Eating Behaviors 15 (2014) 519–522
Contents lists available at ScienceDirect
Eating Behaviors
The relationship between controlling feeding practices and boys' and girls' eating in the absence of hunger Holly Harris, Kimberley M. Mallan ⁎, Smita Nambiar, Lynne A. Daniels School of Exercise and Nutrition Science and Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, QLD 4059, Australia
a r t i c l e
i n f o
Article history: Received 19 March 2014 Received in revised form 7 May 2014 Accepted 14 July 2014 Available online 23 July 2014 Keywords: Eating in the absence of hunger Child eating behavior Self-regulation Controlling feeding practices
a b s t r a c t Parental controlling feeding practices have been directly associated with maladaptive child eating behaviors, such as eating in the absence of hunger (EAH). The aims of this study were to examine EAH in very young children (3–4 years old) and to investigate the association between maternal controlling feeding practices and energy intake from a standardized selection of snacks consumed ‘in the absence of hunger’. Thirtyseven mother–child dyads enrolled in the NOURISH RCT participated in a modified EAH protocol conducted in the child's home. All children displayed EAH, despite 80% reporting to be full or very full following completion of lunch 15 min earlier. The relationships between maternal and child covariates and controlling feeding practices and EAH were examined using non-parametric tests, and were stratified by child gender. For boys only, pressure to eat was positively associated with EAH. Neither restriction nor monitoring practices were associated with EAH in either boys or girls. Overall, the present findings suggest that gender differences in the relationship between maternal feeding practices and children's eating behaviors emerge early and should be considered in future research and intervention design. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction The use of controlling feeding practices by parents has been hypothesized to increase a child's risk of overeating and becoming overweight. The mechanism through which this relationship is hypothesized to occur is that extrinsic controlling feeding practices undermine the child's ability to recognize and respond appropriately to cues of hunger and satiety; thus their intrinsic capacity to selfregulate energy intake is compromised (Faith, Scanlon, Birch, Francis, & Sherry, 2004; Gregory, Paxton, & Brozovic, 2010). ‘Eating in the absence of hunger’ (EAH) is conceptualized as a heightened response to food cues characterized by a child's inability to self-regulate energy intake (Francis & Birch, 2005). This is particularly likely to occur in the presence of energy-dense palatable foods. Observational studies have found that over 90% of children ate snacks when they were offered, despite having just eaten a meal, demonstrating the propensity for eating to be reinstated in a satiated child in the presence of palatable snack cues (Hill et al., 2008). Adiposity and BMI Z score have been positively correlated with EAH in various age groups through observational or self-reported measures (Hill et al., 2008; Kral et al., 2010; Shomaker et al., 2010; Tanofsky-Kraff et al., 2008; Zocca et al., 2011). ⁎ Corresponding author at: Institute of Health and Biomedical Innovation, Queensland University of Technology, 60 Musk Ave., Kelvin Grove, Brisbane, QLD 4059, Australia. Tel.: +61 7 3138 6171; fax: +61 7 3138 6030. E-mail address: [email protected] (K.M. Mallan).
http://dx.doi.org/10.1016/j.eatbeh.2014.07.003 1471-0153/© 2014 Elsevier Ltd. All rights reserved.
To date there is limited research investigating EAH in very young children and how this behavior may be related to parental controlling feeding practices. Furthermore, there is inconsistent evidence for whether controlling feeding practices impact boys and girls similarly (Blissett, Meyer, & Haycraft, 2006; Faith et al., 2006; Francis & Birch, 2005; Moens & Braet, 2007; Rhee et al., 2009). One observational, longitudinal study (Francis & Birch, 2005) found that maternal restrictive feeding practices when daughters were aged 5 were a significant predictor for EAH at the age of 9, but this was dependent on mother's BMI. There has been limited investigation of maladaptive eating behaviors in younger children, in their own food environment. The purpose of the present study was to pilot a novel modification of the EAH paradigm in order to investigate whether self-reported maternal controlling feeding practices (pressure to eat, restriction and monitoring) were associated with EAH in preschool aged boys and girls. 2. Methods 2.1. Study design and participants Participants in the current study were recruited from the NOURISH randomized controlled trial (RCT) (Daniels et al., 2009). NOURISH aimed to evaluate the efficacy of a community-based intervention that provided anticipatory guidance of feeding practices to first-time mothers. The NOURISH RCT enrolled 698 first-time mothers from two Australian capital cities, Brisbane and Adelaide, in 2008–2009. Eligibility criteria included: term infants N 35 weeks,
520
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
≥ 2500 g; mothers ≥ 18 years, primiparous; and a facility with spoken and written English. Infants with diagnosed congenital abnormalities or chronic health conditions were not eligible. Further details on the recruitment and retention protocols for NOURISH have been described in detail elsewhere (Daniels et al., 2009, 2012). NOURISH data collection occurred at: birth; T1 (4 months), T2 (14 months), T3 (2 years), and T4 (3.7 years). The present study commenced immediately following T4. Only active NOURISH participants living in Brisbane (N = 180) were invited to participate. Children with a diagnosed food allergy/intolerance or behavioral, sleep or medical conditions which may affect eating were not eligible. Approval for the NOURISH RCT was obtained from 11 Human Research Ethics Committees covering the Queensland University of Technology (QUT), Flinders University and all the recruitment hospitals. The trial was registered with the Australian and New Zealand Clinical Trials Registry Number 12608000056392. Approval for the present study was obtained from QUT. 2.2. Materials and measures 2.2.1. Semi-standardized lunch and standardized snacks The lunch items included one sandwich consisting of two slices of bread (white/wholemeal/wholegrain), spread (butter/margarine/ mayonnaise), and filling (ham/ham and cheese/cheese/chicken/chicken and cheese/egg); 250 mL of full fat milk or 175 g of flavored yogurt; and fruit (fresh/tinned/100% fruit juice). The lunch serving provided on average ~2700 kJ which is almost half of their daily energy requirement; estimated to be ~6000 kJ (BMR plus physical activity level (PAL) of 1.6) (National Health and Medical Research Council, 2005). The snack items included savory biscuits, sweet biscuits, fruit ‘leathers’, potato chips and a cereal bar; providing a total of 2104 kJ. 2.2.2. Covariates Maternal and infant characteristics collected in NOURISH included: maternal age at delivery, education, maternal BMI and infant gender (T1). The child's age was calculated from their birth date to the day of their EAH experiment (months). Introduction to solids (weeks) was obtained from the mothers' self-report (T2). Breastfeeding duration (weeks) was derived from a corroboration of data collected across T1– T3 (Howard, Mallan, Byrne, Magarey, & Daniels, 2012). Measured weight and height of the children were available from T4. The WHO Anthro software program version 3.2.2 was used to calculate the BMIZ which adjusts for age and gender using WHO reference norms (WHO Multicentre Growth Reference Study Group, 2006). 2.2.3. Controlling feeding practices Three subscales from the Child Feeding Questionnaire (Birch et al., 2001) were used to measure controlling feeding practices: pressure to eat (4 items), restriction (8 items) and monitoring (3 items). Response options were from low (1) to high (5). 2.2.4. Eating in the absence of hunger Eating in the absence of hunger was quantified as total energy consumed from the snacks (kJsnacks). Snack foods were weighed preand post-experiment and energy consumed was determined using Foodworks Professional (version 9) software. This program uses the AUSTNUT 2007 database from the National Children's Nutrition and Physical Activity Survey (Food Standards Australia New Zealand, 2008). 2.2.5. Satiety scale A validated ‘Fullness Chart’ was used to assess child self-reported satiety immediately following the lunch meal (Faith, Kermanshah, & Kissileff, 2002). The scale consists of 5 ordinal response options from ‘empty’ to ‘very full’.
