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,**
*
The Department of Food Science and Technology,
The Division of Hematology and Oncology, Department of Internal Medicine, The James Cancer Hospital and Solove Research Institute, Columbus OH and
**
The Ohio State University Nutrition Program, Columbus, OH 43210
3To whom correspondence should be addressed. E-mail: schwartz.177{at}osu.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • tomato • lycopene • lipoprotein oxidation • oxidative stress • humans
A number of human epidemiologic and clinical studies have suggested health benefits of tomatoes and processed tomato products (1 –4 ). The most often cited mechanism underlying these observations is the potential for tomato products to modulate radical-mediated oxidative damage that may contribute to the initiation and progression of many chronic disease processes (5 ). Although tomatoes contain an array of phytochemicals, most of the attention has been focused on lycopene, the predominant carotenoid present in tomatoes, which is responsible for the familiar red color. Lycopene exhibits a highly conjugated structure, contributing to its ability to quench singlet oxygen more efficiently than other carotenoids commonly found in the diet (6 ). The distribution of carotenoids in the lipophilic portion of the cell suggests an improved resistance of lipoproteins to oxidative damage (7 ,8 ).
Tomatoes and an array of processed tomato products account for the majority of lycopene consumed (9 ); watermelon, pink grapefruit, guava and other foods contribute to intake. Although human epidemiologic studies employ food composition databases to estimate intake from different foods, it is now clear that the bioavailability of carotenoids, including lycopene, from various sources is profoundly influenced by food processing, cooking and other components in the meals such as lipids and fiber, as well as physiologic and genetic factors controlling digestion and absorption (10 –12 ). A better understanding of lycopene bioavailability will improve our interpretation of human epidemiologic studies and help investigators design intervention trials to assess potential health benefits of lycopene.
Lycopene is a 40-carbon acyclic carotenoid and exists in multiple isomeric forms in vivo (13 ). Interestingly, the all-trans form of lycopene comprises 79–91% of the total lycopene found in tomato-based products (13 –17 ), whereas >50% of total lycopene found in serum and the 80–90% found in tissues exist as cis-lycopene isomers (13 ). The processes that influence isomer patterns, the mechanisms of interconversion and the potential biological end points that may be influenced by different isomers remain an essentially unexplored area of research.
The goal of this study was to explore the interrelationships among the intake of different commonly consumed processed tomato products, blood carotenoid and lycopene isomer profiles, and biomarkers of oxidative stress. The objectives of this study were as follows: 1) to determine the rate and magnitude of change in plasma total lycopene and isomer patterns over a period of 1 wk of consumption of a lycopene-free diet; 2) to determine the rate and magnitude of change in plasma total lycopene and isomer patterns over a period of 15 d after dietary intervention with Campbell’s Condensed Tomato Soup (CS),4 Campbell’s Ready To Serve Tomato Soup (RTS) or V8 Vegetable Juice (V8); and 3) to assess the effect of dietary intervention on several biomarkers of oxidative damage [i.e., ex vivo lipoprotein oxidation, urinary 8-hydroxy-2'-deoxyguanosine (8-OH-2'-dG), and urinary F(2)-isoprostane (8-epi-PGF2
)].
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Participants were healthy, nonpregnant, nonsmoking adults (n = 60; 30 men/30 women). The age and weight (means ± SEM) were 52.1 ± 1.9 y and 88.4 ± 3.0 kg for men and 53.1 ± 1.7 y and 70.9 ± 3.3 kg for women. Exclusions included those with gastrointestinal disease that may have altered food digestibility such as pancreatic insufficiency, hepatic disease, diabetes and metabolic enzyme deficiencies. The study was approved by the Biomedical Sciences Institutional Review Board of The Ohio State University, Columbus, OH. The objectives, requirements, and risks/benefits of the study were clearly outlined and informed written consent was obtained for each subject.
Study design.
