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Infant feeding and obesity at 11 years: Prospective birth cohort study. MARILDA BORGES NEUTZLING1,2, PEDRO RODRIGUES CURI HALLAL1,2,.

International Journal of Pediatric Obesity. 2009; 4: 143149

ORIGINAL ARTICLE

Infant feeding and obesity at 11 years: Prospective birth cohort study

MARILDA BORGES NEUTZLING 1 , 2 , PEDRO RODRIGUES CURI HALLAL 1 , 2 , ´ JO1, BERNARDO LESSA HORTA1, MARIA DE FA ´ TIMA CORA LUIZA PAVIN ARAU 1 1 ALVES VIEIRA , ANA MARIA BAPTISTA MENEZES & CESAR GOMES VICTORA1 1

Post-Graduate Program in Epidemiology, Federal University of Pelotas, Brazil, 2Post-Graduate Program in Physical Education, Federal University of Pelotas, Brazil

Abstract Objective. To evaluate the association between breastfeeding duration, introduction of solid or semi-solid foods before four months of age and overweight/obesity at 11 years. Methods. Prospective population-based birth cohort study, including 1 204 adolescents aged 11 years who were born in Pelotas (Brazil), in 1993, and were previously interviewed at birth, six and 12 months of age. Five explanatory variables were used: duration of any breastfeeding, duration of exclusive or predominant breastfeeding, ever breastfeeding, introduction of solid or semi-solid foods before four months of age, and feeding pattern at four months of age. Risk of overweight was defined as body mass index (BMI)]85th percentile, and obesity was defined as BMI ]85th percentile plus triceps and subscapular skinfolds ]90th percentile, using the National Center for Health Statistics curves. Results. The prevalence of risk of overweight and obesity at 11 years were 23.2% and 11.6%, respectively. The lowest prevalence of both outcomes was found among subjects who were breastfed for one to three months. However, tests for linear trend or heterogeneity did not result in a significant association between breastfeeding indicators and anthropometry at 11 years. Adjustment for sex, skin color, birth weight, maternal schooling, smoking during pregnancy and maternal pre-pregnancy BMI did not alter the findings. Conclusions. Our results do not support the hypothesis that breastfeeding has a long-term lasting effect on anthropometry in this population.

Key words: Obesity, infant feeding, longitudinal, cohort studies, adiposity

Introduction As overweight children and adolescents are at an increased risk of becoming obese adults (1,2), it is important to identify risk factors for overweight and obesity in early life. Most studies on the long-term effects of breastfeeding on health suggest that breastfeeding has a protective effect on the prevalence of obesity in childhood (3) or adolescence (4) although not all studies have found consistent results (5,6). Few of them explored the effect of the introduction of solid or semi-solid foods on the prevalence of overweight or obesity later on, and results of such studies are inconsistent (5,7). Relatively few studies on this issue were carried out in low or middle-income settings (810). In the 1993 birth cohort from Pelotas, Brazil, there was no association between breastfeeding and overweight

at four years (9), while an analysis of the 1982 cohort in the same city found no effect of breastfeeding on body composition at 18 years (8). On the other hand, Siqueira and coworkers (10) found that children and adolescents aged 614 years from a private school in Sao Paulo, who were never breastfed, presented the highest prevalence of obesity. The present study aimed at assessing the effect of: total breastfeeding duration; predominant breastfeeding duration; introduction of solid or semi-solid food before four months of age on overweight and obesity at the age of 11 in children from the 1993 Pelotas (Brazil) birth cohort study. Methods Pelotas is a southern Brazilian city with 320 000 inhabitants, located near the Uruguayan border. In

Correspondence: Marilda Borges Neutzling, Programa de Po´s-graduac¸a˜o em Epidemiologia, Universidade Federal de Pelotas, Rua Marechal Deodoro 1160  38 piso, CEP. 96020-220, Pelotas, RS, Brazil. Fax: 55 53 328 41300. E-mail: [email protected]

(Received 10 August 2008; accepted 4 September 2008) ISSN Print 1747-7166 ISSN Online 1747-7174 # 2009 Informa UK Ltd DOI: 10.1080/17477160802453530

