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Journal of the American College of Nutrition, Vol. 25, No. 2, 135-143 (2006)
Published by the American College of Nutrition

The Contribution of Ready-to-Eat Cereals to Daily Nutrient Intake and Breakfast Quality in a Mediterranean Setting

Anneke van den Boom, PhD, Lluís Serra-Majem, MD, PhD, Lourdes Ribas, MD, Joy Ngo, RD, MPH, Carmen Pérez-Rodrigo, MD, PhD, Javier Aranceta, MD, PhD and Reginald Fletcher

Community Nutrition Research Centre, University of Barcelona Science Park, Barcelona (A.v.d.B., L.S.-M., L.R., J.N.)
Department of Clinical Sciences, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria (L.S.-M.)
Community Nutrition Unit, Ayuntamiento de Bilbao, Bilbao (C.P.-R., J.A.)
SPAIN, Kellogg’s Company of Great Britain, Manchester, ENGLAND (R.F.)

Address reprint requests to: Dr. L. Serra-Majem, Community Nutrition Research Centre, Parc Cientific de Barcelona, Baldiri Reixac 4, Torre D, 08028 Barcelona, SPAIN. E-mail: nutricom{at}pcb.ub.es


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 CONCLUSIONS
 ACKNOWLEDGMENTS
 REFERENCES
 
Objectives: To examine if and how ready-to-eat cereals (RTEC) contribute to the quality of the diet of children, adolescents and young adults in a Mediterranean setting.

Methods: A random sample of 3534 subjects aged 2 to 24 years in Spain was studied. Food and nutrient intakes were determined by a 24 hour recall. RTEC consumption was assessed by a quantitative food frequency questionnaire. Additional questions on socioeconomic level and nutritional knowledge were administered. Cereal consumption was classified into non-consumers and daily intakes between 1 and 20g, 21 and 40g, and more than 40g. After excluding the underreporters the final sample consisted of 2852 individuals.

Results: About half of the population (49.8%) reported eating RTEC. Macronutrient profile improved with increasing cereal consumption. Intakes of thiamine, riboflavin and vitamin B6 increased significantly with increasing consumption of RTEC in all age-sex groups, whereas niacin and folate intake improved in almost all groups and calcium, iron and vitamin D in at least half of the groups. Except for magnesium, vitamin B12 and vitamin E in males, consumption of RTEC was significantly associated with increased coverage of the daily nutrient requirements for all micronutrients studied. Higher levels of RTEC consumption was associated with a greater consumption of dairy products, and related to better breakfast quality.

Conclusions: Level of RTEC consumption is associated with a better nutritional profile in the diets of Spanish children, adolescents and young adults and a lower risk for inadequate micronutrient intakes. RTEC consumers have better quality breakfasts, in terms of both food choices as well as energy and nutrient content.

Key words: dietary intakes, ready-to-eat cereals, breakfast, children, adolescence, Spain


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 CONCLUSIONS
 ACKNOWLEDGMENTS
 REFERENCES
 
The nutritional importance of breakfast has now been well established, both for its contribution to daily nutrient intake [14] and for its influence on cognition and mental performance [5,6]. Several of these studies have also confirmed the important contribution of ready-to-eat cereals (RTEC) to daily nutrient intake and breakfast quality [1,2,713]. However, most of these studies have been carried out in countries where the consumption of RTEC is traditionally high. In southern Europe, consumption of RTEC is a more recent phenomenon and consequently few studies have evaluated the influence of RTEC on nutrient intake and the type of breakfast in these countries. In Spain, only Ortega et al [11] have evaluated the level of RTEC consumption, but the sample was limited to Madrid and surroundings and to children between the ages of 9 and 13 years. A more representative population study was therefore needed to assess the contribution of RTEC to dietary quality in Mediterranean children, adolescents and young adults. The enKid study, a national study assessing the food habits and nutrient intake of more than 3500 individuals between 2 and 24 years in Spain, provided an excellent opportunity to investigate this issue.

MATERIALS AND METHODS
The methods have been described in detail elsewhere [1416]. In summary, a random sample of 3534 subjects aged 2 to 24 years was interviewed at home by a team of 43 specially trained dietitians. Interviews were performed throughout the year and homogeneously from Monday to Sunday in order to avoid the influence of seasonal as well as day-to-day variations. Persons with a quotient below 1.14 for the energy intake divided by Basal Energy Expenditure were considered underreporters, as established by Goldberg et al [17], and were excluded for all analyses except for description of RTEC consumption.

