REVISIÓN

 

B-Vitamin status and intake in European adolescents. A review of the literature

Estado vitamínico e ingesta de vitaminas en adolescentes europeos. Revisión bibliográfica

 

 

J. Al-Tahan¹, M. González-Gross^1,2 and K. Pietrzik¹

¹Institut für Ernährungs- und Lebensmittelwissenschaften. Fachgebiet Humanernährung. Rheinische Friedrich-Wilhelms Universität. Germany.
²Facultad de Ciencias de la Actividad Física y del Deporte. Universidad Politécnica de Madrid. Spain.

Dirección para correspondencia

 

 

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ABSTRACT

Background: National and international recommendations for the intake of B vitamins in adolescents consist of estimates and extrapolations from adult values. Due to increasing growth and therefore relatively high energy and nutrient requirements adolescents are a vulnerable group from the nutritional point of view. In addition, a deficient intake of several B vitamins is strongly connected with the development of cancer, neural tube defects and cardiovascular diseases.
Objective: The aim of this work is to assess dietary intake and status of B vitamins and homocysteine of European adolescents on the basis of published data.
Methods: The database Medline (www.ncvi.nlm.nih.gov) was searched for terms like “vitamin B”, “homocysteine”, “Europe”, etc. Studies published between June 1980 and December 2004 were analysed for this review. Results of the intake of B vitamins were compared with the EAR or AI, respectively, as recommended by the U.S. Institute of Medicine. Due to lacking reference values for adolescents results of blood status as well as homocysteine were compared to different thresholds for adults.
Results: Considering the limitations of the comparability between the reviewed studies e.g. by different methodologies, sample size, age groups, the average intake of B vitamins surpassed the EAR and AI. Boys were better supplied with B vitamins than girls. The intake decreased with increasing age in both genders. A possible deficiency of folate was noticed and girls in particular seemed to be more at risk. Clear regional tendencies for the vitamin intake could not be observed. Results of vitamin B₆, B₁₂, folate in blood, and homocysteine were levelled in-between the thresholds. Though the great standard deviation of folate increased the probability of a deficient supply in parts of the population.
Conclusions: European girls seem to be at risk of folate deficiency. Supplements and fortified food were not taken into consideration by most of the published studies which additionally distorts the real intake. Standardized methods of dietary surveys and reference values for B vitamins as well as homocysteine still must be established. Hence, further investigations are of great relevance.

Key words: B-Vitamins. Homocysteine. Adolescents. Europe. Review

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RESUMEN

Antecedentes: Las recomendaciones, tanto nacionales como internacionales, sobre el consumo de vitamina B por adolescentes, se basan en valoraciones y extrapolaciones de datos de adultos. Los adolescentes debido a su crecimiento y desarrollo, y, por ello, a la necesidad relativamente alta de energía y nutrientes, son desde el punto de vista de la nutrición un grupo vulnerable. Además, una insuficiente ingesta de varias vitaminas B se relaciona con el desarrollo de cáncer, defectos del tubo neural y enfermedades cardiovasculares.
Objetivo: El objetivo de este trabajo es valorar el estado vitamínico y de homocisteina y la ingesta de vitaminas B en adolescentes europeos, basándose en datos publicados.
Método: La base de datos Medline (www.ncvi.nlm.nih.gov), se analizó en función de términos tales como “Vitamina B” “Homocisteina”, “Europa”…, etc. Para esta revisión se analizaron estudios publicados entre junio de 1980 y diciembre de 2004. Los resultados de ingesta de vitamina B se compararon, respectivamente, con los de EAR y AI, según recomendación del Instituto de Medicina de EEUU. Debido a las lagunas de valores de referencia para adolescentes, los resultados se compararon con los diferentes umbrales para adultos.
Resultados: Considerando las limitaciones de la comparación en la revisión de estudios, por ejemplo: diferentes metodologías, tamaño de muestras, grupos de edad, etc., la media de ingesta de vitamina B sobrepasa a la de EAR y AI. Los chicos están mejor proveídos de vitamina B que las chicas. La ingesta decrecía con la edad en ambos géneros. Se apreciaba una posible deficiencia de fólico y las chicas, en particular, parecían padecer más riesgos. No se observaron claras tendencias regionales en la ingesta de vitaminas. Los niveles de vitaminas B₆ y B₁₂, fólico y homocisteina en sangre se encontraron dentro de los valores de referencia. No obstante, la enorme desviación estándar de fólico incrementaba la posibilidad de un deficiente consumo en parte de la población.
Conclusión: Las chicas europeas parecen estar a riesgo de deficiencia de fólico. Los suplementos y alimentos enriquecidos no fueron considerados en la mayoría de los estudios publicados, lo cual desvirtuaba la ingesta real.Todavía se deben establecer métodos estandarizados de registro dietético y valores de referencia, tanto para vitaminas del grupo B como para homocisteina. Por lo tanto, son necesarias investigaciones futuras.

Palabras clave: Vitamina B. Homocisteina. Adolescentes. Europa. Revisión.

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Introduction

Adolescence is characterized by relatively high energy and nutrient requirements compared to remaining life stages on the one hand and a peculiar lifestyle and dietary habits on the other hand. Due to increasing growth, change of body composition and lack of interest in nutrition adolescents are a vulnerable group from the nutritional point of view. Irregular meals, high consumption of products rich in sugar and fat may lead to nutritional deficits^1,2. According to Rolland-Cachera et al.³, the possibility of good nutrition is continuously improving in Western European countries whereas the nutritional intake and quality is decreasing, propitiating the prevalence of nutrition-related diseases. During adolescence eating habits and lifestyle factors are mostly established. Increasing evidence demonstrates that the risk factors for the most prevalent chronic diseases start to implement at this early phase^4-6. Additionally, recent studies confirm former data referring to the connection between diet quality and cognitive development^{7, 8}, attention, intellectual⁹ and physical¹⁰ performance.