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1993, all hospital deliveries were identified and children have been contacted on several occasions. Their mothers were interviewed soon after delivery, and children were weighed and measured. At 6 and 12 months of age, all low birth weight children and a systematic sample of 20% of the remaining were targeted for follow-up. Because of unequal sampling probabilities for low and normal birth weight children, weighted analyses were performed. The following exposures were considered: total breastfeeding (BF) duration in months; predominant breastfeeding (PBF) duration in months (water, teas or juice were incorporated in addition to breast milk, but solid or semi-solid foods were not), ever breastfed (yes/no), introduction of solid or semi-solid foods (for example, fruit, vegetables, beans, rice, eggs, yogurts, etc) before four months of age (yes/no). Exclusive breastfeeding was very rare at the time of the study, so that predominant breastfeeding was used as an explanatory variable. If the child had been weaned or other foods introduced by the age of 6 months, information from this visit was used. If weaning happened between 6 and 12 months, information from the latter interview was used. Feeding pattern at four months of age was also considered, with the following categories: (a) PBF; (b) breast milk plus solids or semi-solids; (c) breast milk plus non-human milk plus solids or semi-solids; and (d) non-human milk plus solids or semi-solids. No children received breast plus non-human milk without foods, or non-human milk without foods. In 20045, all cohort participants were eligible for a follow-up visit, except the 141 who were known to have died. A citywide and a school census were carried out to help locate cohort members. Weight was measured using a SECA (Birmingham, UK) scale (100 g accuracy). Height was measured using a portable stadiometer (1 mm accuracy). Triceps and subscapular skin folds were measured using a CESCORF caliper (0.1 mm accuracy). Body mass index (BMI) was calculated. Nutritional status was categorized using the World Health Organization recommendation (11); risk of overweight was defined as BMI ]85th percentile, and obesity was defined as BMI ]85th percentile, and triceps and subscapular skinfolds ]90th percentile, using the National Center for Health Statistics (NCHS) curves. The following variables were considered as possible confounders: maternal schooling (highest grade achieved), maternal smoking during pregnancy (yes/ no), maternal pre-pregnancy BMI, birth weight (in grams), family income (in minimum wages), sex, skin color (white/black and mixed). At all stages of the cohort study, 10% of the interviews were

repeated by field supervisors for quality control purposes. With the sample size included, it was possible to detect statistically significant relative risks of 0.7 or smaller with a statistical power of 80%, and confidence level of 95%. Analyses were performed using Stata and SPSS, including chi-square tests for heterogeneity or linear trend in the unadjusted analyses, and Wald tests in the adjusted models. Poisson regression was used in the multivariable analysis, as suggested for binary outcomes with high prevalence (12). All stages of the 1993 cohort were approved by the Federal University of Pelotas Medical School Ethics Committee. Mothers or guardians provided written informed consents in each visit. Further details of the methodology of the 1993 Pelotas (Brazil) birth cohort study are available elsewhere (13). Results Out of the 5 265 live born children in 1993, only 16 were not included in the birth cohort study, and 1 460 were sampled for follow-up at six and 12 months; 96.8% and 93.4% respectively, of these children sampled were traced. At 11 years, 4 452 adolescents were traced; added to the 141 known to have died, they represented 87.5% of the original cohort. In this analysis, we included the 1 204 subjects with data available at birth, six and 12 months, and 11 years. Table I describes the sample in terms of sex (49.6% boys), skin color (3/4 white), birth weight (9.8% B2 500 g), family income (18% of the families earning less than one minimum wage per month), maternal schooling (27.2% B4 years), maternal smoking during pregnancy (1/3 of the mothers smoked during pregnancy), maternal pre-gestational BMI (22.6% 25 kg/m2). With respect to breastfeeding, only 3.9% of children had never been breastfed, whereas almost one quarter were breastfed for less than one month and only 18.3% were breastfed for 12 months or more. The proportion of subjects who were predominantly breastfed for less than one month was 27.4%, and 14.9% were predominantly breastfed for at least four months. With respect to solid or semi-solid foods, 85.1% of children had already received it before four months of age. In terms of the variable combining PBF with introduction of other foods, most children received both non-human milk and other foods at the age of four months. With regard to the use of non-human milk, alone or in combination with breast milk, 21.2% received cow’s milk, 33.5% formula and 18.1% both. The frequencies of risk of overweight

Infant feeding and obesity in adolescence Table I. Description of the sample in terms of maternal and child’s characteristics. Variable

