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Research Institute of Child Nutrition (FKE), Dortmund, Germany
2To whom correspondence should be addressed. E-mail: alexy{at}fke-do.de.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • sugars • fortification • nutrient density • children • adolescents
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The nutrient density of a diet can be influenced by several factors. One is sugar in the form of added sugars, i.e., isolated mono-, di- and oligosaccharides. Diets high in added sugars are often suspected of raising EI and lowering nutrient density, as reported in adults (1
) and particularly in children and adolescents (2
–5
). Natural intrinsic sugars and added sugars are indistinguishable in chemical analysis or physiologic metabolism, but added sugars provide merely energy and no essential nutrients. Indeed, a comparison of different sources of sugars (added, extrinsic, total) and nutrient intake showed the highest association with added sugars (1
).
However, the negative association between added sugars intake and nutrient density may be counteracted by food fortification. In the present-day diet of children and adolescents fortified food, e.g., beverages, dairy, cereals, contribute considerably to the intake of vitamins and minerals in Germany (6
) and the United States (7
), but often these foods also contain added sugars. Therefore, foods that are simultaneously fortified with vitamins and minerals and sweetened with added sugars could counteract nutrient dilution.
The effects of fortification on nutrient density have not been evaluated in the dietary practices of children and adolescents. The ongoing DOrtmund Nutritional and Anthropometric Longitudinally Designed (DONALD)-Study allows such an analysis including the examination of time trends as well as age trends of dietary habits throughout the growth period.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The DONALD-Study is an ongoing mixed longitudinal cohort study collecting detailed data on diet, metabolism, growth and development from healthy subjects between infancy and adulthood (once per year for subjects older than 2 y of age). Details have been described elsewhere (6
,8
,9
). The study started in the middle of 1985 with children and adolescents of different ages participating in exclusively anthropometric studies at our institute. Since then, yearly cohorts of 
40–50 healthy infants have been enrolled. Mothers are recruited in maternity wards or are informed by other study participants.
Dietary survey.
Parents of the children or the older subjects themselves weighed and recorded all foods and fluids consumed as well as leftovers using electronic food scales (± 1 g) on 3 consecutive days. Product information from wrappers, cartons, etc. were kept and evaluated with the dietary records by our dieticians. Semiquantitative recording (e.g., number of spoons, scoops) was allowed if weighing was not possible. However, in 75% of the completed records >90% of the food items were weighed. Week days (71.4%) and weekend days (28.6%) were proportionally distributed in the sample.
To validate dietary recording, the ratio of reported EI and predicted basal metabolic rate (BMR) was used according to Goldberg et al. (10
). BMR was calculated using the equations of Schofield (11
), including measured heights and weights of the individuals. The mean EI:BMR ratios of the sample (Table 1
) were in the recommended range of plausible dietary information (between 1.28 and 1.79 for children aged 1–5 y, between 1.39 and 2.24 for boys aged 6–18 y, and between 1.30 and 2.10 for girls aged 6–18 y) according to Torun et al. (12
).
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4900 food items (60% foods, composites, and commercial products, 30% commercial infant food products, and 10% special preparations). The nutrient contents of common foods were taken from standard nutrient tables. Those of commercial food products were determined by either using the product labels or simulating recipes form the ingredients listed, including nutrient contents of fortified food. Food products were defined as fortified, if the food label indicated fortification with at least one of the following nutrients: vitamins A, E, C, thiamin, riboflavin, vitamin B-6, folate, calcium, magnesium, zinc and iron.
Added sugars were defined as all refined sugars (e.g., sucrose, maltose, lactose, glucose and dextrin) used as an ingredient in processed foods or added at home in the kitchen or at the table, as done previously (2
,13
,14
).
Statistical analysis.
SAS procedures (Version 6.12) were used for data analysis (15
). Energy, nutrient and food group intakes were calculated as individual means of the 3 recorded days. Results are presented as means ± SD. Because previous evaluations showed that the macronutrient intake of 2- to 3-y-olds differed from all groups of older children, records were stratified into two age groups (2–3 y and 4–18 y) with the latter also being classified by sex.
