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Home , Carotene, Fucoxanthin, Lutein, Lycopene

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FF:&TL RE : From to Humans J.K. Collins and P. Perkins-Veazie U.S. Department of Agriculture, Agriculture Research Service, South Central Agriculture Research Laboratory, Lane, OK 74555 W. Roberts Wes Watkins Agricultural Research Center, Lane, OK 74555

Additional ijulev non/s. varotenoid, , , bitter melon, red , gac, epidemiology, cancer Abstract. Lycopene is a that imparts a red or red— color to some and . This has been extensivel y studied over the last 10 y ears because of its potent activit and medical evidence that dietary intake can reduce the incidence of and some cancers. The PUFPOSC of this rev ies is to provide researchers in the areas of horticulture and food science a current summary of available information on lycopene in plants, stabilization and extraction, and potential health benefits as delineated in current medical studies.

Lycopene Synthesis phytoenc (C40 molecule) from head-to-head and tomatoes (Davis et al., 2003). In tomato- condensation (Jones and Porter. 1999: Sand- based foods, 79% to 91% of the lycopene is in Lycopene is one of 600 mann, 2001) (Fig. 1). is converted the trans form and 95/a to 2 l% is in the cis form naturally found in plants, bacteria, fun gi, and into zeta by phytoene desaturase and (Clinton et al., 1996). In red watermelon, Trans (Jones and Porter. 1999). Like other lycopene is converted from zeta carotene by lycopene predominates at 92% to 95% of total carotenoids such as and beta-carotene, zeta carotene desaturase (Sandmann. 2001). lycopene and is the primary carotenoid (Per- lycopene has dual roles in humans and plants as From lycopene, the pathway is split and kins-Veazie et al., 2001). Lycopene cis and a free-radical scavenger (Jones and Porter, cyclization of lycopene call al one or Trans composition of other foods has not been 1999). In plants, lycopene confers antioxidant both ends to form monocyclie (delta-carotene well characterized. protection for photosystem events and appears and gamma-carotene) and dicyclic com- in during npening, and is specu- pounds (alpha carotene and beta carotene) Genetic Effects lated to improve attraction, consumption, and (Fig. 1). Although the general synthesis of dissemination by herbivores (Homero- carotenoids has been extensively researched, Tomato germplasm (red fnut) varies from Mcndez and Britton. 2002: Ronen et al., the regulatory enzymes involved in control- 10 to 150 mg/kg lycopene (Arias et al.. 2000: 1999). In humans, lycopene is thought to act ling carotenoid synthesis in plants are not Dumas et al.. 2003: Raffo Cl al., 2006: Thomp- by scavenging singlet oxygen and peroxy completely understood (Fraser et al., 2001). son et al., 2000). Red-fleshed watermelon radicals and deactivating excited molecules or Structurally, lycopene is an unsaturated hy- appears to have a carotenoid synthesis path- DNA chain-breaking agents (Stahl et al., 1997). drocarbon with all polyene chain way similar to tomato (Tadmor et al., 2004), Carotenoids can be synthesized in bacteria, structure made up of 40 carbons and 56 and waternwlon gennplasm ranges in lyco- algae, fungi, and green plants, and currently hydrogen molecules (Ronen et al.. 1999). It pene content from 30 to 120 mg/kg (Perkins- two synthesis pathways have been found has II conjugated and two nonconjugated Veazie et al., 2001; Perkins-Veazie et al., (Sandmann. 2001). In fungi, carotenoids are double bonds and lacks the beta-iononc ring 2006). Both orange tomatoes and orange derived through the (MVA) structure that can be enzymatically converted contain small amounts of lyco- pathway (Sandmann, 2001). In plants, the into A (Ych and Hu. 2000). pene (<5 mg/kg), but none is found in yellow independent pathways MVA and methylery- types. roots call accumulate lyeo- thritol phosphate (MEP) synthesize the five- Sources of Lycopene pene as well as alpha and beta-carotene carbon units isopentenyl diphosphate (IPP) (Horvitz et al., 2004: Surles et al.. 2004). and its isomer, diethylallyl diphosphate Common plant sources of lycopene in the The genes responsible for carotenoid synthesis (DMAPP), needed as precursors for carote- Western diet are tomatoes (Licopersicon e.scu- in are still being identified with an noids (Botella-Pavia et al., 2004). It is thought lentuni), processed tomato products, water- eventual goal to develop carrot germplasm that plant carotenoids synthesized in chioro- melon (Citrullus lanatus). Brazilian containing >100 mg/kg (Santos and Simon, plasts and chromoplasts arise primarily from (Psidium guajava), and red grapefruit (Citrus 2002: Phillip Simon, personal communica- the MEP pathway (Botella-Pavia et al., 2004). paradi.ri) (Tables I and 2) (Holden et al.. 1999). tion). Red grapefruit, thought to originate from Three molecules of IPP and one of DMAPP Other plant sources not normally consumed in somatic mutations that occurred in vegetative plus the presence of geranylgernanyl diphos- the United States but now being considered as buds or branches of pale -fruited vari- phate synthase forms geranylgeranyl diphos- a source for lycopene use include eties (Corazza-Nunes et al., 2002), contains 2 phate (GGPP), a molecule used in several autumn (Eaeleagnu.s angusti,lolia), red to 22 mg/kg lycopene, depending on variety pathways, including carotenoids. Two mole- carrots (Daucus .sp.). rose hips (Rosaceae sp.), and production environment (Patil et al., 2004; cules of GGPP (2 C20 molecules) form bitter melon, and gac (Mormidica sp.) USDA, 2005a). (Fordham et al., 2001; Ishida et al., 2004: Plant-breeding programs have used both Nguyen and Schwartz, 1998; Yen et al., traditional and molecular methods to enhance Received for publication 3 Mar. 2006. Accepted 1981) (Table I). Some spices and condiments levels of lycopene and other carotenoids in for publication 2 Apr. 2006. Mention of trade names such as salad dressings that contain tomato fruits. More breeding research has been con- or commercial products in this article is solely for the sauce also provide minute amounts of lycopene ducted with tomato, probably because the visible purpose of providing specific information and does (Table 2). Lycopene occurs as cis or trans color changes that occur during fruit ripening not imply recommendation or endorsement by the isomers and is readily identified in foods using help pinpoint changes in carotenoid U.S. Department of Agriculture. All programs and high-performance liquid and enzymes (Ronen et al., 2000). Single-gene services of the U.S. Department of Agriculture are (Khachik et al., 1995). Guides for caroten- color mutants of tomatoes were first documented offered on a nondiscriminatory basis without regard to oid analysis in foods, including extraction and in the 1940s, resulting from crosses with a nor- race, color, national origin, religion, sex, age, marital status, or handicap. The article cited was prepared by detection methodologies, have been published mal tomato (Ltcopersicon esculentiun, a USDA employee as part of his or her official duties. (Craft, 2001; Fish et al., 2002; Rodriguez- Mill) and a wild species (Licopersicon esculen- To whom reprint requests should be addressed: Amaya, 2001), and rapid spectrophotometric lion, Humb) to produce a high beta-carotene- e-mail jcollins-usdaifIane-ag.org. methods have been developed for watermelon containing orange fruit (Ronen et al., 2000;

