Epidemiological research has shown socio-economic differences in health at all ages throughout Europe(1). These inequalities in health have been reported to vary between countries and between socio-economic indicators(Reference Mackenbach, Kunst and Cavelaars2, Reference James, Nelson and Ralph3). A possible explanation for these inequalities is a less optimal nutritional status in disadvantaged groups. For example, those with lower income suffer from higher rates of obesity, CVD and certain cancers that are linked to nutrition and diet(Reference James, Nelson and Ralph3, Reference Darmon4). This may be due to the fact that groups with limited economic means consume unhealthy foods that are cheap, energy-dense and nutrient-poor. Socio-economic position, as measured by income for instance, has been found to be one of the most important predictors of diet quality(Reference Darmon4).
Since the proportion of (economically) disadvantaged populations is higher in Central and Eastern European (CEE) countries(Reference Walters and Suhrcke5–Reference López-Azpiazu, Sánchez-Villegas and Johansson9) it is highly relevant to evaluate whether differences in nutritional status may contribute to higher morbidity and mortality in CEE as compared with other European countries.
Assessment of dietary intake and nutritional status for European populations has been an emerging focus for the last two decades. However, current nutritional data are lacking for CEE populations(Reference Bobak and Marmot10, Reference Zunft, Ulbricht and Pokorný11). This hinders research on nutritional health, which is needed to underpin nutrition policies for CEE populations with sizeable disadvantaged groups.
To fill the knowledge gap mentioned above, an additional approach is needed to deal with the standard searches conducted in known (open access) literature databases, i.e. the identification of commonly overlooked grey literature sources from CEE countries. So far, available nutritional data in CEE have often only been used for local health policies and have remained largely unexploited because they are either not published in an accessible manner or not available in English(1, Reference Parízková12, Reference Charzewska13).
In the present study, we compare micronutrient intakes and status in CEE with those in other European countries using both open access sources and grey literature sources. A better use of the latter data from CEE and its further exploitation will enable evaluation of the current nutritional situation of CEE populations to enhance regional policy making.
Methods
EURRECA
The present study was carried out within the context of the EURRECA (EURopean micronutrient RECommendations Aligned) Network of Excellence (http://www.eurreca.org). This network aims to advance methodology for setting micronutrient requirements and recommendations, and to identify vulnerable groups regarding micronutrient intake and status(Reference Cavelaars, Doets and Dhonukshe-Rutten14, Reference Viñas, Barba and Ngo15). To answer our research question, we used the standardized dietary intake/status methodology recommended by EURRECA (more details are below). We focused on the EURRECA top ten micronutrients, prioritized on the basis of the amount of new scientific evidence, their relevance to public health and the variations in current micronutrient recommendations (vitamin B12, folate, Fe, Zn and iodine (intake and status) and vitamin C, vitamin D, Ca, Se and Cu (intake only))(Reference Cavelaars, Doets and Dhonukshe-Rutten14).
Search methodology
Data on CEE countries were collected from PubMed and grey literature for intake and status, and from the WHO Vitamin and Mineral Nutrition Information System (VMNIS) database (http://www.who.int/vmnis/database/en/) for status. For other European countries, we used available comprehensive reviews, primarily the European Nutrition and Health Report 2009 (ENHR II) for intake(Reference Elmadfa, Meyer and Nowak16) and PubMed and WHO VMNIS for status only. Review of the EFSA (European Food Safety Authority) Concise and Comprehensive European Food Consumption Databases did not result in additional data.
We searched for studies on intake and/or status in PubMed published from January 1990 until April 2010 using common medical subject headings (MeSH) and free text search terms: Micronutrients (listed) OR Biomarkers of status (listed) AND General intake/status terms with terms for adequacy, i.e. intake/status (requirement* or recommend* or adequacy or inadequacy or adequate or inadequate or cut point or threshold – in title and abstract) AND Country (CEE and non-CEE countries, listed).
The WHO Global Micronutrient Databases on Iodine Deficiency and Anaemia were used to collate information on iodine and Fe status.
