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Green and yellow vegetables can maintain body stores of vitamin A in Chinese children^1,2,3

¹ From the Jean Mayer US Department of Agriculture, Human Nutrition Research Center on Aging at Tufts University, Boston; the Tai-an Medical College, Tai-an City, Shandong, China; the Institute of Nutrition and Food Hygiene, Chinese Academy of Preventive Medicine, Beijing; and the International Atomic Energy Agency, Vienna.

² Supported by the Ministry of Public Health, People's Republic of China; USDA/ARS contract no. 58-1950-9-001; International Atomic Energy Agency grant no. RIHU-NAHRES 8708/8714; and Thrasher Research Fund no. 02813-2.

³ Address reprint requests to G Tang, Jean Mayer USDA, Human Nutrition Research Center on Aging at Tufts University, 711 Washington Street, Boston, MA 02111. E-mail: GTang{at}hnrc.tufts.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: Vitamin A activity of plant provitamin A carotenoids is uncertain.

Objective: The objective was to determine whether plant carotenoids can sustain or improve vitamin A nutrition during the fall season in kindergarten children in the Shandong province of China.

Design: The serum vitamin A concentration of 39% of the children was <1.05 µmol/L and of 61% of the children was 1.05 µmol/L. For 5 d/wk for 10 wk, 22 children were provided 238 g green-yellow vegetables/d and 34 g light-colored vegetables/d. Nineteen children maintained their customary dietary intake, which included 56 g green-yellow vegetables/d and 224 g light-colored vegetables/d. Octadeuterated and tetradeuterated vitamin A were given before and after the interventions, respectively, and their enrichments in the plasma were determined by gas chromatography–mass spectrometry. Serum retinol and carotenoid concentrations were measured by HPLC.

Results: Carotenoid nutrition improved after consumption of green-yellow vegetables. Serum concentrations of retinol were sustained in the group fed green-yellow vegetables but decreased in the group fed light-colored vegetables (P < 0.01). The isotope-dilution tests confirmed that total-body vitamin A stores were sustained in the group fed green-yellow vegetables, but decreased 27 µmol (7700 µg retinol) per child, on average, in the group fed light-colored vegetables (P < 0.06).

Conclusion: Green-yellow vegetables can provide adequate vitamin A nutrition in the diet of kindergarten children and protect them from becoming vitamin A deficient during seasons when the provitamin A food source is limited.

Key Words: Green-yellow vegetables • deuterated vitamin A • China • kindergarten children • total-body vitamin A stores

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Recommendations for sustainable improvements in vitamin A status are that they should be food based, commence early in life, and be consumer driven (1). At issue, however, are practical means for incorporating foods that are sufficiently rich in provitamin A carotenoids into the diets of those most vulnerable to vitamin A deficiency in ways that will meet the recommendations and sustain adequate vitamin A status. Nested within the issue of planning or evaluating food-based approaches is some uncertainty about the actual bioavailability of provitamin A carotenoids and thus uncertainty about the extent to which the theoretical bioavailability and conversion to retinol are accurate. Even though the conversion of ß-carotene to vitamin A in humans has been shown both in vitro and in vivo (2–5) and was investigated by using stable-isotope-labeled synthetic ß-carotene (6–9), the bioavailability of provitamin A carotenoids from plant food sources is uncertain.

In China, plant provitamin A carotenoids account for 70% of dietary vitamin A (10). As in many developing countries, seasonal variations in availability of plant foods result in fluctuations in intake, and thus vitamin A status declines during the fall and winter seasons. Plant foods consumed during the fall months by people living in the province of Shandong, south of Beijing, are mainly cabbage, Chinese cabbage, potato, and turnip. Children's diets contain even smaller quantities of plant carotenoids than those of the adults, a factor thought to contribute to the problems of vitamin A deficiency among Chinese children (11). In general, the regular diet of adults at this time of year in Shandong, China, provides 2 mg carotenoids/d, with 1 mg/d as ß-carotene (12).

The effectiveness of plant carotenoids in combating vitamin A deficiency or vitamin A inadequacy was questioned by de Pee et al (13), who provided lactating women with stir-fried, dark-green leafy vegetables, and by Bulux et al (14), who added 50 g cooked carrots to the daily diets of children aged 7–12 y. Both studies found no evidence of nutritional benefit of vitamin A after an increased consumption of dark green or yellow vegetables.

