Genetic Taste Sensitivity To Bitter And Children's Fussy Eating

Fussy eating is a common problem in childhood and is usually characterized by an inadequate diet variety due to rejection of specific familiar foods, new food items (food neophobia), or rejection of food textures [1]. Fussy eating (also called 'picky', 'selective', or 'choosy' eating) is associated with a limited intake of vegetables [2, 3], a high intake of sweets [3], and with both underweight [4] and overweight [5]. Given the impact of vegetable consumption and a normal weight development on health in childhood and adulthood (ref), a better understanding of factors that could affect children's fussy eating behavior is important.
Twin studies provided evidence for the heritability of fussy eating, food neophobia, and food preferences [6-8]. Dubois et al. proposed that genetic variation in taste perception, in particular biter tasting, might explain the strong heritability of food fussiness [7]. Large individual differences exists in the ability to taste bitter compounds, of which phenylthiocarbamide (PTC) and its chemical relative 6-n-propylthiouracil (PROP) are the most studied examples [6, 9]. Approximately 70% of Caucasians in the USA and Western Europe perceive these compounds as bitter and are so-called 'tasters', while the 30% 'non-tasters' are insensitive to the bitter taste of these compounds. Variation in PTC/PROP sensitivity has been strongly associated with variants of the TAS2R38 bitter receptor gene [10].
Sensitivity to the PROP bitter taste phenotype has been inversely related to enjoyment of bitter foods, and the acceptance and consumption of bitter-tasting vegetables, especially in laboratory research [6, 11]. Little is known about the contribution of the bitter taste genotype TAS2R38 and the PROP phenotype to children's fussy eating behavior. In a preliminary report from the ALSPAC study, PROP taster status was positively associated with children's food fussiness, which was repeatedly assessed with a single question asking the mother whether her child has been choosy with food since a certain age [12]. Another study, however, reported no association between PROP taster status and children's food neophobia, as assessed with the Food Neophobia Scale [13].
In this study, we aimed to enhance understanding whether differences in genetic variation in bitter taste perception contribute to children's fussy eating. Our objective was to determine the relation of both the TAS2R38 gene and a PROP taster test with children's fussy eating at the age of 4. We expected that children with the genotype or phenotype for bitter tasting are more likely to have fussy eating behavior.


Research question:
Is children's bitter sensitivity related to fussy eating?

Background:
The ability to taste the bitter substance 6-n-propylthiouracil (PROP) is inherited and has been strongly related to variants in the TAS2R38 gene. Genetic sensitivity to bitterness is associated with BMI as shown previously in Generation R (Bouthoorn et al., 2013), but questions remain regarding the underlying mechanisms. Eating behavior is an important factor in body weight, that might be affected by the ability to taste bitter. It has been shown that bitter sensitivity affects food intake, for example, it is associated with lower acceptance of some foods such as bitter-tasting vegetables in both adults and children (Wardle & Cooke, 2008). As lower acceptance of some foods is a characteristic of fussy eaters, genetic taste sensitivity to bitter might be related to food fussiness in children.

Hypothesis:
PROP tasters and carriers of the bitter-sensitive alleles of the TAS2R38 gene show more fussy eating.

Method:
Bitter sensitivity: DNA was isolated from the cord blood (N ?? 5500) and peripheral blood collected at the research center (N ?? 300). We used the A49P variant of the TAS2R38 gene (rs713598), which has been strongly associated with bitter sensitivity. Children were classified as Ala/Ala (AA) if they were homozygous for the bitter-insensitive allele. Children were classified as Ala/Pro (AP) if they were heterozygous for the bitter-insensitive allele. If children were homozygous for the bitter-sensitive allele, they were classified as Pro/Pro (PP). In addition, taste sensitivity to bitter was assessed when children were six years old by letting them taste PROP. Children were classified as 'non-bitter tasters' if they reported that the substance tasted like water or like nothing, and also if they indicated the substance tasted good. Children who reported that the substance taste bad, bitter, sour, yucky or spicy were classified as 'bitter-tasters'. Previous work in Generation R indicated that the ability to taste PROP was largely determined by differences in TASR38 genotype (Bouthoorn et al., 2013).

