toddler nutrition

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ToddlerNutrition

• Nutrient Intakes of Toddlers vs Recommendations

• Metabolic Programming• Overweight Status and Risk• DHA in Toddler Nutrition

Toddler NutritionTABLE OF CONTENTS

Executive Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .6

Nutrient Intakes of Toddlers vs Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .9Recommended Intakes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .10Macronutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .11Micronutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .14Over Consumption of Micronutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .20

Metabolic Programming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .23The Intrauterine Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .24Birth Weight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .24Maternal Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .25Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .25Toddlers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .25References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26

Overweight Status and Risk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .27Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28Prevalence of Overweight in Children . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28Definitions of Overweight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .29Health Risks Associated with Overweight in Childhood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .29Energy Imbalance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .29Family and Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .31Infant Nutrition and Growth Pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .32What To Do? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .33References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .34

DHA in Toddler Nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .37Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .38Sources of DHA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .38Physiological Roles for DHA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39DHA and the Growing Brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39Indicators of DHA Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .40DHA Intakes of Toddlers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .40DHA Status of Toddlers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .41Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .42References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .42

TA B L E O F C O N T E N T S

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Medical and drug information is constantly evolving because of ongoing research and clinical experience that are often subject to interpretation. While care has been taken to ensure the accuracy of the informationpresented, the reader is advised that Mead Johnson & Company, and the authors, editors, reviewers,contributors, and publishers of this material are not responsible for the continued currency of the informationcontained in this material, or any errors or omissions that might appear in this material, or for anyconsequences arising out of, or resulting from, the use of the material for any purpose or reason whatsoever.Because of the dynamic nature of medical and drug information, readers are advised that decisions regardingdrug or any other therapy must be based on the independent judgment of the clinician, information about adrug (eg, as reflected in the literature), and changing medical practices.

The Editors and Mead Johnson & Company

Toddler Nutrition

Contributors:

Robert Baker, MD, PhD Professor of Pediatrics

State University of New York at BuffaloCo-Chief, Digestive Disease and Nutrition Center

Women and Children’s Hospital of Buffalo

Benjamin H. Caballero, MD, PhDProfessor of Pediatrics, International Health and Maternal and Child Health

Director, Center for Human Nutrition, Bloomberg School of Public HealthJohns Hopkins University

Barbara A. Dennison, MD Clinical Professor of Epidemiology

State University of New York at AlbanyDirector, Bureau of Health Risk Reduction

Division of Chronic Disease Prevention and Adult HealthNew York State Department of Health

Sheila M. Innis, PhD, MScProfessor, Department of Pediatrics

Director, Nutrition Research ProgramBC Research Institute for Children’s and Women’s Health

University of British Columbia

Rebecca Simmons, MDProfessor of Pediatrics

Center for Research on Reproduction and Women’s Health Children’s Hospital of Philadelphia

University of Pennsylvania Medical Center

Bonny Specker, PhD Professor, Nutrition, Food Science and Hospitality

Chair & Director, Ethel Austin Martin Program in Human NutritionSouth Dakota State University

1.7 g alpha-linolenic acid per day and 88 mg DHA/day with the lowest intake of about 40 mg DHA/day occurring at 18 to 24 months of age. Researchers also evaluated the DHA concentration of red blood cellphosphatidylethanolamine in 18- to 60-month-old children and found these DHA levels to be lower than that of newborns, breastfed infants, or children of older ages. DHA concentration of the 18- to 60-month-oldchildren was comparable to that of 3-month-old infants fed formula without DHA. The importance of adequate n-3 fatty acid nutrition and the relatively low DHA concentration observed in toddlers indicate that n-3 fatty acid nutrition of children ages 1 to 5 years deserves further investigation.

Overweight is a critical health care issue for toddlers and the prevalence and extent of overweight in toddlers is increasing dramatically. Children with a body mass index (BMI) at or above the 85th but less than the 95thpercentile for age and sex are considered to be “at risk of overweight.” Children with a BMI at or above the 95thpercentile for age and sex are considered “overweight.” Overweight contributes to numerous health conditions in childhood as well as increased morbidity and mortality in adulthood. The energy imbalance leading to thechildhood obesity epidemic may be related to physical inactivity and food consumption trends (increased portionsizes, frequent consumption of fast foods and sweet beverages and decreased consumption of vegetables).Family and environmental characteristics including television-viewing habits appear to be important predictorsof overweight in children. Television viewing appears to affect weight by influencing eating behaviors, foodchoices, and activity patterns.

Infant nutrition and infant growth patterns may influence weight status later in childhood and adulthood. Rapidgrowth during early infancy has been linked to overweight later in childhood and early adulthood.5 Breastfeedingmay help protect against later obesity, but it is difficult to determine if weight differences between children andadults who were breastfed compared with those who were formula fed are due to factors in human milk,differences in characteristics of mothers who breastfeed versus those who formula feed, and/or differences inmaternal feeding and parenting practices.

Many parents do not recognize that their children are overweight or at risk of overweight. In addition, pediatrichealth care providers may not routinely screen for overweight by measuring or plotting BMI for age. The AmericanAcademy of Pediatrics now urges physicians to routinely screen toddlers for overweight by measuring BMI and toimplement steps to help prevent this increasingly prevalent problem.

E X E C U T I V E S U M M A RY

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Executive SummaryToddlers (children ages 1 to 5 years) experience rapid growth and development. During periods of rapid growthand development, a child may be particularly vulnerable to inappropriate dietary patterns and nutrition. Expertshypothesize that insufficient or excess supply of energy and/or other nutrients during critical periods of growthmay program a child to develop health conditions such as overweight, diabetes and hypertension in childhood or later in life. In addition, some micronutrient deficiencies during early life result in irreversible deficits indevelopment.

Toddlers’ eating patterns and behaviors prompt concern about the nutritional adequacy of their diets. As toddlers transition from a liquid nutrient dense diet of predominantly breast milk and/or infant formula to a diet consisting primarily of table foods, their diets may become less dense in some nutrients. Toddlers are also learning to feed themselves and are neophobic, rejecting foods that are new because they are unfamiliar.Parents often describe toddlers as picky eaters.

Despite the potential importance of toddler nutrition and the characteristics of toddlers’ eating patterns andbehaviors, the nutritional needs of toddlers have not been well defined. Relatively little data on toddler nutritionand the long-term health consequences of toddler nutrition exist.

The Dietary Reference Intakes (DRI) are the best standards based on current scientific evidence available forevaluating toddlers’ nutrient intakes. Data indicate that young children consume more energy than DRIestimated requirements but meet recommended intakes of carbohydrate and protein. Fiber intakes, however,rarely meet recommendations. Added sugars are a potential nutritional concern because intakes of more than20% to 25% of energy may dilute the nutrient density of children’s diets.

Intake data indicate that toddlers between the ages of 1 and 5 get recommended amounts of most vitamins andminerals. Yet pediatric health care providers should not be complacent about micronutrient intakes. Iron deservescontinued attention since iron deficiency in the first years of life is relatively common and may have irreversiblenegative consequences on development. In addition, calcium and vitamin D are critical for bone health and peakbone mass and should receive continued emphasis. As other beverages displace milk in toddlers’ diets, calciumand vitamin D intakes decrease. Preliminary data indicate that significant numbers of toddlers approachingschool age may not get recommended amounts of these nutrients. Intake data indicate that vitamin E intakes by young children are lower than recommendations. The nutritional significance of this finding is not known.Possible over consumption of some micronutrients may be an issue for some young children. Over consumptionof vitamin A deserves consideration and unwarranted supplementation should be avoided. Further data onrecommended upper levels of intake for vitamins and minerals are needed since there are few data specific to toddlers.

The importance of dietary n-3 fatty acids, including docosahexaenoic acid (DHA), for infant brain and retinaldevelopment and in adult health, highlights the need to investigate DHA status and n-3 fatty acid nutrition inchildren, particularly those between the ages of 1 and 5 years at which time brain development is continuing.Infants between the ages of 1 and 6 months who consume breast milk or formula with 3.7 g fat/100 mL and 0.3% of the fatty acids as DHA will receive 86 mg DHA with an intake of 780 mL of breast milk or formula per day. Recent studies have estimated that toddlers and children ages 18 to 60 months consume about

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The potential impact of inappropriate toddler nutrition and the relative paucity of data on toddlers promptedMead Johnson Nutritionals to gather a group of pediatric nutrition experts to discuss 4 areas of nutrition forhealthy toddlers in the U.S.: energy, macronutrient and micronutrient intakes, metabolic programming,overweight status and risk, and docosahexaenoic acid (DHA) nutrition. This monograph summarizes theirpresentations and includes additional data and positions published since the panel’s discussion. The goal of the monograph is to raise awareness of toddler nutrition issues and the importance of food patterns andnutrient intakes for healthy toddlers among pediatric health care professionals.

7I N T R O D U C T I O N

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IntroductionAlthough growth velocity is greater during infancy than in toddlerhood, toddlers do experience rapid growth and development. During periods of rapid growth and development, a child may be particularly vulnerable toinappropriate dietary patterns and nutrition. Experts hypothesize that insufficient or excess supply of energyand/or other nutrients during critical windows of growth and development may program a child to develophealth conditions such as overweight, diabetes, and hypertension in childhood or later in life. In addition, somemicronutrient deficiencies during early life result in irreversible deficits in mental and motor development. Newresearch on the importance of specific nutrients in promoting growth and development of infants and long-termhealth of adults is prompting scientists to consider the potential importance of these nutrients for toddlers as well.

Toddlers’ eating patterns and behaviors prompt concern aboutthe nutritional adequacy of their diets. The toddler years arecharacterized by a transition from a predominantly defined,nutrient dense, liquid diet of breast milk or infant formula to a diet consisting primarily of table foods provided by 3 mealsand snacks daily.1 Toddlers’ diets may become less dense insome nutrients as they transition from an infant diet to a dietof solid foods.1 Toddlers are also developing the motor skillsrequired to feed themselves and this may influence nutrientintake.2 Toddlers are often described as having food“neophobia.” That is, they express dislike or reject foods thatare new because they are unfamiliar. Young children oftenrequire repeated exposure to a food before accepting it.3 Manyparents consider their toddlers to be picky eaters, and thisincreases as toddlers age. Carruth and colleagues reportedthat 35% of caregivers of 12- to 14-month-olds considered theirtoddlers to be picky eaters. For caregivers of toddlers ages 19to 24 months, the percentage was 50%.4 Neophobia and the perception of having a picky eater may influence thenutritional quality of the diets offered to and consumed by toddlers.

Despite the potential importance of toddler nutrition and characteristics of toddlers’ eating patterns andbehaviors, the nutritional needs of toddlers have not been well studied. Breast milk and breastfed babies are thestandards for infant nutrition; and, using these standards, the nutritional needs of infants have been fairly welldefined as infant formulas have been developed and studied. National surveys in the U.S. have evaluated thenutritional status and nutritional intakes of older children and adults for many years. In contrast, relatively fewtoddlers are included in these surveys. Moreover, there are few data on physiological nutrient requirements ofyoung children and potentially adverse or beneficial effects of increased nutrient intakes by young children.5 Inaddition, little is known about the physical activity patterns of young children and how activity affects nutrientrequirements and growth. Few nutritional status indicators have been identified that are specific to this agegroup. Consequently, the nutritional needs of toddlers are less well defined.

6 I N T R O D U C T I O N

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WHAT IS A TODDLER?

The term toddler comes from the

wide-based, unsteady, toddling

gait of a child learning to walk.

Pediatric medicine has no official

definition of toddlers but

toddlerhood is generally thought

to begin at 12 months of age and

can include preschoolers up to 5

years of age.

