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Article

Carotenoid Intakes, Assessed by Dietary Questionnaire, Are Associated with Plasma Carotenoid Concentrations in an Elderly Population

Jean Mayer U.S. Department of Agriculture Human Nutrition Center on Aging at Tufts University, Boston, MA 02111, ^a Department of Nutritional Sciences, University of Connecticut, Storrs, CT, 06269 and ^b Framingham Heart Study, Framingham, MA 01702

	ABSTRACT

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High intakes of fruits and vegetables and of carotenoids are associated with a lower risk for a variety of chronic diseases. It is therefore important to test the validity of dietary questionnaires that assess these intakes. We compared intakes of five carotenoids, as calculated from responses to the Willett 126-item food-frequency questionnaire, with corresponding biochemical measures. Subjects included 346 women and 201 men, aged 67–93 y, in the Framingham Heart Study. Unadjusted correlations were higher among women than men as follows: -carotene 0.33 and 0.18, ß-carotene, 0.36 and 0.25; ß-cryptoxanthin, 0.44 and 0.32; lycopene, 0.35 and 0.21; and lutein + zeaxanthin, 0.27 and 0.10, respectively. Adjustment for age, energy intake, body mass index (BMI, kg/m²), plasma cholesterol concentrations and smoking reduced the gender differences, respectively, to the following: -carotene 0.30 and 0.28; ß-carotene, 0.34 and 0.31; ß-cryptoxanthin, 0.45 and 0.36; lycopene, 0.36 and 0.31; and lutein + zeaxanthin, 0.24 and 0.14. Plots of adjusted mean plasma carotenoid concentration by quintile of respective carotenoid intake show apparent greater responsiveness among women, compared with men, to dietary intake of - and ß-carotene and ß-cryptoxanthin, but similar blood-diet relationships for lycopene and lutein + zeaxanthin. Reported daily intake of fruits and vegetables correlated most strongly with plasma ß-cryptoxanthin and ß-carotene among women and with plasma - and ß-carotene among men. With the exception of lutein + zeaxanthin, this dietary questionnaire does provide reasonable rankings of carotenoid status among elderly subjects, with the strongest correlations for ß-cryptoxanthin. Appropriate adjustment of confounders is necessary to clarify these associations among men.

KEY WORDS: • carotenoids • dietary questionnaire • humans • plasma • phytochemicals

	INTRODUCTION

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With increasing evidence that fruit and vegetable consumption is associated with reduced risk for a variety of chronic diseases, there is growing interest in the examination of intake and status of specific phytochemicals, particularly carotenoids (National Research Council Committee on Diet and Health 1989 ). Until recently only ß-carotene and total carotenoids were quantitatively assessed with the use of dietary methodology because of the lack of specific food composition data. With the availability of a new database on carotenoids released by the USDA in 1993 (Mangels et al. 1993 ), it is now easier to assess intakes of the individual carotenoids. In addition to ß-carotene, these include -carotene, ß-cryptoxanthin, lycopene and lutein + zeaxanthin. Each of these has hypothetical health effects, making its individual assessment important. The recent negative results of major ß-carotene supplementation trials, despite a wealth of studies showing protective effects of higher plasma ß-carotene concentrations from dietary intake, demonstrate the need to examine other phytochemicals that may coexist with ß-carotene in the diet (Hennekens et al. 1996 , Omenn et al. 1996 , The Alpha-Tocopherol and Beta Carotene Cancer Prevention Study Group 1994 ).