Baseline blood samples from subjects who had fasted for 12 h were collected at the onset of the study for analysis of plasma carotenoids, vitamin E and vitamin A profiles. Participants consumed a lycopene-free diet for the next 7 d before being randomized to one of three treatment groups. During the washout phase, subjects were provided with a detailed list of all known lycopene-containing foods and asked to record any consumption of these foods daily. A second blood sample from subjects who had fasted for 12 h was drawn after the 7-d washout period. In addition to measuring the changes in plasma carotenoids, vitamin E and vitamin A on the blood sample obtained at the end of the washout period, ex vivo lipoprotein oxidation was analyzed. A 12-h overnight urine sample was also collected at the end of the 7-d washout period to determine pretreatment levels of 8-OH-2'-dG and 8-epi-PGF2. Individuals were then randomly assigned to receive CS [300 mL/d, 10 3/4 oz., 2 1/2 servings (as prepared); 35 ± 1 mg lycopene/d], RTS (320 mL/d, 10 2/3 oz., 1 1/3 servings; 23 ± 1 mg lycopene/d) or V8 (340 mL/d, 11 1/2 fl. oz., 1 serving; 25 ± 1 mg lycopene/d), provided by The Campbell Soup Company, Camden, NJ. These products served as their only source of lycopene throughout the 15-d dietary intervention phase. Again, subjects avoided all other lycopene-containing foods outlined on the list. After the 15-d tomato product dietary intervention, a third and final blood sample was collected from subjects who had fasted for 12 h. Complete plasma carotenoid, vitamin E, and vitamin A profiles along with susceptibility of lipoproteins to oxidation were determined. Concentrations of 8-OH-2'-dG and 8-epi-PGF2 in 12-h urine samples were also measured.
Blood sampling.
Venous blood samples were obtained in the General Clinical Research Center at The Ohio State University Medical Center, Columbus, OH. Blood was collected in 10-mL EDTA tubes under dim light. Blood samples were centrifuged at 4°C and 1500 x g for 10 min in a Beckman Coulter Allegra 6R Centrifuge (Fullerton, CA). Plasma was allocated for immediate analysis or for storage at -80°C. Total blood and plasma volumes were recorded for each sample.
Tomato products and plasma analysis.
Carotenoid profiles of CS, RTS and V8 as well as plasma total carotenoid, vitamin E, and vitamin A concentrations were determined using the HPLC methodology of Epler et al. (18 ).
Plasma lycopene extraction.
An equal volume of ethanol containing 0.1% BHT was added to 150 µL of plasma. The sample was mixed using a vortex for 10 s before the addition of 750 µL of hexane/acetone (2:1) with 0.1% BHT. Samples were mixed again with the vortex. The sample was centrifuged at 5585 x g in a Corning-Costar 10MVSS Microcentrifuge (New York, NY) for 60 s and the lycopene-containing hexane layer was transferred to a glass vial. The plasma extraction procedure was performed multiple times on each sample to ensure the total removal of lycopene. The combined hexane layers were dried under nitrogen and analyzed according to the HPLC method conditions used to separate the lycopene isomers.
Plasma lycopene isomer chromatography.
A Waters 2690 separation instrument (Milford, MA) equipped with a Waters 996 Photodiode Array Detector was employed as part of the reversed-phase HPLC system used to separate plasma lycopene isomers. Separations were carried out using analytical (250 mm x 4.6 mm id) 3-µm polymeric C30 columns prepared at the National Institute of Standards and Technology (Gaithersburg, MD) according to Sander et al. (19 ). In-line guard columns packed with C30 stationary phase were used for all separations. Separation of lycopene isomers was performed at 1.0 mL/min using a linear gradient of 40–50% methyl-t-butyl ether in methanol/ammonium acetate (98:2) for 45 min.
Markers of oxidative stress.
Plasma EDTA-free LDL + VLDL were isolated via precipitation with MgCl2 and dextran sulfate (20
). The plasma LDL + VLDL cholesterol concentration was analyzed using a cholesterol kit from Sigma Diagnostics (St. Louis, MO) and normalized to 75 mg/L using a 2% PBS solution. Lipoprotein oxidation was initiated with 8 µmol/L CuSO4. The formation of conjugated dienes was monitored at 234 nm and 37°C over a 4-h period (21
). All measurements were performed in quartz crystal cuvettes. The lag period was determined by the time interval between the initiation with copper and the time at which the intersection of the line tangent to the slow propagation phase passed through the line tangent to the rapid propagation phase. The CV for the assay, including intra-assay and interassay factors, was <5%. Urine was collected for 12 h overnight and stored at -80°C before analysis. Concentrations of urinary 8-epi-PGF2 and 8-OH-2'-dG were measured using a competitive ELISA (Genox, Baltimore, MD).