N U T R I E N T I N TA K E S O F TO D D L E RS VS R E C O M M E N DAT I O N S

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Nutrient Intakes of Toddlers vs Recommendations

Contributors:

Robert Baker, MD, PhD Professor of Pediatrics

State University of New York at BuffaloCo-Chief, Digestive Disease and Nutrition Center

Women and Children’s Hospital of Buffalo

Benjamin H. Caballero, MD, PhDProfessor of Pediatrics, International Health and Maternal and Child Health

Director, Center for Human Nutrition, Bloomberg School of Public HealthJohns Hopkins University

Bonny Specker, PhD Professor, Nutrition, Food Science and Hospitality

Chair & Director, Ethel Austin Martin Program in Human NutritionSouth Dakota State University




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s RECOMMENDED INTAKESBetween 1941 and 1989, the Food and Nutrition Board of the Institute of Medicine prepared the RecommendedDietary Allowances to provide “standards to serve as a goal for good nutrition.”6 In 1997, the Institute of Medicinepublished the first in a set of Dietary Reference Intakes (DRI), which replace the previous Recommended DietaryAllowances.7 According to Yates et al., “DRIs are reference values that are quantitative estimates of nutrientintakes to be used for planning and assessing diets for healthy people.”8 DRI have been established for energyand the macronutrients that provide energy (carbohydrate, protein and fat)9 as well as micronutrients (vitaminsand minerals).7, 10-12 The DRI include Estimated Average Requirements (EAR), Recommended Dietary Allowances(RDA), Adequate Intakes (AI), and the Tolerable Upper Intake Levels (UL).9 For nutrients that yield calories,Acceptable Macronutrient Distribution Ranges (AMDR) were also established.9 Estimated Energy Requirements(EER) are used for determining energy needs.9 Table 1 defines terms associated with the DRI.8, 9

Table 1. Definitions of Terms Associated With the Dietary Reference Intakes8,9

Estimated Average Requirement (EAR): The average daily nutrient intake level estimated to meetthe requirements of half the healthy individuals in a particular life stage and gender group. TheEAR is used to develop the RDA.

Recommended Dietary Allowance (RDA): The average daily dietary nutrient intake level sufficientto meet the nutrient requirements of nearly all (97% to 98%) healthy individuals in a particularlife stage or gender group. RDA can also be used as intake goals for individuals.

Adequate Intake (AI): The recommended average daily intake level based on observed orexperimentally determined approximations of nutrient intake by a group (or groups) ofapparently healthy people that are assumed to be adequate—used when an RDA cannot bedetermined. AI can also be used as intake goals for individuals.

Tolerable Upper Intake Level (UL): The highest average daily nutrient intake level that is likely topose no risk of adverse health effects to almost all individuals in the general population. As intakeincreases above the UL, the potential risk of adverse effects may increase.

Acceptable Macronutrient Distribution Range (AMDR): Ranges of macronutrient intakes (as apercentage of calories) that are associated with reduced risk of chronic disease while providingrecommended intakes of other essential nutrients. Little data on the consequences of exceedingAMDR in young children exist, however.

Estimated Energy Requirement (EER): The average dietary energy intake that is predicted tomaintain energy balance in a healthy adult of a defined age, gender, weight, height and level ofphysical activity, consistent with good health. In children, the EER is taken to include the needsassociated with the deposition of tissues consistent with good health.


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Limitations of the data on toddler nutrition made defining toddlers’ nutrient requirements extremelychallenging. For most nutrients there are no data on toddlers’ physiological requirements resulting from directassessment. Most nutrient intake recommendations for toddlers come from observations of intake. In addition,there are few nutritional status indicators specific for this age group. It is not clear if nutritional status indicatorsused for older children and adults are valid for toddlers. There are little data on the adverse or beneficial effects of high nutrient intakes in children. Finally, there are few data on physical activity patterns of young children and how they affect nutrient requirements and growth. Despite the limitations, the DRI are the best standardsavailable based on current evidence for evaluating toddlers’ macronutrient and micronutrient intakes.

MACRONUTRIENTSIn 2002, DRI were established for energy, carbohydrate, protein, and fat.9 Data indicate that young childrenconsume more energy than estimated requirements, and intakes meet recommendations for carbohydrate andprotein. Fiber intakes, however, rarely meet recommendations.

Total EnergyCalculations for estimated energy requirements (EER) for young children were based on research in which energyneeds were determined using the doubly labeled water method. This method is more accurate than factorialmethods and measurements of basal metabolic rate used for making past energy estimates. The doubly labeledwater method allows measurement of energy output under normal everyday conditions; it represents patterns of energy expenditure over several days; it reflects differences in basal metabolic rate during awake and sleepstates; and it includes the energy cost of all physical activities.

EER for children equals total energy expenditure plus energy deposition. Total energy expenditure is influencedby age, sex, height, weight, and physical activity level and these variables are included in the calculations. Theenergy deposition value is an estimate of the amount of daily energy required for growth.9 The new equationsare provided in Table 2.9

Table 2. Equations for Estimating Energy Requirements9

Children 13 to 35 months (boys and girls)EER = (89 x weight in kg-100) + 20 [the estimated kcal needed for energy deposition]

Boys 3 through 8 yearsEER = 88.5-61.9 x age in years + physical activity level x (26.7 x wt in kg + 903 x ht in m) + 20 [theestimated kcal needed for energy deposition]

Physical activity levels: 1.00 for sedentary; 1.13 for low active; 1.26 for active; 1.42 for very active

Girls 3 through 8 yearsEER = 135.3-30.8 x age in years + physical activity level x (10.0 x wt in kg + 934 x ht in m) + 20 [theestimated kcal needed for energy deposition]

Physical activity levels: 1.00 for sedentary; 1.16 for low active; 1.31 for active; 1.56 for very active

As part of the Feeding Infants and Toddlers Study, Devaney and colleagues evaluated energy intakes of toddlersages 12 to 24 months.13 They found that usual energy intakes exceed EER for children in all percentiles of usualintake (Figure 1). Average intake was 1249 kilocalories per day while average EER was 950 kilocalories per day.13 Ingeneral this is consistent with other surveys that indicate that children consume more than estimatedrequirements.9

Figure 1. Energy Intakes and Estimated Energy Requirements of 1- to 2-Year-Old Toddlers(adapted from7)

FatTable 3. Acceptable Macronutrient Distribution Ranges for Fat9

1 to 3 years: 30% to 40% of energy from fat

4 to 18 years: 25% to 35% of energy from fat

The DRI committee did not establish an EAR, RDA, AI, or UL for total fat for children9 because there wasinsufficient evidence for defining a total fat intake in childhood that would support growth while decreasing therisk of obesity, diabetes, or coronary heart disease. The committee did, however, establish AMDR for fat. Thehigher range for fat for children ages 1 to 3 years reflects the transition from a diet primarily consisting of breastmilk and/or infant formula, both which provide about 50% of calories from fat, to a diet primarily consisting ofsolid foods. The lower range for children over the age of 3 years is similar to recommendations for adults.Devaney et al. reported that 29% of toddlers between the ages of 1 and 2 years had fat intakes less than 30% ofcalories and 9% had fat intakes exceeding 40% of calories.13 Although reduced fat intakes have been linked tolower intakes of certain micronutrients in other studies,14 intakes of most micronutrients in the Feeding Infantsand Toddlers Study were adequate.13


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s Table 4. Recommended Intakes (AI) and Acceptable Macronutrient Distribution Ranges for n-6 and n-3 Fatty Acids9

Linoleic acid and n-6 fatty acidsAI: 7 to 10 g/day of linoleic acidAMDR for n-6 fatty acids: 5% to 10% of total energy

α-Linolenic acid and n-3 fatty acidsAI: 0.7 to 0.9 g/day of α-linolenic acid (includes small amounts of eicosapentaenoic acid [EPA] and docosahexaenoic acid [DHA])

AMDR for α-linolenic acid: 0.6% to 1.2% of total energy. Up to 10% of this can come from EPA and DHA.

Recommended adequate intakes (AI) for the essential fatty acids, linoleic acid (C18:2n-6; an 18 carbon, 2-doublebond, n-6 fatty acid), and α-linolenic acid (C18:3n-3; an 18-carbon, 3-double bond, n-3 fatty acid) were established(Table 4). AMDR were also established for n-6 and n-3 fatty acids.9

CarbohydrateTable 5. Recommended Intakes (RDA or AI) and Acceptable Macronutrient Distribution

Ranges for Carbohydrate, Fiber, and Added Sugars9

RDA/AI RDA/AI AMDR1- to 3-year-olds 4- to 8-year-olds

Carbohydrate 130 g/day 130 g/day 45% to 65% of energyFiber ~19 g/day ~25 g/day Not determinedAdded Sugars Not determined Not determined _< 25% of energy*

*AMDR for added sugars not determined. Value is maximal intake level.

Total CarbohydrateThe recommended intake (RDA) for total carbohydrate by young children is 130 grams per day9 and is the same asthe RDA for adults, which was based on a carbohydrate intake that was associated with blood ketone levels thatwere no higher than ketone levels after an overnight fast. No UL for carbohydrate was established because therewas no definitive evidence that a high carbohydrate diet leads to obesity, diabetes, or coronary heart disease inchildren. Data indicate that toddlers’ intakes meet the RDA for carbohydrate. Devaney and colleagues found thataverage carbohydrate intake of 1- to 2-year-olds was 165 g/day.13 The USDA Continuing Survey of Food Intakes byIndividuals 1994-96, 1998 (CSFII) found that the average carbohydrate intakes of 1- to 2-year-olds and 3- to 5-year-olds were 179 g/day and 227 g/day, respectively.15

FiberRecommendations (AI) for total fiber intakes for children wereestablished at 14 grams of fiber/1000 kilocalories.9 The FeedingInfants and Toddlers Study, however, found that average fiberintake of toddlers between the ages of 1 and 2 years was belowthe recommendation and was 8 g/day.13 Children in the 90thpercentile of fiber consumption consumed 12 g/day. In the USDAContinuing Survey of Food Intakes by Individuals 1994-96, 1998(CSFII), 1- to 2-year-old children consumed 9 grams of fiber dailyand 3-to 5-year-old children consumed 11 grams.15

Added SugarsAdded sugars are a potential nutritional concern because highintakes may dilute the nutrient density of children’s diets. Amaximal intake level for added sugars was suggested at no morethan 25% of energy.9

“Added sugars are defined as sugars and syrups that are added to foods during processing or preparation.”Examples of added sugars include white sugar, raw sugar, corn syrup, high-fructose corn syrup, malt syrup,honey and molasses.13

ProteinTable 6. Recommended Intakes (RDA) and Acceptable Macronutrient Distribution

Ranges for Protein13

RDA AMDR1- to 3-year-olds 1.10 g/kg/day (~13 g/day) 5% to 20% of energy4- to 8-year-olds 0.95 g/kg/day (~19 g/day) 10% to 30% of energy

The 2002 DRI protein intake recommendations decreased slightly from the 1989 RDA.6, 13 Protein intakerecommendations were based on data indicating nitrogen intakes required for maintenance, replacement oflosses and growth. No UL was established for protein because there was insufficient evidence of adverse healtheffects from humans consuming high levels. Dietary intakes of protein by young children typically exceedestimated needs.

MICRONUTRIENTSNutrient intake data indicate that toddlers between the ages of 1 and 5 get recommended amounts of mostmicronutrients (Tables 7 and 8).7, 10-13, 15 Despite data indicating that young children are consuming recommendedintakes for most micronutrients, iron deserves continued attention since iron deficiency in the first years of life isrelatively common and may have irreversible negative consequences on development.17 In addition, calcium andvitamin D are critical for bone health and peak bone mass and should receive continued emphasis. Nutrientintake data indicate that vitamin E intakes by young children are low and should be considered. Possible overconsumption of some micronutrients may be an issue for some young children.

