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© 2002 The American Society for Nutritional Sciences J. Nutr. 132:3161-3167, October 2002


Nutritional Epidemiology

Frequent Intake of Tropical Fruits That Are Rich in ß-Cryptoxanthin Is Associated with Higher Plasma ß-Cryptoxanthin Concentrations in Costa Rican Adolescents1

Michael S. Irwig, Ahmed El-Sohemy*, Ana Baylin, Nader Rifai{dagger} and Hannia Campos2

Department of Nutrition, Harvard School of Public Health, Boston, MA 02115; * Department of Nutritional Sciences, University of Toronto, Toronto, Canada; and {dagger} Children’s Hospital of Boston, Department of Laboratory Medicine, Boston, MA 02115

2To whom correspondence should be addressed. E-mail: hcampos{at}hsph.harvard.edu.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Dietary tocopherols and carotenoids may play a role in preventing cancer and cardiovascular diseases. Because these may begin to develop during adolescence, dietary patterns during this period could influence long-term risk. The objective of this study was to examine the intake and plasma concentrations of the major carotenoids and tocopherols in 159 adolescents (mean ± SD, 15.5 ± 2.5 y old) living in Costa Rica. All participants completed a 135-item food-frequency questionnaire and provided a fasting blood sample. Carotenoid and tocopherol intakes were adjusted for total energy and plasma concentrations for total cholesterol. The relative abundance of carotenoids in the diet was similar to their distribution in plasma; lycopene was the most abundant, followed by ß-carotene and lutein + zeaxanthin. {gamma}-Tocopherol was more abundant than {alpha}-tocopherol in the diet, but {alpha}-tocopherol was approximately sevenfold higher in plasma. The highest diet-plasma correlations (adjusted for age, sex and body mass index) were 0.38 for ß-cryptoxanthin, 0.33 for {gamma}-tocopherol and 0.17 for lutein + zeaxanthin (all P < 0.05). All other correlations were r < 0.15. Papaya intake was the best food predictor of plasma ß-cryptoxanthin concentrations (r = 0.41). Subjects that frequently (>=3/d) consumed tropical fruits with at least 50 µg/100 g ß-cryptoxanthin (papaya, tangerine, orange and watermelon) had twofold the plasma ß-cryptoxanthin concentrations of those with intakes of <4/wk (P for trend = 0.0009). In sum, the diet-plasma carotenoid and tocopherol correlations were generally low in Costa Rican adolescents. Intakes of ß-cryptoxanthin and papaya, a tropical fruit frequently consumed in Latin America, were the best predictors of ß-cryptoxanthin concentrations in plasma.


KEY WORDS: • adolescents • biomarker • Hispanic • dietary assessment • carotenoid • tocopherol


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Cancer and cardiovascular diseases are the leading causes of death in Latin American countries such as Costa Rica, and among Hispanics living in the United States (1Citation ). Guidelines aimed at reducing the risk of these chronic diseases have stressed the importance of initiating intervention during childhood and adolescence because this is a critical period when the onset of disease may occur and lifetime habits are established (2Citation –5Citation ). Because of the important role of nutrition in both cancer and cardiovascular disease (6Citation ), more information on dietary patterns during early life is essential for designing effective preventive strategies.

Intake of fruits and vegetables has been associated with a reduced risk of cardiovascular disease and cancer at several sites (7Citation –12Citation ). Because the major carotenoids found in the diet and human plasma, {alpha}-carotene, ß-carotene, lycopene, ß-cryptoxanthin, lutein and zeaxanthin, are found mainly in fruits and vegetables, it is possible that they contribute to the protection of these plant products against chronic diseases (13Citation –15Citation ). Carotenoids can reduce adhesion molecules on the surface of endothelial cells, a potential protective function against atherosclerosis (16Citation ). As precursors of retinoids, they may play a role in tumor suppression (17Citation ). Interestingly, some carotenoid products with chemical structures that resemble that of retinoids may regulate tumor cell growth independently of their conversion to retinoic acid (18Citation ). Furthermore, carotenoids have the ability to reduce lipid peroxidation and scavenge free radicals, properties that may protect tissues and DNA from oxidative damage (19Citation –23Citation ).

