key assessment

PEDIATRIC REVIEW

The role of responsive feeding in overweight during infancy and toddlerhood: a systematic review

KI DiSantis1, EA Hodges2, SL Johnson3 and JO Fisher4

1Center for Clinical Epidemiology and Biostatistics, School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; 2Family Health Division, School of Nursing, The University of North Carolina at Chapel Hill, Chapel Hill, NC, USA; 3Department of Pediatrics, Section of Nutrition, University of Colorado-Anschutz Medical Campus, Aurora, CO, USA and 4Department of Public Health, Temple University, Center for Obesity Research and Education, Philadelphia, PA, USA

A chronic mismatch of caregiver responsiveness to infant-feeding cues, such as feeding when the infant is not hungry, is hypothesized to have a role in the development of overweight by impairing an infant’s response to internal states of hunger and satiation. Although this concept of mismatch or discordance has long been acknowledged in scholarly writings, a systematic assessment of the evidence supporting the role of discordant responsiveness during infant feeding in the early origins of overweight is lacking. This review was undertaken to assess evidence for this hypothesized relationship between discordant responsiveness in feeding and overweight in infancy and toddlerhood, framed within the larger social-environmental context of the infant–caregiver dyad. A systematic method was used to extract articles from three databases of the medical, psychology and nursing fields. The quality of evidence collected was assessed using Oxford University Centre for Evidence Based Medicine’s level of evidence and through a narrative review. The systematic search resulted in only nine original research studies, which met a priori inclusion/exclusion criteria. Several studies provide support for the conceptual model, but most were cross-sectional or lower quality prospective studies. The need for consistent definitions, improved measures and longitudinal work is discussed. In conclusion, this review reveals preliminary support for the proposed role of discordant responsiveness in infant/child overweight and at the same time highlights the need for rigorous investigation of responsive feeding interactions in the first years of life.

International Journal of Obesity (2011) 35, 480–492; doi:10.1038/ijo.2011.3; published online 22 March 2011

Keywords: infant; feeding behavior; responsiveness; appetite regulation; self-regulation; overweight

Introduction

Infancy is believed to be a sensitive period for the develop-

ment of energy intake regulation1 and overweight.2–6 In the

first 2 years of life, infants and toddlers are dependent on

their caregivers to provide adequate and appropriate nutri-

tion. For this reason, the potential influence of feeding

dynamics on overnutrition and the development of over-

weight is seemingly intuitive. Scholarly work on early life

origins of overweight, however, has largely ignored the

possible impacts of social and behavioral transactions on

infant feeding. We focus on one particular aspect of these

caregiver–infant transactions: responsive feeding. In this

review, we define responsiveness within the context of

overweight, as involving prompt, contingent and develop-

mentally appropriate responses to the infant’s hunger and

satiety cues. As the review will describe, the degree to which

feeding interactions are responsive is believed to hold

importance in infant development by nurturing or impeding

the development of self-regulation. Self-regulation, generally

defined as ‘the ability to regulate reactionsyand to function

more independently in a personal and social context, (pg 93)’

is said to have multi-dimensional influence on functioning,

including behavioral, emotional and cognitive actions.7 The

early development of this general capacity is profoundly

affected by supportive caregiver–infant interactions and it is

likely that these interactions have a similar impact on the

development of eating self-regulation. We present a model in

which a caregiver’s responsiveness that is congruent with

infant-feeding cues encourages the development of infant self-

regulation as it relates to energy intake, and eventually obesity.

Overweight and accelerated weight gain in infancy and toddlerhood

The problem of pediatric overweight is evident before the

preschool years. Data collected in the National Health and Received 21 June 2010; revised 6 December 2010; accepted 26 December

2010; published online 22 March 2011

Correspondence: Dr KI DiSantis, School of Medicine, Center for Clinical

Epidemiology and Biostatistics, University of Pennsylvania, 8th floor Blockley

Hall, 423 Guardian drive, Philadelphia PA 19104, USA.

E-mail: [email protected]

International Journal of Obesity (2011) 35, 480–492 & 2011 Macmillan Publishers Limited All rights reserved 0307-0565/11

www.nature.com/ijo

Nutrition Examination Survey 2007–2008 indicated that

approximately 10% of infants and toddlers were above the

95th percentile for weight-for-length; the prevalence was as

high as 14.9% in Hispanic males.8 These numbers are

of concern because heavy infants are at increased risk of

overweight in later stages of development.9,10 Analysis of the

CDC Pediatric Nutrition Surveillance System data revealed

that overweight infants (0–11 months) were 2.9–4.3 times

more likely to be overweight between the ages of 1 and 4

years than non-overweight infants.11 Accelerated weight

gain during the first 2 years of life, independent of birth

weight and parental weight status, has also been associated

with a greater risk of overweight during childhood12–17 and

young adulthood4,18–21 (see Stettler and Iotova22 for a

review). Though discussion of etiology has favored biological

explanations, caregiver–infant feeding interaction, like re-

sponsiveness, is implicit when considering the potential

contributing factors of infant weight gain.14,23

Caregiving and self-regulation among infants and toddlers

Why might caregiver responsiveness be a formative dimen-

sion of feeding during the first 2 years of life? Responsiveness

is a dimension of infant–caregiver interactions, which has

been said to shape an infant’s ability to acquire self-

regulation.7 Early relationships with caregivers engender an

infant’s development in numerous ways, but a supportive

environment to enhance the development of self-regulation

of energy intake holds unique importance for childhood

obesity risk. Supporting infant self-regulation of energy

intake may provide the necessary conditions to facilitate

development of regulatory capacity and autonomy through-

out infancy and into childhood. It is believed that infants

and young children are born with a nascent capacity for self-

regulation that becomes actualized through cause–effect

learning, which occurs when their behavior is consistently

met with a prompt, developmentally appropriate response.24

Responsive caregiving has been studied for decades in

domains outside of child feeding and growth, and has been

positively associated with a wide range of developmental

outcomes in infancy and early childhood including

emotional, language and cognitive capacity, as well as the

security of attachment to the mother (see Ziv et al.25 for a

review). Such synchronous interactions are thought to

provide fundamental support for opportunities to learn

mastery and self-regulation.26 Early infant emotions, for

example, stem from physical states, including temperature,

sleep states and hunger.7 Newborns exhibit emotional

reactivity to these physical states and express discomfort

via crying, but begin to show signs of self-regulated behavior

by 3 months of age.27 Examples of self-regulated behavior

include turning the body or head away from undesirable

stimuli and moving the hands toward the head and mouth.7

Caregivers support this developmental progression from

emotional reactivity to self-regulation by their consistent,

accurate and appropriate responses to infant cues, which

foster expectations in the developing infant about predict-

able patterns of interaction.7 However, accurate interpreta-

tion by caregivers is complicated by the fact that infant

crying can reflect discomfort due a variety of physical states

including sleep, temperature and hunger states.28 Thus, it

should be acknowledged that caregiver and child are

mutually influencing one another over time through the

consistency, meaning and appropriate interpretation of one

another’s behaviors.

Caregiver influences on the infant’s development of

self-regulation of feeding behavior parallels emotional devel-

opment. In their monthly feeding observations of 26 mother–

infant pairs over the first year of life, Ainsworth and Bell29

observed that mothers who exhibited more sensitive pacing

and prompt responses to the infant during feeding had infants

who cried less in early infancy and demonstrated greater

attachment to their mothers at the end of the first year,

compared with mothers who adhered to rigid feeding

schedules. This supports the hypothesis that caregiver respon-

sivity affects infant outcomes and development.30,31 However,

the relationship between caregiver and infant is bidirectional

and can also be affected by the clarity of infant cues.32,33 Some

infants demonstrate ambiguous signals, and have fewer

behaviors in general, including fewer elicited and spontaneous

vocalizations, fewer smiles, less gaze and joint attention and

poor signals to indicate their needs (including hunger cues). In

such cases, a caregiver’s responsiveness might be discordant

with infant needs (due to poor clarity of cues) or might be a

low level because few cues are exhibited.

