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European Journal of Clinical Nutrition (2002) 56, 252–263 ß 2002 Nature Publishing Group All rights reserved 0954–3007/02 $25.00 www.nature.com/ejcn ORIGINAL COMMUNICATION Fat content of the diet among pre-school children in Britain; relationship with food and nutrient intakes

I Rogers1 and P Emmett* and the ALSPAC Study Team1

1Unit of Paediatric and Perinatal Epidemiology, Division of Child Health, University of Bristol, Bristol, UK

Objective: To investigate the relationship between the percentage of energy from fat and food and nutrient intakes at 18 and 43 months of age. Design: Diet was assessed using a 3 day unweighed food record. The children were divided into quartiles of fat intake as a percentage of energy (QFI), and food and nutrient intakes in the different QFIs were compared. Subjects: A total of 1026 children at 18 months and 863 children at 43 months, taking part in the Avon Longitudinal Study of Pregnancy and Childhood, participated. Results: At 18 months the mean (s.d.) fat intake was 31.2 (2.8) % of energy in the lowest QFI and 43.1 (2.2) % in the highest. Energy intake increased slightly with increasing QFI. The percentage of energy derived from total sugar, and in particular non- milk extrinsic sugar fell as QFI increased, as did the ratio of polyunsaturated to saturated fatty acids. Intakes of retinol equivalents and zinc increased significantly with increasing QFI, while intakes of iron and most water soluble vitamins fell. There was a particularly marked fall in vitamin C intake as fat intake increased, from 11.8 mg=MJ in the lowest QFI, to 6.0 mg=MJ in the highest (P < 0.001). Consumption of whole milk increased substantially with percentage energy from fat, from 51 g=MJ in the lowest QFI to 116 g=MJ in the highest (P < 0.001), while consumption of fruit and fruit juice fell. The results obtained at 43 months were very similar. Conclusions: The chances of a suboptimal intake of zinc and retinol were higher at lower fat intakes. However, intakes of the fat- soluble vitamins E and D were unrelated to fat intake and intakes of iron and vitamin C fell as fat intakes increased. Some suggestions for improving diet in this age group have been given. Sponsor: University of Bristol. European Journal of Clinical Nutrition (2002) 56, 252 – 263. DOI: 10.1038=sj=ejcn=1601335

Keywords: fat; micronutrients; iron; vitamin C; food groups; milk; pre-school children

Introduction the age by which an ‘adult’ level of fat intake should be A certain level of fat is vital in any diet, as a source of adopted. An argument for limiting fat intake in children is essential fatty acids and fat-soluble vitamins. It also has the that atherogenesis is a lifelong process, and may be acceler- advantage of carrying considerable amounts of energy in a ated by a high-fat diet due to its effect on blood lipid levels. small volume, making it a particularly important part of the Post-mortem studies have shown that the relationship diet of those, such as children, who have high energy between blood lipid levels and the extent of atherosclerotic requirements but relatively small appetites. However, the lesions is already present in childhood (Newman et al, 1986; optimal level of fat in the diet of children is disputed, as is Berenson et al, 1998). Furthermore, a preference for a high-fat diet established in childhood may be hard to change in later life. On the other *Correspondence: P Emmett, Unit of Paediatric and Perinatal hand, it has been feared that limiting fat intake by children Epidemiology, Division of Child Health, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK. may reduce the supply of energy and fat-soluble vitamins to E-mail: [email protected] inadequate levels (Lifshitz & Tarim, 1996). Guarantor: I Rogers. As a result there are many disparities in the recommenda- Contributors: Both authors collaborated closely in producing the data tions regarding fat intake by children issued by different and writing the paper. Received 13 March 2001; revised 9 August 2001; organisations. In 1990 the United States Department of accepted 6 September 2001 Agriculture (USDA) and Department of Health and Human Fat content of pre-school children’s diet I Rogers et al 253 Services (DHHS) suggested that after the age of 2 y children dren are different from those for adults — in this study most should consume a diet in which less than 30% of energy was mothers believed a low-fat diet to be desirable even for derived from fat (US Department of Agriculture & US Depart- infants (Morgan et al, 1995). Unfortunately, there is very ment of Health and Human Services, 1990). In 1992 the little information on the relationship between fat intake and American Academy of Pediatrics recommended that chil- dietary quality in representative free-living populations of dren’s diets should contain an average of 30% of energy children under 2 y of age (Ra¨sanen & Ylo¨nen, 1992; Lagstro¨m from fat, but advised against diets with less than 30% of et al, 1999). International differences in official advice and energy from fat (American Academy of Pediatrics Committee traditional feeding practices for children mean that country- on Nutrition, 1992). By 1998 the same committee advised specific information on this subject is very important. In this that, while no restriction of fat or cholesterol intake was paper we describe the relationship between fat intake and recommended before 2 y of age, between the ages of 2 and 5 dietary quality in a cohort of 18-month-old children in the children should gradually adopt a diet that, by age 5, con- south-west of England. To extend this further we have also tains less than 30% but more than 20% of energy from fat examined this relationship using dietary data obtained from (American Academy of Pediatrics Committee on Nutrition, the same sample at 43 months. 1998). In Canada, a joint working group from the Canadian Pediatric Society and Health Canada advised that ‘from the age of 2 until the end of linear growth there should be a Methods gradual transition from the high fat diet of infancy to a diet Study sample and design which includes no more than 30% of energy from fat and no This study forms part of ALSPAC, a geographically based more than 10% of energy from saturated fat’ (Health and cohort study investigating factors influencing the health and Welfare Canada, 1993). The guidelines issued by USDA and development of children. All pregnant women resident the DHHS in 1995 (US Department of Agriculture & US within a defined part of the county of Avon in south-west Department of Health and Human Services, 1995) also took England with an expected date of delivery between April this stance, ie recommending a gradual reduction of fat 1991 and December 1992 inclusive were eligible. Between 80 intake from the age of 2 onwards. However, by 2000 they and 90% of these enrolled (14 893 pregnancies). The ALSPAC had reverted to the position they held in 1990, ie all children cohort was broadly representative of pregnant women aged 2 and over should consume 30% of energy or less from nationally in terms of characteristics such as housing fat (US Department of Agriculture & US Department of tenure, marital status, access to a car etc, although when Health and Human Services, 2000). In their report on ‘Nutri- compared to 1991 national census data of women with tional Aspects of Cardiovascular Disease’ (Department of children aged under 1 y, mothers participating in ALSPAC Health Report on Health and Social Subjects, 1994) the were more likely than those in Britain overall to live in Committee on Medical Aspects of Food Policy in the UK owner-occupied accommodation and to have access to a recommended that by the age of 5 y children should be car, and less likely to have one or more persons per room consuming diets with an average fat content of around and to be from a non-white ethnic group. The biases in the 35%. No specific recommendations on fat intake were ALSPAC cohort have been described in more detail elsewhere made for children under 2, and it was suggested that (Golding et al, 2001; ALSPAC website: www.ich.bris.ac.uk/ ‘Between the ages of 2 and 5 y a flexible approach to the alspac.html). A proportion of the children born in the last 6 timing and extent of dietary change should be taken’. How- months of the study (equivalent to 10% of the whole cohort) ever, it is recommended that children should be given full- were selected at random to take part in a sub-study known as fat milk to drink until the age of 2 (Department of Health, Children in Focus (CIF). These children attended research 1994). In contrast, in Finland, parents are advised to give clinics at which a variety of physical and developmental their 1 – 2-y-old children low-fat (1.9%) milk products (Hasu- measures were taken approximately every 6 months (ALSPAC nen et al, 1989), and the Nordic Nutrition Recommendations website: www.ich.bris.ac.uk/alspac.html). The dietary infor- are that 1 – 3-y-old children should receive 30 – 35% of their mation used in this study was obtained at the CIF clinics energy from fat (Standing Nordic Committee on Food, held between December 1993 and June 1994 and January 1989). and July 1996, when the children were 18 and 43 months of Currently, children under the age of 2 are exempt from age, respectively. Ethical approval for the study was obtained the recommendations on fat intake in most countries. How- from the ALSPAC Ethics and Law Sub-Committee and from ever, as these children will be consuming mainly family the three Medical Ethics Committees in the Avon study area. foods, their diet will almost certainly be affected by the recommendations pertaining to all other age groups. A recent study of 55 children in the US found that 22% of Dietary assessment children at 12 months and 33% of children at 18 months Diet at 18 and 43 months was assessed using an unweighed consumed less than 30% of energy from fat (Picciano et al, dietary record completed for 3 days, not necessarily conse- 2000). Furthermore, a British study has shown that it is not cutive, including 2 weekdays and 1 weekend day. A week well understood that the dietary recommendations for chil- before the clinic the child’s primary carer was sent three 1

