Journal of the American College of Nutrition, Vol. 24, No. 2, 122-128 (2005)
Published by the American College of Nutrition
Costa Rican Adolescents have a Deleterious Nutritional Profile as Compared to Adults in Terms of Lower Dietary and Plasma Concentrations of Antioxidant Micronutrients
Edmond K. Kabagambe, BVM, PhD,
Ana Baylin, MD, PhD,
Michael S. Irwig, MD,
Jeremy Furtado, BS,
Xinia Siles, RN,
Mi Kyung Kim, PhD and
Hannia Campos, PhD
Department of Nutrition, Harvard School of Public Health, Boston, MA 02115 (E.K.K., A.B., J.F., H.C.)
Division of Metabolism, Endocrinology and Nutrition, University of Washington, Seattle, WA 98195 (M.S.I.)
Centro Centroamericano de población, Universidad de Costa Rica, San Pedro de Montes de Oca, Costa Rica (X.S., H.C.)
Department of Preventive Medicine, Hanyang University College of Medicine, Seoul, South Korea (M.K.K.)
Address reprint requests to: Dr. Hannia Campos, Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave, Building 1, Boston, MA 02115. E-mail: hcampos{at}hsph.harvard.edu
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ABSTRACT
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Objective: Most prospective studies in adult populations show an inverse association between consumption of fruits and vegetables and the risk of cardiovascular disease and all-cause mortality. Fruits and vegetables are rich in antioxidants. The objective was to determine whether nutrient intakes and plasma concentrations of antioxidants of adolescents are similar to those of their parents or grandparents as a way of assessing whether dietary habits of parents are passed on to their adolescent children.
Methods Parents or grandparents (n = 159) aged 29–77 y were selected from the participants of the myocardial case-control study in Costa Rica. One adolescent child or grandchild (12–20 y) was identified for each parent or grandparent. Nutrient intakes and plasma antioxidant concentrations were assessed using a validated food-frequency questionnaire and by high performance liquid chromatography, respectively.
Results As compared to adults, adolescents consumed greater quantities of fruit, dairy products, red meat, carbonated drinks and polyunsaturated fat, but lower quantities of fiber and micronutrients (carotenoids, vitamins A and B6, folate, potassium, magnesium and zinc). Plasma concentrations of all carotenoids, except for lycopene, were lower in adolescents than in adults (p < 0.05). Intakes of lycopene (r = 0.16, p = 0.05), 
-tocopherol (r = 0.19, p = 0.03) and 
-tocopherol (r = 0.21, p = 0.01) in adolescents were correlated with those of adults. Plasma concentrations of lycopene (r = 0.20, p = 0.02), -tocopherol (r = 0.18, p = 0.03) and -tocopherol (r = 0.28, p = 0.001) in adolescents were also correlated with those of adults. These data may suggest that adolescents may acquire habitual consumption of foods rich in micronutrients from adults.
Conclusion: As a proportion of energy, diets of Costa Rican adolescents contain less micronutrients than those of their adult relatives. Parents should be aware of this trend and its association with poor health status.
Key words: antioxidants, carotenoids, tocopherols, biomarkers, diet, Costa Rica
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INTRODUCTION
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Most [1–5] but not all [6] prospective studies in adult populations show an inverse association between the consumption of fruits and vegetables and the risk of cardiovascular disease and all-cause mortality. This beneficial effect has also been shown for cancer in some prospective [7,8] and case-control studies [9–12]. The reduction in risk is thought to be due to antioxidants such as carotenoids, which are abundant in fruits and vegetables. Many [13–16] but not all [17–19] epidemiological studies in adults suggest that individual carotenoids in diet or plasma may protect against cancer and cardiovascular disease, and may decrease atherosclerotic progression [20,21]. Except for one recent study on leukemia [22] in which low antioxidant vitamin intakes in children and adolescents were associated with greater adverse effects of chemotherapy, comparable data in adolescents are lacking, partly because of the rarity of certain cancers and cardiovascular disease in the adolescent population. However, the onset of cardiovascular disease and the acquisition of dietary habits may be established during adolescence. For example, in the Nurses Health Study, women who consumed 2.5 servings/d of fruits and vegetables in adolescence had a 46% reduction in risk of ovarian cancer whereas no such effect was detected after adolescence [7]. Unfortunately, most adolescents (e.g., 75% in the US) do not eat the recommended 5 daily servings of fruits and vegetables [23] and may, in general, eat unhealthy diets. The dietary habits of children are influenced by previous eating behavior [24], parental attributes [25] such as dietary composition [26], family income and education [27,28]. As children progress through adolescence their dietary habits worsen and may persist into adulthood [29]. Data comparing the intakes of micronutrients, macronutrients, physical activity and food patterns of adolescents and adults in Costa Rica are lacking. Costa Rica is one of many countries with an increasing prevalence of type 2 diabetes [30] and mortality due to cardiovascular disease [31]. In order to identify areas for dietary intervention among adolescents, we compared the diets and plasma antioxidant concentrations of adolescents and adults in an attempt to determine whether dietary habits of adolescents correspond to those of their parents or grandparents.