2.3. Procedure The protocol for this experiment was adapted from EAH in older children (Birch, Fisher, & Davison, 2003; Faith et al., 2006; Hill et al., 2008; Kral et al., 2010; Lee & Keller, 2012) and has been described elsewhere (Mallan, Nambiar, Magarey, & Daniels, 2014). All participants were tested in their own home at their ‘usual’ lunchtime. A member of the research team delivered all of the food to be offered to the child but was not present during the experiment. The child's mother was provided with standardized written instructions for completing the protocol and her understanding was confirmed prior to commencement of the experiment. The mother presented the child with the lunch meal for up to 30 min or until they indicated that they felt ‘full’ (i.e. verbally or ceased eating). The mother then assisted her child to respond to the Fullness Chart. The child was given 15 min to engage in self-directed play after which the mother presented all snack items to the child for another 15 min as per a previous EAH protocol (Kral et al., 2010). 2.4. Data management and statistical analysis All analyses were conducted using SPSS version 21. Bivariate analyses between feeding practices and EAH (kJsnacks) and between NOURISH group allocation, covariates (see 2.2.2) and EAH were stratified by child gender as per the study aim. Due to the small sample size and non-normal distribution of some of the variables for these analyses nonparametric Spearman's rho correlations or Mann–Whitney U tests were used. None of the covariates were significantly associated with EAH thus adjusted analyses were not performed. 3. Results Characteristics of the sub-sample of mother–child dyads are shown in Table 1. Only 2 children were overweight at T4 (BMIZ N2) (WHO, 2008). There were no baseline differences between participants from the control and intervention groups (all p ≥ .082). Relative to the sample of N = 698 mothers enrolled in the NOURISH RCT, the subsample of N = 37 mothers had a similar mean age at delivery (M = 31.8, SD = 4.3 years vs. M = 32.8, SD = 4.9 years), but lower BMI at baseline (M = 23.3, SD = 3.7 vs. M = 26.0, SD = 5.3). In the current study, mothers with a university level education were overrepresented (95% vs. 58%). Responses on the satiety scale indicated that 81% (n = 30) of the children were either ‘full’ or ‘very full’ following lunch (median = 5,
Table 1 Characteristics of the subsample of participants (N = 37 mother–child dyads) recruited from the NOURISH RCT (Daniels et al., 2009). Variable
Median (IQR); % (n)
Maternal characteristics Age at delivery (years) University education (yes) BMI (kg/m2)a Breastfeeding duration (weeks) b Child age first introduced solids (weeks) c
32 (30, 35) 95 (35) 21.9 (21.1, 26.1) 56 (45, 80) 24 (22, 26)
Child characteristics Age (months) Gender (female) Child BMIZ d
52 (45, 54) 57 (21) 0.22 (−0.20, 1.02)
a Maternal BMI calculated from measured height and weight data collected at NOURISH baseline (T1: mean age = 4.3 ± SD = 1.0 months). b Data from corroboration of breast feeding duration reported retrospectively from mother at NOURISH T1/T2/T3. c Infant age (weeks) when solids were first introduced, reported retrospectively at NOURISH T2 (mean age = 13.7 months ± SD = 1.3 months). d Calculated from NOURISH T4 measured height and weight data (mean age = 46.6 ± SD = 2.8 months).
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
IQR: 4, 5). Nevertheless all children ate from the available snacks. Median energy consumption from the standardized snacks (i.e., EAH) and relationship between EAH and controlling feeding practices as a function of gender are presented in Table 2. There was no gender difference for snack intake (p = .27) nor was there a difference according to the NOURISH group (p = .46). Restriction and monitoring were not significantly associated with EAH for boys or girls (p values = .36–.73). For boys only, pressure was positively associated with EAH (Spearman's rho = .55, p = .026), but this relationship was not significant for girls (p = .68).