Because nutrient intakes depend largely on energy intake, adjustment for total energy intake was necessary. As described by Willet (16
), several approaches for total energy intake adjustment are possible; one is the calculation of nutrient densities, as used here. The percentage of energy from fortified food of total energy intake was calculated. Additionally, total energy intake was controlled for in the regression models used.
For data analysis, 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) (17
). An exponential structure of covariance was specified to consider correlations of repeated measurements dependent on the absolute time interval of repeated measurements within a subject. We tested the following two models in detail.
Model 1 was developed to predict the effect of total energy intake (in MJ/d) and the intake of fortified food [in the percentage of energy intake (E%)] on added sugars intake (in E%). The model also controlled for time trends (in years since the beginning of the DONALD-Study in 1985) and age (in years).
The equation for model 1 is:
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Model (2
) was developed to predict the effect of added sugars intake (E%), intake of fortified food (E%), and total energy intake (MJ/d) on nutrient density. The model also controlled for time trends (in years since the beginning of the DONALD-Study in 1985) and age (in years).
The equation for model 2 is:
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To compare the quantitative effects of added sugars and energy intake on nutrient densities, we also calculated the standard regression coefficients (ß1stand and ß2stand). In a third step of analysis, we tested model 2 without controlling for intake of fortified food.
The coefficients for independent variables (
or ß) represent their predicted change when the reported independent variable increased by one unit. For example, if the coefficient for energy intake in model 1 (1) was equal to 0.5, we could say that an additional energy intake of 1 MJ/d correlated with an increase in intake of added sugars by 0.5 E%. Values in the text are means ± SD.
Ethical considerations.
The DONALD-Study is exclusively observational, nonintervening, and noninvasive as approved by the International Scientific Committee of the Research Institute of Child Nutrition.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Of the 2785 different food items eaten by the study participants, 897 of them (32%) were fortified, and 501 were fortified and sweetened with added sugars (=56% of fortified food items). The nutrient most frequently used for fortification was vitamin C (590 food items), followed by thiamin, riboflavin, vitamins B-6 and E and folate (>400 food items). The minerals mostly used were calcium (181 food items) and iron (165 food items).
Overall intakes.
Table 1
shows overall intakes of energy, added sugars and fortified food.
The intake of added sugars (E%) was lowest and the intake of fortified food (E%) was highest in the youngest age group.
Overall nutrient densities and recommended nutrient densities are given in Table 2
. Recommended nutrient densities were calculated from the German Reference Nutrient Intakes (17
), which correspond in principle to the recent U.S. Dietary Reference Intakes. In general, nutrient densities in the diet of the DONALD-Study sample were higher than recommended nutrient densities for vitamins C, riboflavin, vitamin B-6, magnesium, and zinc, similar for vitamins A and E, thiamin and iron (boys), and lower for folate, calcium (girls) and iron (girls).
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Results of model 1 are shown in Table 3
. Added sugars intake was positively associated with energy intake and intake of fortified food in all age groups. Time trends were found only in the 2- to 3-y-old group. Here, added sugars intake decreased slightly but significantly. With age, added sugars intake increased in 2- to 3-y-olds and decreased in 4- to 18-y-old girls, but remained stable in 4- to 18-y-old boys.
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As shown in Tables 4
5
6
, associations between energy intake and nutrient densities were negative for most nutrients and associations with added sugars intake were always negative. In contrast, the intake of fortified food was positively associated with nutrient densities of vitamins and, with few exceptions, also of minerals. Effects of fortification exceeded the effects of added sugars intake for most nutrients (ß2stand > ß1stand).
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Nutrient densities in the examples of thiamin and calcium separated in both fortified and nonfortified food and p33 quantiles of added sugars intake is shown in Figure 1
. With increasing added sugars intake, nutrient density from nonfortified food decreased but increased from fortified food. With thiamin, a nutrient often used for fortification, the effect of fortification was greater than the nutrient dilution effect of added sugars in 2- to 3-y-olds, so that the nutrient density of the total diet was higher in children with high added sugars intakes than in those with a moderate intakes. For calcium, the positive effect of fortification on nutrient density was smaller because this nutrient is not very commonly added. Comparable effects were found for all other vitamins and minerals, depending on the amount and frequency of fortification.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The added intake of sugars in the diet of children and adolescents from the DONALD-Study (10–13 E%) was similar to the values found in a representative study in Germany (12–14 E% total sucrose in 4- to 18-y-olds) (3
) and in Denmark (14 E% added sugars in 4- to 14-y-olds) (2
). Sugar intakes in Great Britain (17.5 E% nonmilk extrinsic sugars in preschool boys, 18.2 E% in girls) (4
), and the United States (16 E% added sugars in 2- to 5-y-olds, 20 E% in 12- to 19-y-olds) (19
) were higher. All surveys have in common that sugar intake was above the former limit of 10 E% (19
).
