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Breastfeeding and risk of child obesity
Kathryn G. Dewey, PhDKathryn G. Dewey, PhD
Program in International and Community NutritionProgram in International and Community Nutrition
University of California, DavisUniversity of California, Davis
Study selection criteria
N N >> 100 per feeding group 100 per feeding group Age at follow-up > 3 yAge at follow-up > 3 y Outcome = % overweight or obeseOutcome = % overweight or obese
Studies in preschool childrenAuthor, year, Author, year,
sitesite
N, ageN, age Feeding groupsFeeding groups OutcomesOutcomes ResultsResults
[*p < 0.05][*p < 0.05]
Armstrong, Armstrong, 2002, Scotland2002, Scotland
32,20032,200
3-4 y3-4 y
EBF vs. EFF at 6-8 EBF vs. EFF at 6-8 wkwk
BMI > 95BMI > 95thth
BMI > 98BMI > 98thth
AOR 0.72*AOR 0.72*
AOR 0.70*AOR 0.70*
Bogen, 2004, Bogen, 2004, USAUSA11
73,45873,458
4 y4 y
BF < 8 wk, 8-15 wk, BF < 8 wk, 8-15 wk, 16-26 wk, > 26 wk 16-26 wk, > 26 wk (+/- concurrent FF)(+/- concurrent FF)
BMI BMI >> 95th 95th AOR 0.71 for AOR 0.71 for 16-26 wk w/o 16-26 wk w/o FF*FF*
Hediger, 2001,Hediger, 2001,
USAUSA
2,6852,685
3-5 y3-5 y
Ever BF vs. EFFEver BF vs. EFF
(+ dur. full BF)(+ dur. full BF)
BMI 85-94BMI 85-94thth
BMI BMI >> 95 95thth
AOR 0.63*AOR 0.63*
AOR 0.84AOR 0.84
Grummer-Grummer-Strawn, 2004, Strawn, 2004, USAUSA
177,304177,304
(12,587)(12,587)
4 y4 y
BF < 1, 1-3, 3-6, 6-12, BF < 1, 1-3, 3-6, 6-12, or or >> 12 mo, vs. EFF 12 mo, vs. EFF
BMI BMI >> 95 95thth AOR for White, AOR for White, non-Hispnon-Hisp
0.70* (6-12 mo)0.70* (6-12 mo)
0.49* (0.49* (>> 12 mo) 12 mo)
O’Callaghan, O’Callaghan, 1997, Australia1997, Australia
3,9093,909
5 y5 y
BF durationBF duration BMI 85-94BMI 85-94thth
BMI > 95BMI > 95thth
NSNS
Burke, 2005, Burke, 2005, AustraliaAustralia
2,0872,087
1-8 y1-8 y
EFF vs. BF EFF vs. BF << 4 mo, 5- 4 mo, 5-8, 9-12, > 12 mo8, 9-12, > 12 mo
BMI BMI >> 95 95thth Highest risk in Highest risk in BF BF << 4 mo* 4 mo*
11Only among white children whose mothers did not smokeOnly among white children whose mothers did not smoke
Studies in school-aged childrenAuthor, year, siteAuthor, year, site N, ageN, age Feeding groupsFeeding groups OutcomesOutcomes ResultsResults
Von Kries, 1999,Von Kries, 1999,
GermanyGermany
9,3579,357
5-6 y5-6 y
Ever BF vs. EFFEver BF vs. EFF
(+ dur. EBF)(+ dur. EBF)
BMI > 90BMI > 90thth
BMI > 97BMI > 97thth
AOR 0.79*AOR 0.79*
AOR 0.75*AOR 0.75*
Wadsworth, 1999,Wadsworth, 1999,
UKUK
3,7313,731
6 y6 y
Ever BF vs. EFF Ever BF vs. EFF (+ dur. BF)(+ dur. BF)
BMI > 90BMI > 90thth
BMI > 97BMI > 97thth
RR 0.95RR 0.95
RR 0.88RR 0.88
Bergmann, 2003, Bergmann, 2003, GermanyGermany