4. Discussion This study examined the relationship between maternal controlling feeding practices and children's EAH. The present findings suggest that children as young as 3 years are responsive to palatable food cues, even in the absence of ‘hunger’. Over eighty percent of participants identified that they were full or very full following the lunch meal, yet every child in the study ate some portion of the highly palatable snacks. Thus it appears that the recognition of satiety did not result in reduced snack consumption. Rather, as expected, food consumed during the EAH phase appeared to be motivated by hedonic hunger, not physiological hunger; consistent with previous studies investigating EAH in older children (Birch et al., 2003; Hill et al., 2008; Kral & Faith, 2009; Moens & Braet, 2007). EAH was higher in boys whose mothers reported higher pressure to eat. The present finding of an association for boys but not girls is strikingly similar to a large cross-sectional Dutch study (N = 596) of 7 to 12 year old children in which significant positive associations between child perception of parental pressure to eat and both emotional eating and external eating were found for boys but not girls (van Strien & Bazelier, 2007). The current findings are also consistent with data from a large (N = 560) cross-sectional study of Australian 5–6 year olds which showed that pressure to eat was associated with higher reported savory and sweet snack food consumption (Campbell, Crawford, & Ball, 2006). Replication in a larger, more diverse sample is needed before further elucidation on the gender specificity of the relationship between pressure and EAH. Surprisingly, restriction was not associated with EAH in either boys or girls. Restricting a certain type of food has been associated with a greater desire to eat and over consumption of these foods once available (Jansen, Mulkens, Emond, & Jansen, 2008; Jansen, Mulkens, & Jansen, 2007). However, the available evidence for the association between mothers' use of restriction and child eating behaviors is conflicting (Fisher, Mitchell, Smiciklas-Wright, & Birch, 2002; Francis & Birch, 2005). A longitudinal study examining maternal feeding practices found that overweight mother's use of restriction of daughters' intake at age 5 predicted EAH, in a laboratory environment, across the ages of 5–9 years old and weight status. However, this relationship did not hold true in mothers who were not overweight (Francis & Birch, 2005). A study of the same cohort revealed that high maternal
521
restriction predicted energy intake EAH in overweight and nonoverweight daughters (Birch et al., 2003). Possible reasons for the absence of a relationship between EAH and restriction in this study include the small sample size, a sample that consisted mainly of mothers of a healthy weight status and only moderate (median = 2.9; IQR: 2.4, 3.4) levels of restriction reported by mothers. It may be that only high levels of restriction are likely to have an impact on child eating behavior. Perhaps the null finding regarding monitoring and EAH is not unexpected. To some degree, monitoring may be considered as a covert, non-directive form of control, in response to parental perceptions of children's weight and/or eating behavior style (Farrow, Galloway, & Fraser, 2009; Gregory et al., 2010). Thus, if the child is not aware of the practice then it may not have negative ramifications for the development of self-regulation ability. 4.1. Limitations The response rate of 17% suggests the presence of volunteer bias which limits the generalizability of the results to university educated, first-time Australian mothers with healthy weight children. Due to the small sample size the power to detect significant associations between energy intake and controlling feeding practices was limited. We attempted to eliminate observer (researcher) bias by requesting the mother to carry out the experiment. Although adherence to the protocol was verbally confirmed by all mothers at the end of the testing session, without more specific data on maternal behavior during the experiment potential effects of mothers cannot be equivocally ruled out. Other potential confounders, such as the presence of siblings/ other adults, child mood, or intake of foods prior to the experiment were not accounted for. 4.2. Conclusion The present study indicated that even young children are responsive to environmental, rather than physiological cues to eat (Birch et al., 2003). An impaired ability to respond to satiety cues and self-control food intake in an environment in which children are frequently confronted with an abundance of energy dense foods is likely to have undesirable ramifications on a child's energy balance and weight status. Pressure by mothers was positively associated with EAH at age 3– 4 years, but only for boys. Given the cross-sectional nature of these data, claims regarding causality are unfounded; rather a bidirectional relationship between parental feeding practices and child eating behaviors is likely to exist. Role of funding sources We acknowledge funding sources. The Australian National Health and Medical Research Council has provided funding for NOURISH 2008–2010 and 2012–2014. Additional funding was provided by H. J. Heinz (post-doctoral fellowship to Dr. Kimberley Mallan), Meat & Livestock Australia (MLA), the Department of Health South Australia, Food Standards Australia New Zealand (FSANZ), and the Queensland University of Technology. These funding sources had no involvement in the present study.
Table 2 Associations between controlling feeding practices and eating in the absence of hunger (kJsnacks) for boys and girls. Eating in the absence of hunger (kJsnacks)a Controlling feeding practices (CFQ) (Birch et al., 2001)
Pressure Restriction Monitoring
Median = 1.5 (IQR: 1.0, 2.8) Median = 2.9 (IQR: 2.4, 3.4) Median = 4.3 (IQR: 4.0, 5.0)
Boys (n = 16)
Girls (n = 21)
Median = 636 kJ (IQR: 405, 713)
Median = 442 (IQR = 343, 665)
Spearman's rho
p value
Spearman's rho
p value
.55 .12 .25
.026 .67 .36
.10 −.09 −.08
.68 .69 .73
a Standardized snacks offered: bite-sized savory biscuits (25 g), bite-sized sweet biscuits (23 g), fruit ‘leathers’ (flat, pectin-based fruit-flavored snack) (16 g), potato chips (25 g) and a cereal (rice bubbles) bar (22 g); energy consumed (kJsnacks) ranged from 84 to 1158 kJ.
522
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
Contributors H. Harris contributed to data collection and processing and contributed to writing the first draft of the manuscript. K. M. Mallan conducted the analysis and contributed to the study design, data collection, and writing of the first draft of the manuscript. S. Nambiar contributed to the study design and data collection. L. A. Daniels contributed to the study design. All authors contributed to and have approved the final manuscript. Conflict of interest All authors declare that they have no conflicts of interest. Acknowledgments We acknowledge the NOURISH investigators: Associate Professor Anthea Magarey, and Professors Diana Battistutta, Jan Nicholson, Ann Farrell, Geoffrey Cleghorn and Geoffrey Davidson. We acknowledge the contribution to intervention development by Dr. Rebecca Perry and Chelsea Mauch. We sincerely thank all the NOURISH participants and recruiting, intervention and assessment staff including Dr. Carla Rogers, Jacinda Wilson, Josephine Meedeniya, Gizelle Wilson, and Kylie Markow.