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 254 day dietary diaries in which they were asked to record in fizzy drinks and cordials, fruit, fruit juice, chips and fried household measures everything the child ate or drank. The potatoes and vegetables (excluding potatoes). diaries were coded using the computer program DIDO (Diet Pearson chi-square test and the Mantel – Haenszel test for In, Data Out) which is designed for direct entry of dietary linear association were used to test for association between records, and has been shown to improve the speed and QFI group and categorical variables. The categorical variables accuracy of dietary coding compared with manual methods investigated were sex of the child, mother’s highest educa- (Price et al, 1995). Portion size assumptions in this study were tional qualification and nutrient intake above or below the based largely on the booklet ‘Food Portion Sizes’ (Ministry of reference nutrient intake (RNI; Department of Health Report Agriculture, Fisheries and Food, 1993), which describes stan- on Health and Social Subjects, 1991). For the purposes of this dard British portion sizes, and scaled down appropriately for study the mother’s highest educational qualification was children. The output from DIDO was analysed using an in- classified as low (CSE or vocational), medium (O Level) or house dietary analysis program and a British nutrient data- high (A Level or degree). base (based on McCance and Widdowsons The Composition of The sexes were combined for analyses relating to nutrient Foods (Holland et al, 1991b) and its supplements (Holland intakes and food consumption variables, as the main out- et al, 1988, 1989, 1991a, 1992a, b, 1993; Chan et al, 1994, come of interest was food=nutrient consumption per MJ, 1995, 1996) along with manufacturers’ data) to produce which has been shown not to differ between the sexes in estimates of daily nutrient intake. The dietary methods these age groups (Cowin et al, 2000; Emmett et al, 2001). used have been described in more detail elsewhere (Cowin All statistical analyses were performed using the package & Emmett, 1999; Cowin et al, 2000; Emmett et al, 2001). SPSS. Non-milk extrinsic sugar (NME sugar) was calculated from total sugars by deducting all the sugar provided by fresh fruit, vegetables and milk and part of that provided by tinned fruit, Investigation of effect of under-reporting baked beans, yogurt and fromage frais and baby foods. (NME Under-reporting was defined as a reported energy intake of sugar is sugar that is not incorporated in the cellular struc- less than 120% of basal metabolic rate (BMR), as calculated ture of a food, or derived from milk eg sugar in confectionery from the equations given in the 1985 WHO=FAO=UNU or fruit juices). Dietary recommendations on limiting sugar report on energy and protein requirements (FAO=WHO= intake generally refer to this type of sugar, rather than sugar UNU, 1985). The number of under-reporters in each QFI present in the cellular structure of fruit and vegetables.) was compared using the Pearson chi-squared test. The ana- Nutrient intakes from supplements were not assessed in lyses comparing nutrient intakes and nutrient densities in this study. each QFI were repeated excluding under-reporters.