Several studies have compared the dietary intake measures of carotene or ß-carotene equivalents with plasma concentrations of carotene or total plasma carotenoids (Boeing et al. 1997 , Jacques et al. 1993 , Jarvinen et al. 1993 , Liu et al. 1992 , Roidt et al. 1988 , Stryker et al. 1988 , Willett et al. 1983 ). One report has related general carotene intake with individual plasma carotenoids (Bingham et al. 1997 ); more recently, several studies have compared the intakes of individual carotenoids with their respective plasma concentrations (Brady et al. 1996 , Coates et al. 1991 , Forman et al. 1993 , Michaud et al. 1998 , Peng et al. 1995 , Ritenbaugh et al. 1996 Scott et al. 1996 , Yong et al. 1994 ). Six of these measured dietary intake of carotenoids with modified versions of the Block food-frequency questionnaire (Brady et al. 1996 , Coates et al. 1991 , Forman et al. 1993 , Peng et al. 1995 , Ritenbaugh et al. 1996 , Yong et al. 1994 ), and three used diet records (Forman et al. 1993 , Scott et al. 1996 , Yong et al. 1994 ). We are aware of only one study that used the Willett food-frequency questionnaire (Michaud et al. 1998 ). In this study, we examine the relationship between intake of individual carotenoids, as measured with the Willett 126-item food-frequency questionnaire (Rimm et al. 1992 , Willett et al. 1987 ), and plasma concentrations in a sample of 201 men and 346 women, aged 67–93 y, participating in the Framingham Heart Study.

	METHODS

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Subjects.

The Framingham Heart Study is a longitudinal cohort study that was initiated in 1948 to examine risk factors for heart disease. Approximately 5200 men and women were examined at baseline (Dawber et al. 1951 ). At the 20th examination (1988–89), more than half of the original cohort had died; 1401 subjects were examined. Of these, a total of 230 men, aged 68–91 y, and 408 women, aged 67–93 y, without diagnosed cardiovascular disease, cerebrovascular disease or cancer were selected for analysis of plasma carotenoids. These individuals were selected to avoid potential confounding due to the possible effects of these chronic diseases on nutrient metabolism. Completed, usable food-frequency questionnaires were available for 201 men and 346 women; these comprise the sample used here.

Dietary measures.

Usual dietary intake was assessed at the 20th examination with a semiquantitative 126-item food-frequency questionnaire (Rimm et al. 1992 , Willett et al. 1987 ). Questionnaires were mailed to the subjects before the examination, and they were asked to complete them and bring them to the exam. This questionnaire instructs subjects to complete frequency of consumption of individual foods, with the assumption of a standard portion size, which is provided on the questionnaire for guidance. For fruits and vegetables, these are usually either one piece, one-half cup or a small glass of juice. The questionnaire also includes questions about use of vitamin and mineral supplements and allows specification of the type of breakfast cereal most frequently used. This food-frequency questionnaire has been validated for many nutrients including dietary carotene, and in several populations against multiple diet records and/or plasma measures, (Ascherio et al. 1992 , Jacques et al. 1993 , Willett et al. 1983 ). We know of only one study that has examined the validity of this questionnaire for individual carotenoids (Michaud et al. 1998 ). Questionnaires resulting in energy intakes <2.51 or >16.74 MJ (600 and 4000 kcal, respectively) per day, or with >12 food items left blank were considered invalid and excluded from further analysis. Of 1068 food frequencies, 92 (8.6%) were eliminated on the basis of these criteria. Individual carotenoid intakes were calculated at Harvard University with a carotenoid database developed for the questionnaire from the USDA carotenoid database (Mangels et al. 1993 ). Reported frequency of individual fruit and vegetable items were standardized to daily intake and summed to obtain the average number of reported servings of fruits and vegetables consumed per day for each person.

Plasma measures.

The methodology for assessing the plasma carotenoids has been described (Vogel et al. 1997 ). Briefly, blood samples were collected from nonfasting subjects during the 20th examination into vacutainer tubes containing EDTA (1.5 g/L final concentration); plasma was separated after centrifugation of blood at 1000 x g for 20 min at 4°C. Plasma aliquots were stored at -80°C. Carotenoid concentrations were measured with a reversed-phase HPLC method described by Barua et al. (1993) , using ß-apo-8'-carotenyl-myristate in methanol as an internal standard. The HPLC system included a Model 717 autosampler (Millipore, Milford, MA), and carotenoid data were monitored with a Varian 2550 detector (Palo Alto, CA), set at 450 nm. The analyte peaks were identified by retention times and quantified using standard curves of external standards (Sigma Chemical, St. Louis, MO) for each analyte.

