategies. Future explorations of taste sensitivity and hedonic capacity may benefit from using multiple assessments of anhedonia, including those more specifically developed to assess the construct within clinical populations, as well as online measures, aiming to assess the construct in real-time. Such a broader attempt to capture this multidimensional construct, should also take into consideration the anticipatory (wanting) versus consummatory (liking) dichotomy of anhedonic states. Furthermore, despite claims that the SHAPS was designed to be unaffected by nationality (Snaith et al., 1995) at least one item required a slight rewording to fit the UAE context. In the item worded “I would find pleasure in small things, e. g. bright sunny day, a telephone call from a friend” it was deemed necessary to drop the “bright sunny day” phrase, especially since in the UAE rain is more likely to be viewed as pleasurable, and sunny day temperatures can reach upwards of 50 1C. A further limitation was the use of university students. Whilst this does not influence the generalizability of the taste test scores, it seriously limits the generalizability of the hedonic capacity scores. Future explorations of the relationship between PTC taste-sensitivity and anhedonia would greatly benefit from explorations within sizable clinical populations (including matched controls), particularly in the context of MDD characterized by anhedonia. Furthermore, if PTC test strips are used to assess taste-sensitivity to bitter compounds, then the introduction of a dummy strip (plain paper) might help identify and exclude false positives, thereby further strengthening the study design. In conclusion, this study (to the best of our knowledge) represents the first attempt to directly explore the relationship between PTC taste sensitivity and hedonic capacity. The findings suggest that there is a modest relationship between these two clinically relevant variables; further research with a clinical sample and matched controls is merited. Acknowledgments We are grateful to the Emirates Foundation for Philanthropy and the National Research Foundation for its support of this research project during 2011/13. Appendix A See Appendix Fig. A1 here. References American Psychiatric Association, 2000. DSM-IV-TR: Diagnostic and Statistical Manual of Mental Disorders, 4th ed., revised. American Psychiatric Press, Washington, DC. Bartoshuk, L., 1993. The biological basis of food perception and acceptance. Food Quality and Preference 4, 21–32. Blakeslee, A., Fox, A., 1932. Our different taste worlds. Journal of Heredity 23, 97–107.
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Buckner, J.D., Thomas, E.J., Pettit, J.W., Lewinsohn, P.M., Schmidt, N.B., 2008. Implications of the DSM′s emphasis on sadness and anhedonia in major depressive disorder. Psychiatry Research 159, 25–30. DiCarlo, S.T., Powers, A.S., 1998. Propylthiouracil tasting as a possible genetic association marker for two types of alcoholism. Physiology & Behavior 64, 147–152. Fast, K., Duffy, V., Bartoshuk, L., 2002. New psychophysical insights in evaluating genetic variation in taste. In: Rouby, C., Schaal, B.M., Dubois, D., Gervais, R., Holley, A. (Eds.), Olfaction, Taste and Cognition, Cambridge University Press, New York, pp. 391–407. Franken, I.H.A., Muris, E.R.P., 2007. The assessment of anhedonia in clinical and non-clinical populations: further validation of the Snaith–Hamilton Pleasure Scale (SHAPS). Journal of Affective Disorders 99, 83–89. Goldstein, G., Dau, H., Tepper, B., 2005. Adiposity in middle-aged women is associated with genetic taste blindness to 