B vitamins consist of a group of eight vitamins. Generally, B vitamins are involved in carbohydrate, protein and fat metabolism. Especially vitamin B₆, B₁₂ and folic acid contribute to healthy growth and development due to their important role in cell formation. A deficiency of B vitamins is linked to several diseases, such as neural tube defects, cardiovascular diseases and cancer^11-13. The vitamin B status of European adolescents is not well known. It is very recent that research has got interest in studying this population group. May be the idiosyncrasy of the adolescent population which makes it difficult to analyze correctly their nutritional status^{14, 15} has contributed to this fact. Therefore, good and evidence-based information on nutritional requirements of healthy children and adolescents in Europe is scarce.

Furthermore, the comparability of available data on dietary intakes and nutritional status in populations of adolescents in Europe bears plenty of difficulties as recently stated by Lambert et al.¹⁶. This is mainly due to the lack of consensus on methodological approaches used. In their systematic review of surveys of dietary intake and status in children and adolescents conducted in Europe, Lambert et al.⁸ analyzed seventy-nine surveys from 23 countries. From them, data on energy, protein, fats, carbohydrates, alcohol, vitamins, minerals and trace elements were collected and tabulated. Data on energy, protein, total fat and carbohydrate were given in a large number of surveys, but information was very limited for some micronutrients. The aim of the present review is to complement the review done by Lambert et al. with a more in-depth analysis of vitamin B status of European adolescents. Therefore, we have searched for additional studies not included in their review. Furthermore, reviewed studies do not include all B vitamins, but especially focus on thiamin, riboflavin, pyridoxin, cobalamin and folic acid status. Biotin, niacin and pantothenates are analyzed less frequently. Homocysteine (tHcy), a product of methionin metabolism, is strongly connected with folic acid, cobalamin and pyridoxin status and is regarded to be a good indicator for vitamin status (vitamin B₆, B₁₂, and folate). So far, there exist no reference values for tHcy status in children and adolescents. As an independent risk factor for cardiovascular diseases tHcy is also dealt with in this paper.

 

Material and Methods

Studies evaluating the intake of B vitamins and blood values of B vitamins and tHcy in adolescents of European countries were included in this review. Adolescence is defined as a period of young persons in the process of evolving from a child into an adult, i.e. roughly between the ages of thirteen and seventeen¹⁷. However, cut-off points vary in different articles so that data from younger and older persons had to be included. Due to the scarcity of available data all surveys that had been found were used. The database Medline (www.ncvi.nlm.nih.gov) was searched for studies published between June 1980 and December 2004. Terms like “adolescents”, “vitamin B”, “homocysteine”, “European”, names of European countries and technical terms of the different B vitamins were entered as well as combinations out of these terms. In addition, references of relevant articles were viewed for further information.

Intake data of B vitamins have been compared to the Estimated Average Requirements (EAR) and the Adequate Intakes (AI) established by the Institute of Medicine¹⁸ (table I). As stated by the US Institute of Medicine, EAR and Recommended Dietary Allowances (RDA) for thiamin, riboflavin, vitamin B₆, folates and vitamin B₁₂ were extrapolated from adult values. For biotin and pantothenates, as data were too sparse to set an EAR, an AI was developed. The method is explained elsewhere¹⁸. The EAR is the value within the Dietary Reference Intakes recommended to be used in order to estimate the prevalence of inadequate nutrient intake of a life stage or gender group¹⁹. For those nutrients without an EAR, the AI should be used for analysis.

Lacking reference values for adolescents obliged us to compare blood values with thresholds for adults in order to assess vitamin deficiency (table II). Different blood reference values had been investigated by Schrijver²⁰. The reference value for the biomarker methylmalonic acid (MMA) is adapted from Klee and Thomas^{21, 22}. Elevated MMA values (> 0.4 μmol/L) may indicate a deficiency of vitamin B₁₂ for adults. According to Bässler et al.¹² tHcy > 10 μmol/L correlates with a higher risk for cardiovascular diseases. The upper borderline of tHcy is 10-17 μmol/L in accordance with Kasper [23].

 

 

Results

With the method explained above 83 studies were found including 14 review articles. Sixty-nine articles gave detailed information which is shown in the tables III-VII. Thirty-six studies of these 68 articles were cross-sectionally designed, 15 were case-control studies, eight were cohort studies and nine were review articles. Five studies were found comprising a sample size of less than 50 persons. There were nine studies between 50-100, 22 studies between 100 and 500, 11 studies between 500 and 1000 and 11 with more than 1000 participants. One study did not state the sample size.

Looking at the countries where the studies were carried through, 11 of them took place in the United Kingdom (UK), eight in Spain (ESP) and Germany (GER) each, five in Poland (POL), four in the Netherlands (NL) and Norway (NW) each, three in Sweden (SW), Austria (A), Italy (IT), Greece (GR), France (F) and in the Czech Republic (CZ) each, one in Belgium (B), Switzerland (CH), Denmark (DEN), Estonia (EST) and in the Slovak Republic (SLOVAK) each.

In an attempt to illustrate and to compare reviewed data, Figure 1 depicts the mean B vitamin intakes of adolescents in several European countries. Of all data available from one country, the average intake was calculated by adding primarily the arithmetic means and dividing by the number of studies conducted in one country. When not applicable weighed and geometric mean, and median were included in this calculation instead of the arithmetic mean. Results are shown in a falling order from the country with the highest to the country with the lowest intakes. Clear geographical tendencies can not be seen. Intakes of vitamin B₁₂ and folates are higher in Southern Europe (Spain, Portugal, France) and Denmark and lower in the United Kingdom. Remarkable is that Nordic countries as Sweden, Denmark, Norway and Eastern Europe (Slovakia and Estonia) are represented with highest intakes especially for riboflavin and niacin intakes. Portugal, Czech Republic, Denmark and Germany have the lowest intakes for these vitamins. The distribution of the remaining vitamins is too inconsistent to give evidence. All in all, these data have to be taken with caution as they come from different studies which used different methodologies. These data may be not representative for a country.

