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Human Nutrition and Metabolism

Enrichment of Tomato Paste with 6% Tomato Peel Increases Lycopene and ß-Carotene Bioavailability in Men¹

Emmanuelle Reboul^*, Patrick Borel^*, Céline Mikail, Lydia Abou, Monique Charbonnier^*, Catherine Caris-Veyrat^**, Pascale Goupy^**, Henri Portugal, Denis Lairon^* and Marie-Josèphe Amiot^*,2

^* INSERM, U476 "Nutrition Humaine et lipides," INRA, UMR 1260, Univ Méditerranée Aix-Marseille 2; Faculté de Médecine; and IPHM, Marseille F-13385, France; Service de Chimie Analytique, Faculté de Pharmacie, Marseille F-13385, France; and ^** INRA, UMR A408 "Sécurité et Qualité des Produits d’Origine Végétale," Domaine Saint Paul, Avignon F-84914, France

²To whom correspondence should be addressed. E-mail: Marie-Jo.Amiot-Carlin{at}medecine.univ-mrs.fr.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
A high intake of tomato products is associated with a lower incidence of upper aerodigestive tract and prostate cancers. This beneficial effect might be explained by a higher intake of carotenoids such as lycopene and/or ß-carotene. Because tomato peels, usually eliminated during tomato processing, are a valuable source of these carotenoids, we designed a study to examine whether a tomato paste enriched in tomato peels (ETP, 6% peel) increases the absorption of these carotenoids compared to a classically made tomato paste (CTP). Carotenoid bioaccessibility was evaluated using an in vitro digestion model by measuring the amount of carotenoids transferred from the pastes to micelles. Carotenoid absorption by human intestinal cells (Caco-2) was evaluated after the addition of carotenoid-rich micelles (obtained from the in vitro digestion of the 2 pastes). Carotenoid bioavailability in humans was assessed by measuring chylomicron carotenoid responses in a postprandial experiment in which 8 healthy men consumed 2 meals containing either the ETP or the CTP. ETP contained 47.6 mg lycopene (58% more than CTP) and 1.75 mg ß-carotene (99% more than CTP) per 100 g of paste. In micelles, 30% more lycopene and 81% more ß-carotene were recovered after ETP than after CTP in vitro digestion. The amount of carotenoids absorbed by Caco-2 cells was 75% greater (P 0.05) for lycopene and 41% greater (P 0.05) for ß-carotene after the addition of micelles from ETP than from CTP. After ETP intake the chylomicron ß-carotene response was 74% greater than after CTP intake, and the lycopene response tended to be greater (34.1%, P = 0.093). Peel enrichment of tomato paste with tomato peel is an interesting option for increasing lycopene and ß-carotene intakes.

KEY WORDS: • tomatoes • peels • lycopene • ß-carotene • bioavailability

Epidemiological and clinical studies have suggested health benefits of tomatoes and tomato-based food products (1–3). Tomatoes contain a large variety of micronutrients (ß-carotene as provitamin A, vitamin C, folate, and potassium) and microconstituents, including lycopene and polyphenols that are considered potent antioxidants (4–6). Because of its highly conjugated structure, lycopene, the main carotenoid present in tomatoes, can lower oxidative stress. Its ability to quench singlet oxygen was shown to be twice as high as that of ß-carotene (7,8). In addition, lycopene could act through nonoxidative mechanisms such as gene regulation (9), gap-junction communication (10,11), or immune function (12). All these biological activities greatly depend on the bioavaibility of lycopene. Previous studies reported that the bioavailability of lycopene is markedly modified by processing and chemical environment, especially lipids and fibers (13–16). During the processing of tomatoes into pastes or sauces, a large proportion of lycopene, as well as other antioxidants, is removed by discarding peels. Peels are particularly rich in carotenoids and phenolic antioxidants, but very little information is available regarding their bioavailability from tomato peels.