References Birch, L. L., Fisher, J. O., & Davison, K. K. (2003). Learning to overeat: Maternal use of restrictive feeding practices promotes girls' eating in the absence of hunger. American Journal of Clinical Nutrition, 78, 215–220. Birch, L. L., Fisher, J., Grimm-Thomas, K., Markey, C., Sawyer, R., & Johnson, S. (2001). Confirmatory factor analysis of the Child Feeding Questionnaire: A measure of parental attitudes, beliefs and practices about child feeding and obesity proneness. Appetite, 36, 201–210. Blissett, J., Meyer, C., & Haycraft, E. (2006). Maternal and paternal controlling feeding practices with male and female children. Appetite, 47, 212–219. Campbell, K. J., Crawford, D. A., & Ball, K. (2006). Family food environment and dietary behaviors likely to promote fatness in 5–6 year-old children. International Journal of Obesity, 30, 1272–1280. Daniels, L., Magarey, A., Battistutta, D., Nicholson, J., Farrell, A., Davidson, G., et al. (2009). The NOURISH randomised control trial: Positive feeding practices and food preferences in early childhood — A primary prevention program for childhood obesity. BMC Public Health, 9, 387. Daniels, L., Wilson, J., Mallan, K., Mihrshahi, S., Perry, R., Nicholson, J., et al. (2012). Recruiting and engaging new mothers in nutrition research studies: Lessons from the Australian NOURISH randomised controlled trial. International Journal of Behavioral Nutrition and Physical Activity, 9, 129. Faith, M. S., Berkowitz, R. I., Stallings, V. A., Kerns, J., Storey, M., & Stunkard, A. J. (2006). Eating in the absence of hunger: A genetic marker for childhood obesity in prepubertal boys?*. Obesity, 14, 131–138. Faith, M. S., Kermanshah, M., & Kissileff, H. R. (2002). Development and preliminary validation of a silhouette satiety scale for children. Physiology & Behavior, 76, 173–178. Faith, M., Scanlon, K., Birch, L., Francis, L. A., & Sherry, B. (2004). Parent–child feeding strategies and their relationships to child eating and weight status. Obesity Research, 12, 1711–1722. Farrow, C. V., Galloway, A. T., & Fraser, K. (2009). Sibling eating behaviours and differential child feeding practices reported by parents. Appetite, 52, 307–312. Fisher, J. O., Mitchell, D. C., Smiciklas-Wright, H., & Birch, L. L. (2002). Parental influences on young girls' fruit and vegetable, micronutrient, and fat intakes. Journal of the American Dietetic Association, 102, 58–64.
Food Standards Australia New Zealand (2008). AUSNUT 2007 — Australian food supplement and nutrient database for estimation of population nutrient intakes. Canberra: Food Standards Australia New Zealand. Francis, L. A., & Birch, L. L. (2005). Maternal influences on daughters' restrained eating behavior. Health Psychology, 24, 548–554. Gregory, J. E., Paxton, S. J., & Brozovic, A.M. (2010). Pressure to eat and restriction are associated with child eating behaviours and maternal concern about child weight, but not child body mass index, in 2- to 4-year-old children. Appetite, 54, 550–556. Hill, C., Llewellyn, C. H., Saxton, J., Webber, L., Semmler, C., Carnell, S., et al. (2008). Adiposity and ‘eating in the absence of hunger’ in children. International Journal of Obesity, 32, 1499–1505. Howard, A. J., Mallan, K. M., Byrne, R., Magarey, A., & Daniels, L. A. (2012). Toddlers' food preferences. The impact of novel food exposure, maternal preferences and food neophobia. Appetite, 59, 818–825. Jansen, E., Mulkens, S., Emond, Y., & Jansen, A. (2008). From the Garden of Eden to the land of plenty: Restriction of fruit and sweets intake leads to increased fruit and sweets consumption in children. Appetite, 51, 570–575. Jansen, E., Mulkens, S., & Jansen, A. (2007). Do not eat the red food!: Prohibition of snacks leads to their relatively higher consumption in children. Appetite, 49, 572–577. Kral, T. V. E., & Faith, M. S. (2009). Influences on child eating and weight development from a behavioral genetics perspective. Journal of Pediatric Psychology, 34, 596–605. Kral, T. V. E., Moore, R. H., Stunkard, A. J., Berkowitz, R. I., Stettler, N., Stallings, V. A., et al. (2010). Adolescent eating in the absence of hunger and relation to discretionary calorie allowance. Journal of the American Dietetic Association, 110, 1896–1900. Lee, H., & Keller, K. L. (2012). Children who are pressured to eat at home consume fewer high-fat foods in laboratory test meals. Journal of the Academy of Nutrition and Dietetics, 112, 271–275. Mallan, K. M., Nambiar, S., Magarey, A.M., & Daniels, L. A. (2014). Satiety responsiveness in toddlerhood predicts energy intake and weight status at four years of age. Appetite, 74, 79–85. Moens, E., & Braet, C. (2007). Predictors of disinhibited eating in children with and without overweight. Behaviour Research and Therapy, 45, 1357–1368. National Health and Medical Research Council (2005). Nutrient reference values for Australia and New Zealand. Canberra: National Health and Medical Research Council. Rhee, K. E., Coleman, S. M., Appugliese, D. P., Kaciroti, N. A., Corwyn, R. F., Davidson, N. S., et al. (2009). Maternal feeding practices become more controlling after and not before excessive rates of weight gain. Obesity, 17, 1724–1729. Shomaker, L. B., Tanofsky-Kraff, M., Zocca, J. M., Courville, A., Kozlosky, M., Columbo, K. M., et al. (2010). Eating in the absence of hunger in adolescents: intake after a large-array meal compared with that after a standardized meal. The American Journal of Clinical Nutrition, 92, 697–703. Tanofsky-Kraff, M., Ranzenhofer, L. M., Yanovski, S. Z., Schvey, N. A., Faith, M., Gustafson, J., et al. (2008). Psychometric properties of a new questionnaire to assess eating in the absence of hunger in children and adolescents. Appetite, 51, 148–155. van Strien, T., & Bazelier, F. G. (2007). Perceived parental control of food intake is related to external, restrained and emotional eating in 7–12-year-old boys and girls. Appetite, 49, 618–625. WHO (2008). Child growth standards: Training course on child growth assessment. Geneva: World Health Organization. WHO Multicentre Growth Reference Study Group (2006). WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Zocca, J. M., Shomaker, L. B., Tanofsky-Kraff, M., Columbo, K. M., Raciti, G. R., Brady, S. M., et al. (2011). Links between mothers' and children's disinhibited eating and children's adiposity. Appetite, 56, 324–331.