Vitamin A status has been evaluated by using dietary assessment tools, functional tests such as dark adaptation testing, isotope-dilution techniques, and biochemical methods such as the measurement of blood concentrations of vitamin A, retinol binding protein, and blood responses to a dose of vitamin A or dehydrovitamin A (relative-dose-response and modified-relative-dose-response tests) (15). Of these methods, total-body vitamin A stores can only be measured quantitatively by using techniques based on isotope dilution (16–20).

The purpose of this study was to determine whether vitamin A status can be sustained or improved by increasing the dietary intake of carotenoid-rich vegetables during seasons when the natural availability of plant-based carotenoids is low and vitamin A status is therefore in jeopardy. To target young children, a vulnerable population in China, and to ensure that all the food provided in the intervention was consumed by the target group, an intervention was conducted in a kindergarten where the children consume nearly all of their meals during weekdays. The intervention was conducted over a 10-wk period, the approximate duration of the typical seasonal decline in the availability of foods rich in provitamin A carotenoids. To strengthen the assessment of the biological effect of the intervention, vitamin A isotopically labeled with deuterium was administered before and after the intervention with either green-yellow or light-colored vegetables, and the total-body vitamin A stores were measured by isotope-dilution techniques.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Subjects
The study was carried out in a kindergarten in Tai-an city, Shandong province, 600 km south of Beijing. Most inhabitants are middle-income, working people. The intervention was explained during a parent-teacher meeting and informed consent was obtained from parents before their children participated. The study was approved by the Committee on Human Research, the Institute of Nutrition and Food Hygiene, Chinese Academy of Preventive Medicine, Beijing, and by the Human Investigation Committee at Tufts University and the New England Medical Center, Boston.

The kindergarten population was composed of children from the Shandong province aged 3–7 y. All the children who regularly attended the Red Gate Kindergarten, who were aged 5–6.5 y, who were generally healthy, and who could eat 3 meals at school every weekday (5 d/wk, excluding holidays), were considered eligible for enrollment. Children with a fever at the time of enrollment in the study (>38°C) or a C-reactive protein concentration >6 mg/L were excluded from the study.

Design
Of the 300 children in the kindergarten school, 50 who had already been divided by teachers into 2 kindergarten classes with identical socioeconomic backgrounds met the eligibility criteria and were enrolled in the study. One of the groups was arbitrarily selected by the teachers to consume dark-green and yellow vegetables (green-yellow-vegetable group), whereas the other group was to consume light-colored vegetables (light-colored-vegetable group), which were customarily provided through the school meal program during the fall season (from September to November). The trial was carried out over 16 consecutive weeks, which included an initial 3-wk period to assess vitamin A status before the interventions, a 10-wk period (47 school days) of vegetable intervention, and a 3-wk final period to assess vitamin A status after the interventions. Forty-six children (27 in the green-yellow-vegetable group and 19 in the light-colored-vegetable group) finished the study. However, of these children, 5 subjects in the green-yellow-vegetable group were unable to donate sufficient blood samples for analyses. Thus, data from a total of 41 children (22 in the green-yellow-vegetable group and 19 in the light-colored-vegetable group) were included in the final analysis. These children were aged 5.3–6.4 y, had a height between 26% and 91%, and had a weight between 30% and 95% of the Chinese National Nutrition Survey standards of 1992 (10). In comparison, these anthropometric data fell between the 10th and 85th percentiles for height and the 5th and 95th percentiles for weight in the growth charts of the US National Center for Health Statistics (21). The characteristics of participants at baseline and after the intervention are shown in Table 1. Vitamin A concentrations were 1.05 µmol/L in 61% of the children and <1.05 µmol/L in 39% of the children at the beginning of the intervention (22).

Supplementation and recording of nutrient intakes
The availability of fruit and vegetables in Shandong province fluctuates with the season. In the fall, light-colored vegetables such as cabbage, Chinese cabbage, potatoes, and turnips are most abundant and least expensive, as are tangerines, which tend to be a rich source of cryptoxanthin. All vegetables used in the intervention were purchased at the local market.