Interviews included a 24-hour recall, a quantitative food frequency questionnaire and a complete questionnaire about general information. The questionnaire was completed by trained dietitians who used the household measures found in the subject’s own homes to estimate volumes and portion sizes.

The 24 h recall was used to estimate food, energy and nutrient intakes. The dietitian elicited the time and place where the food was eaten and which meal it represented. Breakfast was defined as the first eating occasion involving a solid food or a beverage that occurred after waking up and before 10 a.m. during weekdays and before 11 a.m. on the weekends. A second 24-hour recall was performed in 25% of the sample to adjust for the intra-individual variability.

Food intake was converted into nutrient intake using the Spanish nutrient database from Mataix et al [18] completed with information from the French [19] and British [20] food composition tables.

The food frequency questionnaire was used to classify individuals according to their RTEC level of consumption, as most Spanish consumers do not have these cereals on a day-to-day basis. It consisted of a quantitative questionnaire with 169 food items. There were three items regarding breakfast cereal consumption, which represented cereal categories for the family, for children and for those high in fiber. In the case of affirmative responses, there were questions about the frequency (daily, weekly, monthly, and number or times consumed) and the usual portion sizes. These data were used to calculate the total daily cereal consumption, which was classified into four categories [10]: 1) Non consumers, 2) Intakes from 1–20 g/day, 3) Intakes from 21–40 g/day and 4) Intakes >40 g/day. These intakes would correspond to the following cohorts: non-consumers, consumption of breakfast cereals two to three times a week (weekly consumers), once daily (daily consumers), and more than once daily (frequent consumers).

The general questionnaire contained information on socio-economic family background, demographics, level of education, place of residence, knowledge of nutrition and healthy eating guidelines and food preferences. Socio-economic status as well as parental educational levels were categorized as low, medium or high. The population size was categorized according to the number of inhabitants (less than 10,000, 10,000 to 50,000, 50,000 to 350,000 and more than 350,000).

A breakfast score was created to evaluate the quality of breakfast. The score was based on the 24 h recall data and the scoring was as follows: one point was given if breakfast contained a dairy product, similarly, another point was added if it contained a cereal product (bread, biscuits, RTEC, etc.), and an additional one if breakfast contained fruit. Thus, a complete breakfast that included a dairy product, fruit and cereals obtained a maximum of three points.

Statistical Analysis
The data were analysed using SPSS statistical package (version 10.0). The subjects’ dietary food and nutrient intakes were examined as a function of different variables (gender, age group, socio-economic status, level of RTEC consumption). Student’s t-test was used for comparison of the means between two groups. One way analysis of variance was used for comparison between more than two groups. The chi-square statistic was computed for comparison of proportions. Log-transformed variables were used to improve normality as tested by the Kolmogorov-Smirnov test. P values <0.05 were indicators of an acceptable level of significance.

Data from the 24 h recalls were adjusted for intra-individual variability in order to accurately estimate distribution of intakes and percentage of population groups below defined cut-off points. The Reference Nutrient Intakes utilised were those elaborated by the "Centro Superior de Investigaciones Cientificas," Complutense University of Madrid [21] for the Spanish population. The threshold value for folate was modified from being 200 mcg to 400 mcg for women aged 13 to 24 years.

RESULTS
The final study sample consisted of 2852 individuals: 1346 boys and 1506 girls after excluding underreporters. The distribution by age, sex and region of the sample did not differ significantly from the Spanish population for these age groups.

About half of the population (49.8%) reported eating RTEC. 26.4% of the individuals were weekly consumers (1–20 g/day), 15.6% were daily consumers (21–40 g/day) and 7.8% were frequent consumers (more than one serving per day). Consumption was highest in the age group of 10–13 years and declined significantly in the older cohort aged 18–24 years. The consumption of RTEC increased significantly (p <0.001) with increasing socio-economic status of the family (59% of consumers in high socio-economic status and 45.1% in low socio-economic status) and parental educational level (p <0.001). Cereal consumption was also significantly higher with increasing number of inhabitants in the place of residence (57.2% of consumers in places with more than 350,000 inhabitants, and 45.7% in places with less than 10,000 inhabitants) (p ≤0.01).