480480
6 y6 y
BF BF >> or < 3 mo or < 3 mo BMI > 90BMI > 90thth
BMI > 97BMI > 97thth
AOR 0.53*AOR 0.53*
AOR 0.46*AOR 0.46*
Reilly, 2005,Reilly, 2005,
UKUK
8,2348,234
7 y7 y
EBF EBF >> 2 mo or < 2 mo or < 2 mo, vs. EFF2 mo, vs. EFF
BMI BMI >> 95 95thth Lower risk if Lower risk if EBF*, if non-EBF*, if non-smoking mothersmoking mother
Toschke, 2002,Toschke, 2002,
Czech RepublicCzech Republic
33,76833,768
6-14 y6-14 y
Ever BF vs. EFF, Ever BF vs. EFF, (+ duration BF)(+ duration BF)
BMI > 90BMI > 90thth
BMI > 97BMI > 97thth
AOR 0.80*AOR 0.80*
AOR 0.80*AOR 0.80*
Liese, 2001,Liese, 2001,
GermanyGermany
2,1082,108
9-10 y9-10 y
Ever BF vs. EFFEver BF vs. EFF
(+dur. BF, EBF)(+dur. BF, EBF)
BMI > 90thBMI > 90th AOR 0.66*AOR 0.66*
Gillman, 2001, Gillman, 2001,
USAUSA
15,34115,341
9-14 y9-14 y
Pred BF vs. Pred Pred BF vs. Pred FF 0-6 moFF 0-6 mo
BMI > 95BMI > 95thth AOR 0.78*AOR 0.78*
Studies in older adolescentsAuthor, year, siteAuthor, year, site N, ageN, age Feeding groupsFeeding groups OutcomesOutcomes ResultsResults
Kvaavik, 2005,Kvaavik, 2005,
NorwayNorway
635635
13 y13 y
BF > 3 mo vs. BF > 3 mo vs. EFFEFF
BMI > 95BMI > 95thth AOR 0.15*AOR 0.15*
Kramer, 1981,Kramer, 1981,
CanadaCanada
427427
12-18y12-18y
Ever BF vs. EFFEver BF vs. EFF
(+dur. full BF)(+dur. full BF)
> 120% median > 120% median weight for htweight for ht
RR 0.31*RR 0.31*
Tulldahl, 1999,Tulldahl, 1999,
SwedenSweden
781781
17-18y17-18y
EBF > vs. EBF > vs. << 2 mo 2 mo BMI > 85BMI > 85thth RR 0.70*RR 0.70*
Poulton, 2001,Poulton, 2001,
New ZealandNew Zealand
1,0371,037
3-26 y3-26 y
BF > 6 mo vs. BF > 6 mo vs. EFFEFF
BMI > 25 kg/mBMI > 25 kg/m22 AOR 0.25-1.01AOR 0.25-1.01
Li, 2003, Li, 2003,
UKUK
2,6312,631
4-18 y4-18 y
Duration BF vs. Duration BF vs. BF < 1 wkBF < 1 wk
BMI > 95BMI > 95thth AOR 0.68-2.02AOR 0.68-2.02
Victora, 2003, Victora, 2003,
BrazilBrazil
2,2502,250
18 y (18 y (♂♂))
Duration Pred BFDuration Pred BF BMI > 85BMI > 85thth
skinfolds > 90skinfolds > 90thth
Significant Significant linear trendlinear trend
Nelson, 2005, Nelson, 2005,
USAUSA
11,99811,998
850 sib 850 sib pairspairs
12-21 y12-21 y
BF BF >> 9 mo vs. 9 mo vs. EFFEFF
BMI BMI >> 85 85thth AOR 0.78* (F)AOR 0.78* (F)
AOR 0.83 (M)AOR 0.83 (M)
NS for sib pairsNS for sib pairs
Additive interactions of maternal prepregnancy BMI and breastfeeding on childhood overweight. Li et al. Obesity Res 2005;13:362-371 (2-14 years of age)
0
5
10
15
20
25
30
35
% Overweight
never <4 mo >4 mo
Breast-feeding (months)
< 2525-29
> 30
Maternal BMI
31.5
6.0
Breastfeeding and childhood obesity – a systematic review. Arenz et al. Intl J Obes, 2004; 28:1247-56.
