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European Journal of Clinical Nutrition (2006) 60, 909–914

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ORIGINAL ARTICLE

Evaluation of dietary fibre intake from infancy to adolescence against various references – results of the DONALD Study U Alexy, M Kersting and W Sichert-Hellert Research Institute of Child Nutrition, Dortmund, Germany

Objective: To evaluate dietary fibre intake from infancy to adolescence against various reference standards expressed on a body weight, age or energy intake (EI) basis and to describe age and 15-year time trends. Design and subjects: The ongoing longitudinal (open cohort) Dortmund Nutritional and Anthropometric Longitudinally Designed Study with a total of 7810 3-day dietary records from 980 infants, children and adolescents aged 6 months to 18 years collected between 1990 and 2004. Results: Absolute dietary fibre intakes (g/day) increased with age from infancy to adolescence; dietary fibre density (g/1000 kcal) reached a maximum at 1 year and remained constant after the transition to the family diet. Expressed as g/kg body weight, dietary fibre intake increased during infancy with a maximum at 1 year, but decreased thereafter during childhood and adolescence. Dietary fibre intake was low irrespective of the reference used and showed no time trends, with the exception of a small negative trend in 4–8-year olds and 9–13-year-old girls. Conclusion: As intake of dietary fibre in our sample was significantly associated with EI and fibre density remained constant after infancy, our data support an energy-based approach for establishing a reference value for children and adolescents.

European Journal of Clinical Nutrition (2006) 60, 909–914. doi:10.1038/sj.ejcn.1602400; published online 15 February 2006 Keywords: dietary fibre; infants; children; adolescents; dietary survey; energy intake

Introduction Dietary fibre is defined as non-digestible carbohydrates (NDC) and lignin that are intrinsic and intact in plants (Institute of Medicine, 2002). It is important for maintenance of gastrointestinal health and is protective in decreasing the risk of coronary heart disease (CHD). Other potential functions of dietary fibre are under discussion, that is, effect on satiety and weight maintenance, and the prevention of diabetes, colon or breast cancer (Institute of Medicine, 2002). As potential negative effects of dietary fibre, a lower bioavailability of minerals and gastrointestinal distress, for

Correspondence: Dr U Alexy, Research Institute of Child Nutrition Dortmund (FKE), Heinstueck 11, Dortmund 44225, Germany. E-mail: [email protected] Guarantor: U Alexy. Contributors: All authors were involved in the concept of the paper. UA was primarily responsible for the data analysis. WS contributed to statistical analysis. MK and UA collaborated in writing the paper. Received 26 July 2005; revised 18 November 2005; accepted 2 December 2005; published online 15 February 2006

example, flatulence, are under discussion (Institute of Medicine, 2002). Differences in the interpretation of the evidence base, in the use of different disease or functional end points and in the analytical methodology of fibre used resulted in substantially different reference intakes (Prentice et al., 2004). Knowledge about the physiological effects of dietary fibre is primarily based on data from adults; studies with children are scarce. Therefore, the reference intakes for dietary fibre during childhood and adolescence are mostly pragmatic values expressed on a body weight, age or energy intake (EI) basis (Prentice et al., 2004). The recent US dietary fibre reference intakes (Institute of Medicine, 2002) are based on data cited for adults, which showed that at least 14 g dietary fibre per 1000 kcal reduced the risk of CHD. Multiplied by the median EI of the respective age group, dietary reference intakes (here: Adequate intakes) for children and adolescents aged 1–18 years were set by the Institute of Medicine. As it was stated that ‘individuals consuming less than the median EI of a particular (age) category need less fibre than the recommendation

