Enhanced bioavailability of lycopene when consumed as cis-isomers from tangerine compared to red tomato juice, a randomized, cross-over clinical trial

Molecular Nutrition and Food Research

Volumn 59, Issue 4, 2015, Pages 658-669

  Cooperstone, Jessica L ^a   Ralston, Robin A ^a   Riedl, Ken M ^a,b   Haufe, Thomas C ^a,c   Schweiggert, Ralf M ^d   King, Samantha A ^e   Timmers, Cynthia D ^b   Francis, David M ^a   Lesinski, Gregory B ^b,e   Clinton, Steven K ^b,e   Schwartz, Steven J ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d UNIVERSITY OF HOHENHEIM   (Germany)

^e THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Bioavailability; Carotenoids; Chromoplast; Tangerine tomato; Tetra cis lycopene

Indexed keywords

CITRUS RETICULATA; LYCOPERSICON ESCULENTUM;

CAROTENOID; CHOLESTEROL; HEMOGLOBIN; LIPOPROTEIN; LIPOPROTEIN TRIGLYCERIDE; LYCOPENE; NEUROSPORENE; PHYTOENE; PHYTOFLUENE; TRIACYLGLYCEROL; ZETA CAROTENE;

ADOLESCENT; ADULT; BIOAVAILABILITY; BLOOD; BODY MASS; CHEMISTRY; CITRUS; CONTROLLED STUDY; CROSSOVER PROCEDURE; FEMALE; FRUIT AND VEGETABLE JUICE; HEMATOCRIT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; ISOMERISM; MALE; METABOLISM; RANDOMIZED CONTROLLED TRIAL; TANDEM MASS SPECTROMETRY; TOMATO; YOUNG ADULT;

ADOLESCENT; ADULT; BIOLOGICAL AVAILABILITY; BODY MASS INDEX; CAROTENOIDS; CHOLESTEROL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CITRUS; CROSS-OVER STUDIES; FEMALE; FRUIT AND VEGETABLE JUICES; HEMATOCRIT; HEMOGLOBINS; HUMANS; ISOMERISM; LIPOPROTEINS; LYCOPERSICON ESCULENTUM; MALE; TANDEM MASS SPECTROMETRY; TRIGLYCERIDES; YOUNG ADULT; ZETA CAROTENE;

EID: 84926121552     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400658     Document Type: Article

References (49)