0 1
O'Callaghan 1997
Bergmann 2003
Hediger 2001
Li 2003
Poulton 2001
von Kries 1999
Liese 2001
Toschke 2001
Gillman 2001
Meta-analysis
Adjusted odds-ratioSource: Arenz et al. Intl J Obes, 2004
AOR 0.78 (0.71, 0.85)
Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Owen et al. Pediatrics 2005;115:1367-77. Reviewed 61 studies; 28 with odds ratio estimatesReviewed 61 studies; 28 with odds ratio estimates OR for any BF, all studies: 0.87 (0.85-0.89)OR for any BF, all studies: 0.87 (0.85-0.89)
For infants: For infants: OR = 0.50 (0.26-0.94)OR = 0.50 (0.26-0.94) For young children:For young children: OR = 0.90 (0.87-0.92)OR = 0.90 (0.87-0.92) For older children: For older children: OR = 0.66 (0.60-0.72)OR = 0.66 (0.60-0.72) For adults: For adults: OR = 0.80 (0.71-0.91)OR = 0.80 (0.71-0.91)
Adjusted for SES, parental BMI & maternal smoking) for any BF, all Adjusted for SES, parental BMI & maternal smoking) for any BF, all studies: AOR = 0.93 (0.88-0.99)studies: AOR = 0.93 (0.88-0.99)
Protective effect of BF stronger in 4 studies in which initial feeding Protective effect of BF stronger in 4 studies in which initial feeding groups were exclusive: OR = 0.76 (0.70-0.83)groups were exclusive: OR = 0.76 (0.70-0.83)
Stronger relationship with longer duration of BF:Stronger relationship with longer duration of BF: OR = 0.81 (0.77-0.84) for BF OR = 0.81 (0.77-0.84) for BF >> 2 mo 2 mo OR = 0.89 (0.86-0.91) for any BF durationOR = 0.89 (0.86-0.91) for any BF duration
Bergmann et al. (Germany)N=480; BMI at 0-6 y
Percentage of children > 90th percentile
Poulton & Williams (New Zealand)N=1,037, born 1972-73BMI at 3, 5, 7, 9, 11, 13, 15, 18, 21, 26 y
In those BF > 6 mo, a lower risk of obesity In those BF > 6 mo, a lower risk of obesity was observed at 9-18 years of age, but not was observed at 9-18 years of age, but not at younger ages (3-8 years) or in adulthood at younger ages (3-8 years) or in adulthood (> 18 years)(> 18 years)
Is puberty / adolescence a critical period, Is puberty / adolescence a critical period, when the influence of infant feeding mode when the influence of infant feeding mode is most clearly expressed? is most clearly expressed?
YesYes NoNoBogenBogen HedigerHedigerGrummer-StrawnGrummer-Strawn O-Callaghan O-Callaghan Von KriesVon Kries WadsworthWadsworthToschkeToschke LiLiLieseLiese VictoraVictoraGillmanGillman BurkeBurkePoulton (trend)Poulton (trend)Nelson (in girls)Nelson (in girls)
Is there a dose-response relationship between BF duration and lower risk of child obesity?
Harder et al. Duration of breastfeeding and risk of overweight: a Harder et al. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 2005;162:1-7.meta-analysis. Am J Epidemiol 2005;162:1-7.
Included 17 studies:Included 17 studies:Duration BFDuration BF OROR< 1 mo< 1 mo 1.001.001-3 mo1-3 mo 0.81*0.81*4-6 mo4-6 mo 0.76*0.76*7-9 mo7-9 mo 0.67*0.67*> 9 mo> 9 mo 0.68*0.68*
* Significantly different from reference group. [No control for * Significantly different from reference group. [No control for potential confounders.]potential confounders.]
Is there a dose-response relationship between BF duration and lower risk of child obesity?
Does exclusivity of breastfeeding matter?