Total cholesterol and HDL cholesterol were measured in fresh plasma at the laboratory of the Framingham Heart Study using Abbott cholesterol reagent and an ABA-200 analyzer (Abbott Diagnostics, Irving, TX) (McNamara and Schaefer 1987 ). Non-HDL cholesterol was calculated as the difference between total cholesterol and HDL cholesterol.

Statistical analysis.

All statistical analyses were performed using SAS (release 6.12, SAS Institute, Cary, NC) on a VAX mainframe computer. Descriptive means are presented in the untransformed scale. Neither the dietary nor the plasma carotenoid measures were normally distributed, and both sets of variables were normalized using square-root transformations. Transformed variables were used for all correlational analyses. We used Pearson correlations to estimate associations between the dietary and plasma measures for each carotenoid for men and women separately. For ß-carotene only, correlations were also estimated for the subset of subjects not using supplements containing ß-carotene (there were no supplement users for the other carotenoids). Partial correlations were used to adjust first for age and total energy intake and then also for body mass index (BMI), plasma cholesterol concentrations, and smoking for men and women, respectively. Because intake of most nutrients and other food constituents correlates with energy intake, adjustment for this variable allows an assessment of the correlation independent of sample variation in total energy intake, partially adjusting for differences in intake that may be due to body size or activity levels, and for some of the measurement error inherent in the questionnaire (Willett and Stampfer 1986 ). Other adjustment variables have been previously shown to relate to plasma carotenoid concentrations in this population (Vogel et al. 1997 ).

To estimate the relationship between total number of fruits and vegetables reported as servings consumed per day and each of the carotenoids, we used Pearson correlations to compare the distribution of each plasma carotenoid (square-root transformed for normality) with total number of servings of fruits, vegetables, and combined fruits and vegetables (also square-root transformed for normality). Both the crude and adjusted correlations (as described above) were calculated.

We estimated mean plasma carotenoid concentrations for respective intake quintiles, for women and for men, using the General Linear Models (GLM) procedure, with adjustment for age, energy intake, BMI, plasma HDL and non-HDL cholesterol concentrations, and smoking. These mean values were then plotted along with their 95% confidence intervals, separately for men and women. Finally, we identified and ranked the major food contributors to the intake of each carotenoid.

	RESULTS

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Table 1 presents a description of the study population of men and women. The ages ranged from 67 to 93 y. BMI were high at 27.0 kg/m² for men and 26.1 kg/m² for women. Just slightly >10% of the subjects were current smokers, although many more (50% of the men and 39% of the women) were former smokers.

View larger version (19K): [in this window] [in a new window]   Figure 1. Plasma -carotene concentration (µg/d) in elderly men (, n = 201) and women (, n = 346) plotted against median daily -carotene intake (µmol/L) by quintile, adjusted for age, energy intake, body mass index, plasma cholesterol concentrations and smoking status.Values are means ± 95% confidence interval. Within gender, means with no common letters differ, P < 0.05.

View larger version (19K): [in this window] [in a new window]   Figure 3. Plasma ß-cryptoxanthin concentration (µg/d) in elderly men (, n = 201) and women (, n = 346) plotted against median daily ß-cryptoxanthin intake (µmol/L) by quintile, adjusted for age, energy intake, body mass index, plasma cholesterol concentrations and smoking status.Values are means ± 95% confidence interval. Within gender, means with no common letters differ, P < 0.05.

View larger version (20K): [in this window] [in a new window]   Figure 4. Plasma lycopene concentration (µg/d) in elderly men (, n = 201) and women (, n = 346) plotted against median daily lycopene intake (µmol/L) by quintile, adjusted for age, energy intake, body mass index, plasma cholesterol concentrations and smoking status.Values are means ± 95% confidence interval. Within gender, means with no common letters differ, P < 0.05.