Dietary fibre from infancy to adolescence U Alexy et al

910 which is based on the median EI’ (Institute of Medicine, 2002), the fibre density (i.e. g dietary fibre/1000 kcal) can be used as the virtual reference to estimate the adequacy of dietary intake. In 1993, the America Academy of Pediatrics (AAP) Committee on Nutrition recommended a dietary fibre intake of 0.5 g/kg body weight for children older than 2 years, with a maximum of 35 g/day (AAP, 1993). In 1995, the American Health Foundation (AHF) proposed a dietary fibre intake range during childhood and adolescence (42 years) between that approximately equivalent to the child’s age þ 5 g/day up to the child’s age plus 10 g/day as a safe and tolerable level (Williams et al., 1995). For infants, specific reference values for dietary fibre intake have not been provided up to now. The American Dietetic Association recommended a variety of solid plant foods for very young children, to ensure an adequate dietary fibre intake (Marlett et al., 2002). Agostoni et al. (1995) suggested a gradual increase of dietary fibre intake to 5 g/day during the second 6 months of life by introducing increasing amounts of fruits and vegetables. The few existing studies dealing with dietary fibre intake in infants, children and adolescents from industrialized countries reported intakes below the respective reference used (Nicklas et al., 1995b; Hampl et al., 1998; Decarli et al., 2000; Royo-Bordonada et al., 2003). There is particular lack of data concerning possible long-term changes in dietary habits, especially in children and adolescents of Western industrialized countries. In this report, we evaluate dietary fibre intake from infancy to adolescence against various references and describe time trends between 1990 and 2004, using data from the Dortmund Nutritional and Anthropometric Longitudinally Designed (DONALD) Study.

Subjects and methods Study design The DONALD Study is an ongoing longitudinal (open cohort) study (started in 1985) collecting detailed data on diet, growth, development and metabolism between infancy and adulthood. Details have been described elsewhere (Kroke et al., 2004). The study sample at the outset included infants, children and adolescents recruited from earlier cross-sectional studies in schools and kindergartens (nE470). After 1989, infants were recruited (E40 per annum) and followed until the age of 20 years (girls) and 23 years (boys). Study participants are recruited in the city of Dortmund and surrounding communities via personal contacts, maternity wards or paediatric practices. Healthy German babies (age 3–6 months) whose mothers and/or fathers are willing to participate in a longterm study are eligible (Kroke et al., 2004). The regular assessments (quarterly for infants, bi-annual for toddlers, else yearly) include records of dietary intake and behaviour, anthropometry, urine sampling, interviews on life-style and European Journal of Clinical Nutrition

health-related issues and a medical examination (Kroke et al., 2004). The Scientific Committee of the Research Institute of Child Nutrition has approved the study, which is exclusively observational and non-invasive. All examinations and assessments are performed with parental consent and later on with the children’s consent.

Dietary survey Parents of the children or the older subjects themselves weighed and recorded all foods and fluids consumed and recipes of home-prepared meals using electronic food scales (71 g) on 3 consecutive days. Semiquantitative recording (e.g. number of spoons, scoops) was allowed if weighing was not possible. To validate dietary recording, the reported EI to predicted basal metabolic rate (BMR) ratio was used. Basal metabolic rate was calculated using the equations of Schofield (1985), including the measured height and weight of the individuals. The mean7s.d. EI:BMR ratios of the sample were 1.570.26 (o1 year), 1.4370.25 (1–5 years), 1.4170.27 (males 6–18 years) and 1.3570.27 (females 6–18 years), and are plausible according to Torun et al. (1996).

Nutrient database Energy and nutrient intakes were calculated using our nutrient database LEBTAB, which is continuously updated by all newly recorded food items. Nutrient contents of staple foods were taken from standard nutrient tables, predominantly German (Souci et al., 2000) (48% of items) and US (18% of items) (USDA, www.nal.usda.gov). The dietary fibre content in these databases was determined by different enzymatic methods (Souci et al., 2000). Nutrient contents of commercial food products were determined either by using the product labels or by simulating recipes from the ingredients listed. Since 2003, functional fibres, that is, fibres used as food additives in various types of commercial products (Institute of Medicine, 2002),have been specified in LEBTAB. For estimation of dietary fibre in accordance with the definition of the Institute of Medicine (2002), these functional fibre ingredients were excluded here, just as fibre additives in prebiotic foods, for example, oligosaccharides. Nutrient supplements were excluded from analysis.

