Abstract
OBJECTIVE:
To identify predictors of eating in the absence of hunger (EAH) in low-income toddlers, describe affect during EAH, test EAH as a predictor of body mass index (BMI), and examine the type of food eaten as a predictor of BMI.
METHODS:
EAH, indexed as kilocalories (sweet, salty, and total) of palatable foods consumed after a satiating meal, was measured (n = 209) at ages 21, 27, and 33 months. Child gender, age, race/ethnicity, and previous exposure to the foods; maternal education and depressive symptoms; and family chaos, food insecurity, and structure were obtained via questionnaire. Child and mother BMI were measured. Child affect was coded from videotape. Linear regression was used to examine predictors of EAH and the association of kilocalories consumed and affect with 33 month BMI z-score (BMIz).
RESULTS:
Predictors of greater total kilocalories included the child being a boy (P < .01), being older (P < .001), and greater maternal education (P < .01). Being in the the top quartile of sweet kilocalories consumed at 27 months and showing negative affect at food removal had higher BMIz (β = 0.29 [95% confidence interval 0.10 to 0.48] and β = 0.34 [95% confidence interval, 0.12 to 0.56], respectively).There was no association of salty kilocalories consumed or positive affect with BMIz.
CONCLUSIONS:
There was little evidence that maternal or family characteristics contribute to EAH. EAH for sweet food predicts higher BMIz in toddlerhood. Studies investigating the etiology of EAH and interventions to reduce EAH in early childhood are needed.
What’s Known on This Subject:
Eating in the absence of hunger (EAH) is a measurable, genetically linked behavior that is associated with overweight in children ages 3 to 13 years. Previous work has shown the potential for behavioral intervention.
What This Study Adds:
EAH occurs in toddlers. Consumption of sweet, but not salty, foods increases across toddlerhood during EAH, and greater EAH predicts greater adiposity at age 33 months.
Eating behaviors, including greater food responsiveness, greater food enjoyment, less satiety responsiveness, lesser capacity to voluntarily inhibit eating, greater impulsivity, and lesser self-control have been linked with greater obesity risk and have been the topic of substantial investigation.1 The continued consumption of foods past satiety, referred to as eating in the absence of hunger (EAH),2 is correlated with greater food responsiveness and enjoyment, and less satiety responsiveness,3 as well as greater adiposity.4–15 Interventions that reduce responsiveness to food cues16–18 have been shown to reduce EAH, but interventions that increase children’s awareness of hunger and satiety cues had no effect.16 Thus, EAH may primarily reflect food enjoyment and responsiveness as opposed to sensitivity to hunger and satiety cues.
There are a number of gaps in the existing literature. First, we have been unable to identify any studies of EAH that have focused on low-income children, who are at particularly high risk for childhood obesity19 or children younger than age 3 years. Second, though some studies have examined the stability or change in EAH with age,5,6,9–11,15 none have done so in children younger than 4 years. Third, studies examining maternal and family characteristics as predictors of child EAH2,4,5,7–11, 14,20–23 have been in predominantly white cohorts with the exception of 1 study that examined only Hispanic children.8 Fourth, children exhibit a liking for sweet taste even in the newborn period,24,25 but whether the association between EAH and adiposity differs based on the type of food eaten in the absence of hunger has not been described. In addition, most studies on early childhood2,4–15,20–22, 26,27 examine only the amount consumed as an outcome; we have been unable to find any studies that have also examined children’s affect during the EAH protocol and how this affect may be associated with child adiposity. We posit that affect during the EAH protocol reflects food enjoyment and responsiveness, each of which have been correlated with kilocalories consumed during EAH3 and greater adiposity in older children.28
Therefore, within a diverse cohort of low-income children followed longitudinally at ages 21, 27, and 33 months, we sought to address 4 objectives: (1) to examine child, maternal, and family characteristics predictive of EAH across toddlerhood; (2) to describe child affect during EAH; (3) to test the prospective association of EAH with BMI z-score (BMIz) at age 33 months; and (4) to examine the type of food eaten and the association with BMIz.