Plant oils are rich sources of vitamin E (24Citation ). {alpha}-Tocopherol is the most biologically active form of vitamin E and is the most abundant in plasma and tissues (25Citation ). Although {gamma}-tocopherol is estimated to have one half the antioxidant activity of {alpha}-tocopherol (26Citation ), {gamma}-tocopherol is more abundant in the U.S. and Costa Rican diets (27Citation ,28Citation ). Furthermore, plasma concentrations of {gamma}-tocopherol are more responsive to intake than {alpha}-tocopherol (28Citation ,29Citation ). There is growing evidence that {gamma}-tocopherol may have beneficial effects independent of its antioxidant properties (30Citation ), although {gamma}-tocopherol was not associated with protection against myocardial infarction in Costa Rica (31Citation ). The {gamma}-tocopherol status of adolescents has not been reported previously.

A number of studies have compared dietary intake of the major carotenoids and tocopherols with their plasma concentrations in diverse adult populations (32Citation –37Citation ). However, few studies have investigated the relationship between intake and plasma concentrations of the major carotenoids in healthy adolescents (38Citation ), and data on micronutrient intake in this age group are scarce. The purpose of this study is to determine the intake and plasma concentrations of carotenoids and tocopherols in healthy adolescents from Costa Rica, examine the correlations between diet and plasma, and identify the best food predictors of plasma concentrations.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study design and subjects.

We studied randomly selected adolescents (n = 161) whose parents or grandparents were participants of a population-based case-control study of myocardial infarction (39Citation ). This group was selected to achieve a high participation rate because the research team had established previous contact with eligible adults. Stratified random sampling was used to obtain equal numbers of males and females between 12 and 20 y old. To make valid comparisons between groups in relation to anthropometric measurements and plasma concentrations, pregnant females were ineligible for the study. Only one descendant per adult was eligible to participate in this study. In the case of multiple eligible children and/or grandchildren, one subject was chosen at random. The former adult participants were contacted by telephone to inquire whether they had any eligible biological descendants living in the metropolitan area of San José, Costa Rica. Of the 1062 participants from the adult study, 83% (n = 881) had a telephone and lived in the metropolitan San José area. In total, 388 phone calls were placed to achieve a sample size of 161 adolescents. Of the 388 calls, 84% (n = 325) resulted in successful contact of the former adult participant and 16% (n = 63) had an incorrect/changed telephone number. Of those successfully contacted, 53% (n = 173) had an eligible subject, i.e., a child or grandchild between 12 and 20 y old who had a telephone and lived in the metropolitan San José area. Participation was 93%. A medical student spoke to each subject and their parent(s) to explain what the study entailed, namely, an interview, various anthropometric measurements, a test of physical fitness and a fasting blood sample. As a benefit to the subjects, it was explained that they would receive free blood tests for total cholesterol and glucose by portable monitors, copies of a guide to good nutrition in Spanish, and personalized certificates of appreciation that included the results for the blood tests, height, weight, blood pressure and fitness score. Subjects approved participation in the study by signing a consent form. For those adolescents <18 y old, an adult approved participation by signing the consent form as well. The protocol for the study was approved by the Human Subjects Committee of the Harvard School of Public Health and the University of Costa Rica. Data were collected in San José, Costa Rica, from September 1998 through April 1999. The interviews were conducted in the subjects’ homes for 98% (n = 157) of the subjects. The remaining 2% (n = 4) were conducted at the project’s downtown fieldwork station. The mean interview length was 35 min.

Dietary assessment.