In the reviewed studies, the focus was set on either biochemical methods (33 studies) or assessment of dietary intake (27 studies). The applied methods subdivide into prospective methods as seven-day weighed dietary records (7 studies), seven-day weighed dietary records with duplicate diets (one study), three-day dietary records (5 studies), four-day estimated food diary (one study) and retrospective methods such as diet history (5 studies), seven-day diet history (one study), 24- hour recall (10 studies), 48-hour recall (one study), food frequency questionnaire (12 studies), not further explained questionnaire (3 studies) and interview (2 studies). The biochemical methods divide into blood samples (32 studies) and 24-hour urine (one study). A combination of biochemical and dietary intake methods was applied in 11 studies. However, studies working at dietary intake often used combined methods e.g. 24-hour recall and food frequency questionnaire.

Those who compared their results of dietary intake with any reference data preferred national recommendations. Only in one review article²⁴ the EAR were chosen as reference values for the population.

All studies analyzed data of both genders except for Van Poppel et al.²⁵, Cruz¹ and Kafatos et al.²⁶. The study carried out by Van Poppel et al.²⁵ was performed only on males as part of the Dutch Nutrition Surveillance System. Cardiovascular risk factors, hematological, iron and vitamin status as well as food consumption by means of 24-hour recall were assessed in 126 boys. Kafatos et al.²⁶ investigated three composite Cretan diets of which one diet is representative of 12-year old boys by means of a seven-day weighed dietary record, chemical analyzes and the Greek food database.

 

Dietary intake of B vitamins

Tables III, IV and V summarize the intakes of B vitamins by increasing age groups. Except for Decarli et al.⁵, all studies show a higher vitamin intake in boys than in girls. Bergström et al.²⁷ and Droese et al.²⁸ explained this by the higher amount of food that boys eat and observed the same nutrient density for boys and girls. Decarli et al.⁵ carried out a dietary survey by the 3-day dietary record technique in the area of the Canton of Vaud, Switzerland. Mean total intakes of vitamin B₁₂ and folates of boys and girls were the same. In contrast, the boys’ intakes of B₁, B₆, niacin and especially B₂ and pantothenates were significantly higher than the girls’. As stated by these authors, nutrient intake increases with age, due to the higher amount of food that is consumed by a growing subject. However nutrient density remains the same or decreases with increasing age.

 

Supplementation and fortified food

The minority of the analysed studies aimed to detect the use of vitamin supplements. In Norway, Bjorke Monsen et al.²⁹ identified 17% of the total study population as daily users of vitamin supplements that contained cobalamin and/ or folate. Fifty-six percent of the supplements used contained both vitamins, and this percentage was equally distributed among the age groups 1-10, 10-15 and 15-19 years. In contrast, in Belgium De Laet et al.³⁰ mentioned that 2.6% of the 10-14-year-old and 4.6% of the 15-19-year-old sample regularly took vitamin supplements containing folate, vitamin B₆ or vitamin B₁₂. Serum concentrations of folate and vitamin B₁₂ were comparable with children not taking any supplements. In a case-control study dealing with dietary intake of young vegans and omnivores in Sweden³¹, omnivores used dietary supplements less frequently than vegans (43% compared with 87%). Sex differences could not be observed.

In Germany, Sichert-Hellert et al.³² found a significant rise in intakes of fortified nutrients with time. Between 1987-1995, the intake of vitamin B₁, B₂, B₆ and niacin from fortified food rose from 8-19% to 20-32%. In contrast, folate intake from fortified food increased more slightly from 19% to 29%.

High cereal eaters comprise a special subgroup of adolescents. Due to the fortified breakfast cereals they have a higher intake of B vitamins. Cereals provide 5% of total energy for girls, but 18% of folate, thiamin and riboflavin, 15% of B₆ and 13% of niacin³³. Articles working on Ready-To-Eat-Cereals (RTEC) show similar results^{34, 35}.

 

B-Vitamin status

Table VI depicts all studies dealing with B vitamin status. Detailed information mainly is given on serum folate, serum vitamin B₆ and B₁₂. Other parameters like red blood cell (RBC) folate, methyl-malonic acid (MMA), pyridoxalphosphate (PLP) and pyridoxic acid (PA) are mentioned in some studies. No sex differences were observed except for Marktl et al.³⁶ in Viennese children. In their study, boys were better supplied with thiamine and riboflavin than girls, but not with pyridoxine. The authors also pointed out the correlation of vitamin status and socio-economic level. Generally, a negative correlation between folate, B₁₂ and age can be seen. Bjorke Monsen et al.²⁹ described a maximum concentration of serum cobalamin at years ~3-7. Afterwards, there is a gradual decrease towards the concentration observed in adults. RBC folate showed a stable median concentration of ~220 nmol/L.

 

Homocysteine

Table VII shows several studies dealing with tHcy. The majority of the revised studies report an agedependant tHcy status. De Laet et al. and Tonstad et al.^{30, 37} called the results in younger subjects as ~50% of the values detected in adults. Some authors additionally observed inverse relationships between tHcy and blood indices of folate and vitamin B₁₂ ^{29, 38, 39}. Bates et al.⁴⁰ also found negative correlations with tHcy and vitamin B₆ as well as seasonal variations of tHcy with an unexpected minimum of tHcy in winter.

Gender differences are reported by some authors but not by all^{29, 41}. Some of the revised studies revealed significantly higher tHcy concentrations in boys than in girls. Sex differences enhanced during and after puberty ⁴². Kosch et al.⁴³ spoke of a tendency towards two age dependant peaks during infancy and during puberty (9,0 μmol/L).

tHcy positively correlated with sugar intake in one study³⁷. Additionally, tHcy concentrations were elevated in obese adolescents taking part in a weight-reduction program. The determining factor was the lean body mass⁴⁴. A link between tHcy and creatinine was mentioned in four studies^{37, 39, 45, 46}.

