Abstract
Background:
Appetite traits and feeding practices have been linked to children’s weight status. For example, eating in response to food cues (high food responsiveness (FR)), and poor regulation of intake (low satiety responsiveness (SR)), increase risk for obesity. Appetitive traits of infants, and feeding practices, are typically measured by parent-report. The purpose of this study was to use a modified eating in the absence of hunger (EAH) paradigm, measuring infants’ intake 30 min after a typical meal, to test whether infant acceptance of a second meal is associated with parent-reported appetitive traits or feeding practices.
Methods:
Healthy infants aged 3–5 months (N = 54) were fed a typical meal and then offered a second meal by bottle 30 min later. Appetitive traits and feeding practices were assessed with surveys. Analyses of covariance were used to assess whether appetitive traits differed by acceptance of the second meal after adjusting for covariates.
Results:
Fifty-nine percent of infants accepted the second meal and these infants had greater parent-reported FR (M = 3.06 ± 0.58 vs M = 2.43 ± 0.80, p < 0.01) and lower SR (M = 1.87 ± 0.62 vs M = 2.67 ± 0.87, p = 0.01), compared to infants who rejected it. Group differences remained after adjusting for infant age, feeding mode, weight-for-length, and maternal body mass index. No other appetitive traits or feeding practices differed by group.
Conclusions:
Results expand research in older children by showing that infant response to a modified EAH protocol is associated with parent-reported FR and SR. Future research with this protocol in infants should investigate the consistency of this behavior across time and examine whether response to this protocol predicts subsequent growth.
1. Introduction
Individuals who are more responsive to food cues and less responsive to satiety have greater risk for obesity (Birch & Doub, 2014; DiSantis, Hodges, & Fisher, 2013; Llewellyn, Trzaskowski, van Jaarsveld, Plomin, & Wardle, 2014; van Jaarsveld, Llewellyn, Johnson, & Wardle, 2011). In children, these traits can be assessed objectively with paradigms such as eating in the absence of hunger (Birch & Fisher, 1998; Fisher & Birch, 1999; Fogel, McCrickerd, Fries, et al., 2018), compensation for a preload (Carnell, Benson, Pryor, & Driggin, 2013; Remy, Issanchou, Chabanet, Boggio, & Nicklaus, 2015), and changes in the rate of intake across a meal (Carnell et al., 2013; Ohkuma et al., 2015; Remy et al., 2015). However, there are no objective methods to assess for appetitive traits, such as responsiveness to food cues and satiety, in infants. Instead, assessment depends on parent report, which introduces the potential for bias due to variation in parental experience and perception of infant behavior. It has been found that parent report of appetitive traits early in infancy are associated with infant weight gain (Quah, Chan, Aris, et al., 2015; van Jaarsveld et al., 2011). Given that infancy is a critical period during which rapid weight gain increases the risk for later obesity and comorbid disease (Druet, Stettler, Sharp, et al., 2012; Karaolis-Danckert et al., 2006; Ong & Loos, 2006), it is important to identify methods to objectively examine appetitive and satiation behaviors in infants.
The eating in the absence of hunger (EAH) paradigm involves giving children time alone to play in a room with toys and a variety of palatable sweet and savory snacks after they have eaten a meal to apparent satiety (Birch, Fisher, & Davison, 2003; Fisher & Birch, 1999; Fisher & Birch, 2002). Children are instructed to help themselves to the toys and/or food while the investigator steps away. The amount of snack food consumed during this assessment is the outcome of interest. Intake during the EAH is associated with appetitive traits. Specifically, children who consume more food during the test are rated by parents as having lower satiety responsiveness, higher food responsiveness, higher enjoyment of food, and increased emotional eating (Boutelle et al., 2011; Moens & Braet, 2007). Additionally, overweight children are more likely to engage in EAH (Butte, Cai, Cole, et al., 2007; Cutting, Fisher, Grimm-Thomas, & Birch, 1999; Fisher & Birch, 2002; Moens & Braet, 2007). To our knowledge, no prior study has attempted to modify this paradigm to assess infants’ response to food cues. Although an infant’s diet is primarily milk, individual differences in response to the opportunity to consume more milk after being fed to apparent satiety may provide an objective measure of appetitive traits.