Fussy eating: Fussy eating was assessed with the Children's Eating Behaviour Questionnaire (CEBQ), when children were 4 years old (Wardle et al., 2001) using two different approaches:
1) Children's score on the CEBQ subscale food fussiness (FF, 6 items, e.g. 'my child decides that s/he doesn't like food, even without tasting it'). Each item was answered on a Likert-type scale with possible scores ranging from 1 (never) to 5 (always). A scale scores is calculated by summing the items if at least 75% of the items were completed. Higher scores indicate more food fussiness.
2) Fussy eater classification, which has been determined previously (Tharner et al., 2014) based on Latent Profile Analyses on five subscales of the CEBQ (2 food approach scales: food responsiveness, e.g. 'my child is always asking for food' and enjoyment of food, e.g. 'my child loves food'; and three food avoidance scales: satiety responsiveness, e.g. 'my child gets full up easily', slowness in eating, e.g. 'my child takes more than 30 minutes to finish a meal', and FF). Fussy eaters were characterized by high scores on the food avoidant scales and low scores on the food approach scales. The probability of being classified as a 'fussy eater' may also be used as a continuous variable to indicate degree of fussy eating.
Brief summary of the main findings:
Our hypothesis was not supported: both PROP-taster status and rs713598 genotype were unrelated to fussy eating. These findings suggest that fussy eating is a more complex phenomenon that is not simply determined by children's ability to taste bitter.

For more detail, see below.
1) Study sample.


2) Sample characteristics
Bitter sensitivity
rs713598 genotype AA N (% of valid) 1050 (32.7)
AP N (% of valid) 1607 (35.6)
PP N (% of valid) 554 (17.3)
Missing N (%) 1302 (28.8)
PROP-tasters N (% of valid) 2961 (78.0)
Missing N (%) 716 (15.9)

Fussy eating
At 4 years, sumscore mean (SD) 17.7 (4.94)
At 4 years, yes N (% of valid) 250 (5.6)

Family characteristics
Marital status, single N (% of valid) 424 (10.4)
Missing N (%) 446 (9.9)
Maternal education, primary N (% of valid) 234 (5.4)
Missing N (%) 182 (4.0)
Family income <2000'/month N (% of valid) 622 (16.1)
Missing N (%) 649 (14.4)
BMI mother at enrolment mean (SD) 23.3 (3.93)
Missing N (%) 1054 (23.4)
Age mother at intake, years mean (SD) 31.5 (4.57)
Missing N (%) 1 -
Maternal stress composite score (0-1) mean (SD) 0.14 (0.20)
Missing N (%) 1012 (22.4)

Child characteristics
Ethnicity, non-Western N (% of valid) 1201 (26.8)
Missing N (%) 29 (0.6)
Sex, boy N (% of valid) 2251 (49.9)
Missing N (%) 1 -
Firstborn N (% of valid) 2569 (56.9)
Missing N (%) 0 -
Cow's milk allergy N (% of valid) 248 (5.5)
Missing N (%) 483 (10.7)
Never breastfed N (% of valid) 326 (8.9)
Missing N (%) 843 (18.7)
Gestational age at birth, weeks mean (SD) 39.88 (1.76)
Missing N (%) 14 (0.3)
Weight at birth, grams mean (SD) 3451 (560)
Missing N (%) 3 -
BMI SD for age at 4 years mean (SD) 0.88 (0.95)
Missing N (%) 1626 (36.0)


3) Prop-taster status and RS713598 genotype

Table 3.1 PROP-taster status by bitter-sensitivity genotype
PROP-taster status
Genotype Non-Taster Taster Chi-Square (df) p
ALL
AA (bitter insensitive) 295 (82.6%) 256 (20.6%) 473,474 (2) .000
AP 51 (14.3%) 767 (61.7%)
PP 11 (3.1%) 221 (17.8%)

Caucasian
AA (bitter insensitive) 295 (82.6%) 256 (20.6%) 473.474 (2) .000
AP 51 (14.3%) 767 (61.7%)
PP 11 (3.1%) 221 (17.8%)
Non-Caucasian
AA (bitter insensitive) 129 (71.3%) 105 (15%) 233.106 (2) .000
AP 37 (20.4%) 407 (58.2%)
PP 15 (8.3%) 187 (26.8%)

Boy
AA (bitter insensitive) 222 (80.1%) 178 (18.8%) 366.656 (2) .000
AP 40 (14.4%) 572 (60.4%)
PP 15 (5.4%) 197 (20.8%)
Girl
AA (bitter insensitive) 206 (77.2%) 184 (18.3%) 343.857 (2) .000
AP 50 (18.7%) 609 (60.7%)
PP 11 (4.1%) 211 (21.0%)

' Children homozygous for the bitter-insensitive allele were classified as Ala/Ala (AA), children heterozygous for the bitter-insensitive allele as Ala/Pro (AP), and children homozygous for the bitter-sensitive allele as Pro/Pro (PP).