Contents lists available at ScienceDirect
Eating Behaviors
The relationship between controlling feeding practices and boys' and girls' eating in the absence of hunger Holly Harris, Kimberley M. Mallan ⁎, Smita Nambiar, Lynne A. Daniels School of Exercise and Nutrition Science and Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, QLD 4059, Australia
a r t i c l e
i n f o
Article history: Received 19 March 2014 Received in revised form 7 May 2014 Accepted 14 July 2014 Available online 23 July 2014 Keywords: Eating in the absence of hunger Child eating behavior Self-regulation Controlling feeding practices
a b s t r a c t Parental controlling feeding practices have been directly associated with maladaptive child eating behaviors, such as eating in the absence of hunger (EAH). The aims of this study were to examine EAH in very young children (3–4 years old) and to investigate the association between maternal controlling feeding practices and energy intake from a standardized selection of snacks consumed ‘in the absence of hunger’. Thirtyseven mother–child dyads enrolled in the NOURISH RCT participated in a modified EAH protocol conducted in the child's home. All children displayed EAH, despite 80% reporting to be full or very full following completion of lunch 15 min earlier. The relationships between maternal and child covariates and controlling feeding practices and EAH were examined using non-parametric tests, and were stratified by child gender. For boys only, pressure to eat was positively associated with EAH. Neither restriction nor monitoring practices were associated with EAH in either boys or girls. Overall, the present findings suggest that gender differences in the relationship between maternal feeding practices and children's eating behaviors emerge early and should be considered in future research and intervention design. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction The use of controlling feeding practices by parents has been hypothesized to increase a child's risk of overeating and becoming overweight. The mechanism through which this relationship is hypothesized to occur is that extrinsic controlling feeding practices undermine the child's ability to recognize and respond appropriately to cues of hunger and satiety; thus their intrinsic capacity to selfregulate energy intake is compromised (Faith, Scanlon, Birch, Francis, & Sherry, 2004; Gregory, Paxton, & Brozovic, 2010). ‘Eating in the absence of hunger’ (EAH) is conceptualized as a heightened response to food cues characterized by a child's inability to self-regulate energy intake (Francis & Birch, 2005). This is particularly likely to occur in the presence of energy-dense palatable foods. Observational studies have found that over 90% of children ate snacks when they were offered, despite having just eaten a meal, demonstrating the propensity for eating to be reinstated in a satiated child in the presence of palatable snack cues (Hill et al., 2008). Adiposity and BMI Z score have been positively correlated with EAH in various age groups through observational or self-reported measures (Hill et al., 2008; Kral et al., 2010; Shomaker et al., 2010; Tanofsky-Kraff et al., 2008; Zocca et al., 2011). ⁎ Corresponding author at: Institute of Health and Biomedical Innovation, Queensland University of Technology, 60 Musk Ave., Kelvin Grove, Brisbane, QLD 4059, Australia. Tel.: +61 7 3138 6171; fax: +61 7 3138 6030. E-mail address: [email protected] (K.M. Mallan).
http://dx.doi.org/10.1016/j.eatbeh.2014.07.003 1471-0153/© 2014 Elsevier Ltd. All rights reserved.
To date there is limited research investigating EAH in very young children and how this behavior may be related to parental controlling feeding practices. Furthermore, there is inconsistent evidence for whether controlling feeding practices impact boys and girls similarly (Blissett, Meyer, & Haycraft, 2006; Faith et al., 2006; Francis & Birch, 2005; Moens & Braet, 2007; Rhee et al., 2009). One observational, longitudinal study (Francis & Birch, 2005) found that maternal restrictive feeding practices when daughters were aged 5 were a significant predictor for EAH at the age of 9, but this was dependent on mother's BMI. There has been limited investigation of maladaptive eating behaviors in younger children, in their own food environment. The purpose of the present study was to pilot a novel modification of the EAH paradigm in order to investigate whether self-reported maternal controlling feeding practices (pressure to eat, restriction and monitoring) were associated with EAH in preschool aged boys and girls. 2. Methods 2.1. Study design and participants Participants in the current study were recruited from the NOURISH randomized controlled trial (RCT) (Daniels et al., 2009). NOURISH aimed to evaluate the efficacy of a community-based intervention that provided anticipatory guidance of feeding practices to first-time mothers. The NOURISH RCT enrolled 698 first-time mothers from two Australian capital cities, Brisbane and Adelaide, in 2008–2009. Eligibility criteria included: term infants N 35 weeks,
520
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
≥ 2500 g; mothers ≥ 18 years, primiparous; and a facility with spoken and written English. Infants with diagnosed congenital abnormalities or chronic health conditions were not eligible. Further details on the recruitment and retention protocols for NOURISH have been described in detail elsewhere (Daniels et al., 2009, 2012). NOURISH data collection occurred at: birth; T1 (4 months), T2 (14 months), T3 (2 years), and T4 (3.7 years). The present study commenced immediately following T4. Only active NOURISH participants living in Brisbane (N = 180) were invited to participate. Children with a diagnosed food allergy/intolerance or behavioral, sleep or medical conditions which may affect eating were not eligible. Approval for the NOURISH RCT was obtained from 11 Human Research Ethics Committees covering the Queensland University of Technology (QUT), Flinders University and all the recruitment hospitals. The trial was registered with the Australian and New Zealand Clinical Trials Registry Number 12608000056392. Approval for the present study was obtained from QUT. 2.2. Materials and measures 2.2.1. Semi-standardized lunch and standardized snacks The lunch items included one sandwich consisting of two slices of bread (white/wholemeal/wholegrain), spread (butter/margarine/ mayonnaise), and filling (ham/ham and cheese/cheese/chicken/chicken and cheese/egg); 250 mL of full fat milk or 175 g of flavored yogurt; and fruit (fresh/tinned/100% fruit juice). The lunch serving provided on average ~2700 kJ which is almost half of their daily energy requirement; estimated to be ~6000 kJ (BMR plus physical activity level (PAL) of 1.6) (National Health and Medical Research Council, 2005). The snack items included savory biscuits, sweet biscuits, fruit ‘leathers’, potato chips and a cereal bar; providing a total of 2104 kJ. 2.2.2. Covariates Maternal and infant characteristics collected in NOURISH included: maternal age at delivery, education, maternal BMI and infant gender (T1). The child's age was calculated from their birth date to the day of their EAH experiment (months). Introduction to solids (weeks) was obtained from the mothers' self-report (T2). Breastfeeding duration (weeks) was derived from a corroboration of data collected across T1– T3 (Howard, Mallan, Byrne, Magarey, & Daniels, 2012). Measured weight and height of the children were available from T4. The WHO Anthro software program version 3.2.2 was used to calculate the BMIZ which adjusts for age and gender using WHO reference norms (WHO Multicentre Growth Reference Study Group, 2006). 2.2.3. Controlling feeding practices Three subscales from the Child Feeding Questionnaire (Birch et al., 2001) were used to measure controlling feeding practices: pressure to eat (4 items), restriction (8 items) and monitoring (3 items). Response options were from low (1) to high (5). 2.2.4. Eating in the absence of hunger Eating in the absence of hunger was quantified as total energy consumed from the snacks (kJsnacks). Snack foods were weighed preand post-experiment and energy consumed was determined using Foodworks Professional (version 9) software. This program uses the AUSTNUT 2007 database from the National Children's Nutrition and Physical Activity Survey (Food Standards Australia New Zealand, 2008). 2.2.5. Satiety scale A validated ‘Fullness Chart’ was used to assess child self-reported satiety immediately following the lunch meal (Faith, Kermanshah, & Kissileff, 2002). The scale consists of 5 ordinal response options from ‘empty’ to ‘very full’.