6-n-propylthiouracil. Obesity Research 13, 1017–1023. Graham, K., Massak, A., Demers, A., Rehm, J., 2007. Does the association between alcohol consumption and depression depend on how they are measured? Alcoholism, Clinical and Experimental Research 31, 78–88. Guo, S.W., Reed, D.R., 2001. The genetics of phenylthiocarbamide perception. Annals of Human Biology 28, 111–142. Houseman, M., 1997. Marriage networks among Australian aboriginal populations. Australian Aboriginal Studies 2, 2–23. Intranuovo, L.R., Powers, A.S., 1998. The perciebed bitterness of beer and 6-n-propylthiouracil (PROP) taste sensitivity. Annals of the New York Academy of Sciences 855, 813–815. Joiner, T.E., Perez, M., 2004. Phenylthiocarbamide tasting and family history of depression, revisited: low rates of depression in families of supertasters. Psychiatry Research 126, 83–87. Leventhal, A.M., Chasson, G.S., Tapia, E., Miller, E.K., Pettit, J.W., 2006. Measuring hedonic capacity in depression: a psychomentric analysis of three anhedonia scales. Journal of Clinical Psychology 62, 1545–1558. Loas, G., 1996. Vulnerability to depression: a model centered on anhedonia. Journal of Affective Disorders 41, 39–53. Mascie-Taylor, C.G.N., Mcmanus, I.C., Maclarnon, A.M., Lanigan, P.M., 1983. The association between phenylthiocarbamide (PTC) tasting ability and psychometric variables. Behavior Genetics 13, 191–196. Prescott, J., Swain-Campbell, N., 2000. Responses to repeated oral irritation by capsaicin, cinnamaldehye and ethanol in PROP tasters and non-tasters. Chemical Senses 25, 239–246. Reed, D., Bartoshuk, L., Duffy, V., Marino, S., Price, A., 1995. Propylthiouracil tasting: determination of underlying threshold distributions using maximum likelihood. Chemical Senses 20, 529–533. Reed, D., Nanthakumar, E., North, M., Bell, C., Bartoshuk, L.M., Price, R.A., 1999. Localization of a gene for bitter-taste perception to human chromosome 5p15. American Journal of Human Genetics 64, 1478–1480. Robinson, M.D., Clore, G.L., 2002. Episodic and semantic knowledge in emotional self-report: evidence for two judgment processes. Journal of Personality and Social Psychology 83, 198–215. Schrader, G.D., 1997. Does anhedonia correlate with depression severity in chronic depression? Comprehensive Psychiatry 38, 260–263. Shankman, S.A., Nelson, B.D., Harrow, M., Faull, 2010. Does physical anhedonia play a role in depression? A 2-year longitudinal study. Journal of Affective Disorders 120, 170–176. Snaith, R.P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., Trigwell, P., 1995. A scale for the assessment of hedonic tone the Snaith–Hamilton pleasure scale. British Journal of Psychiatry 167, 99–103. Tadmouri, G., Nair, P., Obeid, T., Al Ali, M., Al Khaja, N., Hamamy, H., 2009. Consanguinity and reproductive health among Arabs. Reproductive Health 6, 6–17. Tepper, B., 1998. 6-n-propylthiouracil: a genetic marker for taste, with implications for food preference and dietary habits. American Journal of Human Genetics 65, 1271–1276. Tepper, B., Christensen, C.M., Cao, J., 2001. Development of brief methods to classify individuals by PROP taster staus. Physiology & Behavior 73, 571–577. Thomas, J., Al Ali, M., Al Hashmi, A., Rodriguez, A., 2012. Convergent validity and internal consistency of an Arabic Snaith Hamilton pleasure scale. International Perspectives in Psychology: Research, Practice, Consultation 1, 46–51. Whittemore, P.B., 1986. Phenylthiocarbamide (PTC) tasting and reported depression. Journal of Clinical Psychology 42, 260–263. Whittemore, P.B., 1990. Phenylthiocarbamide (PTC) tasting, genetics, and depression. Journal of Clinical Psychology 46, 262–272.