' Overall, 22% of children were PROP non-tasters. Of the non-tasters, 80% were homozygous for the bitter-insensitive allele. Only 3% of non-tasters were PP carriers. 80% of tasters carried at least one P allele. This corresponds to previous findings in Generation R (Bouthoorn et al., 2013).

' There were some slight differences in these proportions in Caucasians (82% of non-tasters were AA) and non-Caucasians (71% of non-tasters were AA) and between boys (80% of non-tasters were AA) and girls (77% of non-tasters were AA), but the overall picture remains the same in these subgroups.

'These findings are confirmed by results shown in Table 3.2: Children with either AP or PP genotype were much more likely to be PROP-tasters than non-tasters. The same was found for Caucasians and non-Caucasians examined separately and for boys and girls examined separately.
Table 3.2 Association between bitter-sensitivity genotype and PROP-taster status
PROP-taster status
Genotype N B (SE) OR (95% CI) p
ALL 2495
AA (bitter insensitive) ref 1 -
AP 2.742 (.131) 15.52 (12.01; 20.04) .000
PP 2.921 (.215) 18.55 (12.19; 28.25) .000

Caucasian 1601
AA (bitter insensitive) ref 1 -
AP 2.852 (.168) 17.33 (12.47; 24.09) .000
PP 3.142 (.321) 23.15 (12.35; 43.39) .000
Non-Caucasian 880
AA (bitter insensitive) ref 1 -
AP 2.604 (.216) 13.51 (8.85; 20.65) .000
PP 2.729 (.299) 15.32 (8.53; 27.51) .000

Boy 1224
AA (bitter insensitive) ref 1 -
AP 2.881 (.192) 17.84 (12.24; 25.99) .000
PP 2.796 (.286) 16.38 (9.35; 28.70) .000
Girl 1271
AA (bitter insensitive) ref 1 -
AP 2.613 (.179) 13.64 (9.61; 19.36) .000
PP 3.067 (.325) 21.48 (11.35; 40.64) .000

Note: results of logistic regression analyses, genotype was dummy coded.


4) Bitter sensitivity and fussy eating

Note: All models presented in section 4 were run with additional adjustments for child sex (only main effects models), child BMI at outcome, firstborn status, gestational age at birth, birth weight, maternal age, maternal educational level, marital status, family income, maternal smoking during pregnancy, maternal psychological stress. Missing covariates were imputed by multiple imputation techniques in SPSS version 21.00 (10 sets). As adjustments did not significantly change the effects estimates, unadjusted results from unimputed data are presented.

4.1) Bitter sensitivity and fussy eating full sample, adjusted for Caucasian genotype
Food fussiness
(z-score) Fussy eater classification
N B (SE) p N B (SE) OR (95% CI) p
ALL
Prop-taster (yes) 2480 -.010 (.050) .830 2467 -.369 (.206) .691 (.462; 1.034) .073
RS713598
Continuous coding (insensitive) 3192 -.022 (.027) .412 3177 .120 (.121) 1.127 (.889; 1.430) .323
No. bitter sensitive alleles 3192 .015 (.026) .551 3177 -.098 (.117) .906 (.720; 1.141) .403
Bitter sensitive 3192 .001 (.038) .977 3177 -.050 (.171) .951 (.680; 1.331) .770

Boys
Prop-taster (yes) 1217 -.058 (.073) .427 1213 -.505 (.274) .604 (.353; 1.032) .065
RS713598
Continuous coding (insensitive) 1607 -.012 (.039) .760 1600 .230 (.168) 1.258 (.906; 1.748) .171
No. bitter sensitive alleles 1607 .005 (.037) .901 1600 -.186 (.161) .830 (.605; 1.140) .250
Bitter sensitive 1607 -.002 (.055) .620 1600 -.136 (.231) .872 (.554; 1.373) .556