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MATERIALS AND METHODS
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Study Design and Subjects
The design of this study has been previously described [32,33]. Briefly, we studied 161 randomly selected male and female adolescents (12 to 20 y old) whose parents or grandparents (subsequently referred to as adults) participated in a population-based case-control study of myocardial infarction (MI) in Costa Rica [32]. This population of adolescents was selected to achieve a high participation rate because the research team had already established contact with the adults. Out of the 1062 adult participants from the MI study, 83% (n = 881) had a telephone and lived in the metropolitan San José area. In total, 388 calls were placed and 84% (325/388) of them resulted in successful contact of the former adult participant. Fifty three percent (173/325) of them had an adolescent eligible for inclusion in this study (a child or grandchild between the ages of 12 and 20 who had a telephone and lived in the metropolitan area of San José). Pregnant females were ineligible to facilitate valid comparisons between groups in relation to anthropometric measurements and plasma carotenoid concentrations. Only one eligible adolescent per adult was randomly selected to participate in this study. Participation was 93% (161/173) for eligible adolescents. For each adolescent and adult, a medical student explained that the study involved an interview, 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, a fitness score, and measurements of height, weight and blood pressure. Subjects approved participation in the study by signing a consent form. For those adolescents under 18 y old, an adult approved participation by signing the consent form as well. The Human Subjects Committee of the Harvard School of Public Health and of the University of Costa Rica approved all of the study protocols. For adolescents, data were collected in San José, Costa Rica, from September 1998 through April 1999. Most of the interviews (98%, 157/161) were conducted at the subjects’ homes while the remaining (2%, 4/161) were conducted at the project’s downtown fieldwork station. The mean interview length was 35 minutes [33]. Corresponding anthropometric data, dietary intake, plasma concentration of carotenoids and other characteristics of the adults were obtained from the existing MI study database [32].
Dietary Assessment
We assessed dietary intake using a food frequency questionnaire (FFQ) specifically designed and validated for use among the Costa Rican population [34,35]. The FFQ assessed the intake of fruits, vegetables and other foods that are commonly consumed in Costa Rica. Carotenoid intakes were computed using the recently published data on concentration of carotenoids in commonly consumed Costa Rican foods [36]. This questionnaire has been specifically validated for the intake of carotenoids and consumption of fruits and vegetables in adolescents [33] and among adult Costa Ricans [34,37] and the intakes from the FFQ were similar to those estimated by others using 24-hr dietary recalls [38].
Carotenoids in Plasma
The procedures for blood collection and analysis of carotenoids in plasma in this study have been previously described [33,34]. Briefly, blood was collected in the morning at each subject’s home following an overnight fast. Blood samples were collected in tubes containing 0.1% EDTA and stored in a cooler with ice packs at 4°C. Within four hours, the specimens were centrifuged at 1,430 G for 20 min at 4°C to obtain plasma. Plasma samples were then stored in a freezer at –80°C for 1–7 months until they were transported over dry ice to the Harvard School of Public Health for analysis.
Concentrations of the major carotenoids (-carotene, ß-carotene, lycopene, ß-cryptoxanthin, and lutein + zeaxanthin) and tocopherols in plasma were measured using high performance liquid chromatograph as previously described [33,34]. 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 in Boston [33].
Statistical Analyses
We used SAS software (SAS Institute Inc., Cary, NC, version 8) for all statistical analyses. Two subjects were excluded due to missing data. The final sample consisted of 159 adolescents and 159 adults. Individual carotenoids and other nutrients were loge- or square root-transformed to improve normality. Normalized intakes (fatty acids, protein, carbohydrate, fiber and micronutrients) were regressed on total energy intake to obtain energy-adjusted nutrient intakes for each subject [34,39]. The same method was used to adjust plasma carotenoids for total plasma cholesterol concentrations. We used the Tukey multiple comparison test to compare the intakes and plasma concentrations between adolescents and adults after adjusting for gender and lack of independence between adolescents and adults. We also adjusted the means of the plasma carotenoid concentrations for smoking status. In these analyses a variable identifying the adolescent-parent or grandparent pair was included in the REPEATED statement of MIXED PROCEDURE of SAS to adjust for non-independence.