Our results clearly showed a slight but general trend of declining nutrient densities of vitamins and minerals with increasing percentage of energy from added sugars, as found by others (2
,14
,20
,21
). This effect was greater when the influence of fortification was not considered, supporting our hypothesis of the masking of nutrient dilution by fortification.
The nutritional importance of this nutrient dilution by added sugars in the diet is controversial. Compared with the present recommendations, intakes of most nutrients were adequate in our study, independent of added sugars intake as also stated by Forshee and Storey (13
), Lyhne and Ovesen (2
), Gibson et al. (1
), and Lewis et al. (14
). Intakes of folate, calcium and iron were of borderline adequacy, but here, nutrient dilution of added sugars was only small. For folate, nutrient density decreased with a maximum of -0.33 µg/MJ if added sugars increased by 1 E%. For calcium, this value was -1.54 mg/MJ and for iron -0.02 mg/MJ. These are only minor differences from the recommended nutrient intakes (folate, 42 µg/MJ; calcium, 121 mg/MJ; and iron, 1.5 mg/MJ).
We did not examine the influence of added sugars intake on intakes of other food groups. Forshee and Storey (13
) found that individuals who consume more added sugars are predicted to eat more grains but fewer vegetables and fruits. Just these food groups confer a benefit beyond nutrients, because they contain many phytochemicals that may be beneficial to health, although they are not nutrients in the true sense of the word and not added back in fortification. This means that added sugars may not only dilute nutrients, but also nonnutrient food components.
Consumption of fortified food counteracted this nutrient dilution effect of added sugars, because positive effects of fortification of nutrients frequently used for fortification (vitamins E and C, thiamin, riboflavin and vitamin B-6) were greater than the negative effect of added sugars. Overall, fortified food provided 8% of total EI and was positively associated with added sugars intake. Another analysis of the DONALD-Study data showed a clear positive time trend of consumption of fortified food in German children and adolescents (22
). Evaluated in the percentage of new German Reference Nutrient Intakes (18
), fortification was an important source for vitamin B-6 (80%) and vitamin C, thiamin, riboflavin, and vitamin E (40–50%), in contrast to low contributions to vitamin A, folate, iron (10–20%) and calcium (5%) (23
). In the United States in 1989–1991, fortified food contributed up to 30% of nutrient intake (as the percentage of RDA) (7
). The high consumer acceptance of fortified food in the context of its association with nutrient density shows that it is necessary to consider fortification in any dietary analysis. Additionally, the positive association between fortification and nutrient density could help to improve the current borderline nutrient intakes, e.g., for vitamin E, folate, calcium and iron, which are seldom used for fortification at present.
In a market survey in Germany, we found most fortified products among the food groups beverages, sweets and cereals (24
), which are also important contributors to added sugars intake (3
). Thus, 56% of all fortified food products in Germany also contained added sugars (24
). As described by Sichert-Hellert et al. (6
) based on the DONALD-Study between 1985 and 1996, intake of added sugars from fortified food (percentage of total intake) increased disproportionately to EI (percentage of total intake). Obviously, fortification is used as a marketing instrument by the food industry to valorize nutritionally unfavorable, high-sugar products.
Although consumption of fortified food increased during the last decade (6
), nutrient densities remained almost stable in our sample over time. Even for the nutrient used most often in fortification, vitamin C, we found only a small and not significant increase during the study. Other heterogeneous changes in food selection seem to mask the effect of fortification on nutrient density over time.