Few studies work at the influence of methyl-tetrahydrofolate-reductase (MTHFR) genotype on tHcy concentration. Raslova et al.⁴⁷, Gallistl et al.³⁹ and Kosch et al.⁴³ analyzed the 677 C → T MTHFR mutation. However, none of the authors found an association between tHcy and the 677 C →T MTHFR mutation. In contrast, Mainou Cid et al.³⁸ revealed a higher tHcy concentration in 80% of the children (of parents with cardiovascular diseases (CVD)) with the T/T genotype. Suboptimal B vitamin levels were also associated.

 

Discussion

Before comparing and assessing the viewed results, several difficulties should be mentioned. Generally, in order to get an idea of a population’s nutrient supply further statistical tools e. g. mean, standard deviation, median and percentiles are needed. The majority of the revised studies only published mean and standard deviation. Additionally, as EARs are developed by medians, the correct assessment of the dietary results is only possible by using the median. Furthermore, it is important to consider the distribution of the nutrient supply. If the population’s nutrient supply is normally distributed median ± 2SD describes the normal intake values of a healthy and well-nourished group. The 2.5^th percentile (EAR -2SD) represents the minimal requirement of a specific nutrient. Therefore, the dimensions of undernourishment are shown by the 2.5^th percentile. The median of a population’s intake might be higher than the EAR despite a larger group of individuals whose intake is below the 2.5^th percentile. In this paper, means have been used to compare results instead of medians due to the lacking information.

For a comparable study it is also necessary to have both identical methods of measurement and identical cut-off points. Furthermore, age groups should cope with those of recommended intakes (9-13 and 14-18 years). Observing the published results, chosen age ranges are quite random and make comparison even more difficult. Another problem, already recognized by many authors, are the food composition databases. For example, Kersting et al.⁴⁸ evaluated the vitamin intake of 1- to 18-year-old children participating in the DONALD-Study (Dortmund Nutritional and Anthropometric Longitudinally Designed Study) with the food database LEBTAB. Other countries used different food databases e.g. the food data bank of the Swedish Food Administration²⁷, the French food composition Table 5 or McCance & Widdowson´s food tables⁴⁹. Different food databases reduce the comparability between European countries. Even within a country there are sometimes different food databases that make comparability even worse⁵⁰. Subsequently, standardized food databases are also needed. However, modified parts that reflect a country’s dietary custom could be useful. As objectives vary between the distinct scientific groups different priorities are set up and eventually different methods of measurement are used. A European multicenter-study like the recently started HELENAStudy (Healthy Lifestyle in Europe by Nutrition in Adolescence) including homogeneous objectives, one central planning and standardized implementation may solve this problem in many aspects¹⁵.

The combination of biochemical methods and dietary intake assessment leads to more accurate data about the nutritional status of human beings. However, the selection of methods depends on the vitamin and on the practicability. In the case of folate the ideal method would be a combination of intake data, RBC folate, plasma folate and tHcy concentration²⁴. Folate intake data on its own are skewed due to the immense variability (30-90%) in losses during preparation. As a water soluble and heat sensible vitamin folate can be easily washed out and destroyed by cooking^{12, 51}. Bates et al.⁵² explained that on the basis of plasma PLP levels, very few of the young people had poor vitamin B₆ status: only 0.5% on the basis of a 20 nmol/L cut-off or 6% on the basis of a 30 nmol/L cut-off. In contrast, around 54% had a poor status on the basis of a cut-off of 1.80 for erythrocyte aspartate aminotransferase activation coefficient (EAATAC). However, the authors admitted that the latter indicator could be very methoddependent and may not be appropriate for their study. The commonly used parameter serum B₁₂ is imprecise for the assessment of vitamin B₁₂. 50% of the elderly population show biochemical alterations (holo TC, MMA) despite of serum B₁₂ values in normal ranges. More accurate but also more expensive are the parameters that test the metabolic active part of holo-transcobalamin and methylmalonic acid^53-55.

Mean dietary intake of B vitamins except folate mostly exceeds the EAR and AI in both, age groups and genders. Exceptions have been found in articles done by Southon et al.⁵⁶, Decarli et al.⁵ and Kersting et al.⁴⁸. In the DONALD study, the age group 10-11 shows niacin intakes lower than the EAR. The risk of a deficient niacin intake is relatively high. Applying the AIs of the younger age group (9-13 years) for biotin, results of Southon et al. indicate an inadequate intake. The prevalence of deficient biotin intake is more obvious for girls than for boys. Decarli et al.⁵ also take two age groups together. Results for pantothenic acid intake are lower than the AI of the younger age group (4mg/d). So, a suboptimal intake of pantothenic acid is even more legible for the older adolescents. Nearly every viewed study shows a high prevalence of suboptimal folate intake. In doing so, girls are more at risk for folate deficiency than boys due to the smaller amount of food they eat. In the study conducted by Serra Majem et al.⁵⁷, the analyzed population aged 6-24 years was classified according to the score obtained in the KIDMED test. This test was developed by the same authors and analyzes the compliance to the Mediterranean Diet. It is remarkable that females of the age group 15-24 years had all suboptimal intakes of folate (< 2/3 RNI). The previous reference values for folate (200μg/d) were elaborated by the Nutrition Department in 1994. Considering that the updated recommendations were doubled to 400μg/d folate supply must have been even worse for this age group. McNulty et al.⁵⁸ reported the micronutrient intake of schoolchildren from Northern Ireland. Data were collected within the scope of a larger study of coronary risk factors. Using the diet history method during an interview in combination with a food photographic atlas dietary intake data were obtained. The results of folate intake were the lowest of all studies, the medians lay 50% to 66% below the EAR. There is only one study carried out by Deheeger et al.⁵⁹ where the folate intake exceeds the EAR in all age groups as well as in both gender groups. Fortified food and especially RTEC clearly make a contribution to the improvement of the vitamin B status. However, before giving any recommendations for the intake of supplements or fortified food, it is necessary to find out the present-day status of B vitamins in healthy adolescents. Observations made in this work concerning geographical tendencies agree with the general statement of the article done by Lambert et al.¹⁶. Clear regional trends can not be seen. Furthermore, in this work countries with highest or lowest intakes, respectively, differ from those countries mentioned in Lambert’s article.