2.3. Procedure The protocol for this experiment was adapted from EAH in older children (Birch, Fisher, & Davison, 2003; Faith et al., 2006; Hill et al., 2008; Kral et al., 2010; Lee & Keller, 2012) and has been described elsewhere (Mallan, Nambiar, Magarey, & Daniels, 2014). All participants were tested in their own home at their ‘usual’ lunchtime. A member of the research team delivered all of the food to be offered to the child but was not present during the experiment. The child's mother was provided with standardized written instructions for completing the protocol and her understanding was confirmed prior to commencement of the experiment. The mother presented the child with the lunch meal for up to 30 min or until they indicated that they felt ‘full’ (i.e. verbally or ceased eating). The mother then assisted her child to respond to the Fullness Chart. The child was given 15 min to engage in self-directed play after which the mother presented all snack items to the child for another 15 min as per a previous EAH protocol (Kral et al., 2010). 2.4. Data management and statistical analysis All analyses were conducted using SPSS version 21. Bivariate analyses between feeding practices and EAH (kJsnacks) and between NOURISH group allocation, covariates (see 2.2.2) and EAH were stratified by child gender as per the study aim. Due to the small sample size and non-normal distribution of some of the variables for these analyses nonparametric Spearman's rho correlations or Mann–Whitney U tests were used. None of the covariates were significantly associated with EAH thus adjusted analyses were not performed. 3. Results Characteristics of the sub-sample of mother–child dyads are shown in Table 1. Only 2 children were overweight at T4 (BMIZ N2) (WHO, 2008). There were no baseline differences between participants from the control and intervention groups (all p ≥ .082). Relative to the sample of N = 698 mothers enrolled in the NOURISH RCT, the subsample of N = 37 mothers had a similar mean age at delivery (M = 31.8, SD = 4.3 years vs. M = 32.8, SD = 4.9 years), but lower BMI at baseline (M = 23.3, SD = 3.7 vs. M = 26.0, SD = 5.3). In the current study, mothers with a university level education were overrepresented (95% vs. 58%). Responses on the satiety scale indicated that 81% (n = 30) of the children were either ‘full’ or ‘very full’ following lunch (median = 5,
Table 1 Characteristics of the subsample of participants (N = 37 mother–child dyads) recruited from the NOURISH RCT (Daniels et al., 2009). Variable
Median (IQR); % (n)
Maternal characteristics Age at delivery (years) University education (yes) BMI (kg/m2)a Breastfeeding duration (weeks) b Child age first introduced solids (weeks) c
32 (30, 35) 95 (35) 21.9 (21.1, 26.1) 56 (45, 80) 24 (22, 26)
Child characteristics Age (months) Gender (female) Child BMIZ d
52 (45, 54) 57 (21) 0.22 (−0.20, 1.02)
a Maternal BMI calculated from measured height and weight data collected at NOURISH baseline (T1: mean age = 4.3 ± SD = 1.0 months). b Data from corroboration of breast feeding duration reported retrospectively from mother at NOURISH T1/T2/T3. c Infant age (weeks) when solids were first introduced, reported retrospectively at NOURISH T2 (mean age = 13.7 months ± SD = 1.3 months). d Calculated from NOURISH T4 measured height and weight data (mean age = 46.6 ± SD = 2.8 months).
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
IQR: 4, 5). Nevertheless all children ate from the available snacks. Median energy consumption from the standardized snacks (i.e., EAH) and relationship between EAH and controlling feeding practices as a function of gender are presented in Table 2. There was no gender difference for snack intake (p = .27) nor was there a difference according to the NOURISH group (p = .46). Restriction and monitoring were not significantly associated with EAH for boys or girls (p values = .36–.73). For boys only, pressure was positively associated with EAH (Spearman's rho = .55, p = .026), but this relationship was not significant for girls (p = .68).