The purpose of this study was to determine if infant response to a modified EAH paradigm was associated with parent-reported appetitive traits. Specifically, we hypothesized that mothers of infants who accepted a second meal 30 min after the end of the previous meal would report the infant as more responsive to food cues and/or less responsive to satiety. Secondary goals were to examine whether infants who accepted versus rejected the second meal differed in terms of weight-for-length z-score (WLz), WLz change from birth to study visit prior to the test, maternal body mass index (BMI), or parental feeding practices.
2. Methods
2.1. Participants
Mother-infant dyads (N = 54) enrolled in several studies investigating maternal metabolic health and infant growth participated in this protocol. Infants were eligible if they were aged 3–5 months, healthy, above the 5th percentile in terms of weight-for-length based on World Health Organization (WHO) standards, and had no prior diagnosis of failure to thrive or any current condition that could interfere with normal feeding and growth. The study included infants fed formula and/or breastmilk so long as the infant was accustomed to taking a bottle.
2.2. Protocol
Mothers brought their infants to the clinic not less than 90 min following a prior meal. Research assistants recorded the time of the previous meal, along with the content of the meal and amount consumed or, for breastfed infants, the duration of the meal. Mothers who routinely used bottles to feed their infants brought two prepared bottles of either breastmilk or formula. The amount of breastmilk or formula in the bottle for the first meal was equivalent to the amount the infant typically takes at a meal. For infants routinely fed from the breast, mothers brought one bottle of breastmilk to the clinic visit. Research assistants recorded the content of the bottle and how it was prepared, if formula. The first and second meal tests ensued as described below. Mothers completed questionnaires after the first meal test and prior to the second meal. The Institutional Review Board at the University of Alabama at Birmingham approved this protocol and mothers provided informed consent to participate.
2.3. Meal tests
Wearing only a clean diaper, infants were weighed immediately prior to the first meal to the nearest 1 g on the seca® 728 infant scale (seca® Hamburg, Germany). Research assistants measured infant length to the nearest 0.1 cm using the stadiometer portion of the seca® 728 infant scale. Also collected prior to the meal, for bottle fed infants, was bottle weight, with breastmilk or formula, using the Ohaus® CS2000 scale (Ohaus Corp, Parsippany, NJ). Research assistants instructed mothers to feed their infant from breast or bottle per their usual routine at home. The meal was timed with a stopwatch pausing only for breaks to burp, anytime the infant paused suckling and removed his/her mouth from the breast or bottle, or fell asleep. The first meal ended with guidance from the research assistant and according to the following criteria: the infant fell asleep and did not awaken when the nipple was removed from his/her mouth, the infant refused to eat more after two attempts to restart the feed, or the infant emptied the bottle. Wearing the same diaper as prior to the meal, infants were weighed again immediately after the meal; as was the bottle if used. To measure any milk lost during the meal, an absorbent pre-weighed paper towel or cloth captured spillage or spit-up during the meal and was weighed again after the meal.
For the second meal, the previously prepared bottle was offered to the infants 30 min after the end of the first meal. Research assistants measured the weight of the infant and the bottle immediately prior to this meal as previously described. Termination of the second meal attempt occurred if the infant finished the bottle, refused to suck from the nipple after two attempts, or at the mothers’ discretion after the infant had been drinking for at least 30 s. Mothers were permitted discretion to terminate this second meal because in the earliest subset of participants, some mothers were not comfortable allowing their infants to continue eating so soon after the previous meal. As with the first meal, a stopwatch recorded meal duration. The infant and bottle were reweighed after this meal adjusting for any spillage or spit-up as previously described.
Dichotomization of infants occurred based on acceptance or rejection of the second meal. Consumption of at least 10 g of milk defined acceptance of the second meal. This 10 g threshold was identified following completion of this test in the first 15 infants, where it was observed that up to 10 g of milk was removed from the bottle when infants mouthed or chewed the nipple but did not properly latch and suck, whereas > 10 g of milk was removed for infants that latched and actively sucked.
2.4. Questionnaires
As part of the protocol for the parent studies, demographic information and pregnancy and infant history were self-reported by mothers via questionnaires. For this study, the following variables were extracted: maternal age, maternal BMI post-partum, infant race, infant birth WLz, infant gestational age, infant sex, and whether the infant was ever breastfed. From data collected at the study visit, infant age at study visit, infant WLz at study visit, WLz change since birth, feeding mode at first meal, and amount consumed at first meal were tabulated. These variables were explored as potential covariates for use in statistical models.
