Abstract
We investigated the effects of early experience on sweet and sour preferences in children. Eighty-three children were divided into four groups based on the type of formula fed during infancy and age. By using a forced-choice, sip-and-swallow procedure, we determined the level of sweetness and sourness preferred in juice. Children who were fed protein hydrolysate formulas, which have a distinctive sour and bitter taste and unpleasant odor, preferred higher levels of citric acid in juice when compared to older children who were fed similar formulas. No such difference was observed between the groups for sweet preference. However, the level of sweetness preferred in juice was related to the sugar content of the child's favorite cereal and whether the mother routinely added sugar to their foods. These data illustrate the wide variety of experiential factors that can influence flavor preferences during childhood.
Keywords: taste, early experience, hydrolysate formula, maternal behaviors, preferences
INTRODUCTION
In the biography on the life of his children, Charles Darwin (1877) astutely noted that children are living in different sensory worlds than adults. One century after these keen observations were made, the scientific investigation of taste preferences during human ontogeny began. This body of research has focused primarily, but not exclusively, on sweet tastes and has repeatedly demonstrated, as Darwin noted, the strong acceptance of sweet-tasting sugars during infancy and childhood (Desor, Green, & Maller, 1975a; Enns & Itallie, 1979; Maller & Desor, 1973; Nisbett & Gurwitz, 1970; Peiper, 1961/1963; Steiner, 1977), with preference levels decreasing to resemble that of the adult during late adolescence (Desor & Beauchamp, 1987).
The heightened preference for sweet taste during early development is universal and evident in children around the world (e.g., Brazil: Tomita, Nadanovsky, Vieira, & Lopes, 1999; France: Bellisle, Dartois, Kleinknecht, & Broyer, 1990; Iraq: Jamel, Sheiman, Watt, & Cowell, 1997; Israel: Steiner, 1977; Mexico: Vazquez, Pearson, & Beauchamp, 1982; Netherlands: De Graaf & Zandstra, 1999; North America: Beauchamp & Cowart, 1987; Desor et al., 1975a). However, individual variations do exists (Beauchamp & Moran, 1984; Enns &Itallie, 1979; Nilsson & Holm, 1983). Genetic variation (Bartoshuk, 2000; Drewnowski, Henderson, & Shore, 1997; Looy & Weingarten, 1992), as well as early experience (Beauchamp & Moran, 1982, 1984), play a role in establishing such individual differences. For example, children who were fed sweetened water during the first several months of life exhibited a greater preference for sweetened water at two years of age when compared to those who had little of no experience with sweetened water (Beauchamp & Moran, 1984). Through dietary experiences, children develop a sense of what foods should or should not taste sweet (Cowart & Beauchamp, 1986; Sullivan & Birch, 1990).
In comparison to sweet taste, much less is known about the ontogeny of sour taste preferences. Unlike the innate preference for sweet tastes (Desor, Maller, & Turner, 1977), newborns reject the sour taste of citric acid as evidenced by facial grimacing (Steiner, 1977) and reduced intake (Desor, Maller, & Andrews, 1975b). That experiences during infancy impact upon sour preferences during childhood is suggested by our recent study (Mennella & Beauchamp, 2002). In that study, we exploited the substantial flavor variation inherent in commercially available infant formulas—traditional milk-based formulas and those based on hydrolyzed proteins. Although each formula brand has its own characteristic flavor profile, milk-based formulas often are described as being slightly sweet and having “sour and cereal-type” aromas whereas protein hydrolysate formulas (e.g., Nutramigen, Alimentum) have an extremely unpalatable, offensive taste and “off” odor due primarily to its sourness and bitterness, perhaps because many amino acids taste sour or bitter (Cook & Sarett, 1982). When compared to children who had been fed milk-based formulas during their infancy, 4- to 5-year-old children who were fed protein hydrolysate formulas during the first year of life were significantly more likely to prefer sour-flavored (.04 M citric acid) apple juices and less likely to make negative facial responses during the taste tests. We suggest that the inherent variation in these two classes of formula provides a particularly apt model system to study the role of preweaning flavor experiences on later preference behaviors because these formulas differ profoundly in flavor and because exposure is frequent and repeated (Beauchamp & Mennella, 1998; Mennella & Beauchamp, 1996).