The aim of the present study was thus to evaluate the bioavailability of lycopene from tomato peels in order to enrich the carotenoid content of tomato paste. The bioavailability was determined using 3 complementary and acknowledged models: 1) an in vitro digestion model (17) to evaluate bioaccessibility (bioaccessibility of a fat-soluble nutrient is the proportion of this micronutrient extracted from food matrix and solubilized in mixed micelles; it is assumed that solubilization into mixed micelles is one of the most important steps of the absorption process); 2) the human Caco-2 (TC-7 clone) intestinal cell line (18); and 3) postprandial chylomicron responses in humans (19).

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Chemicals. All-trans lycopene (95.5% pure), ß-carotene (95.6% pure), and echinenone (98% pure), used as internal standard for HPLC analysis, were kindly provided by F. Hoffmann-La Roche. DMEM containing 4.5 g/L glucose and trypsin-EDTA (500 and 200 mg/L, respectively) was purchased from BioWhittaker. Fetal bovine serum (FBS)³ was purchased from Biomedia, and nonessential amino acids and penicillin/streptomycin were purchased from Gibco BRL. Pepsin, porcine pancreatin, porcine bile extract, and pyrogallol were purchased from Sigma-Aldrich. Foods were purchased from a local supermarket.

    Tomato pastes. Tomatoes (2 equivalent samples of 150 kg, a mixture of varieties for processing) were donated by Sonito. Upon receipt, tomatoes were washed before being processed. Classical tomato paste was prepared from whole fruits using a pilot line at CTCPA equipped with Bertuzzi materials: hammer crusher, sieve (Bertuzzi, 0.8 mm), and concentrator. For enriched tomato paste, the first step was a steam peeling of tomatoes. Tomato peels were centrifuged (3000 x g, 15 min) and finely ground with an Urshel crusher (Comitrol type equipped with a microcutting head giving particle size around 1 µm). Crushed peels were incorporated into classical tomato puree. The 2 purees (classical and enriched) were concentrated to 15° Brix (checked by refractometry) to give a classical tomato paste (CTP) and an enriched tomato paste (ETP), respectively. Glass containers (200 mL) were filled with hot tomato paste and then flash-pasteurized at 85°C for 1 min. Carotenoid content was determined in 6 individual glass containers. The CV was 3%.

    Carotenoid bioaccessibility from the tomato pastes. Lycopene and ß-carotene bioavailability, i.e., the percentage of these microconstituents transferred into micelles, was estimated using an in vitro model (17). Meal components (6.7 g boiled potato puree, 1.2 g fried 10% fat beef meat, 0.2 g olive oil, and 2 g tomato paste) were mixed with 32 mL 0.9% NaCl containing 12.6 g/L pyrogallol as an antioxidant. The mixture was homogenized for 10 min at 37°C in a shaking water bath. To mimic the gastric step, the pH was adjusted to 4 ± 0.02 with about 500 µL of 1 mol/L HCl, and then 2 mL of porcine pepsin (40 g/L in 0.1 mol/L HCl) was added. The homogenate was incubated at 37°C in a shaking water bath for 30 min. To mimic the intestinal step, the pH of the partially digested mixture was raised to 6 ± 0.02 by adding around 800 µL of 0.9 mol/L sodium bicarbonate, pH 6.0. Then a mixture of porcine bile extract and pancreatin (9 mL containing 2 g/L pancreatin and 12 g/L bile extract in 0.1 mol/L trisodium citrate, pH 6.0) and 4 mL bile extract at 100 g/L were added. Samples were incubated in a shaking water bath at 37°C for 30 min to complete the digestion process. Micelles were separated from oil droplets and food particles by ultracentrifugation (30,000 x g for 18 h at 10°C using a Kontron TST 41–14 SW rotor). The aqueous fraction was collected from the centrifuge tube using a needle attached to a 10-mL syringe. Then it was filtered through a 0.22-µm filter (Millipore). Aliquots were stored at –80°C under nitrogen until analysis.