4. Discussion This study examined the relationship between maternal controlling feeding practices and children's EAH. The present findings suggest that children as young as 3 years are responsive to palatable food cues, even in the absence of ‘hunger’. Over eighty percent of participants identified that they were full or very full following the lunch meal, yet every child in the study ate some portion of the highly palatable snacks. Thus it appears that the recognition of satiety did not result in reduced snack consumption. Rather, as expected, food consumed during the EAH phase appeared to be motivated by hedonic hunger, not physiological hunger; consistent with previous studies investigating EAH in older children (Birch et al., 2003; Hill et al., 2008; Kral & Faith, 2009; Moens & Braet, 2007). EAH was higher in boys whose mothers reported higher pressure to eat. The present finding of an association for boys but not girls is strikingly similar to a large cross-sectional Dutch study (N = 596) of 7 to 12 year old children in which significant positive associations between child perception of parental pressure to eat and both emotional eating and external eating were found for boys but not girls (van Strien & Bazelier, 2007). The current findings are also consistent with data from a large (N = 560) cross-sectional study of Australian 5–6 year olds which showed that pressure to eat was associated with higher reported savory and sweet snack food consumption (Campbell, Crawford, & Ball, 2006). Replication in a larger, more diverse sample is needed before further elucidation on the gender specificity of the relationship between pressure and EAH. Surprisingly, restriction was not associated with EAH in either boys or girls. Restricting a certain type of food has been associated with a greater desire to eat and over consumption of these foods once available (Jansen, Mulkens, Emond, & Jansen, 2008; Jansen, Mulkens, & Jansen, 2007). However, the available evidence for the association between mothers' use of restriction and child eating behaviors is conflicting (Fisher, Mitchell, Smiciklas-Wright, & Birch, 2002; Francis & Birch, 2005). A longitudinal study examining maternal feeding practices found that overweight mother's use of restriction of daughters' intake at age 5 predicted EAH, in a laboratory environment, across the ages of 5–9 years old and weight status. However, this relationship did not hold true in mothers who were not overweight (Francis & Birch, 2005). A study of the same cohort revealed that high maternal
521
restriction predicted energy intake EAH in overweight and nonoverweight daughters (Birch et al., 2003). Possible reasons for the absence of a relationship between EAH and restriction in this study include the small sample size, a sample that consisted mainly of mothers of a healthy weight status and only moderate (median = 2.9; IQR: 2.4, 3.4) levels of restriction reported by mothers. It may be that only high levels of restriction are likely to have an impact on child eating behavior. Perhaps the null finding regarding monitoring and EAH is not unexpected. To some degree, monitoring may be considered as a covert, non-directive form of control, in response to parental perceptions of children's weight and/or eating behavior style (Farrow, Galloway, & Fraser, 2009; Gregory et al., 2010). Thus, if the child is not aware of the practice then it may not have negative ramifications for the development of self-regulation ability. 4.1. Limitations The response rate of 17% suggests the presence of volunteer bias which limits the generalizability of the results to university educated, first-time Australian mothers with healthy weight children. Due to the small sample size the power to detect significant associations between energy intake and controlling feeding practices was limited. We attempted to eliminate observer (researcher) bias by requesting the mother to carry out the experiment. Although adherence to the protocol was verbally confirmed by all mothers at the end of the testing session, without more specific data on maternal behavior during the experiment potential effects of mothers cannot be equivocally ruled out. Other potential confounders, such as the presence of siblings/ other adults, child mood, or intake of foods prior to the experiment were not accounted for. 4.2. Conclusion The present study indicated that even young children are responsive to environmental, rather than physiological cues to eat (Birch et al., 2003). An impaired ability to respond to satiety cues and self-control food intake in an environment in which children are frequently confronted with an abundance of energy dense foods is likely to have undesirable ramifications on a child's energy balance and weight status. Pressure by mothers was positively associated with EAH at age 3– 4 years, but only for boys. Given the cross-sectional nature of these data, claims regarding causality are unfounded; rather a bidirectional relationship between parental feeding practices and child eating behaviors is likely to exist. Role of funding sources We acknowledge funding sources. The Australian National Health and Medical Research Council has provided funding for NOURISH 2008–2010 and 2012–2014. Additional funding was provided by H. J. Heinz (post-doctoral fellowship to Dr. Kimberley Mallan), Meat & Livestock Australia (MLA), the Department of Health South Australia, Food Standards Australia New Zealand (FSANZ), and the Queensland University of Technology. These funding sources had no involvement in the present study.
Table 2 Associations between controlling feeding practices and eating in the absence of hunger (kJsnacks) for boys and girls. Eating in the absence of hunger (kJsnacks)a Controlling feeding practices (CFQ) (Birch et al., 2001)
Pressure Restriction Monitoring
Median = 1.5 (IQR: 1.0, 2.8) Median = 2.9 (IQR: 2.4, 3.4) Median = 4.3 (IQR: 4.0, 5.0)
Boys (n = 16)
Girls (n = 21)
Median = 636 kJ (IQR: 405, 713)
Median = 442 (IQR = 343, 665)
Spearman's rho
p value
Spearman's rho
p value
.55 .12 .25
.026 .67 .36
.10 −.09 −.08
.68 .69 .73
a Standardized snacks offered: bite-sized savory biscuits (25 g), bite-sized sweet biscuits (23 g), fruit ‘leathers’ (flat, pectin-based fruit-flavored snack) (16 g), potato chips (25 g) and a cereal (rice bubbles) bar (22 g); energy consumed (kJsnacks) ranged from 84 to 1158 kJ.
522
H. Harris et al. / Eating Behaviors 15 (2014) 519–522
Contributors H. Harris contributed to data collection and processing and contributed to writing the first draft of the manuscript. K. M. Mallan conducted the analysis and contributed to the study design, data collection, and writing of the first draft of the manuscript. S. Nambiar contributed to the study design and data collection. L. A. Daniels contributed to the study design. All authors contributed to and have approved the final manuscript. Conflict of interest All authors declare that they have no conflicts of interest. Acknowledgments We acknowledge the NOURISH investigators: Associate Professor Anthea Magarey, and Professors Diana Battistutta, Jan Nicholson, Ann Farrell, Geoffrey Cleghorn and Geoffrey Davidson. We acknowledge the contribution to intervention development by Dr. Rebecca Perry and Chelsea Mauch. We sincerely thank all the NOURISH participants and recruiting, intervention and assessment staff including Dr. Carla Rogers, Jacinda Wilson, Josephine Meedeniya, Gizelle Wilson, and Kylie Markow.