Methods
Participants and Recruitment
Participants were recruited via flyers posted in community agencies serving low-income families between 2011 and 2014. The study was described as examining whether children with different levels of stress eat differently. Inclusion criteria were that the biological mother was the legal guardian, had an education level less than a 4-year college degree, and was at least 18 years old; the family was eligible for Head Start, the Women Infant and Children Program, or Medicaid and was English-speaking; and the child was between 21 and 27 months old, was born at a gestational age ≥36 weeks, and had no food allergies or significant health problems, perinatal or neonatal complications, or developmental delays. Mothers provided written informed consent. The University of Michigan institutional review board approved the study.
Mother–child dyads were invited to participate in 3 data collections at ages 21, 27, and 33 months; the data collection procedures at each age spanned across 5 days and included measures regarding eating behavior and biobehavioral self-regulation. A total of 244 dyads participated. Most (n = 186) dyads entered the study when the child was age 21 months, but 58 entered the study when the child was age 27 months to maximize recruitment; measures obtained at study entry are henceforth referred to as “baseline” measures. This report is limited to children who participated in at least 1 EAH protocol (scheduled to be obtained on the fifth day of data collection at each age) and one anthropometric measurement (scheduled to be obtained on the first day of data collection at each age). A total of 209 of the 244 participants participated in the EAH protocol at a minimum of 1 age point at which they also provided anthropometry. The 209 participants included in this analysis did not differ from the excluded participants with regard to child gender, child age, maternal BMI, maternal education, maternal depression, family chaos, food security, or family structure. Of the children with complete data included in this report, 47.4% were non-Hispanic white compared with 25.7% of those not included (P = .02). A total of 52 children (24.9%) participated at only 1 age point, 85 (40.7%) participated at only 2 age points, and 72 (34.4%) participated at all 3 age points. Mother–child dyads who participated at 2 or 3 age points did not differ at baseline from those who participated at only 1 age point with regard to child gender, child age, child race/ethnicity, maternal BMI, maternal education, maternal depressive symptoms, food security, or family structure. Those in the sample who participated at 2 or 3 age points, compared with those who participated at only 1, were more likely to report higher family chaos (Confusion, Hubbub, and Order Scale [CHAOS] score, 4.3 [SD, 3.3] vs 3.1 [SD, 3.0] [P = .03]).
EAH Protocol
Mother–child dyads were invited to participate in a standardized protocol2 to assess the child’s EAH at ages 21, 27, and 33 months in the child’s home. The mother was asked to have the child fast for 1 hour and then serve the child a typical lunch that included at least 2 different foods and 1 drink.
After the lunch ended, a research assistant presented a standardized plate of foods (Table 1) and told the child, “Here are some special treats you can eat.” Mothers reported how often the child had eaten the food in the past 4 weeks (Table 1). To reduce food neophobia,29 the experimenter ate 1 Oreo cookie off of the plate and said, “I'm going to have one, too. Mmm, this is really good. You can eat as much as you want.” The child was given free access to the food. The mother was asked not to interact with the child during the protocol. After 10 minutes, the plate of food was removed. The remaining food was weighed and the amount consumed was calculated.
TABLE 1.
Foods Presented in EAH
| Food | Serving | Weight (gm) per Serving, Mean (SD) | Kilocalories per Serving, Mean (SD) | Frequency of Eating in Last 4 wka, Mean (SD) | ||
|---|---|---|---|---|---|---|
| 21 mo | 27 mo | 33 mo | ||||
| Sweet foods | ||||||
| Nabisco Original Chips Ahoy chocolate chip cookies | 2 cookies | 22.0 (0.7) | 106.4 (3.5) | 1.0 (1.1) | 1.0 (1.1) | 0.7 (0.7) |
| Nabisco Original Oreo cookies | 2 cookies | 23.2 (0.8) | 109.3 (3.9) | 1.0 (1.0) | 0.9 (0.9) | 0.8 (0.7) |
| Keebler Animal Cookies, Frosted | 5 cookies | 19.0 (1.5) | 97.9 (7.0.8) | 0.2 (0.7) | 0.2 (0.5) | 0.2 (0.5) |
| Nabisco Rainbow Candy Blast Chips Ahoy cookies | 2 cookies | 33.4 (1.2) | 176.8 (6.4) | 0.1 (0.4) | 0.2 (0.5) | 0.2 (0.4) |
| Kellogg’s Keebler Fudge Stripe chocolate-coated cookies | 2 cookies | 23.6 (3.4) | 122.1 (17.7) | 0.2 (0.5) | 0.2 (0.4) | 0.2 (0.5) |
| Salty Foods | ||||||
| Pringles potato chips | 10 chips | 18.2 (0.7)) | 97.6 (3.6) | 1.6 (1.2) | 1.7 (1.2) | 1.6 (1.1) |
| Frito-Lay Cheetos cheese puffs | 10 puffs | 20.3 (3.3) | 108.8 (17.5) | 1.0 (1.3) | 1.1 (1.1) | 0.8 (1.0) |
Response options: 0 = never; 1 = 1to 3 times in the past 4 weeks; 2 = 1 time per week; 3 = 2 to 4 times per week; 4 = 5 to 6 times per week; 5 = 1 time per day; 6 = 2 to 3 times per day; 7 = 4 to 5 times per day; 8 = >6 times per day.