To this notion, Wright and colleagues34,35 have argued

that appropriate responses to infant-feeding cues are critical

for self-regulation and self-control of food intake to develop

to its fullest potential. This argument is evidenced by

experimental studies, which have demonstrated that infants

as young as 6 weeks of age could adjust the volume of

formula intake in response to its energy content to maintain

daily energy intake.36–38 Observational research has also

provided evidence of such a capacity, including data from

3022 children (6 to 24 month old ) participating in the

Feeding Infants and Toddlers Study showing inverse relation-

ships between the number of daily feeds and the size of

feeds.39 In the context of developmental literature on

responsive parenting, self-regulation of energy intake in

infancy and toddlerhood is viewed as the extent to which

feeding environments and interactions allow the biological

potential of the child for self-regulation to be actualized.40

A potential role for responsive feeding

Although contribution of responsive feeding to self-regula-

tion and overweight in early development has been

Responsive feeding and infant overweight KI DiSantis et al

481

International Journal of Obesity

suggested in scholarly writings for decades,35,41–44 systematic

inquiry appears limited. This review was undertaken to

characterize empirical support for the assertion that varia-

tion in the concordance of a caregiver’s responsiveness and

an infant’s hunger and satiety cues has a fundamentally

important role in growth by supporting energy self-regula-

tion in infancy and toddlerhood. Figure 1 presents the

conceptual framework that guided the review by articulating

potential pathways through which caregiver responsiveness

to infant-feeding cues influences child intake and growth.

Drawing from the developmental literature, feeding respon-

siveness is defined for the purposes of this review as prompt,

contingent and developmentally appropriate responses to

the child’s hunger and satiety cues.24,45 The bidirectional

nature of feeding is implicit in this definition, with the

caregiver dependent on the infant to provide clear, un-

ambiguous cues and the infant dependent on the caregiver’s

accurate interpretation of and appropriate response to those

cues for obtaining adequate and appropriate nutrition.

Given the aforementioned variance in the clarity of infant-

feeding cues, caregivers may be challenged to a lesser or

greater degree in their interpretation of cues. Likewise, less-

responsive caregivers may challenge the infant to provide

clearer cues (within a repertoire that may be relatively

limited in the first months of life). Thus, when we refer to

caregiver feeding responsiveness, we are referring to a

characteristic of the caregiver–child dyad’s level of concor-

dance in interactions during feeding. Responsiveness to

child-feeding cues has previously been included as part of an

internationally recognized framework of infant-care

practices oriented toward the prevention of malnutrition

and the support of child mental, social and physical

development.31,44,46 In that work, responsive feeding has

been broadly conceptualized to involve the caregiver’s

adaptation to the child’s psychomotor abilities for feeding

and provision of a structured feeding environment with a

goal of facilitating energy consumption to offset the effects

of malnutrition.44 In contrast, this review focuses solely on

the role of caregiver responsiveness to feeding cues in

supporting the capacity of infants to self-regulate energy

intake for optimal growth in a context of obesity risk.

Figure 1 was developed drawing from scholarly writing

dating back almost a half century.35,41–44 In this model,

discordant caregiver responsiveness to infant cues, specifi-

cally feeding without hunger and feeding beyond satiety, is

hypothesized to impair infant-satiety response. Such impair-

ments are suggested to promote energy intake beyond needs

for growth via increases in meal size and/or feeding

frequency. Overweight and rapid weight gain during infancy

and toddlerhood are the main growth-related outcomes of

interest. This model acknowledges feeding responsiveness as

being nested within a broader social-environmental context

that influences the way in which caregivers feed their

children,47 including cultural influences (e.g., ethnicity/

race48), policy and prevailing feeding guidance (e.g., World

Health Organization Recommendations on Breastfeeding49),

parental beliefs/goals/values,50 and parental knowledge of

development.51 These are all the factors brought in to the

feeding relationshipFand all can have considerable effects

on the relationship. This model acknowledges these ele-

ments, which are at the foundation of building a responsive

feeding relationship. The review was initiated to assess the

amount and quality of empirical evidence available to

support this proposed model.

Materials and methods

Literature-search strategy

We performed a systematic literature review of responsive

feeding using the three major databases from three dis-

ciplines (medicine, psychology and nursing): MEDLINE via

PubMed (United States National Library of Medicine,

Bethesda, MD, USA), PsycINFO (American Psychological

Association, Washington, DC, USA) and CINAHL (Ebscohost,

Glendale, CA, USA). These databases were searched for

articles listed from the database’s inception to September

2009. Database limits were used to restrict the search to

research in humans and infants (from birth to 24 months).

As listed in Table 1, a list of 25 search terms were generated

by the research team to identify relevant articles addressing

Accelerated Weight Gain/ Overweight

Accelerated Weight Gain/ Overweight

Infant Caregiver

Clarity of Hunger and Satiety Cues

Discordant Feeding

Responsiveness

Discordant Feeding

Responsiveness

Increased Feeding Frequency/Amount Increased Feeding Frequency/Amount

Accurate Interpretation

Developmentally Appropriate Response

Awareness Of Feeding Cues

Impaired Self-Regulation •Diminished satiation/satiety

•Increased energy intake

Impaired Self-Regulation •Diminished satiation/satiety

•Increased energy intake

Figure 1 Figure 1 presents a model for the pathway from discordant feeding

responsiveness to accelerated weight gain and/or overweight. This model

suggests that chronic mismatch between a caregiver’s responsiveness and an

infant’s feeding cues can result in increased feedings (amount and/or

frequency), which eventually lead to the acceleration of weight gain and

overweight via impaired infant self-regulation. A caregiver’s responsiveness

refers to both the amount and quality of responsive behaviors. The model

illustrates that caregiver and infant relationship is reciprocal, which is

impacted by the clarity of infant cues. The model also acknowledges that

the caregiver–infant dyad exists within a socio-environmental context, which

might impact the relationship.

Responsive feeding and infant overweight KI DiSantis et al

482

International Journal of Obesity

the concepts outlined in the conceptual model (Figure 1),

including responsive feeding, self-regulation, feeding/

hunger cues, as well as terms related to obesity, such as rapid

weight gain. The phrases/terms in quotations were searched

for the exact phrase/term, whereas the other terms were not

put in quotations to allow for a variety of combination terms

to be searched. All search terms that included the word ‘Infant’

were repeated using the term ‘Child’ to ensure an extensive

search of the infant population.

Study selection and grading

Article titles and their abstracts were briefly reviewed by the

first author (KI DiSantis) using the selection criteria. Those

that met and questionably met the inclusion/exclusion

criteria were then thoroughly reviewed for eligibility by all

the authors. Inclusion criteria included the following:

original research, published in English, published up to

September 2009, involving healthy full-term infants, aged

0–24 months of child age, including infant feeding/eating

and/or infant weight/growth outcomes, and oriented toward

child overweight/rapid weight gain and/or obesity. Owing to

concerns about socioeconomic and cultural consistency

across studies, and the goal of focusing on overnutrition

and obesity (as opposed to slow growth and malnutrition),

exclusion criteria included research conducted in developing

countries. In addition, given the focus on infant overweight

and obesity, research that focused on growth faltering

(organic or non-organic) or low birth weight was excluded.

Although including growth faltering and malnutrition

studies would increase the quantity of articles extracted,

they likely would not have added to the content of this

review as responsive feeding in these studies are investigated

in relation to a very different set of outcomes, including

promotion of energy intake and weight gain.

The quality assessment phase measured the level of

evidence provided by each included study and utilized the

Oxford University Centre for Evidence Based Medicine

(CEBM) levels of evidence system.52 This system was

developed to be an advancement of the Canadian Task Force

on the Periodic Health Examination grading system of 1979.

The ‘level’ of evidence is graded, primarily based on the rigor

of the study design (e.g., randomization in interventions),

sampling (e.g., response rate), longitudinal versus cross-

sectional, outcome assessment (e.g., negative assessment if

outcome measure is imprecise) and the follow-up rate, with

‘1a’ being the highest and ‘5’ being the lowest level. Levels of

evidence were independently assigned to the included

papers by two of the study authors. A consensus approach

was used to resolve discordant assessments, in which a third

reviewer independently graded the article and discussion by

all authors was used to assign a final rating.