Kindergarten children in the province usually consume 2 meals and 2 snacks per day at school (breakfast at 0800, morning snack at 1000, lunch at 1200, and afternoon snack at 1400) and eat supper at home. During the 10-wk intervention period, the 50 original participants, who had already been divided by teachers into 2 kindergarten classes, consumed all 3 meals (including supper at 1700) at school. Each meal or snack for the green-yellow-vegetable group was patterned after the comparable meal or snack for the light-colored-vegetable group, both in terms of composition and preparation method, except for the substitution of the darker-colored vegetables for the lighter-colored ones. During the vegetable intervention, the 2 groups consumed equal amounts of energy, fat, protein, and preformed vitamin A (determined by Chinese food-composition tables; 23) but different amounts of carotenoids (as determined by HPLC and a paper chromatographic method, as described below). The recommended dietary allowance (RDA) of vitamin A for this age group in China is 750 µg retinol equivalents (RE)/d (24, 25).

The 2 groups of children ate in their separate classrooms to obviate the possibility that food could be exchanged between them or consumed by other family members. Food preparation methods included traditional stir-frying or steaming of minced green-yellow vegetables or light-colored vegetables. Food was provided to each child in near identical portions ladled from a big pot by the same cook. Vegetable consumption for each meal, per child, was calculated based on the amount of fresh vegetables used to make the total meal and the number of children who shared the meal. Compliance was ensured by the kindergarten teachers. All food from the pot was finished at each meal. For foods consumed at home on weekends and holidays, a food diary was completed by parents and collected by teachers weekly. This information was used to calculate the food intakes at home and to check for any unusually high intakes of carotenoids or preformed vitamin A. The results showed that both groups consumed equal amounts of nutrients but consumed fewer vegetables during weekends and holidays than during school days (data not shown).

Dilution of deuterated retinol and estimation of total-body vitamin A stores
On the basis of previous studies (16–20), total-body vitamin A stores can be calculated by using a modified version of the equation of Bausch and Rietz (19). We administered vitamin A labeled with 2 different amounts of deuterium before and after the intervention to estimate changes in total-body vitamin A stores that occurred over the 10-wk vegetable intervention. Each child was given a physiologic dose (3.0 mg, or 0.45 µmol/kg body wt) of octadeuterated vitamin A (all-trans-10,14,19,19,19,20,20,20-[²H₈]retinyl acetate; D₈ vitamin A) 21 d before the vegetable intervention began and a dose of tetradeuterated vitamin A (all-trans-10,19,19,19-[²H₄]retinyl acetate; D₄ vitamin A) after the vegetable intervention ended because our analytic method can differentiate D₄ retinol from D₈ retinol in the circulation. Under red lights, D₄ and D₈ vitamin A in ethanol were each dissolved in 170 mg corn oil, blown over a nitrogen flow and vacuum dried overnight until weight-stable, and encapsulated into no. 4 gelatin capsules before being administered. Teachers and health workers distributed the vitamin A capsules and water to the children, who consumed them orally and then immediately ate their lunches, which contained 30% of energy from fat.

Children (n = 41) either had their blood drawn at 3 d (3-d subgroup; n = 23), to investigate vitamin A status qualitatively, or at 21 d (21-d subgroup; n = 18), to investigate vitamin A status quantitatively by measuring total-body vitamin A stores, after being given the labeled doses of vitamin A. On the basis of our previous experiments (26), 21 d was chosen as the equilibrium time point after consumption of labeled vitamin A.

Vitamin A status
To assess baseline vitamin A status before the intervention began, we gave all children a labeled D₈ vitamin A dose on the same day (0 d) and collected serum samples at 3 or 21 d. The intervention began immediately after the 21-d sample. The second labeled vitamin A dose (D₄ vitamin A) was given 2 d after completion of the 10-wk dietary intervention to allow for absorption of the dietary carotenoids. Serum samples were again collected at 3 d from the 3-d subgroup and at 21 d from the 21-d subgroup after the D₄ vitamin A dose. During these 2 periods (before the intervention and after the intervention), all children ate their routine breakfast and lunch at school but ate their supper at home (see above). The changes in total body stores before and after the intervention were measured. The differences in changes in total body stores between the 2 groups were evaluated against the differences in provitamin A carotenoid intakes between the 2 groups.