Results Statistical methods Response rate The children were divided into four groups according to Completed dietary diaries were received from 563 boys and their quartile of fat intake as a percentage of energy (QFI). 463 girls at 18 months (77% of the 1341 children invited), Differences in nutrient intakes between different fat intake and from 488 boys and 375 girls at 43 months (69.1% of the groups were investigated using one-way analysis of variance. 1249 children invited). The overall compositions of the diets The nutrients investigated were energy, total carbohydrate, at 18 (Cowin et al, 2000) and 43 (Emmett et al, 2001) months starch, total sugar, NME sugar, protein, polyunsaturated have been described in more detail elsewhere. (PUFA), saturated (SFA) and monounsaturated (MUFA) fatty acids, non-starch polysaccharides (NSP), vitamin C, thiamin,

riboflavin, niacin equivalents, vitamin B6, folate, carotene, Mean fat intake and composition of the different fat retinol, retinol equivalents, vitamin D, vitamin E, calcium, intake groups potassium, iron and zinc. If necessary variables were appro- The mean (s.d.) percentage energies from fat in the four priately transformed to reduce skewness in the distribution quartiles at 18 months were 31.2 (2.8), 36.1 (0.9), 39.1 (0.8) prior to analysis. and 43.1 (2.2). This corresponded to a mean (s.d.) fat intake The Kruskal – Wallis test was used to analyse differences in in grams of 37.3 (8.1), 44.3 (8.1), 50.4 (10.2) and 55.4 (12.7). food consumption between different QFI groups. The food At 43 months the corresponding figures were 30.4 (2.5), 34.8 groups investigated were biscuits, crisps and savoury snacks, (0.9), 37.7 (0.9) and 41.8 (2.0) for percentage energy from fat, meat products (ie burgers, sausages, pies and kebabs), red and 44.4 (10.1), 52.4 (9.0), 59.3 (11.1) and 66.9 (13.2) for fat meat and dishes, chicken and other poultry, fish, chocolate, intake in grams. buns, cakes and puddings, bread, breakfast cereals, cheese, The number of boys and girls in each fat intake group was spreading and cooking fats, whole milk, semi-skimmed milk, approximately equal, with sex of the child apparently not sugars, preserves and sweet spreads, sugar confectionery, associated with QFI. The highest educational level of ‘non-diet’fizzy drinks and cordials, ‘diet’ or reduced-sugar mothers of children in the different fat intake groups at 18

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 255 and 43 months is shown in Table 1. The Pearson chi-square intake rose; however, at 43 months, the lowest percentage test showed no significant association between QFI and of energy from protein was in the third highest QFI. maternal educational level at 18 months. However, the For most water-soluble vitamins both the absolute intake Mantel – Haenszel test for linear association revealed a sig- and the nutrient density decreased significantly with increas- nificant trend, with the number of mothers of high educa- ing QFI. This fall was particularly marked at both ages for tional level decreasing as QFI increased (w2 ¼ 7.84, P ¼ 0.005). vitamin C. At 18 months riboflavin intake increased slightly At 43 months the association between QFI and maternal as fat intake rose, but this was no longer true at 43 months. educational level was statistically significant by Pearson chi- The intake of retinol and retinol equivalents increased con- square, with an excess of children with mothers with high siderably as fat intake rose at both 18 and 43 months. This educational level in the lowest QFI, and a shortfall in the was despite a significant drop in carotene intake with number of children with mothers of medium educational increasing QFI at both ages. However, there was no associa- level. However, the Mantel – Haenszel test found no tion between QFI and the levels of vitamin E or D in the diet. significant linear trend at 43 months. Calcium intakes increased markedly across the QFIs, and at 18 months only there was also a slight increase in zinc intakes. However, iron and potassium intakes fell at both ages. Nutrient intakes and quartile of fat intake Tables 2 and 3 show mean energy intake and the mean nutrient intake per MJ by QFI at 18 and 43 months, respec- Comparison with the dietary reference values tively. The analysis was repeated using absolute nutrient In Britain the Reference Nutrient Intake (RNI) is a commonly intakes and the results were extremely similar (data not used benchmark of the nutrient adequacy of a diet. The RNI shown). is a nutrient intake which should be adequate for 97.5% of The relationship between the intake of fat and other the population, and is specific to age and sex group (Depart- nutrients was very similar at both 18 and 43 months. At ment of Health Report on Health and Social Subjects, 1991). both ages there was a small but significant increase in energy For most vitamins and minerals investigated, almost no intake with increasing QFI. The percentages of energy children were consuming less than the reference nutrient derived from total carbohydrate, starch, total sugar and intake (RNI) at either 18 or 43 months (Cowin et al, 2000; NME sugar all fell as fat intake rose, most of the drop in Emmett et al, 2001). This was, however, not the case for total sugar intake being accounted for by NME sugar. Intakes vitamin C (RNI ¼ 30 mg=day), vitamin A (RNI ¼ 400 mg=day), of NSP also fell as fat intake rose. The percentage of energy iron (RNI ¼ 6.9 mg=day), zinc (RNI ¼ 5.0 mg=day) and cal- from all three types of fatty acids increased significantly cium (RNI ¼ 350 mg=day). The percentages of children at 18 across the QFI categories. However, the increase in the and 43 months consuming below the RNI for these nutrients percentage of energy from PUFA was very small, the differ- in each QFI are shown in Figure 1. In all cases there was a ences in fat intake across the quartiles being almost entirely significant association with fat intake category (P < 0.001 in accounted for by increases in MUFA and SFA. Consequently, all cases, except for iron at 18 months where P ¼ 0.002, and there was a large drop in the ratio of polyunsaturated:satu- calcium at 43 months where P ¼ 0.011). With increasing fat rated fatty acids (P:S ratio) as the percentage of energy from intake the chances of consuming less than the RNI for zinc, fat increased. At 18 months there was a small but significant calcium and vitamin A decreased, while the chances of increase in the percentage of energy from protein as fat consuming less than the RNI for vitamin C or iron increased.