15N U T R I E N T I N TA K E S O F TO D D L E RS VS R E C O M M E N DAT I O N S

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s Table 7. Recommended Nutrient Intakes vs Average Nutrient Intakes for Children 1 to 3 Years of Age7,10-13,15,18

RDA/AI Average intakes, Average intakes, Average intakes, UL, 1-toNutrient 1- to 3- 1- to 2- 1- to 2- 3-year-olds, 3-year-

year-olds year-olds, FITS year-olds, CSFII CSFII olds

Vitamin A, mcg RE 300 694 739 782 600Vitamin D, mcg 5 8.7 6.0 (1- to 3-year-olds) 50Vitamin E, mg TE 6 5 4.8 5.4 *200Vitamin C, mg 15 91 103 106 400Thiamin, mg 0.5 1.2 1.13 1.32 NDRiboflavin, mg 0.5 1.8 1.71 1.82 NDNiacin, mg 6 13 12.8 15.5 *10Vitamin B-6, mg 0.5 1.3 1.3 1.47 30Folate, mcg 150 318 198 263 *300Vitamin B-12, mcg 0.9 3.7 3.2 3.54 ND

Calcium, mg 500 939 854 843 2500Phosphorus, mg 460 968 966 1034 3000Magnesium, mg 80 184 187 201 *65Iron, mg 7 9.8 10.8 12.3 40Zinc, mg 3 6.9 7.4 8.5 7Copper, mg 0.34 Not reported 0.7 0.8 1Selenium, mcg 20 Not reported 59.8 68.9 90Values in bold type are RDA.*UL for vitamin E, niacin, and folate apply to synthetic forms obtained from supplements, fortified foods, or a combination of the two. UL formagnesium represents intake from a pharmacological agent only and does not include intake from food or water.

ND=not determined.

IronThe prevalence of iron deficiency in toddlers ages 1 to 2 years in the United States has decreased in the pastdecade from 9% to 7%.19 For children ages 3 to 5 years, however, iron deficiency increased from 3% to 5%.19 Themost severe form of iron deficiency, iron deficiency anemia, occurs in about 2% of 1- to 2-year-olds in the U.S.19

Infants and toddlers are at greater risk of iron deficiency in the first two years of life than older andpreadolescent children due to rapid growth.20 Children in households with inadequate financial resources weremore likely to have iron deficiency anemia.21 In a study involving 12–36 month old children from WIC clinics inCalifornia, Schneider et al., noted a prevalence of iron deficiency and anemia in the population.22 Females in thisstudy population demonstrated lower iron stores than boys. Early iron deficiency can adversely affect mental andmotor development and behavior,23-25 and some effects are not reversible with iron therapy, persisting severalyears after the deficiency is corrected.17

Toddlers who may be at greatest risk of iron deficiency include those who were born with low iron stores due toprematurity, who experienced intrauterine growth retardation, or who had a mother with gestational diabetes.20

Toddlers who did not receive adequate dietary iron in the first year of life are also at greater risk. Inadequate ironintakes during infancy can result from feeding low iron infant formula, feeding milk (cow, goat and/or soy)

Definitions of Fiber wereestablished in 200016:Dietary fiber: fiber naturally present infoods of plant origin, such as celluloseand the fibers in oat and wheat bran.

Functional fiber: fiber that has beenisolated, extracted, or synthesized andhas proven beneficial effects inhumans, such as resistant starch.

Total fiber: the sum of dietary fiber andfunctional fiber.

Table 8. Recommended Nutrient Intakes vs Average Nutrient Intakes for Children 4 and 5 Years of Age7,10-12,15

Nutrient RDA/AI, Average Average UL,4- to 8- intakes, intakes, 4- to 8-

year-olds 4-year-olds, CSFII 5-year-olds, CSFII year-olds

Vitamin A, mcg RE 400 834 832 900Vitamin D, mcg 5 Not reported Not reported 50Vitamin E, mg TE 7 5.9 6.3 *300Vitamin C, mg 25 106 99 650Thiamin, mg 0.6 1.42 1.47 NDRiboflavin, mg 0.6 1.9 1.97 NDNiacin, mg 8 17 18.1 *15Vitamin B-6, mg 0.6 1.54 1.61 40Folate, mcg 200 283 279 *400Vitamin B-12, mcg 1.2 3.73 3.84 ND

Calcium, mg 800 864 887 2500Phosphorus, mg 500 1085 1136 3000Magnesium, mg 130 212 222 *110Iron, mg 10 13.4 13.9 40Zinc, mg 5 9.3 9.7 12Copper, mg 0.44 0.9 0.9 3Selenium, mcg 30 75.1 80.7 150

Values in bold type are RDA.*UL for vitamin E, niacin, and folate apply to synthetic forms obtained from supplements, fortified foods, or a combination of the two. UL for magnesium represents intake from a pharmacological agent only and does not include intake from food or water.ND=not determined.

instead of breast milk or iron fortified infant formula, and not providing supplemental iron source to a breastfedinfant.20 Data also indicate that iron density of the diet decreases as toddlers transition away from an infant diet.1

Toddlers who do not consume iron from meat or other food sources may also be at risk.

The American Academy of Pediatrics (AAP) recommends several steps for preventing iron deficiency.20 Infantsshould be breastfed and breastfed infants should receive a supplemental iron source by 4 to 6 months of age.If infants receive infant formula as a supplement to or in place of breast milk, only iron-fortified formula shouldbe used during the first 12 months of life. Milk (cow, goat, soy) should not be introduced before 12 months of age.Iron-rich foods, such as iron fortified cereal and meats should be introduced at weaning.20 Physicians shouldscreen infants and toddlers at risk of developing iron deficiency by measuring hemoglobin or hematocrit levelsbetween 9 and 12 months of age, and 6 months later at 15 to 18 months of age.20 The AAP recommends thatchildren ages 1 to 5 years should avoid consuming more than 24 ounces of milk per day because large amounts of milk may displace iron-rich foods in the diet.20

Calcium and Vitamin DLittle data on the calcium requirements of toddlers and young children exist. Lack of data prevented the DRIcommittee from setting an RDA for calcium. Only AI have been established for this nutrient. The AI for calcium


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s for children ages 1 through 3 is 500 mg per day, and for children ages 4 through 8 is 800 mg per day.7 The optimalcalcium intake for young children, however, has not been determined.

Nutrient intake data indicate that average calcium intakes by 1- to 3-year-old toddlers exceed the AI of 500 mg per day. Reported average calcium intakes were 939 mg13 and 854 mg per day for 1- to 2-year-olds15

and 843 mg per day for 3-year-olds.15 Intake data indicate that average calcium consumption by 4- and 5-year-oldchildren exceeds the AI of 800 mg per day, with 864 mg per day consumed by 4-year-olds, and 887 mg per dayconsumed by 5-year-olds.15

Lack of data also prevented the DRI committee from establishing an RDA for vitamin D for children 1 to 8 years of age. The AI for toddlers 1 to 3 years and children ages 4 to 8 years is 5 mcg (200 IU) per day.7

The Feeding Infants and Toddlers Study evaluated vitamin D intakes by 1- to 2-year-old toddlers and reportedaverage intakes of 8.7 mcg (348 IU) per day.13 Moore and colleagues summarized vitamin D data from CSF II andNHANES III and report intakes of 6.0 and 5.7 mcg/d for children 1 to 3 years of age, respectively.18 Data from bothstudies indicate that approximately 50%–60% of this age group is meeting the adequate intake level (5 mcg/day)established for vitamin D.

Specker and colleagues conducted a preliminary analysis of calcium and vitamin D intakes of 5449 1- to 5-year-oldchildren in NHANES III. The unpublished results were based on raw data and did not take into account thesampling scheme used by NHANES III (Figure 2). They found that among children 1 to 5 years of age, the lowest calcium intakes (747 mg/day) were by toddlers ages 24 to 35 months. Children 36 to 47 months had anaverage calcium intake of 768 mg per day, while children 48 to 60 months had an average intake of 803 mg perday. About 50% of the children in these older age groups, however, had calcium intakes below the AI of 800 mg.Average vitamin D intakes were lowest for toddlers ages 24 to 35 months (5.31 mcg/day). About 50% of childrenages 24 to 60 months had vitamin D intakes less than the AI of 5 mcg per day, which is in agreement with Mooreand colleagues findings for 1- to 3-year-olds.18

In their evaluation of NHANES III data, Specker and colleagues noted sex, regional, and ethnic differences incalcium and vitamin D intakes: females have lower intakes than males; toddlers in the South have lower intakesthan toddlers in other regions; and, non-Hispanic blacks have lower intakes than other ethnic groups. Fulgoni andcolleagues reported calcium intakes for 0- to 3-year-olds were significantly lower in African-American childrenthan in children of other races (CSFII: Female: 614 vs 818*; Male: 724 vs 869*; NHANES [1999-2000]: Female 682 vs809; Male: 756 vs 981*; *P<0.05).26

Low intake of milk, which serves as a source of calcium and vitamin D in the diet, in childhood and adolescencewas associated with a decrease in bone mineral content and density, as well as an increased risk of fracture inwomen.27 NHANES III data on children and adolescents aged 8 to 18 years indicate that a higher intake of low-nutrient dense foods is related to a lower intake of several micronutrients, including calcium.28 Greer et al., in therecent AAP position on calcium, provide a summary of data sets regarding calcium intakes and demonstrate that,with an increase in age, the percentage of children and adolescents achieving the recommended intakes ofcalcium decreases from approximately 93% at less than a year of age to 30% between the ages of 12 and 19.29

Figure 2. NHANES III Preliminary Results. Calcium (upper panel) and Vitamin D (lower panel)Intake by Age (Specker et al., unpublished)

Vitamin D fortified liquid milk is a primary source of calcium and vitamin D in toddlers’ diets, and as milk intakesdecrease, dietary intakes of calcium and vitamin D decrease. Skinner and colleagues reported that 100% juice,fruit drinks, and carbonated beverages may displace milk in the diets of 1- to 2-year-old toddlers leading to dietswith lower calcium density.30 In addition, toddlers who consume more energy from table food consume less milkleading to lower calcium intakes.31


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s These observations, along with research reporting that milk intakes decrease as other beverages and table foodsare added to the diet, indicate that appropriate calcium and vitamin D intakes should receive continuedemphasis. The establishment of dietary practices ensuring adequate calcium intake is important in childhood.29

Adequate calcium intake during childhood and adolescence contributes to the attainment of peak bone mass, animportant factor in reducing the risk of skeletal disorders such as fractures and osteoporosis.29

Vitamin EVitamin E functions as an antioxidant and helps protect cells from free radical damage and is needed for normalcellular structure and function. The Feeding Infants and Toddlers Study reported that 58% of toddlers ages 12 to24 months had vitamin E intakes less than the estimated average requirement of 5 mg per day.13 Data from theUSDA Continuing Survey of Food Intakes by Individuals 1994-96, 1998 also indicate that vitamin E intakes forchildren ages 1 to 5 years are lower than recommended levels (Tables 7 and 8).15 Researchers with Feeding Infantsand Toddlers Study requested readers to interpret vitamin E findings with caution.13 Vitamin E intakerecommendations (DRI) for children over 1 year were extrapolated from adult values and may be imprecise.13 Inaddition, it is difficult to assess vitamin E added to foods through fats and cooking oils, and there is variability in reported vitamin E content of foods among food composition databases.13

OVER CONSUMPTION OF MICRONUTRIENTSNutrient intake data indicate that 1- to 2-year-old toddlers may have vitamin A and zinc intakes above the UL of600 mcg per day and 7 mg per day, respectively.13, 15 Average vitamin A intake by 1- to 2-year-old toddlers in theFeeding Infants and Toddlers study was 694 mcg per day with 35% of the toddlers having vitamin A intakes abovethe UL.13 The USDA Continuing Survey of Food Intakes by Individuals 1994-96, 1998 (CSFII) data indicate that 1- to2-year-olds consumed an average of 739 mcg per day and 3-year-olds consumed an average of 782 mcg per day.15

Devaney and colleagues pointed out that there is a narrow margin between the RDA for vitamin A and the UL.13

They concluded that there is a need to avoid unnecessary vitamin A supplementation, and there is also a need forbetter data to use for setting UL for young children.13 In the Feeding Infants and Toddlers study, 43% of thetoddlers had zinc intakes above the UL of 7 mg/day.13 Average zinc intakes of children ages 1 to 3 ranged from 6.9mg13 to 8.5 mg per day.15 Devaney and colleagues concluded that the UL for zinc needs further substantiationsince it was based on one study of full-term infants who received infant formula that provided about 4.5 mg zincper day.13 No adverse effects on copper status due to zinc intakes were documented in that study. Despite the lackof adverse effects, the study was used to determine the UL.