Blood sampling
A fasting serum sample (<3 mL whole blood) was drawn from the forearm by venipuncture after an oral dose of labeled vitamin A. The serum samples were transferred to no-additive Vacutainers (Becton Dickinson, Franklin Lakes, NJ) covered with aluminum foil to prevent light damage and set at room temperature (25°C) for 30 min. The samples were centrifuged at 800 x g at room temperature for 10 min. Serum was separated, transferred to Cryo Tubes (Nunc Inc, Rochester, NY), and kept at -20°C until it was shipped to Beijing (within 1 wk). The samples were stored in Beijing at -70°C and then shipped to Boston on dry ice, where they were kept at -70°C until analyzed. All samples were analyzed in Boston by gas chromatography–mass spectrometry within 10 mo of being obtained.

Sample analysis
An HPLC apparatus equipped with a C₃₀ column and using methyl tertbutylether:methanol:water as the mobile phase was used to analyze concentrations of carotenoids and retinoids in serum (27), and a gas chromatography–electron capture negative chemical ionization mass spectrometry apparatus equipped with a 15-m DB-1 column and an on-column injector was used to determine the enrichment of labeled vitamin A in serum (28), with a CV <9%. The total carotenoid contents of the vegetables were determined by using paper chromatography (23), and individual carotenoids in food were determined by using extraction without saponification (29) and HPLC (27).

Statistics
Effects of the vegetable interventions were assessed by analysis of covariance (ANCOVA), with vegetable intervention, time of measurement, and their interaction as experimental factors and baseline values as the covariate. We checked for the presence of an interaction between vegetable intervention and baseline values but eliminated it from the final model, except where the interaction was statistically significant (P < 0.05). Baseline differences between the treatment groups were assessed by using Student's t test. ANCOVA was used to adjust the means after the intervention when there were differences between the groups at baseline. Student's t test for paired samples was used to look for differences before and after the intervention for each combination of diet intervention and time of measurement. An unpaired t test was used to test for significant differences between the 3-d and 21-d subgroups and for differences between the yellow-green- and light-colored-vegetable groups after the interventions. STATVIEW 5.0 (SAS Institute Inc, Cary, NC) was used for statistical calculations and a P value < 0.05 was considered significant unless otherwise specified.

	RESULTS

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Food consumption
Actual nutrient intakes from the meals provided at school during the interventions are shown in Table 2. Intakes of energy, fat, protein, preformed vitamin A, iron, and calcium were not significantly different between groups. Both groups consumed 30% of energy as fat, which is comparable with typical dietary intakes of children in the region. The nutrient intakes remained the same as in the diets that the subjects normally consumed, but the intakes of green-yellow vegetables were different. Each child in the green-yellow-vegetable group ate 238 g dark-green, leafy and yellow vegetables/d, such as spinach, Chinese chive, broccoli, carrots (fresh and dried), and red yam, and 34 g light-colored vegetables/d, such as cabbage, Chinese cabbage, potato, cucumber, and turnip. Each child in the light-colored-vegetable group consumed 56 g dark-green, leafy and yellow vegetables and 224 g light-colored vegetables/d (<10 µg total carotenoids). The total carotenoid content of the 238 g green-yellow vegetables consumed daily by the green-yellow-vegetable group was 8280 µg, as determined by paper chromatography (23). Of this total amount, 4670 µg was ß-carotene, 4200 µg was lutein, and 810 µg was other provitamin A carotenoids (700 µg -carotene, 60 µg cryptoxanthin, and 50 µg 13-cis-ß-carotene), as determined by HPLC (27). The total carotenoid content of the 56 g green-yellow vegetables consumed daily by the light-colored-vegetable group was 1340 µg, of which 700 µg was ß-carotene, 600 µg was lutein, and 40 µg was other carotenoids.