According to the 24 h recall information, 66.9% of the RTEC was consumed for breakfast, 1.9% as a mid-morning snack, 5.4% at lunch time, 11.5% at the merienda (the Spanish mid-afternoon snack), 10.8% at dinner and 3.5% at any other time.

RTEC and Nutrient Intake
Table 1 gives an overview of the mean daily intakes of energy and nutrients, categorised by level of RTEC consumption. Energy intake did not differ significantly between non-consumers and RTEC consumers, except in the group of boys between 14 and 17 years, where heavy cereal consumers (>40 g/day) had a higher energy intake (2755 kcal) than non-consumers (2520 kcal) (p = 0.012). Compliance with recommended macronutrient profiles expressed as a percentage of the daily energy intake, improved significantly with increasing levels of RTEC consumption, i.e. the amount of energy provided by carbohydrates increased whereas the percentage of calories from fat and proteins decreased.


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Table 1. Mean Daily Energy and Nutrient Intake in a Spanish Population Aged 2 to 24 Years by Level of RTEC Consumption Having Excluded Underreporters1

 
In the two higher age groups, dietary fiber intake increased significantly (p <0.001) with increasing level of RTEC consumption, except for the male group aged 18–24 years. In men aged 14–17 years, non consumers had 18.5g of fiber versus 20.1g in heavy RTEC consumers. Comparing these same categories, women aged 14–17 years consumed 14.5g versus 15.5g respectively, and women aged 18–24 years 15.0g and 18.5g, respectively. In regards to sodium, no significant differences in sodium intake were found between RTEC consumers and non-consumers.

When evaluating the consumption of RTEC and micronutrient intake, it was observed that the intake of certain nutrients increased significantly (p <0.05) with increasing levels of RTEC consumption in the different age-sex groups. Table 2 shows the p-value for the average increase in nutrient intake with increasing levels of RTEC consumption by age-sex groups.


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Table 2. P-value for the Increase in Average Nutrient Intake with Increasing Level of RTEC Consumption by Age-Sex Groups (Underreporters Excluded1)

 
Intakes of thiamine, riboflavin and vitamin B6 increased significantly with increasing levels of RTEC consumption in all age-sex groups, whereas niacin and folate intake improved in almost all groups, and calcium, iron and vitamin D in at least half of the groups.

Intakes of micronutrients that are not typically added to breakfast cereals (magnesium, vitamin A, vitamin C and vitamin E) did not show any consistent association with level of RTEC consumption. This was also true for Vitamin B12, although cereals are typically fortified with this nutrient.

When comparing the micronutrients with the Spanish RNIs, we observed that the level of RTEC consumption was significantly associated with an improved likelihood of meeting daily nutrient requirements for all the micronutrients studied, including those not traditionally added to RTEC (Table 3). To estimate the risk for inadequate nutrient intake, the percentages of the population sample with intakes less than 1/3 (Table 3) were calculated. In addition, the percentage of the sample with intakes below 2/3 of the RNI was evaluated.


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Table 3. Risk of Inadequate Energy and Nutrient Intakes in Spanish Boys and Girls Aged 2 to 24 Years, Excluding Underreporters1, by Level of RTEC Consumption and Sex

 
The level of RTEC consumption is clearly associated with a reduced number of individuals having nutrient intakes below 2/3 of the RNI. No subjects had mineral intakes below 1/3 of the RNI. With respect to iron, it is important to highlight that none of the male individuals had iron intakes below 2/3 of the RNI. All individuals with iron intakes below 2/3 of the RNI were females between the ages of 10 and 24 years. However, none of them had iron intakes below 1/3 of the RNI. Among those aged 10 to 17 years, no female individual met the RNI for iron, and in the group of 18–24 years, only 1.4% had adequate intakes. As the level of RTEC consumption increases there is an accompanying decrease in the percentage of females with iron intakes below 2/3 RNI.

With respect to vitamins, no individual had intakes below 2/3 of the RNI for either thiamine or vitamin B12. Only a small proportion of the population had intakes below 2/3 of the RNI for vitamin B6 (2.7%) or vitamin C (8.1%).

