Nutrient Intakes of Toddlers and Preschoolers in Greece: The GENESIS Study

RESEARCH Research and Professional Briefs

Nutrient Intakes of Toddlers and Preschoolers in Greece: The GENESIS Study YANNIS MANIOS, PhD; EVANGELIA GRAMMATIKAKI; STALO PAPOUTSOU; THODORIS LIARIGKOVINOS, MSc; KATERINA KONDAKI, MSc; GEORGE MOSCHONIS, MSc

ABSTRACT There are only a few studies assessing the nutrient intake of Greek children in the literature. Therefore, the aim of this study was to assess the nutrient adequacy of the diets of a representative sample of 2,374 toddlers and preschoolers with full anthropometric and dietary intake data. Usual nutrient intakes were calculated after adjusting raw data for within-person variance and correcting for underreporting. The percentages of children meeting or not meeting recommendations for energy and nutrient intakes were estimated. Differences in mean values were tested with one-way analysis of variance, while ␹2 and Fisher exact tests were used to explore the association between categorical variables. For both fat and carbohydrate, a substantial percentage of toddlers and preschoolers had usual intakes outside the acceptable macronutrient distribution range, whereas protein was less than this range. “At risk of overweight” and “overweight” children consumed more total energy, protein, and fat compared with their normal-weight counterparts, whereas no differences were found for micronutrient intakes. The estimated prevalence of inadequacy was found to be between 10% and 25% for niacin, vitamin E, and folate. Usual intakes exceeding the Tolerable Upper Intake Levels were recorded for zinc and copper. J Am Diet Assoc. 2008;108:357-361.

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nfancy and childhood are both critical periods of rapid physical growth and cognitive and emotional development. It is well-recognized that nutrition in these age groups is also fundamental for future health status. Eco-

Y. Manios is an assistant professor, E. Grammatikaki is a dietitian–public health nutritionist, S. Papoutsou is a clinical dietitian–nutritionist, T. Liarigkovinos is a dietitian–public health nutritionist, K. Kondaki is a public health nutritionist, and G. Moschonis is a clinical dietitian–nutritionist, all with the Department of Nutrition & Dietetics, Harokopio University, Athens, Greece. Address correspondence to: Yannis Manios, PhD, Department of Nutrition and Dietetics, Harokopio University, 70, El.Venizelou Ave, 176 71 Kallithea, Athens, Greece. E-mail: [email protected] Copyright © 2008 by the American Dietetic Association. 0002-8223/08/10802-0006$34.00/0 doi: 10.1016/j.jada.2007.10.042

© 2008 by the American Dietetic Association

nomic growth and high access to food currently observed in developed countries has led to food overconsumption, which in turn has resulted in an increasing prevalence of obesity (1,2), high blood pressure (3,4), and metabolic syndrome (5) in children. Therefore, the need to monitor children’s health- and diet-related indexes is still emerging. In several industrialized countries, national epidemiological surveys have been conducted, describing dietary intakes of toddlers and preschool children. Unexpectedly, in addition to overconsumption of food and energy, these studies indicated a contradictory coexistence of inadequate intakes for certain nutrients and excessive intakes of others (6-8). Similar findings have also been derived from surveys conducted in Europe (9-11), but in Greece there are only a few studies assessing the nutrient intake of Greek children, most limited to small local cohorts (12). Probably the most comprehensive data are those provided by Roma-Giannikou and colleagues (13) on a stratified multiform sample of 2- to 14-year-old children conducted approximately 10 years ago. This paper focuses on the usual nutrient intakes of the GENESIS (Growth, Exercise and Nutrition Epidemiological Study In preSchoolers) cohort (14) and describes: (a) usual energy and macronutrient intake in the total population as well as by children’s weight status, and (b) inadequate or excessive nutrient intakes compared with children’s requirements. MATERIALS AND METHODS The GENESIS cohort was randomly selected after applying a multistage sampling procedure, which is described in more detail elsewhere (14). The cross-sectional study was done from April 2003 to July 2004. All children attending nursery schools were invited to participate in the study and no children or nursery schools were excluded. A representative sample of 2,374 children age 1 to 5 years old with full anthropometric and dietary data was included in the analysis. Approval to conduct the survey was granted by the Ethical Committee of Harokopio University of Athens, Greece. Data on anthropometrical indexes (ie, body weight, recumbent length, and stature) of children were obtained by the use of standard procedures in all study sites (14). Body mass index was calculated as kg/m2. The Nutstat module of EpiInfo (15) was used to determine children’s age- and sex-specific percentiles for weight, length, and body mass index. The weight-for-length percentiles were used to classify children up to 24 months old as “overweight” (ⱖ95th percentile), whereas children older than