Table 1 Percentages of children in three maternal education categories according to QFI at 18 and 43 months

Quartile of fat intake as a percentage of energy

Maternal education 1234w2 P

18 months Low 16.8 20.5 23.8 25.4 9.6 0.143 Medium 37.2 36.6 33.7 39.1 High 46.0 42.9 42.5 35.5 (n ¼ 250) (n ¼ 254) (n ¼ 252) (n ¼ 248)

43 months Low 23.4 22.3 19.7 17.0 12.9 0.044 Medium 27.3 39.3 40.8 38.2 High 49.3 38.4 39.4 44.8 (n ¼ 209) (n ¼ 211) (n ¼ 213) (n ¼ 212)

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 256 The results were very similar at both ages, except that fewer Food intakes and quartile of fat intake children met the RNI for iron, vitamin C and zinc at 18 than Adjusting for energy consumption had very little effect on at 43 months. the relationship between fat intake and food consumption at

Table 2 Mean=geometric mean (95% CI) nutrient densities at 18 months according to QFI

By quartile of fat intake as a percentage of energy

Nutrient density 1 2 3 4 Whole sample Pb

Energy (MJ)c 4.32 4.46 4.68 4.64 4.53 < 0.001 (4.22, 4.44) (4.36, 4.56) (4.57, 4.79) (4.52, 4.77) (4.47, 4.58) CHO, E%a 54.0 48.8 45.5 41.1 47.4 < 0.001 (53.5, 54.5) (48.6, 49.1) (45.3, 45.8) (40.7, 41.5) (47.0, 47.7) Starch, E%a 23.0 21.4 20.5 18.4 20.8 < 0.001 (22.3, 23.6) (20.9, 22.0) (19.9, 21.0) (17.9, 19.0) (20.5, 21.1) Sugar, E%a 30.8 27.2 24.8 22.5 26.3 < 0.001 (30.1, 31.5) (26.6, 27.7) (24.3, 25.4) (22.0, 23.0) (26.0, 26.7) NME sugar, E%a,d 15.1 12.8 10.9 8.4 11.7 < 0.001 (14.3, 15.9) (12.2, 13.5) (10.3, 11.4) (7.9, 8.8) (11.3, 12.0) Protein, E%a 14.8 15.1 15.4 15.8 15.3 < 0.001 (14.5, 15.1) (14.8, 15.4) (15.2, 15.7) (15.5, 16.1) (15.1, 15.4) PUFA, E%a,c 3.81 3.97 4.14 4.11 4.01 0.019 (3.66, 3.97) (3.81, 4.13) (3.98, 4.31) (3.93, 4.30) (3.92, 4.09) SFA, E%a 14.2 17.2 18.9 21.5 18.0 < 0.001 (13.9, 14.5) (16.9, 17.4) (18.6, 19.2) (21.2, 21.9) (17.7, 18.2) MUFA, E%a 10.0 11.5 12.6 13.8 12.0 < 0.001 (9.9, 10.2) (11.4, 11.7) (12.5, 12.8) (13.6, 13.9) (11.9, 12.1) P:S ratioc 0.27 0.23 0.22 0.19 0.23 < 0.001 (0.26, 0.29) (0.22, 0.25) (0.21, 0.23) (0.18, 0.20) (0.22, 0.23) Cholesterol (mg=MJ)c 24 29 31 36 30 < 0.001 (23, 25) (28, 30) (30, 32) (35, 38) (29, 30) NSP (g=MJ) 1.66 1.53 1.40 1.19 1.44 < 0.001 (1.60, 1.72) (1.47, 1.58) (1.36, 1.45) (1.14, 1.24) (1.42, 1.47) Vitamin C (mg=MJ)c 11.8 9.5 8.0 6.0 8.6 < 0.001 (10.7, 12.9) (8.7, 10.4) (7.3, 8.7) (5.6, 6.5) (8.2, 9.0) Thiamin (mg=MJ)c 0.20 0.19 0.18 0.17 0.19 < 0.001 (0.19, 0.20) (0.18, 0.20) (0.18, 0.19) (0.17, 0.18) (0.18, 0.19) Riboflavin (mg=MJ) 0.32 0.32 0.33 0.34 0.33 < 0.001 (0.30, 0.33) (0.31, 0.33) (0.32, 0.33) (0.33, 0.35) (0.32, 0.33) Niacin equivalent (mg=MJ)c 3.85 3.71 3.62 3.47 3.66 < 0.001 (3.76, 3.93) (3.62, 3.79) (3.55, 3.69) (3.40, 3.54) (3.62, 3.70)

Vitamin B6 (mg=MJ) 0.26 0.24 0.23 0.22 0.24 < 0.001 (0.25, 0.27) (0.23, 0.24) (0.23, 0.24) (0.21, 0.22) (0.23, 0.24) Folate (mg=MJ) 30.9 29.5 28.0 26.6 28.7 < 0.001 (30.0, 31.8) (28.6, 30.3) (27.2, 28.7) (25.9, 27.3) (28.3, 29.1) Carotene (mg=MJ)d 298 295 269 242 275 0.004 (271, 326) (268, 324) (248, 291) (220, 264) (263, 287) Retinol (mg=MJ)c 65.5 79.4 80.2 96.0 79.6 < 0.001 (61.4, 69.9) (74.3, 84.7) (76.3, 84.3) (90.9, 101.4) (77.2, 82.0) Retinol equivalent (mg=MJ)c 102 121 116 131 117 < 0.001 (96, 110) (113, 129) (111, 123) (124, 138) (114, 121) Vitamin D (mg=MJ)c 0.27 0.26 0.26 0.27 0.27 0.991 (0.24, 0.29) (0.25, 0.28) (0.25, 0.28) (0.25, 0.29) (0.26, 0.28) Vitamin E (mg=MJ)c 0.92 0.89 0.90 0.90 0.90 0.912 (0.87, 0.96) (0.86, 0.94) (0.86, 0.94) (0.86, 0.95) (0.88, 0.92) Calcium (mg=MJ) 157 167 178 199 175 < 0.001 (151, 163) (162, 172) (173, 183) (193, 204) (172, 178) Potassium (mg=MJ) 395 377 370 365 377 < 0.001 (386, 404) (370, 383) (363, 377) (358, 373) (373, 381) Iron (mg=MJ)c 1.26 1.18 1.08 0.97 1.12 < 0.001 (1.22, 1.30) (1.14, 1.22) (1.05, 1.12) (0.93, 1.00) (1.10, 1.14) Zinc (mg=MJ) 1.04 1.07 1.08 1.12 1.08 < 0.001 (1.01, 1.07) (1.04, 1.09) (1.06, 1.11) (1.10, 1.14) (1.07, 1.09)

aE%, percentage of energy. bBased on ANOVA. cGeometric means shown, as nutrient transformed to the natural logarithm. dGeometric means shown, as nutrient transformed to the square root.