Contents lists available at ScienceDirect
Psychiatry Research journal homepage: www.elsevier.com/locate/psychres
The relationship between taste sensitivity to phenylthiocarbamide and anhedonia Justin Thomas n, Wahda Al-Mesaabi, Eman Bahusain, Meera Mutawa Department of Natural Science and Public Health, Zayed University, PO Box 144534, Abu Dhabi, United Arab Emirates
art ic l e i nf o
a b s t r a c t
Article history: Received 24 January 2013 Received in revised form 10 August 2013 Accepted 22 November 2013 Available online 4 December 2013
It has been proposed that taste sensitivity to bitter compounds such as, phenylthiocarbamide (PTC) and 6-n-propylthiouracil (PROP), represents a genetic marker for an increased vulnerability to depressive illness. Previous explorations of this idea have proven equivocal. This study refines and further explores this idea by focusing specifically on anhedonia (diminished hedonic capacity), a key symptom in some depressive illness, linked also with sensory pleasure. It is hypothesized that diminished PTC taste sensitivity will be associated with more general decrements in hedonic capacity (anhedonia). An opportunity sample of 198 university students were assessed using paper strips impregnated with PTC, the same participants also completed a widely used assessment of hedonic capacity, the SnaithHamilton Pleasure Scale (SHAPS). Hedonic capacity scores positively correlated with PTC taste sensitivity; specifically, heightened hedonic capacity was associated with heightened sensitivity to the bitter taste of PTC. Furthermore, modest differences were observed between those least (non-tasters) and most (supertasters) sensitive to PTC, with non-tasters reporting significantly lower hedonic capacity scores than supertasters. PTC taste sensitivity may represent a peripheral risk factor for anhedonia. & 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hedonic capacity PTC Genetic Depression
1. Introduction Genetic differences in taste sensitivity to bitter compounds were first reported in the 1930's (Fast et al., 2002; Blakeslee and Fox, 1932). Physiologically, these genetic differences manifest as varying densities of taste buds on the tongue, more specifically, varying densities of the fungiform papillae (Fast et al., 2002). Within the taste sensitivity literature individuals with the highest densities of fungiform papillae are generally referred to as “supertasters”, distinguishing them from “tasters” (an intermediate group) and “non-tasters”, those individuals with the lowest densities of fungiform papillae (Bartoshuk, 1993). Rather than examining fungiform papillae densities, taste status (whether one is supertaster, taster or non-taster) can also be reliably established by exploring individual taste sensitivity to bitter compounds such as phenylthiocarbamide (PTC) and 6-n-propylthiouracil (PROP). A typical testing protocol involves impregnating a strip of paper with a 3–5 micrograms of PTC, which individuals then place on their tongues. Supertasters have the highest sensitivity and lowest detection thresholds for PROP/PTC, and generally report the taste – even at low doses – as extremely bitter. Tasters and non-tasters have respectively higher detection thresholds and lower taste sensitivities, with non-tasters n
Corresponding author. E-mail address: [email protected] (J. Thomas).
0165-1781/$ - see front matter & 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2013.11.026
being the least sensitive of all (Reed et al., 1995; Tepper, 1998). Occasionally within the PTC/PROP taste-sensitivity literature a simpler bimodal, or dichotomous classification is used: taster vs. non-taster. In such cases no distinction is made between supertasters and tasters, both are simply categorized and referred to as tasters. Variations in PTC taste sensitivity are thought to influence dietary habits, and have therefore been associated an increased risk of developing health problems such as, cardiovascular diseases, obesity and some forms of cancer (Goldstein et al., 2005). A small number of studies have also attempted to explore the relationship between PTC taste sensitivity and psychological health. One of the earliest studies exploring this relationship used PTC sensitivity to establish taste status, and also administered a self-report inventory (Cattell′s 16PF) to assess personality traits amongst university students (Mascie-Taylor et al., 1983). The results suggested that tasters tended to be significantly more “tense” and “apprehensive”, compared with their non-taster counterparts. Based on this finding Whittemore (1986) hypothesized that tasters might be more vulnerable to depression. Exploring this idea in subsequent studies, using family history data and a small group of depressed patients, Whittemore reports longer and more severe depressive episodes for those with heightened taste sensitivity (tasters/supertasters), as well as higher rates of familial depressive illness (Whittemore, 1986, 1990). It should be noted,
J. Thomas et al. / Psychiatry Research 215 (2014) 444–447
that Whittemore′s study with depressed participants, relied on only 23 patients, all of them female. In a more recent examination of the relationship between depression and PTC/PROP taste sensitivity, Joiner and Perez (2004) proposed that supertaster status might actually provide a protective factor. They argue that heightened PTC/PROP taste sensitivity has been associated with greater aversion to alcohol (DiCarlo and Powers, 1998), and that heavy alcohol use is associated with depression (see Graham et al., 2007 for review). Based on this reasoning Joiner and Perez suggest that the supertaster′s greater aversion to the taste of alcohol might represent a protective factor against heavy alcohol use, thereby, indirectly reducing the risk of depression. Joiner and Perez also suggest that the heightened PTC/PROP taste sensitivity of supertasters may lead to them experiencing more intense pleasure in regards to taste, and perhaps by extension, in other sensory modalities