Results

Systematic review results

The results of the systematic review are detailed in Table 1

and illustrated in Figure 2. The search of three databases with

25 aforementioned keywords provided 1877 hits. Owing to

the fact that these databases contain subscriptions to the

same journals or indexes, it was not possible to derive a

unique number of hits. After elimination of redundant

abstracts, 82 unique abstracts were deemed appropriate for

full-abstract review based on the first author’s brief review of

article titles and abstracts. These abstracts were then

thoroughly reviewed by all authors based on the a priori

inclusion/exclusion criteria described above to determine

whether they would be selected for final analysis. First, 14

articles were excluded because they were not original

research studies, performed research in a population other

than infants of 0–24 months and/or the research was

performed with regard to malnutrition/growth faltering

(Figure 2). The 68 remaining articles were assessed to

determine whether some aspect of infant/child obesity was

directly measured (eating behavior, intake weight and/or

growth) and whether caregiver-feeding practices/behaviors

were assessed (Figure 2). A total of 29 articles were excluded

because some aspect of infant overweight/obesity or infant

eating/intake outcomes was not directly measured. In most

of these excluded cases, feeding observations or other

feeding measures were used as a tool to investigate general

parental responsiveness or general infant–caregiver

Table 1 Systematic review search results by search term

Search terms Number

of hits

from three

databases

Abstracts

selected for

detailed

review

Abstracts

selected

as meeting

criteria

for CEBM

grading

Responsive feeding 6 5 0

Caregiver feeding styles 6 2 0

Rapid weight gain and eating 6 2 0

Infant feeding and responsiveness 85 13 0

Child feeding and responsiveness 43 0 0

Self-regulation and eating 19 3 0

Infant-feeding cue or infant-feeding cues 13 1 0

Parent feeding styles 12 1 0

Rapid weight gain and Feeding 24 3 1

Feeding interactions 94 13 1

Infant feeding practices 328 9 2

Feeding and satiety response 7 2 1

Infant and satiety response 8 4 0

‘Infant growth’ and overweight 107 2 0

‘Infant feeding’ and obesity 99 3 2

Child and hunger cues 10 0 0

Child and fullness cues 1 0 0

Infant and hunger cues 20 2 0

Infant and fullness cues 1 0 0

Satiety cues and infant 12 2 1

Satiety cues and child 3 0 0

Internal cues and infant 26 1 0

Internal cues and child 18 0 0

Self-regulation and infant nutrition 41 5 1

‘Care for development’ and feeding 888 9 0

Total 1877 82 9

Abbreviation: CEBM, Oxford University Centre for Evidence Based Medicine.

Responsive feeding and infant overweight KI DiSantis et al

483

International Journal of Obesity

interaction, but the observations were never presented in the

context of infant eating/intake outcomes or were not

directed toward obesity outcomes child overweight/obesity.

Overall, 30 articles were excluded because of lack of

assessment of caregiver-feeding practices/behaviors, for

instance, in which feeding characteristics and infant growth

might have been assessed but no aspect of responsiveness

was measured. After screening all abstracts, a total of nine

articles met the inclusion/exclusion criteria and were

included in the systematic review (Figure 2).

The results of evidence-level grading for the nine articles,

based on CEBM criteria, are provided in Table 2. All articles

were graded as being a ‘2c’ level or lower level, meaning the

design was cross-sectional or a lower quality cohort study or

case–control study. Table 2 also provides additional details

related to the quality of the research studies, including

sampling characteristics, methods of measuring feeding

responsiveness and a brief outcome summary. Below we

briefly review these articles and their implications following

the framework of the conceptual model in Figure 1.

Narrative review

Socioenvironmental context of discordant responsiveness. Feed-

ing interactions take place within a wider social-environ-

mental context, consisting of a wide range of factors like

biobehavioral issues, culture, psychosocial status, physical

environments and history at individual, family and com-

munity level. Mogan53 was the only article in the review that

considered context, by evaluating associations of both

parental and infant weight status with maternal sensitivity

to infant cues. Parental weight status is an individual-level

variable, but in this study they accounted for the differences

between dual and caregiver households with varying combi-

nations of parents classified as normal or overweight.

Parental weight status was categorized into three groups:

(1) two normal weight parents, (2) one overweight and one

normal and (3) two overweight parents. Mothers and infants

were observed during six feeding sessions from age 0 to 6

months to assess feeding interactions. The observations were

coded using the Nursing Child Feeding Assessment Scale,

which contained the following subscales: mother’s sensitiv-

ity to cues, response to distress, social –and emotional

growth fostering, cognitive fostering and the infant’s clarity

of cues and responsiveness to their mother. This measure,

particularly the mother’s sensitivity to cues and infant

responsiveness subscales, allowed for the assessment of

discordance in responsiveness in a bidirectional manner as

presented in Figure 1. Although the methodology was

strong, the authors did not find that these responsive

feeding behaviors of the mother and/or infant differed

among the parental weight groups. However, infant weight

status differed significantly at 6 months of age according to

parent weight group, with infants who had one or two

overweight parents being more likely to be at or above the

90th percentile for weight. Mogan53 did not report on

relationships between maternal feeding responsiveness and

infant weight status at 6 months, so it is unclear whether any

relationship existed in this sample. Although this study used

observational data, which assessed the bidirectional feeding

relationship, it neither found relationship between parental

weight status and responsive maternal–infant feeding inter-

actions nor did it report on the association of responsive

feeding with infant weight at 6 months. Other studies of

older children have connected maternal weight status with

unresponsive feeding practices (i.e., restriction in feeding),54

but are outside the developmental scope of this review.

Discordant responsiveness and feeding frequency and amount. As

Figure 1 illustrates, discordant responsiveness in feeding

might lead to increased feeding frequency or amount.

Numerous circumstances of discordance could combine to

result in increased feeding frequency (including feeding an

infant in the absence of hunger cues, misperception of

hunger cues) and increased amounts of food (including

ignoring fullness cues, or misperception of fullness cues). If

this were to continue over a period of time, the risk of

increased energy would increase. Kavanagh et al.55 per-

formed a double-blinded, randomized intervention, which

focused on using education on feeding responsiveness and

prevention of overfeeding to reduce the risk of overfeeding

(infants were 3–10 weeks at enrollment). The control group

82 studies identified for full abstract review

4 excluded due to not being original research

8 excluded due to sample being malnourished, premature, or having other health problem

involved in eating and/or weight

68 studies performed in samples with healthy infants 0-24 months

9 original research studies performed in samples with healthy infants 0-24 months with obesity

outcomes and measuring and/or feeding and eating included in evidence-based systematic review

78 studies original research

76 studies performed in sample aged 0-24 months

39 studies performed in samples with healthy infants 0-24 months

with obesity outcomes

29 excluded due to outcome not being a direct measurement of

obesity

30 excluded child eating or maternal feeding was not either

predictor or outcome

2 excluded due to sample age

Figure 2 Flow diagram of article extraction.

Responsive feeding and infant overweight KI DiSantis et al

484

International Journal of Obesity

Table 2 Systematic review results

Article Design, setting and variables Sample

characteristics

Measure of responsiveness

(type, description)

Summary of results CEBM

level

assigned

Social-environmental context of discordant responsiveness

Mogan53 Design: prospective cohort

Setting (country): US

Independent variable(s)/intervention:

Parents’ weight status (1 parent

overweight, 2 parents overweight,

2 parents normal weight)

Outcome(s): parent–child

interaction during six feedings

from 0 to 6 months and infant

weight status.

n¼78 for feeding

behavior analysis

n¼62 for infant

weight status

analysis

Age: 55–70 h

Age(s) at

follow-up:

0–6 months

Race/ethnicity:

88.5% White,

5.1% Asian, 2.6%

East Indian, 1.3%

Black and 2.6%

other.

Type: observational measure

Description of measure: Nursing

Child Feeding Assessment Scale,

subscales: maternal sensitivity to

cues, clarity of child cues, child’s

responsiveness to parent during

feeds.

Feeding behaviors did not differ

among the parental weight groups

but a higher proportion of infants

with two overweight parents

had a growth percentile X90th

percentile at 6 months.

2c

Discordant responsiveness and increased feeding frequency/amount

Kavanagh

et al.55

Design: double-blind, RCT

Setting (country): US

Independent variable(s)/intervention:

educational intervention with

general feeding guidelines and

information on awareness of

infant-satiety cues (single, 45-min

session); Control participants

received general feeding

guidelines only.

Outcome(s): formula intake

(ml h�1; non-weighed, 2-day

record) and weight gain.

n¼61 at BSL

n¼38 at follow-up

Age: 3–10 weeks

Age(s) at follow-

up: 4–5 months

Race/ethnicity: not

reported.