Results of serum vitamin B₁₂, serum total vitamin B₆ and PLP all exceed the threshold for adults. Only one study investigated MMA²⁹. Results (0.17 and 0.14 μmol/L) are lower than 0.4 μmol/L indicating that there is no sign for an impaired vitamin B₁₂ status. Apart from two studies^{29, 60} results of serum folate exceed the reference values for blood. This is not contradictory to the results of folate intake. Despite a suboptimal nutrient intake normal biochemical parameters like serum folate are feasible. Regarding the standard deviations and lower ranges, 44% of these values are in-between the reference values or below. There is only one study that incorporated RBC folate⁶¹. Results (597 nmol/L ± 241) are close to the upper threshold value (500-600 nmol/L). However, the great standard deviation leads to the conclusion that a few of the 15-20- year-old definitely have a suboptimal supply. Adolescents’tHcy values do not exceed the reference range for adults (10-17 μmol/L). As shown in previously published studies^30,37 tHcy for adolescents corresponds to ~50% of values detected in adults and increases with age.

It is important to bear in mind that adolescents are not small grown-ups. This group has its own specific needs. Adolescents clearly have higher nutrient requirements than other life-stages due to the rapid growth and metabolic changes. Therefore the assessment with adult values lacks of comparability. Possibly adolescents also have higher normal blood values. Thus, further investigations are necessary in order to set new reference values for adolescents.

 

Conclusion

Mean dietary intake of B vitamins except for folate mostly exceed Estimated Average Requirements and Adequate Intakes in both, age groups and genders. Boys are better supplied than girls and the intake of B vitamins falls with increasing age. Inadequate intake can be seen only for folate and again girls are more at risk for folate deficiency. Clear geographical tendencies do not exist. Results for B vitamins in blood mostly exceed thresholds. However, blood samples might be unrepresentative for the population and the assessment with adult thresholds lacks of comparability.

In order to evaluate these intake data correctly, percentiles, means and standard deviations should be indicated in nutrition surveys which are missing in the reviewed literature. Representative blood samples are lacking for most age groups. Further, more accurate methods should be chosen instead of cheaper alternatives. Before giving any recommendations for B vitamin supplementation the real vitamin B status of European adolescents should be established.

A prerequisite to make intake data more accurate is the adaptation of food databases to the local food habits including fortified food. The same methods as well as the same reference values should be utilized for a better comparison between European studies. Estimated Average Requirements should be assessed in order to analyze a group’s dietary intake. Reference values for B vitamins and tHcy in blood specimens for European adolescents still must be established. There is a strong need for further investigations.

 

References

1. Cruz JA: Dietary habits and nutritional status in adolescents over Europe-Southern Europe. Eur J Clin Nutr 2000; 54 (Supl.1):S29-35.        [ Links ]

2. Biesalski HK, Fürst P, Kasper H, et al.: Ernährungsmedizin. Thieme Verlag. Pages. Stuttgard, New York, 2. ed. 1999.        [ Links ]

3. Rolland-Cachera MF, Bellisle F, Deheeger M: Nutritional status and food intake in adolescents living in Western Europe. Eur J Clin Nutr 2000; 54 (Supl. 1): S41-46.        [ Links ]

4. Sweeting H, Anderson A, West P: Socio-demographic correlates of dietary habits in mid-to-late adolescence. Eur J Clin Nutr 1994; 48:736-748.        [ Links ]

5. Decarli B, Cavadini C, Grin J, Blondel-Lubrano A, Narring F, Michaud PA: Food and nutrient intakes in a group of 11 to 16 year old Swiss teenagers. Int J Vitam Nutr Res 2000; 70:139-147.        [ Links ]

6. Koletzko B, de la Gueronniere V, Toschke AM, von Kries R: Nutrition in children and adolescents in Europe: what is the scientific basis? Introduction. Br J Nutr 2004; 92 (Supl. 2):S67-73.        [ Links ]

7. Bourre JM: The role of nutritional factors on the structure and function of the brain: an update on dietary requirements. Rev Neurol (Paris) 2004; 160:767-792.        [ Links ]

8. Liu J, Raine A, Venables PH, Mednick SA: Malnutrition at age 3 years and externalizing behavior problems at ages 8, 11 and 17. Am J Psychiatry 2004; 161:2005-2013.        [ Links ]

9. Ortega RM, González-Fernández M, Paz L, et al.: Influence of iron status on attention and intellectual performance of a population of Spanish adolescents. Arch Latinoam Nutr 1993; 43:6-11.        [ Links ]

10. Lukaski HC: Vitamin and mineral status: effects on physical performance. Nutrition 2004; 20:632-644.        [ Links ]

11. Bailey LB, Gregory JF: Folate Metabolism and Requirements. J Nutr 1999; 129:779-782.        [ Links ]

12. Bässler KH, Golly I, Loew D, Pietrzik K: Vitamin-Lexikon. Urban & Fischer. Pages. München Jena, 3. ed. 2003.        [ Links ]

13. Molloy AM: Folate Bioavailability and Health. Int J Vitam Nutr Res2002; 72:46-52.        [ Links ]

14. Livingstone MBE, Robson PJ, Wallace JMW: Issues in dietary intake assessment of children and adolescents. Br J Nutr 2004; 92 (Supl. 2):S213-S222.        [ Links ]