Statistical analysis SASs procedures (Version 8.2; Statistical Analysis System, Cary, NC, USA) were used for data analysis. Energy and nutrient values were calculated as individual means of the values of three recorded days. P-values below 0.05 were considered as significant. For infants, dietary fibre intake was displayed at 6, 9 and 12 months. Infants 3 months old were not included in the analysis, because they usually do not consume dietary

Dietary fibre from infancy to adolescence U Alexy et al

911 fibre-containing foods. For children and adolescents, records were stratified into four age groups (1.5–3-, 4–8-, 9–13- and 14–18-year olds). The latter two age groups were also classified by sex, according to the agegrouping of the US Institute of Medicine (2002). To examine the trends of total fibre intakes, a mixed linear model was used, in which the means of the data and the covariance structure, and the effect of repeated measurements were measured (PROC MIXED) (Littel et al., 1996). An exponential structure of covariance was specified to consider the correlation of repeated measurements dependent on the absolute time interval of repeated measurements within the same subject. A model was developed to analyse the influence of time (in years since 1990) and age at the time of recording (in years) on dietary fibre intake (in g/day), controlling for EI (MJ/day) and sex. The non-standardized coefficients for independent variables (b) represent the predicted change of dietary fibre intake (g/day) per unit change in the respective independent variable. For the trend analysis, records of infants and toddlers were summarized into two age groups, reflecting the typical

dietary habits of the weaning period (0.5–1 year) and the transition to the family diet (1.5–3 years). Owing to the age course of dietary fibre intake during the weaning period, a non-linear model, including age and age*age as influencing variables, was used, because this showed a better fit than the according linear model.

Results Between 1990 and 2004 a total of 7810 dietary records from 980 infants, children and adolescents (476 males, 504 females) aged 6 months to 18 years, coming from 727 families, were collected and evaluated (Table 1). Each participant collected between 1 (n ¼ 51) and X16 records (n ¼ 23). Over the study period, the mean (s.d.) age ranged from 4.8 (4.4) to 7.0 (5.3) years. Dietary fibre intake in absolute amounts (g/day) increased with age and doubled between the ages of 6 and 9 months, and once again between the ages of 1 and 9–13 years. During adolescence, the dietary fibre intake remained fairly constant, with higher intakes in boys than in girls (Table 2).

Table 1 Sample characteristicsa Age/gender groups

Number of records (N) Number of individuals (N) Age (years) Body weight (kg) Body height (cm)

Energy intake MJ/day

6 months (boys þ girls) 9 months (boys þ girls) 1 year (boys þ girls) 1.5–3 years (boys þ girls) 4–8 years (boys þ girls) 9–13 years (boys) (girls) 14–18 years (boys) (girls)

0.5 0.8 1.0 2.2 5.9

(0.4) (0.4) (0.5) (0.6) (1.4)

7.7 8.9 9.8 13.1 22.2

(0.9) (1.0) (1.1) (2.2) (5.1)

67 71 75 90 118

(2) (2) (3) (7) (10)

2.57 3.00 3.38 4.12 5.86

kcal/day

477 503 537 1554 2248

477 497 530 653 631

(0.45) 614 (0.50) 719 (0.60) 807 (0.81) 985 (1.21) 1400

(107) (119) (143) (194) (290)

809 787

221 221

10.9 (1.4) 10.8 (1.4)

40.4 (10.5) 40.0 (11.4)

149 (11) 148 (11)

8.02 (1.62) 1917 (388) 7.09 (1.44) 1692 (344)

448 447

133 125

15.8 (1.4) 15.8 (1.4)

66.1 (12.7) 60.4 (11.5)

177 (9) 168 (7)

10.07 (2.36) 2406 (564) 7.51 (1.76) 1792 (420)

a

Data are presented as mean (s.d.), if not indicated otherwise.