As part of this protocol, mothers completed the Baby Eating Behavior Questionnaire (BEBQ) (Llewellyn, van Jaarsveld, Johnson, Carnell, & Wardle, 2011) and the Infant Feeding Questionnaire (IFQ) (Baughcum, Powers, Johnson, et al., 2001) prior to administration of the second meal. The BEBQ measures appetitive traits in infants and is a modified version of the Child Eating and Behavior Questionnaire (CEBQ) which is a well validated and reliable tool for use in parents of older children (Wardle, Guthrie, Sanderson, & Rapoport, 2001). During initial psychometric analysis of the BEBQ, four appetitive traits explained 59.7% of the variance with factor loadings greater than four: enjoyment of feeding (EF) (4 items), food responsiveness (FR) (6 items), satiety responsiveness (SR) (3 items), and slowness of eating (SE) (4 items) (Llewellyn et al., 2011). EF measures the pleasure one derives from eating, and FR measures the desire to eat (Llewellyn et al., 2011). SR measures one’s threshold for fullness, and SE, the rate at which one eats (Llewellyn et al., 2011). A single question, general appetite (GA), was included that measures overall appetite (Llewellyn et al., 2011). The 18-item BEBQ is completed by parents by choosing “never,” “rarely,” “sometimes,” “often,” or “always” for each question. Answers are scored on a 1 to 5 scale, and then averaged to provide a subscale score for each appetitive trait. In the current sample, the alpha coefficient of each subscale was as follows: EF α = 0.35, FR α = 0.82, SE α = 0.63, and SR α = 0.47. Apart from the FR subscale, each alpha coefficient is lower than that reported in the validation of the BEBQ (EF α = 0.81, FR α = 0.79, SE α = 0.76, and SR α = 0.73) (Llewellyn et al., 2011) which could be attributed to the small sample size combined with a low number of items for the subscale.
The IFQ measures maternal beliefs and practices regarding infant feeding (Baughcum et al., 2001). The questionnaire contains 20 questions that assess concern for the infant being underweight (4 items), concern about hunger (3 items), awareness of hunger and fullness cues (4 items), concern about overweight (3 items), feeding on a schedule (2 items), providing food to calm an infant (2 items), and social interaction during feeding (2 items) (Baughcum et al., 2001). Values of internal consistency for the initial study and the current are very similar, the Cronbach alpha for the values from the initial study are reported first: Concern about underweight, (α = 0.71 vs α = 0.61), concern about hunger (α = 0.74 vs α = 0.74), awareness of cues (α = 0.65 vs α = 0.59), and concern about overweight (α = 0.55 vs α = 0.58) (Baughcum et al., 2001). For the three subscales with only two items, Pearson correlation was performed, and again, results were similar, the initial study is reported first: Feeding on a schedule (r = 0.48 vs r = 0.56), using food to calm (r = 0.44 vs r = 0.55), and social interaction (r = 0.24 vs r = 0.14) (Baughcum et al., 2001). These values indicate that even in our small sample, the tool provided reliability similar to that in the initial psychometric analysis done on a large sample (n = 453) (Baughcum et al., 2001).
3. Statistical analyses
Milk consumption at the second meal was calculated as the bottle start weight minus the end weight, adjusted for spillage or spit-up. Breastfeeding history (versus never breastfed) was examined to determine whether infants who had ever been breastfed should be analyzed independently from those who had only received formula. Chisquared test was used to determine if there was a significant difference between infants who accepted the second meal and breastfeeding history.
The change in bottle weight pre- and post-meal or, for breastfed infants, the change in infant weight pre- and post-meal, was calculated to provide the amount consumed at the first meal. This calculation included adjustment for spillage or spit-up. Infant WLz at birth and at the study visit were calculated based on WHO reference data. The calculation of WLz at study visit minus WLz at birth provided the change in WLz, with a positive value indicating an increase in WLz from birth to the study visit. Independent groups t-tests for continuous variables and chi-square test for categorical variables were used to examine whether the following variables differed between infants who accepted versus rejected the second meal: mom age, mom BMI, infant race, infant sex, infant gestational age at birth, infant age at study visit, and feeding mode at first meal (breastfed or bottle fed).