We divided the subjects into tertiles of intake of a given food or food group and determined the proportion of adolescents and adults with low, moderate and high intakes of that food or food group. We tested the significance of the differences in the distributions using the chi square test. A p < 0.05 was considered statistically significant. Preliminary analyses showed that children from parents who were cases of myocardial infarction were not different from those who are from control parents. Thus the analyses presented below are not stratified or adjusted for the MI status of the parent or grandparent.
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RESULTS
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Table 1 shows the characteristics of the Costa Rican adolescents and adults in this study. As compared to adults, adolescents smoked less, were more physically active, were less overweight and had significantly lower plasma concentrations of total cholesterol, low-density lipoprotein cholesterol and triacylglycerol (p < 0.05 for all). Table 2 compares the dietary intakes between adolescents and adults. As compared to adults, adolescents had higher intakes of total energy, total fat, animal fat, monounsaturated fat, polyunsaturated fat and vitamin E, but lower intakes of protein, fiber, vitamin A, vitamin B6, folic acid, potassium, magnesium and zinc (p < 0.05 for all). There were no significant differences in the intake of saturated fat, trans fat and carbohydrates.
Intakes and plasma concentrations of carotenoids and tocopherols in adolescents and adults are presented in Table 3. Except for lycopene and ß-carotene, the plasma concentrations of all the other carotenoids were significantly lower (p < 0.05) for the adolescents than for the adults. As compared to adults, adolescents had both an increase in intake and plasma concentrations of lycopene (p < 0.05). The intake of ß-carotene, ß-cryptoxanthin and lutein + zeaxanthin were also significantly higher (p < 0.05) in adults than in adolescents. Both intake and plasma concentrations of -tocopherol were significantly higher (p < 0.05) in adults than in adolescents. Plasma concentrations of -tocopherol were also significantly higher (p < 0.05) in adults than in adolescents. Intake of -tocopherol in adolescents was also lower than in adults but the difference was not significant (p > 0.05). Although mean carotenoid and tocopherols intakes and plasma concentrations in adolescents were significantly different from those in adults, these measurements were somewhat correlated. For instance, the intakes of -carotene (r = 0.09, p = 0.32), ß-carotene (r = 0.05, p = 0.59), ß-cryptoxanthin (r = 0.10, p = 0.22), lycopene (r = 0.16, p = 0.05), lutein + zeaxanthin (r = 0.11, p = 0.20), -tocopherol (r = 0.19, p = 0.03) and -tocopherol (r = 0.21, p = 0.01) in adolescents were correlated with the corresponding intakes in adults. Plasma concentrations of -carotene (r = 0.09, p = 0.31), ß-carotene (r = 0.10, p = 0.23), ß-cryptoxanthin (r = 0.00, p = 0.97), lycopene (r = 0.20, p = 0.02), lutein + zeaxanthin (r = 0.13, p = 0.13), -tocopherol (r = 0.18, p = 0.03) and -tocopherol (r = 0.28, p = 0.001) in adolescents were also somewhat correlated to those in adults.
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Table 3. Mean Daily Intakes and Plasma Concentrations of Carotenoids and Tocopherols in Adolescents and Adults in Costa Rica
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Table 4 shows proportions of adolescents and adults with low, moderate and high intakes of fruits, vegetables, and other food groups. Most adolescents consumed more servings of fruits than adults. On average, adolescents consumed more orange juice, mangos, raw carrots, ketchup, pizza, peas, beans, coleslaw and broccoli, while adults consumed more papaya, avocado, yellow squash and cucumber. Consumption of dairy products and red meat was significantly higher among adolescents than adults. A significantly higher proportion of adolescents consumed greater amounts of carbonated drinks (sodas), fried potatoes, snacks and less of traditional starchy foods such as cassava (Table 4). Consumption of staple foods such as rice by adolescents was similar to that in adults.
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Table 4. Proportion of Adolescents and Adults in the Low, Middle and High Tertiles of Intake of Selected Foods in Costa Rica
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DISCUSSION
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In this study we have shown that the plasma concentrations of -carotene, ß-cryptoxanthin and lutein + zeaxanthin and the intakes of ß-carotene, ß-cryptoxanthin and lutein + zeaxanthin in adolescents were significantly lower than those in adults. Lycopene was the only carotenoid in which intake and plasma concentrations were significantly higher in adolescents than adults. These data also suggest that, as compared to adults, adolescents consumed diets that were higher in total energy, dairy products, red meat, carbonated drinks, fried potatoes and snacks. As a proportion of total energy intake, adolescents consumed diets lower in dietary fiber and micronutrients (e.g., tocopherols, potassium, magnesium, zinc and some vitamins).