HORTSCiENCE VOL. 41(5) AUGLFST 2006 1135

yellow shoulder in processing tomatoes GGPP grown in California (Hartz et al., 1999), Psy implying a role for in lycopene

Phytoene synthesis or degradation. Hydroponically Pd., I grown tomatoes responded to increased rates cm CRTISO of K and P with increased lycopene (20% to ç.Carexe ZdS 30%) (Dumas et al., 2003: Trudel and Ozbun, 1971). Fresh market tomatoes, watermelon, / Lcy-e (CelL-c) Lcy-b (CelL-b) \ \ CycB copene (7Z.9Z,77,97- Lycopene) and red grapefruit had little or no increase in lycopene with increased soil K rates in field CycB Lcy-b (CelL-b) Lcy.b (CelL-b) J, experiments (Fontes et al., 2000: Patil and Alva, 2002; Perkins-Veazie and Roberts, CuR-b 2003). Applications of P at high rates failed to increase lycopene levels in juice from processing tomatoes (Oke et al., 2005). Vdel J, Zepl Lycopene production in response to water quality and amount depends on crop and axahn germplasm. When watermelon plants were We Zepi irrigated at full, three-fourths or one-half of evapotranspiration rates, fruit lycopene con- id—rdh tents were not significantly different (Lesko- MKS var et al., 2004). Tomato response to water availability depended on type and cultivar OH HO with a decrease in lycopene found with decreased soil water in three cultivars, and an increase in lycopene seen in or greenhouse-grown beefsteak types (Dumas Abbreviations: GGPP=Geranylgeranyl diphosphate, Psy (cr!B)=Phytoene desaturase, et al., 2003). Using saline water (to 0.25% NaCl w/v) increased lycopene content of Pds (crlP) = Phytoene synthase, Zds (crtQ) =Zeta-carotene desaturase, Lyc-e (CTRL- tomatoes (Dc Pascale et al., 2001; Krauss et al., 2006). Use of other types of ions for e)= Lycopene epsilon-cyclase, CycB = specific lycopene cyclase, Lcy-b salinity treatments (such as calcium or sul- fate) has not been reported. (CtrL-b)=Lycopene B-cyclase, CRTISO=Carotenoid isomerase, CrtR-b=B-ring Postharvest Storage Treatments hydoxylase, CrtR-e= Epsilon-ring hydroxylase, Zep 1= epoxidase, The most common stimulators of lyco- Vda= deepoxidase, Nxs =neoxanthin synthase pene synthesis in harvested fruit are storage temperature and ethylene. Generally, storage Figure published with permission: Source: Isaacson et al., 2002. temperatures of 20 to 30 °C stimulate lyco- pene production, whereas temperatures of Fig. I. Caroienoid biosynthesis pathway. 5 °C or less reduce lycopene (Hobson, 1987; Soto-Zamora et al., 2005) (Table 4). Ethyl- ene, a plant hormone, stimulates ripening, Tomes et al., 1954). The genes and enzymes in tomato , including lycopene, in cell wall softening. and subsequent lycopene controlling carotenoid synthesis in tomatoes response to environment are covered exten- formation in tomatoes and bitter melon. have been identified through cloning and sively in a review by Dumas et al. (2003). Application of exogenous ethylene to water- molecular characterization (Ronen et al., Lycopene synthesis and degradation in toma- melon caused cellular breakdown of placen- 2000). Nine genetic loci (15 alleles) control- toes is sensitive to air temperatures and tal tissue in immature and mature fruit and ling color pigmentation have been found, and light intensity (Table 3). High temperatures increased lycopene content by 10% (Don additional genes may exist (Sacks and Fran- (>32 °C) are known to suppress lycopene Huber, University of Fla., personal commu- cis, 2001). The crimson gene (og) has been synthesis (Goodwin and Jamikorn, 1952: nication). Compounds that block ethylene bred into many of the commercial tomato- Tomes, 1963). Excessive solar radiation can receptors such as carbon dioxide and 1- processing materials that are currently used affect lycopene accumulation (Adergoroye methylcyclypropane (l-MCP) also block or (Thompson et al., 2000). This gene confers an and Joliffe, 1987: Hamauzu et al., 1998). It slow ethylene-triggered lycopene formation, inability to acquire beta-carotene at the same is also known that red light stimulates carot- and their effects depend on stage of ripeness rate as normal red tomatoes (r) but increa- enoid accumulation in tomato and far-red light and temperature (Table 4) (Baldwin, 2004). ses the amount of lycopene that is formed blocks accumulation, probably from phyto- Controlled and MA storage (low 02/high (Mohr, 1979). However, many of the chromes in the fruit (Alba ci al., 2000). CO2 at 20%,40%, or 60%) blocked lycopene other high-pigment genes are not used in Watermelon lycopene synthesis is not synthesis in fresh market tomatoes harvested breeding materials because they impart negatively affected by temperatures in the at mature green, light pink, and turning stages undesirable plant characteristics (i.e., poor range of 20 to 37 °C (Vogele. 1937). In red (Buescher, 1979). In another study, CA germination, brittle stems) (Sacks and grapefruit, not much has been researched in storage (302 or 20% CO,) for 150 h Francis. 2001). this area, but it is known that lycopene content reduced lycopene and total carotenoid bio- is reduced between 4 and 210 (Meredith and synthesis by 40% and prevented ethylene Environmental Effects Young. 197 1; Purcell et al., 1968). production in the long shelf-life tomato Although potassium (K) and phosphorous varietyCF l 14 (Sozzi et al., 1999). Lycopene Environmental production conditions (P) are needed for lycopene synthesis, re- formation in mature green tomatoes was de- such as temperature, light, uptake, sponse is dependent on rate, crop, germ- la y ed for 6 to IS dat 15 to 25 °C after treatment salinity, and irrigation affect lycopene devel- plasm, growing conditions, and growth with 0.25 EL iiLL l-MCP (Mostofl et al., opment in plant materials (Table 3). Changes stage. Extra soil potassium is needed to avoid 2003). However, the l-MCP treatment did not