However, for several vitamins the risk of inadequate intake was not negligible. With the exception of one boy in the age group of 14–17 years, none of the subjects met the RNI for vitamin D and only 4.2% of boys and 1% of girls met 2/3 of the RNI for vitamin D. Increased levels of RTEC consumption were significantly associated with a decreased risk of having vitamin D intake levels below 1/3 of the RNI (p <0.001) in the female population (those falling below 1/3 of the RNI were more numerous in the non-consumer cohort (63%) as compared to the high cereal consumers (50%)).

Referring to vitamin E, only 4.6% met the recommendations. Vitamin E intakes below 2/3 of the RNI were observed in 41.3% of the males and in 67.6% of the females. Only 0.7% of the entire population did not meet 1/3 of the RNI for vitamin E.

In the case of vitamin A, only 24% of the population met the RNI for this vitamin. Sixty-four percent of the male population and 61.7% of the females did not meet 2/3 of the RNI for this vitamin. However, only a small proportion (1.2%) had intakes below 1/3 of the RNI. Increased levels of RTEC consumption were significantly associated with a decreased risk of having vitamin A intake levels below 2/3 of the RNI in women (p <0.001).

Less than 9% of the male population had intakes of folate below 2/3 of the RNI, but 63.9% of the female population had folate intakes below 2/3 of the RNI and 10.5% had intakes below 1/3 of the RNI. Increased levels of RTEC consumption were strongly associated (p <0.001) with a decreased risk of having inadequate folate intakes at all levels studied (below 2/3 RNI, below 1/3 RNI).

No subjects had intakes above the tolerable upper intake level (UL) for any micronutrient with which RTECs are fortified and for which this level is established [33].

RTEC and Food Intake
The intake of several foods increased or decreased with increasing level of RTEC consumption. Increased level of RTEC consumption was clearly associated with a greater use of dairy products (Table 4). This was due to a high consumption of milk, especially in males, although this association was not statistically significant in all age-sex groups.


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Table 4. Mean Daily Consumption of Dairy Products by Level of RTEC Consumption and Sex (Underreporters Excluded1)

 
In males, an increased consumption of RTEC was also associated with a decreased consumption of red meat (p <0.05) as well as of alcoholic beverages (p <0.005). In females, the consumption of fruit increased with higher consumption of RTECs. In boys and girls aged 2–5 years and 6–9 years, it was observed that an increase in the level of RTEC consumption was associated with a decreased consumption of pastry, although this difference was not statistically significant.

Breakfast Quality
A linear relationship was seen between the breakfast score and increasing levels of RTEC consumption (Table 5).


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Table 5. Level of RTEC Consumption and Breakfast Score (Excluding Underreporters)1

 
The percentage of energy provided at breakfast as a percentage of total daily energy intake increased with increasing levels of RTEC consumption, both in males and in females (14.6% of the energy provided at breakfast in non consumers, 15.2% in 1 to 20 g/day consumers, 16.1% in 21 to 40 g/day consumers and 16.4% in consumers of more than 40 g/day) (p ≤0.001).


    DISCUSSION
 
In many studies RTEC are called breakfast cereals or fortified breakfast cereals. We prefer the name ready-to-eat cereals as these cereals are not necessarily eaten only for breakfast. In fact, a third of the Spanish children did not eat RTEC for breakfast but at other times of the day. Nicklas et al [22] in the Bogalusa Heart Study had already shown that a significant number of children, 42%, consumed RTEC at times other than at breakfast.

RTEC are high in unrefined carbohydrates (albeit, they may be sugar rich and thus higher in unrefined sugar) and are usually fortified with a range of micronutrients, including iron, thiamine, riboflavin, niacin, vitamin B6, folic acid, vitamin B12 and vitamin D. Several varieties are high in dietary fiber, as they contain wholegrains, bran or dried fruit.

The importance of RTEC has been increasing in the diets of Spanish children, adolescents and young adults over the last decade. As seen in this study, consumption is still higher in larger cities and higher socio-economic groups, which confirms that these types of changes generally tend to follow such patterns. Compared to other European countries, the level of RTEC consumption is still low in Spain (according to the previously shown data, about half of the Spanish population were RTEC consumers). Sommerville and O’Reagan in Ireland [8] demonstrated that 86.4% of population between 8 and 18 years were RTEC consumers and Crawley [7] in the UK found that 78.7% of males and 63.1% of females in 16–17 year old adolescents consumed RTEC.