Dietary information was obtained using a 135-item semiquantitative food-frequency questionnaire (FFQ)3 specifically designed for the Costa Rican population by including all the fruits, vegetables and other foods that are commonly consumed in Costa Rica. This questionnaire was validated previously for carotenoid and tocopherol consumption among adult Costa Ricans (28Citation ,32Citation ,40Citation ). Because this FFQ has not been formally validated in adolescents, we compared the results of this study to those reported by Monge-Rojas (41Citation ) who used 3-d food records among adolescents from Costa Rica living in the urban area. In general, intakes from these two studies using two different dietary assessment methods were remarkably similar. For example, intakes of total fat, saturated, monounsaturated and polyunsaturated fatty acids (% energy) were 32, 12, 12 and 5.6 in this study and 32, 12, 9 and 6 in the study by Monge-Rojas (41Citation ). Intakes of cholesterol (mg), fiber (g) and folate (µg) (per 4.18 MJ) were 110, 7.3 and 119, and 109, 8 and 119, respectively. As in the validation study among Costa Rican adults (40Citation ), the estimated total energy intake by FFQ among adolescents was higher than the average of dietary recalls (41Citation ).

The FFQ contained 15 questions on fruit and fruit juice intake, and 28 questions on vegetable intake. Each item had a specified portion size and nine possible coding responses, which ranged from never or <1/mo to >=6/d. Portion sizes for the food items in the FFQ were calculated on the bases of standardized serving sizes as specified by the School of Nutrition at the University of Costa Rica (42Citation ). Nutrient intake calculations for each subject were computed by multiplying the frequency of each food by the nutrient content of the specified portion, using composition values from the USDA (43Citation ). The carotenoid database used in this analysis was derived from the Nutrition Coordinating Center (NCC) at the University of Minnesota and included the updated USDA-NCC Carotenoid Database for U.S. foods (44Citation ). Subjects selected only one type of fat or oil that was used most frequently for cooking and frying at home. During the FFQ interview, the interviewer rated the credibility of the adolescent subjects as good (n = 116), regular (n = 42) or poor (n = 3). This subjective rating was based on consistency in answers to certain items and the ability to estimate averages in food consumption. Because no differences in reported carotenoid and tocopherol intakes were found between credibility ratings, all subjects were included in the analysis.

Plasma collection and laboratory analysis.

Blood was collected in the morning at each subject’s home after he or she had fasted overnight. Blood samples were collected in tubes containing 0.1% EDTA and stored in a cooler with ice packs at 4°C. Within 4 h, the specimens were centrifuged for 20 min at 4°C and 1430 x g to separate the plasma, buffy coat and red cells. Plasma samples were then stored in a freezer at -80°C for 1–7 mo until they were transported over dry ice to the Harvard School of Public Health for analysis.

Concentrations of {alpha}-tocopherol, {gamma}-tocopherol, {alpha}-carotene, ß-carotene, lycopene, ß-cryptoxanthin, lutein and zeaxanthin in plasma samples were measured as previously described (28Citation ,32Citation ). Briefly, plasma samples (250 µL) were mixed with 250 µL ethanol containing 10 mg all-rac-tocopherol/L (Tocol; Matreya, Pleasant Gap, PA) as an internal standard, extracted with 4 mL of hexane, evaporated to dryness under nitrogen and reconstituted in 100 µL ethanol-dioxane (1:1, v/v) and 150 µL acetonitrile. Samples were quantitated by HPLC on a Restek Ultra C18 150 mm x 4.6 mm column with a 3-µm particle size (Restek, Bellefonte, PA). The column was encased in a water bath to prevent temperature fluctuations and equipped with a trident guard cartridge system. A mixture of acetonitrile/tetrahydrofuran/methanol/1% ammonium acetate solution (68:22:7:3) was used as the mobile phase with a flow rate of 1.1 mL/min. A Hitachi L-7100 pump in isocratic mode, an L-4250 UV-visible light detector set at a wavelength of 445 nm for carotenoids and 300 nm for tocopherols, and a programmable AS-4000 autosampler with water-chilled tray interfaced with a D-6000 interface module were used for analysis (Hitachi, San Jose, CA). The system manager software (D-7000, version 3.0; Hitachi) was used for peak integration and data acquisition. Because lutein and zeaxanthin coelute on the chromatogram, the two were grouped and presented as lutein + zeaxanthin. The minimum detection limits for each carotenoid in plasma was ~0.01 µmol/L. The CV were 5.2% for {alpha}-carotene, 5.6% for ß-carotene, 2.5% for ß-cryptoxanthin, 6.4% for lycopene, 3.6% for lutein + zeaxanthin, 2.3% for {alpha}-tocopherol and 4.6% for {gamma}-tocopherol. The accuracy and precision of the analytical methods used were monitored through the laboratory participation in the Quality Assurance Program of the National Institute of Standards and Technology (Gaithersburg, MD).

