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How Does Maternal and Child Feeding Behavior Relate to Weight Gain and Failure to Thrive? Data From a Prospective Birth Cohort

^a Department of Child Health, Glasgow University, Glasgow, United Kingdom
^b Department of Child Health, Newcastle University, Newcastle, United Kingdom
^c Department of Psychology, University of Durham, Durham, United Kingdom

	ABSTRACT

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OBJECTIVES. The aim of this study was to study the influences of child and maternal feeding behavior on weight gain and failure to thrive in the first year of life.

METHODS. The Millennium Infant Study recruited a population birth cohort in Northeast England shortly after birth and studied them prospectively to the age of 13 months. Parents completed questionnaires at 6 weeks and 4, 8, and 12 months. Appetite was rated on a 5-point scale at each age, and a core group of questions was used to generate scores of oromotor dysfunction, avoidant eating behavior, maternal feeding anxiety, and response to food refusal. Routinely collected weights were used to assess weight gain using the thrive index (TI); weight faltering was defined as TI below the 5th percentile from birth to age 6 weeks or 4, 8, or 12 months.

RESULTS. Of 923 eligible infants, 75% of the mothers returned at least 1 questionnaire and 2 weights. Weight gain to 6 weeks was independently related to appetite and oromotor dysfunction rated at 6 weeks. Appetite rated at 6 weeks and 12 months both independently predicted weight gain to 12 months. Some avoidant eating behavior was seen in most children by 12 months old, but there was no relationship with weight gain or faltering after adjustment for appetite. However, the extent to which caregivers responded to food refusal was a significant inverse predictor of weight gain, even after adjustment for appetite.

CONCLUSIONS. Inherent child appetite characteristics seem to be an important risk factor for weight faltering and failure to thrive, but high maternal promotion of feeding may also have an adverse influence.

Key Words: failure to thrive • feeding behavior • maternal responsiveness • maternal-child interaction • weight gain

Abbreviations: RTFR—response to food refusal • TI—Thrive Index

Faltering weight gain in infancy, traditionally called "failure to thrive," is a common pediatric presentation and remains a clinical enigma. As discussed in a previous article,¹ parental and environmental factors seem to explain only a minority of cases, as does underlying organic disease,^2–4 although the underlying causal role of under nutrition is now well recognized.⁵ Successful feeding in infancy depends on a complex interaction between caregiver and child, which could potentially become disordered as a result of characteristics or behaviors of either parent or child, or a mismatch between the 2.⁶ Higher rates of feeding behavior problems^7–10 and low appetites¹¹ have been reported in previous studies, but most of these^{8–10, 12} relied on referral to a hospital or clinic, so there may have been selective referral and parents were interviewed only after poor weight gain had been identified, which raises the possibility of recall bias. Studies using direct observation have had mixed results; one with referred cases found disordered satiation in weight-faltering infants compared with controls.¹² In 2 other observational studies, based on population screened cases, one found no difference in feeding behavior,⁴ but the other, in older children, did find substantial differences.¹³ However, observational work is highly labor-intensive, so these studies are fairly small and must, by necessity, sample only small numbers of meals.

Thus, the Millennium Infant Study, a population-based prospective cohort study, was set up to further explore, among other questions, how feeding behavior relates to weight faltering by collecting information on both maternal and child behavior during the feeding process for a large number of children starting before weight faltering became manifest. This article considers how child and maternal feeding behavior relate to overall weight gain and the occurrence of weight faltering in the cohort.

	METHODS

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The Millennium Infant Study approached the mothers of all infants born to Gateshead resident mothers shortly after birth, in 34 prespecified weeks, June 1999 through May 2000,¹ and 82% consented to join the study. Basic demographic information was collected at recruitment, and parents then received questionnaires at 6 weeks and 4, 8, and 12 months when they completed questions about feeding and other issues as well as transcribing routinely collected weights. At the age of 13 months, the infant was weighed and measured by a research nurse. The study received approval from the Gateshead local research ethics committee. For this analysis, infants born before 37 weeks' gestation were excluded.