1136 IIORTS( H\(F Vot . 41(5) At ti j 2006

Table I. Plant material sources of lycopene (mg/kg). Exposure of tissue to oxygen and formation of ice crystals may cause losses of total Food Lycopene lycopene in frozen fruit. For instance, pureed Fruits and Vegetables Scientific Name content Reference watermelon had less ice crystal formation and lost less lycopene than diced fruit held for (cooked) Asparagus officinalis 0,30 U.S. Department of Agriculture. 2005 Fordhain ci al., 2001 a year at -20 °C, and only 5% to 10% of Autumn olive wnhellata 150-540 O( Carrots, orange 0.02 U.S. Department of Agriculture. 2005 lycopene was lost in watermelon held at -80 Ripe tomatoes Licopersieon 25.73 U.S. Department of Agriculture. 2005 (Fish and Davis, 2003). Frozen cubed toma- esculentuni toes also lost less lycopene when held at Gac Fruit-aril Moinordica 348-1902 Aoki et al., 2002: Ishida et al.. 2004 lower temperatures (Table 4) (Lisiewska and cochinchinesis Kmiecik, 2000). Even the type of storage U.S. Department of Agriculture, 2005 Grapefruit Citrus paiaclwi 14.19 container can affect losses, with red grape- 52.04 U.S. Department of Agriculture. 2005 Psidiimni gua/ava fruit concentrates stored in plastic containers Japanese Diospiros kaki 1.59-5.34 dc Ancos et al., 2000; U.S. Department of Agriculture. 2004 having less lycopene loss than that stored in Pitanga Eugenia uniflora 73.00 Rodriguez-Amaya, 1999 metal cans (Lee and Coates, 2002). Red cabbage Brassica oleracea 0.20 U.S. Department of Agriculture, 2005 Heat processing can cause lycopene loss (Capitata Group) and isomerization, depending on processing Red carrots Daucus ca,ota. 61.00 Cavalcante and Rodriguez-Amaya. time and temperature. Canned tomato prod- 1992; Surlcs et al., 2004 ucts are processed using hot break (heating to Red-fleshed Carica papaya 19.41 Rodriguez-Amaya, 1999 95 °C) or cold break (heating to 65 °C) Red navel orange Citrus sintiisis 3.90 Lee, 2001 methods. In the hot break method, the pectin Capsicum annhlloil 3.08 U.S. Department of Agriculture. 2005 Sweet red peppers enzymes are destroyed from the heat, Watermelon Citrullus lanatus 45.32 U.S. Department of Agriculture. 2005 whereas in cold break, pectin enzymes are Dcv Weight Priiniis ar,neniaca, 3.20-19.00 dcRigal et al.. 2000; still active resulting in pectin breakdown. Kiiacliik et al.. 1991 The cold break method is used for juices Bitter melon-aril vIoniordica charantia 411.00 Tran and Raymundo, 1999 and soups because it reduces viscosity and Rose hips Rosaceae canina 21.82 Hodisan Ct al.. 1997 results in improved color and flavor com- Swede Brassica rapa 0.50 Burns et al., 2003 pared with the hot break method (Anthon and Barrett, 2003). Tomatoes processed under conventional industrial heat or hot break. cold break, or super cold break processing Table 2. Processed (hod sources of lycopenc (mg/kg and as mgscr\ log). methods had a 9% to 28% loss in total Content lycopene (Nguyen and Schwartz, 1998; Re Food Lycopene per kg Ong) Per sers ing size Common serving et al., 2002; Takeoka et al., 2001). Processed foods Combined heat and pressure can have Na Sauce from 328.90 na a detrimental effect on carotenoid stability. 287.64 75.36 1 cup Tomato paste Persimmon fruit purees treated with 300 MPa Prepared sauce 159.90 39.98 I cup of pressure for 15 min at 25 °C had no Canned tomato sauce 151.52 37.12 1 cup Canned pizza sauce 127.10 na Na decrease in lycopene or total carotenoids juice cocktail 96.60 23.38 I cup compared with 50, 150. and 400 MPa high- Tomato juice. canned 90.37 21.96 1 cup pressure sterilization processing treatments at Tomato soup 54.60 13.32 1 cup 25 °C (de Ancos et al., 2000). Condiments and Spices A higher amount of surface area in a prod- Catsup 170.07 2.55 I Tbsp. uct exposed to drying, as well as drying 1 Tbsp. Salsa-ready to serve 108.76 1.74 method, induces lycopene loss and nega- 4.29 0.07 1 Tbsp. Barbecue sauce tively affects stability. Tomato halves, which Salad Dressings have far less surface area than pulp or Thousand Island 25.97 0.41 I Tbsp. Russian 6.27 0.097 I Tbsp. processing byproducts (peel, seed, etc), re- French 3.73 0.058 I Tbsp. tained lycopene when dried at 80 °C, but lost Spices 12% lycopene when dried at 110 °C (Zanoni Cinnamon--ground 0.29 0.0007 1 tsp. et al., 1999). Air, vacuum, and osmotic- Chili powder 0.21 . 0.0005 1 tsp. vacuum drying are the least damaging to Black pepper 0.06 0.0001 1 tsp. tomato pulp or processing waste lycopene Sources: Nguyen and Schwartz, 1998; USDA. 2005a. (2% to 4% initial loss), and spray drying is the most damaging (Shi et al., 1999). In spray-dried tomato pulp, increasing air tem- affect final lycopene content compared with fresh-cut tomatoes sliced at the mature green peratures and flow rates increased initial the control (MostofI et al., 2003). stage and ripened for 16 d compared with lycopene loss from 8% to 21% (Goula and control tomatoes that were not cut at green Adamopoulos, 2004). Once dried, lycopene is very unstable, Processing and Preservation stage (Mencarelli and Saltveit, 1988). This may have been the result of the rapid rise in with losses as high as 60% to 97% (Giova- Several processing systems, from mini- endogenous ethylene production and subse- nelli and Paradiso, 2002). The rate of degra- mal processing to heating, canning, drying, quent color change from the slicing treat- dation is increased by exposure to high and extraction, have been studied relative to ment. Like with intact fruits, carotenoid temperatures, light and oxygen, and low lycopene preservation. Fresh-cut plant mate- losses, primarily isomerization and degrada- moisture content resulting in isomerization rials generally show small amounts of carot- tion, most likely vary among plant materials from trans- to cis- forms and from autoox- enoid loss with little changes in lycopene and processing techniques with more studies idation of trans-lycopene (Giovanelli and isomerization. Fresh-cut watermelon held for needed to determine losses in fresh-cut and Paradiso, 2002). In early studies on dried 10 d at 2 °C or 5 °C lost 6 0% to 11% total minimally processed plant materials. tomato powders, researchers found signifi- lycopene (Perkins-Veazie and Collins, 2004), Even in a plant matrix, lycopene is readily cant lycopene loss from samples stored under whereas no losses in lycopene were found in oxidized during commercial frozen storage. air compared with those that were stored