To collect grey literature data on intake and or status from CEE countries, we cooperated with the United Nations University/Standing Committee on Nutrition Network for Capacity Development in Nutrition in Central and Eastern Europe (NCDN CEE)(17). This network gathers nutritional researchers and public health specialists from all CEE countries, whose representatives were introduced to the purpose of the present study and with the search criteria for collection of grey literature at their NCDN annual meeting in November 2008. They were asked to identify potentially relevant data from their countries, translate the data to English if necessary and send them to us for further screening.
Titles and abstracts from every source were screened, and for potentially relevant papers and reports, full texts were retrieved. Subsequently, we assessed which studies were eligible for our study using the following inclusion criteria.
1. The population studied should be representative for the country and apparently healthy, and data gathered should have had a sample size of at least 100 per gender group(Reference Murphy, Guenther and Kretsch18).
2. The study should include information on mean usual micronutrient intake and apply one of the following dietary intake methods (EURRECA best practice dietary intake methods): a validated FFQ or validated diet history; a food diary/register with at least 7 d; three or more 24 h recalls or registers; or three or fewer 24 h recalls with an adjustment for intra-individual variability(Reference Carriquiry19). Initially, these criteria were applied to both CEE and non-CEE data; however, keeping this condition for CEE data would have resulted in very few studies for assessment. For this reason, CEE studies on intake that used one or more 24 h recalls (with no adjustments for intra-individual variability) or other dietary assessment methods were included as well. If more than one country-representative study that fulfilled the inclusion criteria were available, the choice of the study to be presented graphically was made by giving preference to the one that was most recently published.
3. Regarding nutritional status, data gathered should include information on mean or median status using best practice biomarkers defined in the context of EURRECA: Hb, serum/plasma ferritin or serum/plasma transferrin receptor for Fe; erythrocyte (red cell) folate, serum/plasma folate or serum/plasma homocysteine for folate; serum/plasma total B12, serum/plasma methylmalonic acid or serum/plasma holotranscobalamin for vitamin B12; serum/plasma Zn for Zn; and urinary iodine (24 h or spot), serum or dried whole blood spot thyroglobulin or serum thyroid-stimulating hormone for iodine(20–Reference Gibson27).
Data analyses
We compared mean intakes and median (or mean) status levels between countries, between regions and with external reference values to evaluate differences between countries and indications for inadequacies. When several studies were available for one country, studies were ranked for their eligibility considering representativeness of the sample for the country, dietary assessment method used and year of the study (most recent were given preference).
To study regional variations in micronutrient intake and/or status, Europe was divided into four geographical regions: (i) CEE (Albania, Bosnia-Herzegovina, Bulgaria, Croatia, Czech Republic, Estonia, Latvia, Lithuania, Hungary, Macedonia, Montenegro, Poland, Romania, Serbia, Slovakia and Slovenia); (ii) Mediterranean (Greece, Italy, Portugal and Spain); (iii) Western Europe (Austria, Belgium, France, Germany, Ireland, The Netherlands, Switzerland and the UK); and (iv) Scandinavia (Denmark, Finland, Iceland, Norway and Sweden).
Regional comparisons were made when data for a specific micronutrient and population group were available for at least three CEE countries. This comparison included the calculation of weighed mean regional intakes and median status levels, plotting of country means (medians) and subsequently the description of: (i) differences in intake and/or status across European regions and (ii) observed mean intake and/or status in CEE countries in contrast to nutritional reference values. Variables considered in the description were differences in dietary assessment method (checked also by differences in mean daily energy consumption) and study population. In cases where data were available for fewer than three CEE countries, data from CEE countries were compared with the data from other European countries published in ENHR II(Reference Elmadfa, Meyer and Nowak16) or from single studies, selecting those with the most comparable data (regarding age group, status biomarker, dietary assessment method and year of the study).