Plasma cholesterol and triglyceride concentrations were determined enzymatically on the Hitachi 911 analyzer (Roche Diagnostic Systems, Somerville, NJ) at the Department of Laboratory Medicine at the Children’s Hospital of Boston. The measurement of triglycerides was corrected for the presence of endogenous glycerol. The HDL cholesterol was determined by a homogeneous assay (HDL Plus, Roche Diagnostics) on the Hitachi 911 analyzer. Total cholesterol was determined with run-to-run CV of 1.8 and 1.5% at 3.32 and 6.92 mmol/L, respectively; HDL-cholesterol CV of 2.8 and 2.0% at concentrations of 0.91 and 1.71 mmol/L, respectively; and triglyceride CV of 1.8 and 1.7% at 0.90 and 1.88 mmol/L, respectively. LDL cholesterol concentrations were estimated for all subjects with triglyceride concentrations <4.52 mmol/L using the Friedewald equation (45Citation ). The laboratory is certified by the National Heart, Lung, and Blood Institute and the Centers for Disease Control Lipid Standardization Program.

Statistical analyses.

SAS software (SAS Institute, Cary, NC, version 8) was used for all statistical analysis. Of the 161 participants, those with missing data were excluded (n = 2). The final sample of 159 subjects consisted of 81 males and 78 females. As needed, carotenoids and tocopherols were loge or square-root transformed to improve normality. Transformed nutrients were regressed on total energy intake to obtain energy-adjusted nutrient intake for each individual (46Citation ). The same method was used to adjust plasma carotenoids and tocopherols for total plasma cholesterol concentrations because they are transported mainly in plasma lipoproteins, and this contributes to extraneous variation. Partial Spearman correlation coefficients adjusted for age, sex and body mass index (BMI) were calculated to determine associations between carotenoid and tocopherol intake and their concentrations in plasma. The same approach was used to determine the association between plasma carotenoids and the number of servings of individual fruits and vegetables. The general linear model with Bonferroni multiple comparisons was used to compare the plasma {gamma}-tocopherol concentrations by type of oil used for cooking. There were only four subjects who reported use of vitamin supplements. Data on tocopherol intake are presented with and without these subjects. Plasma concentrations and diet-plasma correlation coefficients were not modified when these supplement users were excluded; thus, they were included in the analyses. Because adjusting for smoking did not modify the results, it was not included as a covariate.