	DISCUSSION

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At least six studies have examined individual associations between dietary carotenoids, as measured by the Block food-frequency questionnaire, and plasma carotenoid concentrations (Brady et al. 1996 , Coates et al. 1991 , Forman et al. 1993 , Peng et al. 1995 , Ritenbaugh et al. 1996 , Yong et al. 1994 ). The earliest of these studies used a database developed specifically for the Block questionnaire, based on limited analytic data and extrapolation of values for similar foods (Coates et al. 1991 ). The more recent studies have used the database developed by the USDA and the National Cancer Institute (Mangels et al. 1993 ). These databases have been compared and shown to yield different quantitative estimates, but similar correlations with blood concentrations (Ritenbaugh et al. 1996 , Vandenlangenberg et al. 1996 ). Correlations reported by these studies range from 0.24–0.51 for -carotene; 0.21–0.58 for ß-carotene; 0.36–0.46 for ß-cryptoxanthin; 0–0.37 for lycopene; and 0.09–0.45 for lutein + zeaxanthin. Our findings for each of these carotenoids fall within these ranges and are higher than those reported by most of these studies for lycopene and ß-cryptoxanthin, but lower for lutein + zeaxanthin.

We were able to identify only one study that has examined the association between individual carotenoid intakes, as measured by the Willett food-frequency questionnaire, and corresponding plasma carotenoid concentrations (Michaud et al. 1998 ). Looking only at nonsmokers, Michaud et al. (1998) reported higher correlations for -carotene than those reported here for both men and women (0.47 vs. our 0.28 for men, and 0.48 vs. our 0.30 for women). Among men, their correlations were higher than those seen here for ß-cryptoxanthin (0.43 vs. our 0.36), lycopene (0.47 vs. our 0.31) and lutein (0.40 vs. our 0.14). Conversely, our correlations for ß-cryptoxanthin and lycopene were higher for women than theirs (0.45 vs. 0.32 and 0.36 vs. 0.21, respectively).

Other studies have compared intake of total carotenoids from the Willett questionnaire to plasma carotenoid concentrations. Willett et al. (1983) reported a correlation of 0.29 for this association, which increased to 0.35 when fully adjusted for age, gender, energy intake and blood lipid concentrations. Jacques et al. (1993) found that this association was much stronger for women (r = 0.49, P < 0.001) than for men (r = 0.19, not significant). In this study, we also found higher unadjusted correlations among women than among men for -carotene (0.33 vs. 0.18 for women and men, respectively), and ß-carotene (0.36 vs. 0.25). However, the gender differences closed considerably with adjustment for total energy intake, age, BMI, plasma cholesterol concentrations and smoking status. This suggests that the carotenoid diet-plasma association is confounded by one or more of these variables and that they should be adjusted in studies that examine these associations. Willett et al. (1983) found a significant negative association between BMI and plasma carotene concentration and a significant positive association between plasma cholesterol and plasma carotene concentration (smoking was not included in that study). Several others (Albanes et al. 1997 , Marangon et al. 1998 , Pamuk et al. 1994 ) demonstrated the negative effect of smoking on plasma carotene concentrations. We have shown previously (Vogel et al. 1997 ) that BMI was negatively associated with of all the individual carotenoid concentrations except for lycopene in this sample, and that smoking was negatively associated with - and ß-carotene and ß-cryptoxanthin concentrations, but not with lycopene and lutein + zeaxanthin.

We found that correlations were greatest for ß-cryptoxanthin, which is found primarily in only a few foods, mainly orange juice and oranges (79%) and peaches (14%). This was followed by lycopene, found mostly in tomatoes and tomato products (81%). Correlations were also reasonably high for - and ß-carotene, both found mainly in carrots (77 and 37%, respectively). Correlations were lowest (and not even significant for the male subset) for lutein + zeaxanthin, which is found primarily in green leafy vegetables, but with significant contributions from a much wider variety of foods. Although not completely consistent, the other studies that have examined these have tended to report greater correlations for ß-cryptoxanthin and/or - and ß-carotene than for lycopene or lutein (Brady et al. 1996 , Coates et al. 1991 , Forman et al. 1993 , Michaud et al. 1998 , Peng et al. 1995 , Ritenbaugh et al. 1996 , Yong et al. 1994 ). The ability of the questionnaire to capture intake with a few well-defined food items reduces error of estimate and associated misclassification of dietary intake. In addition to limitations of the questionnaire, these differences in correlation strength may be due to several factors, including the day-to-day variability of the plasma measure of the nutrient, or issues related to the bioavailability of individual carotenoids.

