Diet patterns of lactovegetarian adolescent girls: Need for devising recipes with high zinc bioavailability

Diet patterns of lactovegetarian adolescent girls: Need for devising recipes with high zinc bioavailability

Nutrition 26 (2010) 390–398 Applied nutritional investigation www.nutritionjrnl.com Diet patterns of lactovegetarian adolescent girls: Need for dev...

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Nutrition 26 (2010) 390–398

Applied nutritional investigation

www.nutritionjrnl.com

Diet patterns of lactovegetarian adolescent girls: Need for devising recipes with high zinc bioavailability Rama Tupe, M.Sc. and Shashi A. Chiplonkar, Ph.D.* Agharkar Research Institute, Pune, India Manuscript received January 5, 2009; accepted May 23, 2009.

Abstract

Objective: Populations subsisting on plant foods are believed to be at a high risk of mineral deficiencies. The aim of the present study was to examine the diet patterns of vegetarian adolescent girls for zinc adequacy and devise recipes to improve bioavailable zinc intakes. Methods: A cross-sectional survey was carried out in 630 schoolgirls (10–16 y old) from Pune, India, from 2006 to 2007. Diet was assessed by a 24-h recall method on 3 random days. Diet patterns were identified by principal component analysis. Nutrient intakes were estimated using the cooked-foods database of our laboratory. Twenty recipes representing the diet patterns were formulated using foods that have a high zinc content and using methods such as sprouting/fermentation. In vitro zinc dialyzability of the recipes was determined by simulating gastrointestinal conditions and atomic absorption spectrometry. Results: Five diet patterns were identified reflecting intakes of different cereals. Girls in the five diet patterns had inadequate intakes of energy, protein, and micronutrients including zinc compared with the recommended dietary intakes of India. In the new cereal-based recipes, the average contents of energy, protein, iron, calcium, zinc, b-carotene, and vitamin C per 100 g of cooked weight were 205 kcal, 6.2 g, 2.5 mg, 105 mg, 1.5 mg, 716 mg, and 4.4 mg, respectively. Therefore, a supplement of 200 g of the recipe would fulfil 75% of the daily zinc requirement of adolescents and increase other micronutrient intake manifolds. Conclusion: Diets of Indian schoolgirls were deficient in zinc. Zinc-rich recipes with high bioavailability have the potential to alleviate zinc deficiency in adolescents. Ó 2010 Elsevier Inc. All rights reserved.

Keywords:

Diet; Adolescents; Micronutrients, Zinc-rich recipes; Zinc dialyzability

Introduction Eating healthy is an important part of a healthy lifestyle and healthful nutritional practices need to be inculcated during childhood and early adolescence. However, various studies across the world including India have reported unwholesome food habits in adolescents such as consumption of aerated drinks, fried foods, and non-inclusion of fruits and vegetables in the diet [1–3]. A significant proportion of Australian and Chinese adolescents have food intakes that fall short of their respective recommendations of healthy

*Corresponding author. Tel.: þ91-20-2565-4357; fax: þ91-20-25651542. E-mail address: [email protected] (S. A. Chiplonkar). 0899-9007/10/$ – see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.nut.2009.05.018

eating [4,5]. This results in nutritional deficiencies in adolescents, which in turn may affect their health [6]. Apart from caloric needs, adolescents require adequate amounts of micronutrients such as iron, vitamin A, calcium, and zinc to support the growth spurt. Nutritional surveys have shown that adolescents have the highest prevalence of deficiencies of calcium, iron, zinc, and vitamins A and C [7–12]. Nevertheless, studies on zinc intakes in Indian adolescents are scarce [13]. Most Indian adolescents are lactovegetarians, and even in the non-vegetarian Indian consumption of meat is less frequent [14,15], implying a higher risk of iron and zinc deficiencies. Despite the need to improve nutrient intakes of adolescents, very limited information exists about the eating habits of Indian adolescents. Dietary pattern analysis contributes to a better understanding of the relation between diet and health and developing