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24 months were classified as “at risk of overweight” (ⱖ85th and ⬍95th percentile) and “overweight” (ⱖ95th percentile) using the body mass index-for-age percentiles. Dietary intake data were obtained for 2 consecutive weekdays and 1 weekend day. During the 2 weekdays, a team member weighed and recorded all foods children consumed at the nursery, and information about the food consumed outside the nursery was obtained during an interview with the parent/guardian. The procedure followed is described in more detail elsewhere (14). To ensure quality, food models and sample household measurements (such as cups and spoons) were used to specify serving sizes, a trained dietitian checked the food records for any misrecorded or missing information, while a random 10% of all records was re-entered in the food database by a different person than the one entering the original data. The data were then compared with the original to ensure inter-researcher reliability. Food intake data were analyzed with Nutritionist V diet analysis software (version 2.1, 1999, First Databank, San Bruno, CA), which was extensively amended to include traditional Greek foods and recipes, as described in Food Composition Tables and Composition of Greek Cooked Food and Dishes (16,17). Furthermore, the databank was updated with nutrition information of chemically analyzed commercial food items widely consumed by infants and preschoolers in Greece. Following a standard procedure described in more detail elsewhere (14,18), usual intakes of energy, macronutrients, and micronutrients were estimated, removing the effects of day-to-day (within-subject) and subject-by-subject (between-subject) variability in dietary intakes. To check for underreporting, the ratio of reported energy intake (EI) and predicted basal metabolic rate was used. Basal metabolic rate was estimated according to Schofield equations (19), taking into account age, sex, and body weight. Thus, children with EI:basal metabolic rate ratios less than the calculated cutoff values (0.96 or 1.03 depending on the subjects’ physical activity levels, age, and sex) (20-22) were excluded from further analysis, resulting in a final sample of 2,317 children. The intake distributions of the remaining subjects were corrected for within-person variability as described earlier. Methods recommended by the Institute of Medicine were used to assess the usual nutrient intakes of toddlers and preschool children (18). Regarding energy intake, children’s requirements were expressed in terms of estimated energy requirements (EER) (23). For nutrients with an estimated average requirement (EAR), the EAR cutpoint method was used to estimate the proportion of the population with usual intakes less than the EAR (18,24). For nutrients with established tolerable upper intake levels (ULs), the proportion of toddlers and preschoolers with usual intake from food exceeding the UL was calculated. Finally, the proportion of toddlers and preschoolers with usual intakes outside the acceptable macronutrient distribution ranges (AMDR) for fat, protein, and carbohydrate intakes as a percentage of energy intake was examined (23). Continuous variables are expressed as mean⫾standard deviation, as medians, or as percentiles, whereas categorical variables are expressed as proportions (%). The Kolmogorov-Smirnov test was used to determine normality

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of distribution of the examined variables. For the comparison of means between groups the one-way analysis of variance was used, using the Bonferroni rule to correct for the inflation in type 1 error due to multiple post-hoc comparisons. ␹2 and Fisher exact tests were used to explore the association between categorical variables. All P values reported are two-tailed. Statistical analysis was done with the SPSS version 13.0 (2004, SPSS Inc, Chicago, IL). The level of statistical significance was set at Pⱕ0.05. RESULTS AND DISCUSSION Based on the anthropometric data, mean weight and height were 16.9⫾3.4 kg and 99.9⫾8.5 cm, respectively. The prevalence of “at risk of overweight” and “overweight” in the cohort was 16.7% and 16.4%, respectively. No differences were found between sexes regarding the prevalence of “at risk of overweight” and “overweight” (data not shown). More information about anthropometric characteristics of the cohort has been presented in detail previously (14). The magnitude of these results can be better assessed when compared with results from a representative US population of similar age (2), indicating a much higher prevalence of “at risk of overweight” and “overweight” among Greek preschoolers. The alarming rate of this finding can be easily realized when considering that currently obesity among adults in the United States and Greece are comparable (25), whereas an increasing rate of obesity among children and adolescents has been recorded in Greece during the last 2 decades (1). Table 1 shows usual intake of energy and macronutrients by body weight status as well as in the total population. Both the mean and median usual intakes of energy, as well as the estimated percentiles of usual intake, were more than the comparable percentiles of the EER distributions (data not shown). Mean usual EI was 17% more than the mean EER in the total population (data not shown). “At risk of overweight” and “overweight” children had larger EIs compared with their normal-weight counterparts (P⬍0.001). Regarding macronutrients, for both fat and carbohydrate a substantial percentage of toddlers and preschoolers had usual intake outside the AMDR, whereas protein intake was within the AMDR. In particular, 21.0% had intakes less than the AMDR for carbohydrate, whereas 59.5% of children had intakes of more than the AMDR for fat. Overweight children consumed less energy from carbohydrate and more from fat as well as more saturated fat compared with their normal-weight counterparts. An important finding was that mean energy intakes of the GENESIS toddlers and preschoolers exceeded their requirements, as calculated using EER equations. These results agreed with the findings of nutritional surveys conducted both in Greece (13) and the United States (7) in which children age 1 to 5 years had mean EI more than their requirements. However, the EI distributions for GENESIS were less than those recorded for Greek preschoolers 10 years ago (13). The three National Health and Nutrition Examination Survey (NHANES) studies (from the early 1970s to 1988-1994) had similar findings (6). These secular trends in EI suggest that increased energy intake over time is not the major contributor to