To evaluate whether there is an indication for inadequacy in micronutrient intake, the mean usual intake was compared with the ANR (Average Nutrient Requirement; amount of nutrient which is sufficient for 50 % of the apparently healthy population) derived for the Nordic countries (Nordic Nutrition Recommendations, NNR)(28, Reference Doets, de Wit and Dhonukshe-Rutten29), as these are the most recent reference values set for a series of European countries.Footnote * If an ANR for a micronutrient was not set by NNR (Ca and vitamin D in adults, all micronutrients in children), the ANR published for the USA/Canada by the US Institute of Medicine was used(22). Relevant ANR are given in the figure captions. To assess adequacy of levels of status markers, we used guidance on cut-off values from EURRECA experts(Reference Hooper, Ashton and Harvey30–Reference Fairweather-Tait and Harvey33). These cut-off values were based on key references mostly published by the WHO in cooperation with other institutions(20–Reference Gibson27). The specific values used are added to figure captions, table footnotes or text where applicable.
Results
Literature search and data availability
The search on micronutrient intake/status for all age ranges in CEE in the PubMed database resulted in 1949 titles and abstracts, out of which 121 were left after screening for potential relevance. The key reason for exclusion was that studies did not report mean intake or status. For one hundred and thirteen, full manuscripts were obtained and checked for compliance with the inclusion criteria; eight studies were inaccessible. Finally, thirty-eight studies were kept for further analysis, of which the grey literature added nine studies in total and contributed primarily data on micronutrient intake in adults. The WHO VMNIS database provided thirty-four studies on iodine and Fe status. A detailed overview of the study characteristics is given in Table 1.
M, males; F, females; 24hR, 24 h recall; 3dDR, 3 d diet record; HFCS, household food consumption survey.
*For all studies: supplements are not included in the assessment.
†Grey literature.
Comparison of micronutrient intakes
Micronutrient intake data were most abundant for Ca, folate, Fe, vitamin B12, vitamin C and vitamin D in adults. Figures 1 to 6 plot the mean micronutrient intakes (with 95 % confidence intervals) geographically (by country in four regions) and information is given on the dietary assessment method, age range of the study population, number of subjects and mean energy intake for males and females.
Observed mean Ca intake (Fig. 1) among females in CEE countries (pooled estimated mean: 869 mg/d) was in general lower than those in other European countries. The pooled means were 978, 1006 and 881 mg/d for Scandinavian, Western European and Mediterranean countries, respectively. The observed mean intake among females in Estonia, Hungary and Lithuania was below the ANR (source: NNR), which indicates that there is a risk of inadequacy. Similar results were observed for CEE males (pooled estimated mean: 862 mg/d); the pooled mean Ca intakes for Scandinavian, Western European and Mediterranean countries were 1130, 1129 and 885 mg/d, respectively. In CEE, four out of eight countries had a mean intake below the ANR among males, and in three countries among females. Within CEE, relatively high levels of Ca intake were observed for Croatia and Serbia. This can likely be explained by the different age range of the study population in the Croatian study (university students, 18–30 years) and the different dietary assessment method used in the Serbian study (intake data were collected per household and calculated per person using the consumption units). This explanation is supported by the fact that mean energy intakes in these studies are also relatively high. This remark also holds for the levels of intake of other micronutrients from these two studies.
Figure 2 shows the observed mean intakes for folate. In CEE the mean pooled intake (307 μg/d) was slightly higher than in the other regions (Scandinavia: 235 μg/d, Western Europe: 278 μg/d, Mediterranean: 275 μg/d), which was due to the relatively high value for Croatia. In CEE, Hungarian and Estonian females had mean intake below the ANR, indicating a risk of inadequacy. Among CEE males, the estimated mean intake (302 μg/d) was in the same range as those in other regions (Scandinavia: 268 μg/d, Western Europe: 322 μg/d, Mediterranean: 287 μg/d). Hungarian males had folate intake below the ANR.
These results correspond with the previous publication by de Bree et al. (Reference de Bree, van Dusseldorp and Brouwer34) which indicated that mean dietary folate intake in Europe is in line with recommendations.
The observed mean Fe intakes are shown in Fig. 3. The pooled mean intake among females from CEE (13 mg/d) was similar to those from the other European regions (range: 11–13 mg/d). For all CEE countries the mean intake of females was above the ANR with the exception of Hungary. For males, the mean estimated intake in CEE (16 mg/d) was slightly higher than that in other regions (range: 13–15 mg/d); all countries reported an observed mean intake higher than the average daily requirements.