Bogen et al. Obesity Research 2004;12:1527-1535
Relationship between obesity at age 4 y and duration of breastfeeding and concurrent formula use for whites (solid line) and blacks (dashed line)
Breastfeeding duration and obesity at 4 y among white children whose mothers did not smoke during pregnancy [Bogen et al., 2004]
BF durationBF duration AORAORNever 1.00< 8 wk 0.978-15 wk w/ FF 0.848-15 wk w/o FF 0.8016-26 wk w/ FF 0.8616-26 wk w/o FF 0.71*> 26 wk w/ FF 0.70*> 26 wk w/o FF 0.55** p < 0.05, adjusted for maternal age, education, parity, marital status, pregnancy
conditions, delivery method, child sex, birth weight, birth order, birth year. Inclusion of maternal BMI did not alter the results.
Breastfeeding and subsequent obesity: potential explanations
Learned self-regulation of energy intakeLearned self-regulation of energy intake Metabolic programmingMetabolic programming
InsulinInsulin LeptinLeptin Consequences of high protein intake in early Consequences of high protein intake in early
lifelife Residual confounding by attributes of mothers Residual confounding by attributes of mothers
and/or family environmentand/or family environment
Learned self-regulation of energy intake
Breastfeeding allows infant to control intake based Breastfeeding allows infant to control intake based on internal satiety cueson internal satiety cues
Bottle-fed infants may be encouraged to finish Bottle-fed infants may be encouraged to finish bottle even if they are fullbottle even if they are full
This may lead to later differences in ability to self-This may lead to later differences in ability to self-regulate energy intakeregulate energy intake
Infant self-regulation of breast milk intake K.G. Dewey & B. Lonnerdal Acta Paediatr Scand 1986; 75: 893-8
18 exclusively breastfeeding mothers stimulated 18 exclusively breastfeeding mothers stimulated milk supply by daily expression of extra milk for 2 milk supply by daily expression of extra milk for 2 wk. All but 4 increased milk volume by > 73 g/d.wk. All but 4 increased milk volume by > 73 g/d.
Among the 14 infants with access to increased Among the 14 infants with access to increased milk volume, most increased intake in the first 2 d, milk volume, most increased intake in the first 2 d, but returned to near baseline levels of intake after but returned to near baseline levels of intake after 1-2 wk1-2 wk
Intake increased more in fatter than leaner infantsIntake increased more in fatter than leaner infants Breastfed infants self-regulate milk intakeBreastfed infants self-regulate milk intake
Differences in milk intake between BF and FF infants increase between 1 and 5 mo
600700
800900
10001100
1200
1 mo 3 mo 5 mo
Age (mo)
Milk
Inta
ke (
ml/d
)
BF
FF-C
FF-MP
FF-LP
b
bb
a aa
b
b
b,c
ca
Dewey et al., EB 2004
Response to introduction of solid foods differs between breastfed and formula-fed infants
In BF infants, breast milk intake declines In BF infants, breast milk intake declines when solid foods are introducedwhen solid foods are introduced
In FF infants, formula intake does not In FF infants, formula intake does not decline when solid foods are introduceddecline when solid foods are introduced
Heinig et al., Acta Paediatr 1993;82:999-1006Heinig et al., Acta Paediatr 1993;82:999-1006
Effects of over-feeding in early life?
Animal studiesAnimal studiesIn baboons, overfeeding in infancy In baboons, overfeeding in infancy fat depot mass during puberty, especially fat depot mass during puberty, especially
in in females (Lewis et al., 1986)females (Lewis et al., 1986)
Human studiesHuman studiesRapid weight gain during infancy is Rapid weight gain during infancy is
correlated with childhood obesitycorrelated with childhood obesity(Ong et al., 2000; Stettler et al., 2002; (Ong et al., 2000; Stettler et al., 2002;
Cameron et al., 2003; Ekelund et al., 2006)Cameron et al., 2003; Ekelund et al., 2006)
Stettler et al. (U.S.)Pediatrics 2002;109:194-199
N=19,397 children born 1959-65N=19,397 children born 1959-65
Outcome: BMI > 95th percentile at age 7 yOutcome: BMI > 95th percentile at age 7 y
Rate of weight gain during the first 4 mo was Rate of weight gain during the first 4 mo was associated with risk of child obesity, even after associated with risk of child obesity, even after adjustment for weight at 1 yearadjustment for weight at 1 year
Almost 20% of obesity attributable to having a Almost 20% of obesity attributable to having a high rate of weight gain 0-4 mohigh rate of weight gain 0-4 mo
Weight gain in the first week of life and overweight in adulthood. Stettler et al. Circulation 2005;111:1897-1903.