The present study was built upon these previous findings and was designed to determine whether early experience with hydrolysate formulas influences preferences for a wider range of sour-flavored (0–0.070 M citric acid) apple juices in 4- to 5-year-old as well as older aged (6- to 7-year-old) children. Preference for a range of sweetened apple juices also was assessed for two reasons. First, the addition of citric acid to apple juice not only enhances its sour taste but also suppress its sweetness (Schifferstein & Frijters, 1990). Therefore, heightened sour preferences may be secondary to diminished sweet preferences. Second, there have been reports in the literature that infants who are feeding, or have been fed, protein hydrolysate formulas have a reduced preference for sweet foods (MacDonald et al., 1994; Still et al., 1996.) As a first step in evaluating the role of maternal factors on children's flavor preferences, we also queried children and mothers individually about their habits and preferences.
SUBJECTS AND METHODS
Subjects
Mothers of 4- to 7-year-old children were recruited from advertisements in local newspapers. Four groups of children (N = 83; 42 girls, 41 boys) were formed based on their age (age groups: 4–5 years vs. 6–7 years) and early formula history (formula groups: milk formula vs. hydrolysate formula). There were no significant differences among the groups in the number of months that these children were fed formula during infancy, F(1, 79) = 2.19, p = .14. However, as expected, children in the hydrolysate group fed a milk- or soy-based formula during their first months (1.9 ± .4) of life and then, usually following their pediatrician's recommendation, were switched to hydrolysate until, on average, 11.8 (± .9) months of age. The vast majority of children in the hydrolysate group (83%) began this type of formula during the first 3 months of life. None of the children who were fed milk-based formulas were ever fed hydrolysate formulas.
All children were reported by their mothers to be healthy at the time of testing. Thirteen children were excluded because they could not understand the task. The procedures used in this study were approved by the Office of Regulatory Affairs at the University of Pennsylvania, and informed consent was obtained from each mother prior to testing.
Procedures
Children and their mothers were tested at the Monell Center on 2 days separated by 3.0 ± 0.5 days. Testing took place in a closed room specifically designed for sensory testing with a high air-turnover ventilation system. Each child sat at a small table designed for children. The mother, who was unaware of the hypothesis being tested, completed questionnaires about her child's feeding habits and preferences (discussed later) and sat approximately 2 ft behind the child, out of the child's view (see Mennella & Garcia, 2000). Mothers were asked to refrain from talking during the testing session, and replays of videotapes verified that they indeed did not talk during testing.
After the child acclimated to the room and personnel, we assessed the child's preference for sourness (0–0.070 M citric acid) during one test session and their preference for sweetness (.16–.93 M sucrose) during another. To this end, six solutions with different concentrations of citric acid (0, .007, .012, .022, .039, and .070 M) were made by dissolving citric acid (Sigma Chemical) in apple juice and six solutions which differed in sugar concentrations were made by either diluting the stock .34 M solution of apple juice (Mott's Inc., Stamford, CT) with water (.16 and .22 M) or by adding sucrose to the stock solution (.47, .66, and .93 M).
An age-appropriate, gamelike task that was fun for children and minimized the impact of language development were used to examine flavor preferences. Using a forced-choice procedure, each child was presented with all possible pairs of solutions (six solutions yield 15 possible pairs), one pair at a time, on each testing day. Ten ml of each stimuli were presented in identically colored opaque tumbler cups, containing a slit through which the child could sip its contents without seeing the color of the solution presented. The child was asked to taste each solution of the pair and to point to which of the pair he or she liked better. The order of presentation of the solutions was randomized within and between each pair. A 10-sec interval separated each pair of solutions, and a 5-min interval separated the tasting of the first eight pairs from the last seven pairs. During these intervals, children were offered a sip cup containing water and a small unsalted cracker to cleanse their palate.
Mothers completed a 10-item scale that measured their food neophobia, an 8-item scale that measured general neophobia (Pliner & Hobden, 1992), and a 25-item scale that measured temperament and food neophobia in their children (Pliner & Loewen, 1997). All but four of the mothers completed the temperament scales. They also were asked to indicate how often they added sugar to their child's diet and whether they perceived their child as a picky eater. Without communicating to the child, each mother was asked to write down their child's favorite cereals and candies. It should be noted that mothers completed this task before their child answered similar questions: “What is your favorite cereal (or candy) in the whole world?” and “Which cereal (or candy) do you ask your mom to buy the most?” All but four of the children were able to answer these questions. Mother–child agreement was 65% for the child's most favorite cereal and 54% for their favorite candy. The sugar content (g/100 g) of these cereals then was determined.
Statistical Analyses
Separate ANOVAs were conducted to determine whether there were significant differences between the groups on the age, body mass index (BMI: mass (kg)/height (m)2, and temperament scores of the children as well as the age and variety seeking (with regards to foods), and food and general neophobia scores of the mother. Least significant difference analyses were performed to investigate significant effects. Pearson chi-squares were performed to determine whether there were group differences in ethnicity, proportion of girls to boys, and the mothers’ habit of adding sugar to their children's diet (e.g., those who never vs. those who frequently added sugar to their child's diet).