The mean intakes of vitamin B12 are shown in Fig. 4. The pooled levels for both females and males in CEE (4 and 7 μg/d, respectively) were similar to the pooled means for Scandinavia and Western Europe, whereas the highest means were observed in the Mediterranean countries (7 μg/d in females, 8 μg/d in males). For both genders in all countries, mean intake values were above the ANR.
The mean observed vitamin C intake (Fig. 5) in CEE females (pooled estimate: 134 mg/d) was similar to that in Western European countries (136 mg/d) and higher than in Scandinavia and the Mediterranean (107 and 119 mg/d, respectively). The same held for CEE males: the pooled estimate for CEE was 118 mg/d, for other regions it ranged from 93 to 142 mg/d. Both genders in CEE countries had mean intake above the ANR.
The pooled mean vitamin D intakes for females and males of CEE countries were 3 and 4 μg/d, respectively (Fig. 6). These values were comparable to those of the other regions; pooled estimates for females and males were 7·8 μg/d in Scandinavia, 2·4 μg/d in Western Europe and 3·3 μg/d in Mediterranean countries. The mean intakes in CEE and in other regions were below the ANR with exception of Norway.
Data for the other micronutrients (Cu, iodine, Se and Zn) were limited and available for one or two CEE countries and for some population groups only (see Table 2).
24hR, 24 h recall; HFCS, household food consumption survey.
Reference values: Average Nutrient Requirement (value from Nordic Nutrition Recommendations or US Institute of Medicine) for adults per d: Cu 0·7 mg; iodine 100 μg; Se 30 μg for females, 35 μg for males; Zn 5 mg for females, 6 mg for males.
The mean Cu intake in CEE countries was comparable to those in other European countries, 1·2–1·9 mg/d(Reference Elmadfa, Meyer and Nowak16), except for Serbia, which reported the highest intake. The mean intakes were above the reference values set for Cu. Iodine intake data were available only for Serbia, and the mean intake was in the range of other regions (108–253 μg/d for males; 101–194 μg/d for females)(Reference Elmadfa, Meyer and Nowak16) being above the ANR. Se intake data for CEE adults were available for Croatia, and the mean intake value was above the range observed in the other regions (36–73 μg/d for males; 31–55 μg/d for females)(Reference Elmadfa, Meyer and Nowak16). The mean intakes for both genders were well above the ANR. Data on mean Zn intake were available for three CEE countries, and the values were similar to those for non-CEE countries (7·8–13·6 mg/d for males; 7·8–10·3 mg/d for females)(Reference Elmadfa, Meyer and Nowak16); the average intakes were considerably above the ANR.
Data on micronutrient intakes in CEE children were available from Croatia, Hungary and Serbia. The mean micronutrient intakes in these countries (Table 3) were in range of intakes in children in other European countries(Reference Elmadfa, Meyer and Nowak16): Ca (600–1381 mg/d), Cu (0·8–1·9 mg/d), folate (138–428 μg/d), iodine (94–209 μg/d), Fe (7·7–17·9 mg/d), Se (28–110 μg/d), vitamin C (78–197 mg/d), vitamin D (1·2–4·8 μg/d) and Zn (6·5–14·6 mg/d), except for the intake of vitamin B12 in Hungary, which was lower in comparison to other European regions (2·9–11·8 μg/d). In these three CEE countries, mean daily intakes below the ANR were observed for Ca (except in boys in Serbia), folate, vitamin D and for Se in Croatia.
HFCS, Household food consumption survey.
Reference values: Average Nutrient Requirement (value from US Institute of Medicine) for children per d: Ca 1100 mg; Cu 0·5 mg; folate 250 μg; iodine 73 μg; Fe 6 mg; Se 35 μg; vitamin B12 1·5 μg; vitamin C 39 mg; vitamin D 10 μg; Zn 7 mg.