Statistical analysis.
All statistical calculations were performed using software from StatView (SAS Institute, Cary, NC). Repeated-measures ANOVA or two-sample paired Student’s t test was employed for within group comparisons. ANOVA was used for between group comparisons with significance assessed using Fisher’s Protected Least Significant Difference test. P-values <0.05 were considered to be statistically significant. Values in the text are means ± SEM.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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92% of total lycopene in the all-trans form (Fig. 1A
). Higher amounts of ß-carotene, -carotene and lutein were present in V8 compared with other tomato products due to the presence of juice from other vegetables.
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-carotene (0.18 ± 0.02), ß-carotene (0.72 ± 0.11), cis-ß-carotene (0.089 ± 0.009), -cryptoxanthin (0.059 ± 0.004), ß-cryptoxanthin (0.30 ± 0.02), lutein (0.21 ± 0.02), retinol (1.94 ± 0.10), retinyl palmitate (0.046 ± 0.016), -tocopherol (39.43 ± 3.09), 
-tocopherol (3.32 ± 0.54) and 
-tocopherol (0.17 ± 0.03) did not change significantly due to product consumed or time of sampling. In addition, plasma concentrations (mmol/L) of triglycerides (1.53 ± 0.20) were not significantly altered throughout the study. The concentrations of plasma total cholesterol were not different among dietary groups but did decrease (mmol/L) from 5.23 ± 0.20 at baseline, to 4.98 ± 0.17 after the washout period, to 4.74 ± 0.17 after intervention (P < 0.05, baseline vs. intervention). Plasma total lycopene concentrations decreased 35% (P < 0.0001) for the 60 participants during the 7-d washout period (Table 2
).
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-carotene, ß-carotene and lutein (µmol/L) from 0.19 ± 0.06, 0.72 ± 0.17 and 0.20 ± 0.03 to 0.25 ± 0.04 (32%), 0.83 ± 0.13 (15%) and 0.22 ± 0.02 (10%), respectively, after dietary intervention with V8 reflect the elevated amounts of these carotenoids present in this product (Table 1)
. Of the carotenoids analyzed in plasma after 15 d of tomato product intervention, only plasma concentrations of lycopene and zeaxanthin were significantly increased. Zeaxanthin concentrations were not altered during the washout period, but increased from 0.10 ± 0.01 µmol/L after the washout period to 0.13 ± 0.01 µmol/L after intervention (30%, P < 0.01). Assessment of each group showed concentrations of plasma lycopene, after dietary intervention, to be significantly higher than levels during the washout period. Total lycopene concentrations increased for those consuming CS, RTS and V8 (compared with the washout period for each group) by 123% (P < 0.0001), 57% (P < 0.01), and 112% (P < 0.0001), respectively (Table 2) . On the basis of total lycopene consumption (mg/15 d), subjects who consumed CS, RTS or V8 had similar plasma total lycopene responses. (Table 3 ). This may indicate that these tomato products provided a similar bioavailable source of lycopene.