Independent groups t-tests were analyzed to determine if each construct of the BEBQ and the IFQ differed based on acceptance of the second meal. Cohen’s d was calculated as a measure of effect size. For each BEBQ and IFQ variable found to differ between groups, analysis of covariance (ANCOVA) was used to determine if the association changed when controlling for each covariate. Assumptions for all statistical tests were met. R and R Studio version 3.4.3 was used for all analyses (RStudio Team, Boston, MA, 2016).
4. Results
Table 1 provides the descriptive statistics of this sample. Infants were primarily African-American (59.3%), born at 36 weeks gestation or greater (M = 39, range 36–42) with a mean birthweight of 3.329 kg (range 1.730–4.540). Seventy-five percent of the infants had ever received breastmilk and 38.9% of infants still regularly fed from the breast. Mean age of infants was 16 weeks (range 12–22 weeks) at the study visit. Table 2 shows results of descriptive statistics for the sample by acceptance of the second meal. Fifty-nine percent of infants accepted the second meal. There was no significant difference in breastfeeding history between each group; 77% of those who rejected the second meal were ever breastfed and 75% of those who accepted the second meal. Additionally, examination of ever breastfed with each subscale of the BEBQ and the IFQS found no significant associations (results not reported). Based on these findings, infants ever breastfed and those never breastfed were combined for further analyses.
Table 1.
Descriptive statistics (N = 54).
| Categorical variables | n | % |
|---|---|---|
| Maternal marital status | ||
| Single | 32 | 57.4 |
| Married | 23 | 42.6 |
| Maternal highest education level | ||
| Less than high school | 7 | 13.0 |
| High school graduate | 14 | 25.9 |
| Partial college | 12 | 22.2 |
| College graduate | 21 | 38.9 |
| Employment status | ||
| Unemployed | 27 | 50.0 |
| Part-time | 10 | 18.5 |
| Full-time | 17 | 31.5 |
| Race/ethnicity | ||
| African-American | 32 | 59.3 |
| Caucasian | 21 | 38.9 |
| Hispanic | 1 | 1.9 |
| Infant sex | ||
| Male | 30 | 55.6 |
| Female | 24 | 44.4 |
| Ever breastfed | ||
| Yes | 41 | 75.9 |
| No | 13 | 24.1 |
| Started complementary foodsa | ||
| Yes | 13 | 26 |
| No | 37 | 74 |
| Continuous variables | Mean ± SD | Range |
| Maternal age (years) | 26.0 ± 5.9 | 16–40 |
| Maternal BMI | 31.2 ± 8.5 | 17.8–56.5 |
| Infant birth weight (kg) | 3.33 ± 0.47 | 1.73–4.54 |
| Gestational age at birth (weeks) | 39.5 ± 1.1 | 36.9–42.0 |
| Infant age at study visit (days) | 114.8 ± 25.1 | 84.7–158.9 |
n = 50.
Table 2.
Participant characteristics (data are mean ± SD or N [%]).
| Variable | Rejected 2nd meal (n = 22) | Accepted 2nd meal (n = 32) | p-Value |
|---|---|---|---|
| Ever fed breastmilk (%) | 17 (77%) | 24 (75%) | 1 |
| Maternal age at enrollment (years) | 27.9 ± 6.7 | 24.7 ± 5.0 | 0.07 |
| Maternal marital status (single) | 11 (50%) | 20 (63%) | 0.53 |
| Maternal education level (college graduate) | 9 (41%) | 12 (38%) | 0.11 |
| Maternal employment status (unemployed) | 11 (50%) | 16 (50%) | 0.75 |
| Maternal BMI (kg/m2) | 34.5 ± 8.5 | 28.8 ± 7.9 | 0.02 |
| Infant race, African-American (%) | 10 (45%) | 22 (69%) | 0.15 |
| Infant sex, male (%) | 13 (59%) | 17 (53%) | 0.88 |
| Gestational age at delivery (days) | 275.1 ± 8.3 | 277.6 ± 7.7 | 0.27 |
| Infant birth WLz | −0.75 ± 1.16 | −0.87 ± 1.29 | 0.73 |
| Infant age at study visit (days) | 117.6 ± 25.8 | 112.8 ± 24.9 | 0.49 |
| Breastfed first meal | 10 (45%) | 12 (38%) | 0.59 |
| Amount consumed at first meal (grams)a | 104.8 ± 37.3 | 114.8 ± 64.9 | 0.48 |
| Infant WLz at study visit | −0.08 ± 1.01 | 0.09 ± 0.98 | 0.54 |
| Infant WLz change, birth to study visit | 0.69 ± 1.28 | 0.93 ± 1.46 | 0.49 |
| Taking complementary foods (yes)b | 7 (33%) | 6 (19%) | 0.50 |
BMI, body mass index; WLz, weight-for-length z-score.
