Experimental Biology and Medicine 227:914-919 (2002)
© 2002 Society for Experimental Biology and Medicine
SYMPOSIA
Bioavailability of all-trans and cis-Isomers of Lycopene
Thomas W.-M. Boileau*,
Amy C. Boileau
and
John W. Erdman, Jr
,1
* Department of Human Nutrition and Food Management, The Ohio State University, Columbus, Ohio 43210;
Ross Products Division, Abbott Laboratories, Inc., Columbus, Ohio 43215; and
Division of Nutritional Sciences, University of Illinois, Urbana-Champaign, Illinois 61801
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Abstract
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Lycopene, the predominant carotenoid in tomatoes, is among the major carotenoids in serum and tissues of Americans. Although about 90% of the lycopene in dietary sources is found in the linear, all-trans conformation, human tissues contain mainly cis-isomers. Several research groups have suggested that cis-isomers of lycopene are better absorbed than the all-trans form because of the shorter length of the cis-isomer, the greater solubility of cis-isomers in mixed micelles, and/or as a result of the lower tendency of cis-isomers to aggregate. Work with ferrets, a species that absorbs carotenoids intact, has demonstrated that whereas a lycopene dose, stomach, and intestinal contents contained 6–18% cis-lycopene, the mesenteric lymph secretions contained 77%-cis isomers. The ferret studies support the hypotheses that cis-isomers are substantially more bioavailable then all-trans lycopene. In vitro studies suggest that cis-isomers are more soluble in bile acid micelles and may be preferentially incorporated into chylomicrons. The implications of these findings are not yet clear. Rats appear to accumulate lycopene in tissues within the ranges reported for humans, suggesting that they can be used to study effects of lycopene isomers on disease processes. Investigations are underway to determine whether there are biological differences between all-trans and various cis-isomers of lycopene regarding its antioxidant properties or other biological functions.
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Introduction
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Lycopene, the red pigment in tomatoes, is a C40, open-chain hydrocarbon carotenoid (Fig. 1
). Rotation of any of its 11 conjugated double bonds allows for the formation of a number of cis-geometrical isomers, which may have implications regarding the biological action of this carotenoid. Although the potential health-promoting effects of lycopene have been known since the late 1950s (1), much of the recent interest in lycopene bioavailability (BV) is a result of Giovannucci et al.’s publication (2) associating a significant, 35% reduction in prostate cancer risk in men in the upper quartile of tomato intake. Because tomatoes account for over 80% of the lycopene in American diets, a hypothesis was generated suggesting that lycopene was responsible for this reduction in cancer risk. To determine the biological plausibility that lycopene was the protective component of tomatoes, Clinton and colleagues (3) analyzed the lycopene content of the human prostate. Using newly developed C30 column HPLC technology, these investigators were the first to have demonstrated that indeed lycopene is found in the human prostate and, interestingly, it was found there as 15-18 cis geometrical isomers despite dietary lycopene sources being mainly all-trans lycopene. The possibility that specific isomers perform unique biological functions has led to the investigation of factors that determine the isomeric composition of both foods and tissues.
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Figure 1. Structures of common carotenoids found in human serum and tissues. Lycopene lacks the ß-ionone ring end structure of ßC and lutein and does not contain any hydroxyl groups. Cis-geometrical isomers are formed by the introduction of a cis double bond in the polyene chain. all-trans and 5-cis-lycopene are the two most common isomers found in human and animal tissues.
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Digestion and Absorption of Lycopene
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The matrix in which lycopene is found in foods appears to be an important determinant of its BV (4), and release of lycopene from this matrix is the first step in the absorptive process (5). The process of cooking usually makes lycopene more bioavailable by its release from the matrix into the lipid phase of the meal. Food processing also has been shown to increase BV. Tomato paste (6) and tomato puree (7) have been shown to be more bioavailable sources of lycopene than are uncooked food sources such as a raw tomato.The uptake of lycopene into intestinal mucosal cells is aided by the formation of bile acid micelles (Fig. 2). Because bile production is stimulated by dietary fat, consuming fat with a lycopene-containing meal increases the efficiency of absorption (8). Data from human studies in India have suggested that a minimum of 5–10 g of fat in a meal is required for the absorption of carotenoids (9). Conversely, a number of other investigators have found that carotenoids are absorbed from lower-fat meals. The amount of fat needed may depend upon the carotenoid in question (10). Regardless, it is generally accepted that the amount of fat (40% of calories) in a typical American diet is ample to provide for optimal lycopene absorption.Factors such as certain fibers (11–13), fat substitutes (14), plant sterols (15), and cholesterol lowering drugs (16) that interfere with the incorporation of lycopene into micelles can potentially decrease the efficiency by which this carotenoid is absorbed. Certain fat substitutes may also create a hydrophobic sink in the lumen of the small intestine, binding lycopene and thereby making it unavailable for uptake.The uptake of lycopene by the brush border membrane of the intestinal mucosal cell is thought to be by passive diffusion, and little is known about the intra-mucosal processing of lycopene (Fig. 2). It remains to be elucidated whether lycopene is transported intracellularly by specific proteins or whether it migrates in lipid droplets (17). Within the enterocyte, ß-carotene (ßC) and other pro-Vitamin A (VA) carotenoids such as 
-carotene and ß-cryptoxanthin can be metabolized to vitamin A or retinol by a specific enzyme, ßC-15,15‘ dioxygenase (18, 19). Unlike ßC, lycopene is not metabolized to VA but oxidative metabolites of lycopene have been found in human serum although little is known about the sites and mechanisms involved in their formation (20).Lycopene exits the mucosal cell in chylomicrons, which are secreted via the mesenteric lymph system into the blood (Fig. 2). Through the action of lipoprotein lipase on chylomicrons, lycopene and other carotenoids have the potential to be taken up passively by various tissues, including adrenals, kidney, adipose, spleen, lung, and reproductive organs before clearance of chylomicron remnants by the liver via the chylomicron receptor. Carotenoids can accumulate in the liver or can be repackaged into very low-density lipoprotein (VLDL) and sent back into the blood. Uptake of carotenoids into tissues from VLDL and LDL is thought to occur via the LDL receptor, and the tissues with the highest concentrations of carotenoids (liver, adrenal, testes) tend to have high LDL receptor activity. Lycopene is a predominant carotenoid in the human liver, adrenals, adipose tissue, testes, and prostate (3, 21–24).
