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Department of Animal and Nutritional Sciences and * Department of Psychology, University of New Hampshire, Durham, NH 03824
3To whom correspondence should be addressed. E-mail: Joanne.Burke{at}unh.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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27, those with a BMI < 27 had higher serum concentrations of ß-carotene (P = 0.002), and higher MPOD at 60' (P = 0.04) and 120' (P = 0.01). These findings suggest that carotenoid-rich diets and serum carotenoids positively contribute to MP status.
KEY WORDS: • aging • carotenoids • macular pigment
Limited data exist on the amount of macular pigment (MP)4 found in the healthy human retina (1–4), although its presence may confer health benefits (2–8). Three isomeric carotenoids, lutein (L), zeaxanthin (Z), and mesozeaxanthin (MZ) are the principal MP components (9). Both L and Z are of dietary origin, whereas the presence of MZ is attributed to the conversion of L to MZ in the retina (9). It is purported that these dihydroxy-carotenoids are selectively deposited in the retina where they filter out light in the potentially harmful region of the visible spectrum (
400–500 nm) (8,10–12), engage in antioxidant reactions (2,8,13–15), contribute to the preservation of visual sensitivity and resolution (4,16–18), and protect against eye diseases such as macular degeneration (19–21).
Carotenoids consist of a group of >600 lipophilic compounds (22). Concentrations of carotenoids in human serum and tissue are extremely variable and reflect not only diet and supplement use, but factors such as carotenoid chemistry (23), the food matrix (24), individual efficiency of absorption (25), fat intake (26,27), competition among carotenoids for absorption (28), cholesterol and lipoprotein status (29), metabolic status (30), body composition (31,32), and BMI (33). Some studies indicate that as BMI approaches or exceeds clinically defined obesity (30 kg/m2), there are lower circulating levels of carotenoids (33–36), whereas others did not detect a difference (37).
Dietary and serum L and Z (L + Z) concentrations are often positively associated with MP (6,38). Conflicting results were reported on the influence of sex (6,39), age (17,18,40,41), and BMI (37,42,43) on MP. Previous studies examined MP in subjects < 50 y old at a single retinal site, typically the 30-min (30') locus, and in one eye (1,39,44). In this study, we investigated carotenoids and MP in an exclusively older cohort, at multiple retinal sites: 10 min (10'), 30', 60 min (60'), and 120 min (120'). If dietary or lifestyle practices can enhance MP, and possibly delay or prevent vision loss, improved quality of life and decreased health care costs may be realized.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Anthropometrics. Participants removed their shoes for height and weight measurements. Weight was recorded to the nearest lb, and height to the nearest quarter inch. BMI was calculated as wt (kg)/height (m2). BMI was assessed as a dichotomous variable; a cutoff value of 27 kg/m2 was used based on the work of Hammond et al. (42), Campbell and Gerich (47), Facchini et al. (30), and Neuhouser et al. (33).
Dietary assessments. The 122-item FFQ from the Fred Hutchinson Cancer Research Center was used to assess annual dietary practices (48). The FFQ database was derived from the Minnesota Nutrition Coordinating Center (NCC), which included the USDA-NCC database for carotenoids and was used in a similar study (39). Portion sizes were reviewed. The estimated energy intake was expected to fall within 2090–20900 kJ/d, a range used in a previously published study (45). One subject did not return the FFQ, and another’s data were outside the energy range. No subject reported using L or Z supplements at levels > 250 µg as found in some over-the-counter multivitamins.
The nationally available 7-item Eating Habits Screener© from the Block Dietary Data Systems assessed fruit and vegetable intake. Initially, subjects were grouped into 4 consumer levels (low, medium, high, and very high) based on the Screener’s categories. Because >50% of the subjects’ scores exceeded the average American intake using the Screener’s cutoff values, categories for this study were rescaled; "low" consumer scores of 7–11 (n = 10) reflected intakes of <3 servings of fruit and vegetables/d, "medium" scores of 12–15 (n = 31) were similar to the average American of <4 servings/d. Both high consumers with scores of 16–19 (n = 35) and very high consumers (n = 22) with scores of 20–24 met or exceeded 5 servings/d.