15. Moreno LA, Kersting M, de Henauw S, et al.: How to measure dietary intake and food habits in adolescence: the European perspective. Int J Obes 2005; 29 (Supl. 2):S66-S77.        [ Links ]

16. Lambert J, Agostoni C, Elmadfa I, et al.: Dietary intake and nutritional status of children and adolescents in Europe. Br J Nutr 2004; 92 (Supl. 2): S147-211.        [ Links ]

17. Hornby: Oxford Advanced Learner’s Dictionnary of Current English. Oxford University Press. Pages. Oxford, 5. ed. 1995.        [ Links ]

18. Dietary Reference Intakes for thiamin, riboflavin, niacin, vitamin B₆, folate, vitamin B₁₂, pantothenic acid, biotin and choline/a report of the Standing Comittee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on Folate, Other B Vitamins, and Choline and Subcommittee on Upper Levels of Nutrients, Food and Nutrition Board. Institute of Medicine. National Academy Press. Pages. Washington DC. 1998.        [ Links ]

19. Dietary Reference Intakes. Applications in dietary assessment: a report of the Interpretation and Uses of Dietary Reference Intakes and Upper Reference Levels of Nutrients, and the Standing Committee on Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. Washington, DC: National Academy Press, 2000.        [ Links ]

20. Schrijver J: Biochemical markers for micronutrient status and their interpretation. In: Modern lifestyles, lower energy intake and micronutrient status. Springer Verlag. Pages. 1991.        [ Links ]

21. Klee GG: Cobalamin and folate evaluation: measurement of methylmalonic acid and homocysteine vs vitamin B₁₂ and folate.Clin Chem 2000; 46:1277-1283.        [ Links ]

22. Thomas L: Vitamin B₁₂. In: Labor und Diagnose. Pages. Frankfurt a.M. 2000.        [ Links ]

23. Kasper H: Ernährungsmedizin und Diätetik. Urban Fischer. Pages. München. 2004.        [ Links ]

24. Gonzalez-Gross M, Prinz-Langenohl R, Pietrzik K: Folate status in Germany 1997-2000. Int J Vitam Nutr Res 2002; 72:351-359.        [ Links ]

25. Van Poppel G, Schneijder P, Lowik MR, Schrijver J, Kok FJ: Nutritional status and food consumption in 10-11 year old Dutch boys (Dutch Nutrition Surveillance System). Br J Nutr 1991; 66:161-169.        [ Links ]

26. Kafatos A, Verhagen H, Moschandreas JA, Apostolaki J, van Westerop JJM: Mediterranean diet of Crete: foods and nutrient content. J Am Diet Assoc 2000; 100:1487-1493.        [ Links ]

27. Bergström E, Hernell O, Persson LA: Dietary changes in Swedish adolescents. Acta Paediatr 1993; 82:472-480.        [ Links ]

28. Droese W, Stolley H, Kersting M: [Energy and nutrient supply during childhood. VII. Vitamins. (author’s transl)]. Monatsschr Kinderheilkd 1980; 128:415-421.        [ Links ]

29. Bjorke Monsen AL, Refsum H, Markestad T, Ueland PM: Cobalamin Status and Its Biochemical Markers Methylmalonic Acid and Homocysteine in Different Age Groups from 4 Days to 19 Years. Clin Chem 2003.        [ Links ]

30. De Laet C, Wautrecht JC, Brasseur D, et al.: Plasma homocysteine concentration in a Belgian school-age population. Am J Clin Nutr 1999; 69:968-972.        [ Links ]

31. Larsson CL, Johansson GK: Dietary intake and nutritional status of young vegans and omnivores in Sweden. Am J Clin Nutr 2002; 76:100-106.        [ Links ]

32. Sichert-Hellert W, Kersting M, Alexy U, Manz F: Ten-year trends in vitamin and mineral intake from fortified food in German children and adolescents. Eur J Clin Nutr 2000; 54:81-86.        [ Links ]

33. Gibson S: Micronutrient intakes, micronutrient status and lipid profiles among young people consuming different amounts of breakfast cereals: further analysis of data from the National Diet and Nutrition Survey of Young People aged 4 to 18 years. Public Health Nutr 2003; 6:815-820.        [ Links ]

34. Preziosi P, Galan P, Deheeger M, Yacoub N, Drewnowski A, Hercberg S: Breakfast type, daily nutrient intakes and vitamin and mineral status of French children, adolescents, and adults. J Am Coll Nutr 1999; 18:171-178.        [ Links ]

35. Serra-Majem L: Vitamin and mineral intakes in European children. Is food fortification needed? Public Health Nutr 2001; 4:101-107.        [ Links ]

36. Marktl W, Rudas B, Brubacher G: The vitamin status of Viennese school children aged 11-12 years. Int J Vitam Nutr Res 1982; 52:198-206.        [ Links ]

37. Tonstad S, Refsum H, Sivertsen M, Christophersen B, Ose L, Ueland PM: Relation of total homocysteine and lipid levels in children to premature cardiovascular death in male relatives. Pediatr Res 1996; 40:47-52.        [ Links ]

38. Mainou Cid C, Garcia Giralt N, Vilaseca Busca MA, et al.: [Hyperhomocystinemia and 677C T methylenetetrahydrofolate reductase polymorphism as a cardiovascular risk factor in childhood]. An Esp Pediatr 2002; 56:402-408.        [ Links ]

39. Gallistl S, Sudi K, Mangge H, Erwa W, Borkenstein M: Insulin is an independent correlate of plasma homocysteine levels in obese children and adolescents. Diabetes Care 2000; 23:1348-1352.        [ Links ]

40. Bates CJ, Mansoor MA, Gregory J, Pentiev K, Prentice A: Correlates of plasma homocysteine, cysteine and cysteinyl-glycine in respondents in the British National Diet and Nutrition Survey of young people aged 4-18 years, and a comparison with the survey of people aged 65 years and over. Br J Nutr 2002; 87:71-79.        [ Links ]