Serum carotenoid concentration
When the results for the 3-d and 21-d subgroups were combined, serum concentrations of all-trans-ß-carotene, 13-cis-ß-carotene, -carotene, cryptoxanthin, lutein, zeaxanthin, and lycopene were not significantly different between the 2 groups at baseline (Table 3). Because of the vegetable-intervention effect, final serum concentrations of all-trans-ß-carotene, 13-cis-ß-carotene, -carotene, lutein, and zeaxanthin were greater in the green-yellow-vegetable group than in the light-colored-vegetable group.

In the green-yellow-vegetable group (21-d subgroup), serum concentrations of 13-cis-ß-carotene, -carotene, cryptoxanthin, and zeaxanthin were still significantly higher than baseline values. In the light-colored-vegetable group, 23 d postintervention, serum concentrations of all-trans-ß-carotene, 13-cis-ß-carotene, -carotene, lutein, and zeaxanthin were not significantly different from baseline; in contrast, serum concentrations of cryptoxanthin were significantly higher than baseline values.

The changes in serum concentrations of cryptoxanthin were greater in the green-yellow-vegetable group than in the light-colored-vegetable group (P = 0.03, ANCOVA). The increase in cryptoxanthin in the green-yellow-vegetable group was significantly correlated (r = 0.3, P = 0.01) with the initial serum cryptoxanthin concentration. However, the increase in cryptoxanthin in the light-colored-vegetable group was not significantly correlated with the initial serum concentration of cryptoxanthin. The decreases in serum lycopene concentrations in both groups after the intervention were not due to the intervention because there were no significant differences between the green-yellow-vegetable and light-colored-vegetable groups.

Serum retinol concentration
At the beginning of the study, the mean serum concentration of retinol in the green-yellow-vegetable group was significantly lower than that in the light-colored-vegetable group (Table 4). Thirteen of 22 children in the green-yellow-vegetable group had a serum retinol concentration <1.05 µmol/L, whereas 3 of 19 children in the light-colored-vegetable group had serum retinol concentrations <1.05 µmol/L. After the intervention, the change in serum concentrations of retinol in the light-colored-vegetable group was significantly greater than that in the green-yellow-vegetable group. There was an interaction between treatment and the initial retinol concentration: those with higher baseline retinol concentrations showed greater treatment effects. After the intervention, 8 of 22 children in the green-yellow-vegetable group had serum retinol concentrations <1.05 µmol/L, whereas 14 of 19 children in the light-colored-vegetable group had serum retinol concentrations <1.05 µmol/L (22). Serum concentrations of retinol collected 3 or 21 d after the labeled vitamin A doses were administered were not significantly different within a treatment group.

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

The analysis of serum samples drawn before the intervention showed that the initial concentrations of all the carotenoids were similar in both groups. After the intervention, the serum concentration of most carotenoids increased significantly in the green-yellow-vegetable group, and these higher concentrations of carotenoids were sustained for as long as 23 d after the intervention period ended. This finding supports the previous finding of long carotenoid half-lives in humans (30). In both groups at the end of the study, there was a significant decrease in serum lycopene concentrations from baseline because of a seasonal drop in the consumption of tomato products. Conversely, there were significant increases in serum cryptoxanthin concentrations in both treatment groups because of a seasonal increase in the consumption of citrus fruit. The striking increases in serum cryptoxanthin concentrations in both groups at relatively low daily dietary intakes (100 µg in the green-yellow-vegetable group and 30 µg in the light-colored-vegetable group) indicate that serum responses to different dietary carotenoids are different, as was observed in other human investigations (31, 32).

We observed a trend toward an increase in mean serum vitamin A concentrations in children in the green-yellow-vegetable group because of their increased consumption of green-yellow vegetables during the intervention period. However, during this period, serum vitamin A concentrations decreased significantly in the light-colored-vegetable group. Our ANCOVA, which controlled for initial retinol concentrations, indicated that the decrease in serum retinol concentrations in the light-colored-vegetable group was not due to a regression to the mean. Furthermore, our isotope-dilution data also showed a significant vegetable-intervention effect on changes in the percentage enrichment of retinol in the light-colored-vegetable group. A similar response was reported for blood retinol in an intervention study of preschool children fed 50 g cooked ivy gourd containing 1200 µg ß-carotene (31). There was no significant change in serum retinol in the group that consumed cooked ivy gourd for 2 wk, whereas there was a significant decrease in serum retinol in a second group that did not receive the intervention.