Girls
Prop-taster (yes) 1263 .043 (.068) .526 1254 -.201 (.315) .818 (.441; 1.516) .523
RS713598
Continuous coding (insensitive) 1585 -.034 (.037) .351 1576 -.007 (.176) .993 (.703; 1.403) .968
No. bitter sensitive alleles 1585 .029 (.036) .421 1576 .006 (.172) 1.006 (.718; 1.408) .974
Bitter sensitive 1585 .010 (.052) .959 1576 .058 (.256) 1.060 (.641; 1.752) .820
Note: Results of separate linear (food fussiness score) and logistic (fussy eater classification) analyses adjusted for Caucasian genotype. Interaction effects were calculated in models containing also the main effects. Continuous coding: higher codes represent more bitter insensitivity (A allele, positive strain); no. bitter sensitive alleles = number of P alleles coded as (0, 1, or 2; Bitter sensitive is coded as P-carriers (PA/PP) versus homozygous A (bitter insensitive). Interaction effects of Prop-taster and RS variables with child sex were also tested: all interactions were non-significant.

' Table 4.1 shows that there were no significant associations between PROP-taster status and RS713598 genotype with fussy eating at 4 years, also when boys and girls were examined separately. All child sex interactions were non-significant and are therefore not shown here.

' Some associations were almost significant, but in the unexpected direction, e.g. PROP-taster status was related to a lower risk of being a fussy eater, mainly in boys. However, considering the large number of tests, these findings are likely due to chance.

4.2) Bitter sensitivity and fussy eating in Caucasians
Caucasians
Food fussiness
(z-score) Fussy eater classification
N B (SE) p N B (SE) OR (95% CI) p
Prop-taster (yes) 1600 -.037 (.061) .547 1595 -.290 (.270) 0.75 (0.44; 1.27) .281
RS713598
Continuous coding (insensitive) 2051 .027 (.034) .426 2046 .318 (.173) 1.374 (.978; 1.930) .067
No. bitter sensitive alleles 2051 -.029 (.033) .374 2046 -.261 (.166) .770 (.556; 1.006) .115
Bitter sensitive (PA/PP) 2051 -.032 (.046) .485 2046 -.146 (.224) .846 (.557; 10341) .515

Interaction effects *gender
Prop-taster (yes) 1600 .025 (.031) .405 1595 .118 (.137) 1.125 (.860; 1.471) .391
RS713598
Continuous coding (insensitive) 2051 .011 (.034) .736 2045 -.097 (.174) .907 (.645; 1.275) .575
No. bitter sensitive alleles 2051 -.011 (.033) .735 2045 .073 (.166) 1.075 (.776; 1.489) .663
Bitter sensitive 2051 -.007 (.023) .768 2045 .102 (.113) 1.107 (.887; 1.382) .368
Note: Results of separate univariate linear (food fussiness score) and logistic (fussy eater classification) analyses. Interaction effects were calculated in models containing also the main effects. Continuous coding: higher codes represent more bitter insensitivity (A allele, positive strain); no. bitter sensitive alleles = number of P alleles coded as (0, 1, or 2; Bitter sensitive is coded as P-carriers (PA/PP) versus homozygous A (bitter insensitive).

4.3) Bitter sensitivity and fussy eating in Non-Caucasians
Non-Caucasians
Food fussiness
(z-score) Fussy eater classification
N B (SE) p N B (SE) OR (95% CI) p
Prop-taster (yes) 880 .042 (.085) .620 872 -.483 (.318) .617 (.330; 1.151) .129
RS713598
Continuous coding (insensitive) 1141 -.101 (.044) .021 1131 -.084 (.173) .920 (.655; 1.129) .629
No. bitter sensitive alleles 1141 .089 (.043) .037 1131 .075 (.169) 1.078 (.774; 1.502) .655
Bitter sensitive (PA/PP) 1141 .069 (.067) .302 1131 .083 (.269) 1.087 (.641; 1.843) .757

Interaction effects *gender
Prop-taster (yes) 880 .023 (.042) .582 872 .009 (.162) 1.009 (.734; 1.386) .957
RS713598
Continuous coding (insensitive) 1141 -.043 (.044) .328 1131 -.145 (.174) .865 (.614; 1.216) .404
No. bitter sensitive alleles 1141 .047 (.043) .274 1131 .127 (.170) 1.135 (.813; 1.584) .457
Bitter sensitive 1141 .022 (.034) .502 1131 -.023 (.135) .977 (.750; 1.274) .864
Note: Results of separate univariate linear (food fussiness score) and logistic (fussy eater classification) analyses. Interaction effects were calculated in models containing also the main effects. Continuous coding: higher codes represent more bitter insensitivity (A allele, positive strain); no. bitter sensitive alleles = number of P alleles coded as (0, 1, or 2; Bitter sensitive is coded as P-carriers (PA/PP) versus homozygous A (bitter insensitive).