The dietary intakes observed in this study, together with the trend in developing countries towards increased obesity [26], diabetes [30,40] and cardiovascular disease [41] underscore the importance of research into the dietary habits of adolescents. Developing countries, which contribute the largest proportion of the global burden of cardiovascular disease and where CVD mortality occurs at an early age as compared to developed countries [41], are undergoing a nutritional transition in which economic growth is accompanied by decreasing physical activity and increased consumption of diets poor in micronutrients and fiber but high in fat and total energy [42,43]. In these countries, this trend toward consumption of unhealthy foods has not been only attributed to improvements in the national economies and the globalization of food production and supply [42], but also to increased food advertising, especially among adolescents, in developed countries [44,45]. It is therefore important to understand the food quality and dietary patterns of adolescents in developing countries to design interventions that will educate adolescents on healthy dietary habits. Our study, which assessed nutrient intakes using a validated food-frequency questionnaire [34] and plasma carotenoid concentrations as biomarkers of intake [37], attempted to describe the nutritional habits of adolescents and adults to determine whether adults could serve as a potential source of information on good dietary habits.
We found that the diet of adolescents was poor in most micronutrients (e.g., carotenoids, vitamins and minerals) and this was also reflected in the lower plasma concentrations of carotenoids in adolescents than in adults. The diet of Costa Rican adolescents could predispose to obesity and chronic disease, hence a need for a campaign to promote an increased intake of foods rich in micronutrients. Although, lycopene, a carotenoid associated with a protective effect on the risk of cancer, cardiovascular disease and atherosclerotic progression [15,20,21], was significantly higher in adolescents than in adults, this may reflect a poor dietary pattern in adolescents. The higher intake of lycopene in adolescents is likely due to consumption of ketchup and pizza (rich sources of lycopene) but not due to other sources of lycopene such as tomatoes, tomato sauce and watermelon, for which intakes were similar between adolescents and adults. Frequent consumption of pizza, a food with a high glycemic index and high in saturated and trans fatty acids could in the long-term predispose to chronic diseases. The poor intake of micronutrients in adolescents is also reflected by the high consumption of fried potatoes, snacks and carbonated drinks.
We observed correlations between adolescents and adults, albeit small, in both intake and plasma concentrations of carotenoids and tocopherols. These correlations may indicate that the diets of adolescents are influenced by those of adults. This observation is consistent with previous studies in the US and Europe reporting that previous eating behavior [24] and parental attributes, such as dietary composition, may influence dietary habits of children [25,27–29]. The correlations observed, especially for plasma lycopene (r = 0.20), -tocopherol (r = 0.18) and -tocopherol (r = 0.28) in adolescents and adults, may suggest that adolescents may acquire habitual consumption of foods rich in micronutrients from adults.
Although the total consumption of fruits was higher in adolescents than in adults, plasma concentrations of -carotene, ß-cryptoxanthin and lutein + zeaxanthin and intakes of ß-carotene, ß-cryptoxanthin and lutein + zeaxanthin observed in adults were significantly higher than those in adolescents. This may be due to the higher consumption of papaya, cooked carrots, yellow squash and cucumber for adults than adolescents. Also, the total consumption of vegetables in adults tended to be higher than in adolescents, although the differences were not significant. Previously Irwig and others [33] showed that papaya, a fruit frequently eaten by the general Costa Rican population and by the adults in this study, was the best predictor of ß-cryptoxanthin and was a good source of other carotenoids. Nevertheless, we observed modest correlations between intake and plasma carotenoid concentrations between adolescents and adults. Parents may play an important role in influencing the dietary behaviors of their children. Our study signals the need for educational programs in developing countries to promote healthier eating patterns among adolescents. This recommendation needs to be further examined by a prospective study.
In summary, adolescents as compared to adults consumed greater quantities of fruits, dairy products, red meat, carbonated drinks and polyunsaturated fat, and lower quantities of vegetables, fiber and micronutrients (carotenoids, vitamins A and B6, folate, potassium, magnesium and zinc). Plasma concentrations of all carotenoids, except for lycopene, were lower in adolescents than in adults. The low correlations between adolescent and adult intakes and plasma concentrations of carotenoids and tocopherols suggest that although parents may influence the dietary habits of their children and serve as a good target for promoting healthy dietary habits among adolescents, other factors need to be considered.
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ACKNOWLEDGMENTS
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We are grateful to all the study participants and the staff of Projecto Salud Coronaria, San José, Costa Rica. This study was supported by a research grant HL 49086 from the National Institutes of Health and by an American Heart Association Medical Research Fellowship provided through Cornell University Medical College to M.S. Irwig.
Received July 27, 2004.
Accepted November 16, 2004.
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ABSTRACT
INTRODUCTION