Intakes of niacin and magnesium by children 1 to 5 years of age may appear to be above the UL for thesenutrients.13,15 The UL for niacin, however, is specific to synthetic forms found in supplements and fortified foods.10

Food composition databases do not distinguish between naturally occurring niacin and synthetic forms added tofoods.13 Therefore, Devaney and colleagues could not determine the percentage of children who exceed the UL forsynthetic niacin.13 The UL for magnesium is specific to supplements and pharmacological agents and does notinclude magnesium in food or water.7


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s REFERENCES1. Skinner JD, Ziegler P, Pac S, et al. Meal and snack patterns of infants and toddlers. J Am Diet Assoc. 2004;104(suppl):

S65-S70.2. Carruth BR, Ziegler PJ, Gordon A, et al. Developmental milestones and self-feeding behaviors in infants and toddlers.

J Am Diet Assoc. 2004;104(suppl):S51-S56.3. Birch LL, McPhee L, Shoba BC, et al. What kind of exposure reduces children's food neophobia? Looking vs tasting.

Appetite. 1987;9:171-178.4. Carruth BR, Ziegler PJ, Gordon A, et al. Prevalence of picky eaters among infants and toddlers and their caregivers'

decisions about offering a new food. J Am Diet Assoc. 2004;104(suppl):S57-S64.5. Ong KK, Loos RJ. Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions.

Acta Paediatr. 2006;95:904-908.6. Institute of Medicine. Recommended Dietary Allowances. 10th Edition. Washington, D.C.: National Academy Press; 1989.7. Institute of Medicine. Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride.

Washington, D.C.: National Academy Press; 1997.8. Yates AA, Schlicker SA, Suitor CW. Dietary Reference Intakes: the new basis for recommendations for calcium and related

nutrients, B vitamins, and choline. J Am Diet Assoc. 1998;98:699-706.9. Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and

Amino Acids. Washington, D.C.: National Academy Press; 2002.10. Institute of Medicine. Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12,

Pantothenic Acid, Biotin, and Choline. Washington, D.C.: National Academy Press; 2000.11. Institute of Medicine. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids. Washington, D.C.:

National Academy Press; 2000.12. Institute of Medicine. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron,

Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. Washington, D.C.: National Academy Press; 2001.13. Devaney B, Ziegler P, Pac S, et al. Nutrient intakes of infants and toddlers. J Am Diet Assoc. 2004;104(suppl):S14-S21.14. Nicklas TA, Webber LS, Koschak M, et al. Nutrient adequacy of low fat intakes for children: the Bogalusa Heart Study.

Pediatrics. 1992;89:221-228.15. U.S. Department of Agriculture, Agricultural Research Service. Food and Nutrient Intakes by Children. 1994-96, 1998. 1999.

Available at: http:www.barc.usda.gov/bhnrc/foodsurvey/home.htm. Accessed March 1, 2004.16. Institute of Medicine. Dietary Reference Intakes Proposed Definition of Dietary Fiber. Washington, D.C.: National Academy

Press; 2001.17. Lozoff B, Jimenez E, Hagen J, et al. Poorer behavioral and developmental outcome more than 10 years after treatment for

iron deficiency in infancy. Pediatrics. 2000;105:E51.18. Moore C, Murphy MM, Keast DR, et al. Vitamin D intake in the United States. J Am Diet Assoc. 2004;104:980-983.19. Looker AC, Cogswell ME, Gunter EW. Iron Deficiency–United States, 1999-2002. MMWR. 2002;51:897-899.20. Iron Deficiency. In: Kleinman R, ed. Pediatric Nutrition Handbook. 5th ed: American Academy of Pediatrics. 2004:299-312.21. Skalicky A, Meyers AF, Adams WG, et al. Child Food Insecurity and Iron-Deficiency Anemia in Low-Income Infants and

Toddlers in the United States. Matern Child Health J. 2006;10:177-185.22. Schneider JM, Fujii ML, Lamp CL, et al. Anemia, iron deficiency, and iron deficiency anemia in 12-36-mo-old children from

low-income families. Am J Clin Nutr. 2005;82:1269-1275.23. Lozoff B, Klein NK, Nelson EC, et al. Behavior of infants with iron-deficiency anemia. Child Dev. 1998;69:24-36.24. Walter T, Kovalskys J, Stekel A. Effect of mild iron deficiency on infant mental development scores. J Pediatr. 1983;102:

519-522.25. Walter T, De Andraca I, Chadud P, et al. Iron deficiency anemia: adverse effects on infant psychomotor development.

Pediatrics. 1989;84:7-17.26. Fulgoni V III, Nicholls J, Reed A, et al. Dairy consumption and related nutrient intake in African-American adults and

children in the United States: continuing survey of food intakes by individuals 1994-1996, 1998, and the National Healthand Nutrition Examination Survey 1999-2000. J Am Diet Assoc. 2007;107:256-264.

27. Kalkwarf HJ, Khoury JC, Lanphear BP. Milk intake during childhood and adolescence, adult bone density, andosteoporotic fractures in US women. Am J Clin Nutr. 2003;77:257-265.

28. Kant AK. Reported consumption of low-nutrient-density foods by American children and adolescents: nutritional andhealth correlates, NHANES III, 1988 to 1994. Arch Pediatr Adolesc Med. 2003;157:789-796.

29. Greer FR, Krebs NF, Committee on Nutrition. Optimizing bone health and calcium intakes of infants, children, andadolescents. Pediatrics. 2006;117:578-585.

30. Skinner JD, Ziegler P, Ponza M. Transitions in infants' and toddlers' beverage patterns. J Am Diet Assoc. 2004;104:S45-S50.31. Briefel RR, Reidy K, Karwe V, et al. Toddlers' transition to table foods: Impact on nutrient intakes and food patterns.

J Am Diet Assoc. 2004;104(suppl):S38-S44.

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Contributor:

Rebecca Simmons, MDProfessor of Pediatrics

Center for Research on Reproduction and Women’s Health Children’s Hospital of Philadelphia

University of Pennsylvania Medical Center

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MATERNAL DIABETESStudies of the offspring of mothers with pregestational (type 1 or type 2) and/or gestational diabetes alsoindicate that an abnormal intrauterine environment results in long-term health consequences. Children andadults born to mothers with diabetes have increased obesity in adolescence,8 more often experience impairedglucose tolerance9,10 and impaired insulin secretion,11,12 and have increased prevalence of type 2 diabetes.8

GROWTHPatterns of growth in infancy and childhood may influence later health. Soto and colleagues evaluated infantswith gestational ages of 37 to 41 weeks. They reported that small for gestational age (SGA) babies whose weightscrossed percentile lines on a standard growth chart had significantly higher fasting insulin levels at 1 year of agethan appropriate for gestational age (AGA) or SGA babies who did not exhibit this weight pattern.13 SGA babieswhose lengths crossed percentile lines on standard growth charts had higher insulin secretion than AGA babiesor SGA babies who did not exhibit this length pattern.13 It is not known, however, whether these findings at 1 yearof age persist throughout life. Bavdekar and colleagues reported that 8-year-old children who were low-birth-weight infants but were heavy at age 8 had higher insulin concentrations, insulin resistance, and high levels oftotal and LDL cholesterol. In this study, the most adverse cardiovascular risk profiles were found for children whowere light at birth but who had grown relatively heavy and tall at age 8.14 Law and colleagues found that 22-year-old adults who had been small at birth but who gained weight rapidly between the ages of 1 and 5 years had thehighest adult blood pressures.15 Forsen et al. found that for both men and women, low birth weight followed byhigh growth rates after age 7 increased the risk of type 2 diabetes.16

Not all research supports the hypothesis that low birth weight and post-natal growth pattern contribute to laterhealth consequences. For example, Wilkin and colleagues concluded that insulin resistance at age 5 years is afunction of excess current weight rather than low birth weight or weight change.17

Rapid weight gain in which healthy infants gain beyond their expected growth channel has been linked toincreased risk of overweight later in life. Healthy infants who gained weight unusually rapidly during the first 4months of life were more likely to be overweight at 718 and 20 years of age,19 and rapid growth of healthy infantsduring the first 12 months of life has also been linked to increased body mass index at 6 years of age.20 Whilethese studies indicate that unusually rapid growth during infancy may increase risk of obesity later in life, thereare no known safe and effective interventions in early infancy for preventing childhood and adult obesity.19 Inaddition, more rapid growth may be an appropriate goal for infants with chronic illness and/or failure to thrive.

TODDLERSLittle data on the long-term health consequences of toddler food and nutrient intakes exist; therefore, this areadeserves further scrutiny. Moreover, the toddler years may be an opportune time to implement appropriate orspecific dietary interventions in children exposed to an abnormal intrauterine environment, or in those whoexperienced unusually rapid growth, in order to help influence future health. Unfortunately, however, no humanstudies have determined whether dietary interventions in these at-risk children are appropriate or effective.Clearly, more research is needed.

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In 1990, Barker proposed that “the womb may be more important than the home.”1 The period from conceptionto birth is a time of rapid growth, cellular replication and differentiation, and functional maturation of organsystems. These processes are very sensitive to alterations in the intrauterine milieu. Programming describes themechanisms whereby a stimulus or insult at a critical period of development has lasting or lifelong effects. It hasbeen recognized for nearly 70 years that the environment in which a child grows and develops could have long-term effects on subsequent health and survival. Multiple epidemiology studies have linked low birth weight tothe later development of a number of adult diseases, including hypertension, coronary artery disease, stroke,diabetes, kidney disease, and breast cancer. Although there are little data on the effects of toddler nutrition onlater health, the toddler years are characterized by continued physiological development. Experts now suggestthat this hypothesis be expanded to include evaluation of the early years of childhood.

THE INTRAUTERINE ENVIRONMENTAn abnormal intrauterine environment due to placental insufficiency or metabolic conditions of the mother, suchas diabetes mellitus, appears to increase the risk of obesity and type 2 diabetes in her offspring. Placentalinsufficiency results in decreased levels of energy, nutrients, hormones and growth factors supplied to the fetusvia the placenta, while diabetes mellitus results in increased levels. Experts hypothesize that both scenarioscause changes in gene expression, structure, and/or function of rapidly developing fetal cells with the alterationscontributing to health consequences in later childhood and adulthood.

BIRTH WEIGHTBirth weight may reflect conditions in the intrauterine environment. Placental insufficiency results in an infantwith growth retardation while maternal diabetes often results in a large for gestational age neonate. Low birthweight due to small for gestational status at birth (rather than appropriately sized preterm infants) is linked toincreased risk for developing obesity and type 2 diabetes.