Table 2 Overall intake of dietary fibre in 0.5–18-year-old participants of the DONALD study 1990–2004a Age/gender groups

Dietary fibre intake g/day

6 months (boys þ girls) 9 months (boys þ girls) 1 year (boys þ girls) 1.5–3 years (boys þ girls) 4–8 years (boys þ girls) 9–13 years (boys) (girls) 14–18 years (boys) (girls)

4.45 8.88 10.19 10.48 14.52

(2.92) (2.86) (3.29) (3.44) (4.56)

g/MJ 1.73 2.97 3.06 2.60 2.52

(1.06) (0.87) (0.90) (0.79) (0.66)

g/1000 kcal 7.23 12.41 12.79 10.87 10.56

(4.44) (3.64) (3.75) (3.32) (2.78)

g/kg 0.58 1.01 1.05 0.81 0.67

(0.38) (0.33) (0.33) (0.27) (0.19)

19.47 (5.89) 17.73 (5.01)

2.47 (0.65) 2.57 (0.67)

10.35 (2.71) 10.74 (2.79)

0.50 (0.16) 0.47 (0.15)

23.85 (7.71) 20.07 (6.43)

2.41 (0.63) 2.74 (0.74)

10.10 (2.63) 11.47 (3.09)

0.37 (0.13) 0.35 (0.13)

DONALD ¼ Dortmund Nutritional and Anthropometric Longitudinally Designed. a Mean (s.d.).

European Journal of Clinical Nutrition

Dietary fibre from infancy to adolescence U Alexy et al

912 Calculated as nutrient density (g/1000 kcal), dietary fibre intake was lowest at 6 months, but increased with age and reached a maximum in the 1-year olds. During childhood and adolescence the fibre density was fairly constant, with higher intakes in girls (Table 2). Calculated as g/kg body weight, dietary fibre intake also reached a maximum between the ages of 9 months and 1 year. The following decrease continued further till adolescence. Using the study sample data of EI, body weight and age, the recommended dietary fibre intakes in g/day were calculated from the different approaches of dietary reference intakes (AAP, 1993; Williams et al., 1995; Institute of Medicine, 2002) (Figure 1). During childhood, the nutrient density-based recommended intakes of the Institute of Medicine were the highest, and showed distinct sex differences, which increased with age. The body weightbased reference intakes of the AAP were similar to the age þ 5 rule of the AHF until the age of 7 years, but showed a higher increase after the age of 8 years. Distinct sex differences were detectable soon at the age of 15 years. The age þ 5 rule resulted in a steady increase of recommended dietary fibre

40

g/day

30

intake without sex differences, and was the lowest recommended value during adolescence. On average a total of 75% of 3-day records from children X2 years complied with the ‘age þ 5 rule’ (Williams et al., 1995), with a range between 42% in 14–18-year-old females and 84% in 2–8-year olds (Table 3). Compared with the body weight-based reference (AAP, 1993),an intake of 60% of the total 3-day records was adequate, but the percentage of records with an adequate intake decreased with age and was higher in boys than in girls. Overall, only 15% of records reached the fibre density of 14 g/1000 kcal used as a basis for the reference intakes (Institute of Medicine, 2002). The percentage of records with adequate intake decreased with age, but increased in female adolescents (Table 3). Table 4 gives the trends in intake of dietary fibre (g/day). No significant time trends were found during the study period, between 1990 and 2004, except for a negative trend in 4–8-year olds and 9–13-year-old females. A significant non-linear age trend in dietary fibre intake was found in the youngest age group; the 4–8-year olds and the 9–13-year-old females showed positive age trends. The association between

Table 3 Percentage of 3-day-records with adequate intakes compared with different reference values

14 g /1000 kcal, boys ; girls 0.5 g/kg body weight, boys ; girls Age + 5, boys and girls

Age/gender groups

Reference value Age þ 5 (%)

20 10 0

0.5

1

2

4

6 8 10 Age (years)

12

14

16

18

Figure 1 Recommended values for dietary fibre intake expressed as g/day, calculated from the study sample data and three approaches of reference values expressed as per EI (Institute of Medicine, 2002), body weight (AAP, 1993) and age (Williams et al., 1995).