To determine whether early experience was related to sour preferences, we determined the number of times (of 10) each child preferred the two most sour juices (.04 and .07 M citric acid) as “tasting better.” Please recall that our previous findings revealed that children who were fed hydrolysates were more likely to prefer sour apple juice (.04 M). Similarly, we also determined the number of times (of 15) that each child preferred the apple juices with added sugar (.47, .66, and .93 M sucrose). To determine whether there were significant differences in sweet and sour preferences between the groups, separate ANOVAs were conducted with age group (4–5 vs. 6–7 years) and formula history (milk vs. hydrolysate) as the between-subject variables. Finally, to determine whether preference for sweetness in juices was related to preference for sweetness in cereal, a multiple regression was performed between the average sugar concentration of the child's most favorite cereals and the number of times children preferred the apple juices with the added sugar. All summary statistics are expressed as means ± SEM.
RESULTS
Subject Characteristics
Salient characteristics of the four groups of children and their mothers are listed in Table 1. For those children who were 4 to 5 years of age, there was no significant difference between the formula groups (milk vs. hydrolysate) in their age: F(1, 37) = 1.26, p = 0.27, BMI (kg/m2): F(1, 37) = 0.51, p = 0.48, the proportion of girls to boys: χ2(1) = 0.02, p = 0.88, or the age of the mothers: F(1, 37) = 1.13, p = 0.30. Likewise, there were no significant differences between the formula groups for those who were 6 to 7 years of age on any of these measures, children's age: F(1, 41) = 0.07, p = 0.80, BMI: F(1, 41) = 0.18, p = 0.68, sex ratio: χ2(1) = 0.10, p = 0.76, or mothers’ age: F(1, 42) = 3.77, p = 0.06. However, the two formula groups did differ in their ethnicity, χ2(2) = 6.53, p < 0.04. That is, significantly more subjects in the hydrolysate group were Caucasian and less were African American (77% Caucasian, 17% African-American, 6% Other) when compared to those who were fed milk formulas (44% Caucasian, 52% African-American, 4% Other). However, there was no main effect of ethnicity on any of the outcome variables examined (ps > .05).
Table 1.
Group I |
Group 2 |
|||
---|---|---|---|---|
Characteristics | Milk-Based Formula | Hydrolysate Formula | ||
Age range (yr) | 4–5 | 6–7 | 4–5 | 6–7 |
Age (yr) | 5.5±0.1 | 6.8±0.1 | 5.4±0.1 | 6.9±0.1 |
Sex F/M | 11/10 | 14/13 | 9/9 | 8/9 |
Body Mass Index (kg/m2) | 16.6±0.6 | 16.1±0.6 | 16.7±0.5 | 17.2±0.5 |
Child temperament measuresa | ||||
Shynessb | 2.3±0.2 | 2.5±0.2c | 2.6±0.2 | 1.9±0.2 |
Emotionality | 2.9±0.2 | 2.7±0.2 | 2.9±0.2 | 3.1±0.2 |
Sociabilityb | 3.8±0.1 | 3.4±0.1c | 3.3±0.2 | 3.8±0.2d |
Negative reactions to food | 3.2±0.2 | 3.1±0.2 | 3.0±0.2 | 3.5±0.2 |
Activityb | 4.2±0.2 | 4.0±0.1c | 3.5±0.2 | 4.0±0.1 |
Percentage of mothers reporting That Their child is picky eater | 47.6 | 51.9 | 44.4 | 64.7 |
No. Mother–child pairs | 21 | 27 | 18 | 17 |
Measures ranged from 1–5; 1 = not at all characteristic of the child; 5 = very characteristic of the child. All summary statistics are expressed as mean ± SEM.
Significant age (4–5, 6–7 years) by formula (milk, hydrolysate) group interaction; p < 0.05.
Significantly different from 4–5 hydrolysate group.
Significantly different from 4–5 milk group.