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targeted dietary interventions. Diet patterns do reflect the actual practices in the population under study and as such provide useful information to plan need-based populationspecific strategies [16]. A meta-analysis of intervention trials has indicated that multi-micronutrient interventions including zinc improve linear and possibly ponderal growth in children [17]. More sustainable food-based approaches such as natural fortification to improve micronutrient intakes of the children must be pursued. Most studies regarding enhancement of dietary quality and micronutrient status, especially those of iron and zinc, in schoolchildren were based on snacks including meat or dried fish [18,19]. Fortified wheat- and milk-based porridge with micronutrients and zinc was also found to have a positive effect on growth [20]. A study suggesting vegetarian food supplements, i.e., green leafy vegetables, has been done to improve the micronutrient status of Indian adults [21]. However, no such diet modification has been reported in schoolchildren. Considering the dietary habits of vegetarian adolescents, there is a need to develop sustainable dietary intervention using zinc-rich vegetarian food sources such as pearl millet, chickpeas, lentils, pumpkin seeds, and sesame to improve the zinc intake of adolescents. Vegetarian food sources of zinc also contain large quantities of phytates, which are known to be potent inhibitors of zinc absorption from composite meals. Several traditional household food-preparation methods such as thermal and mechanical processing, soaking, fermentation, and germination/ malting can increase zinc bioavailability in plant-based diets by increasing the physicochemical accessibility [22,23]. Use of these methods and appropriate food selection can improve bioavailable zinc intake in vegetarians. In the present study the diet patterns of Indian adolescent girls were evaluated for zinc adequacy and modifications were suggested in their existing diets to enhance intake of bioavailable zinc. Materials and methods Subjects All girls (n ¼ 662) were enrolled from two secondary schools of Pune, Maharashtra State, in Western India, for the cross sectional study. The age range of the girls in these schools was observed to be 10–16 y. Clinical examination was done by a physician to assess the health status of the girls. Only those who were free from chronic and acute illnesses were included in the study. The exclusion criteria are given below. Exclusion criteria Girls with any illness such as fever or respiratory or gastrointestinal infections, those taking medical treatment, or those with any illness in the recent past were excluded. Thirty-two girls met the exclusion criteria. Hence, data were collected for the remaining 630 apparently healthy girls.

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Prior consent of parents and willingness of the girls were obtained before the start of the study. The protocols were approved by the local ethical committee of the Zensar Foundation, India. The date of birth was recorded for each girl and age was calculated from the survey date. Body weight was measured to the nearest 0.1 kg on a weighing scale (Libra Industries, Mumbai, India) and standing height was measured to the nearest 0.1 cm with a stadiometer. Body mass index (BMI) was calculated as weight in kilograms divided by height squared in meters. Weight, height, and BMI were compared with the age- and sex-specific growth charts of India by Agarwal et al. [24,25] and the recent BMI growth charts 2007 of the World Health Organization (WHO) [26]. Assessment of dietary intakes Dietary intake was assessed by 24-h recall on 3 random days (non-consecutive) of a week including a holiday. Each girl was asked about the intake of food items consumed during the day at breakfast, lunch, dinner, and snacks, using standard cups and spoons by the trained investigators through a face-to-face interview. The recipes of food items were also recorded. The portion size was obtained by the average of actual weights of one serving of each food item from their households. This was done for each of the food items consumed such as rice, vegetables, chapatti (unleavened wheat pancake), etc. The individual food consumption was condensed to 12 food subgroups based on the major ingredients (Table 1). Plain rice, rice flakes, puffed rice were categorized under rice. Foods such chapatti, paratha, roti, and samolina were categorized under wheat. Unleavened pancakes and recipes including whole grain flours of pearl millet and sorghum Table 1 Dietary patterns identified by principal component analysis of mean consumption of foods in 12 food subgroups Food subgroup

Rotated factor pattern* RO

Rice Whole wheat Pearl millet Sorghum Bakery products Fried foods Sprouts Non-sprouted pulses Green leafy vegetables Other vegetables Milk Fruits

SnO

WO

PO

SO

0.457 0.673

0.356 0.300

0.368

0.794

0.859 0.336 0.781 0.311 0.768

0.326 0.300

0.535 0.444 0.750

0.449

0.604 0.764

PO, pearl millet-based observed diets; RO, rice-based observed diets; SnO, snack-type observed diets; SO, sorghum-based observed diets; WO, wheat-based observed diets * Varimax-rotated factor loadings for the factors. Values <0.30 are not listed.

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were included under the respective cereal groups. White bread, bun, cake, and biscuits were grouped under bakery products, and deep-fried potato balls, stuffed rolls, onionlegume balls, etc., under fried foods. Pulses were classified into two subgroups, i.e., sprouted and non-sprouted pulses. Vegetables were divided into two subgroups, i.e., green leafy vegetables and other vegetables. Daily nutrient intakes were calculated by applying nutritive values of cooked foods from the database of our laboratory [27]. This database refers to the contents of nutrients; phytates and fiber were estimated using five independent replicates of 246 food samples, which were analyzed in duplicate in the laboratory. For the consumption of raw foods such as fruits and salads, the nutritive value tables of National Institute of Nutrition (NIN), India, were applied [28]. Bioavailable zinc intakes were calculated by applying a predictive model for vegetarian meals, which included intakes of phytate, zinc, and folic acid as explanatory variables [29]. A similar predictive model was used for estimating the bioavailable iron intakes consisting of intakes of vitamin C, phytate, and tannins as explanatory variables [30]. Bioavailable zinc (or iron) intakes were estimated using these models separately for meals at breakfast, lunch, snacks, and dinner. The sum of all these bioavailable zinc (or iron) intakes was taken to be the whole day’s bioavailable intakes of zinc (or iron) for that girl.