%

Adolescent’s sex Male Female

49.6 50.4

Adolescent’s skin color White Blackmixed

70.9 29.1

Birth weight (g) B2 500 ]2 500

9.8 90.2

Family income (in minimum wages) 51 1.13 3.16 6.110 ]10

18.0 45.5 22.3 7.4 6.8

Maternal education (years) 0 14 58 ]9

2.5 24.7 48.2 24.6

Smoking during pregnancy Yes No

33.1 66.9

Maternal BMI (pregestational) B18.5 kg/m2 18.524.99 kg/m2 25.029.99 kg/m2 ]30 kg/m2

8.8 68.7 16.6 6.0

Duration of total breastfeeding (months) B1 12.9 35.9 68.9 911.9 ]12

22.7 26.9 14.7 7.5 9.8 18.3

Duration of predominant breastfeeding (months) B1 11.9 22.9 33.9 ]4

27.4 19.2 21.4 17.1 14.9

Ever breastfed Yes No

96.1 3.9

a The highest number of missing values was 37 (pre-pregnancy BMI). PBFPredominant breastfeeding; BFBreastfeeding; BMIBody mass index.

and obesity at 11 years of age were 23.2% and 11.6%, respectively (data not shown in Table I). Table II presents the association between breastfeeding and the potential confounding variables. Total breastfeeding duration was significantly associated with sex, skin color and maternal schooling. Predominant breastfeeding was associated with skin

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color, birth weight, maternal schooling, and maternal pre-pregnancy BMI. Ever breastfeeding was significantly associated with birth weight; the association with skin color was of borderline significance (P 0.06). Maternal schooling was associated with the introduction of solid or semi-solid foods before four months of age. Table III shows that the risk of overweight was not related to breastfeeding duration, although a protective effect was apparent for children who were breastfed for one to three months compared with those breastfed for 12 months or longer. Results were unchanged after adjustment for sex, skin color, birth weight, maternal schooling, smoking during pregnancy and pre-pregnancy BMI. As for the feeding pattern at age four months, children who received non-human milk were at approximately 30% lower risk of overweight than those who did not. Additional analyses (not presented) showed similar risk of overweight for children receiving cow’s milk and formula. Table IV shows the corresponding analyses for obesity. Although the risk for children breastfed for 12.9 months was still somewhat lower, the differences are not significant. As in the preceding analyses, there was no association with ever breastfeeding or age of introduction of solids and semisolids. Unlike what was observed for overweight, there was no association with the feeding pattern at four months. Discussion Our results fail to show a consistent association between breastfeeding or introduction of complementary foods and the risk of overweight or obesity in young adolescents. The only significant findings were reduced risks of overweight among children breastfed for one to three months, and for those receiving non-human milk at the age of four months, but these were not significant for obesity. Although it is tempting to attribute this finding to a critical window, this result must be interpreted with caution, because such findings were not observed in other studies (4,14), nor even in our population (8,9). Some limitations of our study need to be mentioned. First, duration of exclusive breastfeeding in Pelotas in 1993 was so short that we were not able to analyze this variable separately. Second, body composition data (lean and fat mass separately) are not available, although our definition of obesity at 11 years includes two skinfolds, as recommended by the World Health Organization (11). Strengths of this study include the prospective design, with information on breastfeeding collected in infancy and early childhood, minimizing the likelihood of recall bias.

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% males

% white skin color

Birth weight (g) (mean9s.d.)

% poor (1st quintile of income)

Maternal schooling in years (mean9s.d.)

Maternal BMI in kg/m2 (mean9s.d.)