The Dutch famine study reported by Ravelli and colleagues in 1976 suggested long-term implications of analtered intrauterine environment and resulting low birth weight.2 The Dutch famine occurred in the westernNetherlands from October 1944 until May 1945. During this time, daily food rations provided as little as 580kilocalories per day. Ravelli et al. reported on their evaluation of 94,800 19-year-old men who had been exposedto the famine in utero or early infancy. Infants who had been exposed to the famine in utero frequently had fetalgrowth retardation and abnormally low birth weight. At 19 years of age, men who had been exposed to thefamine in utero during the first 2 trimesters of pregnancy had significantly higher rates of obesity than men inthe eastern Netherlands who were not exposed to the famine. The researchers speculated that early nutritionaldeprivation affected the differentiation of hypothalamic centers that regulated food intake and growth.2 In laterstudies, lighter birth weight was linked to the development of type 2 diabetes in adult men3 and women,4 PimaIndian children,5 Taiwanese children,6 and both monozygotic and dizygotic twins.7

While lighter birth weight appears to increase the risk of obesity and type 2 diabetes, very high birth weightsmay also increase risk. A study of Pima Indians found that infants with lower birth weights (<2.5 kg) and thosewith high birth weights (>4.5 kg) had higher prevalence of diabetes at ages 10 to 14 and 15 to 19 years.5 Wei andcolleagues6 also reported a “U-shaped” relationship between birth weight and development of type 2 diabetesduring childhood. Infants in Taiwan with birth weights less than 2.5 kg or greater than 4.0 kg when delivered atterm were more likely to develop type 2 diabetes between 6 to 18 years of age than children with birth weightsbetween these values.

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REFERENCES1. Barker DJ. The fetal and infant origins of adult disease. BMJ. 1990;301:1111.2. Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med.

1976;295:349-353.3. Hales CN, Barker DJ, Clark PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;303:

1019-1022.4. Rich-Edwards JW, Colditz GA, Stampfer MJ, et al. Birthweight and the risk for type 2 diabetes mellitus in adult women.

Ann Intern Med. 1999;130:278-284.5. Dabelea D, Pettitt DJ, Hanson RL, et al. Birth weight, type 2 diabetes, and insulin resistance in Pima Indian children and

young adults. Diabetes Care. 1999;22:944-950.6. Wei JN, Sung FC, Li CY, et al. Low birth weight and high birth weight infants are both at an increased risk to have type 2

diabetes among schoolchildren in Taiwan. Diabetes Care. 2003;26:343-348.7. Poulsen P, Vaag AA, Kyvik KO, et al. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic

twin pairs. Diabetologia. 1997;40:439-446.8. Dabelea D, Knowler WC, Pettitt DJ. Effect of diabetes in pregnancy on offspring: follow-up research in the Pima Indians.

J Matern Fetal Med. 2000;9:83-88.9. Silverman BL, Metzger BE, Cho NH, et al. Impaired glucose tolerance in adolescent offspring of diabetic mothers.

Relationship to fetal hyperinsulinism. Diabetes Care. 1995;18:611-617.10. Plagemann A, Harder T, Kohlhoff R, et al. Glucose tolerance and insulin secretion in children of mothers with

pregestational IDDM or gestational diabetes. Diabetologia. 1997;40:1094-1100.11. Sobngwi E, Boudou P, Mauvais-Jarvis F, et al. Effect of a diabetic environment in utero on predisposition to type 2 diabetes.

Lancet. 2003;361:1861-1865.12. Gautier JF, Wilson C, Weyer C, et al. Low acute insulin secretory responses in adult offspring of people with early onset

type 2 diabetes. Diabetes. 2001;50:1828-1833.13. Soto N, Bazaes RA, Pena V, et al. Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-

age infants at age 1 year: results from a prospective cohort. J Clin Endocrinol Metab. 2003;88:3645-3650.14. Bavdekar A, Yajnik CS, Fall CH, et al. Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8 years,

or both? Diabetes. 1999;48:2422-2429.15. Law CM, Shiell AW, Newsome CA, et al. Fetal, infant, and childhood growth and adult blood pressure: a longitudinal study

from birth to 22 years of age. Circulation. 2002;105:1088-1092.16. Forsen T, Eriksson J, Tuomilehto J, et al. The fetal and childhood growth of persons who develop type 2 diabetes.

Ann Intern Med. 2000;133:176-182.17. Wilkin TJ, Metcalf BS, Murphy MJ, et al. The relative contributions of birth weight, weight change, and current weight to

insulin resistance in contemporary 5-year-olds: the EarlyBird Study. Diabetes. 2002;51:3468-3472.18. Stettler N, Zemel BS, Kumanyika S, et al. Infant weight gain and childhood overweight status in a multicenter, cohort

study. Pediatrics. 2002;109:194-199.19. Stettler N, Kumanyika SK, Katz SH, et al. Rapid weight gain during infancy and obesity in young adulthood in a cohort of

African Americans. Am J Clin Nutr. 2003;77:1374-1378.20. Gunnarsdottir I, Thorsdottir I. Relationship between growth and feeding in infancy and body mass index at the age of

6 years. Int J Obes Relat Metab Disord. 2003;27:1523-1527.

M E TA B O L I C P R O G R A M M I N G

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Contributor:

Barbara A. Dennison, MD Clinical Professor of Epidemiology

State University of New York at AlbanyDirector, Bureau of Health Risk Reduction

Division of Chronic Disease Prevention and Adult HealthNew York State Department of Health

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DEFINITIONS OF OVERWEIGHT Health experts recommend evaluating body mass index (BMI) as a screening tool to determine if children areoverweight or at risk of overweight.5 When there is a question or uncertainty whether the excess weight reflectsexcess body fat, additional assessment such as measurement of triceps skin-fold thickness may be indicated. BMIis expressed as body weight in kilograms divided by the square of height in meters (kg/m2). This is a weight forheight index that tends to reflect excess body fat and is relatively easy to use. The U.S. Department of Health andHuman Services Centers for Disease Control and Prevention (CDC) publishes sex-specific growth charts of BMI byage.6 The BMI percentiles indicated on the charts are derived from a nationally representative sample of children.Once BMI is calculated, it is plotted against age on the sex-specific charts and the BMI percentile-for-age isdetermined. Children with a BMI at or above the 85th but less than the 95th sex-specific percentile-for-age areconsidered to be at risk of overweight. Children with a BMI at or above the 95th sex-specific percentile-for-ageare considered “overweight.”

HEALTH RISKS ASSOCIATED WITH OVERWEIGHTIN CHILDHOOD Overweight in childhood warrants concern because it tends to persist over time and the greater the degree ofoverweight, the greater the risk and degree of overweight in adulthood.7 Moreover, overweight is associated withincreased health problems in childhood8 (Table 2) as well as increased morbidity9,10 and mortality in adulthood.11

Table 2. Health Problems Associated With Overweight in Childhood8

Cardiovascular Pulmonary• Hypercholesterolemia • Asthma• Dyslipidemia • Obstructive sleep apnea syndrome• Hypertension • Pickwickian syndrome

Endocrine Orthopedic• Hyperinsulinism • Genu verum• Insulin resistance • Slipped capital femoral epiphysis• Impaired glucose tolerance • Arthritis• Type 2 diabetes

Mental Health Gastrointestinal/hepatic• Depression • Nonalcoholic steatohepatitis• Low self-esteem • Gall bladder disease

ENERGY IMBALANCEEnergy imbalance contributes to overweight: children who consume more energy (calories) than needed for activities of daily life, physical activity plus growth, become overweight. Research indicates that overconsumption of calories by toddlers may be a bigger problem than previously realized.12,13 Devaney and colleaguesfound that reported energy intakes of toddlers ages 12 to 24 months exceeded estimated energy requirements by 31%.12 While over consumption is probably an important issue for toddlers, it is unlikely that the discrepancy


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INTRODUCTIONChanging environment and lifestyles have led to an imbalance in energy intake and expenditure resulting in anepidemic of overweight and obesity among adults, adolescents, and children, including toddlers. It is importantto understand characteristics and behaviors associated with the development of overweight in toddlers, sochildren at risk can be identified and steps taken to prevent or slow the progression of childhood overweight.

PREVALENCE OF OVERWEIGHT IN CHILDRENThe prevalence of overweight among children 2 to 19 years of age has tripled in the past three decades, increasingfrom 5.1% in 1971–1974 to 17.1% in 2003–2004. During this same period, the prevalence of those “at risk ofoverweight” has increased from 10.2% to 16.5%.1 For children ages 2 to 5 years the prevalence of overweight hasmore than doubled from 4.9% in 1971–1974 to 13.9% in 2003–2004.1,2 In addition to the increasing prevalence ofoverweight, the degree of overweight in childhood has increased. That is, overweight children have become evenmore overweight.2,3

Ogden and colleagues compared NHANES data from 2003–2004 with that from 1999–2000 and 2001–2002.1

The sample included almost 4,000 subjects between 2 and 19 years of age. The percentage of 2- to 19-year-oldswho was overweight increased from 13.9% and 15.4% in 1999–2000 and 2001–2002, respectively, to 17.1% in2003–2004. Among subjects aged 2 to 5 years the percentage that was overweight increased from 10.3% in1999–2000 to 13.9% in 2003–2004. Further results from this study are presented in Table 1.

Thompson and colleagues report that in the National Heart, Lung, and Blood Institute Growth and Health Study, the incidence of overweight in females was greater between the ages of 9 and 12 years than in lateradolescence.4 Furthermore, girls who were overweight in childhood were 11 to 30 times more likely to be obese in early adulthood. Overweight in this study was associated with both elevated blood pressure and unhealthyblood lipid profiles.

Table 1. Prevalence (%) of Risk of Overweight and Overweight*

All Male FemaleAge (years) 2–19 2–5 6–11 12–19 2–19 2–5 6–11 12–19 2–19 2–5 6–11 12–19At risk ofoverweight or overweight†

1999–2000 28.2 22.0 29.8 30.0 28.9 21.9 31.9 30.0 27.4 22.2 27.4 30.0

2001–2002 30.0 23.5 32.2 31.1 30.6 24.2 32.6 31.5 29.4 22.8 31.6 30.6

2003–2004 33.6 26.2 37.2 34.3 34.8 27.3 36.5 36.8 32.4 25.2 38.0 31.7

Overweight‡

1999–2000 13.9 10.3 15.1 14.8 14.0 9.5 15.7 14.8 13.8 11.2 14.3 14.82001–2002 15.4 10.6 16.3 16.7 16.4 10.7 17.5 17.6 14.4 10.5 14.9 15.72003–2004 17.1 13.9 18.8 17.4 18.2 15.1 19.9 18.3 16.0 12.6 17.6 16.4

*Adapted from 21.†BMI for age at 85th percentile or higher.‡BMI for age at 95th percentile or higher.