A modified version of the equation of Bausch and Rietz (16, 17), which was used to calculate total-body vitamin A stores in humans, was verified by using surgical liver biopsies (19, 20). We believe that the use of physiologic doses of labeled vitamin A in the isotope-dilution tests would improve the correlation because the empirical parameters in the original equation were derived from studies that used physiologic doses of radioisotopic materials (16, 17). We used doses of D₈ or D₄ retinyl acetate of 0.45 µmol/kg body wt because our gas chromatography–mass spectrometry method accurately evaluates low enrichment (28).

In the green-yellow-vegetable group, there was no significant difference in mean serum isotopic enrichments measured on days 3 or 21 before or after the intervention, reflecting no significant change in total-body vitamin A stores in response to the dietary intervention. In the light-colored-vegetable group, mean serum isotopic enrichments measured on day 3 showed a trend of increasing percentage enrichment after the intervention compared with that before the intervention, indicating that vitamin A stores were lower. This was confirmed by mean serum isotopic enrichments measured on day 21 in the light-colored-vegetable group, the percentage enrichment of which had increased significantly. This finding indicated a significant vegetable-intervention effect. Thus, total-body vitamin A stores calculated by using the modified Bausch and Rietz equation showed a decreasing trend in total-body vitamin A stores (P < 0.06) in the children fed light-colored vegetables. Decreased total-body retinol stores averaged 27 ± 12 µmol (7700 ± 3400 µg)/child, or 5.3 ± 2.3 µg/kg body wt. Our results showed that the additional 186590 µg all-trans-ß-carotene and 38540 µg -carotene, cryptoxanthin, and 13-cis-ß-carotene eaten by the green-yellow-vegetable group prevented a loss of 27 ± 12 µmol (7700 ± 3400 µg) retinol from each child's liver; therefore, under the particular conditions of our study, provitamin A carotenoids (mainly ß-carotene) of vegetable origin provided an estimated vitamin A equivalence of 27 to 1 (ie, 27 µg ß-carotene from vegetable was nutritionally equivalent to 1 µg retinol) with a range of 19 to 1 to 48 to 1 by weight or a molar ratio of 14 to 1 with a range of 10 to 1 to 26 to 1 (assuming that -carotene, cryptoxanthin, and 13-cis-ß-carotene have half the vitamin A activity of all-trans-ß-carotene). This is lower than the conversion factors of 6 µg ß-carotene or 12 µg other provitamin A carotenoid to 1 µg retinol, but is close to that in a recent report from Indonesia of a calculated ß-carotene retinol equivalence of 26 to 1 by weight in leafy vegetables and carrots (32).

Previous investigations showed that vitamin A status as well as vitamin A intake influence the disposition of vitamin A (33, 34). That is, the disposal rate of vitamin A varies with vitamin A status and vitamin A intake: the disposal rate is greater when vitamin A status, intake, or both are higher. A higher disposal rate of vitamin A could explain our observation that the group fed the green-yellow vegetables with a high provitamin A content for 10 wk did not increase their total body stores significantly. On the other hand, the initial high vitamin A status of the group fed the light-colored vegetables showed a greater treatment effect and had a disposal rate of vitamin A that was high enough to deplete total body stores significantly over a 10-wk period, whereas the provitamin A in the light-colored vegetables was not high enough to cover the loss.

Our study showed that vitamin A nutrition in Chinese kindergarten children was sustained by supplying green-yellow vegetables with meals served at school. In the group not eating sufficient plant carotenoids, the concentration of vitamin A in liver as well as in serum decreased. Thus, this study showed the effectiveness of carotenoid-rich vegetables for providing adequate vitamin A nutrition to children of this age. It remains to be tested whether the feeding of green-yellow vegetables would be able to raise or maintain vitamin A stores in children whose gastrointestinal tracts have not been cleared of intestinal parasites. In many regions of the world, green-yellow vegetables are only available in certain seasons. Therefore, our studies suggest that in areas where the availability of green-yellow vegetables is seasonal, educational programs should be instituted to encourage a high consumption of carotenoid-containing plants during the season of plentiful supply.

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