With regards to child temperament measures, there were no significant interactions between age or formula-history groups on the children's negative reactions to foods, F(1, 76) = 1.98, p = .16, or emotionality, F(1, 79) = 1.02, p = .32, nor was there a significant difference in the percentage of mothers who reported that their child was a picky eater (Fisher's exact p = .36). However, there was a significant interaction between age and formula-history groups on children's shyness, F(1, 78) = 4.62, p < .05, sociability, F(1, 78) = 11.42, p < .01, and activity levels, F(1, 79) = 4.70, p < .05. Post hoc analyses revealed that 4- to 5-year-old children who were fed hydrolysate formulas were perceived by their mothers as being less social (p < .05) and less active (p < .05), and tended to be perceived as more shy (p = .05) when compared to 6- to 7-year-old children who were fed similar formulas. In contrast, younger aged children who were fed milk-based formulas were perceived by their mothers as being more social (p < 0.05) when compared to older aged children who were fed similar formulas. Further analyses of the children's temperament revealed no significant main effect of child's temperament on any of the outcome variables examined (ps > .05).
For mothers’ eating habits, there was no significant interaction between age and formula-history groups on the mothers’ variety-seeking behavior to foods: F(1, 78) = .02, p = .90, food neophobia: F(1, 76) = .03, p = .90, or general neophobia: F(1, 76) = 1.90, p = .17, as determined by questionnaires nor were there differences between the groups in the mothers’ habit of adding sugar (Fisher's exact p > .05) to their children's foods.
Effect of Early Experience and Age on Sour Preferences
As seen in Figure 1, there was a significant interaction between age group (4–5 vs. 6–7 years) and formula group (milk vs. hydrolysate) in the children's preference for the extreme sour juices, F(1, 79) = 4.91, p < .05. That is, children who were 4 to 5 years of age and fed hydrolysate formulas during their infancy preferred these sour juices significantly more than did older children who were fed similar formulas, F(1, 33) = 5.81, p < .05. No such age-related difference was observed in children who were fed milk-based formulas during infancy, F(1, 46) = .54, p = .50.
Effect of Early Experience and Age on Sweet Preferences
Unlike that observed for sour preference, there was no significant interaction between age group and formula group in their preference for sweetened juices, F(1, 79) = .10, p = .76 (Figure 2). That is, children of both age groups and early feeding history were significantly more likely to prefer the juices with added sugar (ps < .001). Moreover, there was no significant interaction between the groups in the sugar content of the children's favorite cereals, F(1, 75) = .63, p = .43, which was, on average, 30.6 + 1.5 g/100 g.
Because there were no significant differences of age or formula-history groups on the mothers’ habit of adding sugar to their child's foods, children were divided into two groups: those whose mothers reported that they never added sugar to their foods (n = 29) versus those whose mother did so on a routine basis (n = 51) to further investigate whether maternal behaviors are related to children's preferences. Table 2 reveals that children whose mothers reported adding sugar to their foods on a routine basis were significantly more likely to prefer apple juices with added sugar, F(1, 78) = 4.68, p < .05, and reported that they preferred a cereal with a significantly higher sugar content, F(1, 74) = 6.02, p <. 05, when compared to children whose parents reported that they never added sugar to their children's foods. The mothers who added sugar also were more likely to be African Americans, χ2(2) = 17.06, p < .0001, and were older in age, F(1, 78) = 11.03, p < .001, when compared to mothers who never added sugar to their child's diet.
Table 2.
Does Mother Add Sugar to Child's Food? |
||
---|---|---|
Frequently | Never | |
Children's age (yr) | 6.2±0.1 | 6.2±0.2 |
Ethnicity (%)a | ||
African American | 47% | 3.5% |
Caucasian | 47% | 93% |
Other | 6% | 3.5% |
Mother's age (yr) | 34.1±0.8 | 38.3±1.0b |
Children's Body Mass Index (kg/m2) | 16.3±0.4 | 17.0±0.4 |
No. times (of 15) that child preferred apple juices with added sugar | 9.6±0.32 | 8.4±0.47a |
Sugar content of favorite cereals (g/100g) | 32.9±1.7 | 25.2±2.8a |
No. mother–child pairs | 51 | 29 |
p < 0.05
p < 0.001.
DISCUSSION
This study expands upon our previous findings and demonstrates that the type of formula fed during infancy influences sour, but not sweet, preferences several years after the last exposure to the formula. However, these effects were only observed when children were 4 to 5 years of age. In other words, children who were fed protein hydrolysate formulas, which have distinctive sour and bitter tastes and unpleasant odors, preferred higher levels of citric acid in juice when compared to 6- to 7-year-old children who were fed hydrolysate formulas. Because there was no significant difference in sweet preference between the groups, the preference for the more sour juices (which also were less sweet) in the younger children does not appear to be due to a reduced sweet preference.