% maternal smoking

Duration of total breastfeeding (months) B1 12.9 35.9 68.9 911.9 ]12 P*

56.6 48.9 55.6 50.5 39.0 42.1 0.003

76.8 70.7 71.2 71.4 76.3 60.6 0.03

3 114 (608) 3 175 (524) 3 179 (475) 3 231 (507) 3 216 (485) 3 210 (493) 0.27

22.0 16.3 21.0 13.2 19.0 23.0 0.19

6.2 (3.3) 6.7 (3.6) 6.7 (3.4) 8.9 (4.2) 7.3 (3.7) 6.0 (3.0) B0.001

23.0 (4.4) 22.2 (3.8) 22.3 (3.3) 22.7 (3.7) 22.7 (3.6) 23.0 (3.6) 0.56

32.1 39.5 30.5 28.9 32.2 29.0 0.10

Duration of predominant breastfeeding (months) B1 11.9 22.9 33.9 ]4 P*

53.5 49.8 47.9 44.2 50.6 0.31

77.5 69.6 65.0 64.6 76.5 B0.01

3 103 (586) 3 158 (493) 3 242 (524) 3 184 9471) 3 231 (512) 0.01

19.7 21.0 18.2 19.4 19.6 0.96

6.4 (3.6) 6.2 (3.5) 6.6 (3.2) 7.2 (3.8) 7.4 (3.5) 0.001

23.3 (4.3) 22.8 (3.7) 22.6 (3.7) 22.6 (3.6) 22.3 (3.3) 0.001

32.3 32.5 39.3 32.5 27.2 0.11

Ever breastfed Yes No P*

49.4 53.2 0.61

70.4 83.0 0.06

3 186 (517) 2 945 (724) 0.002

19.8 12.8 0.23

6.7 (3.6) 6.0 (3.2) 0.18

22.8 (3.8) 22.7 (4.2) 0.84

33.4 25.5 0.26

Introduction of solid or semi-solid foods before 4 months Yes 49.5 No 50.6 P* 0.79

70.1 78.5 0.08

3 167 (530) 3 166 (562) 0.16

19.4 19.6 0.96

6.6 (3.5) 7.4 (3.5) 0.006

22.9 (3.9) 22.3 (3.3) 0.08

34.1 27.2 0.07

76.5 65.9 60.2 74.6 B0.01

3 231 (512) 3 223 (447) 3 183 (516) 3 147 (556) 0.16

19.6 18.1 20.4 19.3 0.96

7.4 (3.5) 6.9 (3.5) 6.4 (3.7) 6.6 (3.5) 0.02

22.3 (3.3) 22.6 (3.6) 23.1 (3.8) 22.9 (4.0) 0.02

27.2 36.4 26.9 36.1 0.02

Feeding pattern at four months of age PBF]4 months BFsolid or semi-solid food BFsolid or semi-solid foodmilk Milksolid or semi-solid food P*

50.6 38.7 47.0 53.6 0.005

*x2 test (sex, skin color, poverty and maternal smoking) and one-way analysis of variance (birth weight, maternal schooling and maternal body mass index  BMI). PBFPredominant breastfeeding; BF Breastfeeding; BMIBody mass index; s.d.Standard deviation.

M. B. Neutzling et al.

Table II. Relationship between breastfeeding, infant feeding and child, and family characteristics (n1 204).

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Infant feeding and obesity in adolescence Table III. Prevalence of overweight, crude and adjusted prevalence ratios (PR) for overweight at 11 years. Adjusted analysisa

Crude analysis Prevalence of overweight

PR (CI 95%)

P-value

PR (CI 95%)

P-value

Duration of total breastfeeding (months) B1 12.9 35.9 68.9 911.9 ]12

25.7 17.3 21.0 25.3 29.7 26.2

0.99 0.66 0.81 0.97 1.14 1.00

(0.711.38) (0.460.95) (0.541.21) (0.611.54) (0.771.70)

0.09

0.92 0.61 0.81 0.77 1.04 1.00

(0.661.27) (0.430.86) (0.551.18) (0.481.23) (0.701.56)

0.06a

Duration of predominant breastfeeding (months) B1 11.9 22.9 33.9 ]4

23.4 22.9 21.0 21.0 28.9

0.81 0.79 0.73 0.73 1.00

(0.581.14) (0.551.14) (0.501.06) (0.491.07)

0.44

0.80 0.82 0.71 0.74 1.00

(0.571.12) (0.571.17) (0.491.01) (0.511.10)

0.64a

Ever breastfed Yes No

23.3 21.3

1.09 (0.611.93) 1.00

0.77

0.95 (0.531.72) 1.00

0.87a

Introduction of solid or semi-solid foods before 4 months Yes 22.3 No 28.9

0.77 (0.581.03) 1.00

0.08

0.77 (0.581.02) 1.00

0.07

Feeding pattern at four months of age PBF]4 months BFsolid or semi-solid food BFsolid or semi-solid foodmilk Milksolid or semi-solid food

1.00 1.00 (0.701.45) 0.67 (0.440.99) 0.74 (0.551.00)

0.05

1.00 1.00 (0.701.43) 0.69 (0.471.02) 0.73 (0.540.99)

0.05a

28.9 28.9 19.1 21.3

a Likelihood-ratio test for heterogeneity adjusted for infant’s sex, infant’s skin color, infant’s birth weight, family income (first quintile), maternal schooling, smoking during pregnancy and maternal pregestational body mass index. PBFPredominant breastfeeding; BF Breastfeeding.