Comparison of micronutrient status
For micronutrient status most CEE data were available for iodine and Fe status in children. Figures 7 and 8 show the median urinary iodine concentrations and the mean (sd) Hb concentrations, respectively, for children in Europe. The data on iodine and Fe status were retrieved mainly from the WHO VMNIS database. Exceptions are the data for The Republic of Srpska and Serbia. CEE countries had lower median urinary iodine levels than other European regions: mild iodine deficiency (median urinary iodine <100 μg/l) in CEE was found in children and adolescents from Estonia, Hungary, Latvia and Lithuania, whereas children in Albania suffered from moderate iodine deficiency (median urinary iodine <50 μg/l). Data from other European countries showed an adequate iodine status (median urinary level >100 μg/l) for all countries, except for Italy and Belgium.
The mean Hb levels in CEE children and adolescents were lower than in other European countries, for which the data were scarce. Mean levels were in general above the cut-off values; only infants in Lithuania were at risk of Fe-deficiency anaemia (Hb <110 g/l), whereas children in Romania had borderline concentration.
CEE data on iodine and Fe status in adults, and on folate, vitamin B12 and Zn status for all population groups, were too limited to allow between-region comparisons. An overview of the available status data for CEE populations is presented in Table 4.
WHO database, WHO Vitamin and Mineral Nutrition Information System; M, males; F, females.
Proposed cut-off values(20–Reference Gibson27, Reference Hooper, Ashton and Harvey30–Reference Fairweather-Tait and Harvey33): serum folate 10 nmol/l for adults; urinary iodine 100 μg/l for adults, 150 μg/l for pregnant women; Hb 130 g/l for males, 120 g/l for females, 110 g/l for pregnant women; serum vitamin B12 150 pmol/l for adults; serum Zn 10 μmol/l for children and females, 10·7 μmol/l for males.
Median urinary iodine concentration in CEE adults ranged from 51 to 158 μg/d, similar to those in other European regions (source: WHO VMNIS database for non-CEE countries; not included in the table). In CEE, mild iodine deficiency (median urinary iodine <100 μg/l) was observed in Romanian females. In other regions, both males and females from Italy, France and Germany had mean urinary iodine levels below the cut-off.
Prevalence of iodine deficiency in Europe was recently outlined by Zimmerman and Andersson(Reference Zimmermann and Andersson35). For CEE countries (data on school-aged children; if not available, pre-school children, adolescents or adults) iodine deficiency was reported in Albania, Estonia, Hungary, Latvia and Lithuania.
For Fe status, CEE data were available only for Serbia(Reference Gurinović, Kadvan and Vukotić36) and for females from Macedonia(Reference Parízková12). Reported mean Hb concentrations were in the same range as those in other European countries included in the WHO global database (e.g. Spain, France, Denmark and Finland) and above the cut-off value of 120 or 130 g/l.
Overall, the results on Fe status (Hb levels above the cut-offs) confirm the results on Fe intake for all countries in the present study (except Hungary).
Data on folate status were available for adults in Croatia, Czech Republic and Hungary. Mean serum folate levels in CEE were comparable to those from other European countries (range mean: 16 to 18 nmol/l)(Reference Planells, Sanchez and Montellano37–39), with the exception of Norwegian adults (7 nmol/l)(Reference Vogiatzoglou, Smith and Nurk40). The mean serum folate levels in CEE populations and in other regions were above the cut-off values for both genders, except for Roma mothers in Czech Republic. The findings on folate status are in accordance with observed results on folate intake from the present study for all European regions (except Hungary and Estonian females).
For vitamin B12 status, only one study from CEE was identified. In the Czech Republic reported mean levels of serum vitamin B12 were comparable to those in other European countries, such as Norway(Reference Vogiatzoglou, Smith and Nurk40), and above the reference value (150 pmol/l). These findings are consistent with the vitamin B12 intake results from the present study (Fig. 4).