For ß-cryptoxanthin, the nutrient with the strongest diet-plasma correlation, we created a variable that consisted of the sum of servings per day of fruits that were consumed by this population, and that contained at least 50 µg of ß-cryptoxanthin/100 g of food (44Citation ). Four tropical fruits met these criteria; the highest was papaya with 761 µg/100 g, followed by tangerine (485), orange (122) and watermelon (103). These results were consistent with the European Carotenoid Database (47) (except for papaya for which no data were provided), albeit the estimates differed (1309 for tangerine, 266 for orange and 62 µg/100 g for watermelon). Except for watermelon in which no ß-cryptoxanthin was detected, these fruits also had the highest ß-cryptoxanthin concentrations in fruit samples from Costa Rica (unpublished data from our laboratory), 404 for papaya, 428 for tangerine and 48 µg/100 g for orange. We created quintiles of fruit intake and used multiple linear regression models to accomplish the following: 1) test for trends across the median plasma ß-cryptoxanthin concentrations at each quintile of intake; 2) compare the average values of plasma concentrations at each quintile; and 3) adjust for age, sex and BMI. Robust estimators of the variance were used in the regression models, thus eliminating the need to normalize the dependent variable (48Citation ,49Citation ). This multiple linear regression model allowed us to describe the relationship between dietary and plasma ß-cryptoxanthin without being restricted by linearity assumptions. A plot from this analysis was created to provide a visual description of this relationship.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The general characteristics of the studied population are shown in Table 1Citation . Height, weight and total energy intake were greater in males than females. Males were more likely to smoke (15%) and be overweight (19%) compared with females (1 and 14%, respectively). Total cholesterol was significantly higher in females but this was due mainly to 18% higher HDL cholesterol. Table 2Citation shows dietary intake and plasma concentrations of the major carotenoids and tocopherols. Lycopene and ß-carotene were the most abundant carotenoids in both the diet and plasma, whereas {alpha}-carotene and ß-cryptoxanthin were the least abundant. Despite similar intakes, females had higher plasma concentrations of ß-cryptoxanthin and ß-carotene than males (P < 0.05). In both males and females, dietary intake of {gamma}-tocopherol was higher than {alpha}-tocopherol, yet plasma concentrations of {alpha}-tocopherol were approximately sevenfold higher. Consumption of fruit at least once per day was reported by 84% of adolescents. The most widely consumed fruits that accounted for ~97% of total fruit intake were papaya, banana, pineapple, mango, orange, watermelon, cantaloupe and tangerine. Only 34% of adolescents reported that they consumed green vegetables such as lettuce, spinach, mustard greens, cabbage and broccoli at least once per day.


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TABLE 1 General characteristics, plasma lipids and macronutrient intake of Costa Rican male and female adolescents aged 12–20 y1

 

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TABLE 2 Dietary intake and plasma concentrations of carotenoids and tocopherols in Costa Rican male and female adolescents aged 12–20 y12

 
Spearman correlations between intake and plasma concentrations for each of the major carotenoids and tocopherols are shown in Table 3Citation . The strongest correlations observed were for ß-cryptoxanthin (r = 0.38), {gamma}-tocopherol (r = 0.33) and lutein + zeaxanthin (r = 0.17) (all P < 0.05). The weakest correlation was seen with {alpha}-tocopherol (r = 0.05).


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TABLE 3 Spearman partial correlation coefficients between carotenoid and tocopherol intake and carotenoid and tocopherol plasma concentrations in Costa Rican male and female adolescents aged 12–20 y1

 
We next examined which of the fruits and/or vegetables correlated best with individual plasma carotenoids. Papaya intake was correlated with all carotenoids except lycopene; the highest correlation was with ß-cryptoxanthin (r = 0.41) (Table 4Citation ). Other fruits and vegetables that were correlated with plasma concentrations of ß-cryptoxanthin such as pineapple, banana, cucumber, tomato and lettuce do not contain ß-cryptoxanthin. Intake of these fruits was associated with intake of papaya, a food with a high content of ß-cryptoxanthin. Papaya is generally consumed in a fruit salad that also contains pineapple and banana. High correlations between ß-cryptoxanthin and this fruit salad were also observed. When all fruits and vegetables were entered together in a regression model, only papaya remained a significant correlate of plasma ß-cryptoxanthin (data not shown). Bananas and plantains were correlated with {alpha}-carotene, whereas significant correlations with ß-carotene were observed for pineapple, cucumber, tomato and broccoli. It should be noted that a significant negative correlation was observed between plasma {alpha}-carotene concentrations and cantaloupe, a food with relatively low content of {alpha}-carotene. Other nonsignificant negative correlations were observed.