Affect was coded from video on a scale from 0 (none) to 2 (high intensity). Positive affect was coded for the 10 seconds during which the research assistant was delivering the plate to the child and the 40 seconds after plate presentation. Negative affect was coded for the 10 seconds during which the research assistant was moving to remove the plate from the child and the 10 seconds after plate removal. Inter-rater reliability was high (Cohen’s κ > 0.80). A child whose positive affect was >0 after plate presentation was categorized as having “positive affect at food presentation.” A child whose negative affect was >0 after plate removal was categorized as having “negative affect at food removal.”
Anthropometry
Weight, length, and height of the child were measured by trained research staff. Weight-for-length z-score (WLZ) and BMIz were calculated based on the US Centers for Disease Control and Prevention growth charts.30 Mothers’ weight and height were measured and BMI calculated.
Questionnaires
Mothers reported child gender, birth date, and race and ethnicity; for this analysis, child race/ethnicity was categorized as non-Hispanic white versus not. Mothers reported maternal education (more than a high school diploma versus not), and family structure (single mother versus not). The Center for Epidemiologic Studies-Depression scale is a valid, reliable 20-item questionnaire31 designed to measure depressive symptoms. Mothers respond to a scale ranging from 0 (rarely or none of the time) to 3 (most or all of the time), and responses are summed so that a higher score indicates more symptoms (range, 0–60). CHAOS32 consists of 15 statements (true = 1, false = 0) that are designed to assess chaos in the home environment; scores range from 0 to 15, with higher scores reflecting more chaos. The US Department of Agriculture 18-item Household Food Security Survey33 categorizes households as food secure versus not.
Statistical Analysis
Analyses were conducted by using SAS 9.4 (SAS Institute, Inc, Cary, NC). Univariate statistics were used to describe the sample. Bivariate analyses were conducted by using t tests and χ2 tests. One-way repeated measure ANOVAs were used to test whether total, sweet, and salty calorie consumption differed across 21, 27, and 33 months. Cochran Q tests were used to test whether positive affect at food presentation and negative affect at food removal differed across 21, 27, and 33 months. If ANOVA or Cochran Q test results were significant (P < .05), then post hoc comparisons were conducted using paired t tests or McNemar tests.
Generalized estimating equations, using all available cases, were used to predict calories consumed, positive affect at food presentation, and negative affect at food removal, accounting for repeated measures within subjects. Predictor variables were added in 3 steps: child characteristics (gender, age, race/ethnicity, and previous exposure to the EAH foods), maternal characteristics (BMI, education, and depressive symptoms); and family characteristics (household chaos, food security, and family structure). Child age, maternal BMI, depressive symptoms, and family structure were time varying covariates. At each step, variables that were statistically significant (P < .05) were retained and 95% confidence intervals were calculated. For binary variables, parameter estimates were converted to odds ratios.