Type: Educational intervention

Description of measure:

intervention group received

feeding responsiveness

education, in addition to

general infant-feeding

guidelines.

The intervention group did not

differ significantly in formula intake

or weight gain in the hypothesized

direction, as the control group

reported lower formula intake

at 4–5 months and the intervention

group had greater weight gain

(grams per week).

2b

Discordant responsiveness and impaired self-regulation

Rybski et al.56 Design: cross-sectional

Setting (country): US

Independent variable(s)/

intervention: maternal behaviors

during bottle feedings during six

feedings over a 24-h periods

Outcome(s): Infant-eating

behaviors (total feeding time,

sucking behaviors) and Infant

energy intake (24-h weighed

record).

n¼10

Age: 72 h

Race/ethnicity:

100% White.

Type: Observational measure

Description of measure:

observed maternal behaviors

during feedings (verbal

interaction, eye contact,

tender and caretaking

touching).

No association between the

measured maternal feeding

behaviors and either infant

eating behaviors or 24-hour

energy intake, but it is important

to consider that mothers were

not allowed to hold their infants

during any feeds, which would

clearly limit the amount of

behaviors a mother can perform.

4

Discordant responsiveness and infant weight gain/overweight.

Baughcuma

et al.70 Design: cross-sectional

Setting (country): US

Independent variable(s)/intervention:

child overweight (o90th percentile)

and mother’s obese status

(BMI X30)

Outcome(s): infant-feeding

styles.

n¼453

Age: 11–24

months

Race/ethnicity:

77% non-Hispanic

White, 16.6% non-

Hispanic Black,

1.4% Hispanic

White and 5%

others

Type: Self-report survey

Description of measure: Infant

Feeding Styles Questionnaire

(IFQ), subscales: Awareness of

infant’s hunger and satiety

cues, Feeding infant on

schedule, using food to calm

infant’s fussiness, social

interaction with infant

during feeding

The IFQ subscales failed to associate

responsive feeding behaviors to

concurrent weight status of either

infant (11–23 months) or mother.

2c

Dubois et al.69 Design: case–control

Setting (country): Canada

Independent variable(s)/intervention:

Infant weight status (Obese cases

(o90th percentile), normal controls

(25th–75th percentile))

Outcome(s): energy intake (3-day

non-weighed, record) and

maternal-feeding practices

n¼89 (47 cases,

42 controls)

Age: 4–9 months

Race/ethnicity: not

reported.

Type: qualitative self-report

Description of measure:

Open-ended questions on

mother’s past feeding practices

(e.g., breastfeeding) and

mother’s concepts and

attitudes toward infant

feeding.

Maternal responsiveness was an

identified theme. Obese and control

infants did not differ in the following

maternal responsiveness to feeding,

energy intake, or in her timing of

breastfeeding cessation or

supplementation introduction.

3b

Responsive feeding and infant overweight KI DiSantis et al

485

International Journal of Obesity

(n¼ 21) received a 45-min educational session on general

guidelines for infant feeding, including appropriate age of

introduction of complementary foods, safe preparation of

complementary foods, responsive feeding practices, when

feeding complementary foods, and information on low-cost

ways of providing nutritionally balanced meals. The inter-

vention group (n¼19) was given similar information but

additionally provided with educational information on

being aware of infant-satiety cues when breastfeeding or

bottle feeding (e.g., understanding early versus late cues) and

were encouraged to only prepare 6 ounces of formula per

feeding. The outcome measures were both infant weight and

length and formula intake (measured at baseline, 2 weeks

after the class and at about 4 months. Kavanagh et al.55

found no differences between the intervention and control

groups with regard to formula intake at any of the time

points and bottle-emptying behavior, and conversely the

intervention group infants were heavier and taller at 4

months. Thus, this study did not provide support for the

conceptual model. Kavanagh et al.55 acknowledged short-

comings in this small study including that at baseline

the intervention group infant’s were taller and heavier than

the control group, the bottle records were not weighed

and a considerable loss to follow-up rate with only 38%

Table 2 (continued)

Article Design, setting and variables Sample

characteristics

Measure of responsiveness

(type, description)

Summary of results CEBM

level

assigned

Farrow and

Blissett62

Design: prospective cohort.

Setting (country): UK

Independent variable(s)/intervention:

Maternal control in feeding

at 6 months.

Outcome(s): Infant growth

(standardized to reference

adjusting for age and gender)

from birth to 6 months and from

6 to 12 months.

n¼69

Age: 6 months

Age(s) at

follow-up:

12 months

Race/ethnicity: not

reported.

Type: observational

Description of measure: Feeding

Interaction Scale, a coding

system for feeding observations

measuring maternal control

and infant autonomy.

Maternal control moderated infant

weight gain, with infants’ low

control mothers regulating their

growth from birth–12 months

and infants’ high control mothers

having poor growth regulation.

Breast-fed infants had mothers

that were less controlling

than non-breastfed infants.

2b

Li et al.64 Design: -prospective cohort

Setting (country): US

Independent variable(s)/intervention:

BF intensity (% all milk feedings

that were breastmilk) and bottle–

emptying behaviors (maternal

self-report), at multiple time

points from 1 to 6 months.

Outcome(s): excess infant weight

gain from 7 to 12 month old.

n¼1896

Age: B1 month

Age(s) at follow-

up: 2–12 mon

Race/ethnicity:

83.6% non-

Hispanic White,

6.9% non-Hispanic

Black and 9.5%

Hispanic.

Type: Self-report survey

Description of measure: survey

of infant’s bottle use behavior

(four 5-point Likert scale

questions), focused on bottle

emptying and mother’s

encouragement to finish

a bottle.

High breastfeeding intensity resulted

in significantly reduced excess weight

gain. Infants who often emptied

bottles in the first 6 months of life

were 69% more likely to have excess

weight gain in the second half of

infancy, compared with those who

rarely emptied bottles, but mother’s

self-reported encouragement to

empty bottles was not related to

excess weight gain.

2c

Saxon et al.60 Design: retrospective cohort

Setting (country): US

Independent variable(s)/intervention:

Infant weight, length, head

circumference at birth, 2, 4- and

6 months.

Outcome(s): mother’s reported

feeding practice from birth to

9 months.

n¼48

Age: 12 months.

Race/Ethnicity:

81% White, 11%

Hispanic, 3% black

and 3% Asian.

Type: Self-report survey

Description of measure: feeding

practices survey (14-items)

focused on demand and

scheduling feeding (e.g., who

(mother or baby) determined

when the baby ate; does

mother recognize fussiness

as a hunger cue).

Feeding style (on-demand versus

scheduled) was not associated with

any growth variables across the first

year of life. However, predicting

growth changes based on current

feeding styles might not capture

the prospective effect of feeding

on growth, as current feeding

behaviors might have changed in

response to infant growth changes.

4

Worobey et al.65 Design: prospective cohort.

Setting (country): US

Independent variable(s)/intervention:

maternal sensitivity to infant-feeding

cues and infant-feeding record

(24-h recall) at 3 and 6 months.

Outcome(s): Infant weight gain

from birth–3 months, 3–6 months

and 6–12 months.

n¼96

Age: newborn

(enrolled at first

WIC visit)

Age(s) at

follow-up: 3, 6

and 12 months.

Race/ethnicity:

76% Hispanic and

24% Black.

Type: observational

Description of measure:

maternal sensitivity to cues

subscale of the Nursing Child

Feeding Assessment Scale.

Infants gained more from 6 to 12

months if their mothers were less

sensitive to satiety cues. Also, infants

whose mother’s reported a greater

number of feeds per day had greater

growth from 6 to 12 months.

Growth between other time points

were not significantly related to the

feeding variables.

3b

Abbreviations: BMI, body mass index; BSL, baseline; BF, breastfeeding; CEBM, Oxford University Centre for Evidence Based Medicine; RCT, randomized control trial;

UK, United Kingdom; US, United States; WIC, United States Special Nutritional Supplement Program for Women, Infants and Children. aNote: Two studies were

presented within this article, but only the study performed within an infant sample was presented in this review.

Responsive feeding and infant overweight KI DiSantis et al

486

International Journal of Obesity

of the original sample completing both the class and the

assessments.