H0aTSLII\cr Voc. 41)5) At s 2006 I I Table 3. Production practices and environmental effects during drying season on lycopene content. odors" possibly resulting from the autoox- Variable Range Commodity Result Reference idation of lycopene into smaller ketone and Air >32 °C Tomato Decreased lycopene, Goodwin and Jamikom, aldehyde compounds (Anguelova and War- temperature increased beta-carotene 1952; Tonics, 1963; the sen. 2000) and darkening of red powders Vogele, 1937 to brick-red color resulting from an increase 20-37 °C Watermelon No change in lycopene Vogele, 1937 in 5-hydroxymethyl-2-furfural (HMF) com- 4-21 C Grapefruit Reduced lycopene Meredith and Young, pounds, especially when powders are air- content 1971; Purcell et al., 1968 dried, spray-dried, or stored above room Fertility Increased K Tomato Increased lycopene in Fontes et al., 2000; controlled Trudel and Ozbun, temperatures (Anguelova and Warthesen, environment. 1971 2000; Giovanelli and Paradiso, 2002; Zanoni no change in field et al., 1999). Increased P Tomato Increased lycopene in 2003; Dumas, controlled Oke et al., 2005 Extraction Products environment, no change in field Extraction of lycopenc from its plant Irrigation 40% to 70% soil Tomato Increased lycopene in Dumas, 2003 matrix for use as natural food colorants or water depletion cherry types reduced in supplements is of considerable commercial slicing types. interest, currently valued at $34 million in the ET 0.5 to 1.0 Watermelon No change in lycopene Leskovar et al.. 2004 United States (Frost and Sullivan Company, ET = evapotranspiration. 2003). Although lycopene extraction was studied extensively in the 1950s, more suc- Table 4. Storage practices and their effects on lycopene content. cessful methods of extraction and recovery have been developed. Considerable lycopene Variable Range Crop Result Reference loss can happen during processing and stor- Temperature 20-30 °C Tomato Accelerates lycopene Hobson, 1987 accumulation at all age, and depends on surface area of the color stages material, temperature, atmosphere, exposure <5 °C Tomato Reduces lycopene Halt, 1961 time, and light during processing and storage by 50% in mature (Rodriguez-Amaya, 2001). In addition to green. 10% in red concerns about recovery and stability, isom- >20 °C Watermelon Increases lycopene Perkins-Veazie ct al., erization of lycopene from trans to cis forms content by 20% in ripe 2005 can occur. <5 °C Watermelon Reduces lycopenc Perkins-Veazie et al., Supercritical fluid extraction has been content in ripe 2005 explored more recently as a method for fruit by 10% >35 °C Bitter melon Decreased lycopene Tran and Ramundo, lycopene extraction from byproducts (i.e., in arils 1999 skin and ) of tomato processing (Rozzi Atmosphere Oxygen 3% Tomato Reduced lycopene Sozzi et al., 1999 et al., 2002). Pressure, temperature, extrac- content tion modifiers and solvents affect recovery, CO2 20% Tomato Reduced lycopene Sozzi et al., 1999 with 41% to 61% lycopene recovered from content tomatoes (Baysal et al., 2000; Gomez-Prieto CO, 5% to 10% Tomato Delayed color Buescher, 1979 et al., 2003; Rozzi et al., 2002) (Table 5). development Usually, CO2 is used as the extraction solvent and ethanol is used as the modifier. Gener- l-MCP 250 pIlL Tomato Delayed lycopene Mostofi et al.. 2003 accumulation in ally, lycopene recovery increases when pres- mature green sure or extraction temperatures increase, but 70-110 pI/L Cherry Tomato Delayed lycopene Opiyo and Ying, 2005 lycopene isomerization may occur. Lycopene accumulation and extraction or semipurification efficiency has color development been studied most extensively with tomato. l-MCP = 1-methyl-cyclopropane. Methodologies may need to be altered with other lycopene -contain ing plant materials, and the degree of isomerization, as well as lycopene loss, need to be documented in all under nitrogen or vacuum packed (Miers et (Anguelova and Warthesen, 2000; Lovric studies. al., 1958; Wong and Bohart, 1957). Freeze- et al., 1970). dried and oven-dried tomato pulp had similar Critical moisture level relative to surface Lycopene Absorption in Humans initial lycopene losses, but oven-dried pulp area also affects lycopene stability. Critical was more stable after 4 months of storage at moisture levels of 20% to 40% and temper- Studies on lycopene related to human ambient temperature, light, and atmosphere atures lower than 18 °C were necessary to health is recent, unlike beta-carotene, a pro- in closed containers (Sharma and Le Maguer, prevent lycopene losses in dried tomato carotenoid that was heavily re- 1996). In tomato powders, lycopene is re- halves stored under vacuum (Zanoni et al., searched. An estimated 50% of daily ported to isomerize from trans to cis forms as 2000). Conversely, tomato pulp air-dried to lycopene intake is from heat processed to- much as 30% 1060% after 6 weeks of storage, 9% moisture was more stable than pulp at mato products such as tomato sauce and paste with rate of loss dependent on temperature 23% moisture after storage at 4, 30, and 37 °C that is more readily absorbed from the gas- and light conditions under storage (Anguelo- (Giovanelli and Paradiso, 2002). Researchers trointestinal tract than lycopene from raw va and Warthesen, 2000). Tomato powders concluded that some water was necessary to tomatoes (Bohm and Bitsch, 1999). Lyco- stored at 45 °C for 6 weeks had the most protect against oxidative changes initiated by pene from other foods such as watermelon is lycopene loss and isomerization (60%) (An- metal ions and hydroperoxide molecules, but readily absorbed by humans without heat guelova and Warthesen, 2000). Cold also too much could enhance the movement of processing, indicating that the plant matrix negatively affected stability, with a 30% oxidative substrates, promoting lycopene is important for digestion and absorption lycopene loss in powders stored at -10, 2, loss (Giovanelli and Paradiso, 2002). Oxida- (Edwards et al.. 2003). Lower blood levels or 6 °C in the dark compared with those tive changes reported during storage of dried of lycopene were found in subjects ingesting stored at 20 or 25 °C under light or dark tomato are the development of "grassy off- muffins prepared with red carrots than from