Biochemical assessment. Analysis for ß-carotene (BC), lycopene (LY), L and Z were conducted using a modified procedure based on previously published methods by our laboratory (6,39). Blood from fasting (10–12 h) subjects was drawn into serum separation Vacutainer® tubes (#36–6511SS, Gel and Clot Activator® gray and red tiger top, Becton Dickinson) and centrifuged at 1650 x g for 15 min at 4°C (Beckman Model Centrifuge TJ-6). Samples were stored at –80° (Beckman Model Refrigeration Unit TJ-R). Carotenoids were analyzed using an HPLC system (Hewlett Packard 1100/Agilent Technologies) equipped with a photodiode array detector (HP 1100 series) set at 452 nm. The C-18 analytical column (4.6 x 250 mm Bakerbond Mallinckrodt Baker) was kept at a constant temperature (24.8°C) using a CH-30 column heater (Eppendorf/Brickman) and temperature controller (Eppendorf TC-50). The mobile phase consisted of 100% methanol buffered with 0.1% ammonium acetate. A flow rate of 1.5 mL/min transitioned to methanol:methylene chloride (80:20, v:v) buffered with 0.1% ammonium acetate.
Methods were developed and stored using Hewlett Packard/Agilent HP 3365 Series II Chemstation. Quantification was performed with peak area ratios to internal standards and by simultaneously running laboratory standards. Tocopherol acetate and retinyl acetate were used as internal standards. HPLC performance was monitored by periodically assaying samples from the National Institute of Standards and Technology. Each carotenoid sample was analyzed in duplicate on the same day. Although L and Z were quantified separately, their results were also combined to yield an aggregate L + Z value.
Vision assessment. The Early Treatment of Diabetic Retinopathy Study chart and the Amsler Grid assessed visual acuity and retinal integrity. Macular pigment optical density (MPOD) was measured in individuals who had a best-corrected visual acuity of 20/60 and who perceived the Amsler Grid without distortion.
Heterochromatic flicker photometry was used to measure MPOD at 4 fovea loci in each subject’s right eye: 10', 30', 60', and 120'. Earlier work by Hammond and Fuld (45) demonstrated a high concordance between a subject’s left and right eye. The parafoveal target was centered at 420' (7°) of nasal eccentricity and had a visual angle of 120' (20). For each locus assessed, 6–8 measures were taken; the mean was calculated and log transformed. The test stimuli used were produced by a Macular Metrics® optical system; this instrument’s design and detailed validation results are available (49).
Statistical analysis.
A Pearson Product Moment Correlation was used to assess relations between reported carotenoid intake from the FFQ and MPOD, and serum concentrations and MPOD. A 1-factor ANOVA was used to determine differences among the 4 Eating Habits Screener consumer groups as well as the age-quartiles. For significant tests, the strength of association was calculated with partial eta squared (
p2) and for post hoc analysis, Tukey’s HSD was used to test all pairwise comparisons. Because age, sex and BMI may affect MPOD (6,17,42), a multivariate analysis of covariance was used to analyze the differences between men and women, the 2 BMI groups, and the possible interactions between these factors. To assess the effect of age, quartile ranges were initially calculated on the basis of the distribution of the recruited subjects’ ages 45–49, 50–55, 56–61, and 62–75 y; the last quartile age range was adjusted to 62–73 y because MP data from the one 75-y-old subject did not meet inclusion criteria. A P-value < 0.05 was considered significant. Results are expressed as means ± SEM unless otherwise noted. Statistical analyses were preformed using SPSS 9.0® (1999) and Microcal Origin 7.5® (2003).
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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$50,000. Many reported never having routinely smoked cigarettes. Of the former habitual smokers, nearly 75% reported quitting smoking >15 y ago. Only one participant identified herself as being other than white of non-Hispanic origin.