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Figure 2. Critical events in the intestinal uptake of lycopene isomers. Free lycopene isomers from dietary sources are incorporated into mixed micelles, taken up by the mucosal brush border membrane, and packaged into chylomicrons for secretion into lymph tissue. Very little is known (?) about the intra-mucosal transport and metabolism of lycopene isomers and mechanisms by which they are incorporated into chylomicrons.
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Sources of cis-Lycopene Isomers
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Lycopene Isomers in Foods.
Although lycopene exists in human and animal tissues mainly as cis-isomers, lycopene is found in most food sources primarily as the all-trans isomer (80–97% all-trans; Table I). As noted above, heated and processed food products contain more BV sources of lycopene than uncooked sources. Clearly the release of lycopene from the matrix is one important factor modulating lycopene BV, but it has also been suggested that formation of cis-isomers also increases BV. Several studies have investigated the possibility that food processing and cooking results in the isomerization of all-trans lycopene to cis-isomers. Nguyen and Schwartz (25) demonstrated that, unlike ßC, little isomerization of all-trans lycopene to cis-lycopene was noted with thermal processing (Table II). Similarly, Schierle et al. (26) found that heating tomato paste for up to 3 hr in either water or oil resulted in only small increases in cis-isomers. Even dehydration, which is performed at high heat over relatively long periods of time, only results in small increases in cis-lycopene isomers in tomato products (Table II). These studies suggest that thermal treatment and processing result in only small increases (<10%) in cis-lycopene content of foods and it is clear that other physiological processes are responsible for the large differences in cis: trans ratios observed between foods and tissues.
Lycopene isomerization in the stomach.
The hypothesis that lycopene is isomerized in the stomach as a result of low pH has recently been investigated. Re et al. (27) performed in vitro incubations with lycopene from commercially available capsules (The Boots Company, Nottingham, UK) or tomato puree and with either a commercially available simulated gastric juice (Sigma-Aldrich Chemical, St. Louis, MO) or human gastric juice obtained at endoscopy. Their results indicated that the percent cis-isomers in both lycopene sources increased after incubation with gastric juices, but the capsules increased more than the puree suggesting a stabilizing effect of food matrix (Table III).The development of animal models whose absorption of carotenoids mimics that of humans has aided in understanding factors that affect BV of lycopene isomers (28). Of the laboratory animals that appear to absorb carotenoids similarly to humans, gerbils and ferrets are the best characterized and most frequently studied.Our in vivo studies in ferrets support modest gastric isomerization of lycopene. In ferrets orally dosed with lycopene, the percentage of lycopene cis-isomers increased from 6.2% in stomach contents to 17.5% in the intestinal contents (29; Fig. 3). Thus it appears that both thermal processing and exposure to the low pH of the stomach result in small increases in cis-lycopene isomers, but this isomerization cannot explain the observation that intestinal mucosal cells contained 58.8% cis-lycopene.
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Table III. Influence of Gastric Juices on Isomerization of Lycopene From Capsules or Tomato Puree After 1-min or 3-hr Incubations
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Figure 3. Percentage of lycopene as cis-isomers in ferret tissues after an oral lycopene dose (40 mg of lycopene/kg body weight as LycoredTM mixed in soybean oil). Ferrets were killed after a 2-hr lymph collection and all digestive and tissue fractions were analyzed by HPLC with separations performed on a C30 column.
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Preferential Absorption of Lycopene Isomers.