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 257 either 18 or 43 months, so only the results for food intake per The mean weight of food consumed per unit energy in MJ are shown. each QFI at 18 months is shown in Table 4. The most striking

Table 3 Mean=geometric mean (95% CI) nutrient densities at 43 months according to QFI

Quartile of fat intake as percentage energy

Nutrient density 1 2 3 4 Whole sample Pb

Energy (kJ)c 5.28 5.47 5.71 5.82 5.57 < 0.001 (5.13, 5.42) (5.35, 5.61) (5.57, 5.86) (5.68, 5.97) (5.50, 5.64) CHO, E%a 55.4 51.1 48.8 44.1 49.9 < 0.001 (55.0, 55.9) (50.8, 51.5) (48.5, 49.1) (43.7, 44.5) (49.5, 50.2) Starch, E%a 26.0 24.9 23.2 21.1 23.8 < 0.001 (25.3, 26.7) (24.3, 25.5) (22.5, 23.8) (20.4, 21.7) (23.4, 24.1) Sugar, E%a 28.9 25.8 25.2 22.7 25.6 < 0.001 (28.2, 29.7) (25.1, 26.4) (24.5, 25.8) (22.1, 23.3) (25.3, 26.0) NME sugar, E%a 19.0 16.4 16.6 13.5 16.4 < 0.001 (18.2, 19.9) (15.7, 17.2) (16.0, 17.2) (12.9, 14.1) (16.0, 16.8) Protein, E%a 14.2 14.1 13.6 14.2 14.0 0.014 (13.9, 14.6) (13.8, 14.5) (13.3, 13.9) (13.9, 14.5) (13.9, 14.2) PUFA, E%a,c 4.45 4.88 4.71 4.98 4.75 < 0.001 (4.28, 4.63) (4.71, 5.05) (4.51, 5.91) (4.75, 5.22) (4.65, 4.85) SFA, E%a 12.9 15.2 16.9 19.3 16.1 < 0.001 (12.6, 13.1) (15.0, 15.5) (16.6, 17.2) (19.0, 19.7) (15.9, 16.3) MUFA, E%a 10.0 11.5 12.3 13.5 11.8 < 0.001 (9.9, 10.2) (11.4, 11.6) (12.2, 12.5) (13.3, 13.7) (11.7, 12.0) P:S ratioc 0.35 0.32 0.28 0.26 0.30 < 0.001 (0.33, 0.37) (0.31, 0.34) (0.27, 0.30) (0.24, 0.28) (0.29, 0.31) Cholesterol (mg=MJ)c 21 24 26 31 25 < 0.001 (20, 23) (23, 26) (25, 27) (29, 32) (25, 26) NSP (g=MJ)d 1.63 1.48 1.32 1.22 1.41 < 0.001 (1.56, 1.70) (1.43, 1.53) (1.27, 1.37) (1.17, 1.26) (1.38, 1.44) Vitamin C (mg=MJ)c 10.1 8.0 7.1 6.2 7.71 < 0.001 (9.2, 11.1) (7.3, 8.7) (6.5, 7.7) (5.7, 6.7) (7.37, 8.07) Thiamin (mg=MJ)c 0.19 0.17 0.16 0.15 0.17 < 0.001 (0.18, 0.20) (0.17, 0.18) (0.16, 0.17) (0.15, 0.16) (0.17, 0.17) Riboflavin (mg=MJ) 0.26 0.26 0.25 0.27 0.26 0.086 (0.25, 0.27) (0.25, 0.27) (0.24, 0.26) (0.26, 0.28) (0.25, 0.26) Niacin equivalent (mg=MJ)c 3.87 3.71 3.43 3.36 3.59 < 0.001 (3.76, 3.98) (3.61, 3.80) (3.35, 3.52) (3.28, 3.44) (3.54, 3.63) c Vitamin B6 (mg=MJ) 0.25 0.24 0.22 0.20 0.23 < 0.001 (0.24, 0.26) (0.23, 0.24) (0.21, 0.23) (0.20, 0.21) (0.22, 0.23) Folate (mg=MJ)c 28.5 27.1 25.0 23.9 26.0 < 0.001 (27.4, 29.5) (26.2, 27.9) (24.2, 25.8) (23.1, 24.7) (25.6, 26.5) Carotene (mg=MJ)c 211 197 187 171 191 0.047 (189, 235) (178, 218) (168, 207) (154, 191) (181, 201) Retinol (mg=MJ)c 44.3 52.7 57.1 75.1 56.2 < 0.001 (42.0, 46.6) (50.0, 55.5) (54.1, 60.3) (70.7, 79.9) (54.6, 58.0) Retinol equivalent (mg=MJ)c 73.0 77.4 80.9 100.3 82.3 < 0.001 (68.2, 78.1) (72.2, 82.9) (75.5, 86.8) (93.9, 107.2) (79.5, 85.2) Vitamin D (mg=MJ)c 0.28 0.29 0.27 0.28 0.28 0.620 (0.26, 0.29) (0.27, 0.31) (0.26, 0.29) (0.26, 0.30) (0.27, 0.29) Vitamin E (mg=MJ)c 0.98 1.06 1.01 1.01 1.01 0.091 (0.93, 1.02) (1.02, 1.11) (0.97, 1.06) (0.96, 1.06) (0.99, 1.04) Calcium (mg=MJ) 126 130 131 152 135 < 0.001 (120, 132) (125, 134) (126, 137) (146, 157) (132, 137) Potassium (mg=MJ) 356 334 321 315 331 < 0.001 (346, 366) (327, 342) (314, 328) (307, 322) (327, 336) Iron (mg=MJ)c 1.20 1.12 1.05 0.97 1.08 < 0.001 (1.16, 1.23) (1.09, 1.15) (1.02, 1.09) (0.93, 1.00) (1.06, 1.10) Zinc (mg=MJ)c 0.89 0.87 0.87 0.91 0.89 0.063 (0.86, 0.92) (0.85, 0.90) (0.84, 0.89) (0.89, 0.94) (0.87, 0.90)