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between calorie intakes and estimated energy requirements are actually this high since the prevalence ofoverweight would be even higher than reported.12 The authors speculate that the discrepancy may have beencaused, in part, by parents over-estimating the amount of food actually consumed by the child. Alternately, theestimated energy requirements might be underestimated secondary to parents underestimating the child’sweight. For example, parents might have reported the child’s weight at the most recent checkup instead of thechild’s current weight. Nevertheless, these researchers stated that the high energy intakes relative to estimatedrequirements “reinforce the importance of encouraging health professionals to monitor the weight gain ofinfants and toddlers….”12

Several food consumption trends could contribute to over consumption of calories and to overweight: increasingportion sizes, frequent use of fast foods, consumption of sweet beverages, and decreased consumption ofvegetables, to name a few. Typical food portion sizes have increased dramatically over the past 20 years14 andlarger portion sizes promote increased food consumption by children.15,16 Bowman and colleagues reported thaton a typical day, about 30% of children 4 to 19 years of age consumed food from a fast food restaurant.17 Childrenwho consumed fast foods ate almost 200 calories more per day than children who did not consume fast foodsand their diets were of poorer quality. Children who consumed fast foods also consumed higher amounts ofsugar-sweetened beverages, less milk, and fewer fruits andvegetables.17

Intake of sweet beverages has been linked to weight gain andoverweight in children.18 Ludwig and colleagues reported thatfor each additional serving of a sweetened beverageconsumed by 6th- and 7th-grade children, BMI increased by0.24 kg/m2 and the incidence of obesity increased by about60% (odds ratio 1.6).18 Dennison and colleagues evaluatedtoddlers ages 2 through 5 years and reported that childrenwho consumed more than 12 ounces per day of fruit juice weremore likely to have BMI above the 75th and the 90thpercentiles than children who consumed less than 12 ouncesper day.19 Since then, other research has also noted anassociation between higher fruit juice intakes among childrenand being overweight.20 One study, however, noted a trend but did not find a statistically significant difference.21

In response to the totality of findings, the American Academy of Pediatrics (AAP) Committee on Nutritionrecommends that fruit juice consumption by children 1 to 6 years old be limited to no more than 4 to 6 ouncesper day.22

Sweet beverages may be particularly problematic when it comes to weight control because they providesignificant calories, and people do not compensate for calories consumed from liquid foods as well as theycompensate for calories from solid foods.23 Sweet beverages, including 100% juice, fruit drinks and carbonatedbeverages, may also potentially contribute to overweight by displacing milk in toddlers’ diets, an excellent sourceof dietary calcium.24 Although more studies are needed,25 research indicates that there is a significant negativerelationship between children’s average calcium intake over several years and their body fat at 6 years26 and 8years of age.24 Skinner et al. suggested that children could potentially reduce their body fat by about 0.4% byincreasing their calcium intake with one 8-ounce glass of skim milk or 8 ounces of yogurt per day (about 300 mgcalcium in each).24


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Regular physical activity promotes maintenance of a healthy weight, while physical inactivity has been linked toincreased body fat40 and increased BMI51 in toddlers. The Institute of Medicine23 recommends that childrenparticipate in at least 1 hour of moderately vigorous physical activity per day, while the American Alliance ofHealth, Physical Education, Recreation, and Dance32 recommends that preschool-age children participate in atleast 60 minutes of structured physical activity and at least 60 minutes of unstructured physical activity daily.Furthermore, they recommend that preschoolers should not be sedentary for more than 60 minutes at a timeexcept when sleeping.

FAMILY AND ENVIRONMENTCharacteristics of the child’s family and environment may be important predictors of overweight. A child with an obese parent has a significantly higher risk of being overweight than a child whose parents are not obese.33

Having a mother who is obese appears to be a stronger predictor of childhood overweight than having a fatherwho is obese (odds ratio 2.8–3.6 vs 2.4–2.9, respectively).33 Strauss and Knight reported that children whosemothers were obese had more than three times the risk of overweight than children whose mothers were notobese.34 Parental obesity is a more powerful predictor of a child’s risk of being obese as a young adult amongyounger children (1 to 5 years of age) than older children (6 to 17 years of age), while the risk associated with the child’s overweight status increases with increasing child age.33 Among children, aged 1 to 5 years, those with two obese parents are 13.6–15.3 times more likely to be obese as a young adult compared to those with no obese parents. Among 6- to 17-year-old children, those with two obese parents compared with those with no obese parents, are 2.0–5.6 times as likely to be obese as a young adult. For children of all ages, those with one obese parent compared with those with no obese parents, have an increased odds of 2.2–3.2 of being obeseas a young adult.33 Children who live with a single parent, whose mothers have less than a high school education,whose parents do not work, and whose families have low incomes are at greater risk of being overweight.34 Inaddition, after adjustment for these factors, children who received the least amount of cognitive stimulation athome were twice as likely to become overweight as children who received the highest amount of cognitivestimulation at home.34

Television viewing appears to be an important predictor of overweight status among children as well as adults. Andersen and colleagues found that children (ages 8 to 16 years) who watched 4 or more hours per day of television had significantly greater body fat and a higher BMI than children who watched less than 2 hours.35 Television viewing also increases the risk of being overweight for toddlers.36 Dennison and colleaguesfound that 40% of toddlers (ages 1 to 5 years) had a television in their bedroom, and those with a television intheir bedroom were significantly more likely to be overweight or at a risk of overweight (have a BMI above the85th percentile) than toddlers without a television in the bedroom (odds ratio 1.31).36


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The AAP CON has stated,

“Early recognition of excessiveweight gain relative to lineargrowth should become routine inpediatric ambulatory care settings.BMI…should be calculated andplotted periodically.”18

WHAT TO DO?One of the first steps in preventing childhood overweight is early recognition of the child at increased risk of becoming overweight. Only about one-fifth of parents recognize when their own child is overweight.49

Unfortunately, many pediatric health practitioners often fail to identify children who are overweight or atrisk of overweight because they do not determine BMI or assess BMI percentile for age. The AAP Committee onNutrition recommends that physicians/pediatric care providers calculate and plot BMI by age once a year in allchildren and adolescents, and that they use the BMI percentile-for-age as well as change in BMI percentile, todetermine if the weight gain is excessive relative to linear growth.8 BMI charts and online training modules onusage are available at www.cdc.gov/growthcharts/. Other recommendations related to preventing overweightin children are summarized in Table 3.

Table 3. Physician Measures to Help Prevent Overweight in Children8,13,42,47

• Identify and track patients at increased risk due to family, socioeconomic, ethnic, cultural and/orenvironmental factors

• Promote healthy eating patterns; The USDA Food Guide Pyramid for Young Children is a useful tool

• Calculate and plot BMI-for-age yearly • Promote physical activity; The Institute of Medicine recommends 1 hour of physical activity per

day for children

• Identify excessive weight gain relative to linear growth using change in BMI percentile-for-age• Recommend limiting television and video viewing to no more than 1 to 2 hours per day for children

older than 2 years of age, and discourage any television viewing for children less than 2 years of age

• Promote breastfeeding of infants and advocate for paid maternity leave supportive worksitepolicies/practices

• Recognize and monitor obesity-associated disorders/diseases

If BMI percentile-for-age indicates that a child is at risk of overweight or is overweight, discussion with the familyand weight goals become important. For toddlers with BMI measurements between the 85th and 94thpercentiles, or BMI measurements greater than the 95th percentile and no secondary complications, expertsrecommend that maintaining baseline body weight is the primary weight goal.5 As children maintain theirweight while growing in height, BMI will decrease.5 Improving dietary and physical activity patterns will helpachieve these goals. Toddlers who are overweight (BMI greater than the 95th percentile) and experiencingsecondary complications may be better served by referral to health care professionals specializing in pediatricweight control.

The American Heart Association (AHA) policy on dietary recommendations for children and adolescents has beenendorsed by the AAP.48 Recommendations are food based, not nutrient based. Thus, the recommended number ofservings for grains, fruits, vegetables, milk/dairy, and lean meats/beans are given for children between the ages of


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Television viewing may affect weight by influencing eating behaviors, food choices, and activity patterns.Unpublished data from Dennison and colleagues indicate that over 50% of children who watch television in theirbedrooms always or usually snack while watching television.37 Viewing television during meals is associated withhigher intakes of meat, pizza, salty snacks, and soda and lower intakes of fruits, vegetables, and juice.38 Foodsmost frequently advertised to young children tend to be relatively high in calories, and a study finds that childrenexposed to a television commercial twice in a 30-minute cartoon were 3 times more likely to request theadvertised item.39 The amount of time children watch television is also positively related to how frequently theyrequest advertised food items, and the more often they requested these items, the more likely their parents wereto purchase them.40 The relationship between television viewing and physical activity in toddlers is less clear. Onestudy of preschool children, however, found a weak, negative association with physical activity levels.41 Due to therelationship between television viewing and adverse health effects, such as aggressive behavior and overweightin children, the AAP Committee on Public Education recommends that children over 2 years of age limit theirviewing to no more than 1 to 2 hours per day of non-violent, educational television or other media.42

INFANT NUTRITION AND GROWTH PATTERNInfant nutrition appears to have an important potential impact on weight status. Several research studiesindicate that breastfed infants are less likely than infants fed formula to become overweight as children oradults.43-45 Studies also found that the longer the duration of breastfeeding and the greater the period ofexclusive breastfeeding (feeding no other foods or beverages), the lower the subsequent risk of beingoverweight.45 Since the decision to breastfeed, the duration of breastfeeding, and the period of exclusivebreastfeeding are not random occurrences and cannot be randomized in research studies, it is difficult to know exactly what is responsible for the observed differences between breastfed and formula-fed infants.The decreased risk of overweight might be due to decreased caloric intake secondary to mode of feeding(breastfeeding vs formula feeding), the number of people feeding the infant (one vs many), biological orphysiological factors in human milk, differences in characteristics of mothers who breastfeed compared withthose who formula feed, and/or differences in maternal feeding and parenting practices. Mothers who breastfeedand mothers who do not often differ with respect to educational attainment, race/ethnicity, personal nutritionpractices, and/or other lifestyle behaviors that may lead to biased estimates of the beneficial effects associatedwith breastfeeding.

Rapid weight gain, in which healthy infants gain beyond their expected growth channel, has been linked toincreased risk of overweight later in life. Healthy infants who gained weight unusually rapidly during the first 4months of life were more likely to be overweight at 7 years18 or 20 years of age,19 and rapid growth of healthyinfants during the first 12 months of life has also been linked to increased body mass index at 6 years of age.20

While these studies indicate that unusually rapid growth during infancy may increase risk of obesity later in life,there are no known safe and effective interventions in early infancy for preventing childhood and adult obesity.19

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1 and 18 years by gender. In addition, the statement provides guidelines for improving the nutritional quality ofthe diet after weaning, tips for parents to improve nutrition in young children, and strategies for schools topromote health and nutrition.

The North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition suggests severalapproaches to treating overweight including behavioral reinforcement, dietary modification, strategies toincrease physical activity, therapeutic approaches, and parenting skills to support weight control efforts.49

In 2006 the American Dietetic Association released their position on pediatric overweight following an extensiveliterature review.50 They found:

“…that pediatric overweight intervention requires a combination of family-based and school-based multicomponent programs that include the promotion of physical activity, parenttraining/modeling, behavioral counseling, and nutrition education. Furthermore…community-based and environmental interventions are recommended as among the most feasible ways to support healthful lifestyles for the greatest numbers of children and their families.”

REFERENCES1. Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA.

2006;295:1549-1555.2. Jolliffe D. Extent of overweight among US children and adolescents from 1971 to 2000. Int J Obes Relat Metab Disord.

2004;28:4-9.3. Edmunds LS, Woelfel ML, Dennison BA, et al. Overweight trends among children enrolled in the New York State special

supplemental nutrition program for women, infants, and children. J Am Diet Assoc. 2006;106:113-117.4. Thompson DR, Obarzanek E, Franko DL, et al. Childhood Overweight and Cardiovascular Disease Risk Factors: The National

Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr. 2007;150:18-25.5. Barlow SE, Dietz WH. Obesity evaluation and treatment: Expert Committee recommendations. The Maternal and Child

Health Bureau, Health Resources and Services Administration and the Department of Health and Human Services.Pediatrics. 1998;102:E29.

6. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for HealthStatistics. CDC Growth Charts. 2000. Available at: http:www.cdc.gov/growthcharts. Accessed June 2, 2004.

7. Serdula MK, Ivery D, Coates RJ, et al. Do obese children become obese adults? A review of the literature. Prev Med.1993;22:167-177.

8. American Academy of Pediatrics Committee on Nutrition. Prevention of pediatric overweight and obesity. Pediatrics.2003;112:424-430.

9. Must A, Strauss RS. Risks and consequences of childhood and adolescent obesity. Int J Obes Relat Metab Disord.1999;23(suppl 2):S2-S11.

10. Must A, Jacques PF, Dallal GE, et al. Long-term morbidity and mortality of overweight adolescents. A follow-up of theHarvard Growth Study of 1922 to 1935. N Engl J Med. 1992;327:1350-1355.

11. Gunnell DJ, Frankel SJ, Nanchahal K, et al. Childhood obesity and adult cardiovascular mortality: a 57-y follow-up studybased on the Boyd Orr cohort. Am J Clin Nutr. 1998;67:1111-1118.