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p2 = 0.103, n = 97), 60' (f = 3.23, P = 0.03, p2 = 0.07, n = 98), and the 120' (f = 4.42, P = 0.006, p2 = 0.107, n = 98). The MPOD of the lowest consumers was lower than that of the highest consumer groups at 30' (P = 0 0.007) and 60' (P = 0.016) eccentricity. At 120' eccentricity, the MPOD of the very high consumers was higher than the mean MPOD of both the lowest (P = 0.014) and medium (P = 0.019) consumers.
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-carotene, ß-cryptoxanthin, BC, LY, L and Z, for women was 14.49 mg/d ± 0.808; for men, it was 13.48 mg/d ± 1.009. Although there were differences for serum BC (P = 0.003), LY (P = 0.032), and L (P = 0.031) and L + Z tended to differ (P = 0.064) based on sex, MPOD at all loci did not differ.
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p2 = 0.103, n = 96) and 120' (f = 2.98, P = 0.04, p2 = 0.05, n = 95) eccentricity. The MPOD of the youngest age quartile (45–49 y) and oldest age quartile (62–73 y) was higher than the MPOD of the 2nd age quartile (50–55 y) at 60' (P = 0.005) eccentricity. At 120' eccentricity, the MPOD of the oldest quartile was higher than the MPOD of the 2nd age quartile (P = 0.03). The age groups did not differ when data were adjusted for BMI, dietary carotenoids, or serum carotenoid concentrations (data not shown).
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27 kg/m2 (Fig. 4). MPOD was different at 60' (P = 0.04) and 120' (P = 0.01) eccentricity. Compared with those with a BMI 27 kg/m2, subjects with a BMI < 27 kg/m2 had higher total dietary BC (P = 0.007) intake, higher adjusted carotenoid intakes for BC (P = 0.001) and L + Z (P = 0.001), and higher serum BC (P = 0.002) (Table 3).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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27 kg/m2. Unlike previous studies (51), no association was found with smoking history and MPOD (data not shown). The ability to detect an effect of smoking may have been diminished by the length of time between smoking cessation and MP assessment. Diet and serum carotenoids. Results from this study are similar to others using FFQ data (39,52) that have demonstrated a positive relation between L + Z consumption, serum L + Z concentrations, and MPOD (Fig. 1). Because MPOD was significantly and positively associated with both reported dietary intakes and serum L + Z concentrations, MPOD assessments may prove to be an additional biomarker for noninvasive L + Z assessment. The Eating Habits Screener was a rapid, inexpensive instrument whose results were similar to the more extensive FFQ. However, the Screener findings should be viewed cautiously given the small numbers of subjects in the lowest consumer group, and the fact that our consumers reported above average fruit and vegetable intakes.
Sex. Although women had higher unadjusted BC, higher adjusted BC and L + Z intakes, and higher serum concentrations for BC, LY and L + Z, the mean MPOD results for women were not higher than those for men (Table 2). This is similar to the results of Curran-Celentano et al. (38), but differs from other studies that have indicated higher MPOD in men than women in the Northeast (NE) (P = 0.001) (6), Southwest (SW) (P = 0.005) (41), and the Netherlands (P = <0.005) (53). Women’s MPOD in the present study did not differ from that of men (Table 2), but was higher than previously reported MPOD in NE men (0.38), and women (0.24) at 30' eccentricity (6); MPOD was also higher than previously reported for both Midwest (MW) (f = 0.207; m = 0.215) (39) and SW (f = 0.21; m = 0.24) (41) samples. Our subjects reported higher intakes of dietary L + Z compared with the MW sample (1.1 mg/d) (39). The fruit and vegetable intake of people in the SW was estimated to be 4 servings/d (41), whereas >55% of subjects in the current study met or exceeded the 5-A-Day guidelines (54); serum L + Z concentrations (Table 2) were also higher than those of subjects in the MW (0.372 µmol/L) (39). Additionally, close to 25% of the MW sample had low MPOD (0.00–0.10), whereas in the current study, only 2% of the subjects had a MPOD < 0.10 at 30' eccentricity (data not shown).