aE%, percentage of energy. bBased on ANOVA. cGeometric means shown, as nutrient transformed to the natural logarithm. dGeometric means shown, as nutrient transformed to the square root.

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 258

Figure 1 Proportion of children falling below the reference nutrient intake (RNI) for selected nutrients at 18 and 43 months.

result is the huge increase in whole milk consumption across groups. There were no significant differences between the quartiles of fat intake. It seems likely that this food largely fat intake groups in consumption of biscuits, red meat and accounts for the differences in fat consumption. Other foods dishes, bread, spreading and cooking fats, sugar confection- for which consumption increased significantly with increas- ery or fried potatoes=chips. ing fat intake were crisps and savoury snacks, meat products, At 43 months the results were very similar (Table 5), with chocolate and cheese. Foods for which consumption fell the most marked differences between low- and high-fat diets with increasing fat intake were semi-skimmed milk, buns, being in consumption of whole milk, and fruit and fruit cakes and puddings, breakfast cereals, sugars, preserves and juice. The average volumes of whole milk consumed, how- sweet spreads, fruit, fruit juice and all vegetables. The fall in ever, had fallen considerably since the children were 18 consumption was particularly marked for fruit and fruit months old (although more semi-skimmed milk was drunk juice — for fruit juice there was more than a four-fold differ- at 43 months). There were a number of other minor differ- ence in consumption between the top and bottom QFI. ences from the results obtained at 18 months. Although There was also a considerable drop in the intake of non- consumption of non-diet cordials and fizzy drinks fell with diet fizzy drinks and cordials as fat intake increased, increasing fat intake this difference was not significant. In although there was no significant difference in the intake addition, there were significant decreases in consumption of of diet=low sugar drinks. Intakes of fish and chicken were sugar confectionery and bread as fat intake increased, and a considerably lower in the highest QFI than in the other significant increase in the amount of spreading and cooking

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 259 Table 4 Mean food consumption per unit energy at 18 months according to QFI

Quartile of fat intake as percentage energy

Food weight (g=MJ) 1 2 3 4 Pa

Biscuits 2.7 2.8 2.6 2.5 0.067 Crisps and savoury snacks 1.1 1.1 1.5 1.7 < 0.001 Meat productsb 1.4 1.4 1.9 2.4 < 0.001 Red meat and dishes 4.1 4.6 5.0 4.6 0.271 Chicken and turkey 2.4 2.0 2.2 1.6 0.013 Fish 2.5 2.5 2.3 1.4 < 0.001 Chocolate 1.2 1.6 1.6 1.6 0.016 Buns, cakes and puddings 7.7 7.5 7.5 5.4 0.012 Bread 7.4 7.3 7.0 6.5 0.053 Breakfast cereal 4.9 4.5 3.8 3.0 < 0.001 Cheese 1.1 1.5 1.6 1.8 < 0.001 Spreading and cooking fats 1.2 1.3 1.3 1.3 0.715 Whole milk 51 79 92 116 < 0.001 Semi-skimmed milk 17.8 4.1 3.9 1.7 < 0.001 Sugars, preserves and sweet spreads 1.1 0.8 0.7 0.5 < 0.001 Sugar confectionery 0.6 0.4 0.3 0.2 0.061 Normal cordials and fizzy drinks 36.4 24.7 22.3 11.8 < 0.001 Diet cordials and fizzy drinks 58.1 49.6 50.0 59.0 0.158 Fruit 18.4 14.2 12.9 8.4 < 0.001 Fruit juice 16.1 10.5 5.7 3.6 < 0.001 Fried potatoes 3.7 3.9 3.8 3.6 0.825 All vegetables 8.8 9.4 8.7 7.7 0.022

aBased on Kruskal – Wallis. bBurgers, sausages and pies.

fats eaten. Intakes of fried potatoes=chips differed signifi- Discussion cantly between the fat intake groups, but the lowest con- In this free-living group of children there was a wide range in sumption was by those children with the highest fat intakes. the proportion of energy derived from fat. Comparing rela- tively high- and low-fat diets revealed many significant differences in food and nutrient consumption. Notable dif- ferences in nutrient consumption were higher intakes of Under-reporting energy, calcium, vitamin A and zinc with increasing fat There was no significant association between QFI and intake and lower intakes of vitamin C and iron. The fear number of under-reporters at 18 months, with the propor- that intakes of fat-soluble vitamins might be compromised tion of under-reporters ranging from 2.8% in the third by low-fat diets was not really borne out by these data as the quartile of fat intake to 6.3% in the first quartile (w2 ¼ 3.9, only fat-soluble vitamin positively associated with fat intake P ¼ 0.272). At 43 months, the number of children suspected was retinol — intakes of carotene fell as fat intake rose and to be under-reporting increased significantly with decreasing there was no association with vitamin E or vitamin D. QFI, from 4.7% in the fourth quartile to 14.0% in the first Children with higher-fat diets consumed more whole milk quartile (w2 ¼ 12.6, P ¼ 0.006). Excluding under-reporters had and meat products, and less fruit, fruit juice, cereal products no effect on the associations observed between the intake of and fish. Not all food groups making an important contribu- fat and other nutrients — this was true at both ages (data not tion to fat intake differentiated between low-fat and high-fat shown). diets. These data should therefore be useful in designing food-frequency questionnaires to assess fat intake in pre- school children. We assessed diet using a 3 day unweighed food record. Tracking of fat intake from 18 to 43 months The gold standard for dietary assessment is generally con- Dietary information was available at both 18 and 43 months sidered to be the 7 day weighed intake; however, it was for 755 children. Some 30.7% of these children remained in thought that this method would place too great a burden the same quartile of percentage energy from fat at 18 and 43 upon the parents participating in the survey. Unweighed months, 42.8% had moved by one quartile, 17.5% had food records have been shown to compare well with data moved by two quartiles and 9.0% were in opposite quartiles. obtained from weighed intakes (Bingham et al, 1994). The The correlation between the percentage of energy from fat at correlation between fat intakes at the two timepoints was 18 and 43 months was 0.257 (P < 0.001). quite low, and less than a third of the children were in the