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TABLE 4 Spearman partial correlation coefficients between plasma carotenoid concentrations and fruit and vegetable intake in Costa Rican male and female adolescents aged 12–20 y1

 
Because ß-cryptoxanthin in the plasma correlated best with dietary ß-cryptoxanthin, we investigated the association between intake of fruits that contain at least 50 µg/100 g ß-cryptoxanthin (papaya, tangerine, orange and watermelon) (44Citation ) and plasma concentrations of ß-cryptoxanthin (Fig. 1Citation ). Plasma concentrations of ß-cryptoxanthin increased significantly with increasing number of servings of fruits per day. This trend was due mainly to the consumption of papaya, which is consumed regularly, has a relatively high content of ß-cryptoxanthin and correlated best with plasma ß-cryptoxanthin (Table 4)Citation .



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FIGURE 1 Relation between servings per day of fruits rich in ß-cryptoxanthin and plasma concentrations of ß-cryptoxanthin in randomly selected healthy Costa Rican male and female adolescents between 12 and 20 y old. The following fruits containing at least 50 µg ß-cryptoxanthin/100 g were included: papaya, tangerine, orange and watermelon (44Citation ). Portion sizes were calculated on the bases of standardized serving sizes as specified by the School of Nutrition at the University of Costa Rica (42Citation ). One serving of fruit is defined as one medium piece of fruit or one slice (~112 g). Data points represent the mean ± SEM of the ß-cryptoxanthin plasma concentration in each quintile of fruit intake.

 
Plasma {gamma}-tocopherol concentrations were associated with two major dietary sources, mayonnaise and soybean oil. Subjects who consumed >5 servings of mayonnaise/wk had higher plasma concentrations of {gamma}-tocopherol than those who consumed <1 serving/wk (mean ± SD = 2.9 ± 1.5 vs. 2.2 ± 0.9 µmol/L, P = 0.02). Plasma concentrations of {gamma}-tocopherol were higher in subjects who reported using soybean oil for cooking and frying compared with those who used palm oil shortening (mean ± SD = 2.5 ± 0.9 vs. 1.6 ± 0.2 µmol/L, P < 0.0001). A small proportion of subjects (<10%) who reported using any other type of oil (corn, sunflower, canola or olive) also had higher plasma concentrations of {gamma}-tocopherol than palm oil users (mean ± SD = 2.2 ± 0.8 µmol/L, P = 0.01), but these concentrations did not differ significantly from those using soybean oil. No association was observed between mayonnaise or type of cooking oil and plasma {alpha}-tocopherol.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The present study provides a comprehensive analysis of {alpha}-carotene, ß-carotene, lycopene, ß-cryptoxanthin, lutein + zeaxanthin, {alpha}-tocopherol and {gamma}-tocopherol in the diet and plasma of adolescents living in Costa Rica. The results from our dietary assessment are comparable with a previous study that measured intake of ß-carotene and {alpha}-tocopherol from 263 boys and 246 girls between 10 and 15 y old living in France (50Citation ). In that study, there were no differences in {alpha}-tocopherol intake between males and females, but ß-carotene intakes were lower in the females. We found no differences in either {alpha}-tocopherol or ß-carotene between males and females. Intake of ß-carotene was higher among the females living in Costa Rica compared with those living in France. Carotenoid intakes among Costa Rican adolescents do not differ substantially from those previously reported for Costa Rican adults, except for lycopene (32Citation ), which is considerably higher among Costa Rican adolescents than adults. This difference is most likely due to a greater use of ketchup among adolescents compared with adults (2.3 vs. 1.1 servings/wk, respectively) and not fresh tomatoes or homemade tomato sauce, which were similar (5.8 vs. 6.1 servings/wk, respectively) (data not shown). These dietary data are consistent with higher plasma lycopene concentrations among adolescents in this study compared with Costa Rican adults (32Citation ).

The intake of fruits and vegetables in the present study is higher than those previously reported for Costa Rican adolescents (51Citation ). Although studies in the United States suggest that the reliability of FFQ to assess dietary intake among adolescents is comparable with that found among adults (52Citation –54Citation ), it is possible that these differences are due to the methods used for dietary assessment. In the study by Monge-Rojas (51Citation ), fruit and vegetable intake was assessed using 3-d food records that could underestimate intake (46Citation ). However, it is also possible that the FFQ overestimated fruit and vegetable intake in our study because of the use of long lists, which could lead to overreporting (55Citation ).