Feeding Data
At each age, a wide range of age-relevant questions were asked about various aspects of feeding. When the study was set up, we were unable to identify any survey-based methods of assessing feeding in this age range, so we developed a core pool of questions that prior research^{9, 11, 14} and our own clinical practice suggested might relate to failure to thrive, and these were included in every age-relevant questionnaire. These questions were grouped in advance into various dimensions based on separate hypothesized factors from which, when possible, a score was constructed. These were child factors (appetite, oromotor dysfunction, avoidant eating behavior) and maternal factors (feeding anxiety and response to food refusal [RTFR]); their constituent questions and how they were combined are shown in Table 1.

The appetite, oromotor dysfunction, and maternal feeding anxiety variable scores were skewed with a majority of subjects falling into 1 or 2 categories at 1 end of the distribution, so for most analyses, these were recoded into 3 categories: "normal" comprising 50% to 80% children, borderline, and high or low as appropriate (Table 2). The avoidant eating behavior and response to food refusal scores were all roughly normally distributed, and when necessary, they were divided into low, medium, and high categories (Table 2).

Growth Outcomes
All weights were converted into standard deviation (SD) scores compared with the United Kingdom 1990 growth reference.¹⁶ Overall weight gain and the prevalence of weight faltering were examined. For each child, all available weights within 4 age ranges (1–2, 2–6, 6–9, and 9–18 months) were identified and the average SD score per child for that time period calculated. These supplied SD scores at about the ages of 6 weeks and 4, 8, and 12 months. Weight gain was then assessed using the Thrive Index (TI), a measure of change in weight SD over time, conditional on initial weight (birth), which adjusts for regression to the mean.¹⁷ Weight faltering was defined, for any time interval, as conditional weight gain (TI) below the 5th percentile in the cohort as a whole from birth to that age, and this was defined as sustained if weight faltering was present in 2 of the 4 age bands.¹ The 5th percentile for weight gain varied from a fall of 0.9 weight SDS (birth to 6 weeks) to 1.3 SDS (birth to 12 months). This article concentrates mainly on the correlates of weight gain and faltering rated at ages 6 weeks and 12 months, the first reflecting sole milk feeding and the second established mixed feeding.

Analysis and Power
Spearman's correlations were used for univariate correlations. Multivariate predictors of weight gain (Thrive Index) were explored using linear regression with normally distributed predictor values entered as continuous data and skewed variables entered using the categories described previously. Predictors of weight faltering were explored using logistic regression with all the variables entered as categories. For both forms of regression, models were constructed by first simultaneously entering all variables found to be statistically significant (P < .05) in univariate analysis. Nonsignificant variables were then progressively removed from the model, starting with the least significant, until all remaining variables achieved statistical significance.

The concurrent validity of appetite was assessed using correlation with other relevant questions asked at 6 weeks and 12 months. All possibly relevant questions at each age were entered into a Spearman's correlation matrix with the appetite rating at that age. Those with correlation P < .05 were entered together into a linear multiple regression model with appetite as the dependent variable and then successively removed as noted previously.

The study was amply powered to detect moderate correlations between continuous variables (r = 0.2–0.3) but had only sufficient power (80% power at 95% probability) to detect a relative risk of weight faltering of >2.4, in a 15% subgroup, compared with the remainder.

	RESULTS

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The study recruited 1029 infants, of whom 68 infants born before 37 weeks' gestation were excluded, as well as 33 Ultra-Orthodox Jewish and 8 Muslim infants who showed major differences both in sociodemographic characteristics and in weight gain patterns, which will be the subject of a future article. This left 923 infants (915 mothers) of whom all but 7 (0.8%) were of white British origin; 71% of infants had mothers educated only to 16 years old and 24% lived in unwaged households; 48% were first-born, 50% were initially breastfed, and 25% remained so at 6 weeks; the mean (SD) age of weaning was 14.4 (2.9) weeks. The milk feeding¹⁸ and weaning¹⁹ characteristics of the cohort have been described elsewhere as have the effects of maternal characteristics on weight gain.¹

A questionnaire at 6 weeks was returned for 749 (81%) infants, of whom 734 (98%) had weights at mean (SD) ages 6.6 (0.83) weeks and 688 (92%) at 12.9 (1.5) months. Only 578 (63%) returned questionnaires at 12 months, but of these, 561 (97%) had weights around 6 weeks and 570 (99%) around 12 months. Those subjects who did not return questionnaires or have weights were significantly more deprived than the cohort as a whole, but all social strata were still well represented.¹

The mean (SD) weight standard deviation score was –0.16 (1.07) at birth, –0.02 (0.98) at 6 weeks, and +0.15 (1.03) at 12 months. In total, 92 children (10%) showed weight faltering at some time and 36 (4%) had sustained weight faltering in 2 of the 4 age bands. Of these latter, 22 were still faltering at 12 months, 10 had recovered, and 4 were lost to follow-up.