N= 653 formula-fed infants, measured frequently N= 653 formula-fed infants, measured frequently during infancy & again at 20-32 y of ageduring infancy & again at 20-32 y of age
32% were overweight as adults32% were overweight as adults Weight gain during the first week of life was identified Weight gain during the first week of life was identified
as the most sensitive period regarding the association as the most sensitive period regarding the association with adult overweight: AOR for each 100-g increase with adult overweight: AOR for each 100-g increase was 1.28 (1.08-1.52) [adjusted for sex, birth weight, was 1.28 (1.08-1.52) [adjusted for sex, birth weight, type of formula, age at follow-up, maternal & paternal type of formula, age at follow-up, maternal & paternal weight status, income]weight status, income]
Weight gain during the first week of life ranged from 0 Weight gain during the first week of life ranged from 0 to 400 gto 400 g
Infant feeding, plasma insulin & weight gain
Formula-fed infants have higher plasma insulin Formula-fed infants have higher plasma insulin levels and prolonged insulin response at 6 d of age levels and prolonged insulin response at 6 d of age (Lucas et al., 1981)(Lucas et al., 1981)
Higher insulin levels stimulate greater fat Higher insulin levels stimulate greater fat deposition, and have been associated with deposition, and have been associated with subsequent subsequent weight gain & obesity in Pima Indian weight gain & obesity in Pima Indian children 5-9 y of age (Odeleye et al., 1997)children 5-9 y of age (Odeleye et al., 1997)
Infant feeding and plasma leptin
Plasma leptin is a key regulator of appetite and Plasma leptin is a key regulator of appetite and body fatnessbody fatness
Breastfeeding may affect leptin levels during Breastfeeding may affect leptin levels during infancy and later in lifeinfancy and later in life
Early diet of preterm infants is associated with Early diet of preterm infants is associated with leptin concentration at 13-16 y of age (Singhal et leptin concentration at 13-16 y of age (Singhal et al., 2002)al., 2002)
Ratio of leptin concentration to fat mass at 13-16 y of age, by tertile of human milk intake by preterm infants in early life (median + 95% CI, n=191, p = 0.006; Singhal et al., 2002)
Infant feeding and plasma leptin:postulated mechanism (Singhal et al., 2002)
Greater body fatness during infancy “programs” Greater body fatness during infancy “programs” the leptin-dependent feedback loop to be less the leptin-dependent feedback loop to be less sensitive to leptin later in life (i.e. greater leptin sensitive to leptin later in life (i.e. greater leptin resistance)resistance)
Greater leptin resistance contributes to overeating Greater leptin resistance contributes to overeating and obesityand obesity
In rats, overfeeding before weaning leads to In rats, overfeeding before weaning leads to overweight and leptin resistance in later life overweight and leptin resistance in later life (Plagemann et al., 1999)(Plagemann et al., 1999)
Early protein intake and subsequent body fatness Formula-fed infants consume 66-70% more protein than Formula-fed infants consume 66-70% more protein than
breastfed infants at 3-6 mo; by 12 mo, intakes may be 5-breastfed infants at 3-6 mo; by 12 mo, intakes may be 5-6 times the requirement6 times the requirement
High protein intake stimulates higher insulin secretion High protein intake stimulates higher insulin secretion adipose tissue depositionadipose tissue deposition
Association between high protein intake in early life and Association between high protein intake in early life and overweight in childhood reported by Rolland-Cachera et overweight in childhood reported by Rolland-Cachera et al. (1995) and Scaglioni et al. (2000), but not by Dorosty al. (1995) and Scaglioni et al. (2000), but not by Dorosty et al. (2000)et al. (2000)
Residual confounding? Child feeding practices & parental control over feedingChild feeding practices & parental control over feeding
Mothers who breastfed for Mothers who breastfed for >> 12 mo reported lower levels 12 mo reported lower levels of control over feeding at 18 mo (Fisher et al., 2000)of control over feeding at 18 mo (Fisher et al., 2000)