database of nutrient composition of raw foods [28] and adjusting for observed moisture contents of cooked recipes. Estimation of total and dialyzable zinc of recipes A fresh sample of each recipe was homogenized and analyzed for zinc dialyzability in two independent sets. The method involved a simulated gastrointestinal digestion using pepsin for the gastric stage followed by pancreatin and bile salts for the intestinal stage. The proportion of zinc diffused through a semipermeable membrane (dialysis tubing) was used to measure the zinc dialyzability [32]. The contents of dialysate and homogenate were digested using MLS-1200 mega microwave digestion system with Microwave Digestion Rotor technology (Milestone, Bergamo, Italy, 1996) and the zinc content was determined by using an atomic absorption spectrometer (model 3110, Perkin Elmer, Norwalk, CT, USA). Statistical analyses

Recipes were devised considering the dietary habits of the girls. For each of the five diet patterns, three to four cerealbased recipes were prepared. All the food components in the recipes were procured from local city markets. For every recipe, laboratory analysis was carried out in duplicate for the nutrient contents and zinc dialyzability. For each of the five diet patterns, three to four cereal-based recipes were prepared (Appendix). To optimize dialyzable zinc content of the recipes, the following points were emphasized: 1) selection of zinc-rich foods from nutritive values tables [28], 2) addition of small amounts of sesame, dry coconut, and pumpkin seeds, and 3) use of germination, fermentation, and soaking to improve dialyzability. A small trial was conducted to judge the acceptability of the devised recipes in a pilot sample of 15 girls. Demonstration of the recipes was given to the group of girls and their mothers and they were asked to taste the recipes.

All statistical analyses were carried out using SPSS 11.0 for Windows (SPSS Inc., Chicago, IL, USA). The data were checked for normality by using a one-sample Kolmogorov-Smirnov test. Non-normal variables were log-transformed before performing further statistical analysis. Diet patterns were identified from the food intake data using principal component analysis. The components were rotated by an orthogonal transformation (varimax) to achieve a simpler structure with greater interpretability. The factor score coefficients were estimated by the regression method, which produces uncorrelated scores with a mean of 0 and a standard deviation of 1. The factor score indicated the degree to which the girls’ diet conformed to one of the dietary patterns identified. A high factor score for a given dietary pattern indicated high intake of the food groups constituting that food pattern. Therefore, the mean nutrient intakes and intakes of bioavailable iron and zinc by girls in the highest quintile of loading for each factor were used to demonstrate differences in the diet patterns [33]. For comparison of food intakes and nutrient intakes in the different diet patterns, non-parametric equivalent of one-way analysis of variance, i.e., the Kruskal-Wallis H test, was used for testing differences between diet patterns followed by the Mann-Whitney test for comparison of two means [34]. Spearman’s rank correlations were computed between food and nutrient intakes and anthropometric measurements.

Estimation of nutrient contents of recipes

Results

Moisture and fat contents of cooked foods were measured by methods according to the manual of the NIN [31]. Contents of b-carotene and vitamin C were measured by spectrophotometry as described in the NIN manual [31]. All estimations were done in duplicate. Energy, protein, calcium, and iron contents were computed using the Indian national

Anthropometric measurements

Development of recipes to increase total and dialyzable zinc content

The mean age of the girls was 12.2 6 1.1 y. The mean height and weight of the girls were 143.7 6 8.2 cm and 33.0 6 7.2 kg, respectively. Weight for age of 73.2% girls and height for age of 68.5% girls were below the respective

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Table 2 Selected healthy food intakes of girls across different dietary patterns* Foods Whole grains (%) Sprouts (g/d) Milk (mL/d) Leafy vegetables (g/d) Other vegetables (g/d) Fruits (g/d)

RO 43.8 6 21.7 7.6 6 18.1 20.0 6 50.2 10.4 6 18.6 34.8 6 36.0 —

SnO 52.4 6 19.0 14.9 6 27.6 23.0 6 45.0 9.8 6 17.2 28.7 6 36.3 51.4 6 66.7

WO y

69.1 6 16.8 25.1 6 43.5 87.1 6 100.4x 14.4 6 22.2 76.8 6 60.6{ —

PO

SO

53.5 6 22.6 60.6 6 50.3z 30.4 6 64.2 24.7 6 33.1jj 11.5 6 17.1 —

65.7 6 17.2y 10.2 6 18.2 12.3 6 35.5 26.8 6 34.3jj 50.4 6 56.1{ —

PO, pearl millet-based observed diets; RO, rice-based observed diets; SnO, snack-type observed diets; SO, sorghum-based observed diets; WO, wheat-based observed diets; —, average food intake <5 g/d * Values are means 6 SDs. Kruskal-Wallis test indicated significant differences among the five patterns for all healthy food intakes (P < 0.01). y Mean percentage of whole grains of wheat and sorghum meal patterns were significantly higher than the rice, snack-type, and pearl millet patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons). z Mean sprouts intake of the pearl millet pattern was significantly higher than the other four patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons). x Mean milk intake of the wheat pattern was significantly higher than the other patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons). jj The sorghum and pearl millet patterns had significantly higher mean green leafy vegetable intakes than the other patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons). { The wheat and sorghum patterns showed higher mean intakes of other vegetables than the other patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons).