Differences in MPOD assessment may also have contributed to differences among studies. For instance, a parafoveal reference point of 240' (4°) retinal eccentricity was used in the MW and SW studies, compared with the 420' (7°) used in the current sample. Some optically detectable MP may be present at the 240' loci and may ultimately result in an underestimation of the calculated MPOD value.
Age. Similar to other studies, age did not have a predictable effect on MPOD (Fig. 3). Werner et al. (18) did not find that age affected MPOD in subjects aged 10–90 y, nor did Ciulla et al. (39) in those aged 18–50 y, or Broekmans et al. (53) with subjects aged 18–75 y. Decreases in MPOD were found in those aged 60–84 y, but not in subjects aged 21–63 y (17). Declines in MPOD were also detected in the SW sample, (17–91 y) (P = <0.02) (41) and in subjects aged 21–81 y (2) (P = 0.0006). Elsner et al. (40) proposed that changes in the foveal architecture occur with age, including a broadening of the foveal depression. This type of change may affect the distribution of MP.
BMI.
As in other studies, an inverse relation between BMI and some serum carotenoid levels was detected (33,36). Adjusted BC and L + Z intakes were significantly higher in subjects with a BMI < 27 kg/m2. Although unadjusted L + Z (P = 0.30) and serum Z (P = 0.89) did not differ between the BMI groups, Z is typically present in very low amounts in the diet and serum compared with L, often resulting in high variability in the Z quantities measured (55). In the present study, BMI was not linearly related to MPOD, but when assessed as a dichotomous variable, significantly lower MPOD was detected for those with a BMI 27 kg/m2 (Fig. 4). Hammond et al. (42) reported significantly lower MPOD at 30' eccentricity in subjects with a BMI 29 kg/m2, but in subjects with a BMI < 29 kg/m2, there was no relation between MPOD and BMI (r = 0.00). In those with a greater BMI, increased fluid volume and increased storage capacity of carotenoids may explain much of the lower serum carotenoid concentrations (33,36,56). It is possible that metabolic changes associated with being overweight (30) may also contribute to the lower carotenoid concentrations, and ultimately, lower MPOD.
In conclusion, the results from our study indicated that heterochromatic flicker photometry can be used to measure MPOD in most older adults free from retinal disease. Measurements at multiple sites provided specific data on the distribution of MP. Results are similar to previous studies that demonstrated a positive relation between L + Z intake, serum L + Z concentrations, and MPOD. Additional studies with comprehensive assessments of body mass and composition, coupled with biological assessments are required to determine the possible affects of body weight on carotenoids and MPOD status. Given the sample’s higher than average income and well above average fruit and vegetable consumption, data regarding dietary practices, serum carotenoid concentrations, and MPOD should be gathered from a larger, random sample to be applicable to a wider population. If MP is found to be protective, our findings of positive relations between higher MPOD with greater fruit and vegetable intake and higher MPOD with higher serum carotenoid levels hold promise for successful intervention and prevention strategies.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in part by the New Hampshire Agricultural Experiment Station Multi-State Research Fund (Scientific Contribution Number 2158), by a Dissertation Year Fellowship Grant from the University of New Hampshire, and the American Dietetic Association Foundation’s Jean Hankin Nutritional Epidemiology Award and the Helen Evangeline Gilson Award.
4 Abbreviations used: BC, ß-carotene; HSD, honestly significantly difference; L, lutein; L + Z lutein and zeaxanthin; LY, lycopene; MP, macular pigment; MPOD, macular pigment optical density; MZ, mesozeaxanthin; NE, New England; NCC, Nutrition Coordinating Center; SW, Southwest; MW, Midwest; UNH, University of New Hampshire; Z, Zeaxanthin.
Manuscript received 29 September 2004. Initial review completed 26 October 2004. Revision accepted 21 January 2005.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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