References Birch, L. L., Fisher, J. O., & Davison, K. K. (2003). Learning to overeat: Maternal use of restrictive feeding practices promotes girls' eating in the absence of hunger. American Journal of Clinical Nutrition, 78, 215–220. Birch, L. L., Fisher, J., Grimm-Thomas, K., Markey, C., Sawyer, R., & Johnson, S. (2001). Confirmatory factor analysis of the Child Feeding Questionnaire: A measure of parental attitudes, beliefs and practices about child feeding and obesity proneness. Appetite, 36, 201–210. Blissett, J., Meyer, C., & Haycraft, E. (2006). Maternal and paternal controlling feeding practices with male and female children. Appetite, 47, 212–219. Campbell, K. J., Crawford, D. A., & Ball, K. (2006). Family food environment and dietary behaviors likely to promote fatness in 5–6 year-old children. International Journal of Obesity, 30, 1272–1280. Daniels, L., Magarey, A., Battistutta, D., Nicholson, J., Farrell, A., Davidson, G., et al. (2009). The NOURISH randomised control trial: Positive feeding practices and food preferences in early childhood — A primary prevention program for childhood obesity. BMC Public Health, 9, 387. Daniels, L., Wilson, J., Mallan, K., Mihrshahi, S., Perry, R., Nicholson, J., et al. (2012). Recruiting and engaging new mothers in nutrition research studies: Lessons from the Australian NOURISH randomised controlled trial. International Journal of Behavioral Nutrition and Physical Activity, 9, 129. Faith, M. S., Berkowitz, R. I., Stallings, V. A., Kerns, J., Storey, M., & Stunkard, A. J. (2006). Eating in the absence of hunger: A genetic marker for childhood obesity in prepubertal boys?*. Obesity, 14, 131–138. Faith, M. S., Kermanshah, M., & Kissileff, H. R. (2002). Development and preliminary validation of a silhouette satiety scale for children. Physiology & Behavior, 76, 173–178. Faith, M., Scanlon, K., Birch, L., Francis, L. A., & Sherry, B. (2004). Parent–child feeding strategies and their relationships to child eating and weight status. Obesity Research, 12, 1711–1722. Farrow, C. V., Galloway, A. T., & Fraser, K. (2009). Sibling eating behaviours and differential child feeding practices reported by parents. Appetite, 52, 307–312. Fisher, J. O., Mitchell, D. C., Smiciklas-Wright, H., & Birch, L. L. (2002). Parental influences on young girls' fruit and vegetable, micronutrient, and fat intakes. Journal of the American Dietetic Association, 102, 58–64.
Food Standards Australia New Zealand (2008). AUSNUT 2007 — Australian food supplement and nutrient database for estimation of population nutrient intakes. Canberra: Food Standards Australia New Zealand. Francis, L. A., & Birch, L. L. (2005). Maternal influences on daughters' restrained eating behavior. Health Psychology, 24, 548–554. Gregory, J. E., Paxton, S. J., & Brozovic, A.M. (2010). Pressure to eat and restriction are associated with child eating behaviours and maternal concern about child weight, but not child body mass index, in 2- to 4-year-old children. Appetite, 54, 550–556. Hill, C., Llewellyn, C. H., Saxton, J., Webber, L., Semmler, C., Carnell, S., et al. (2008). Adiposity and ‘eating in the absence of hunger’ in children. International Journal of Obesity, 32, 1499–1505. Howard, A. J., Mallan, K. M., Byrne, R., Magarey, A., & Daniels, L. A. (2012). Toddlers' food preferences. The impact of novel food exposure, maternal preferences and food neophobia. Appetite, 59, 818–825. Jansen, E., Mulkens, S., Emond, Y., & Jansen, A. (2008). From the Garden of Eden to the land of plenty: Restriction of fruit and sweets intake leads to increased fruit and sweets consumption in children. Appetite, 51, 570–575. Jansen, E., Mulkens, S., & Jansen, A. (2007). Do not eat the red food!: Prohibition of snacks leads to their relatively higher consumption in children. Appetite, 49, 572–577. Kral, T. V. E., & Faith, M. S. (2009). Influences on child eating and weight development from a behavioral genetics perspective. Journal of Pediatric Psychology, 34, 596–605. Kral, T. V. E., Moore, R. H., Stunkard, A. J., Berkowitz, R. I., Stettler, N., Stallings, V. A., et al. (2010). Adolescent eating in the absence of hunger and relation to discretionary calorie allowance. Journal of the American Dietetic Association, 110, 1896–1900. Lee, H., & Keller, K. L. (2012). Children who are pressured to eat at home consume fewer high-fat foods in laboratory test meals. Journal of the Academy of Nutrition and Dietetics, 112, 271–275. Mallan, K. M., Nambiar, S., Magarey, A.M., & Daniels, L. A. (2014). Satiety responsiveness in toddlerhood predicts energy intake and weight status at four years of age. Appetite, 74, 79–85. Moens, E., & Braet, C. (2007). Predictors of disinhibited eating in children with and without overweight. Behaviour Research and Therapy, 45, 1357–1368. National Health and Medical Research Council (2005). Nutrient reference values for Australia and New Zealand. Canberra: National Health and Medical Research Council. Rhee, K. E., Coleman, S. M., Appugliese, D. P., Kaciroti, N. A., Corwyn, R. F., Davidson, N. S., et al. (2009). Maternal feeding practices become more controlling after and not before excessive rates of weight gain. Obesity, 17, 1724–1729. Shomaker, L. B., Tanofsky-Kraff, M., Zocca, J. M., Courville, A., Kozlosky, M., Columbo, K. M., et al. (2010). Eating in the absence of hunger in adolescents: intake after a large-array meal compared with that after a standardized meal. The American Journal of Clinical Nutrition, 92, 697–703. Tanofsky-Kraff, M., Ranzenhofer, L. M., Yanovski, S. Z., Schvey, N. A., Faith, M., Gustafson, J., et al. (2008). Psychometric properties of a new questionnaire to assess eating in the absence of hunger in children and adolescents. Appetite, 51, 148–155. van Strien, T., & Bazelier, F. G. (2007). Perceived parental control of food intake is related to external, restrained and emotional eating in 7–12-year-old boys and girls. Appetite, 49, 618–625. WHO (2008). Child growth standards: Training course on child growth assessment. Geneva: World Health Organization. WHO Multicentre Growth Reference Study Group (2006). WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Zocca, J. M., Shomaker, L. B., Tanofsky-Kraff, M., Columbo, K. M., Raciti, G. R., Brady, S. M., et al. (2011). Links between mothers' and children's disinhibited eating and children's adiposity. Appetite, 56, 324–331.