50th percentile of the reference Indian standard [24]. Average BMI was 15.8 6 2.6 kg/m2 and 78.9% of the girls were below the 50th percentile of BMI for age of the reference Indian standard [25] and 81.0% were below the WHO standard [26]. Food and nutrient intakes Analysis of the diet recalls over 3 d revealed that the average intake of cereals was 199 6 69 g/d, that of legumes and pulses was 43 6 39 g/d, and average vegetable intake was 84 6 70 g/ d. The average intake of milk was 45 6 8 g/d. Intakes of fruits and animal foods (meat, fish, and poultry) were 13 6 4 and 7 6 3 g/d, respectively. The average intake of cereals was two-thirds and that of pulses and meat was around four-fifths of recommended food intakes by Indian dietary guidelines for adolescent girls [35]. Intakes of milk, vegetables, and fruit were less than 30% of the recommended amounts. The mean intakes of energy and protein were 1373 6 384 kcal/d and 30.3 6 9.6 g/d, which were 68.7% and 60% of the recommended dietary intakes (RDIs) [35], respectively. The average intakes of micronutrients were 30% to 60% of the respective RDIs. Average zinc intake (3.6 6 1.1 mg/d) was 30% of the RDI and almost all the girls (99.5%) had their zinc intake below the RDI [36]. Among food intakes, only cereal intake exhibited correlations of the order of 0.1 to 0.2 with weight, height, and BMI (P < 0.05). Weight and height were significantly correlated with intakes of energy, protein, calcium, zinc, and iron but not with vitamin intakes. BMI exhibited no significant correlation with nutrient intakes. Diet patterns Using principal component analysis, food intake data were aggregated in five patterns with Eigen values greater than 1 and explained about 55.1% of the variance (Table 1). Each

pattern was labeled according to the food group receiving high factor loading (>0.30) and thus five patterns were identified. The observed diet patterns were categorized as 1) rice meal (RO), 2) snack type (SnO), 3) wheat meal (WO), 4) pearl millet meal (PO), and 5) sorghum meal (SO). These five diet patterns were evaluated with respect to healthy food intakes (Table 2). The Kruskal-Wallis test indicated significant differences among the five patterns for all healthy food intakes (P < 0.01). The Mann-Whitney test resulted in a significantly higher mean percentage of whole grains for WO and SO patterns than for RO, SnO, and PO patterns (P < 0.05). The mean sprouts intake of the PO pattern was significantly higher than the other four patterns (P < 0.05). Sprouts consumption was very low in the RO and SO patterns. Mean milk intake of the WO pattern was significantly higher than the other patterns (P < 0.01). The SO and PO patterns had significantly higher mean green leafy vegetable intakes than the other patterns (P < 0.01). The WO and SO patterns showed higher mean intakes of other vegetables than other patterns (P < 0.05). Fruit consumption was notable only in the SnO pattern. The mean nutrient intakes and intakes of bioavailable iron and zinc by the girls in the highest quintile of loading for each factor are presented in Table 3. The Kruskal-Wallis test indicated significant differences among the five patterns for all nutrient intakes (P < 0.01) except energy and carbohydrate intakes. The Mann-Whitney test indicated that protein and calcium intakes of the WO pattern were significantly higher than the other patterns (P < 0.05). Fat intakes of the RO, SnO, and WO patterns were similar but significantly higher than the SO and PO patterns (P < 0.05). The mean vitamin C intake was significantly higher in the SnO pattern than the RO and PO patterns (P < 0.01). Mean intake of b-carotene of the WO pattern was significantly higher than the RO pattern (P < 0.01), whereas differences in means of the other diet patterns were not significant. Mean iron intake of

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Table 3 Mean daily nutrient intakes and intakes of bioavailable iron and zinc in the highest quintile of dietary pattern scores* Nutrient intake/d

RO

SnO

WO

PO

SO

Energy (kcal) Protein (g) Fat (g) CHO (g) Phytate-Phosphorus (mg) Fiber (g) Vitamin C (mg) b-carotene (mg) Calcium (mg) Iron (mg) Zinc (mg) Bioavailable iron (mg) Bioavailable zinc (mg)

1474 6 358 29.7 6 8.6 55.1 6 13.4z 212.2 6 61.1 191.8 6 85.5 17.8 6 6.6 19.7 6 9.4 588 6 370jj 252 6 120 5.8 6 1.6 2.5 6 1.0** 0.48 6 0.16zz 0.29 6 0.11xx

1452 6 372 29.1 6 7.7 45.3 6 15.1z 231.2 6 55.6 253.8 6 112.1 23.9 6 9.0 36.7 6 13.5x 898 6 548 241 6 78 6.7 6 1.8 2.9 6 1.1yy 0.65 6 0.24 0.35 6 0.13

1629 6 304 38.3 6 5.6y 55.8 6 11.6z 232.7 6 58.9 316.0 6 77.8 20.5 6 6.9 33.1 6 13.5 1354 6 980 534 6 139{ 7.0 6 1.6 4.4 6 0.8 0.66 6 0.18 0.43 6 0.06