Table 1. Intake of energy and macronutrients of toddlers and preschoolers in Greece as usual intake and as percentage of energy intake: Results from GENESISa (n⫽2,317 children) Usual Intake

Energy Usual intake (kcal)b ⬍80% EERc (%) 80%-120% EER (%) ⬎120% EER (%) Protein Usual intake (g) % ⬍EARd Carbohydrate Usual intake (g) % ⬍EAR Fat Usual intake (g) % ⬍EAR SFAf (g) MUFAg (g) PUFAh (g)

Total

Normal weight

At risk of overweight

Overweight

P value

1,404⫾242 2.1 57.9 40.0

1,386⫾233 1.5 56.3 42.1

1,434⫾242*** 3.6 65.5 30.9

1,445⫾270*** 3.1 56.6 40.4

⬍0.001

58⫾12.4 0.0

57.2⫾12.2 0.0

59.6⫾12.4*** 0.0

59.9⫾12.8*** 0.0

159.2⫾32.3 1.3

158⫾31.6 1.5

161.5⫾33.9 1.2

161.6⫾33.5 0.3

62.8⫾14.7 NAe 25.9⫾7.5 25.9⫾6.5 6.5⫾1.9

61.7⫾14.2 NA 25.3⫾7.3 25.4⫾6.3 6.4⫾1.9

64.5⫾14*** NA 26.8⫾7.3*** 26.4⫾6.2*** 6.7⫾1.9

65.8⫾16.7*** NA 27.2⫾8.4*** 26.9⫾7.4*** 6.8⫾2.1***

⬍0.001 ⬍0.001 0.005

Total

Normal weight

At risk of overweight

Overweight

P value

17.1⫾1.6 0.1

17.1⫾1.6 0.2

17.1⫾1.5 0

17.1⫾1.5 0.3

0.733 0.732

45.6⫾0.8 21.0

45.7⫾0.8 19.2

45.6⫾0.8 24.6

45.5⫾0.8*** 24.5

0.003 0.023

40⫾0.9 59.5

39.9⫾0.9 58.2

40⫾0.8 61.9

40.1⫾0.8*** 63

0.008 0.18

16.5⫾3.2 98.0

16.3⫾3.2 97.2

16.8⫾3.2 99.4

16.8⫾3.3 97.4

0.018 0.14

4.2⫾1

4.2⫾0.9

4.2⫾0.9

4.2⫾1

0.802

16.5⫾2.6

16.5⫾2.7

16.6⫾2.5

16.7⫾2.7

0.465

0.001 ⬍0.001 0.732 0.073 0.218 ⬍0.001

Usual Intake as Percentage of Energy Intake

Protein As % energy % Outside AMDRi Carbohydrate As % energy % Outside AMDR Fat As % energy % Outside AMDR SFA As % energy % ⬎10% energy PUFA As % energy MUFA As % energy a

GENESIS⫽the Growth, Exercise and Nutrition Epidemiological Study In preSchoolers. Usual intakes and % energy presented as mean value⫾standard deviation. c EER⫽estimated energy requirement. d EAR⫽estimated average requirement. e NA⫽not applicable. f SFA⫽saturated fatty acids. g PUFA⫽polyunsaturated fatty acids. h MUFA⫽monounsaturated fatty acids. i AMDR⫽acceptable macronutrient distribution range. ***P⬍0.001 compared with normal-weight children. b

the increased prevalence of overweight among youths and children age 2 to 5 years (6,8). Lower levels of physical activity could be the main reason for this phenomenon. The decrease in the frequency of bicycling or walking to and from school that has been observed in other industrialized countries could be a strong indicator of the increased prevalence of overweight (26).