Stahl and Sies were among the first to suggest that cis-lycopene isomers are preferentially absorbed compared with the all-trans isomer. They observed that despite tomato juice dose having only about 20% cis-isomers, the serum was composed of about 50% cis-isomers after consumption of tomato juice by healthy volunteers (8). Using HPLC with C18 column separations these investigators identified four isomers of lycopene, with all-trans being the predominant, but the three other cis isomers (9-, 13-, 15-cis) accounting for the most lycopene.More recent studies conducted in our laboratory (3) and other laboratories (6, 26, 30) have supported the hypothesis that cis-lycopene isomers preferentially accumulate in tissues and serum. Using HPLC and newly developed C30 column technology, our laboratory has demonstrated that lycopene exists in human prostate and serum in as many as 18 different isomeric forms. The most abundant isomeric forms in human tissue and blood are the all-trans and 5-cis isomers, with the sum of cis-isomers accounting for the majority (58–88%) of the total lycopene (Table IV).Our laboratory (29) dosed ferrets orally with lycopene and collected small intestine, lymph, and several tissues to determine cis:trans-isomer ratios. It was observed that despite the dose containing only 9% cis-isomers, mucosa (58.8%), lymph (77.4%), blood (52%), and tissues contained significantly more cis-lycopene isomers than stomach (6%) or intestinal content (17.5%; Fig. 3
). Because the mucosal cells contained 41% more cis-lycopene isomers than intestinal contents, we further examined the uptake of lycopene isomers by bile acid micelles in vitro. Indeed, results suggested that cis-lycopene isomers are more readily taken up by micelles making them more easily absorbed (Table V). These data support the hypothesis that cis-lycopene isomers are more efficiently taken up into the mucosal cells and absorbed into lymph than all-trans lycopene.The mechanisms responsible for the selective incorporation of cis-isomers into micelles are poorly understood. Because the introduction of one or more cis double bonds into a lycopene molecule reduces its length it has been hypothesized that isomerization allows the molecules to ‘‘fit’’ into micelles with greater ease. Alternatively, it has been suggested that linear all-trans isomers may more readily aggregate within the intestine and form crystals, greatly reducing their uptake by micelles (31). The recent development of an in vitro model to study the cellular and physiochemical events involved in carotenoid digestion and intestinal uptake may aid in the further understanding of the BV of cis-lycopene isomers (32).
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Accumulation of Lycopene Isomers in Rodent Tissues
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Few studies have examined the tissue distribution of lycopene in laboratory animals commonly used to study disease processes. Mathews-Roth et al. (33) have shown the liver to be the major site of lycopene accumulation in the rat after a single dose of 14C lycopene. Zhao and co-workers (34) demonstrated in a dose–response feeding trial that lycopene accumulated in liver and extrahepatic tissues of male and female F344 rats in a dose–response manner when fed in the diet for 10 weeks. Liver was found to be the major site of lycopene accumulation, but lung, prostate, mammary glands and serum were also found to accumulate significant amounts of lycopene. Other laboratories have documented similar lycopene tissue distributions (39).Our laboratory further demonstrated that rats could be used as a model to study biological actions of lycopene isomers (35). Male F344 rats fed lycopene-containing diets for 8 weeks achieved lycopene tissue concentrations and isomer patterns similar to those observed for humans (Tables IV & VI). We have also demonstrated that castrated rats accumulate more total lycopene and more lycopene as cis-isomers than intact rats despite eating less total lycopene (Table VII). Additionally, the percentage of lycopene as cis-isomers increased as dietary lycopene concentrations increased (Table VII). These results suggest that hormonal and other physiological factors may also regulate the isomeric ratio of lycopene in tissues.It appears that the rat may be a useful model to study lycopene metabolism and mechanisms by which lycopene modifies biological processes such as cancer. However, since rats inefficiently absorb lycopene, relatively high dietary lycopene concentrations are needed to achieve tissue concentrations similar to those observed in humans. The rat is not the preferred model to study lycopene bioavailability from foods. The gerbil or ferret would be a better model for this type of study (28).
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Table VII. Androgen Status and Dietary Lycopene Concentration Affect Hepatic Lycopene Concentrations and Isomer Patterns in Male F344 Rats Fed Lycopene for 8 Weeksa,b
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Conclusions
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Although the predominant form of lycopene in foods is all-trans, human blood and tissues contain mainly cis-isomers. The potential role for specific lycopene cis-isomers in disease processes has stimulated interest in their sites of formation and BV. It appears that food processing and thermal treatment of foods results in only modest increases in the percentage of cis-lycopene isomers. Studies in humans and animal models support a hypothesis that cis-lycopene isomers are preferentially absorbed. In vitro studies indicate that cis-isomers are more easily taken up by mixed micelles in the intestine and hence are more bioavailable. Further work is necessary to determine other factors influencing the BV of lycopene isomers and their importance in health and disease.
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Footnotes
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1 To whom requests for reprints should be addressed at 457 Bevier Hall 905 S. Goodwin Ave. Urbana, IL. E-mail: jwerdman{at}uiuc.edu 
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Top
Abstract
Introduction