Feeding Behavior and Weight Gain at 6 Weeks
At 6 weeks, most mothers rated their infant's appetite as being very good (Table 2). Mild oromotor problems were seen in only one fifth of children and most mothers showed no evidence of feeding anxiety. In univariate analysis, all 3 of these factors were significantly related to weight gain between birth and 6 weeks, and appetite and maternal anxiety significantly predicted weight faltering to 6 weeks. However, in multivariable analysis, only appetite at 6 weeks remained strongly and oromotor problems weakly independently predictive of weight gain, whereas appetite at 6 weeks was the only independent predictor of weight faltering (Table 3).

Mothers responded to food refusal to a varying extent; the most common response (reported often or sometimes) at both ages was to encourage the child to eat (8 months: 81%; 12 months: 90%) and to offer alternative foods (8 months: 84%; 12 months: 85%). Mothers were less likely offer the same food later (8 months: 34%; 12 months: 33%). Few reported "making" the child eat (8 months: 7%; 12 months: 5%), but this was more common in those who often encouraged the child to eat (aged 8 months relative risk [RR]: = 4.3; P [²] = .003; 12 months RR: 4.5; P = .025) and at 12 months in those who often offered the same food later (RR: 6.6; P = .004). Mothers who tended to offer alternative food immediately or later were also significantly more likely to encourage to eat, but not to offer the same foods or force feed. This is probably why the internal reliability was low at both ages (Cronbach's = .38 at 8 months, 0.33 at 1 year). However, it would seem important to include all 5 possible responses in the composite score, because all represented active responses to food refusal.

Appetite rated at 6 weeks and 12 months, avoidant eating behavior and feeding anxiety rated at 12 months, and response to food refusal at both 8 and 12 months were significantly related to weight gain at 12 months (Table 4). In multivariable regression, both appetite ratings and the RTFR score at 12 months remained independently positively associated with weight gain (Table 4). Weight faltering at 12 months and sustained weight faltering were related to most of the feeding variables in univariate analysis (Table 5). In the multivariable model, appetite at both 6 weeks and 12 months remained a significant predictor of sustained weight faltering, as was the RTFR score at 8 months, whereas the RTFR score at 12 months was the only independent predictor of weight faltering at 12 months. Oromotor dysfunction at 6 weeks showed no relationship to weight gain or weight faltering at 12 months.

	DISCUSSION

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The research literature on the role of infant feeding behavior is fairly sparse, but various previous studies have found infants with failure to thrive rated by their mothers as having lower "appetite,"⁹ being less hungry,^{11, 14, 20} or eating fewer good-sized meals.⁹ Direct observational studies have shown varied results, ranging from striking differences in satiation¹² or parental feeding style¹³ to largely null results,⁴ which was the case in a linked observational study in this cohort.²¹ In this present study, parents made repeated ratings of their child's appetite using exactly the same terminology. As early as 6 weeks, these related significantly to both early and subsequent weight gain. The appetite ratings tracked to some degree, particularly through the later part of the first year, and it will be important, in the future, to examine the possibility that those with the best appetites may be at greater risk of subsequent overweight. Although mothers rated their child's appetite repeatedly over the first year, the indicators of appetite seemed different in the early weeks, when the volume of milk and the vigor of feeding were its main correlates, compared with later in the first year when it seemed to relate more to a general interest in and enthusiasm for food. This may be why appetite rated at both 6 weeks and 12 months independently predicted weight gain across the first year.