1–3 years (boys þ girls) 4–8 years (boys þ girls) 9–13 years (boys) (girls) 14–18 years (boys) (girls)

0.5 g/kg body 14 g/ weight (%) 1000 kcal (%)

84 84

87a 80

22 11

73 66

46 36

10 12

62 42

16 12

9 20

a

Only records of children 42 years old.

Table 4 Trends in intake of dietary fibre (g/day) in 0.5–18-year-old participants of the DONALD Study 1990–2004; results of Proc MIXEDa Age/gender groups

0.5–1 years (boys þ girls) 1.5–3 years (boys þ girls) 4–8 years (boys þ girls) 9–13 years (boys) (girls) 14–18 years (boys) (girls) a

Time

*

Age

Age age

Energy (MJ)

b

s.e.

P

b

s.e.

P

b

s.e.

P

b

s.e.

P

0.03 0.02 0.07

0.02 0.02 0.03

0.1864 0.3232 0.0107

37.86 0.29 0.49

2.62 0.11 0.06

o0.0001 0.0081 o0.0001

19.97

1.66

o0.0001

2.15 1.76 1.76

0.18 0.10 0.07

o0.0001 o0.0001 o0.0001

0.06 0.18

0.07 0.05

0.3378 0.0009

0.09 0.31

0.11 0.10

0.4160 0.0022

1.58 1.59

0.11 0.11

o0.0001 o0.0001

0.07 0.16

0.10 0.09

0.5115 0.0615

0.09 0.24

0.18 0.17

0.6240 0.1599

1.89 2.20

0.13 0.14

o0.0001 o0.0001

b ¼ non-standardized coefficients: predicted change in Y per unit change in X. DONALD ¼ Dortmund Nutritional and Anthropometric Longitudinally Designed; s.e. ¼ standard error of the coefficients.

European Journal of Clinical Nutrition

Dietary fibre from infancy to adolescence U Alexy et al

913 EI (MJ/d) and fibre intake (g/day) was significantly positive in all age groups.

Discussion Until now, there are no scientifically established bases for recommending fibre intake during infancy, childhood and adolescence. The three main current sets of recommendations for fibre intake vary somewhat from each other. Independent of the reference used, dietary habits of children and adolescents in Germany, as reflected by the results of our study, should be improved. When interpreting the percentages of subjects meeting the reference values, it has to be considered that they are based only on 3-day-records. The distribution of 3day intakes looks more wide and flat than the narrower and higher distribution of long-term intakes. Therefore, 3-day records may overestimate the proportion of subjects with inadequate intakes. The reference value proposed by the AAP is a constant value per kg body weight independent of age. However, the energy and food amount needs of children and adolescents per kg body weight decrease with age (Torun et al., 1996). To reach the recommended intakes, the fibre density of the diet would have to increase during childhood and adolescence, an assumption for which no physiological reasons are discernible. Since our data showed a widely constant fibre density during childhood and adolescence, the proportion of subjects meeting these body weight-based recommendations decreased with age. Therefore, such body weight-related reference seems to be too simple and contradictory to the general acceptance of a constant dietary composition in the family environment after the age of 2. The ‘age þ 5’ rule is easy to prescribe and easy to remember even for lay persons (Dwyer, 1995), but it was criticized as being pragmatic and without any firm physiological basis (Aggett et al., 2003). The resulting recommended dietary fibre levels are well below the two other recommendations used here (Figure 1). Therefore, compared with the age þ 5 rule, the fibre intake in our sample nearly seemed to be adequate. However, this recommendation does not consider gender differences of energy needs and food intake amounts and would identify the girls of the DONALD Study to be at a risk of low dietary fibre intake, although the actual fibre density in the diet of females was higher than in males. The ESPGAN Committee on Nutrition argued that an energy-linked reference value could lead to excess amounts in toddlers (Aggett et al., 2003). In fact, our data showed higher recommended values from the energy-based approach than from the age- or body weight-based approach. The actual dietary fibre intakes of toddlers in the DONALD Study were lower than the energy-linked reference. Belgian toddlers, aged 2–3 years, had dietary fibre intakes of 1073 g/ day, which correspond to the results of the DONALD Study (Bosscher et al., 2002). However, during the second semester of the first year of life, the dietary fibre density was even