1138 HORTSCiENCE VOL. 41(5) AUGUST 2006 Table 5. Summary of treatments resulting in greatest lycopene recovery using supercritical fluid extraction activity when used with lycopene include methods. , zeta-carotene, neoxanthin, and Material used Modifier Temperature Pressure Flow Rate %Recovery Reference (Kotake-Nara et al., 2001). One Tomato paste CO215% 55 °C 30 Mpa 4 kg/h Baysal et al.. chemopreventive action of lycopene is upre- waste Ethanol 54 2000 gulation of connexin 43, a gap-junctional Tomato seeds CO2 86 °C 34.5 Mpa 2.5 ml/min Rozzi et al., protein that is involved in cell signaling and skin 61 2002 (Bertram, 1999). When connexin 43 is upre- Tomato skin CO2 40°C 28.1 Mpa 4 ml/niin Gomez et al., gulated, there is a transfer of or and pulp 42 2003 signaling molecules between connected cells, Tomato seeds CO, 80 °C 27.5 Mpa 500 cm2/rnin Cadoni et al., resulting in the growth inhibition of chemi- 64 2000 and skin cally transformed cells (Bertram, 1999). Tomato seeds CO2 80 °C 30.0 Mpa 0.792 kg/h Sabio et al., and skin 80 2003 Sun-dried CO2/10% 66 °C 45.0 Mpa 20kg/hr Vasapollo et al.. Antioxidant Studies tomato oil 60 2004 One of the current theories in disease promotion is the prooxidant/antioxidant the- those prepared with tomato paste, indicating are often matched by age, gender, race, or ory (Meydani et al., 1998). Prooxidants such an interference in absorption from dietary ethnic background to eliminate confounding as superoxide free radicals are produced as fiber (Horvitz et al., 2004). Heat processing variables in the analysis (Portney and Wat- byproducts of normal respiration in the mi- and homogenization is speculated to break kins, 2000). In cohort studies, a group of tochondria of the cell (Fukagawa, 1999). It is protein-carotenoid complexes to release ly- individuals are followed over a length of time thought that l% to 3% of the oxygen taken copene from cell wall linkages and improve to determine if they develop disease condi- into the body is converted into superoxide uptake (Bohm and Bitsch, 1999; Gartner tions and what factors (exposures) influenced species or other reactive oxygen species et al., 1997; het Hof et al., 2000; Shi and Le the disease condition (Portney and Watkins, (Fang et al., 2002). Unless halted, the reactive Magner, 2000). Other researchers have re- 2000). Examples of ongoing cohort studies oxygen radicals can react with DNA bases ported that lycopene is preferentially taken are the Nurses Health Study (80,000 co- and proteins, causing mutations. Radicals can up from a supplement form compared with horts over 28 years) and the Health Profes- also react with unsaturated fatty acids in the tomato juice, again probably a plant matrix sionals Study (47,909 cohorts over 18 years) cell membrane to form lipid peroxy radicals, effect (Pactau et al., 1999). Because lycopene (Giovannucci, 1999; Sesso et al., 2003). which are highly reactive and can cause is a fat-soluble compound, fat ingested with There have been numerous epidemiologic a propagating chain of cellular damage (Fang lycopene improves its uptake in humans studies, both cohort and case-control,that et al., 2002; Fukagawa, 1999). In most cases, (Rao, 2004; Unlu et al., 2005). have correlated fewer occurrences of cancers the human body produces enzymes that slow Lycopene is stored in various organs of of the breast, cervix, lung, stomach, bladder, or halt the action of these reactive oxygen the body with greatest stores in adrenal pancreas, ovary, and prostate with diets high species (Wei and Lee, 2002). However, in glands, , adipose tissue and prostate, in fruits and vegetables (Buiatti et al., 1996; disease states or during aging, the bodys colon, skin, cervix, breast, and lung (Erdman Giovannucci et al., 1995; Grievink et al., enzymes are not as efficient in quenching the et al., 1993; Khachik et al.. 2002a, 2002b). In 2000; Ronco et al., 1999; Sato et al., 2002; activity of these molecules with the imbal- humans, lycopene is isomerized during di- Steinmetz et al., 1993). Of the vegetables, ance in repair mechanisms thought to accel- gestion from trans to cis forms and blood tomato products or lycopene are associated erate the initiation of disease states (Wei and concentrations vary from 0.6 to 1.9 nniol/ml with reduced risk for cancers of the lung, Lee, 2002). Plant-based are (Khachik et al., 2002a). The importance of breast, stomach, and prostate, with the stron- thought to act as antioxidants by scavenging isomer forms on the mechanisms of health gest evidence linking reduction in prostate or halting the action of superoxide or peroxy benefits to human is unknown, but cis iso- cancers in the mens Health Professionals radicals. mers seem to exhibit stronger antioxidant Study with lycopene-containing foods (Dc Numerous in vitro studies have been activity in vitro than trans forms and may Stefani et al., 2000; Giovannucci, 2002; conducted to determine the effectiveness of be preferentially absorbed (Erdman, 2005; Grievink et al., 2000; Levi et al., 2001). Other lycopene as an antioxidant. Carotenoids halt Stahl and Sies, 1992; Stahl et al., 1992). epidemiologic studies have reported reduced free radical activity by physical and chem- Because of the potential health contributions cardiovascular disease with lycopene-rich ical quenching activities in electron transfer, of lycopene, most combination vitamin and diets (Gianetti et al., 2002; Rissanen et al., hydrogen abstraction, and binding with rad- mineral supplements contain 0.3 to 2.0 mg of 2001; Sesso et al., 2003, 2004). ical species (Young and Lowe, 2001). Per- synthesized lycopene, although the U.S. oxynitrite is produced from nitric oxide and Food and Drug Administration has not de- Cancer Cell-Line Studies superoxide and has strong oxidizing proper- termined upper or lower intake levels for ties that can react with protein-lipid com- supplemental lycopene. In human research, in vitro studies pro- plexes. Lycopene, beta-carotene, alpha- vide valuable information on the effective- carotene, lutein, zeaxanthin, and beta-cryp- Epidemiologic Studies ness a compound has in mitigating growth of toxanthin were reported to be efficient cancer cell lines and dosage levels of com- agents in preventing peroxynitrite damage Epidemiologic studies are defined as pounds can be explored before using in (Panasenko et al.. 2000). Carotenoid oxy- "studies on the distribution and determinants intervention studies. In several cancer cell- gen-quenching activity at the cellular level of disease, injury or dysfunction in human line studies, lycopene reduced cancer cell is related to the number of conjugated populations" (Portney and Watkins, 2000). growth and induced apoptosis (cell death) in double bonds present. Lycopene contains Most epidemiologic studies on lycopene are malignant leukemia cell, endometrial, mam- two additional nonconjugated double bonds classified as observational studies and are mary, lung cancer, breast cancer, and prostate compared with other carotenoids. This bond categorized as case-control or cohort studies. cancer cells (Amir et al., 1999; Kotake-Nara structure confers twice as much singlet In case-control studies, case subjects are et al., 2001; Levy et al., 1995; Muller et al., oxygen quenching ability compared with screened for the disorder being studied and 2002). A synergistic effect (more reduction in beta-carotene in human plasma (Di Mascio controls are selected as the comparison group cell proliferation) was found with lycopene et al.. 1989). Lycopene also protects against without the disorder. Subjects are then inter- and low concentrations of 1,25-dihydroxyvi- lipid peroxidation. Low- lipoproteins viewed for history or exposure elements or in tamin D 3 () (Amir et al.. 1999). in human blood are comprised of unsatu- clinical settings and their medical history is Other carotenoids commonly found in plant rated fatty acids and can be oxidized by free reviewed for specific risk factors. Subjects foods that demonstrate synergistic apoptosis radicals and peroxidizing agents. Lycopene