We found a general negative association between energy intake and nutrient density. Obviously, children and adolescents with high-energy intakes consumed higher proportions of low nutrient-dense foods. This conclusion is supported by the positive relationship between added sugars intake and energy intake, as found by others (1
,20
). However, high intake of sugars is negatively associated with indexes of obesity (2
). Therefore, Gibson (1
) concluded that persons who consume diets high in sugars tend to have a more active lifestyle and, therefore, high-energy intakes.
Age trends of nutrient densities were heterogeneous in our analysis. In 2- to 3-y-old children, negative trends were obvious for riboflavin and calcium, pointing to a reduction of the consumption of milk and dairy products in this age group. In the older age groups, nutrient densities increased in general with age, but this was not significant for all nutrients. The overall positive age effects were higher in girls than in boys, indicating a tendency to more healthy dietary habits in adolescent girls.
Some limitations of this study should be considered in interpreting these findings. First, the DONALD-study sample is not representative; upper social class families are overrepresented (8
). However, several evaluations showed no or only minor differences in dietary habits in our sample compared with the previous German National Food Consumption Survey (8
,9
,26
–29
). Also, time trends are comparable, e.g., to findings of the MONICA-Study in Germany (30
).
Second, potential underreporters were not excluded from analysis. In a longitudinally designed study such as the DONALD-Study, direct estimation of underreporting, e.g., by doubly labeled water is not feasible. By indirect identification of underreporting, e.g., with EI:BMR ratio cutoffs, as suggested by Goldberg (10
), a distinction between real underreporters and those with a habitual low energy intake during the recording period is not possible. After excluding 5% of the nonplausible records from 4- to 18-y-old females (EI:BMR below cutoffs recalculated for children and adolescents by Sichert et al. (31
), results were very similar to those of the total sample (data not shown).
Third, our database does not distinguish between the nutrient content of food before fortification and fortification per se. Therefore, the effects of fortification are slightly overestimated.
In summary, the effects of energy intake (negative) and fortification (positive) on nutrient densities were more important than the effects of added sugars intake (negative), time and age (heterogeneous). A significant effect on nutrition of high added sugars intakes can not be proven by our data, as found by others (13
,21
). As we showed in our analysis, this was partly due to fortification, which had a clear positive effect on nutritional quality. However, the extent of food fortification has not been sufficient to raise nutrient densities considerably during the last 17 y. The impact of fortification has to be considered in dietary analyses. Therefore, it is necessary to include the nutrient contents of fortified products in nutrient databases.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: BMR, basal metabolic rate; DONALD, Dortmund Nutritional and Anthropometric Longitudinally Designed; E%, percentage of energy intake; EI, energy intake.
Manuscript received 20 March 2002. Initial review completed 12 April 2002. Revision accepted 17 May 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Gibson, S. A. (1997) Do diets high in sugars compromise micronutrient intakes?. J. Hum. Nutr. Diet 10:125-133.
2. Lyhne, N. & Ovesen, L. (1999) Added sugars and nutrient density in the diet of Danish children. Scand. J. Nutr. 43:4-7.
3. Linseisen, J., Gedrich, K., Karg, G. & Wolfram, G. (1998) Sucrose intake in Germany. Z. Ernahrungswiss. 37:303-314.[Medline]
4. Gibson, S. A. (1997) Non-milk extrinsic sugars in the diets of pre-school children: association with intakes of micronutrients, energy, fat and NSP. Br. J. Nutr. 78:367-378.[Medline]
5. Rugg-Gunn, A. J., Hackett, A. F., Jenkins, G. N. & Appleton, D.R. (1991) Empty calories? Nutrient intake in relation to sugar intake in English adolescents. J. Hum. Nutr. Diet 4:101-111.
6. Sichert-Hellert, W., Kersting, M., Alexy, U. & Manz, F. (2000) Ten-year trends in vitamin and mineral intake from fortified food in German children and adolescents. Eur. J. Clin. Nutr. 54:81-86.[Medline]
7. Berner, L. A., Clydesdale, F. M. & Douglass, J. S. (2001) Fortification contributed greatly to vitamin and mineral intakes in the United States, 1989–1991. J. Nutr. 131:2177-2183.