41. Cotellessa M, Minniti G, Cerone R, Prigione F, Calevo MG, Lorini R: Low total plasma homocysteine concentrations in patients with type 1 diabetes. Diabetes Care 2001; 24:969-971.        [ Links ]

42. Ueland PM, Monsen AL: Hyperhomocysteinemia and B-vitamin deficiencies in infants and children. Clin Chem Lab Med 2003; 41:1418-1426.        [ Links ]

43. Kosch A, Koch HG, Heinecke A, Kurnik K, Heller C, Nowak-Gottl U: Increased fasting total homocysteine plasma levels as a risk factor for thromboembolism in children. Thromb Haemost 2004; 91:308-314.        [ Links ]

44. Gallistl S, Sudi KM, Erwa W, Aigner R, Borkenstein M: Determinants of homocysteine during weight reduction in obese children and adolescents. Metabolism 2001; 50:1220-1223.        [ Links ]

45. Rauh M, Verwied S, Knerr I, Dorr HG, Sonnichsen A, Koletzko B: Homocysteine concentrations in a German cohort of 500 individuals: reference ranges and determinants of plasma levels in healthy children and their parents. Amino Acids 2001; 20:409-418.        [ Links ]

46. Glowinska B, Urban M, Peczynska J, Florys B, Szydlowska E: Elevated concentrations of homocysteine in children and adolescents with arterial hypertension accompanying Type 1 diabetes. Med Sci Monit 2001; 7:1242-1249.        [ Links ]

47. Raslova K, Bederova A, Gasparovic J, Blazicek P, Smolkova B: Effect of diet and 677 C→T 5, 10-methylenetetrahydrofolate reductase genotypes on plasma homocyst(e)ine concentrations in slovak adolescent population. Physiol Res 2000; 49:651-658.        [ Links ]

48. Kersting M, Alexy U, Sichert-Hellert W: Vitamin intake of 1- to 18-year-old German children and adolescents in the light of various recommendations. Int J Vitam Nutr Res 2000; 70:48-53.        [ Links ]

49. Hassapidou MN, Fotiadou E: Dietary intakes and food habits of adolescents in northern Greece. Int J Food Sci Nutr 2001;52:109-116.        [ Links ]

50. Olivares AB, Bernal MJ, Ros G, Martínez C, Periago MJ: Calidad de los datos del contenido en ácido fólico en vegetales recogidos en varias tablas de composición de alimentos españolas, y nuevos datos sobre su contenido en folatos. Nutr Hosp 2005; 21(1) in press.        [ Links ]

51. DACH, Deutsche Gesellschaft für Ernährung ÖGfE, Schweizerische Gesellschaft für Ernährungsforschung, Schweizerische Vereinigung für Ernährung, eds. Referenzwerte für die Nährstoffzufuhr. 1. ed. Frankfurt am Main: Umschau/ Braus, 2001.        [ Links ]

52. Bates CJ, Pentieva KD, Prentice A: An appraisal of vitamin B6 status indices and associated confounders, in young people aged 4-18 years and in people aged 65 years and over, in two national British surveys. Public Health Nutr 1999; 2:529-535.        [ Links ]

53. Bor MV, Nexo E, Hvas A-M: Holo-Transcobalamin Concentration and Transcobalamin Saturation Reflect Recent Vitamin B12 Absorption Better than Does Serum Vitamin B12. Clin Chem 2004; 50:1043-1049.        [ Links ]

54. Lee DSC, Griffiths BW: Human Serum Vitamin B12 Assay Methods - A Review. Clin Biochem 1985; 18:261-266.        [ Links ]

55. Loikas S, Löppönen M, Suominen P, et al.: RIA for Serum Holo- Transcobalamin: Method Evaluation in the Clinical Laboratory and Reference Interval. Clin Chem 2003; 49:455-462.        [ Links ]

56. Southon S, Wright AJ, Finglas PM, Bailey AL, Loughridge JM, Walker AD: Dietary intake and micronutrient status of adolescents: effect of vitamin and trace element supplementation on indices of status and performance in tests of verbal and non-verbal intelligence. Br J Nutr 1994; 71:897-918.        [ Links ]

57. Serra-Majem L, Ribas L, Garcia A, Perez-Rodrigo C, Aranceta J: Nutrient adequacy and Mediterranean Diet in Spanish school children and adolescents. Eur J Clin Nutr 2003; 57 (Supl.1):S35-39.        [ Links ]

58. McNulty E-EJ, Cran G, Woulahan G, Boreham C, Savage JM, Fletcher R, Strain JJ: Nutrient intakes and impact of fortified breakfast cereals in schoolchildren. Arch Dis Child 1996; 75:474-481.        [ Links ]

59. Deheeger M, Bellisle F, Rolland-Cachera MF: The French longitudinal study of growth and nutrition: data in adolescent males and females.J Hum Nutr Diet 2002; 15:429-438.        [ Links ]

60. Saeed BO, Banerjee K, Nixon SJ, Brown K: Plasma homocysteine concentrations in patients with Type 1 diabetes. Diabet Med 2003; 20:867-868.        [ Links ]

61. Chiarelli F, Pomilio M, Mohn A, et al.: Homocysteine levels during fasting and after methionine loading in adolescents with diabetic retinopathy and nephropathy. J Pediatr 2000; 137:386-392.        [ Links ]

62. Koletzko B, Dokoupil K, Reitmayr S, Weimert-Harendza B, Keller E: Dietary fat intakes in infants and primary school children in Germany.Am J Clin Nutr2000; 72:1392S-1398S.        [ Links ]

63. Nelson M, Naismith DJ, Burley V, Gatenby S, Geddes N: Nutrient intakes, vitamin-mineral supplementation, and intelligence in British schoolchildren. Br J Nutr 1990; 64:13-22.        [ Links ]