Weight obtained by weighing infant post-pre feeding for n = 22 breastfed infants, and by post-pre bottle weight for n = 32 bottle-fed infants.
Rejected, n = 21, accepted, n = 29.
A significant difference in maternal BMI was present between groups; this was a medium to large association (d = 0.69, p = 0.02). Mothers of infants who rejected the second meal had a significantly higher BMI than mothers of infants who accepted the second meal (M = 34.5 ± 8.5 vs 28.8 ± 7.9 kg/m2). There were no statistical differences in infant age, feeding mode or amount consumed at first meal, birth WLz, infant WLz at study visit, or change in infant WLz from birth to study visit between infants who accepted versus rejected the second meal.
Statistically significant differences were present with two constructs of the BEBQ. Infants who accepted the second meal had greater FR (M = 3.06 ± 0.58 vs M = 2.43 ± 0.80, p < 0.01) and lower SR (M = 1.87 ± 0.62 vs M = 2.67 ± 0.87, p = 0.01), compared to infants who rejected the second meal. This was a medium to large association. These differences remained after adjusting for maternal BMI and infant characteristics at the study visit (age, feeding mode at first meal, amount consumed at first meal, introduction of complementary foods, WLz, or WLz change since birth). Group differences in FR and SR also remained significant after adjusting for ever breastfed. No significant differences were present in the remaining constructs of the BEBQ (Table 3) or any of the constructs of the IFQ and acceptance of the second meal (Table 4). Of note, 68.5% of mothers answered “often” or “always” to the question that measures GA, “My baby has a big appetite.”
Table 3.
Baby Eating Behavior Questionnaire (BEBQ).
| Rejected M ± SD | Accepted M ± SD | p-Value | Cohen’s d | |
|---|---|---|---|---|
| Enjoyment of feeding (EF) | 4.45 ± 0.54 | 4.50 ± 0.58 | 0.75 | 0.09 |
| Food responsiveness (FR) | 2.43 ± 0.80 | 3.06 ± 0.87 | <0.01 | 0.74 |
| Slowness of eating (SE) | 2.42 ± 0.87 | 2.55 ± 0.78 | 0.57 | 0.16 |
| Satiety responsiveness (SR) | 2.67 ± 1.31 | 1.87 ± 0.62 | 0.01 | 0.83 |
| General appetite (GA) | 3.73 ± 1.07 | 4.03 ± 0.90 | 0.28 | 0.31 |
Cohen’s D: 0.2 small effect, 0.5 medium effect, 0.8 large effect.
Table 4.
Infant Feeding Questionnaire (IFQ).
| Rejected M ± SD | Accepted M ± SD | p-Value | Cohen’s d | |
|---|---|---|---|---|
| Food to calm | 2.98 | 3.30 | 0.36 | 0.26 |
| Feeding on schedule | 2.07 | 2.23 | 0.63 | 0.14 |
| Concern about weight | 1.58 | 1.45 | 0.46 | 0.21 |
| Concern about hunger | 1.65 | 1.92 | 0.42 | 0.22 |
| Awareness of cues | 4.64 | 4.59 | 0.73 | 0.09 |
| Concern about overweight | 1.33 | 1.62 | 0.12 | 0.39 |
| Social interaction | 4.07 | 4.11 | 0.85 | 0.05 |
Cohen’s D: 0.2 small effect, 0.5 medium effect, 0.8 large effect.
5. Discussion
The primary purpose of this study was to determine if infant response to a modified EAH paradigm was associated with appetitive traits as reported by their mothers. Infants who accepted the second meal 30 min after the end of the first meal had higher parent-reported response to food, and lower parent-reported response to satiety, suggesting that this modified EAH paradigm is a useful objective method with which to assess appetitive traits in infants. Prior experience with breastfeeding or mode of feeding (breastfed or bottle) at the first meal did not alter findings, suggesting use of this protocol in all infants who are accustomed to taking a bottle. Although WLz and infant WLz change since birth did not differ by group, the mean BMI of mothers with infants who accepted the second meal was significantly lower than that of mothers of infants who rejected the second meal.