12. Devaney B, Ziegler P, Pac S, et al. Nutrient intakes of infants and toddlers. J Am Diet Assoc. 2004;104(suppl):S14-S21.13. Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and

Amino Acids. Washington, D.C.: National Academy Press. 2002.14. Young LR, Nestle M. Expanding portion sizes in the US marketplace: implications for nutrition counseling. J Am Diet Assoc.

2003;103:231-234.15. Rolls BJ, Engell D, Birch LL. Serving portion size influences 5-year-old but not 3-year-old children's food intakes. J Am Diet

Assoc. 2000;100:232-234.16. Orlet FJ, Rolls BJ, Birch LL. Children's bite size and intake of an entree are greater with large portions than with age-

appropriate or self-selected portions. Am J Clin Nutr. 2003;77:1164-1170.17. Bowman SA, Gortmaker SL, Ebbeling CB, et al. Effects of fast-food consumption on energy intake and diet quality among

children in a national household survey. Pediatrics. 2004;113:112-118.18. Ludwig DS, Peterson KE, Gortmaker SL. Relation between consumption of sugar-sweetened drinks and childhood obesity:

a prospective, observational analysis. Lancet. 2001;357:505-508.


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k 19. Dennison BA, Rockwell HL, Baker SL. Excess fruit juice consumption by preschool-aged children is associated with shortstature and obesity. Pediatrics. 1997;99:15-22.

20. Tanasescu M, Ferris AM, Himmelgreen DA, et al. Biobehavioral factors are associated with obesity in Puerto Rican children.J Nutr. 2000;130:1734-1742.

21. Skinner JD, Carruth BR, Moran J, Iii, et al. Fruit juice intake is not related to children's growth. Pediatrics. 1999;103:58-64.22. American Academy of Pediatrics Committee on Nutrition. The use and misuse of fruit juice in pediatrics. Pediatrics.

2001;107:1210-1213.23. Mattes RD. Dietary compensation by humans for supplemental energy provided as ethanol or carbohydrate in fluids.

Physiol Behav. 1996;59:179-187.24. Skinner JD, Bounds W, Carruth BR, et al. Longitudinal calcium intake is negatively related to children's body fat indexes.

J Am Diet Assoc. 2003;103:1626-1631.25. Weaver CM, Boushey CJ. Milk–good for bones, good for reducing childhood obesity? J Am Diet Assoc. 2003;103:1598-1599.26. Carruth BR, Skinner JD. The role of dietary calcium and other nutrients in moderating body fat in preschool children.

Int J Obes Relat Metab Disord. 2001;25:559-566.27. McCrory MA, Fuss PJ, McCallum JE, et al. Dietary variety within food groups: association with energy intake and body

fatness in men and women. Am J Clin Nutr. 1999;69:440-447.28. Fox MK, Pac S, Devaney B, et al. Feeding infants and toddlers study: What foods are infants and toddlers eating?

J Am Diet Assoc. 2004;104(suppl):S22-S30.29. Nicklas T, Johnson R. Position of the American Dietetic Association: Dietary guidance for healthy children ages 2 to 11

years. J Am Diet Assoc. 2004;104:660-677.30. Li R, O'Connor L, Buckley D, et al. Relation of activity levels to body fat in infants 6 to 12 months of age. J Pediatr.

1995;126:353-357.31. Klesges RC, Klesges LM, Eck LH, et al. A longitudinal analysis of accelerated weight gain in preschool children. Pediatrics.

1995;95:126-130.32. National Association for Sport and Physical Education. Active Start: A Statement of Physical Activity Guidelines for Children

Birth to Five Years. Reston, VA: American Alliance for Health, Physical Education, Recreation and Dance; 2002.33. Whitaker RC, Wright JA, Pepe MS, et al. Predicting obesity in young adulthood from childhood and parental obesity.

N Engl J Med. 1997;337:869-873.34. Strauss RS, Knight J. Influence of the home environment on the development of obesity in children. Pediatrics.

1999;103:e85.35. Andersen RE, Crespo CJ, Bartlett SJ, et al. Relationship of physical activity and television watching with body weight and

level of fatness among children: results from the Third National Health and Nutrition Examination Survey. JAMA.1998;279:938-942.

36. Dennison BA, Erb TA, Jenkins PL. Television viewing and television in bedroom associated with overweight risk among low-income preschool children. Pediatrics. 2002;109:1028-1035.

37. Fitzpatrick E, Edmunds LS, Dennison BA. Positive effects of family dinner are undone by television viewing. J Am DietAssoc. 2007;107:666-671.

38. Coon KA, Goldberg J, Rogers BL, et al. Relationships between use of television during meals and children's foodconsumption patterns. Pediatrics. 2001;107:E7.

39. Borzekowski DL, Robinson TN. The 30-second effect: an experiment revealing the impact of television commercials onfood preferences of preschoolers. J Am Diet Assoc. 2001;101:42-46.

40. Taras HL, Sallis JF, Patterson TL, et al. Television's influence on children's diet and physical activity. J Dev Behav Pediatr.1989;10:176-180.

41. Durant RH, Baranowski T, Johnson M, et al. The relationship among television watching, physical activity, and bodycomposition of young children. Pediatrics. 1994;94:449-455.

42. American Academy of Pediatrics Committee on Public Education. Children, adolescents, and television. Pediatrics.2001;107:423-426.

43. von Kries R, Koletzko B, Sauerwald T, et al. Breastfeeding and obesity: cross sectional study. BMJ. 1999;319:147-150.44. Hediger ML, Overpeck MD, Kuczmarski RJ, et al. Association between infant breastfeeding and overweight in young

children. JAMA. 2001;285:2453-2460.45. Dewey KG. Is breastfeeding protective against child obesity? J Hum Lact. 2003;19:9-18.46. Baughcum AE, Chamberlin LA, Deeks CM, et al. Maternal perceptions of overweight preschool children. Pediatrics.

2000;106:1380-1386.47. U.S. Department of Agriculture, Center for Nutrition Policy and Promotion. The Food Guide Pyramid for Young Children.

2003. Available at: http:www.usda.gov/cnpp/KidsPyra/. Accessed June 2, 2004.48. American Heart Association, Gidding SS, Dennison BA, et al. Dietary recommendations for children and adolescents: a

guide for practitioners. Pediatrics. 2006;117:544-559.49. Baker S, Barlow S, Cochran W, et al. Overweight children and adolescents: a clinical report of the North American Society

for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr. 2005;40:533-543.50. American Dietetic Association. Position of the American Dietetic Association: individual-, family-, school-, and community-

based interventions for pediatric overweight. J Am Diet Assoc. 2006;106:925-945.

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DHA in Toddler Nutrition

Contributor:

Sheila M. Innis, PhD, MScProfessor, Department of Pediatrics

Director, Nutrition Research ProgramBC Research Institute for Children’s and Women’s Health

University of British Columbia

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PHYSIOLOGICAL ROLES FOR DHAThe high concentration of DHA in membrane phospholipids (such as phosphatidylserine and phosphatidyl-ethanolamine) of the brain gray matter, retina, and heart indicates that this fatty acid is vital to the developmentand function of these tissues. Reduced amounts of DHA in nerve cell membranes and in the visual elements ofthe retina are associated with decreased scores on tests of learning, photoreceptor cell function, and visualresolution acuity.10 DHA is also a precursor for 17S-hydroxy-containing docosanoids (docosatrienes and 17S-seriesresolvins) that appear to be important mediators of inflammation and link DHA to immunological function.16

In addition, n-3 fatty acids have been shown to be involved in regulation of gene expression in the brain andother organs.17,18

DHA AND THE GROWING BRAINStudies of autopsy material from human infants have provided evidence that the dietary intake of DHAinfluences the amount of DHA accumulated in the developing infant brain.19 Large amounts of DHA are neededduring brain growth and development to support the synthesis of new membrane lipids. Although the rate ofDHA accretion relative to body weight is highest during the third trimester of pregnancy and first few monthsafter birth,20 human brain growth and remodeling continue well beyond this time. DHA is particularly enriched in synaptic membranes, where it is involved in neurotransmitter metabolism and receptor function.10 Only about1% of the adult number of synapses are present in the human brain at birth, and considerable growth andreorganization of synapses occurs through early childhood.21

The concept of critical periods in development at which the fetus or young child is susceptible to long-lastingeffects of early nutritional deficiencies or other environmental stressors is well established. The effects of earlyiron deficiency, iodine deficiency, and alcohol exposure all provide excellent examples of the long-lasting effectsof early nutrient deficiency or exposure to toxic compounds. One of the effects of reduced DHA in the brain isaltered metabolism of the neurotransmitters dopamine and serotonin.10 A working model, similar to thatdeveloped to explain the effects of iron deficiency on cognitive and behavioral development in infants,22 can be proposed to explain how poor dietary fat choices may adversely affect infant and child development.

Figure 2. Proposed Model to Explain How Poor Dietary Fat Choices May Affect Infantand Child Development


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INTRODUCTIONThe study of the roles of docosahexaenoic acid (DHA; 22:6n-3; a 22-carbon, 6-double bond, n-3 fatty acid) inhuman development, neurologic and visual function, and in reducing the incidence and severity of a variety ofdiseases is a rapidly moving field of research. Dietary DHA has been associated with improvements in visual andcognitive function through epidemiological studies with breastfed1,2 and, in some randomized, controlled studies,formula-fed infants.3-5 In adults, the role of n-3 fatty acids, including DHA, in promoting cardiovascular health, isbecoming increasingly recognized, and is receiving more public emphasis.6-8 The importance of dietary n-3 fattyacids for infant brain and retinal development and in adult health highlights the need to also consider DHAstatus and n-3 fatty acid nutrition in children, particularly those between the ages of 1 and 5 years, at which timeconsiderable brain development is continuing.9

SOURCES OF DHAHumans can make DHA from the essential dietary fatty acid, α-linolenic acid (18:3n-3, LNA),10 which is an 18-carbon polyunsaturated fatty acid with 3 double bonds found in some vegetable oils (like canola, soybean, andflax), nuts, and seeds (such as walnuts). Synthesis of DHA from LNA occurs largely in the liver through a series of desaturation, elongation, and oxidation reactions that convert LNA via eicosapentaenoic acid (20:5n-3, EPA) to DHA (Figure 1).11 Despite the ability to convert LNA to DHA, the activity of the desaturase pathway in humansappears to be low and variable. Estimates derived from studies with stable isotope tracers indicate that theamount of LNA converted to DHA varies from <1% to about 9%; the conversion is higher in less mature infantsthan in older infants, and in pregnant women compared to non-pregnant women.12-15 In addition to LNA, DHA isalso consumed in the diet. However, because the desaturase enzymes required for conversion of LNA to DHA arepresent only in animal cells, DHA is present in the diet only in animal foods (fish, meats, and eggs) and is notfound in foods of vegetable origin (except certain formulated foods and dietary supplements that containsupplemented DHA). In addition, cow and other animal milks and dairy products contain very low amounts ofDHA. Soy and other milk substitutes based on vegetable products are also devoid of DHA. Both human milk andLCPUFA-supplemented infant formula provide DHA.