1411 6 340 32.7 6 10.0 43.5 6 14.0 217.4 6 52.9 240.0 6 79.0 18.8 6 6.0 30.6 6 12.3 1022 6 623 402 6 123 7.4 6 1.5 3.9 6 1.0 0.71 6 0.15 0.44 6 0.08

1484 6 407 29.1 6 8.8 43.5 6 14.2 242.7 6 64.9 358.0 6 108.6 27.3 6 6.5 20.8 6 8.2 911 6 834 268 6 119 8.8 6 1.8# 4.0 6 1.1 0.79 6 0.15 0.42 6 0.11

CHO, carbohydrate; PO, pearl millet-based observed diets; RO, rice-based observed diets; SnO, snack-type observed diets; SO, sorghum-based observed diets; WO, wheat-based observed diets * Values are means 6 SDs. Kruskal-Wallis test indicated significant differences among the five patterns for all nutrient intakes (P < 0.01) except energy and CHO intakes. y Mean protein intake of the WO pattern was significantly higher than the other patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons). z Mean fat intakes of the RO, SnO, and WO patterns were similar but significantly higher than the SO and PO patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons). x Mean vitamin C intake was significantly higher in the SnO pattern than the RO and PO patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons). jj Mean b-carotene intake of the WO pattern was significantly higher than the RO pattern (P < 0.01, Mann-Whitney test results for pairwise comparisons), whereas other differences in means were not significant. { Mean calcium intakes of the WO pattern were significantly higher than the other patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons). # Mean iron intake of the SO pattern was significantly higher than the RO, SnO, and WO patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons) but similar to the PO pattern. ** Mean zinc intake of the RO pattern was significantly lower than the WO, PO, and SO patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons). yy Mean zinc intake of the SnO pattern was significantly lower than the WO and SO patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons). zz Mean intake of bioavailable iron from the RO pattern was the lowest among all patterns (P < 0.05, Mann-Whitney test results for pairwise comparisons) and there were no significant differences among mean bioavailable iron intakes in the SnO, WO, PO, and SO patterns. xx Mean intake of bioavailable zinc of the RO pattern was significantly lower than the WO, PO, and SO patterns (P < 0.01, Mann-Whitney test results for pairwise comparisons) but similar to the SnO pattern.

the SO pattern was significantly higher than the RO, SnO, and WO patterns (P < 0.01) but it was similar to the PO pattern. Mean zinc intake of the RO pattern was significantly lower than the WO, PO, and SO patterns (P < 0.01). Mean zinc intake of the SnO pattern was significantly lower than the WO and SO patterns (P < 0.01). Mean intake of bioavailable iron from the RO pattern was lowest among all patterns (P < 0.05) and there were no significant differences among mean bioavailable iron intakes of the SnO, WO, PO, and SO patterns. Mean intake of bioavailable zinc of the RO pattern was significantly lower than the WO, PO, and SO patterns (P < 0.01) but similar to the SnO pattern. In general, girls with the RO and SnO patterns had low micronutrient intakes, whereas those with the WO or SO patterns had higher amounts of micronutrients in their diets (P < 0.05). However, all diet patterns were deficient in micronutrients including zinc when compared with the RDI [35].

and 6.2 6 1.8 g, respectively. Side-dish items had an average content of 269 6 153 kcal of energy and 9.5 6 3.4 g of protein per 100 g of cooked weight, respectively (Table 4). Mean zinc content of the cereal-based recipes (1.5 mg/ 100 g) was lower than the side-dish items (3.1 mg/100 g of cooked weight; Table 4). Zinc content was highest in the sesame and groundnut ladu side dish, although its percent dialyzability was low. Some of the recipes such as broken wheat with vegetable upma, wheat roti with sprout curry and vegetable salad, and sorghum roti with sprout curry and curd had less than 1 mg of zinc, probably due to their high moisture content. Zinc dialyzability of fermented products (rice with pulses and vegetable idli with spinach paste, whole wheat bread with vegetable sandwich with spinach paste) and sprouts (pulses tikki) was higher than in recipes containing non-sprouted pulses (rice and split pulse with sesame and milk, broken wheat and vegetable upma, pearl millet roti and pulses paste).

Nutrient composition and percent dialyzability of zinc of the recipes

Potential of new recipes as zinc supplements to diet patterns

Average contents of energy and protein per 100 g of cooked weight of cereal-based recipes were 205 6 76 kcal

New recipes were evaluated as promising zinc supplements against the prevailing diet patterns using dialyzable

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Table 4 Nutrient composition of recipes per 100 g of cooked weight and percent zinc dialyzability Recipe code*

Water (%)

Cereal-based recipes R1 43.9 R2 65.2 R3 66.2 Sn1 53.1 Sn2 59.0 W1 66.9 W2 72.8 W3 72.7 W4 40.8 W5 0.8 P1 42.2 P2 46.6 P3 55.3 S1 74.0 S2 41.4 S3 42.5 Mean 6 SD 52.7 6 18.5 Side dishes Sd1 75.7 Sd2 57.1 Sd3 18.0 Sd4 16.9 Mean 6 SD 41.9 6 29.2