Five multivariate linear regression models were used to predict child BMIz at 33 months from kilocalories consumed (total, sweet, and salty), positive affect at food presentation, and negative affect at food removal. To ease interpretation and given preliminary models suggesting that the relationship was nonlinear, we categorized kilocalories consumed into quartiles and compared the top quartile to the bottom 3 quartiles. The top quartiles at age 21 months were ≥114.3 kcal total, ≥84.1 kcal sweet, and ≥40.8 kcal salty. The top quartiles at age 27 months were ≥147.7 kcal total, ≥122.5 kcal sweet, and ≥46.2 kcal salty. These 5 models were fitted for predictors measured at age 21 months and again for predictors measured at age 27 months. Each model was adjusted for child gender, child race/ethnicity, maternal education, maternal BMI, food insecurity, and baseline child WLZ. These models followed the maximum likelihood (ML) approach, which produces valid estimates when missing data are missing at random.
Results
Characteristics of the sample are shown in Table 2. The sample was 51.2% boys, 51.2% white, 25.8% black, and 11.0% Hispanic. The mean WLZ at study entry was 0.51 (SD 1.06). Among the mothers, 38.3% had an education level of a high school diploma or less. The sample size of participants contributing to analyses at each age is shown in Table 3. Amount of food consumed and affect during EAH are shown in Table 4 across ages. Total kilocalories consumed increased with age (P < .001). When examined separately by food type (sweet vs salty), there were only significant increases in the amount of sweet food, but not salty food, consumed. Positive affect at food presentation also increased with age (P = .004). Negative affect at food removal did not change with age.
TABLE 2.
Characteristics of the Sample at Baseline (Study Entry at Either Age 21 or 27 mo; n = 209)
| Variable | N (%) or Mean (SD) |
|---|---|
| Child | |
| Gender | |
| Girls | 102 (48.8%) |
| Boys | 107 (51.2%) |
| Race/Ethnicity | |
| White | 107 (51.2%) |
| Black | 54 (25.8%) |
| American Indian or Alaskan Native | 0 (0.0%) |
| Asian or Pacific Islander | 0 (0.0%) |
| Biracial | 44 (21.1%) |
| Other | 3 (1.4%) |
| Unknown | 1 (0.5%) |
| Ethnicity | |
| Hispanic | 23 (11.0%) |
| Not Hispanic | 185 (88.5%) |
| Unknown | 1 (0.5%) |
| WLZ (CDC norms) | 0.51 (1.06) |
| Maternal | |
| BMI (kg/m2) | 32.0 (9.5) |
| Education | |
| High school or less | 80 (38.3%) |
| More than high school | 129 (61.7%) |
| CES-D score | 12.5 (10.0) |
| Family | |
| CHAOS score | 4.1 (3.3) |
| Food insecurity | |
| Food insecure | 65 (33.9%) |
| Food secure | 127 (66.1%) |
| Family Structure | |
| Single mother | 46 (23.2%) |
| Not single mother | 152 (76.8%) |
CES-D, Center for Epidemiologic Studies-Depression scale.
TABLE 3.
Sample Size Contributing to Analysis at Each Age
| 21 mo | 27 mo | 33 mo | Only 21 mo | Only 27 mo | Only 33 mo | Only 21 and 27 mo | Only 27 and 33 mo | Only 21 and 33 mo | Complete for 21, 27, and 33 mo | Any time point | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Entered study at 21 mo and had complete anthropometry and EAH kcal consumed | 143 | 111 | 94 | 38 | 4 | 3 | 27 | 12 | 11 | 68 | 163 |
| Entered study at 27 mo and had complete anthropometry and EAH kcal consumed | N/A | 43 | 38 | N/A | 8 | 3 | N/A | 35 | N/A | N/A | 46 |
| Total participants (entered study at either 21 or 27 mo) with complete anthropometry and EAH kcal consumed | 143 | 154 | 132 | 38 | 12 | 6 | 27 | 47 | 11 | 68 | 209 |
TABLE 4.
Food Consumed and Affect During EAH Across Age
| Variable | Age | P | ||
|---|---|---|---|---|
| 21 mo (n = 143) | 27 mo (n = 154) | 33 mo (n = 132) | ||
| Kilocalories consumed, mean (SD) | ||||
| Total | 87.3 (50.4)a | 105.4 (65.7)b | 122.6 (72.0)c | <.001 |
| Sweet | 57.6 (52.4)a | 74.4 (60.8)b | 89.5 (69.8)b | <.001 |
| Salty | 29.7 (24.6) | 30.5 (28.4) | 33.1 (32.3) | .30 |
| Affect display, N (%) | ||||
| Positive at food presentation | 96 (67%)a | 124 (81%)b | 116 (88%)b | .004 |
| Negative at food removal | 28 (20%)a | 31 (20%)a | 20 (15%)a | .62 |
Superscript letters that differ within a row indicate the means or proportions are significantly different between 2 ages.