Rybski et al.56 similarly studied the associations between

maternal feeding behaviors and infant intake, in a small

sample of 3-day-old female, white infants. Although the

study observed maternal behaviors related to responsiveness

during bottle feedings (i.e., verbal interaction, eye contact,

tender and caretaking touching), the purpose of the study

was to observe changes in sucking behaviors and intake of

formula across a 24-h period to understand the potential

effects of circadian periodicity. The feeding variables (e.g.,

total feeding time, nutritive sucking time nutritive sucking

count) were measured during six observations set at the same

time for all participants across a 24-h period in a stimuli-free

room, with controlled temperature and lighting. This study

did not find an association between maternal feeding

behaviors and infant energy intake. A potential source of

bias for evaluating feeding responsiveness was that mothers

were not allowed to hold their infants during any feeds,

which could have limited the amount and type of (e.g.,

touching) behaviors a mother was engaged in during a

feeding. In view of these shortcomings of these studies,

additional research is needed to evaluate the effect of

caregiver awareness of infant-feeding cues on infant energy

intake and subsequent weight gain.

Discordant responsiveness and impaired self-regulation. As

shown in Figure 1, we suggest that caregiver feeding

responses that are discordant with infant hunger and

fullness cues could led to impaired satiety response in the

infant. Experimental and observational studies have shown

that infants and toddlers possess an ability to self-regulate

energy intake at and across eating occasions by adjusting

food intake in response to changes in feeding frequency and

the energy content of foods consumed.57–59 Responsive

caregiving is believed to promote cause (i.e., infant cue)

and effect (i.e., caregiver response) learning that is central to

the development of self-regulation.24 Some have suggested

that chronically unresponsive feeding may negatively influ-

ence what children learn about when eating should begin

and end.40,41 This systematic review, however, did not

identify any research that has evaluated the assertion that

feeding interactions affect infant satiation. As such, there is

currently no evidence to suggest that responsiveness influ-

ences child self-regulation of energy intake in infancy or

toddlerhood. The notion that feeding children in the

absence of hunger and continuing to feed beyond fullness

is detrimental to the development of self-regulation has

appeared in scholarly writing for well over half a century.

The findings of this review suggest the need for research

explicitly measuring dimensions of appetite regulation,

including hunger, satiety and satiation. Owing to a lack of

studies and negative finding, evidence that feeding respon-

siveness influences infant self-regulation of energy intake

remains weak.

Discordant responsiveness and accelerated weight gain and overweight

Compared with other areas of the model, a relatively greater

number of studies were identified involving the association

of responsiveness to infant cues with infant weight status

and weight gain. Saxon et al.60 studied maternal feeding

behaviors and subsequent weight gain. The feeding beha-

viors focused on in Saxon et al.,60 measured whether a

mother reported using demand or schedule feeding in the

first 6 months of life, rather than more directly assessing

responsiveness as we have described. However, the authors

describe demand feeding in the same manner as we have

describe responsive feeding, in which the caregiver would

initiate feeding in response to infant-hunger cues, rather

than based on the external factor of time. Mothers retro-

spectively self-reported their feeding practices from birth to

6 months, and were then classified as demand or schedule

feeders based on the answers to these two questions:

(1) I would classify my feeding philosophy as: (answers:

‘Feeding on demand’ or ‘Feeding on a schedule’) and (2) Who

would you say usually determined your baby’s eating routine?

(answers: ‘Me (myself/caregiver)’ or ‘Baby’). They reported

that feeding style did not significantly predict infant weight

gain at 2, 4 and 6 months (controlling for birth weight).

Although Saxon et al.60 findings do not support a relationship

between maternal feeding style and infant’s future weight

status as proposed in the model, a few shortcomings must be

noted. Foremost, demand versus scheduled feeding does not

explicitly capture ‘responsive feeding’ as we have defined it.

Also breastfeeding was not controlled for during analyses,

even though it has been linked to growth particularly in the

first 2 years of life,61 and the two groups had differential levels

of breastfeeding.60 Lastly, evaluating growth (i.e., change with

time) may have been more informative than assessing weight

at each time point controlling for birth weight.

Farrow and Blissett62 examined a well-researched aspect of

responsive feeding, maternal control and its moderating

effects on infant weight gain in the first year of life. Relative

to the other studies reviewed, the maternal behavior of

interest was well aligned with the definition of ‘responsive

feeding’ used here. Maternal control was measured through

the systematic coding of feeding observations (using the

Feeding Interaction Scale,63 in which the observer rates the

mother on a 1–9 scale, with 1 equaling a very controlling

caregiver (e.g., mother is continuously forcing the infant to

eat) and 9 equaling not controlling (e.g., mother is allowing

the infant autonomy to control his or her own feeding,

although supervising the infant). Infant weight was mea-

sured at 6 and 12 months (birth weight was taken from

hospital records). They found that infant weight gain from

birth to 6 months, and from 6 to 12 months were negatively

correlated, indicating that infants appear to self-regulate

their weight in the first year of lifeFhowever, this was only

found in infants with low maternal control in feeding.

Infants with high-maternal control in feeding had the

opposite patternFweight gain from birth to 6 months and

Responsive feeding and infant overweight KI DiSantis et al

487

International Journal of Obesity

from 6 to 12 months was positively correlated, so that a high

weight gainer from birth to 6 months would continue on the

path of high weight gain. This suggests that, although

infants have the capability of self-regulation of energy intake

and weight gain, there is an interaction with the environ-

ment (caregiver feeding control) that can modify the

expression of this potential. Farrow and Blissett’s62 work

offers insight into the role of one aspect of responsive

feeding (maternal control) and infant growth. The prospec-

tive nature of the study along with rigorous measures helps

to add support to the model proposed here.

In a more recent investigation identified, Li et al.64

reported on a population-based survey of US mothers, which

investigated whether breastfeeding duration and frequency,

and exclusiveness and bottle-emptying practices predicted

excess infant weight gain in the interval between 6 and

12 months. These feeding practices were self-reported at

multiple time points from birth to 6 months. Findings

revealed that infants who often emptied bottles in the first 6

months of life were 69% more likely to have excess weight

gain in the second-half of infancy (6–12 months), when

compared with those who rarely emptied bottles.64 Also,

high breastfeeding intensity (combination of duration and

frequency) resulted in significantly reduced excess weight

gain. This study explores the ‘what’ of infant feeding

(breastmilk versus formula), which is often focused on with

relation to obesity, but also explores the ‘how,’ through the

effects of bottle emptying. These findings highlight

behavioral aspects of infant feeding, which affected infant

weight gain in this large sample (n¼1896). An issue in

interpreting these findings is the extent to which bottle-

emptying behaviors reflected infants’ appetites versus

caregivers’ responsiveness to infant-feeding cues. Additional

research is needed to address this issue.

Worobey et al.65 assessed the association of infant growth

with maternal-feeding attitudes related to responsiveness for

their association with infant growth in a sample of low

income, minority women and their newborn infants.

Maternal ‘pushiness’ during feeding (using the Maternal

Feeding Attitudes Questionnaire66) and maternal sensitivity

to infant cues (using the Nursing Child Assessment Feeding

Scale67,68) were assessed in relation to infant growth from

birth to 12 months. After controlling for numerous factors

(such as birth weight, gender, race/ethnicity, maternal age,

maternal body mass index before pregnancy), infant weight

gain between 6 and 12 months was predicted by mothers’

sensitivity to satiety cues such that low-maternal sensitivity

to infant cues resulted in increased weight gain. It should be

noted that infant growth measures lacked standardization, as

change in actual weight was investigated (i.e., weight gained

from 6 to 12 months of age), no change in growth based on a

standardized growth reference (i.e., weight-for-age Z-score

change). As a result, the changes in growth only speak to

change to one’s own baseline not in reference to whether the

individual’s growth would trail, equal or exceed other

individual’s of similar gender and age.