\J di 15A i rr:T r 7006 1139

Table 6. Results of human intervention studies with lycopene, tomato or watermelon. Number of subjects, Amount of gender, age, other Source of lycopene lycopene (rng) condition Variables measured Conclusions Reference Whole tomatoes, 5 20 Lycopene absorption Better lycopene Bohm and tomato juice, and antioxidant absorption from Bitsch, 1999 tomato tests (TEAC, tomato juice and oleoresin TRAP) in plasma. tomato oleoresin than from fresh whole tomatoes. No differences in antioxidant response. Tomato puree II Lycopene absorption Lycopene absorption. Pellcgrini et al., 2000 and antioxidant No differences in tests (TRAP) using antioxidant plasma. response.

Tomato juice 40 25 TBARS, FRAP Lycopene reduced Bob et al., 2000 Glutathione lipid peroxidation enzymes. (TBARS). No differences in other antioxidant tests. Tomato juice 15,45 31 LDL oxidation in Lycopenc reduced low Maryuma et al., 2001 plasma. density lipoprotein oxidation. Synthetic supplement 15 175 Glutathione (GSH and No change in any Hininger et al., 2001 GSGG) and variables. superoxide dismutase, and glutathione peroxidase in plasma. Tomato juice, 20,40 23 Lycopene absorption, Similar lycopene Collins et al., 2004; watermelon juice FRAP, , absorption from Edwards et al., 2003 glutathione tomato and peroxidase in watermelon juice, plasma. no heat processing in watermelon. No differences in antioxidant or cholesterol response. Lycopene-15 mg 15 8 DNA oxidative Lycopene reduced Torbergsen and supplement damage (Comet DNA damage. Collins, 2000 assay). Tomato juice 40 23 DNA oxidative Lyeopene reduced Pool-Zobel et al., 1997 damage (Comet DNA strand breaks. assay). Synthetic 15 26 men with IGF-1, PSA in blood. Lycopene reduced Kucuk et al., 2001 supplement PSA levels (14%) no effect on IGF-l. Tomato sauce 30 32 men with Blood serum and Lyeopene increased in van Breeman prostate cancer prostate lycopene serum and prostate et al., 2002 levels PSA, DNA Reduced PSA oxidative damage levels (17%), DNA Modulation of damage (2 1%), and cancer. tumor size. TEAC = Trolox equivalent antioxidant capacity; TRAP = radical trapping antioxidant parameter; TBARS = thiobarbituric acid reactive substances; DNA = deoxyribonucleic acid; FRAP ferric-reducing ability of plasma; IGF-1 = insulin growth factor-1; PSA = prostate-specific antigen; LDL = low-density lipoproteins.

is primarily attached to low-density lipopro- Three tests are commonly used to quan- analog (Djuric and Powell, 2001). TRAP teins in plasma and is thought to confer tify antioxidant content: Trolox equivalent measures the rate of thermally induced per- protection against lipid peroxidation and antioxidant capacity (TEAC), the radical oxidation of an azo-compound (Pellegrini foam cell production, both of which are trapping antioxidant parameter (TRAP) as- et al., 2000). The FRAP assay measures an implicated in the initiation say, and the ferric-reducing ability of plasma oxidation/reduction reaction by measuring of atherosclerosis (Arab and Steck, 2000; (FRAP). These assays are rapid, relatively the reduction of ferric -triyridltriazine to its Gianetti et al., 2002). In one in vitro study, easy methods for measuring the ability of ferrous form when combined with an antiox- lycopene reduced lipid peroxidation of cells antioxidant compounds to scavenge free rad- idant (Benzie and Strain, 1996). exposed to a peroxidizing agent (ferric icals in blood, purified compounds, or plant In one in vitro antioxidant study, purified nitrilotriacetate) (Matos et al., 2000) with extracts (Bohm et al., 2002; Bub et al., 2000). lycopene and its isomers were compared a greater reduction in lipid peroxidation The TEAC test measures the total antioxidant against beta-carotene, alpha-carotene, and when lycopene was combined with lutein capacity of a compound against a standard zeaxanthin for (TEAC) activity. Lycopene (Stahl et al., 1998). antioxidant, trolox, a water-soluble in cis forms exhibited greater antioxidant