Figure 1. Essential Fatty Acid Metabolism

38 D H A I N TO D D L E R N U T R I T I O N

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DHA STATUS OF TODDLERSIn addition to low intakes of DHA during the toddler years, the DHA status of children ages 18 to 60 months islower than in newborns or breastfed infants or in children of older ages (Figure 3). Innis and colleagues evaluatedthe red blood cell phosphatidylethanolamine (RBC-PE) DHA concentrations of 84 toddlers 18 to 60 months of age(Figure 3). The DHA status of the 18- to 60-month-old children was comparable to that of 3-month-old infants fedformula without DHA. Other investigators have reported lower visual resolution acuity and scores on tests ofmental development in infants fed formulas without DHA and with comparable blood levels of DHA to thoseInnis et al. found in 18- to 60-month-old children.3-5

Figure 3. Fatty Acids (%) From DHA in RBC-PE

One factor that may influence the DHA status of toddlers is the intake of the n-6 fatty acid, linoleic acid. Linoleicacid (LA, 18:2n-6) is an 18-carbon, 2-double bond, n-6 fatty acid and is an essential dietary fatty acid. LA ismetabolized through desaturation and elongation reactions to arachidonic acid (ARA) and is believed to use thesame enzymes as those required to convert LNA to DHA (Figure 1). Dietary sources of linoleic acid are vegetableoils (especially corn, soybean, and safflower oil). It has been suggested that the intakes of linoleic acid in Westerncountries are too high. Further, research in animals has shown that increasing dietary intakes of LA at constantintakes of LNA decreases DHA in tissues.29 Analysis of the dietary intakes of toddlers and young children instudies by Innis revealed an inverse relation between the dietary intake of LA and DHA status, which could not beexplained by differences in the intake of either LNA or DHA. Children in the lowest tertile of RBC-PE DHA had thehighest intakes of linoleic acid, and a significant inverse linear trend was present between the intake of LA andDHA status.27


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INDICATORS OF DHA STATUSClinical signs of inadequate levels of DHA will clearly reflect the functional roles of DHA in the central nervoussystem. These include altered performance on a variety of tests of learning and changes in electroretinograph(ERG) recordings and measures of visual resolution acuity.10 Of importance, there are no overt signs of n-3 fattyacid deficiency, such as growth failure or skin lesions. Measures of the amount of DHA in red blood cellphospholipids or plasma lipids reflect the dietary intake of DHA in infants, as they do in adults.23-26 Biochemicalmarkers of DHA status, or the blood level of DHA at which functional impairment of the central nervous system,heart, or other organs requiring n-3 fatty acids occurs, have not been identified.

DHA INTAKES OF TODDLERSBreastfed infants and infants fed formulas with DHA receive a source of n-3 fatty acids. However, weaning tocow’s milk and the replacement of energy from breast milk and infant formula with cereals, fruits, andvegetables (which are low in fat and have no DHA) will result in a decrease in the amount of n-3 fatty acidsconsumed. Infants between the ages of 1 and 6 months who consume breast milk or formula with 0.3% of thefatty acids as DHA, and 3.7 g fat/dL will receive 86 mg DHA with an intake of 780 mL breast milk or formula perday. Innis and colleagues have estimated the intakes of n-3 fatty acids, as well as that for n-6 linoleic acid andtrans fatty acids among toddlers and young children 18 to 60months of age (Table 1). In toddlers and children 18 to 60months of age, the intake of LNA is about 1.7 g/day and theintake of DHA is about 88 mg/day, with the lowest intake ofabout 40 mg DHA/day occurring at 18 to 24 months of age.27

The richest dietary source of DHA is fatty fish, which is notwidely or consistently consumed by many young children. It isalso important to note that the intake of LNA among manytoddlers is also often low, since at this age many children donot consume significant amounts of LNA frompolyunsaturated oils in salad dressings and unesterifiedmargarines. In addition, the U.S. Environmental ProtectionAgency and Food and Drug Administration haverecommended limits on fish consumption for young childrendue to concerns about potential negative effects of methylmercury, which is a developmental neurotoxin and for whichthe major source of human exposure is fish28. Such concernsover the safety of fish could potentially lower DHA intakes.

Table 1. Linoleic Acid, α-Linolenic Acid, DHA, and Trans Fatty Acid Intakes of Young Children Ages 18 to 60 Months in Canada

All Children 18 to 24 months 24 to 36 months 37 to 60 monthsTotal Fat (% Calories) 32.7±0.6 32±1.8 34.6±1.5 32.4±0.8linoleic acid, g 8.8±0.4 5.8±0.6 9±0.6 9.4±0.6a-linolenic acid, g 1.7±0.12 1.16±0.16 2.02±0.23 1.72±0.17DHA, mg 88±10 41±10 95±16 96±14trans fatty acids, g 4.8±3.1 3.5±1.9 5.3±3.9 5±3.0Values are means ± standard error, adapted from Innis.27


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“If one accepts that formulafeeding without DHA confers a DHAstatus which puts that infant at riskfor lower visual acuity and lowerscores on behavioral tests, then theDHA status of children 18 to 60months could also place toddlers at risk.”“The DHA status of toddlers iscomparable to that of infants fedformula without DHA.”


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Table 2. DHA Status Is Inversely Related to Linoleic Acid Intake in Children 18 to 60 Months

Tertile of RBC-PE DHA1 2 3 4

Median, g DHA/100 g RBC-PE fatty acids 1.8 3.2 4.5 5.9

Diet % kcal from fat 32 33 32 33

Linoleic acid, g 9±0.7 9±0.7 7.5±0.7 6.7±1.0

Linolenic acid, g 1.7±0.2 1.8±0.2 1.3±0.13 1.5±0.2

DHA, mg 91±20 70±12 99±24 92±41

Values are means ± standard error, adapted from Innis.27

The dietary intake data also showed that the intakes of trans fatty acids in toddlers were greater than the intakesof LNA and also inversely related to DHA status (Table 1). Some investigators have hypothesized that trans fattyacids may adversely affect n-3 fatty acid metabolism, infant development, and learning behavior.30,31 The LA andtrans fatty acid intakes of toddlers deserve further evaluation.

SUMMARYRapid brain growth and development continues in the toddleryears, and DHA is an important component of lipids in the brainthat could potentially affect early cognitive and behavioraldevelopment. Research indicates that the DHA status and DHAintakes of toddlers are lower than those of infants and children ofolder ages. The importance of adequate n-3 fatty acid nutritionand the low DHA status of toddlers indicate that n-3 fatty acidnutrition of children ages 1 to 5 years deserves further scrutiny.

REFERENCES1. Innis SM, Gilley J, Werker J. Are human milk long-chain polyunsaturated fatty acids related to visual and neural

development in breastfed term infants? J Pediatr. 2001;139:532-538.2. Jorgensen MH, Hernell O, Hughes E, et al. Is there a relation between docosahexaenoic acid concentration in mothers’

milk and visual development in term infants? J Pediatr Gastroenterol Nutr. 2001;32:293-296.3. Birch EE, Hoffman DR, Uauy R, et al. Visual acuity and the essentiality of docosahexaenoic acid and arachidonic acid in the

diet of term infants. Pediatr Res. 1998;44:201-209.4. Birch EE, Hoffman DR, Castañeda YS, et al. A randomized controlled trial of long-chain polyunsaturated fatty acid

supplementation of formula in term infants after weaning at 6 wk of age. Am J Clin Nutr. 2002;75:570-580.5. Hoffman DR, Birch EE, Castañeda YS, et al. Visual function in breastfed term infants weaned to formula with or without

long-chain polyunsaturates at 4 to 6 months: a randomized clinical trial. J Pediatr. 2003;142:669-677.6. Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and

Amino Acids. Washington, D.C.: National Academy Press. 2002.7. Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease.

Circulation. 2002;106:2747-2757.8. Simopoulos AP, Leaf A, Salem N, Jr. Workshop on the essentiality of and recommended dietary Intakes for omega-6 and

omega-3 fatty acids. J Am Coll Nutr. 1999;18:487-489.9. Rice D, Barone S, Jr. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal

models. Environ Health Perspect. 2000;108(suppl 3):511-533.


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n 10. Innis SM. Perinatal biochemistry and physiology of long-chain polyunsaturated fatty acids. J Pediatr. 2003;143(suppl):S1-S8.11. Sprecher H. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta. 2000;1486:219-231.12. Burdge GC, Wootton SA. Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic

acids in young women. Br J Nutr. 2002;88:411-420.13. Burdge GC, Wootton SA. Conversion of alpha-linolenic acid to palmitic, palmitoleic, stearic and oleic acids in men and

women. Prostaglandins Leukot Essent Fatty Acids. 2003;69:283-290.14. Uauy R, Mena P, Wegher B, et al. Long chain polyunsaturated fatty acid formation in neonates: effect of gestational age

and intrauterine growth. Pediatr Res. 2000;47:127-135.15. Pawlosky RJ, Hibbeln JR, Novotny JA, et al. Physiological compartmental analysis of alpha-linolenic acid metabolism in

adult humans. J Lipid Res. 2001;42:1257-1265.16. Hong S, Gronert K, Devchand PR, et al. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in

murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem. 2003;278:14677-14687.17. Kitajka K, Puskas LG, Zvara A, et al. The role of n-3 polyunsaturated fatty acids in brain: modulation of rat brain gene

expression by dietary n-3 fatty acids. Proc Natl Acad Sci USA. 2002;99:2619-2624.18. Price PT, Nelson CM, Clarke SD. Omega-3 polyunsaturated fatty acid regulation of gene expression. Curr Opin Lipidol.

2000;11:3-7.19. Makrides M, Neumann MA, Byard RW, et al. Fatty acid composition of brain, retina, and erythrocytes in breast- and

formula-fed infants. Am J Clin Nutr. 1994;60:189-194.20. Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr. 1992;120(suppl):

S129-138.21. Levitt P. Structural and functional maturation of the developing primate brain. J Pediatr. 2003;143(suppl):S35-S45.22. Lozoff B, Wachs TD. Functional correlates of nutritional anemias in infancy and early childhood–child development and

behavior. In: Ramakrishnan U, ed. Nutritional Anemias. Boca Raton, FL: CRC Press; 2001:69-88.23. Auestad N, Montalto MB, Hall RT, et al. Visual acuity, erythrocyte fatty acid composition, and growth in term infants fed

formulas with long chain polyunsaturated fatty acids for one year. Ross Pediatric Lipid Study. Pediatr Res. 1997;41:1-10.24. Jensen CL, Maude M, Anderson RE, et al. Effect of docosahexaenoic acid supplementation of lactating women on the fatty

acid composition of breast milk lipids and maternal and infant plasma phospholipids. Am J Clin Nutr.2000;71(suppl):S292-S299.

25. Innis SM. Plasma and red blood cell fatty acid values as indexes of essential fatty acids in the developing organs of infantsfed with milk or formulas. J Pediatr. 1992;120(suppl):S78-S86.

26. Balk E, Chung M, Lichtenstein A, et al. Effects of Omega-3 Fatty Acids on Cardiovascular Risk Factors and IntermediateMarkers of Cardiovascular Disease. Summary, Evidence Report/Technology Assessment: Number 93. AHRQ PublicationNumber 04-E0101-1, March 2004. Rockville, MD: Agency for Healthcare Research and Quality; 2004.

27. Innis SM, Vaghri Z, King DJ. n-6 Docosapentaenoic acid is not a predictor of low docosahexaenoic acid status in Canadianpreschool children. Am J Clin Nutr. 2004;80:768-773.

28. U.S. Department of Health and Human Services & U.S. Environmental Protection Agency. What You Need to Know AboutMercury in Fish and Shellfish. 2004 EPA and FDA Advice for: Women Who Might Become Pregnant, Women Who arePregnant, Nursing Mothers, Young Children. 2004. Available at: http://www.cfsan.fda.gov/~dms/admeng3.html. AccessedApril 7, 2004.

29. Bourre JM, Piciotti M, Dumont O, et al. Dietary linoleic acid and polyunsaturated fatty acids in rat brain and other organs.Minimal requirements of linoleic acid. Lipids. 1990;25:465-472.

30. Koletzko B. Trans fatty acids may impair biosynthesis of long-chain polyunsaturates and growth in man. Acta Paediatr.1992;81:302-306.

31. Wauben IP, Xing HC, McCutcheon D, et al. Dietary trans fatty acids combined with a marginal essential fatty acid statusduring the pre- and postnatal periods do not affect growth or brain fatty acids but may alter behavioral development inB6D2F(2) mice. J Nutr. 2001;131:1568-1573.

“Children in the highesttertile of linoleic acid intakehad the lowest DHA status.”

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