Two studies were identified that assessed infant obesity/

overweight in relationship with responsive feeding. Dubois

et al.69 sampled two groups of infants; 42 normal weight 4–9

months old (25–75th percentiles and 47 overweight 4–9

months old (o90th percentile). They investigated whether

these two groups differed in energy intake, infant feeding

history and maternal reliance on external cues. For ‘maternal

reliance on external cues’, mothers were asked open-ended

questions and their answers were coded with respect to the

following variables: mother usually uses external cues to

initiate or terminate feedings, sometimes tries to feed more

or less than the infant wants and sometimes offers food to

stop infant’s crying. External cues were described as time or

prepared portion of formula/food and infant signals were

described as sucking fingers (hunger) or turning head away

(fullness). Dubois et al.69 found no differences in maternal

reliance on external cues among the groups of overweight

4- to 9-month-old infants (o90th percentile) and normal

infants (25–75th percentiles). However, the method of

measuring maternal feeding responsiveness was not standar-

dized as open-ended questions were used, which had not

been previously validated. Baughcum et al.70 investigated the

affect of maternal-feeding behaviors on weight in an infant

sample (aged 11–23 months). A separate sample of pre-

schoolers was assessed as part of this study;70 however, those

results are not discussed given the focus of this review on

infants and toddlers. Within the infant sample, a number of

aspects of maternal feeding in which responsiveness is

implicit were assessed for the association with infant weight

status, including concern about the infant’s weight (either

over- or underweight), concern about the infant being

hungry, using food to calm the infant and establishing a

feeding schedule. However, no associations were identified

between a particular feeding style and overweight in infants.

Income was found to influence feeding behaviors, for

example low-income mothers of infants reported more

concern about infant hunger and feeding infant on a

schedule. Thus, the findings of Baughcum et al.70 did not

add support for the model. But a criticism is that the purpose

of the study was in part to validate the questionnaires

usedFthese new questionnaires might have failed to

elucidate responsive feeding behaviors. For example, mater-

nal control in feeding, commonly measured through the

validated Child Feeding Questionnaire,71 has previously

been connected with child overweight,72,73 yet in this study,

control was not associated with child overweight. Also

measuring concurrent weight and feeding behaviors might

not reflect any of the effects from feeding behaviors in

infancy on later childhood overweight. Most of the evidence

was gathered to support the connection between responsive

feeding and weight gain/overweight as presented in the

model, and of the six studies identified, three added support.

Summary of the systematic review findings

The evidence gathered was rated at 2b or lower level of the

CEBM system, meaning there was a dearth of high-quality

Responsive feeding and infant overweight KI DiSantis et al

488

International Journal of Obesity

prospective work. Of the nine studies described here, only

three studies (Farrow and Blissett62; Li et al.64; Worobey

et al.65) revealed associations with dimensions of feeding

responsiveness as described for the model. Although these

studies provide preliminary support for an influence of

responsive feeding on infant/toddler weight, there was a

notable lack of evidence to substantiate the assertion that

such a relationship is produced by excessive energy intake.

Further, the methods for measuring responsive feeding as

reviewed in this narrative and as presented in Table 2,

generally reveal a lack of consistency in the manner in which

feeding responsiveness has been operationally defined. This

concern, along with the failure to consider the bidirectional

nature of maternal responsiveness and infant behaviors,

points to the need for further exploration.

Discussion

This systematic review offered the opportunity to describe

the rationale for investigating responsive feeding and over-

weight during infancy and toddlerhood and to assess the

state of the science on this topic. The conceptual model

provided a framework for identifying and thematically

organizing scientific literature on this topic. The systematic

approach adopted here revealed a dearth of rigorous inquiry

on this topic. The three studies that provided the strongest

support for the model (Farrow and Blissett62; Li et al.64;

Worobey et al.65) evaluated maternal responses to satiety

cues and/or bottle-emptying behaviors and their association

with infant growth. Only Li et al.,64 however, assessed

feeding interactions in a longitudinal manner. In general,

all the articles retrieved, supportive or not, lacked prospec-

tive assessments of infant–caregiver interactions as they

relate to self-regulation, growth and obesity, which was

evidenced by the relatively low CEBM levels assigned to the

studies gathered. This is a crucial gap in the current literature

in light of recognition that feeding interactions are nested in

developmental phases. So that capturing caregiver–infant

interactions at one time point only provides insight into that

point in development. That there was a shortage of support

for the proposed model from the primarily cross-sectional

studies in this systematic review should not discourage

further inquiry.

Beyond the dearth of longitudinal work in this area, the

assessment of the dynamic nature of caregiver–infant

feeding interactions is notably lacking. Responsiveness can

be conceived of as a reciprocal dimension of feeding in

which children are responsible for providing clear feeding

cues and the caregiver for responding in a prompt and

developmentally appropriate manner. However, rather than

focusing on how bidirectional aspects of feeding relate with

obesity outcomes (increased energy intake, rapid weight gain

overweight), studies have focused on how infant-eating

behaviors or caregiver (primarily maternal)-feeding

behaviors independently affect these outcomes. This is

potentially because of the lack of assessment tools, which

measure interactions in a dynamic manner, rather than

assessing the infant or the caregiver alone. To move knowl-

edge ahead in the area of feeding behaviors and obesity

prevention, it is necessary to begin to assess the dyad. Such

assessments would aid in evaluating the usefulness of the

proposed model.

In addition to the alternating focus on either infant or

caregiver behaviors, there was a noteworthy lack of consis-

tency in measurement of ‘responsive feeding.’ The variation

in measurement is illustrated by the variety of constructs

reported on by the articles in this review (Table 2). Variables

used to represent responsive feeding included demand/

schedule feeding,60 bottle emptying,64 observational mea-

sures (e.g., NCAST)56 and self-report measures of caregiver

behaviors.62,70 An additional complicating factor is that

previous research in responsive feeding has been largely

oriented toward undernutrition and has conceptualized

feeding responsiveness more broadly than is considered here

for obesity prevention. Measuring responsive feeding in the

framework of obesity prevention may require a different

operational definition of responsive feeding than those used

in the context of undernutrition. In the model explored

here, discordant responsiveness leads to increases in infant

intake, which could lead to chronic energy imbalance and,

eventually, overweight. The relatively new interest in

viewing responsive feeding in the context of child obesity

risk may explain the lack of concerted study on this topic.

Why has feeding responsiveness been largely ignored in

efforts to understand the development of overweight?

Exploration of feeding dynamics and their role in intake

and growth requires a multidisciplinary perspective invol-

ving parenting, pediatric nutrition and child development.

Psychologists have long studied feeding, but viewed it

primarily as a vehicle for studying parent–child relationships

and developmental outcomes other than growth rather than

as phenomena of interest unto itself. Nutritionists have

historically viewed children’s eating behavior in terms of

food and nutrient intake rather than feeding and eating

behavior. As a result most knowledge related to feeding

pertains to what children are fed rather than how children

are fed. Recognition of environmental contributions to

pediatric overweight and challenges to its treatment have

only recently directed scholarly interest toward understand-

ing familial influences on the development of eating

behavior.

Acknowledging that the caregiver–infant dyad and family

is situated within a broader socioenvironment context

encompassing among others, cultural beliefs/practices about

parenting and feeding, policy, education, healthcare and

childcare, it is clear that a great deal of work remains to be

carried out to begin to understand the complexities of

interactions among these factors and the intrapersonal and

interpersonal factors we think shape dyadic feeding inter-

actions. It is overwhelming and beyond the scope of any

Responsive feeding and infant overweight KI DiSantis et al

489

International Journal of Obesity

single study to undertake such a task, but such a broad

conceptual model as proposed here is useful to the field at

large, pointing to particular relationships that are un- or

underexplored and highlighting areas in which interdisci-

plinary collaborations could be fruitful. As first steps in

advancing knowledge in this area, we offer some suggestions.

The development of well-operationalized and rigorously

developed measurement tools is clearly a priority for moving

scientific inquiry forward in this area. Rigorous observational

approaches should be considered in initial research efforts to

characterize feeding responsiveness and to identify dimen-

sions for which self-report may be possible.74 Qualitative

methods may also prove fruitful to identify potential

facilitators and barriers to responsiveness, such as caregiver

feeding knowledge, attitudes and beliefs. Longitudinal

studies will be required to draw inferences about the capacity

of responsiveness to modify child nutritional and growth

trajectories. Beyond closing in on the caregiver–child inter-

actions, a multidisciplinary approach must be taken to

address the complexity of both caregiver–infant interactions

and obesity and how and whether responsive feeding relates

to the entire growth spectrum (undernutrition to obesity).