Plasma concentrations of the major carotenoids were reported previously for healthy adolescents living in the United States and Japan (38Citation ,56Citation ). Consistent with the results of the present study, lycopene and ß-carotene were the most abundant carotenoids in plasma among adolescents living in the United States (38Citation ). In contrast, ß-cryptoxanthin and lutein + zeaxanthin were the most abundant among those living in Japan (56Citation ). Plasma concentrations of {alpha}-carotene and ß-carotene were similar between Costa Rican and Japanese adolescents, and these concentrations were ~130% higher than those of U.S. adolescents. Plasma lycopene concentrations did not differ substantially among adolescents living in the United States, Japan or Costa Rica. Some of the differences seen among adolescents living in different countries may reflect differences in the major food sources of carotenoids or other differences in dietary patterns that affect carotenoid absorption and bioavailability. It is also possible that genetic differences associated with carotenoid metabolism could affect the relative abundance of each carotenoid in plasma.

Daily intake of {alpha}-tocopherol in the present study was similar to that reported for French (50Citation ) and Costa Rican adolescents (57Citation ), but somewhat higher than that reported for adolescents living in the United States (58Citation ). Intakes of {alpha}- and {gamma}-tocopherol were also similar to those reported for Costa Rican adults but plasma {alpha}-tocopherol was considerably lower among the adolescents (28Citation ). This finding is consistent with previous results from the United States and Japan showing lower plasma {alpha}-tocopherol in adolescents (38Citation ,56Citation ). As we previously observed in adults (28Citation ), plasma {gamma}-tocopherol concentrations were considerably lower than {alpha}-tocopherol despite similar or even higher intakes of {gamma}-tocopherol. This difference in bioavailability between {alpha}- and {gamma}-tocopherol is likely due to the preferential incorporation of {alpha}-tocopherol into nascent VLDL by the hepatic {alpha}-tocopherol-transfer protein (59Citation ).

Overall, the correlations we observed between intake and plasma concentrations of the major carotenoids and tocopherols are consistent with those reported for adolescents living in the United States (38Citation ). The highest correlations in both studies were found for ß-cryptoxanthin (r = 0.38 for both), and both studies showed lower correlations (r <= 0.25) for ß-carotene, lycopene, lutein + zeaxanthin and {alpha}-tocopherol. However, the diet-plasma correlations for {alpha}-carotene were much lower in Costa Rica (r = 0.13) compared with the United States (r = 0.31) (38Citation ). The correlation between dietary and plasma {gamma}-tocopherol (r = 0.33) was relatively high and similar to that observed in Costa Rican adults, but most diet-plasma correlations among adolescents in this study were lower than those previously reported for Costa Rican adults (28Citation ,32Citation ). Measurement error associated with the use of an FFQ to estimate intake could account for some of these low associations. A potential caveat of the Costa Rican FFQ for adolescents is that it assumed a single portion size and during adolescence, variation in energy requirements associated with growth can lead to large differences in absolute intake. However, the study by Neuhouser et al. (38Citation ) described above, did take into account portion size and, except for {alpha}-carotene, the results are comparable. Another explanation for these low correlations could be that the FFQ did not contain important sources of carotenoids. Still, a comprehensive list of 43 fruits and vegetables specifically consumed by this population was included and the subjects had the choice of adding any missing items that were consumed frequently and were not included in the questionnaire. Another potential source of error is that we collected only one blood sample, which may reflect recent intake rather than an integrated measurement over 1 y (60Citation ). In addition, the FFQ relies on the recall of foods consumed over the previous year and the reliability of the database containing the carotenoid content in foods, which can vary substantially depending on the geographic region, storage and processing, among others. We used the updated USDA-NCC Carotenoid Database (44Citation ), which compiles numerous reports on the carotenoid content of foods to provide an estimate for each carotenoid as described by Mangels et al. (61Citation ). However, this database contains numerous items with incomplete information and the accuracy and reliability of those with a reported estimate is generally low. Only a few values such as ß-carotene in raw broccoli, canned carrots, pink grapefruit, cantaloupe, peach, sweet potato and tomato, {alpha}- and ß-carotene in raw carrots and spinach, and lycopene in pink grapefruit, tomato and tomato-based products have been recommended to be used with considerable confidence (44Citation ).