Regarding macronutrient intake, there is no concern for inadequacy because almost all children had intakes more than the EAR for protein and carbohydrate and more than the AMDR for fat. Our findings suggest that protein as a percentage of EI has increased in the past decade in Greek toddlers and preschoolers (13). The relatively high fat intake as a percentage of EI observed in the current study

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Table 2. Usual nutrient intake distributions of toddlers and preschoolers in Greece: Results from GENESISa (n⫽2,317 children) Inadequate/Excessive Usual Intakec

Usual Intake Percentilesb

Vitamins Vitamin D (␮g) Vitamin E (␮g) Vitamin K (␮g) Thiamin (mg) Riboflavin (mg) Niacin (mg) Folate (␮gDFE)ij Vitamin C (mg) Minerals Calcium (mg) Iron (mg) Copper (mg) Zinc (mg) Magnesium (mg)

10th

25th

Median

Mean

75th

0.8 4.4 19.3 0.5 0.6 4.4 109 54

1.5 5.1 23.6 0.7 1.0 7.0 126 59

3.3 6.1 28.5 0.8 1.6 10.9 145 68

5.6 6.4 32.2 0.9 2.0 13.5 148 70

7.5 7.5 34.9 1.0 2.7 16.4 168 78

668 5.6 0.5 5.6 141

828 7.2 0.5 6.6 159

1,015 9.6 0.6 7.9 183

1,024 10.0 0.7 8.4 188

1,198 11.9 0.8 9.6 211


>ULe (%)

11.9 8.8 50.8 1.2 4.0 25.6 192 88

NAf 22.2 NA 1.3 6.3 14.5 19.7 0.0

0.6 NAg NAh NAh NAh NAg NAg 0.0

1,392 14.8 0.9 11.7 239

NA 0.2 0.1 0.0 0.0

0.1 0.1 7.7 51.8 NAg

90th

a

GENESIS⫽the Growth, Exercise and Nutrition Epidemiological Study In preSchoolers. Values are the maximum intake observed for each percentile. c Percentage of toddlers and preschoolers with inadequate or excessive usual intakes. d EAR⫽estimated average requirement. Intakes below the EAR are considered as inadequate. e UL⫽Tolerable Upper Intake Level. Intakes above the UL are considered as excessive. f NA⫽not applicable. g The UL value applies to synthetic forms from supplements and/or fortified foods. h The UL value is not determined. i DFE⫽dietary folate equivalents. 1 ␮gDFE⫽1 ␮g of food folate or 0.5 ␮g synthetic (supplemental) folic acid on an empty stomach or 0.6 ␮g folic acid from fortified food or supplement consumed with food. j Folate intake does not include synthetic forms from supplements and/or fortified foods. Therefore 1 ␮gDFE⫽1 ␮g food folate. b

could be attributed to the traditional relatively high consumption of olive oil in the Greek diet and/or to the increasing consumption of high-fat snacks observed in children and adolescents in Greece (27). In contrast, low carbohydrate intakes as a percentage of EI do not conform to the principles of the traditional Greek diet, which is based in fruits, vegetables, and whole grains. In that context, overweight children seem to conform less to the traditional diet model compared with their normal-weight counterparts. Table 2 presents the estimated intake distributions of micronutrients for toddlers and preschoolers. Based on the EAR, the prevalence of inadequate intake was low (⬍5%) for thiamin (1.3%) and riboflavin (6.3%), whereas it seemed to be high for vitamin E (22.2%), niacin (14.5%), and folate (19.7%). For copper and zinc, 7.7% and 51.8% of children, respectively, had usual intake exceeding the UL. Less than 1% of the toddlers had usual intakes of vitamin D exceeding the UL. These findings cannot be compared at a local level because no previous data from Greek cohorts are available. However, data about the intakes of the specific nutrients have been obtained from surveys done in other developed countries. Regarding vitamin E, intakes less than the EAR are not unprecedented. More precisely, in the United States NHANES III showed that the majority of age/sex subgroups had intakes less than the EAR (7,28). Still, 95% of the population surveyed had normal vitamin E plasma