The majority of infants (59%) accepted the second meal. This percentage is similar to other studies in which 67% of toddlers (ages 22–36 months) consumed foods during an EAH paradigm (Corsini, Wilson, Kettler, & Danthiir, 2010) and 73% of preschool children (age 4.5 years) (Fogel et al., 2018). Our findings of greater parent-reported food responsiveness and lower satiety responsiveness among infants who accepted the second meal are consistent with those reported by Carnell and Wardle in 4–5 year old children who completed an EAH protocol (Carnell & Wardle, 2007). The study by Carnell and Wardle also found an association with EF which was not supported in the current study. Interestingly, a study of toddlers (aged 27 and 33 months) found no association with an EAH paradigm and SR or FR (Tan, Walczak, Roach, Lumeng, & Miller, 2018). However, it is possible that child response to this protocol is modified by age and developmental stage of the child. These contradictory findings emphasize the importance of identifying or developing age-appropriate protocols to objectively assess eating behaviors across early childhood.
Rate of infant weight gain has been associated with future obesity risk (Druet et al., 2012; Ong & Loos, 2006). Van Jaarsveld and colleagues found a positive association between appetitive traits and weight gain in infants (van Jaarsveld et al., 2011). Using the BEBQ, they found that mothers who reported the infant as having greater FR and lower SR, weighed more and gained more weight from three to 12 months of age (van Jaarsveld et al., 2011). The current study found no association of response to the EAH protocol with the infant’s current WLz or change in WLz from birth to the age at testing. However, it is possible that EAH response may predict subsequent growth, but it was not possible to examine this in the current study because not all infants were followed beyond this study visit. This would be important to include in future work to determine if acceptance of a second meal at infant age of 3–5 months predicted an infant’s future growth pattern.
Maternal BMI was the only demographic variable found to be significantly different between the groups who accepted the second meal vs rejected it. This finding was unexpected and contradicts prior findings. Francis and Birch reported that, in a study of 5-year-old girls only, those with overweight mothers engaged in more EAH as compared to girls of normal weight mothers (Francis & Birch, 2005). It is possible that the direction of association between maternal weight status and children’s response to the EAH protocol differed in this study of older children versus the current study of infants because of the age difference in these cohorts. For example, although it is known that young children mimic the food related behaviors they observe around them (Birch & Anzman, 2010), the age at which this behavior begins is unknown. It is also possible that women who are normal weight versus overweight differ in terms of their feeding style, particularly as children get older. In prior research, children of mothers who exhibit restrictive feeding practices were more likely to engage in EAH (Birch & Fisher, 2000; Cutting et al., 1999; Engle, Bentley, & Pelto, 2000; Fisher & Birch, 1999), and although the current study found no differences in the feeding practices of mothers whose infants accepted versus rejected the second meal, the IFQ does not correspond to restrictive feeding practices measured in studies of older children. There may also be a biological explanation for why children born to heavier mothers were less likely to accept the second meal. For example, given that infants born to mothers with obesity tend to be larger at birth than infants born to mothers of normal weight (McPhie, Skouteris, Mattick, et al., 2017; Retnakaran, Ye, Hanley, et al., 2012), and then experience a period of catch-down growth (Taal, Vd Heijden, Steegers, Hofman, & Jaddoe, 2013), it is possible that infants born to heavier mothers have less of an appetite as compared to those born to mothers of normal weight. This explanation seems unlikely, however, given that birth weight was not different between the two groups.
Finally, a prior study identified that genetic variants associated with risk for obesity were also associated with recalled infant SR, but not FR, from the first 3 months of life, suggesting that genetic risk for obesity is at least partially mediated via differences in eating behavior (Carnell & Wardle, 2009; Llewellyn et al., 2014; Wardle et al., 2008). However, the direction of these associations was consistent with that seen in adults (i.e. greater appetite associated with greater genetic risk), which appears contrary to the findings of the current study. Other research has noted however, that the association of polygenic risk scores with obesity is not evident at birth, but rather emerges across the first three years of life (Khera, Chaffin, Wade, et al., 2019) suggesting that if the genetic risk for obesity is mediated through eating behavior, it may not be evident in early infancy. In sum, although it is not clear why maternal BMI was lower for infants who accepted versus rejected the second meal in the current study, there are a number of biological and social influences on the development of eating behavior that may become more influential as dietary variability expands, along with children’s autonomy to determine their own intake.