too. This proposed heightened pleasure sensitivity – “hyper-hedonia” – is viewed as conferring protection against depressive illness. This is based on the observation that a diminished ability to experience pleasure – anhedonia – is a cardinal symptom of major depressive disorder (American Psychiatric Association, 2000) and has also been identified as a vulnerability marker for the disorder′s onset (Loas, 1996; Schrader, 1997; Shankman et al., 2010). Joiner and Perez (2004) explored these ideas using a family history methodology similar to those employed by Whittemore (1986). Healthy adults (N ¼ 42) were assessed and assigned to three taste-status groups (Whittmore′s studies had only two groups tasters and non-tasters). Participants were asked about depressive illness within their families, as hypothesized supertasters reported significantly lower rates of depressive illness amongst their 1st degree relatives, than tasters and non-tasters. The results support the idea of heightened PTC/PROP taste sensitivity representing some kind of protective factor in the context of depression. However, the study used a relatively small sample, and was reliant on retrospective self-reports of familial depressive illness. One explanation for the previously equivocal findings in relation to PTC/PROP taste sensitivity and depression (Whittemore, 1986, 1990; Joiner and Perez, 2004) is that depression (MDD) is a heterogeneous syndrome characterized by a wide variety of symptoms some of which are mutually exclusive, for example, weight loss/weight gain; hypersomnia/insomnia. If we suspect the link with depression is related to the symptom of diminished hedonic capacity (anhedonia), then it may prove more fruitful to focus specifically on this symptom. This would directly explore the idea that PTC/PROP taste sensitivity is associated with hedonic capacity, and as such, may reflect some kind of a vulnerability/ protective marker for depression. The present study follows-up on the idea of a link between PTC/PROP taste-sensitivity and hedonic capacity/anhedonia first proposed by Joiner and Perez (2004). However, rather than have participants retrospect about familial depressive illness, this study directly explores the relationship, assessing the hedonic capacity and PTC/PROP taste sensitivity of all participants. If such taste sensitivity reflects some kind of a vulnerability marker for anhedonia, then we might expect hedonic capacity scores to vary as a function of taste-status. To the best of our knowledge, this is the first study to explore the following hypotheses: H1. There will be a positive correlation between PTC taste sensitivity and hedonic capacity. H2. Individuals identified as non-tasters, will report significantly lower hedonic capacity scores than tasters and supertasters.
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2. Method 2.1. Participants Participants were an opportunity sample of 198 Emirati students taking general education courses at Zayed University in the UAE. Females were 60.1% of the sample, reflecting the institution′s gender ratios. The mean age was 22.05 (S.D.¼ 5.9); there were no significant gender differences for age. All participants were bilingual and spoke Arabic as their first language. 2.2. Measures 2.2.1. Snaith–Hamilton Pleasure Scale (Snaith et al., 1995) The SHAPs was translated into Arabic and independently back translated by bilingual masters-level faculty within Zayed University. The psychometric properties of this dual-language instrument has been favorably reported elsewhere (Thomas et al., 2012). The14-item scale assess anhedonia across 4 domains: interest/pastimes, social interaction, sensory experience, and food/drink. The following is an example item: – “I would get pleasure from helping others”. Items are scored from 1 to 4, with 1 anchored to the response “Strongly Disagree”, while a score of 4 is anchored to “Strongly Agree” etc. (Snaith et al., 1995). This scoring method means lower scores are indicative of greater anhedonia (diminished hedonic capacity). Previous psychometric explorations have reported acceptable internal consistency, 0.91 (Franken and Muris, 2007) and 0.86 (Leventhal et al., 2006) for the scale. Similarly, its convergent and discriminant validity, and its test re-test reliability have all, also yielded acceptable correlations (Leventhal et al., 2006; Franken and Muris, 2007). 2.2.2. The PTC taste test strips The test strips were pre-prepared by a commercial supplier, Precision Laboratories. Each strip of blotting paper was 5 cm in length and 0.5 cm in width and had been impregnated with 3–5 micrograms of phenylthiourea-phenylthiocarbamide. This method has become increasingly popular in the field (Tepper et al., 2001) and has been widely used to good effect in previous studies of PTC/PROP taste sensitivity (Intranuovo and Powers, 1998; Dicarlo and Powers, 1998; Reed et al., 1999; Prescott and Swain-Campbell, 2000). 2.3. Procedure Zayed University human subjects ethics committee approved the study. All participants gave informed consent, and were tested in classrooms in groups of approximately 15, over a 2-week period. Participants were tested at the end of class and had not consumed food or beverages for at least 1 h prior to testing. Participants first completed the SHAPS and then were each given PTC impregnated taste-test strips and a taste-rating sheet. The taste-rating sheet was a nine-point scale anchored at 0 with the phrase (in English and Arabic) “no taste at all” through to 9, with the phrase “tastes extremely bad/bitter”. 2.4. Statistical analysis After log transforming the skewed SHAPS scores, all continuous data met the assumptions for parametric statistical analysis. Pearson's product moment was used to conduct the bivariate correlational analysis based on a one-tailed hypothesis. The comparison of mean SHAPS scores between the three taste-status groups was undertaken using a univariate general linear model (ANCOVA) and a post hoc test. All analyses were undertaken using SPSS version 20.