1140 HORTSC!ENCL VOL. 41(5) AUGUST 2006 activity compared with all trans forms, PSA levels and number of prostate malig- is sketchy, but in an animal model of prostate whereas all trans lycopene had greater TEAC nancies (Mohanty et al., 2005). cancer, androgen target genes and inflamma- activity than trans beta-carotene (Bohm tory signaling genes were upregulated with et al., 2002). Additionally, antioxidant activi- Summary the cancer, whereas supplementation with ties vary among foods that contain lycopcne. tomato sauce downregulated gene expression In one study, researchers found higher anti- More than 245 epidemiologic studies (Stacewicz-Sapuntzakis and Bowen, 2005). oxidant activity in heat-processed tomatoes have found that diets rich in fruits and Lycopene seemed to modulate the genes compared with fresh tomatoes, presumably vegetables can protect against cancer, stroke, involved in prostate health. As new findings because processing improved the extraction and cardiovascular disease (Block et al., are made in this field, opportunities will arise and activity of antioxidant compounds 1992; Joshipura et al., 1999, 2001; Steinmetz for plant scientists, food technologists, nutri- (Dewanto et al., 2002). Antioxidant activities and Potter. 1996; Strandhagen et al., 2000). tionists, and medical researchers to work can vary between aqueous and organic ex- Because of these findings, the U.S. Depart- together to create "tailored foods" for indi- tracts from the same food, indicating that ment of Agriculture (2005b) changed the new viduals or subgroups to help combat the other compounds, i.e., vitamin E, and water- dietary guidelines for healthy Americans to plethora of diet-related diseases that affects soluble and , also include five to 13 servings of fruits and the population. express antioxidant activity and contribute vegetables per day, depending on caloric to the whole food antioxidant profile (Diuric intake. Lycopene is one of many phytochem- Literature Cited and Powell, 2001; Takeoka et at., 2001). icals in fruit and vegetables that may act to protect against many of these diseases. Adergoroye, A.S. and P.A. Jolliffe. 1987. Some Human Intervention Studies Because upper and lower intake levels inhibitory effects of radiation stress on to- have not been established for lycopene, most mato fruit ripening. J. Set. Food Agr. 39:297- Currently, no long-term intervention stud- medical and experts agree that 302. ies have been conducted with lycopene be- lycopene from a natural food state is prefer- Alba, R., M.M. Cordonnier-Pratt. and L.H. Pratt. cause the effectiveness, safety, and dosage able to supplements (Liu, 2003; Miller et al., 2000. Fruit-localized phytochromes regulate lycopene accumulation independently of eth- levels of lycopene on human health have not 2002). Some researchers recommend intakes ylene production in tomato. Plant Physiol. been established. Short-term studies have of 6 mg/day of lycopene from food for health 123:363-370. been conducted mostly with lycopene or benefits (Porrini and Rise, 2005). Several Amir, H., M. Karas, J. Giat, M. Danilenko, R. tomato products, with varying results de- commonly available fruits and vegetables Levy, T. Yermiahu, J. Levy, and Y. Sharoni. pending on lycopene dosage levels and type are good sources of lycopene and are also 1999. Lycopene and 1 ,25-dihydroxyvitamin of antioxidant tests used (Table 6).The gen- good sources of other phytochemicals, in- D3 cooperate in the inhibition of cell cycle eral findings are that I) lye opene from pro- cluding vitamin C. vitamin E, other carote- progression and induction of differentiation cessed tomato products such as juice or noids, , minerals, and phenolic in HL-60 leukemic cells. Nutr. Cancer 33: oleoresin is better absorbed than that of fresh compounds. Challenges exist for plant 105-112. tomato; 2) a minimum dosage of 4 mg breeders to enhance lycopene levels in plant Anguclova, T. and J. Warthesen. 2000. Lycopene stability in tomato powders. J. Food Sci. 65:67- lycopene daily is needed to increase plasma materials without altering quality, yield, shelf 70. levels of lycopene and to see reduced DNA life, or other phytochemicals, and for food Anthon, G.E. and D.M. Barrett. 