Nutrient Intake
Observations on the level of RTEC consumption and daily energy intake are not consistent in the literature. In this study, total energy intake was not associated with the level of RTEC consumption, except in boys aged 14–17 years consuming more than 40 grams of cereal per day. Gibson and O’Sullivan [9] and Ruxton et al [23] reported that heavy cereal users had higher energy intakes, both in males and in females as compared to non-users. McNulty et al [10] showed similar findings in 12 year old children, but not in 15 year olds. Nicklas et al [22] and Ortega et al [11] reported no differences in energy intakes, but they had not subdivided their subjects according to the frequency of cereal consumption.

Several studies [4,7,9] have observed a lower total fat intake with increasing levels of RTEC consumption. In the area of Madrid, Ortega et al [11] found a significantly lower fat intake, expressed as a percentage of energy, in a sample of children between 9 and 13 years. The results shown confirmed this finding for the Spanish population (p <0.001).

In the younger age group, no difference was observed in fiber intake between RTEC consumers and non consumers. Ruxton et al [23] had similar findings in a group of Scottish schoolchildren between 7 and 8 years old. Spanish schoolchildren tended to prefer breakfast cereals not supplemented with fiber. In the older age groups, where 22.5% of them consumed adult type RTEC (including the whole-grain and bran-enriched cereals), a higher fiber intake among RTEC consumers was observed (except for the 18 to 24 year old cohort, which had a lower consumption of RTEC).

Concern has been expressed with regard to the sodium content of RTEC relative to its energy content [10,24]. However, we found no significant difference in sodium intake between RTEC consumers and non consumers, in accordance with findings from other studies [2,11]. Moreover, there is a trend towards decreasing sodium levels in RTEC contents [24].

It is troublesome to observe that such a significant part of the young Spanish population do not meet the RNI for nutrients such as vitamins A, D and E, in addition to iron and folates in the case of girls over 10 years of age. Two recent meta-analyses of nutritional studies (one in the general population [25] and the other in children aged 4 to 18 years [26]) investigating the vitamin status of different groups in the Spanish population have shown similar inadequate intakes for minerals and vitamins, although not always in the same proportion as we have found. Vitamins A, D and E were also shown to be the nutrients at risk for inadequate intakes both in males and females, and in females iron and folate as well.

Different studies have demonstrated that iron and folate intakes do not meet the increased requirements in female adolescents and young female adults [2729]. However, significantly less subjects consuming RTEC had inadequate intakes of these nutrients. Similar observations have been made by others [7,8,10,30]. Subar et al reported that RTEC was the most important source for both iron and folates in US children between 2 and 18 years [31] as well as in US adults [32].

The high Spanish RNI for vitamin D (10 mcg) for children aged 2–5 years compared to the US Adequate Intake standard of 5mcg [33] may explain why a greater number of Spanish children did not meet 1/3 of the RNI. It is doubtful that the young Spanish population is likely to have a vitamin D deficiency, as sufficient vitamin D may be produced in the skin under sunlight exposure. In the United Kingdom [34], for instance, a country with considerably less hours of sunshine than Spain, no RNI for vitamin D is set for those aged 4 to 50 years, as it is assumed that sufficient vitamin D production will take place in the body. However, attention should be given to possible risk groups (children with dark skin or infrequent sun exposure, etc.) to assure that they receive sufficient vitamin D. RTEC are fortified with vitamin D and RTEC consumers had on average higher vitamin D intakes than non consumers.

Referring to vitamin A, despite the fact that only 11.5% of the children aged 2–9 years had intakes below the RNI, those aged 10 years and older showed the poorest data, as only 0.5% of them met the RNI. This may be explained by the high Spanish RNI for vitamin A, ranging from 800–1000 mcg/day, for the age-groups between 10 and 24 years [21] compared to the British, ranging from 500–700 mcg/day [34], and US recommendations, ranging from 600–900 mcg/day [33]. Thus, this does not necessarily indicate an inadequate vitamin A status for the Spanish population. In the meta-analysis performed by Ortega et al [25], 14–65.4% of the subjects, both children and adults, had intakes below the RNI, while only 0–33.3% showed deficient blood retinol levels. Although vitamin A is not added to RTEC, vitamin A intake was significantly higher in RTEC consumers than in non consumers. This may be due in part to the higher intake of milk products among RTEC consumers.