3. Results The mean score on the SHAPS was 48.08 (S.D. ¼4.87); for males alone the mean was, 48.34(S.D. ¼4.85), and for females, 47.89 (S.D. ¼5.26). These gender differences were not statistically significant. Similarly no gender differences were observed for PTC taste sensitivity scores between females (M ¼6.48, S.D. ¼3.01) and males (M¼ 5.42, S.D. ¼ 3.44). Using Cronbach′s alpha, the internal reliability of the Arabic translation of SHAPs was acceptable: α¼0.78. Participants were categorized according to the tripartite system. Supertaster status was assigned if the participant reported a PTC taste sensitivity score of 7, 8, or 9. Taster status was assigned for scores of 4, 5, and 6, whereas non-tasters were defined as those reporting scores 1, 2 or 3. This method of assigning taste status
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based on a nine-point category response set is identical to that used by DiCarlo and Powers (1998). In their study the agreement between the nine-point scale, and an alternative form of tastestatus assessment (magnitude matching), reached 84%. In the current study, this nine-point scale method of taste status assignment resulted in 58.8% supertasters, 15.5% tasters and 25.7% non-tasters. The mean SHAPS (Anhedonia) scores for these groups were M¼48.88 (S.D. ¼4.52), M¼ 47.92 (S.D. ¼ 4.25) and M¼ 46.97 (S.D. ¼4.50) respectively. A univariate general linear model (ANCOVA) using SHAPs scores as the dependent variable, taste status as a fixed factor and controlling for gender as a covariate, revealed significant group differences: F(2,185) ¼5.40, p o0.01. As hypothesized, post hoc tests confirmed that non-tasters reported significantly lower ( p o0.05) hedonic capacity (SHAPS) scores than supertasters. 3.1. Correlational analysis As hypothesized, higher SHAPS scores were associated with higher PTC taste sensitivity scores. This relationship was statistically significant with a small effect-size; r ¼0.26, p o0.001. Neither PTC taste sensitivity nor SHAPS scores were correlated with age
4. Discussion Heightened PTC taste sensitivity was associated with higher hedonic capacity scores. The effect size of this finding was small, suggesting there are numerous other factors accounting for the variance in hedonic capacity scores. The finding that non-tasters had significantly lower hedonic capacity scores than supertasters is also modestly supportive of a link between PTC taste sensitivity and anhedonia. These findings support those of Joiner and Perez (2004), who found supertasters reported lower rates of depression amongst their first-degree relatives, a finding they speculated might be explicable in terms of heightened hedonic capacity conferring a protective factor against depressive illness. This hedonic capacity hypothesis might explain the previous equivocal findings with regard to PTC/PROP taste sensitivity and depression. It is possible that it may only be depression typified by anhedonia that shows any relationship with PTC/PROP taste sensitivity. For a diagnosis of major depressive disorder (MDD) the DSM-IV (American Psychiatric Association, 2000) requires the presence of either (a) dysphoria/sadness or (b) anhedonia. A study exploring the MDD symptom profiles exclusively associated with anhedonia, found anhedonic MDD to be occasioned by significantly higher degrees of appetite and weight loss. This was not the case for MDD primarily characterized by dysphoria. Similarly, the absence of anhedonia in MDD was significantly correlated with increased appetite and weight gain (Buckner et al., 2008). It is important to note however that the present study was an analog study, and clinical levels of depression or anhedonia were not explored. As such the present findings, at best, represent an initial exploration of a hypothesis with potentially important implications for understanding individual differences in depressive vulnerability. In contrast to other PTC/PROP taste sensitivity studies undertaken in western industrialized nations, the percentage of supertasters amongst the present Emirati sample was relatively high. However, PROP/PTC taste sensitivity in non-western populations has previously been found to vary widely. A cross-national review of over 370 taste sensitivity studies worldwide, reports that Australian Aborigines, Central Americans, North American Indians and Eskimos all demonstrated very different patterns of responsiveness to PTC/PROP compared with predominantly European or European American populations (Guo and Reed, 2001).