Energy (kcal)

Protein (g)

Fat (g)

Calcium (mg)

Iron (mg)

Zinc (mg)

b-carotene (mg)

Vitamin C (mg)

Zinc dialyzability (%)

244 220 151 200 128 151 123 123 276 388 232 213 171 106 276 278 205 6 76

6.2 8.4 5.8 5.3 4.0 4.5 4.2 4.1 8.6 8.1 8.0 7.1 6.0 3.3 7.2 7.9 6.2 6 1.8

9.0 1.6 3.7 7.1 10.0 8.2 3.4 3.2 6.2 10.2 5.9 4.8 3.7 1.0 13.3 12.8 6.5 6 3.4

55 81 289 127 95 33 64 79 24 62 56 56 96 45 284 199 105 6 81

2.4 1.5 1.7 2.6 1.6 1.3 1.4 1.3 1.9 4.8 4.3 3.6 3.6 1.0 3.1 3.5 2.5 6 1.2

1.3 2.6 1.1 1.6 1.2 0.8 0.7 0.8 1.2 1.4 2.1 2.2 2.2 0.8 2.5 2.2 1.5 6 0.6

340 1352 216 476 2224 1680 100 96 544 328 1040 920 304 80 1240 520 716 6 634

2.8 3.2 — 2.8 6.6 6.0 8.2 5.1 5.0 2.2 7.2 2.1 5.7 2.1 5.3 5.6 4.4 6 2.2

14.0 30.7 12.6 14.4 30.2 12.2 20.7 18.6 15.8 7.5 13.3 14.5 24.9 24.1 11.1 25.6 18.3 6 6.8

93 195 364 426 269 6 152

4.4 11.7 10.9 10.8 9.5 6 3.4

1.3 3.5 0.9 22.0 6.9 6 10.1

64 159 142 547 228 6 216

1.6 3.5 3.8 3.8 3.2 6 1.1

1.6 2.9 2.6 5.1 3.1 6 1.5

480 640 — — 280 6 329

4.9 2.7 — — 1.9 6 2.3

21.0 26.4 12.3 10.2 17.5 6 7.6

P1–P3, pearl millet–based recipes; R1–R3, rice-based recipes; S1–S3, sorghum-based recipes; Sd1–Sd4, side dishes; Sn1–Sn2, snack-type recipes; W1–W5, wheat-based recipes * Recipe codes are described in detail in the Appendix.

zinc contents (Appendix). For each diet pattern, dialyzable zinc intakes of the girls per 100 g of cooked weight were estimated using a predictive model for zinc dialyzability [29]. Figure 1 demonstrates the increase in mean dialyzable zinc content of suggested zinc-rich meals against mean dialyzable zinc intakes of the observed diet patterns. The Kruskal-Wallis

test indicated that mean dialyzable zinc of recipes was significantly higher than that of the respective means of the observed diet patterns (P < 0.01). The predicted amount of dialyzable zinc content per 100 g of cooked weight was lowest for the RO pattern (0.05 mg) and highest for the PO pattern (0.071 mg). Mean dialyzable zinc content of the RO pattern increased by eight times with the new recipes. Similarly, mean dialyzable zinc contents of the new recipes was three to five times more than the other diet patterns. Dialyzable zinc of the side-dish items, i.e., pulses tikki and sesame/groundnut ladu, was more than 10 times that of the contents in the diet patterns.

Other micronutrient contents

Fig. 1. Mean dialyzable zinc content of observed diets and suggested zincrich meals. The Kruskal-Wallis test indicated that the mean dialyzable zinc of recipes was significantly higher than that of the observed diets (P < 0.01). PE, pearl millet-based experimental meals; PO, pearl millet-based observed diets; RE, rice-based experimental meals; RO, rice-based observed diets; SE, sorghum-based experimental meals; SnE, snack-type experimental meals; SnO, snack-type observed diets; SO, sorghum-based observed diets; WE, wheat-based experimental meals; WO, wheat-based observed diets.

b-Carotene and vitamin C contents of the five diet patterns varied from 82 to 158 mg and from 2.8 to 5 mg per 100 g of cooked weight, respectively. Proposed new recipes based on different cereals had 4 to 12 times more b-carotene than the contents of the diet patterns. A marginal (20%) to substantial (95%) increase was observed in vitamin C content of recipes over the five diet patterns. Average contents of iron and calcium of the five diet patterns were 1.05 and 41.4 mg per 100 g of cooked weight, respectively. The new recipes exhibited more than a double increase in mean iron and calcium contents than the five diet patterns.