Table 5 shows results of the multivariate models testing predictors of EAH. Being a boy, older child age, and more maternal education each predicted more kilocalories consumed. Being a boy and older child age each predicted more kilocalories of sweet food consumed. Older child age and food insecurity predicted display of positive affect at plate presentation. None of the child, maternal, or family characteristics predicted kilocalories of salty food consumed or the display of negative affect at food removal.
TABLE 5.
Child, Maternal, and Family Characteristics Predicting EAH Kilocalories Consumed and Affect Displays (n = 209)
| Predictor Variables | Food Consumed Variables | Behavior Variables | |||
|---|---|---|---|---|---|
| kcal Total β (95% CI) | kcal Sweet β (95% CI) | kcal Salty β (95% CI) | Positive Affect at Food Presentation OR (95% CI) | Negative Affect at Food Removal OR (95% CI) | |
| Child | |||||
| Girls vs boys | −21.7 (−35.3 to −8.1)* | −19.2 (−32.9 to −5.5)* | — | — | — |
| Age (mo) | 2.9 (1.8 to 3.9)* | 2.7 (1.6 to 3.7)* | — | 1.12 (1.06 to 1.17)* | — |
| Hispanic or not white vs non-Hispanic white | — | — | — | — | — |
| Frequency of eating in last 4 wk | — | — | — | 0.54 (0.34 to 0.88)* | — |
| Maternal | |||||
| BMI | — | — | — | — | — |
| High school or less versus more than high school | −19.5 (−33.1 to −6.0)* | — | — | — | — |
| Depressive symptoms | — | — | — | — | — |
| Family | |||||
| CHAOS Score | — | — | — | — | — |
| Food Insecure versus not | — | — | — | — | — |
| Single mother versus not | — | — | — | — | — |
Predictor variables were added in 3 steps: child characteristics, maternal characteristics; and family characteristics. At each step, only variables that were statistically significant (P < .05) were retained in the model. The dashes indicate that the variable was not statistically significant and was therefore not retained in the model. CI, confidence interval; OR, odds ratio.
P < .05
Results of the multivariate models predicting BMIz at 33 months are shown in Table 6. Neither kilocalories consumed nor affect at 21 months predicted 33-month BMIz. Both kilocalories of total and sweet food consumed at 27 months predicted greater 33 month BMIz. Kilocalories of salty food consumed at 27 months was not associated with 33 month BMIz. Showing negative affect at food removal at 27 months was associated with higher 33 month BMIz. Positive affect at plate presentation at 27 months was not associated with 33 month BMIz.
TABLE 6.
EAH Food Consumed and Behavior by Age Predicting BMIz at 33 Months
| Age | Primary Predictor | Sample Size | 33 mo BMIze β (95% CI) |
|---|---|---|---|
| 21 mo | Kilocalories consumed (top quartile vs not) | ||
| Total | 89 | 0.17 (−0.10 to 0.45) | |
| Sweet | 89 | 0.24 (−0.04 to 0.52) | |
| Salty | 91 | 0.02 (−0.23 to 0.27) | |
| Affect Display | |||
| Positive at food presentation (vs not) | 91 | −0.16 (−0.40 to 0.08) | |
| Negative at food removal (vs not) | 91 | −0.04 (−0.34 to 0.25) | |
| 27 mo | Kilocalories consumed (top quartile vs not) | ||
| Total | 104 | 0.21 (0.01 to 0.40)* | |
| Sweet | 104 | 0.29 (0.10 to 0.48)** | |
| Salty | 105 | −0.09 (−0.30 to 0.12) | |
| Affect Display | |||
| Positive at food presentation (vs not) | 105 | 0.09 (−0.13 to 0.31) | |
| Negative at food removal (vs not) | 105 | 0.34 (0.12 to 0.56)** |
Each EAH variable was tested as a main effect in a separate model; all models were adjusted for gender, child race/ethnicity, maternal education, maternal BMI, baseline food insecurity, WLZ at 21 mo for 21-mo models and WLZ at 27 mo for 27-mo models.