2003. Thermal damage or reduced low-density lipoprotein processors to maintain lycopene levels in inactivation of lipoxygenase and hydroperoxy- (LDL) oxidation; and 3) lycopene may effec- plant materials without sacrificing initial trienoic acid lycase in tomatoes. Food Chem. tively reduce prostate-specific antigen (PSA) carotenoid levels. 80:1-5. levels and prostate tumor size with 8 to 30 mg Phytochemicals may have independent or Aoki, H., N.T. Kieu, N. Kuze, K. Tomisaka, and N. lycopene daily as a supplement or processed synergistic modes of action to protect cells Van Chuyen. 2002. Carotenoid pigments in tomato source. against free radical damage. They may also GAC fruit (Momordica cochinchinensis Three short-term lycopene intervention affect cancer promotion/progression and halt SPRENG). Biosci. Biotechnol. Biochem. trials have been conducted with men with inflammatory responses (Liu, 2003). More 66:2479-2482. research is needed to determine if compounds Arab, L. and S. Steck. 2000. Lycopene and cardio- confirmed prostate cancer or with premaglig- vascular disease. Amer. J. Clin. Nutr. 71: nant prostate neoplasia (HGPIN). In the first in plant materials, especially carotenoids, can 1691S-1695S. prostate cancer study, 26 men with confirmed cause synergistic activities in vivo and to Arias. R., T.C. Lee, D. Specca, and H. Jones. 2000. prostate cancer were supplemented with determine modes of action. Well-designed Quality comparison of hydroponic tomatoes either 15 mg purified lycopene or a placebo studies that are longer in duration that com- (Lycopersicon esculentum) ripened on and off for 3 weeks before prostatectomy (removal of pare both lycopene and tomatoes/watermelon vine. J. Food Sci. 65:545-548. prostate) (Kucuk et al., 2001). Prostate- together will help clarify the areas of research Baldwin, E.A. 2004. Ethylene and postharvest specific antigen levels (biomarker of prostate that are conflicting. commodities. HoriScience 39:1538-1540. dysfunction) declined by 18% in lycopene Another new emerging area of research Baysal, T., S. Ersus, and D.A. Starmans. 2000. treated subjects compared with unsupple- that may explain the health benefits of lyco- Supercritical CO(2) extraction of beta-carotene and lycopene from tomato paste waste. J. Agr. mented men (14% increase) (Kucuk et al.. pene is nutrigenomics, described as a diet Food Chem. 48:5507-5511. 2001). In a larger research project funded by tailored for your genetics. It is known that Benzie, I.E. and J.J. Strain. 1996. The ferric re- the National Cancer Institute, 32 men with some genetic polymorphisms in humans af- ducing ability of plasma (FRAP) as a measure prostate cancer were supplemented with 30 fect their metabolism of certain foods; com- of antioxidant power: The FRAP assay. Anal. mg lycopene from tomato sauce for 3 weeks mon examples include lactose intolerance Biochem. 239:70-76. (van Breemen et al., 2002). Serum and and alcohol dehydrogenase deficiency (Ger- Bertram, J.S. 1999. Carotenoids and gene regula- prostate tissue lycopene levels increased man, 2005; Peregrin, 2001). Diseases linked tion. Nutr. Rev. 57:182-191. threefold over initial levels, serum PSA to dietary patterns include cardiovascular Block, G., B. Patterson, and A. Subar. 1992. Fruit, levels decreased by 17.5%, and cancer cells disease, diabetes, and some cancers (Ommen vegetables, and cancer prevention: A review of were modulated (Bowen et al., 2002). In and Stierum, 2002). Numerous genetic poly- the epidemiological evidence. Nutr. Cancer morphisms have been recently identified that 18-1-29. a smaller dosage study, 40 patients with Bohm,V and R. Busch. 1999. Intestinal absorp- HGPIN were split into two groups; one half influence heart disease risk (German, 2005). tion of lycopene from different matrices and were given 8 mg lycopene per day and the Preliminary data indicate that prostate cancer interactions to other carotenoids, the lipid other group was not treated. Subjects were risk may be increased in a subset of individ- status, and the antioxidant capacity of human followed for 1 year and then evaluated for uals with a genetic variant who have a low plasma. Fur. J. Nutt. 38:118-125. PSA levels and prostate malignancy. The intake of lycopene (Kristal and Schenk, Bohm, V., N.L. Puspitasari-Nienaber, M.G. treated groups had significantly reduced 2005). Research in this area with lycopene Ferruzzi, and S.J. Schwartz. 2002. Trolox

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