Furthermore, we included in our analysis the main confounding factors reported in previous studies (15), thus reducing the likelihood of residual confounding. In particular, residual confounding due to socio-economic factors is unlikely to account for this association because longer breastfeeding duration was not associated with high socio-economic and educational level (8,9), unlike that which is observed in high-income countries (16). The high follow-up rate minimizes the likelihood of selection bias. Horta et al. (17) concluded that breastfeeding was inversely associated with overweight in adolescence using meta-analytic techniques (pooled odds ratio: 0.69; 95% CI: 0.60; 0.80). Other meta-analyses have found similar results (15,18,19), although Owen et al. (15) concluded that publication bias was likely in the studies on this issue. A few studies from developed countries reported no association (6,20). Virtually all studies included in these metaanalyses derive from high-income countries. We now have three studies that did not find a higher risk of overweight or obesity for children who

were not breastfed, or who were breastfed for short periods. These findings came from two separate birth cohorts from Pelotas, using as outcomes BMI and body composition at 18 years (8), and weightfor-height Z-score at four years (9). We propose three possible explanations for this discrepancy with most of the literature. One possibility is that unlike studies from developed countries, residual confounding by socio-economic status is not present in our analyses (Table II). Second, there may be local peculiarities regarding the type of local weaning foods, which are different from those used in developed countries. Third, a recent study in our population showed that sleeping metabolic rate was higher among 8-month-old babies who received cow’s milk in addition to breast milk, compared with those who received only breast milk (21). Such higher rates may offset the additional nutrient intake associated with non-human milk. Further research is needed to elucidate these possible pathways. Even if breastfeeding has no long-term lasting protective effect on the risk of obesity, its other

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Table IV. Prevalence of obesity, crude and adjusted prevalence ratios (PR) for obesity at 11 years. Adjusted analysisa

Crude analysis Prevalence of obesity

PR (CI 95%)

P-value

PR (CI 95%)

P-value

Duration of total breastfeeding (months) B1 12.9 35.9 68.9 911.9 ]12

14.7 8.0 9.7 11.0 14.4 13.1

1.10 0.62 0.74 0.81 1.08 1.00

(0.681.80) (0.361.08) (0.391.39) (0.381.73) (0.582.01)

0.28

0.99 0.58 0.73 0.64 1.14 1.00

(0.601.64) (0.331.02) (0.401.32) (0.301.35) (0.622.10)

0.17a

Duration of predominant breastfeeding (months) B1 11.9 22.9 33.9 ]4

11.9 13.0 11.3 9.3 12.2

0.96 1.08 0.91 0.75 1.00

(0.561.65) (0.611.90) (0.511.64) (0.391.43)

0.83

0.85 1.05 0.87 0.75 1.00

(0.491.47) (0.591.85) (0.501.53) (0.401.42)

0.81a

Ever breastfed Yes No

11.7 8.5

1.30 (0.473.59) 1.00

0.61

1.34 (0.453.91) 1.00

0.60a

Introduction of solid or semi-solid foods before 4 months Yes No

11.5 12.2

0.93 (0.581.50) 1.00

0.78

0.88 (0.551.41) 1.00

0.60

Feeding pattern at four months of age PBF]4 months BFsolid or semi-solid food BFsolid or semi-solid foodmilk Milksolid or semi-solid food

12.2 12.7 12.0 10.8

1.00 1.05 (0.571.95) 0.97 (0.531.76) 0.88 (0.531.45)

0.62

1.00 1.09 (0.601.99) 0.93 (0.511.68) 0.81 (0.491.33)

0.61

a

a Likelihood-ratio test for heterogeneity adjusted for infant’s sex, infant’s skin color, infant’s birth weight, family income (first quintile), maternal schooling, smoking during pregnancy and maternal pregestational body mass index. PBFPredominant breastfeeding; BF Breastfeeding.

benefits, including short-term protection against infectious diseases and mortality (22), and longterm benefits (17,19) support its continued promotion. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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