higher than during childhood. One can assume that an increased dietary fibre density in the diet of toddlers would not result in excess dietary intakes. Therefore, a single energy-linked reference value from 1 to 18 years would be practicable. Using the recommendation of the Institute of Medicine, constricted on dietary fibre from plant food, infants during the first 6 months of life failed to get any dietary fibre, because during this period exclusive breast feeding is recommended (Institute of Medicine, 2002). However, a variety of definitions of dietary fibre exist. The ESPGHAN Committee on Nutrition (Aggett et al., 2003) defines dietary fibre as NDC. Using this definition, fructo- and galactooligosaccharides present in breast milk (Kunz et al., 2000) as well as the amount of lactose that is not absorbed and escapes into the large intestine are counted in dietary fibre. In this case, dietary fibre is mentionable soon during the pre-weaning phase in infancy (Edwards and Parrett, 2003). Whereas breast-fed infants get such NDS, formula-fed infants do not, as long as common formula products are not supplemented with thickening agents and prebiotic compounds. However, until better assessments of their metabolic and clinical effects, the ESPGHAN committee on Nutrition is advised to be cautious concerning such supplementation (Aggett et al., 2003). During weaning, dietary fibre from plant origin is also included in the diet. However, there is no theoretical reason to establish reference values and only few data on dietary fibre intake in this age group exist (Institute of Medicine, 2002). In Germany, weaning is starting with vegetables (primarily carrots), combined with potatoes, meat and plant oil, followed monthly by two cereal-containing paps (Kersting and Dulon, 2002). Therefore, in the DONALD Study the dietary fibre intakes were somewhat higher than those proposed by Agostoni et al. (1995). The reported mean dietary fibre intake of infants and toddlers from the US Feeding Infants and Toddlers Study was 6 g/day in infants 7– 11 months old and 8 g/day in toddlers 12–24 months old (Devaney et al., 2004), which was near the results of the DONALD Study. In the DONALD Study, the long-term dietary fibre intake remained constant after 1990, although macronutrients, including carbohydrates, showed significant time trends (Alexy et al., 2002). Few other studies exist that have evaluated the time trends of dietary fibre intake. They analysed a time period before this evaluation and also showed no or only a small time trend (Nicklas et al., 1995a; Saldanha, 1995). In conclusion, our data affirm inadequate dietary fibre intakes during childhood and adolescence in Germany, irrespective of the reference used for evaluation. When evaluating the different conceptions behind the dietary fibre reference intakes, we could show some limitations and pitfalls. Dietary reference intakes are based on physiological data or evidence. Therefore, our dietary survey data cannot European Journal of Clinical Nutrition

Dietary fibre from infancy to adolescence U Alexy et al

914 recommend any quantitative amount of dietary fibre. Unless scientific evidence for the origin of reference values during childhood and adolescence is available, reference intakes have to be estimated as done, for example, by the age þ 5 rule or interpolated as done by the Institute of Medicine. Our dietary survey data support the energy-based interpolation of the dietary fibre reference intake for children and adolescents from the existing physiological data of adults to calculate the absolute reference values per day. Although dietary fibre itself does not yield energy, in the diet it comes from energy-yielding foods, for example, grain, fruits and vegetables. Therefore, such an energy-based approach is notably convincing when the reference values were used to deduce food-based dietary guidelines. If the recommended dietary fibre intake varies during childhood and adolescence, different food compositions are needed to reach the fibre reference intakes, resulting in a need of different food-based dietary guidelines. For infants, only a pragmatic reference value based on fibre intakes with a reasonable diet that achieves all other nutrient references would be possible at this time.

Acknowledgements ¨ r Schule und This work was supported by the ‘Ministerium fu Weiterbildung, Wissenschaft und Forschung des Landes ¨r Nordrhein-Westfalen’ and by the ‘Bundesministerium fu Gesundheit’.

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