    Carotenoid absorption by intestinal cells. Caco-2, clone TC-7 cells were a gift from Dr. Monique Roussey (U178 INSERM). Cells, passages 60–70, were grown in 25-cm² flasks (TTP) in the presence of DMEM supplemented with 20% heat-inactivated FBS, 1% nonessential amino acids, and 1% antibiotics (complete medium). Cells were incubated at 37°C in a humidified atmosphere of air/carbon dioxide (90:10, v:v) and the medium was changed every 48 h. Monolayers were subcultured with a 7-d passage frequency when they reached a confluence of about 80% by treatment with 0.25% trypsin-EDTA. For each experiment, cells were seeded at a density of 1 x 10⁶ cells/well and grown on transwells (6-well plate, 24-mm diameter, 1-µm pore size polycarbonate membrane, Becton-Dickinson). The medium used in apical and basolateral chambers was the complete medium. Media were changed every day for 28 d to obtain confluent, differentiated cell monolayers (20). One day before each experiment, the medium used in apical and basolateral chambers was DMEM without phenol red supplemented with 20% heat-inactivated lipid-free FBS, 1% nonessential amino acids, and 1% antibiotics. Before each experiment, the integrity of the cell monolayers was checked by measuring trans-epithelial electrical resistance with a voltohmmeter equipped with a chopstick electrode (Millicell ERS, Millipore). To measure carotenoid absorption by Caco-2 cells, carotenoid-rich micelles coming from the in vitro digestion of the 2 pastes (control and enriched) were used at 1/5 dilution. At the beginning of each experiment, cell monolayers were washed twice with 1 mL PBS on the apical side and 2 mL on the basolateral side. The apical side of the cell monolayers received 1.5 mL micelles while the basolateral side received 2 mL FBS-free medium. Cell monolayers were incubated at 37°C for 3 or 8 h. After the incubation period, media from each side of the membrane were harvested. Cell monolayers were washed twice with 1 mL PBS containing 5 mmol/L taurocholate to eliminate adsorbed carotenoids, scraped, and collected in 100 µL PBS. Absorbed carotenoids were estimated as carotenoids in scraped cells and in the basolateral chambers of the transwells. All samples were stored at –80°C under nitrogen with 0.5% pyrogallol as a protective antioxidant before carotenoids extraction and HPLC analysis. Aliquots of cell samples without pyrogallol were used to estimate protein concentrations with a bicinchoninic acid kit (BCA kit, Pierce). Absorbed carotenoids were expressed as picomoles per milligram of protein.