Points of exploration, include experiences of the infant and

caregiver during feeding from mood and stress,75,76 altera-

tions in neurohormones77 and racial/ethnic differences and

cultural beliefs, which might alter caregivers’ attitude to

optimal responsiveness, can be investigated.78,79 Thus,

efforts to understand the development of infant/child eating

behavior and its importance for growth should take feeding,

its goals and its context into consideration. The dependence

of infants and toddlers on their caregivers to obtain nutrition

and develop eating skills suggests a potentially critical role

for responsive feeding in nutrition and growth from a very

early point in development. A recent study of overweight

children illustrates the need for such early interventions, as

it found that nearly 60% of overweight children became

overweight before the age of 2 years.3 As a potentially

modifiable behavior, responsiveness may represent an

efficacious target for early obesity prevention efforts in the

future.

Conclusion

In conclusion, the notion that a chronic mismatch between

feeding and child cues contributes to the development of

overweight is not new.29,41 On the basis of the findings of

this systematic review, however, the role of feeding respon-

siveness in accelerated growth and overweight remains, to

date, is more speculative than substantive. There is pre-

liminary support for the proposed role of responsiveness in

growth during early development, though the strength of

evidence is relatively weak and the studies are few. These

findings underscore that we are in the early stage of

empirical research on this topic. As such, we conclude that

additional rigorous investigation of feeding responsiveness is

needed, particularly longitudinal studies, within the frame-

work of early obesity prevention efforts among diverse

populations.

Conflict of interest

The authors declare no conflict of interest.

Acknowledgements

This work was supported by the NIH K01 DK 61319-01

(Fisher), USDA 2005-55215-6 16726 (Johnson), NIH DK

56350 (Hodges), RWJF 66523 (Hodges) and Nestle Infant

Nutrition (Fisher).

References

1 Kral TV, Stunkard AJ, Berkowitz RI, Stallings VA, Brown DD, Faith MS. Daily food intake in relation to dietary energy density in the free-living environment: a prospective analysis of children born at different risk of obesity. Am J Clin Nutr 2007; 86: 41–47.

2 Stettler N, Iotova V. Early growth patterns and long-term obesity risk. Curr Opin Clin Nutr 2010; 13: 294–299.

3 Harrington JW, Nguyen VQ, Paulson JF, Garland R, Pasquinelli L, Lewis D. Identifying the ‘tipping point’ age for overweight pediatric patients. Clin Pediatr (Phila) 2010; 49: 638–643.

4 Stettler N, Kumanyika SK, Katz SH, Zemel BS, Stallings VA. Rapid weight gain during infancy and obesity in young adulthood in a cohort of African Americans. Am J Clin Nutr 2003; 77: 1374–1378.

5 Monteiro POA, Victora CG. Rapid growth in infancy and childhood and obesity in later lifeFa systematic review. Obesity Rev 2005; 6: 143–154.

6 Wells JC, Chomtho S, Fewtrell MS. Programming of body composition by early growth and nutrition. Proc Nutr Soc 2007; 66: 423–434.

7 Shonkoff JP, Phillips De. From Neurons to Neighborhoods: the Science of Early Childhood Development. National Academy Press: Washington, DC, 2000.

8 Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007–2008. JAMA 2010; 303: 242–249.

9 Scaglioni S, Agostoni C, Notaris RD, Radaelli G, Radice N, Valenti M. et al. Early macronutrient intake and overweight at five years of age. Int J Obes Relat Metab Disord 2000; 24: 777–781.

10 Mellbin T, Vuille JC. Relationship of weight gain in infancy to subcutaneous fat and relative weight at 10 1/2 years of age. Br J Prev Soc Med 1976; 30: 239–243.

11 Mei Z, Grummer-Strawn LM, Scanlon KS. Does overweight in infancy persist through the preschool years? An analysis of CDC Pediatric Nutrition Surveillance System data. Soz Praventivmed 2003; 48: 161–167.

12 Stettler N, Zemel BS, Kumanyika S, Stallings VA. Infant weight gain and childhood overweight status in a multicenter, cohort study. Pedatrics 2002; 109: 194–199.

13 Reilly JJ, Armstrong J, Dorosty AR, Emmett PM, Ness A, Rogers I et al. Early life risk factors for obesity in childhood: cohort study. BMJ 2005; 330: 1357.

14 Dennison BA, Edmunds LS, Stratton HH, Pruzek RM. Rapid infant weight gain predicts childhood overweight. Obesity 2006; 14: 491–499.

Responsive feeding and infant overweight KI DiSantis et al

490

International Journal of Obesity

15 Dubois L, Girard M. Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes 2006; 30: 610–617.

16 Karaolis-Danckert N, Buyken AE, Bolzenius K, Perim de Faria C, Lentze MJ, Kroke A. Rapid growth among term children whose birth weight was appropriate for gestational age has a longer lasting effect on body fat percentage than on body mass index. Am J Clin Nutr 2006; 84: 1449–1455.

17 Blair NJ, Thompson JMD, Black PN, Becroft DMO, Clark PM, Han DY et al. Risk factors for obesity in 7-year-old European children: the Auckland Birthweight Collaborative Study. Arch Dis Child 2007; 92: 866–871.

18 Stettler N, Kumanyika S, Katz SH, Zemel BS, Stallings VA. Rapid early infancy weight gain and obesity in African American adults. Circulation 2003; 107: E7002.

19 Stettler N, Stallings VA, Troxel AB, Zhao J, Schinnar R, Nelson SE et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation 2005; 111: 1897–1903.

20 Monteiro POA, Victora CG, Barros FC, Monteiro LMA. Birth size, early childhood growth, and adolescent obesity in a Brazilian birth cohort. Int J Obes 2003; 27: 1274–1282.

21 Ekelund U, Ong K, Linne Y, Neovius M, Brage S, Dunger DB et al. Upward weight percentile crossing in infancy and early child- hood independently predicts fat mass in young adults: the Stockholm Weight Development Study (SWEDES). Am J Clin Nutr 2006; 83: 324–330.

22 Stettler N, Iotova V. Early growth patterns and long-term obesity risk. Curr Opin Clin Nutr Metab Care 2010; 13: 294–299.

23 Ong KK, Emmett PM, Noble S, Ness A, Dunger DB, Team AS. Dietary energy intake at the age of 4 months predicts postnatal weight gain and childhood body mass index. Pedatrics 2006; 117: e503–e508.

24 Lamb ME, Easterbrooks MA. Individual differences in parental sensitivity: origins, components, and consequences. In: Lamb ME, Sherrod LR, (eds). Infant Social Cognition: Empirical and Theoretical Considerations. Erlbaum: Hillsdale, NJ, 1981; 127–153.

25 Ziv Y, Cassidy J. Maternal responsiveness to infant irritability: the contribution of Crockenberg and Smith’s ‘Antecedents of mother-infant interaction and infant irritability in the first 3 months of life’. Infant Behav Dev 2002; 25: 16–20.

26 Feldman R, Greenbaum CW, Yirmiya N. Mother-infant affect synchrony as an antecedent of the emergence of self-control. Dev Psychol 1999; 35: 223–231.

27 Bronson MB. Self-regulation in Early Childhood: Nature and Nurture. The Guilford Press: New York, NY, 2000.

28 Green JA, Gustafson GE, Irwin JR, Kalinowski LL, Wood RM. Infant crying: acoustics, perception, and communication. Early Dev Parenting 1995; 4: 161–175.

29 Ainsworth MDS, Bell SM. Some Contemporary Patterns of Mother- infant Interaction in the Feeding Situation Stimulation in Early Infancy. Academic Press: New York, 1969.

30 Bell SM, Ainsworth MD. Infant crying and maternal responsive- ness. Child Dev 1972; 43: 1171–1190.

31 Bornstein MH, Tamis-LeMonda CS. Maternal responsiveness and cognitive development in children. New Dir Child Dev 1989; 1989: 49–61.

32 Goldberg S. Social competence in infancy: a model of parent– infant interaction. Merrill-Palmer Quart 1977; 23: 163–177.

33 Vallotton CD. Do infants influence their quality of care? Infants’ communicative gestures predict caregivers’ responsiveness. Infant Behav Dev 2009; 32: 351–365.

34 Wright P, Fawcett J, Crow R. The development of differences in the feeding behaviour of bottle and breast fed human infants from birth to two months. Behav Process 1980; 5: 1–20.

35 Wright P. Development of feeding behavior in early infancy: implications for obesity. Health Bull 1981; 39: 197–205.

36 Fomon SJ, Filer LJ, Thomas LN, Rogers RR, Proksch AM. Relationship between formula concentration and rate of growth of normal infants. J Nutr 1969; 98: 241–254.