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Discussion We identified five diet patterns that were prevalent in schoolgirls from western India. Each diet pattern was characterized by typical combinations of food subgroups such as rice with pulses, whole wheat with vegetables, sprouts and bakery products, etc. In all five diet patterns, intakes of whole grain, leafy vegetables, sprouts, milk, and fruit were inadequate, suggesting dietary deficiency of macro- and micronutrients in the study population. Other studies in southern and northern Indian adolescents have also observed less consumption of millets, vegetables, fruits, and milk by girls [1,37]. A similar observation has been reported on Australian girls that the daily consumption of foods from the five recommended food groups was inadequate and consumption of fruit was rare [38], leading to micronutrient deficiencies in adolescents. Similar to our study, inadequate macro- and micronutrient intakes have been reported in Indian adolescents in national diet surveys [12,14]; however, data on zinc intake are scarcely reported. In one study on residential schoolchildren in India [20], the average zinc intake (7.0 6 1.1 mg/d) and iron and calcium intakes were higher than those reported in the present study. This may be because our schoolgirls were free-living and did not have a healthy diet compared with the diets of residential schoolchildren. Low habitual zinc intakes (78% of the dietary reference intakes) have also been reported in adolescent girls (14–18 y) from Brazil [39]. Our proposed recipes were rich in zinc and other micronutrients and these were formulated considering the daily food consumption pattern of the girls and by using locally available foods. The girls have reported more than 90% acceptance to almost all of the 20 recipes. In the proposed cereal-based recipes, average contents of energy, protein, iron, calcium, zinc, b-carotene, and vitamin C per 100 g of cooked weight were 205 kcal, 6.2 g, 2.5 mg, 105 mg, 1.5 mg, 716 mg, and 4.4 mg, respectively. Thus, these food-based interventions are feasible to improve micronutrient intakes of the girls. The average zinc content (1.5 mg/100 g of cooked weight) of cereal-based recipes was three times more than the average daily intake (0.47 mg/100 g of cooked weight) of the girls. Therefore, a supplement of 200 g (equivalent to one meal of the girls) of cereal-based recipe will be able to fulfil 75% of the daily zinc requirement of adolescents. It can also increase average contents of b-carotene, vitamin C, iron, and calcium manifolds compared with their habitual diet patterns. Our proposed recipes in this study yield higher zinc (3.3 mg/225 g) than the zinc-rich snacks containing meat for Kenyan schoolchildren providing 2.89 mg/225 g of zinc [18]. Dietary intervention strategies have also been reported to increase intakes of total and bioavailable zinc of maize-based Malawian diets using dried fish by 152% [19], which is less than manifold increase shown in the present study. Moreover, our study attempted to increase the bioavailable

zinc intakes for vegetarians without inclusion of meat or fish products. Inadequate micronutrient intakes have been reported in growing children and adolescents in India [12,14] and across the world [8–10]. Although dietary habits across different states of India are diverse, the recipes proposed in this study are based on different cereals and micronutrient-rich foods and, hence, can be adopted to improve the micronutrient intakes of different population groups. Thus, the new cerealbased recipes will provide food-based interventions for vegetarian populations such as Indians. These recipes need to be tested through supplementation trials for their utility and adequacy in terms of meeting daily requirements. In conclusion, the diets of Indian adolescent girls were deficient in zinc and other micronutrients; dietary interventions in the form of the proposed recipes need to be adopted to alleviate deficiencies of zinc, calcium, iron, b-carotene, and vitamin C. Acknowledgments The authors thank the director of ARI for providing the necessary facilities for carrying out this work. This study was part of a project by the Zensar Foundation, India. References [1] Raghunatha-Rao D, Vijayapushpam T, Subba-Rao GM, Antony GM, Sarma KVR. Dietary habits and effect of two different educational tools on nutrition knowledge of school going adolescent girls in Hyderabad, India. Eur J Clin Nutr 2007;61:1081–5. [2] Vereecken CA, De Henauw S, Maes L. Adolescents’ food habits: results of the Health Behaviour in School-aged Children survey. Br J Nutr 2005;94:423–31. [3] Cavadini C, Siega-Riz A, Popkin BM. US adolescent food intake trends from 1965 to 1996. West J Med 2000;173:378–83. [4] Savige GS, Ball K, Worsley A, Crawford D. Food intake patterns among Australian adolescents. Asia Pac J Clin Nutr 2007;16:738–47. [5] Shi Z, Lien N, Kumar BN, Holmboe-Ottesen G. Socio-demographic differences in food habits and preferences of school adolescents in Jiangsu Province, China. Eur J Clin Nutr 2005;59:1439–48. [6] McNaughton SA, Ball K, Mishra GD, Crawford DA. Dietary patterns of adolescents and risk of obesity and hypertension. J Nutr 2008; 138:364–70. [7] Johnson RK, Johnson DG, Wang MQ, Smiciklas-Wright H, Guthrie HA. Characterizing nutrient intakes of adolescents by socio-demographic factors. J Adolesc Health 1994;15:149–54. [8] Gibson RS, Heath ALM, Ferguson EL. Risk of suboptimal iron and zinc nutriture among adolescent girls in Australia and New Zealand: causes, consequences, and solutions. Asia Pacific J Clin Nutr 2002;11:S543. [9] Mahmoodi MR, Kimiagar SM. Prevalence of zinc deficiency in junior high school students of Tehran City. Biol Trace Elem Res 2001; 81:93–103. [10] Hettiarachchi M, Chandrani L, Rajitha W, David CH, Steven AA. Prevalence and severity of micronutrient deficiency: a cross-sectional study among adolescents in Sri Lanka. Asia Pac J Clin Nutr 2006; 15:56–63. [11] Bhatia V. Dietary calcium intake—a critical reappraisal. Indian J Med Res 2008;127:269–73. [12] Srihari G, Eilander A, Muthayya S, Kurpad AV, Seshadri S. Nutritional status of affluent Indian school children: what and how much do we know? Ind Pediatr 2007;44:199–203.