    Carotenoid bioavailability in healthy subjects. Eight nonsmoking healthy men, 20–40 y of age, with BMI less than 24 kg/m² were selected. Serum glucose, triglycerides, and cholesterol were determined by enzymatic procedures (21–23). The subjects did not use medication and had no history of gastrointestinal (GI) disease or lipid metabolic disorders. Subjects’ characteristics and their nutrient and carotenoid daily intake are reported in Table 1. The daily intake was assessed by a 5-d food diary and analyzed using the Score-AN software (set by Avantage Nutrition). The Souci database was used for nutrients (24) and the USDA website for carotenoids (25). The study was approved by the regional committee on human experimentation of Marseilles. The objectives and requirements were fully explained to the participants and informed written consent was obtained for each subject. Each subject was asked to consume a light meal on the evening before the experiment and to fast overnight. In the morning, an intravenous catheter was inserted into 1 forearm of each subject. An individual baseline blood sample was obtained and then they consumed the control CTP meal or the ETP meal. Each subject received each meal in a random order with a 1-mo interval (cross-over design with a 1-mo wash-out period). Meal compositions are given Table 2. Additional blood samples were drawn 1, 2, 3, 4, 6, and 8 h following the beginning of the meal. Blood samples were stored at 4°C and rapidly centrifuged (610 x g, 4°C, 10 min) to isolate plasma. Small and large chylomicrons were isolated according to Luchoomun and Hussain (26). Triglycerides were measured in chylomicrons using the PAP 150 Biomérieux kit. Carotenoids were measured in chylomicrons according to the following method. Lycopene and ß-carotene were extracted from 500- to 800-µL aliquots in the dark. The carotenoid echinenone was used as an internal standard and was added to the samples in 1 vol of ethanol. The mixture was extracted twice with 2 vol of hexane. The hexanic phases obtained after centrifugation (500 x g, 5 min, room temperature) were evaporated completely under nitrogen; the residue was redissolved in 200 µL acetonitrile/dichloromethane (50:50, v:v). A reverse-phase isocratic HPLC method was performed according to Lyan et al. (27) using a 250 x 4.6 mm i.d. RP C₁₈, 5 µm Zorbax column (Interchim). The mobile phase was 70% acetonitrile, 20% dichloromethane, and 10% methanol. The flow rate was 1.5 mL/min and the column was thermostated at 30°C. The HPLC system was composed of a Waters 2690 separation module and a Waters 2996 photodiode array detector (Waters SA). Carotenoids were detected at 460 nm and identified according to their retention time and their absorption spectra (between 300 and 500 nm) compared to pure standards. Quantification was performed using Waters Millenium 32 software (version 3.05.01) comparing peak area with standard reference curves. All solvents were HPLC grade from SDS.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
ETP had 58% more lycopene and 99% more ß-carotene than CTP. The concentration of lycopene measured in the micelle fraction tended to be higher for ETP than for CTP in the in vitro digestion system: 2.44 ± 0.56 vs. 1.88 ± 0.13 µmol/L, respectively (P = 0.158). Similarly, the micelle ß-carotene concentration was higher after ETP than after CTP digestion: 3.56 ± 0.26 vs. 1.96 ± 0.180 µmol/L (P = 0.0003).

The lycopene absorbed by human intestinal cells was also significantly higher after the addition of micelles from ETP than from CTP at 6 h: 20.1 ± 5.0 vs. 4.3 ± 0.7 pmol/mg protein and at 8 h: 15.3 ± 2.4 vs. 4.3 ± 0.7 pmol/mg protein (Fig. 1A). Similarly, ß-carotene concentration was significantly higher after the addition of ETP than CTP micelles. Values at 3 h were 16.1 ± 4.5 vs. traces (<0.0 ± 0.0) pmol/mg protein and at 8 h, 24.0 ± 2.2 vs. 20.4 ± 1.4 pmol/mg protein (Fig. 1B).

View larger version (16K): [in this window] [in a new window]   FIGURE 1 Effects of micellar carotinoid concentration (CTP or ETP micelles) on lycopene (A) and ß-carotene (B) absorption by differentiated Caco-2 TC-7 cell monolayers. The apical side received 1.5 mL ETP or CTP micelles (1/5 dilution), and the basolateral side received 2 mL FBS-free medium. Data are means ± SEM, n = 4. *Different from CTP micelles at that time, P 0.05.

View larger version (15K): [in this window] [in a new window]   FIGURE 2 Plasma chylomicron lycopene (A) and ß-carotene (B) response in healthy men after CTP or ETP meal intake. Data ( from fasting values) are means ± SEM, n = 8.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

For lycopene, ratios for the 2 tomato pastes (ETP vs. CTP), the bioaccessibility values (in vitro digestion model), and bioavailability data (human study) were 1.6, 1.3, and 1.5, respectively. These close ratios show that (i) peel lycopene bioavailability (and bioaccessibility) is similar to flesh lycopene bioavailability and (ii) constituents present in peel, such as antioxidant polyphenols, do not alter the bioavailability of lycopene.