8. Kersting, M., Sichert-Hellert, W., Lausen, B., Alexy, U., Manz, F. & Schöch, G. (1998) Energy intake of 1- to 18-year-old German children and adolescents. Z. Ernahrungswiss. 37:47-55.[Medline]
9. Alexy, U., Kersting, M., Sichert-Hellert, W., Manz, F. & Schöch, G. (1998) Energy intake and growth of 3- to 36-month-old German infants and children. Ann. Nutr. Metab. 42:68-74.[Medline]
10. Goldberg, G. R., Black, A. E, Jebb, S. A., Cole, T. J., Murgatroyd, P. R., Coward, W. A. & Prentice, A. M. (1991) Critical evaluation of energy intake data using fundamental principles of energy physiology: derivation of cut-off limits to identify under-recording. Eur. J. Clin. Nutr. 45:569-581.[Medline]
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13. Forshee, R. A. & Storey, M. L. (2001) The role of added sugars in the diet quality of children and adolescents. J. Am. Coll. Nutr. 20:32-43.
14. Lewis, C. J., Park, Y. K., Dexter, P. B. & Yetley, E. A. (1992) Nutrient intakes and body weights of persons consuming high and moderate levels of added sugars. J. Am. Diet. Assoc. 92:708-713.[Medline]
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17. Littell, R. C., Milliken, G. A., Stroup, W. W. & Wolfinger, R. D. (1996) SAS System for Mixed Models 1996 SAS Institute Inc Cary, NC. .
18. Deutsche Gesellschaft für Ernährung (DGE) (2000) Referenzwerte für die Nährstoffzufuhr 2000 Umschau/Braus Frankfurt, Germany. .
19. Krebs-Smith, S. M. (2001) Choose beverages and foods to moderate your intake of sugars: measurement requires quantification. J. Nutr. 31:527S-535S.
20. Bowman, S. A. (1999) Diets of individuals based on energy intakes from added sugars. Fam. Econ. Nutr. Rev. 12:31-38.
21. Gibney, M., Sigman-Grant, M., Stanton, J. L. & Keast, D. R. (1995) Consumption of sugars. Am. J. Clin. Nutr. 62(Suppl.):178S-193S.
22. Sichert-Hellert, W., Kersting, M. & Schöch, G. (1999) Consumption of fortified food between 1985 and 1996 in 2- to 14-year-old German children and adolescents. Int. J. Food Sci. Nutr. 50:65-72.[Medline]
23. Sichert-Hellert, W., Kersting, M. & Manz, F. (2001) Changes in time-trends of nutrient intake from fortified and non-fortified food in German children and adolescents: 15 year results of the DONALD study. Eur. J. Nutr. 40:49-55.[Medline]
24. Kersting, M., Hansen, C. & Schöch, G. (1995) Survey of the present-day supply of fortified food products in Germany. Z. Ernahrungswiss. 34:253-260.[Medline]
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26. Kersting, M., Alexy, U. & Sichert-Hellert, W. (2000) Vitamin intake of 1- to 18-year-old German children and adolescents in the light of various recommendations. Int. J. Vitam. Nutr. Res. 70:48-53.[Medline]
27. Alexy, U., Kersting, M., Sichert-Hellert, W., Manz, F. & Schöch, G. (1999) Macronutrient intake of 3- to 36-month-old German infants and children: results of the DONALD Study. Ann. Nutr. Metab. 43:14-22.[Medline]
28. Alexy, U., Kersting, M., Sichert-Hellert, W., Manz, F. & Schöch, G. (1999) Vitamin intake of 3- to 36-month-old German infants and children: results of the DONALD-Study. Int. J. Vitam. Nutr. Res. 69:285-291.[Medline]
29. Kersting, M., Sichert-Hellert, W., Alexy, U., Manz, F. & Schöch, G. (1998) Macronutrient intake of 1- to 18-year-old German children and adolescents. Z. Ernahrungswiss. 37:252-259.[Medline]
30. Alexy, U., Sichert-Hellert, W. & Kersting, M. (2002) 15-year time trends in energy and macronutrient intake in German children and adolescents: results of the DONALD Study. Br. J. Nutr. 87:595-604.[Medline]
31. Sichert-Hellert, W., Kersting, M. & Schöch, G. (1998) Underreporting of energy intake in 1- to 18-year-old German children and adolescents. Z. Ernahrungswiss. 37:242-251.[Medline]
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