Other factors that may account for the generally low correlations observed between plasma and dietary carotenoids include the large interindividual difference in absorption. For example, an equal dose of lycopene can result in plasma lycopene concentrations ranging between 80 and 350 nmol/L (62Citation ). Furthermore, supplementation of one carotenoid could lead to significant reductions of another through competition for similar metabolic mechanisms (63Citation ), and the bioavailability of specific carotenoids can be influenced by concurrent intake of other carotenoids and tocopherols (64Citation ). Taking all of these factors into consideration, the finding of small significant correlations between dietary and plasma carotenoids suggests that these factors are strongly correlated.

It is estimated that in Western countries >70% of ß-cryptoxanthin comes from oranges, orange juice and tangerines, and these are the best food predictors of plasma ß-cryptoxanthin concentrations (34Citation ,47Citation ). In our population, plasma ß-cryptoxanthin was not correlated with citrus products; instead, high correlations were found with papaya, which has a high content of ß-cryptoxanthin (~700–900 µg/100 g) (44Citation ,65Citation ,66Citation ) and is commonly consumed in Costa Rica. Similarly, {alpha}-carotene was positively correlated with papaya, banana and plantain but not with carrots, by far the largest contributor to {alpha}-carotene in Western societies (47Citation ). It is possible that these correlates of {alpha}-carotene in Costa Rica simply represent an indicator of consumption of other foods with higher content of {alpha}-carotene, given that the reported concentrations of {alpha}-carotene in these products is low (44Citation ,47Citation ). Nevertheless, the consumption of these products is high in Costa Rica and a better estimate of their {alpha}-carotene content must be determined because the current information is unreliable (44Citation ). The correlations of plasma ß-cryptoxanthin concentrations with pineapple and banana in our study are most likely due to the consumption of these foods together with papaya as a fruit salad, given that ß-cryptoxanthin has not been detected at all in these products (44Citation ,47Citation ). More studies on the carotenoid content of foods including those that are highly consumed worldwide are warranted.

In sum, the relative abundance of carotenoids in the diet of Costa Rican adolescents is similar to their distribution in plasma, with lycopene as the most abundant, followed by ß-carotene and lutein + zeaxanthin. Lower intake and plasma concentrations were found for {alpha}-carotene and ß-cryptoxanthin. Plasma {gamma}-tocopherol concentrations in adolescents were considerably lower than {alpha}-tocopherol despite similar or even higher intakes of {gamma}-tocopherol.

The diet-plasma correlations were generally low but differed substantially between individual carotenoids and tocopherols, from 0.05 for {alpha}-tocopherol to 0.38 for ß-cryptoxanthin. Papaya, a frequently consumed fruit in Latin America, was the best food predictor of plasma concentrations of ß-cryptoxanthin and other carotenoids, suggesting an alternative source of carotenoids in the diet, particularly in countries in which this fruit is inexpensive and readily available.


    FOOTNOTES
 
1 Supported by an American Heart Association Medical Research Fellowship provided through Cornell University Medical College to M.S.I., and research grant HL 49086 from the National Institutes of Health. Back

3 Abbreviations used: BMI, body mass index; FFQ, food-frequency questionnaire; NCC, Nutrition Coordinating Center. Back

Manuscript received 14 May 2002. Initial review completed 30 May 2002. Revision accepted 23 July 2002.


    LITERATURE CITED
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
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E. K. Kabagambe, A. Baylin, M. S. Irwig, J. Furtado, X. Siles, M. K. Kim, and H. Campos
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