Appetite as a quality has previously tended to be studied more in relation to short-term influences, for example, in relation to short-term satiation.²² Even in the developing world, where undernutrition tends to relate strongly to socioeconomic circumstances, there has been a growing recent recognition that the child's own appetite plays an important role.^{23, 24} Engle, in Nicaragua, observed that mothers of children showing less appetite tend to take a more active role in feeding and suggested that "active" feeding was protective against undernutrition in these circumstances.²⁵ In that study, there was no difference in growth between the 2 groups of infants, but another study in the United States found an inverse association between maternal pressure to eat and fat mass in much older children.²⁶ In our study, children whose mothers promoted feeding highly consistently tended to grow less well, even after allowance for appetite. This may simply be because maternal rating of appetite does not fully describe the child's feeding style, with a more active maternal response to food refusal still simply being a response to their child's tendency to undereat or that mothers are more likely to pressure thinner children to eat. Alternatively, however, maternal pressure to eat may in some cases have an aversive effect, resulting in subsequent food avoidance; certainly, food avoidance in the child proved in all multivariate models to be "explained" by the appetite and response to food refusal variables. The actions reported by mothers in response to food refusal were not in themselves extreme. Very few reported "making" their child eat, but we could not distinguish responsive from intrusive actions, only the frequency of those behaviors. To have a negative effect, either the reported "encouragement" and offers of food would have to be more coercive than parents realize or simply so frequent as to interfere with their child's natural appetite patterns, which would be consistent with the fact that mothers who "encouraged" often were also more likely to take other more punitive actions. It is of note that no evidence was found in this cohort to suggest an association between underpromotion of feeding and faltering growth.

A previous study has suggested that subtle oromotor dysfunction may play an important role in failure to thrive,²⁷ and our previous work found that children with weight faltering were more likely to be reported retrospectively as having difficulty sucking, chewing, or swallowing. In this study, we did find a similar association with slower weight gain and higher rates of weight faltering at 6 weeks but not thereafter. It is possible, however, that had we been able to use a more sophisticated tool,²⁸ we might have found a more enduring relationship.

The strengths of this study were the substantial number of unselected children, studied prospectively, without prior labeling of any kind, although we must rely entirely on maternal ratings of her child's behavior. However, the use of different dimensions has allowed us to begin to disentangle child from parental behavioral characteristics. The numbers of children with clearly subnormal weight gain was small, but we had ample numbers to study predictors of weight gain in general, and these were largely consistent with the predictors of weight faltering. We could only describe weight faltering up to the age of 1 year when, in clinical practice, the most challenging cases will be those whose problems continue into the second and third year of life. However, we know from other studies that most such children have begun to falter early in the first year,^2–4 and these results may shed some light on why some recover early while others do not.

Our measures of behavior were relatively crude and many were being tested for the first time in this study, because at that time, no standardized feeding scale existed for this age range. However, the fact that all domains related significantly to weight outcomes in univariate analysis demonstrates that they have predictive as well as face validity, and future work will consider whether these could together form the basis for a more general infancy feeding scale.

Over half of those with sustained weight faltering also had persistently low rated appetite, but most infants reported as having low appetite did not have weight faltering. Therefore, a key clinical message is that many mothers probably worry about their child's appetite unnecessarily but that poor reported appetite in the context of low weight gain should be taken seriously. The concern then is that efforts to help infants eat more do not instead simply produce aversive reactions to feeding. This raises difficult questions about the best management approach for children with faltering growth with the possibility that well-meant advice could make matters worse. Trials of intensive intervention in weight faltering and failure to thrive have tended to have limited success,^29–31 although our own low key and largely dietary intervention produced both improved growth and, unexpectedly, better reported appetite.³ The challenge for clinicians in the future is to establish and formally evaluate preventive and treatment approaches that reduce, rather than increase, maternal anxiety, while maintaining or increasing their child's dietary intake.

	ACKNOWLEDGMENTS

 
Sport Aiding Research in Kids (SPARKS), Henry Smith Charity, provided funding for this study.

We thank Jayne Kelly, Anne Trail, Alison Smith, Jane Jarvis, and Ann Pattison for their work on the study; Philip Lowe for computing support; and Maureen Black and Patrice Engle for helpful comments on the manuscript. The study would not have been possible without the invaluable support of the midwives at the Gateshead and Newcastle maternity units, the health visitors of Gateshead, and the loyal participation of all the parents.

	FOOTNOTES

 
Accepted Sep 22, 2005.

Address correspondence to Charlotte M. Wright, Professor of Community Child Health, PEACH Unit, QMH Tower, Yorkhill Hospitals, Glasgow G3 8SJ, United Kingdom. E-mail charlotte.wright{at}clinmed.gla.ac.uk

	REFERENCES

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P³Rs:

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