The differences across men and women are important and suggest that the questionnaire performs better among women for these carotenoids. Men may report their fruit and vegetable intake less accurately than do women. However, the observation that men generally have lower plasma concentrations than women of - and ß-carotene and ß-cryptoxanthin, but not of lycopene or lutein + zeaxanthin for the same level of dietary intake, along with the large improvement in the men's correlations seen with adjustment for BMI, cholesterol concentrations and smoking, suggest that other mechanisms may be operating.

Correlations between fruit and vegetable intake and plasma carotenoids were, not surprisingly, lower than those comparing individual carotenoid intake with respective plasma concentrations. However, for - and ß-carotene in both men and women, and for ß-cryptoxanthin in women, simply measuring total fruit and vegetable intake appears to provide a reasonable ranking, with correlations ranging from 0.23 to 0.34. On the other hand, fruit and vegetable intake does not appear to adequately serve as an indicator of lycopene or lutein + zeaxanthin intake. Further exploration of specific food intakes, particularly of tomatoes, may prove to be more useful for lycopene intake. Few studies have compared fruit and vegetable intake directly with individual plasma carotenoid concentrations. For each of the carotenoids (except for lycopene for which their correlation was negative), Polsinelli et al. (1998) found higher correlations than those seen in our study. Their correlations, with just 20 adult women, ranged from 0.31 for ß-cryptoxanthin to 0.73 for -carotene. However, they were comparing 7-d food records with blood that was drawn immediately after the record days. Similar to our results, they found that combined fruit and vegetable intake yielded the highest correlations, compared with intake of either fruits or vegetables alone, except for ß-cryptoxanthin, which is stronger when compared with fruit intake alone.

In conclusion, correlations for lutein + zeaxanthin suggest that the Willett 126-item questionnaire does not provide a reliable estimate of lutein + zeaxanthin status. Further work to either improve specification of foods containing these carotenoids or in understanding the reasons for the low correlation is needed. On the other hand, this questionnaire does appear to provide reasonably valid and useful information about other individual carotenoids, particularly ß-cryptoxanthin, lycopene and ß-carotene.

View larger version (18K): [in this window] [in a new window]   Figure 2. Plasma ß-carotene concentration (µg/d) in elderly men (, n = 201) and women (, n = 346) plotted against median daily ß-carotene intake (µmol/L) by quintile, adjusted for age, energy intake, body mass index, plasma cholesterol concentrations and smoking status.Values are means ± 95% confidence interval. Within gender, means with no common letters differ, P < 0.05.

View larger version (18K): [in this window] [in a new window]   Figure 5. Plasma lutein + zeaxanthin concentration (µg/d) in elderly men (, n = 201) and women (, n = 346) plotted against median daily leutin +zeaxanthin intake (µmol/L) by quintile, adjusted for age, energy intake, body mass index, plasma cholesterol concentrations and smoking status.Values are means ± 95% confidence interval. Within gender, means with no common letters differ, P < 0.05.

	FOOTNOTES

¹ Supported in part by federal funds from the U.S. Department of Agriculture under contract number 53–3K06–5-10, the National Institutes of Health grant number R01 AR/AG 41398, NIH/NHLBI contract number NO1-HC-38038, and by the Storrs Agricultural Experiment Station.

² The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked ''advertisement'' in accordance with 18 USC section 1734 solely to indicate this fact.

³ Current address: Department of Medicine, College of Physicians and Surgeons of Columbia University, New York, NY.

Manuscript received August 5, 1998. Initial review completed September 4, 1998. Revision accepted October 22, 1998.

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