For ß-carotene, the ratios were 2 for the tomato paste contents, 1.8 for bioaccessibility, and 3.8 for bioavailability. The comparable tomato paste content and bioaccessibility ratios suggested that the peel ß-carotene bioaccessibility is similar to flesh ß-carotene bioaccessibility and that peel matrix does not affect ß-carotene bioavailability as described above for lycopene. However, the fact that the bioavailability ratio obtained in the human study was about 100% higher than the ratios for tomato paste contents and bioaccessibility was more difficult to explain. We hypothesize that a factor present in tomato peels could lower the ß-carotene conversion to vitamin A in chylomicrons. Lycopene, like other carotenoids, in minor quantities could act as a competitive inhibitor of dioxygenase that catalyzes the central cleavage of ß-carotene, as was previously shown for canthaxanthin in rat intestine by Grolier et al. (32). Additional experiments are required to confirm and explain this result.

In an absorption study carried out on intestinal cells, experiments using ETP showed a higher absorption of carotenoids than experiments using CTP. The calculated ratios were higher than those for pastes, bioaccessibility, and bioavailability, suggesting the chemical environment may affect the absorption of carotenoids by enterocytes.

The present study provided interesting new data on the bioavailability of tomato paste carotenoids. In all experiments, the amount of ß-carotene absorbed was higher than expected. Indeed, although the lycopene to ß-carotene ratio was close to 30 in tomato pastes, the concentration of ß-carotene in micelles was close to that of lycopene (lycopene:ß-carotene ratio was around 0.8). The carotenoid concentrations were also similar in Caco-2 cells. In chylomicrons, the ß-carotene response was only 73% lower (after CTP intake) and 89% lower (after ETP intake) than the lycopene response. This finding indicates that ß-carotene from tomato paste is much more bioavailable than lycopene. This is in agreement with a recent human study (33), showing that the plasma ß-carotene response to 96 g/d tomato puree for 3 wk was higher than the corresponding plasma lycopene response, although the tomato puree used contained about 10 times more lycopene than ß-carotene. The data obtained herein suggest that the higher bioavailability of ß-carotene in tomato puree is due to its higher bioaccessibility compared to lycopene. Such a higher bioaccessibility could be due to a better solubility of ß-carotene into micelles, to the different localization of carotenoids in tomato cells, or to different physical states of the carotenoids within the tomato puree matrix. These data agree with the correlation recently observed by Gomez-Aracena et al. (34) between tomato intake and plasma ß-carotene. Tomato-derived food products could be considered a good source of ß-carotene in terms of bioavailability. It was suggested that the lycopene response was not dose-dependent, especially for high amounts (35). Our results partially confirmed this observation because the amount of lycopene in chylomicrons was not as high as expected compared to the results obtained in previous studies using lower intakes (19,33). In our study, the dose-dependent increase of lycopene in chylomicrons after ETP intake compared to CTP, even after high intakes, could be due to the presence of some factors in tomato peels that increase lycopene absorption, as described for ß-carotene.

Finally, in the present investigation, postprandial carotenoid response differed among subjects. Such an interindividual variability was previously observed for ß-carotene (36,37). In addition, some subjects in the present study were used to consuming a Mediterrean diet high in tomato food products, as reported in Table 1 (a subject consumed close to 5 mg lycopene/d). It is reasonable to think that for non-Mediterranean subjects a higher biovailability of carotenoids (lycopene and ß-carotene) would be confirmed with more realistic quantities of tomato pastes.

In conclusion, bioavailability of carotenoids from finely crushed peels homogenized in tomato paste appeared to be similar to lycopene from the tomato flesh. Such a peel enrichment of tomato products would be a means to increase the nutritional value of tomato pastes and to enhance the intake of carotenoids.

	ACKNOWLEDGMENTS

 
The authors thank Stéphane Georgé and Gérard Bartholin (CTCPA) for their help in tomato processing and Christine Juhel (Avantage Nutrition) for her help in the human study.

	FOOTNOTES

 
¹ Supported by the Ministère de la Recherche et de la Technologie (AQS 00 P04) and the Regional Council of Provence Alpes Cote d’Azur.

³ Abbreviations used: CTP, classical tomato paste; ETP, enriched tomato paste; FBS, fetal bovine serum.

Manuscript received 27 October 2004. Initial review completed 24 November 2004. Revision accepted 15 January 2005.

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TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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