A strength of this study was the ability of trained researchers to monitor mothers and infants during meals and ensure meals ended based on pre-defined criteria for infant satiety (i.e., falling asleep, refusal to take more, etc.). All mothers completed the BEBQ prior to the modified EAH protocol so they were unaware of how their infants would respond to the protocol. Another strength was the use of objective measures with standardized procedures to record infant weight, length, and intake during the meal test, rather than relying on maternal report.
Several limitations in this study reflect trade-offs between making the test meals as natural as possible from the perspective of the mother and infant, versus standardizing the protocol across infants. For example, mothers brought the infants to the clinic for the study protocol not less than 2 h following the previous meal, but no maximum window of time between the meal and presentation in the clinic was established, resulting in variability across dyads. Another limitation is that in order to make the meals similar to those consumed at home, research assistants instructed mothers to provide the same amount of milk they normally would at home, but this amount differed across infants. Also, due to parental discomfort with infants continuing to consume milk from the second meal, the primary outcome of interest was dichotomized rather than being a continuous measure of total milk consumed, which thereby limited sensitivity to assess individual responses.
Future research should endeavor to standardize the protocol further, record the presence of infant hunger cues prior to the test meal, along with satiety cues following the first meal. Research should also work to identify solutions to increase parental comfort with the protocol, so that infants continue with the second meal, in order to obtain a continuous measure of milk consumption. An additional limitation is that the sample size was too small to permit sub-analyses by infant sex or by the amount of prior experience with a bottle. Although we did not find any differences between infants with prior breastfeeding experience versus those who were solely formula-fed, it is possible that differences in the amount of breastmilk versus formula typically consumed by the infant, or variability in the frequency of bottle use, could have impacted the findings. On a related note, future research should include more comprehensive screening of infant feeding history and include whether there were any changes in feeding mode, or formula type, and the reasons for these changes. Although infants with failure to thrive or any diagnosed medical condition that impacts growth were excluded, it is possible that infants with food allergies, or more mild forms of intolerance, were included in the study, and if so, these histories could have impacted their response to the meal test and/or parental perception of their appetitive traits. The low alpha coefficient of the SR subscale is also a concern, and could be consequent to the combination of the small sample size and the low number of items in that subscale (Field, Miles, & Field, 2012), or potentially because it may be difficult for parents to distinguish infant fullness cues versus other states such as sleepiness. Finally, the initial EAH paradigm for older children measured kilocalories consumed as opposed to grams, and the outcome was a continuous variable rather than dichotomous. This study used grams as the outcome because the kilocalories in breastmilk vary among mothers, but future research should assess the caloric density of breastmilk in order to quantify the energy consumed.
In summary, the primary finding from this study is that, consistent with studies of older children, infants who accept a second meal 30 min after the end of a typical meal have higher parent-rated food responsiveness and lower satiety responsiveness, as compared to infants who reject the second meal. Although more work is needed to standardize this modified EAH paradigm for use in infants, these findings imply that it is possible to objectively measure appetitive traits in infants. Future research in a larger cohort of infants is warranted including repeated assessment of this modified EAH paradigm across several days to investigate reliability across time. Future work should also follow the infant’s weight pattern across the first year of life and into childhood to examine whether an association with prospective weight gain exists. Despite limitations of the current study, the results support the possibility of developing objective methods to characterize infant appetitive traits and ultimately, to assess the role of eating behavior on weight gain and future risk for obesity.
Acknowledgements
Research reported in this work was supported by a UAB HSF GEF Award 2015-01, and by the National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health (K01DK090126, P60DK079626, and P30DK056336), and by the National Heart, Lung, and Blood Institute of the National Institutes of Health (T32HL105349). The content is solely the responsibility of the authors and does not necessarily represent the official views of the UAB HSF, the National Institute of Diabetes and Digestive and Kidney Diseases, the National Heart, Lung, and Blood Institute, or the National Institutes of Health.
Footnotes
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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