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concentrations (29), indicating that there is no cause for concern regarding toddlers’ vitamin E status. In the current study, toddlers and preschoolers had lower usual intakes for niacin and folate compared with the data from the Feeding Infants and Toddlers Survey (FITS) (7). According to Allen (30), there are strong convictions that recommended intakes are probably generous for both niacin and folate, and likely also for all B vitamins because all EAR recommendations are extrapolated down from the intake recommendations for adults. That is why more supporting quantitative data in children are needed to set more precise recommendations before concluding that there is an alarming inadequacy in vitamin E, niacin, and folate intake among Greek preschoolers. Excessive zinc intake was recorded for 51.8% of toddlers and preschoolers in this study. Many other studies have also reported excessive intakes of zinc in this age group (7,31), which could be attributed both to the relatively high intake of zinc as well as the fact that the UL and EAR values have been set quite close (31,32). The lack of an upper fortification limit can lead to the “uncontrolled” fortification of these food products. Still, according to Arsenault and Brown (31), there have been no recent reports of zinc toxicity in US children, and overconsumption of zinc is unlikely to have a negative effect on health status of toddlers and preschoolers (31). Further research is needed into the effect of current zinc

intakes from both food and supplements on the copper status and immune function of children. If no adverse effects are found, the currently recommended UL values may need to be reconsidered (33). CONCLUSION The current study indicates the emerging need for the application of a holistic approach regarding toddlers and preschoolers’ diets that will incorporate both parental and caregivers’ involvement (34). This will help toddlers and preschoolers consume the recommended amounts of macronutrients and micronutrients, thus ensuring optimum growth and minimizing the risk of chronic diseases in adult life. The authors thank Evdokia Oikonomou, Vivian Detopoulou, Anastasia Anastasiadou, Christine Kortsalioudaki, Elina Ioannou, Margarita Bartsota, Manolis Birbilis, and Christos Vassilopoulos for their contribution to the completion of the study. References 1. Magkos F, Manios Y, Christakis G, Kafatos AG. Age-dependent changes in body size of Greek boys from 1982 to 2002. Obesity. 2006; 14:289-294. 2. Jolliffe D. Extent of overweight among US children and adolescents from 1971 to 2000. Int J Obes. 2004;28:4-9. 3. Angelopoulos PD, Milionis HJ, Moschonis G, Manios Y. Relations between obesity and hypertension: Preliminary data from a crosssectional study in primary schoolchildren. Eur J Clin Nutr. 2006;60: 1226-1234. 4. Muntner P, He J, Cutler JA, Wildman RP, Whelton PK. Trends in blood pressure among children and adolescents. JAMA. 2004;291: 2107-2113. 5. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH. Prevalence of a metabolic syndrome phenotype in adolescents. Findings from the Third National Health and Nutrition Examination Survey, 19881994. Arch Pediatr Adolesc Med. 2003;157:821-827. 6. Troiano RP, Briefel RR, Carroll MD, Bialostosky K. Energy and fat intakes of children and adolescents in the United States: Data from the National Health and Nutrition Examination Surveys. Am J Clin Nutr. 2000;72(suppl):S1343-S1353. 7. Devaney B, Ziegler P, Pac S, Karwe V, Barr SI. Nutrient intakes of infants and toddlers. J Am Diet Assoc. 2004;104(suppl 1):S14-S21. 8. Troiano RP, Flegal KM. Overweight children and adolescents: Description, epidemiology, and demographics. Pediatrics. 1998;101(3 Pt 2):497-504. 9. Gregory J, Collins D, Davies P, Hughes J, Clarke P. National Diet and Nutrition Survey: Children aged 1.5 to 4.5 years. Vol. 1. Report of the Diet and Nutrition Survey. London, UK: HMSO; 1995. 10. Andersen N, Fagt S, Groth M, Hartkopp H, Moller A, Ovesen N, Warming D. Dietary intakes for the Danish population 1995. Søborg, Denmark: The National Food Agency of Denmark. 1996. 11. Alexy U, Kersting M, Sichert-Hellert W, Manz F, Schoch G. Macronutrient intake of 3- to 36-month-old German infants and children: Results of the DONALD Study. Dortmund Nutritional and Anthropometric Longitudinally Designed Study. Ann Nutr Metab. 1999;43: 14-22. 12. Aravanis C, Mensink RP, Karalias N, Christodoulou B, Kafatos A, Katan MB. Serum lipids, apoproteins and nutrient intake in rural Cretan boys consuming high-olive-oil diets. J Clin Epidemiol. 1988; 41:1117-1123.

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