Duration of BF associated with less restrictive behavior Duration of BF associated with less restrictive behavior regarding child feeding at 1 year. Compared to FF regarding child feeding at 1 year. Compared to FF mothers, restrictive behavior much less likely among mothers, restrictive behavior much less likely among mothers who EBF for 6 mo [OR 0.27] (Taveras et al., mothers who EBF for 6 mo [OR 0.27] (Taveras et al., 2004)2004)
Highly controlling feeding practices may interfere with Highly controlling feeding practices may interfere with child’s ability to self-regulate energy intake (Birch et al., child’s ability to self-regulate energy intake (Birch et al., 2003)2003)
Residual confounding? (cont)
Physical activityPhysical activity Breastfeeding associated with healthier Breastfeeding associated with healthier
lifestyle, greater physical activity?lifestyle, greater physical activity? Some studies controlled for physical activity Some studies controlled for physical activity
and results were still significantand results were still significant
Residual confounding? Analysis of sibling pairsNelson et al. Epidemiology 2005;16:247-53. In full cohort, odds of being overweight decreased as BF duration In full cohort, odds of being overweight decreased as BF duration
increased, at least among girlsincreased, at least among girls In sibling pairs, no evidence of BF effectIn sibling pairs, no evidence of BF effect
Adjusted for age, sex, birth order and LBW statusAdjusted for age, sex, birth order and LBW status Did not have data on exclusivity of BFDid not have data on exclusivity of BF
Gillman et al. Epidemiology 2006;17:112-114. N=5614 siblings 9-14 y. Compared overweight in sibs BF longer than N=5614 siblings 9-14 y. Compared overweight in sibs BF longer than
mean for sibship with sibs BF shorter than meanmean for sibship with sibs BF shorter than mean Sibs who were BF longer (mean diff 3.7 mo) had lower OR for Sibs who were BF longer (mean diff 3.7 mo) had lower OR for
overweight: 0.94 for each 3.7 mo increase in BF durationoverweight: 0.94 for each 3.7 mo increase in BF duration OR for within-family analysis close to overall estimate, suggesting little OR for within-family analysis close to overall estimate, suggesting little
residual confoundingresidual confounding
Summary of BF & obesity studies
17 of the 21 studies showed an association 17 of the 21 studies showed an association between breastfeeding and a lower risk of obesitybetween breastfeeding and a lower risk of obesity
All of the studies that took into account the All of the studies that took into account the exclusivity of BF showed a significant associationexclusivity of BF showed a significant association
13 of the 16 studies that controlled for maternal 13 of the 16 studies that controlled for maternal BMI showed a significant associationBMI showed a significant association
In meta-analysis, duration of BF showed a dose-In meta-analysis, duration of BF showed a dose-response relationship with risk of child obesity. response relationship with risk of child obesity. Lowest risk was for > 6 mo of BFLowest risk was for > 6 mo of BF
Explanations?
Not solely due to lower fatness during first 2 yNot solely due to lower fatness during first 2 y Potential mechanisms include:Potential mechanisms include:
Learned self-regulation of energy intakeLearned self-regulation of energy intake Metabolic programming due to differences in Metabolic programming due to differences in
milk composition, protein intake, fatness and/or milk composition, protein intake, fatness and/or rate of weight gain in early liferate of weight gain in early life
Residual confounding, e.g. by child feeding Residual confounding, e.g. by child feeding practices, physical activitypractices, physical activity
Clinical & public health implications
Provides further evidence to promote Provides further evidence to promote breastfeedingbreastfeeding
However, role of breastfeeding is probably small However, role of breastfeeding is probably small compared to other factors such as parental compared to other factors such as parental overweight, dietary practices and physical activity overweight, dietary practices and physical activity
Relationship less evident in African-Americans Relationship less evident in African-Americans and Hispanics – not clear whyand Hispanics – not clear why