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To quantify changes of various cis-lycopene isomers throughout this study, isomer peaks were grouped according to elution order during HPLC analysis. Therefore, these lycopene isomers are grouped according to similar physicochemical characteristics (Fig. 1
B). The percentage of all-trans and total cis-lycopene (sum of cis-A, cis-B, cis-C, cis-D, cis-E and 5-cis-lycopene isomers) was altered after the washout period, but was not significantly changed due to tomato product consumption (Table 4
). As a percentage of plasma total lycopene isomers, all-trans-lycopene decreased from 44.4 ± 1.2 to 39.6 ± 1.2 (P < 0.0001), whereas total cis-lycopene increased from 55.6 ± 1.2 to 60.4 ± 1.2 (P < 0.0001) during the washout period. Although the percentage of total cis-lycopene increased significantly throughout the washout period, 
66% of these cis-isomers were in the 5-cis form. All-trans-lycopene and 5-cis-lycopene are the most abundant lycopene isomers present in human plasma. Analysis of individual cis-lycopene isomers showed an increase from 36.4 ± 0.8 to 41.6 ± 1.0 (P < 0.0001) and subsequent decrease to 33.7 ± 0.5 (P < 0.0001) in the percentage of plasma 5-cis-lycopene after the washout period and treatment phases, respectively. The percentage of 5-cis-lycopene was the only cis-lycopene isomer to change significantly during the washout period, suggesting a possible trans-lycopene isomer conversion to and/or biological preservation of 5-cis-lycopene. Dietary intervention with tomato products reduced the percentage of 5-cis-lycopene to baseline amounts and concomitantly raised the percentage of cis-B, cis-D and cis-E lycopene isomers (P < 0.05) above the baseline and/or the washout period levels (Table 4)
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after dietary consumption of tomato products.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Changes in plasma lycopene concentrations occur rapidly with variation in dietary intake. The consumption of a lycopene-free diet for 1 wk is sufficient to significantly lower plasma lycopene concentrations, supporting our earlier observations of a 10- to 14-d half-life for blood lycopene (29 ). Subsequent intervention with tomato products for 15 d significantly increased plasma lycopene levels.
Tomato and tomato product phytochemicals must be readily bioavailable to ensure maximum absorption. Bioavailability is defined as the fraction of an ingested nutrient that is accessible to the body through absorption for use in normal physiologic functions and for metabolic processes (30 ). A number of studies have evaluated the bioavailability of the carotenoid phytochemicals found in tomatoes and tomato products (10 ,29 ,31 –37 ). Increases in plasma lycopene and plasma responses per mg lycopene intake indicate that CS, RTS, and V8 provided a similar bioavailable source of lycopene. Lycopene uptake may be related to processing (12 ) and/or interactions among other phytochemicals present in these tomato products. However, it is important to note that increases in carotenoid intake do not necessarily produce similar increases in plasma uptake and response given that regulatory mechanisms are in place to limit mucosal cell uptake and/or transport in vivo (38 ).
Lycopene exists in multiple isomeric forms. The all-trans form of lycopene predominates in various tomato products. However, without consumption of lycopene-containing products for 1 wk, in vivo concentrations of cis-lycopene increased. A significant increase in the percentage of plasma 5-cis-lycopene was accompanied by a significant decrease in plasma all-trans-lycopene after the washout period. In the absence of a lycopene-containing diet, 5-cis-lycopene was the primary plasma lycopene isomer, suggesting a possible trans-lycopene isomer conversion to and/or biological preservation of 5-cis-lycopene. Additional research is required to identify the mechanism for conversion and to determine the physiologic importance of cis isomers of lycopene in vivo.
Research that supports the in vivo oxidation of LDL contributes to the hypothesis that dietary components may be important for LDL oxidative modification. Carotenoids such as lycopene are highly lipophilic and are commonly found within cell membranes and other lipid components (7 ,8 ). It is therefore thought that the ability of carotenoids to scavenge free radicals may be greatest in a lipophilic environment. The reduced susceptibility of lipoproteins from subjects fed a carotenoid-rich tomato product diet to ex vivo oxidative stress suggests a protective effect against oxidative stress in vivo.
These studies suggest that changes in tomato product intake can significantly modulate carotenoid levels in the bloodstream and alter the unique, yet complex, lycopene isomer patterns that exist in vivo. In addition, these studies imply that consumption of vegetable juice or tomato soup may provide protection from in vivo oxidative damage.
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FOOTNOTES |
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2 Supported by The National Cancer Institute-National Institutes of Health, The OSU Comprehensive Cancer Center, The Campbell Soup Company, and The Bremmer Foundation
4 Abbreviations used: CS, Campbell’s Condensed Tomato Soup; RTS, Campbell’s Ready to Serve Tomato Soup; V8, V8 Vegetable Juice; 8-OH-2'-dG, 8-hydroxy-2'-deoxyguanosine; 8-epi-PGF2, F(2)-isoprostane.
Manuscript received 6 September 2002. Initial review completed 14 October 2002. Revision accepted 3 December 2002.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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