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Appendix

Food composition of recipes Code

Recipes

Cereal-based recipes R1 Sprouts and vegetable pulav

W2

Wheat roti, sprout curry, vegetable salad

W3

Wheat roti, sprout curry, orange

W4 W5 P1

Wheat and leafy vegetable paratha Wheat and pulses ladu Pearl millet roti and pulses paste

P2 P3

Pearl millet roti with onion stalk Pearl millet roti and cabbage salad

S1 S2

Sorghum roti with sprout curry and curd Finger millet and pulse with leafy vegetable paratha with spinach paste Mixed flours with leafy vegetable paratha

R3 Sn1 Sn2

S3 Side dishes Sd1 Sd2 Sd3 Sd4

Sprout vegetable salad Pulses tikki Amaranthus seeds ladu Sesame and groundnut ladu

Rice (50), sprouted lentil (10), sprouted green gram (10), tomato (10), onion (10), coriander leaves (10), mint (10), coconut dry (10) (sprouting, pressure cooking) Fermented batter of parboiled rice (25), split black gram (50), split green gram (25), split chickpea (25), soybean (25) steamed with carrot (10) (fermentation); raw paste of spinach (25), coriander leaves (10), sesame (5), pumpkin seeds (5), lemon juice (5) Rice (35), split red gram (20) with onion (10), tomato (8), sesame (10) (pressure-cook); milk (200) Whole wheat bread (40), with topping of butter (5); sprouts of lentil (10) and green gram (10) (sprouting, fermentation, steaming) Whole wheat bread (40), (fermentation) with topping of butter (5), cucumber (10), tomato (10), raw paste of spinach (25), coriander leaves (10), sesame (5), pumpkin seeds (5), lemon juice (5) Broken wheat (100), split black gram (20), carrot (10), capsicum (10), peas (10), onion (10), tomato (10), groundnuts (25), coconut dry (10) (pressure cook) Unleavened pancake of wheat flour (35), moth bean sprouts (25), onion (10), coriander leaves (5), carrot (25), cucumber (10), onion (25) (sprouting) Unleavened pancake of wheat flour (35), green gram sprouts (25) and soaked soybean (15), onion (10), coriander leaves (10); orange (50) (sprouting) Unleavened pancake of wheat flour (50), fenugreek leaves (25), sesame (5) (shallow frying, leafy vegetables) Wheat flour (25), chickpea flour (25), soybean flour (12), rice flakes (25), pumpkin seeds (25) (roasted) with balls made with jaggery (75) Unleavened pancake of pearl millet flour (90) (roasted); soaked split chickpea (20), green gram (20), coconut (20), lemon (10), coriander leaves (20) Unleavened pancake of pearl millet flour (90) (roasted); onion stalk (65), split green gram (15) (steaming, leafy vegetables) Unleavened pancake of pearl millet flour (90) (roasted); cabbage (25), tomato (20), coriander leaves (10), sesame powder (5), lemon juice (5) (raw salad) Unleavened pancake of sorghum flour (90) (roasted); moth bean sprouts (45), onion (10), coriander leaves (5) (sprouting, steaming), curd (50) Unleavened pancake of finger millet flour (30), chickpea flour (10) fenugreek leaves (10), coriander leaves (10), sesame (10) (green leafy vegetables, shallow frying); paste of spinach (25), coriander leaves (10), sesame (5), pumpkin seeds (5), curd (25) (raw salad) Unleavened pancake of sorghum flour (50), wheat flour (50), pearl millet flour (50), chickpea flour (20), fenugreek leaves (100), sesame (15), oil (5) Bengal gram sprouts (50) (sprouting and cooking); onion (10), coriander leaves (5), tomato (20), lemon juice (5), pomegranate (5) (raw salad) Soybean (50) and chickpea (50) coarsely ground with coriander leaves (10), mint (10) soaked and made in flat rounds (shallow fried) Balls of puffed Amaranthus seeds (20), groundnuts (5), jaggery (20) Balls of roasted sesame (20) and groundnut (10), jagerry (20)

R. Tupe and S. A. Chiplonkar / Nutrition 26 (2010) 390–398

W1

Rice with pulses and vegetable idli with spinach paste Rice and split pulse with sesame and milk Whole wheat bread with sprouts sandwich Whole wheat bread with vegetable sandwich with spinach paste Broken wheat and vegetable upma

R2

Description of recipes (ingredients in grams)