P < .05.
P <0.01.
Discussion
The main findings of this study were that EAH increased during toddlerhood, particularly for sweet foods. Greater intake of sweet food and the display of negative affect when the food was taken from the child predicted greater adiposity. To our knowledge, no other published reports have described EAH in children this young. The results of this study align with previous work in older children reporting that EAH increases with age5,6,9–11,15 and is associated with increased adiposity.4–15 The results also align with work in infants showing that parent-reported greater food responsiveness predicts greater prospective weight gain from ages 3 to 15 months.34
Although older children showed positive affect at food presentation, this positive affect was not associated with greater BMIz at 33 months. Rather, negative affect at food removal predicted greater subsequent BMIz. To our knowledge, no other studies have observed the behavior of children in response to the EAH protocol, and this is the first report describing a link between affect during key points in the EAH protocol and weight gain.
Boys were more likely to display EAH, especially for sweet food, which differs from previous literature that did not detect gender differences in EAH among older children.2,6–8,12–14,22, 26, 27,35,36 The only maternal characteristic related to EAH was maternal education. Maternal BMI was not associated with EAH, which aligns with findings of some studies,22 but not others.8,10,11 It was hypothesized that the characteristics related to household stressors in these low-income families (CHAOS, food insecurity, single mother family structure) would predict EAH. However, no association was found. EAH has previously been shown to be heritable via the fat mass and obesity-associated (FTO) gene.26,27 This behavior may be related to other biological factors that have yet to be identified.
The association between EAH and future weight status did not emerge until age 27 months. EAH is believed to reflect a biological predisposition to increased food cue reactivity. The food cue reactivity is believed to be a type of Pavlovian conditioning.16 As such, it exemplifies a likely gene–environment interaction. For EAH and its effects on weight status to manifest, a child with a biological predisposition to increased food cue reactivity may need to have had sufficient exposure to food cues to elicit EAH. The findings suggest that the food cue reactivity is conditioned with repeated exposure to palatable foods before age 2 years, but the conditioned response is not detectable until age 27 months.
Interpretation of these findings should note the study limitations. The home-based protocol reduced experimental control, but increased ecological validity. The presence of the researcher during the protocol may have influenced the child’s behavior. The fact that the researcher modeled eating a sweet food and not a salty food may have increased the likelihood that the toddlers ate sweet, as opposed to salty, foods. The longitudinal design is a strength, but because of the high-risk nature of the study cohort, attrition was high and there were missing data. Results may not be generalizable to other study populations outside low-income toddlers in the United States. Despite these limitations, the study was able to describe eating behavior in a very young age group longitudinally in a diverse population at a lower socioeconomic level than previous work.
Conclusions
Hedonic intake of sweet food is visible, starts to increase, and predicts weight gain in children younger than age 3 years. Given that EAH increases with age5,6,9–11,15 and behavioral intervention has been shown to reduce EAH,16 this study suggests that the timing of interventions targeting this behavior may need to occur before age 3 years. Developing interventions to reduce EAH that are developmentally appropriate for toddlers may be an important, novel intervention strategy. The lack of association with maternal and family characteristics suggests that further understanding of the etiology of EAH may require more studies about the underlying biology of this behavior.
Glossary
- BMIz
BMI z score
- CHAOS
Confusion, Hubbub, and Order Scale
- EAH
eating in the absence of hunger
- WLZ
weight-for-length z score
Footnotes
Ms Asta conceptualized hypotheses for this report, drafted the initial manuscript, collected data, and approved the final manuscript as submitted; Drs Miller, Rosenblum, and Lumeng conceptualized and designed the parent study, provided critical review of the manuscript, and approved the final manuscript as submitted; Ms Retzloff carried out statistical analyses, provided critical review of the manuscript, and approved the final manuscript as submitted; and Dr Kaciroti conceptualized and designed the parent study, provided oversight of the statistical analyses, provided critical review of the manuscript, and approved the final manuscript as submitted.
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: This work was supported by National Institutes of Health Grant 5R01HD069179. Funded by the National Institutes of Health (NIH).
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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