64. McNeill G, Davidson L, Morrison DC, Crombie IK, Keighran J, Todman J: Nutrient intake in schoolchildren: some practical considerations.Proc Nutr Soc 1991; 50:37-43.        [ Links ]

65. Crawley H: Dietary and lifestyle differences between Scottish teenagers and those living in England and Wales. Eur J Clin Nutr 1997; 51:87-91.        [ Links ]

66. Frost Andersen L, Nes M, Sandstad B, Bjorneboe G, Drevon CA: Food habits among 13-year-old Norwegian adolescents. Scandinavian Journal of Nutrition 1997; 41:150-154.        [ Links ]

67. Frost Andersen L, Nes M, Sandstad B, Bjorneboe G, Drevon CA: Dietary intake among Norwegian adolescents. Eur J Clin Nutr 1995; 49:555-564.        [ Links ]

68. Samuelson G, Bratteby LE, Enghardt H, Hedgren M: Food habits and energy and nutrient intake in Swedish adolescents approaching the year 2000.Acta Paediatr 1996; (Supl. 415):1-19.        [ Links ]

69. Lyhne AN: Dietary habits and physical activity of Danish adolescents. Scandinavian Journal of Nutrition 1998; 42:13-16.         [ Links ]

70. Serra-Majem L, Ribas L, Ngo J et al.: Risk of inadequate intakes of vitamins A, B₁, B₆, C, E, folate, iron and calcium in the Spanish population aged 4 to 18. Int J Vitam Nutr Res 2001;71:325-31.        [ Links ]

71. Serra-Majem L, Garcia-Closas R, Ribas L, Perez-Rodrigo C, Aranceta J: Food patterns of Spanish schoolchildren and adolescents: The enKid Study. Public Health Nutr 2001; 4: 1433-8.        [ Links ]

72. Charzewska J, Chwojnowska Z, Rogalska-Niedzwiedz M, Chabros E: Changes in the nutrition of adolescents in Warsaw in the years 1985-1990.Zywienie czlowieka i metabolism 1992; 17-25.        [ Links ]

73. Czeczelewski J, Huk E, Jusiak R, Raczynski G: Nutrition mode and status and physical fitness of children in a school taken as an example in Biala Podlaska. Zywienie czlowieka i metabolism 1995; 174-183.        [ Links ]

74. Ortega RM, Mena MC, Faci M, Santana JF, Serra-Majem L: Vitamin status in different groups of the Spanish population: a meta-analysis of national studies performed between 1990 and 1999. Public Health Nutr 2001; 4:1325-9.        [ Links ]

75. Moynihan PJ, Rugg-Gunn AJ, Butler TJ, Adamson AJ: Dietary intake of folate by adolescents and the potential effect of flour fortification with folic acid. Br J Nutr 2001; 86:529-34.        [ Links ]

76. Belton NR, Macvean ADL, Richards ND, Elton RA, Moffat WMU, Beattie TF: Nutrient intake in Scottish adolescents.Proc Nutr Soc b 1997; 56:303A.        [ Links ]

77. Louwman MW, van Dusseldorp M, van de Vijver FJ et al.:Signs of impaired cognitive function in adolescents with marginal cobalamin status.Am J Clin Nutr2000; 72:762-9.        [ Links ]

78. Grünberg H, Mitt K, Thetloff M: Food habits and dietary intake of schoolchildren in Estonia. Scandinavian Journal of Nutrition 1996; 41:18-22.        [ Links ]

79. Brazdova Z, Fiala J: Dietary Intake of a Selected Child Population in Brno. Cesk Hyg 1992; 297-300.        [ Links ]

80. Brazdova Z, Matejova H, Fiala J: Intake of selected nutrients by children in the Czeck Republic. Hygiena 2000; 45:10-15.        [ Links ]

81. van Dusseldorp M, Schneede J, Refsum H et al.: Risk of persistent cobalamin deficiency in adolescents fed a macrobiotic diet in early life. Am J Clin Nutr 1999; 69:664-71.        [ Links ]

82. Kahleova R, Palyzova D, Zvara K et al.: Essential hypertension in adolescents: association with insulin resistance and with metabolism of homocysteine and vitamins. Am J Hypertens 2002; 15:857-64.        [ Links ]

83. Pavia C, Ferrer I, Valls C, Artuch R, Colome C, Vilaseca MA: Total homocysteine in patients with type 1 diabetes. Diabetes Care 2000; 23:84-7.        [ Links ]

84. van Beynum IM, Smeitink JA, den Heijer M, te Poele Pothoff MT, Blom HJ: Hyperhomocysteinemia: a risk factor for ischemic stroke in children.Circulation 1999; 99:2070-2.        [ Links ]

85. Vilaseca MA, Moyano D, Artuch R et al.: Selective screening for hyperhomocysteinemia in pediatric patients. Clin Chem 1998; 44:662-4.        [ Links ]

86. Glowinska B, Urban M, Koput A, Galar M: New atherosclerosis risk factors in obese, hypertensive and diabetic children and adolescents.Atherosclerosis 2003; 167:275-86.        [ Links ]

87. Laskowska-Klita T, Szymczak E, Radomyska B: Serum homocysteine and lipoprotein (a) concentrations in hypercholesterolemic and normocholesterolemic children. Clin Pediatr (Phila) 2001; 40:149-54.        [ Links ]

88. Minniti G, Cerone R, Piana A, Armani U, Lorini R: Plasma and serum total homocysteine concentrations in paediatric patients, evaluated by high-performance liquid chromatography with fluorescence. Clin Chem Lab Med 2000; 38:675-6.        [ Links ]

 

 

Correspondence:
Dr. Marcela González-Gross
Facultad de CC. de la Actividad Física y del Deporte
Universidad Politécnica de Madrid
c/ Martín Fierro, s/n
E-28040 Madrid
E-mail: marcela.gonzalez.gross@upm.es

Recibido: 12-III-2006.
Aceptado: 15-V-2006.