Of particular note in this regard are Australian Aborigines, with a non-taster rate of 49.7%. One proposed explanation for the nontaster preponderance amongst the Australian Aborigines is consanguineous marriage. Consanguineous marriage is relatively common within this population (Houseman, 1997) and less genetic heterogeneity may lead to a particular taste status becoming increasingly prevalent. Consanguineous marriage is also a longstanding tradition in the Arab world, a practice that has become increasingly common in the UAE over the past few decades, with consanguinity rates reportedly increasing from 39% to 50.5% in one generation (Tadmouri et al., 2009). The UAE′s relatively high rate of consanguineous marriage may explain the present study′s relative preponderance of supertasters. Both the high rate of Emirati supertasters, and the modest correlational between taste sensitivity and hedonic capacity, are worthy of further exploration. However, the present study has several important limitations that future studies may avoid. Firstly, the reliance on a single – self-report – assessment of hedonic capacity (SHAPS) somewhat reduces confidence in the findings. Despite having good internal reliability in the present study, SHAPS is a self-report measure that asks the individual to respond based on a retrospection of how they have felt over the previous few days. Robinson and Clore (2002) propose that the timeframe within which respondents are asked to consider their emotional state will influence whether semantic, or episodic knowledge retrieval strategies are used. They suggest retrospective
Fig. A1. Transformed distribution of SHAPS scores and Scatter plot of Shaps data alongside taste test scores.
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self-reports are more likely to draw on semantic knowledge, whereas online measures, those where participants are asked to report their feeling in the moment, or within the last few hours, are more likely to draw on episodic retrieval strategies. Future explorations of taste sensitivity and hedonic capacity may benefit from using multiple assessments of anhedonia, including those more specifically developed to assess the construct within clinical populations, as well as online measures, aiming to assess the construct in real-time. Such a broader attempt to capture this multidimensional construct, should also take into consideration the anticipatory (wanting) versus consummatory (liking) dichotomy of anhedonic states. Furthermore, despite claims that the SHAPS was designed to be unaffected by nationality (Snaith et al., 1995) at least one item required a slight rewording to fit the UAE context. In the item worded “I would find pleasure in small things, e. g. bright sunny day, a telephone call from a friend” it was deemed necessary to drop the “bright sunny day” phrase, especially since in the UAE rain is more likely to be viewed as pleasurable, and sunny day temperatures can reach upwards of 50 1C. A further limitation was the use of university students. Whilst this does not influence the generalizability of the taste test scores, it seriously limits the generalizability of the hedonic capacity scores. Future explorations of the relationship between PTC taste-sensitivity and anhedonia would greatly benefit from explorations within sizable clinical populations (including matched controls), particularly in the context of MDD characterized by anhedonia. Furthermore, if PTC test strips are used to assess taste-sensitivity to bitter compounds, then the introduction of a dummy strip (plain paper) might help identify and exclude false positives, thereby further strengthening the study design. In conclusion, this study (to the best of our knowledge) represents the first attempt to directly explore the relationship between PTC taste sensitivity and hedonic capacity. The findings suggest that there is a modest relationship between these two clinically relevant variables; further research with a clinical sample and matched controls is merited. Acknowledgments We are grateful to the Emirates Foundation for Philanthropy and the National Research Foundation for its support of this research project during 2011/13. Appendix A See Appendix Fig. A1 here. References American Psychiatric Association, 2000. DSM-IV-TR: Diagnostic and Statistical Manual of Mental Disorders, 4th ed., revised. American Psychiatric Press, Washington, DC. Bartoshuk, L., 1993. The biological basis of food perception and acceptance. Food Quality and Preference 4, 21–32. Blakeslee, A., Fox, A., 1932. Our different taste worlds. Journal of Heredity 23, 97–107.
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