' As RS713598 genotype coding is based on Caucasians only. Therefore, Caucasians and Non-Caucasians were examined separately in Tables 4.2 and 4.3.

' For Caucasians, results were similar to the findings presented in Table 4.1: there was not association of PROP-taster status and RS713598 genotype with fussy eating.

' In the non-Caucasians, however, we found an association between genotype and food fussiness: Children who carried more bitter sensitive alleles had higher scores on food fussiness. However, this finding was not supported by PROP-taster status (the functional bitter tasting). Also, genotype coding is based on Caucasians, which may cast doubt on the reliability of the codings in the non-Caucasian group. Also, this group is heterogeneous comprised of children with Mediterranean, African, and Asian origins. Thus, the interpretation of these findings needs to be further discussed.


5) Fussy eating and participation in the PROP-test.
Participation in PROP-test
N B (SE) OR (95% CI) p
ALL
Food Fussiness (z-score) 4214 .081 (.051) 1.084 (.981; 1.198) .113
Fussy eater (yes) 4192 .272 (.202) 1.312 (.883; 1.951) .179

Boys
Food Fussiness (z-score) 2094 .071 (.066) 1.074 (.944; 1.222) .280
Fussy eater (yes) 2086 .203 (.263) 1.225 (.731; 2.051) .441

Girls
Food Fussiness (z-score) 2120 .071(.080) 1.074 (.918; 1.255) .373
Fussy eater (yes) 2106 .328 (.317) 1.388 (.745; 2.584) .301

' Finally, we tested whether fussy eating was related to participation in the PROP-test, to make sure that the lack of associations between bitter sensitivity and fussy eating cannot be explained by selective non-participation of fussy eaters in the PROP-test (e.g. fussy eaters might be expected to refuse to try the PROP-liquid). This was not the case, as Table 5 shows: there was no association between fussy eating and participation in the PROP-test.

References
1. Dovey, T.M., et al., Food neophobia and 'picky/fussy'eating in children: A review. Appetite, 2008. 50(2): p. 181-193.
2. Galloway, A.T., et al., Parental pressure, dietary patterns, and weight status among girls who are 'picky eaters'. Journal of the American Dietetic Association, 2005. 105(4): p. 541-548.
3. Tharner, A., et al., Toward an operative diagnosis of fussy/picky eating: a latent profile approach in a population-based cohort. International Journal of Behavioral Nutrition and Physical Activity, 2014. 11(1): p. 14.
4. Dubois, L., et al., Problem eating behaviors related to social factors and body weight in preschool children: A longitudinal study. International Journal of Behavioral Nutrition and Physical Activity, 2007. 4(1): p. 9.
5. Finistrella, V., et al., Cross-sectional exploration of maternal reports of food neophobia and pickiness in preschooler-mother dyads. Journal of the American College of Nutrition, 2012. 31(3): p. 152-159.
6. Wardle, J. and L. Cooke, Genetic and environmental determinants of children's food preferences. British Journal of Nutrition, 2008. 99(S1): p. S15-S21.
7. Dubois, L., et al., Genetic and environmental influences on eating behaviors in 2.5-and 9-year-old children: a longitudinal twin study. International Journal of Behavioral Nutrition and Physical Activity, 2013. 10(1): p. 134.
8. Fildes, A., et al., Nature and nurture in children's food preferences. The American Journal of Clinical Nutrition, 2014: p. ajcn. 077867.
9. Tepper, B.J., et al., Genetic Variation in Taste Sensitivity to 6'n'Propylthiouracil and Its Relationship to Taste Perception and Food Selection. Annals of the New York Academy of Sciences, 2009. 1170(1): p. 126-139.
10. Kim, U.-k., et al., Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science, 2003. 299(5610): p. 1221-1225.
11. Gahagan, S., The Development of Eating Behavior-Biology and Context. Journal of developmental and behavioral pediatrics: JDBP, 2012. 33(3): p. 261.
12. Golding, J., et al., Associations between the Ability to Detect a Bitter Taste, Dietary Behavior, and Growth. Annals of the New York Academy of Sciences, 2009. 1170(1): p. 553-557.
13. Bajec, M.R. and G.J. Pickering, Association of thermal taste and PROP responsiveness with food liking, neophobia, body mass index, and waist circumference. Food quality and preference, 2010. 21(6): p. 589-601.

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