The analysis of the two meta-analyses mentioned [25,26] showed that up to 95.4% of the subjects had intakes of vitamin E below the RNI. Ortega et al [25] demonstrated that the percentage of subjects with deficient blood indicator levels ranged from 0 to 32.6%. The low intakes found in this study, and some of the studies used in the meta-analysis, may be partially due to the lack of compositional data for vitamin E for several foods in the Spanish food composition table that was used [18].

Concern has been expressed that the use of fortified foods might lead to high intakes of certain nutrients with risks of adverse health effects or nutrient imbalances [35]. This is particularly true for nutrients such as vitamins A and D, selenium, iron, copper and zinc, where the safety margin is small [35]. But, some publications are against that concern: referring to iron, Gibson [36] recently reported that higher iron intakes of high cereal consumers were not accompanied by better iron status in British young people aged 4 to 18 years. In the Spanish population, no observation of intakes close to the Tolerable Upper Value Levels were seen for the micronutrients with which RTECs are fortified and for which levels have been established [33]. Vitamin B12 intake was, on average, more than four times the RNI, but there are no indications that this intake may imply any health risks. Concern for excessive nutrient intakes in those children consuming fortified cereals is consequently unfounded.

RTEC and Food Intake
As RTECs are traditionally consumed with milk and yoghurt, it is not surprising to find that an increased level of RTEC consumption is associated with an increased consumption of dairy products, resulting in an increased calcium intake. This observation has been made by several other authors [2,7,9,10,13].

Consumption of RTEC was further related to food choices that are in agreement with a healthy lifestyle, such as a decreased intake of red meat, alcoholic beverages and of pastry, and an increased intake of fruit. Crawley [7] in Britain and Bertrais et al [13] in France, also observed a lower alcohol intake in heavy RTEC consumers (>30g and >40g RTEC daily, respectively). Gibson [4] reported less consumption of snack foods in pre-school children with increasing levels of RTEC consumption. Frequent RTEC consumers may be inclined to eat healthier diets and have healthier lifestyles.

Breakfast Quality
Consumption of RTEC was significantly related to a better breakfast, both with respect to food choices (breakfast score) as well as to the amount of energy provided. This is in agreement with previous studies on the subject. Ortega et al [11] observed that compared to non-RTEC consumers, children who ate RTEC consumed a wider range of foods. Ruxton et al [23] and Preziosi et al [12] showed that the consumption of RTEC was directly linked to the size, and consequently to the energy content, of breakfast.


    CONCLUSIONS
 TOP
 ABSTRACT
 INTRODUCTION
 CONCLUSIONS
 ACKNOWLEDGMENTS
 REFERENCES
 
Conclusions from this study may be summarised as follows:

  1. Increasing levels of RTEC consumption are associated with an improved nutritional intake in Spanish children, adolescents and young adults.
  2. RTEC consumers have lower risks for inadequate micronutrient intake, including those nutrients that are not traditionally added to these cereals.
  3. Concern for excessive nutrient intakes in those individuals consuming fortified cereals, even in children who have smaller safety margins, is unfounded.
  4. Frequent RTEC consumers may be inclined to make healthier food choices, which results in a breakfast of better quality.


    ACKNOWLEDGMENTS
 TOP
 ABSTRACT
 INTRODUCTION
 CONCLUSIONS
 ACKNOWLEDGMENTS
 REFERENCES
 
The enKid study is a project funded by Kellogg’s España SA and Kellogg’s Company, Battle Creek, Mich., USA, via the Fundación Universitaria de Las Palmas de Gran Canaria and the Fundación para la Investigación Nutricional in Barcelona. The authors wish to express their gratitude to all people who contributed to the design, data collection and statistical analysis of the study, and to the families who participated.

Received May 17, 2004. Accepted November 14, 2005.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 CONCLUSIONS
 ACKNOWLEDGMENTS
 REFERENCES
 

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