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 260 Table 5 Mean food consumption per unit energy at 43 months according to QFI

Quartile of fat intake as percentage energy

Food weight (g=MJ) 1 2 3 4 P

Biscuits 2.8 3.4 3.3 2.6 0.004 Crisps and savoury snacks 1.6 2.1 2.4 2.1 < 0.001 Meat productsa 1.5 1.9 2.2 2.3 0.003 Red meat and dishes 4.5 4.4 4.2 4.3 0.803 Chicken and turkey 3.4 3.5 2.8 3.1 0.390 Fish 3.1 3.1 2.2 1.9 0.001 Chocolate 1.7 2.2 2.2 2.1 0.053 Buns, cakes and puddings 9.5 8.2 10.0 8.4 0.013 Bread 10.1 9.0 8.4 8.6 0.003 Breakfast cereal 5.5 4.5 3.5 3.6 < 0.001 Cheese 1.0 1.3 1.6 2.4 < 0.001 Spreading and cooking fats 1.5 1.5 1.7 1.9 0.001 Whole milk 26 40 47 67 < 0.001 Semi-skimmed milk 25.1 14.4 10.0 5.3 < 0.001 Sugars, preserves and sweet spreads 1.6 1.1 1.0 1.0 0.001 Sugar confectionery 1.3 0.9 1.0 0.6 0.008 Normal cordials and fizzy drinks 29.0 22.6 23.1 27.4 0.225 Diet cordials and fizzy drinks 57.6 64.4 61.1 54.9 0.458 Fruit 15.3 12.5 9.9 9.3 < 0.001 Fruit juice 18.4 11.4 9.0 6.6 < 0.001 Fried potatoes 6.1 6.3 5.9 4.6 0.001 All vegetables 8.6 7.8 6.3 6.3 0.003

aBurgers, sausages and pies.

same quartile of fat intake at both 18 and 43 months. This were consuming above the Estimated Average Requirement partly reflects the rapidly changing diet of this age-group (EAR) for energy in all QFIs, while at 43 months less than (Emmett et al, 2001). However, the relationship between 50% of children reached the EAR for energy in any QFI (23.7 food and nutrient intakes and fat intake was very similar at to 44.2%). Despite these differences in energy intake, no the two ages. This was despite the changing relationship effect of QFI on height or BMI could be found at either age between fat intake and maternal educational level at the two (Rogers et al, 2001). timepoints, thus it seems that within the confines of the No specific recommendations on fat intake by children British diet a low-fat diet for children is likely to have a under 5 are given in Britain, although it is recommended particular composition. The low correlation of fat intakes that between the ages of 2 and 5 children gradually adopt a over this relatively short time period (25 months) suggests diet containing around 12% of energy from MUFA, 6% from that the correlation between fat intakes measured many PUFA and 10% from SFA (Department of Health Report on years apart would be very low, and argues against the asser- Health and Social Subjects, 1994). Our data at 43 months tion that establishing a low-fat diet in early childhood will show that, while MUFA intakes were already at roughly the result in a preference for a low-fat diet later in life. recommended level, a considerable drop in SFA intake (from QFI was unassociated with the intakes of vitamins D and 16% of energy) and a small increase in PUFA intake (from 5% E, despite the fact that these vitamins are fat soluble. This of energy) over the next year or so would be needed to was because the foods which distinguished between the achieve the recommendations by the age of 5 y. different QFI groups were not important sources of these We found that children consuming less fat had higher vitamins. For , intakes of whole milk, meat products, intakes of NME sugars. It is recommended that intakes of chocolate, cheese and crisps and savoury snacks increased NME sugars by adults and older children are limited to at significantly with increasing QFI, and between them these most 10% of energy. This is on the basis that too heavy a food groups accounted for 48% of the total fat intake at 18 reliance on NME sugars as an energy source may encourage months, but only 15% of the total vitamin D intake, and passive overconsumption of energy and increase the risk of 20% of the vitamin E intake. dental caries. For individuals with low energy requirements It has been feared that low-fat diets might compromise and intakes, high NME intakes can compete with other food energy intakes in children as a result of reduced energy sources and compromise micronutrient intakes. Extremely density. In this study we found that energy intake increased high intakes of NME sugars (above about 30% of energy) may significantly with QFI at both 18 and 43 months. However, also be associated with elevated concentrations of blood at 18 months the majority of the children (51.2 – 62.6%) cholesterol, glucose and insulin. Mean intakes of NME