Why were the effects of early experience not seen in the older children? It is unlikely that the enhanced sour preference in the younger children was due to a poorer ability to perform the sensory tests. The pair-wise comparison test has been frequently used to determine preference and discriminatory ability in young children (Birch & Marlin, 1982; Kimmel, Sigman-Grant, & Guinard, 1994; Leon, Couronne, Marcuz, & Koster, 1999). Moreover, there were no age-related differences in the level of sweetness preferred, which was determined by procedures identical to those used for determining sour preferences.
We hypothesize that the observed shift in sour preference in those children who were fed hydrolysate during infancy was due to the older children's more expanded experience with foods and flavors (Nicklas, 1995) which, in turn, leads to learning the appropriate level and context of sour taste in different foods. On the other hand, we hypothesize that the heightened preference for sour tastes would persist with continued exposure to hydrolysate formula. Consistent with this hypothesis is the report that adolescent patients with phenylketonuria who were fed a type of protein hydrolysate formula (which is specifically treated with charcoal to remove most of the phenylalanine) throughout childhood and adolescence reported that one of their most preferred flavors, which was often added to the formulas, was lemon (Hogan, Gates, MacDonald, & Clark, 1986).
Because we did not randomly assign children to groups (parents decided which formulas they would feed their infants.), this was not a strict experimental study. Nonetheless, we attempted to match the groups as closely as possible to maximize the probability that any group differences were due only to differences in early formula-feeding experiences. Because there were no significant differences among the groups in the mothers’ variety-seeking scores or food-neophobia scores, the differences observed in the children's behavioral responses to the sour flavor were unlikely to bedue to the mothers’ eating habits or attitudes toward foods.
There were significant age-related differences with temperament. Four- to five-year-old children who were fed hydrolysate formulas were perceived by their mothers as being less social and less active when compared to 6- to 7-year-old children who were fed similar formulas. Despite the paucity of research on sour taste preference, a recent study on sweet taste preference suggested that young adults who scored high on arousability and pleasure gave higher intensity ratings to a sweet solution under mild stress conditions when compared to those who scored low on these temperament scores (Dess & Edelheit, 1998). However, despite the significant age-related differences in temperament observed in the present study, no significant main effect of child temperament was observed for any of the outcome variables.
Are mothers of young children who were on hydrolysate more likely to perceive their children differently? Of interest here is the finding that mothers who switched their children's formula during infancy because of feeding problems were more likely to perceive their 3.5-year-old children as more vulnerable several years after last exposure to the formula, despite no observed difference in the children's personalities or incidence of asthma or eczema (Forsyth & Canny, 1991). Recall that every mother in the hydrolysate group switched her child's formula during infancy. Forsyth and Canny (1991) suggested that the mere experience of changing formula during early infancy has long-term effects on mother–infant interaction and perceptions. Nevertheless, controlled experimental studies in which these formulas are introduced at differing ages and in which later preferences and temperament are determined by examining the child directly and not by maternal reports are needed for confirmation. Such studies are ongoing in our laboratories.
The findings from the present study also indicate that, at least for cereals, it is possible to relate sweet preference as measured in a laboratory setting to preferences for sweets in everyday foods such as cereals, as reported by the child. That experience influences sweet preferences is suggested by the finding that children whose mothers routinely added sugar to their diet preferred higher levels of sugar in apple juice and cereals when compared to children whose mothers reported never adding sugar. Such findings are consistent with previous research demonstrating that experience with sweetened water during infancy resulted in higher preferences for sweetened water at 2 years of age (Beauchamp & Moran, 1982, 1984) and that preference for sweet taste, as assessed by psychophysical methods, is related to carbohydrate intake in healthy adults (Mattes & Mela, 1986).
To be sure, mothers have an important influence on their children's diet (Fisher & Birch, 1999), such as the types of foods eaten (Klesges, Stein, Eck, Isbell, & Klesges, 1991) and frequency of exposure to sweet foods (Ritchey & Olson, 1983). However, these data underscore the importance of obtaining such information from the child directly because parents are not always reliable sources of this type of information. For example, mothers may be more accurate in identifying their child's favorite cereal when compared to candy because parents do most of the cereal purchasing. In conclusion, the findings of the present study illustrate the wide variety of experiential factors that can influence flavor preferences during childhood and highlight the importance of assessing children's preferences directly. The goal of our research program is to identify the early experiences that influence why we like the foods we do.
NOTES
We acknowledge the expert technical assistance of Brian Pollack, Saadia Khan, Mayla Henderson, and Lamoy Morgan. This work was supported by Grant HD37119 from the National Institute of Child Health and Human Development. The research reported in this article was completed as part of the first author's dissertation in the Department of Human Nutrition and Epidemiology, Wageningen University, The Netherlands.
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