37 Fomon SJ, Filmer LJ, Thomas LN, Anderson TA, Nelson SE. Influence of formula concentration on caloric intake and growth of normal infants. Acta Paediatric Scandinavia 1975; 64: 172–181.

38 Kent JC, Mitoulas LR, Cregan MD, Ramsay DT, Doherty DA, Hartmann PE. Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pedatrics 2006; 117: e387–e395.

39 Fox MK, Devaney B, Reidy K, Razafindrakoto C, Ziegler P. Relationship between portion size and energy intake among infants and toddlers: evidence of self-regulation. J Am Diet Assoc 2006; 106 (1S): 77–83.

40 Wright P. Learning experiences in feeding behaviour during infancy. J Psychosom Res 1988; 32: 613–619.

41 Costanzo PR, Woody EZ. Domain-specific parenting styles and their impact on the child’s development of a particular deviance: the example of obesity proneness. J Soc Clin Psychol 1985; 4: 425–445.

42 Bruch H. Eating Disorders: Obesity, Anorexia Nervosa, and the Person Within. Basic Books: New York, 1973.

43 Birch LL, Fisher JO. Development of eating behaviors among children and adolescents. Pediatrics 1998; 101: 539–549.

44 Engle PL, Bentley ME, Pelto G. The role of care in nutrition programmes:current research a research agenda. Proc Nutr Soc 2000; 59: 25–35.

45 Bornstein MH. Sensitive periods in development: structural characteristics and causal interpretations. Psychol Bull 1989; 105: 179–197.

46 Dewey K. Guiding principles for complementary feeding of the breastfed child. PAHO/WHO: Washington, DC, 2003. http://www.who.int/ nutrition/publications/guiding_principles_compfeeding_breastfed.pdf.

47 Bronfenbrenner U. Ecology of the family as a context for human development: research perspectives. Dev Psychol 1986; 22: 723–742.

48 Taveras EM, Gillman MW, Kleinman K, Rich-Edwards JW, Rifas- Shiman SL. Racial/ethnic differences in early-life risk factors for childhood obesity. Pediatrics 2010; 125: 686–695.

49 World Health Organization U. Global Strategy for Infant and Young Child Feeding. WHO: Geneva, 2003.

50 Burdette HL, Whitaker RC, Hall WC, Daniels SR. Maternal infant- feeding style and children’s adiposity at 5 years of age. Arch Pediatr Adolesc Med 2006; 160: 513–520.

51 Susin LR, Giugliani ER, Kummer SC, Maciel M, Simon C, da Silveira LC. Does parental breastfeeding knowledge increase breastfeeding rates? Birth 1999; 26: 149–156.

52 Centre for Evidence-Based Medicine OU. Levels of evidence and grades of recommendation. Available at: http://www.cebm.net/ levels_of_evidence.asp. (Accessed 9 January 2009) 2009.

53 Mogan J. Parental weight and its relation to infant feeding patterns and infant obesity. Int J Nurs Stud 1986; 23: 255–264.

54 Francis LA, Birch LL. Maternal weight status modulates the effects of restriction on daughters’ eating and weight. Int J Obes Relat Metab Disord 2005; 29: 942–949.

55 Kavanagh KF, Cohen RJ, Heinig MJ, Dewey KG. Educational intervention to modify bottle-feeding behaviors among formula- feeding mothers in the WIC program: impact on infant formula intake and weight gain. J Nutr Educ Behav 2008; 40: 244–250.

56 Rybski DA, Almli CR, Gisel EG, Powers J, Maurer Jr M. Sucking behaviors of normal 3-day-old female neonates during a 24-h period. Dev Psychobiol 1984; 17: 79–86.

57 Birch LL, Deysher M. Caloric compensation and sensory specific satiety: Evidence for self regulation of food intake by young children. Appetite 1986; 7: 323–331.

58 Birch LL, Deysher M. Conditioned and unconditioned caloric compensation: evidence for self-regulation of food intake by young children. Learn Motiv 1985; 16: 341–355.

59 Fomon S. Nutrition of Normal Infants. Mosby-Year Books: St Louis, Missouri, 1993.

60 Saxon TF, Gollapalli A, Mitchell MW, Stanko S. Demand feeding or schedule feeding: infant growth from birth to 6 months. J Reprod Infant Psychol 2002; 20: 89–100.

Responsive feeding and infant overweight KI DiSantis et al

491

International Journal of Obesity

61 Kalies H, Heinrich J, Borte N, Schaaf B, von Berg A, von Kries R et al. The effect of breastfeeding on weight gain in infants: results of a birth cohort study. Eur J Med Res 2005; 10: 36–42.

62 Farrow C, Blissett J. Does maternal control during feeding moderate early infant weight gain? Pediatrics 2006; 118: e293–e298.

63 Wolke D, Skuse D. The management of infant feeding problems. In: Cooper P, Stein A (eds). Feeding Problems and Eating Disorders in Children and Adolescents. Harwood: Chur, Switzerland, 1992; 27– 59.

64 Li R, Fein SB, Grummer-Strawn LM. Association of breastfeeding intensity and bottle-emptying behaviors at early infancy with infants’ risk for excess weight at late infancy. Pediatrics 2008; 122 (Suppl 2): S77–S84.

65 Worobey J, Lopez MI, Hoffman DJ. Maternal behavior and infant weight gain in the first year. J Nutr Educ Behav 2009; 41: 169–175.

66 Kramer MS, Barr RG, Leduc DG, Boisjoly C, Pless IB. Maternal psychological determinants of infant obesity. Development and testing of two new instruments. J Chronic Dis 1983; 36: 329–335.

67 Barnard K. Caregiver/Parent-child Interaction Feeding Manual. Uni- versity of Washington School of Nursing: Seattle, WA, 1994. NCAST Publications.

68 Hodges EA, Houck GM, Kindermann T. Reliability of the Nursing Child Assessment Feeding Scale during toddlerhood. Issues Compr Pediatr Nurs 2007; 30: 109–130.

69 Dubois S, Hill DE, Beaton GH. An examination of factors believed to be associated with infantile obesity. Am J Clin Nutr 1979; 32: 1997–2004.

70 Baughcum AE, Powers SW, Johnson SB, Chamberlin LA, Deeks CM, Jain A et al. Maternal feeding practices and beliefs and their relationship to overweight in early childhood. J Dev Behav Pediatr 2001; 22: 391–408.

71 Birch LL, Fisher JO, Castro CN, Grimm-Thomas K, Sawyer R, Johnson SL. Confirmatory factor analysis of the Child Feeding Questionnaire: a measure of parental attitudes, beliefs and practices about child feeding and obesity proneness. Appetite 2001; 36: 201–210.

72 Faith MS, Scanlon KS, Birch LL, Francis LA, Sherry B. Parent-child feeding strategies and their relationships to child eating and weight status. Obes Res 2004; 12: 1711–1722.

73 Spruijt-Metz D, Lindquist CH, Birch LL, Fisher JO, Goran MI. Relation between mothers’ child-feeding practices and children’s adiposity. Am J Clin Nutr 2002; 75: 581–586.

74 Sacco LM, Bentley ME, Carby-Shields K, Borja JB, Goldman BD. Assessment of infant feeding styles among low-income African- American mothers: comparing reported and observed behaviors. Appetite 2007; 49: 131–140.

75 Groer MW. Differences between exclusive breastfeeders, formula- feeders, and controls: a study of stress, mood, and endocrine variables. Biol Res Nurs 2005; 7: 106–117.

76 Farrow CV, Blissett JM. Is maternal psychopathology related to obesigenic feeding practices at 1 year? Obes Res 2005; 13: 1999–2005.

77 Swain JE, Lorberbaum JP, Kose S, Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry 2007; 48: 262–287.

78 Kumanyika SK. Environmental influences on childhood obesity: ethnic and cultural influences in context. Physiol Behav 2008; 94: 61–70.

79 Taveras EM, Gillman MW, Kleinman K, Rich-Edwards JW, Rifas-Shiman SL. Racial/ethnic differences in early-life risk factors for childhood obesity. Pediatrics 2010; 125: 686–695.

Responsive feeding and infant overweight KI DiSantis et al

492

International Journal of Obesity

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.