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 261 sugars in the CIF group at 18 months were 12% of energy. A et al, 2000). This contrasts with our results, where intakes of recent analysis of the 1994 – 1996 Continuing Survey of Food iron and water-soluble vitamins were higher in children on Intakes by Individuals in the US showed that high consu- lower fat intakes. Unfortunately, information on food con- mers of added sugar had lower scores on a healthy eating sumption was not given in all the studies. A lack of children index (Britten et al, 2000). This was particularly true for those from the lower socio-economic groups, who are likely to be at with below average energy intakes. In our survey, higher the most risk of receiving an inadequate diet, was a further NME sugar intakes (and lower fat intakes) were associated problem with some of these studies (Ra¨sanen & Ylo¨nen, 1992; with below average energy intakes. Tonstad & Sivertsen, 1997). Three other studies have looked at the relationship It seems likely that a reduction in fat intake could be between fat intake and dietary quality in children under safely implemented by recommending the use of semi- 2 y of age, two of them Finnish. The largest was STRIP, a skimmed milk in this age group, as in Finland. This might supervised intervention study which aimed to reduce fat prevent the drop in calcium intakes on lower-fat diets intake to less than 35% of energy after 13 months of age, observed in the present study. An American study found and included 1062 infants (Lagstro¨m et al, 1999). The other that the use of skimmed milk enabled children to meet was a small observational study of 46 1 – 2-y-old children in guidelines for limiting fat intake while maintaining adequate Helsinki (Ra¨sanen & Ylo¨nen, 1992). In the STRIP study micronutrient and energy intake (Peterson & Sigman-Grant, higher fat intakes were associated with lower carbohydrate 1997). Alternatively, an upper limit on the amount of milk intakes, and slightly higher energy intakes. There were no included in the diet of the under-fives could be suggested to consistent differences in mineral or vitamin A intakes parents — in our study the number of children consuming between different fat intake groups, but children with more than 750 ml of cow’s milk a day at 18 months increased higher fat intakes consumed more vitamin E, and those from 2.7% in the lowest quartile of fat intake to 16.8% in the with lower fat intakes consumed more vegetables, fruit and highest quartile, and 5.9% of children in the highest quartile berries, and consequently more vitamin C and fibre. In the of fat intake were drinking more than a litre of milk a day. It Helsinki study there were no differences in energy between is possible that limiting milk intake might also have a fat intake groups, and the lowest protein intakes were found positive effect on iron status; a separate analysis of data among children on the highest fat intakes. Intakes of fibre, from this cohort has shown ferritin levels to be negatively zinc, calcium and sugar all fell as fat intake increased, associated with the level of calcium intake and milk and although only the falls in fibre and zinc were significant. dairy product consumption (Cowin et al, 2001). Switching The third study assessed nutrient intake monthly from 12 to from high-fat meat products to lean meats and reducing the 18 months among 55 children in the US (Picciano et al, intake of crisps and savoury snacks are other ways in which 2000). At 12 and 18 months old, respectively, 22 and 33% of fat intake could be reduced in young children without children derived less than 30% of energy from dietary fat, adversely affecting vitamin or mineral intake. One American contrary to recommendations. Very few of the children met study looked at 4 to 10-y-olds participating in a nutrition the recommended intake of vitamin E, intakes of which education programme which aimed to lower LDL cholesterol correlated with percentage energy from fat at 12 months levels via dietary modification. It found that those children old, but not at 18 months. The authors noted the marginal who reduced fat intake most over 3 months tended to do so intakes of iron and zinc by these children, and the need to by replacing high-fat foods with lower fat foods in the meats, stress to parents that the kind of fat-reduction strategies used dairy products and desserts food groups (Dixon et al, 1997). for adults are inappropriate for this age group; however, the Replacing some of the calories derived from milk with oily relationship between fat intake and zinc and iron intakes was fish might also improve the nutrient adequacy of the diet — not reported. oily fish, like milk, is a good source of calcium and retinol A number of other studies have dealt with older pre-school but is also rich in zinc, iron and vitamin D, intakes of which and school-age children (Nicklas et al, 1992; Vobecky et al, are marginal in this population (Cowin et al, 2000; Emmett 1992; Shea et al, 1993; Boulton & Magarey, 1995; Tonstad & et al, 2001). Furthermore, as fish oil is polyunsaturated, Sivertsen, 1997; Ballew et al, 2000). While the results are fairly consumption of some oily fish in place of milk would consistent in showing an inverse relationship between fat improve the P:S ratio of the diet. intake and sugar, fibre and vitamin C, the relationship with In conclusion these data suggest that among pre-school other nutrients is extremely variable, with one study actually children in Britain both low-fat and high-fat diets have finding children with higher fat diets to be at greater risk of an certain advantages and limitations. High-fat diets were asso- inadequate intake of (fat-soluble) vitamin A (Ballew et al, ciated with greater adequacy for calcium, zinc and vitamin A 2000). Only in one study of 8 to 10-y-old children in the intakes. Low-fat diets were associated with greater adequacy USA, however, did the intake of iron and both fat-soluble and for iron and vitamin C along with higher fruit intakes, but water-soluble vitamins all fall as fat intake decreased (Nicklas also with higher intakes of NME sugars. The need to moder- et al, 1992). This seemed to be because low-fat diets were ate sugar intake by young children should be stressed to characterised by low meat intake, a finding also reported parents, while advocating the other dietary improvements in another American survey of 2 to 8-y-old children (Ballew suggested above.

European Journal of Clinical Nutrition Fat content of pre-school children’s diet I Rogers et al 262 Acknowledgements Department of Health Report on Health and Social Subjects (1991): Dietary reference values for food, energy and nutrients for the United We are extremely grateful to all the parents and children Kingdom. London: HMSO. who took part in this study and to the midwives for their Department of Health Report on Health and Social Subjects (1994): help in recruiting them. We would like to acknowledge the Nutritional aspects of cardiovascular disease. London: HMSO. dedicated work of the ALSPAC study team; this includes Dixon LB, McKenzie J, Shannon BM, Mitchell DC, Smiciklas-Wright H & Tershakovec AM (1997): The effect of changes in dietary fat on interviewers, computer technicians, clerical workers, the food group and nutrient intake of 4- to 10-year old children. research scientists, volunteers and managers. 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