Data on Zn status were available for adults and children in three CEE countries. CEE adults from Czech Republic and Hungary had mean Zn status concentrations (13–17 μmol/l) comparable to those in Western European countries (range mean: 13–14 μmol/l)(Reference Thijs, Staessen and Amery41–Reference Hampel, Kuhlberg and Schneider43) and higher than the reference value. Mean status levels for Polish and Czech children were in the range from 12 to 15 μmol/l (above the cut-offs), and similar to findings from other European countries such as the UK (15 μmol/l)(Reference Thane, Bates and Prentice44).
Discussion
The present study reports the first comprehensive overview of CEE nutritional data using both open access and grey literature sources with a twofold objective: evaluation of intake and status for targeted micronutrients in CEE in comparison to (i) those of other European countries and (ii) the reference values.
From the limited data available, the results of this review show no differences in micronutrient intake and status in CEE populations in comparison to other European regions except for intake of Ca in adults, and iodine and Fe status in children (intake and status levels lower in CEE than in non-CEE countries). Comparisons with the intake/status reference values suggest highest risk of inadequacy in intake of vitamin D in all age ranges, and of Ca, folate and iodine in children.
We collated data using EURRECA's best practice guidance on dietary assessment methods and status biomarkers(Reference Hooper, Ashton and Harvey30). In general, CEE studies on micronutrient intake and status for all age ranges were scarce: even after being less strict in inclusion criteria, only a few intake studies could be added to the current comprehensive overview. The largest knowledge gap regarding intake refers to children; whereas data on status were scarce for all population groups, with the exception of Fe and iodine in children. The available studies on micronutrient intake and status studies in CEE countries are diverse with regard to design: they differ in dietary assessment, food composition databases, sampling procedures and age range, and this may confound regional and between-country comparisons. Cooperation with the nutritional network from CEE(17) resulted in obtaining nine studies from grey literature. Even though this was not sufficient to fill an evident knowledge gap in nutritional data from CEE, it added to the existing open sources. However, despite a paucity of data and the variations in methodologies that can influence the true differences in intake(Reference Serra-Majem, Frost Andersen and Henríque-Sánchez45), some regional variations were observed: it seems that nutritional health in CEE in comparison to other European countries is less favourable but only for certain micronutrients.
Since CEE is less affluent compared with other European regions, it would be interesting to examine the variations in micronutrient intake and status within CEE countries across different socio-economic layers. That would indicate specific subgroups that are most at risk of poor nutritional health. For future research, we recommend reviewing grey literature, and its accessibility and reliability need further attention. However, to bring a comprehensive conclusion on the nutritional situation in CEE countries much work is required: for developing tailored, sound, evidence-based nutritional policy, the knowledge gaps and establishing nutritional surveys of comparable quality, covering the diversity of population groups, need to be addressed. The inclusion of CEE countries in pan-European nutritional surveys is highly essential to achieve this objective.
Acknowledgements
Sources of funding: The work reported herein has been carried out within the EURRECA Network of Excellence (http://www.eurreca.org), which is financially supported by the Commission of the European Communities, specific Research, Technology and Development (RTD) Programme ‘Quality of Life and Management of Living Resources’, within the Sixth Framework Programme, project no. FP6 036196-2. This report does not necessarily reflect the Commission's views or its future policy in this area. Conflict of interest: The authors declare that they have no conflicts of interest. Authorship responsibilities: R.N. and A.E.J.M.C. conceptualised the paper, collected the data and drafted the manuscript. A.E.J.M.C. supervised the overall work, assisted with analysis and editing of the manuscript. G.E.B., B.R.-V., J.N., M. Golesorkhi, M.W.M., M.N. and Z.S. helped with data collection, reviewing the literature and analysis. M. Gurinović, M. Glibetić, L.S.M., P.v.V., A.G. and L.C.P.G.M.d.G. were involved in development of the study hypothesis, editing the working versions of the manuscript and provided advice regarding interpretation of the results. Acknowledgements: The authors acknowledge the members of the UNU/SCN Network for Capacity Development in Nutrition in Central and Eastern Europe (http://www.agrowebcee.net/ncdn) for the identification and translation of grey literature. It gave added value to the review and enabled a comprehensive overview of available data and implied to knowledge gaps in CEE.