1. Zu, K. Mucci, L. Rosner, B. A. Clinton, S. K. et al. Dietary lycopene, angiogenesis, and prostate cancer: a prospective study in the prostate-specific antigen era. J. Natl. Cancer Inst. 2014, 35, 2154-2155.
2. Porrini, M. Riso, P. Testolin, G. Absorption of lycopene from single or daily portions of raw and processed tomato. Br. J. Nutr. 1998, 80, 353-361.
3. Clinton, S. K. Emenhiser, C. Schwartz, S. J. Bostwick, D. G. et al. Cis-trans lycopene isomers, carotenoids, and retinol in the human prostate. Cancer Epidemiol. Biomarkers Prev. 1996, 5, 823-833.
4. Richelle, M. Sanchez, B. Tavazzi, I. Lambelet, P. et al. Lycopene isomerisation takes place within enterocytes during absorption in human subjects. Br. J. Nutr. 2010, 103, 1800-1807.
5. Moran, N. E. Cichon, M. J. Riedl, K. M. Grainger, E. M. et al. Pharmacokinetics of 13C-lycopene in healthy adults. FASEB J. 2013, 27, 38.6.
6. Ross, A. B. Vuong, L. T. Ruckle, J. Synal, H. A. et al. Lycopene bioavailability and metabolism in humans: an accelerator mass spectrometry study. Am. J. Clin. Nutr. 2011, 93, 1263-1273.
7. Unlu, N. Z. Bohn, T. Francis, D. M. Nagaraja, H. N. et al. Lycopene from heat-induced cis-isomer-rich tomato sauce is more bioavailable than from all-trans-rich tomato sauce in human subjects. Br. J. Nutr. 2007, 98, 140-146.
8. Castenmiller, J. J. M. West, C. E. Bioavailability and bioconversion of carotenoids. Annu. Rev. Nutr. 1998, 18, 19-38.
9. Boileau, A. C. Merchen, N. R. Wasson, K. Atkinson, C. A. et al. Cis-lycopene is more bioavailable than trans-lycopene in vitro and in vivo lymph-cannulated ferrets. J. Nutr. 1999, 129, 1176-1181.
10. Failla, M. L. Chitchumroonchokchai, C. Ishida, B. K. In vitro micellarization and intestinal cell uptake of cis isomers of lycopene exceed those of all-trans lycopene. J. Nutr. 2008, 138, 482-486.
11. Tomes, M. Flower color modification associated with the gene. Report of the Tomato Genetics Cooperative at the Division of Truck Crops, University of California, Davis. 1952, Vol. 2, p. 12.
12. Isaacson, T. Ronen, G. Zamir, D. Hirschberg, J. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 2002, 14, 333-342.
13. Clough, J. M. Pattenden, G. Naturally occurring poly-cis carotenoids. Stereochemistry of poly-cis lycopene and its congeners in "tangerine" tomato fruits. J. Chem. Soc. Chem. Commun. 1979, 301, 616-619.
14. Nguyen, M. L. Schwartz, S. J. Lycopene stability during food processing. Proc. Soc. Exp. Biol. Med. 1998, 218, 101-105.
15. Burri, B. J. Chapman, M. H. Neidlinger, T. R. Seo, J. S. Ishida, B. K. Tangerine tomatoes increases total and tetra-cis-lycopene isomer concentrations more than red tomatoes in healthy adult humans. Int. J. Food Sci. Nutr. 2009, 60(S1), 1-16.
16. Schweiggert, R. M. Steingass, C. B. Heller, A. Esquivel, P. Carle, R. Characterization of chromoplasts and carotenoids of red- and yellow-fleshed papaya (Carica papaya L.). Planta 2011, 234, 1031-1044.
17. Sitte, P. Falk, H. Liedvogel, B. in: Czygan, F.-C. (Ed.), Pigment Plants, Gustav Fischer Verlag, Stuttgart, Germany 1980, pp. 117-148.
18. Hempel, J. Amrehn, E. Quesada, S. Esquivel, P. et al. Lipid-dissolved γ-carotene, β-carotene, and lycopene in globular chromoplasts of peach palm (Bactris gasipaes Kunth) fruits. Planta 2014, 240, 1037-1050.
19. Mathews-Roth, M. M. Carotenoid pigment administration and delay in development of UV-B induced tumors. Photochem. Photobiol. 1983, 37, 509-511.
20. Engelmann, N. J. Clinton, S. K. Erdman Jr. J. W. Nutritional aspects of phytoene and phytofluene, carotenoid precursors to lycopene. Adv. Nutr. 2011, 2, 51-61.
21. Unlu, N. Z. Bohn, T. Francis, D. Clinton, S. K. Schwartz, S. J. Carotenoid absorption in humans consuming tomato sauces obtained from tangerine or high-beta-carotene varieties of tomatoes. J. Agric. Food Chem. 2007, 55, 1597-1603.
22. Borel, P. Tyssandier, V. Mekki, N. Grolier, P. et al. Chylomicron beta-carotene and retinyl palmitate responses are dramatically diminished when men ingest beta-carotene with medium-chain rather than long-chain triglycerides. J. Nutr. 1998, 128, 1361-1367.
23. Kopec, R. E. Schweiggert, R. M. Riedl, K. M. Carle, R. Schwartz, S. J. Comparison of high-performance liquid chromatography/tandem mass spectrometry and high-performance liquid chromatography/photo-diode array detection for the quantitation of carotenoids, retinyl esters, α-tocopherol and phylloquinone in chylomicron-rich fractions of human plasma. Rapid Commun. Mass Spectrom. 2013, 27, 1393-1402.
24. Kopec, R. E. Riedl, K. M. Harrison, E. H. Curley, R. W. et al. Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma. J. Agric. Food Chem. 2010, 58, 3290-3296.
25. van Vliet, T. Schreurs, W. H. vanden Berg, H. Intestinal beta-carotene absorption and cleavage in men: response of beta-carotene and retinyl esters in the triglyceride-rich lipoprotein fraction after a single oral dose of beta-carotene. Am. J. Clin. Nutr. 1995, 62, 110-116.
26. Hu, X. Jandacek, R. J. White, W. S. Intestinal absorption of beta-carotene ingested with a meal rich in sunflower oil or beef tallow: postprandial appearance in triacylglycerol-rich lipoproteins in women. Am. J. Clin. Nutr. 2000, 71, 1170-1180.
27. Harris, W. M. Spurr, A. R. Chromoplasts of tomato fruits. II. The red tomato. Am. J. Bot. 1969, 56, 380-389.
28. Rosso, S. W. The ultrastructure of chromoplast development in red tomatoes. J. Ultrastruct. Res. 1968, 25, 307-322.
29. Schweiggert, R. M. Mezger, D. Schimpf, F. Steingass, C. B. Carle, R. Influence of chromoplast morphology on carotenoid bioaccessibility of carrot, mango, papaya, and tomato. Food Chem. 2012, 135, 2736-2742.
30. Gupta, R. Kopec, R. E. Schwartz, S. J. Balasubramaniam, V. M. et al. Combined pressure-temperature effects on carotenoid retention and bioaccessibility in tomato juice. J. Agric. Food Chem. 2011, 59, 7808-7817.
31. Kessler, F. Schnell, D. Blobel, G. Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts. Planta 1999, 208, 107-113.
32. Ben-Amotz, A. Lers, A. Avron, M. Stereoisomers of beta-barotene and phytoene in the alga Dunaliella bardawil. Plant Physiol. 1988, 86, 1286-1291.
33. Schweiggert, R. M. Kopec, R. E. Villalobos-Gutierrez, M. G. Högel, J. et al. Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: a randomised cross-over study. Br. J. Nutr. 2014, 111, 490-498.
34. Richelle, M. Lambelet, P. Rytz, A. Tavazzi, I. et al. The proportion of lycopene isomers in human plasma is modulated by lycopene isomer profile in the meal but not by lycopene preparation. Br. J. Nutr. 2012, 107, 1482-1488.
35. Leung, W. Hessel, S. Méplan, C. Flint, J. et al. Two common single nucleotide polymorphisms in the gene encoding beta-carotene 15, 15'-monoxygenase alter beta-carotene metabolism in female volunteers. FASEB J. 2009, 23, 1041-1053.
36. Lietz, G. Oxley, A. Boesch-Saadatmandi, C. Kobayashi, D. Importance of β, β-carotene 15, 15'-monooxygenase 1 (BCMO1) and β, β-carotene 9', 10'-dioxygenase 2 (BCDO2) in nutrition and health. Mol. Nutr. Food Res. 2011, 56, 241-250.
37. dela Seña, C. Narayanasamy, S. Riedl, K. M. Curley, R. W. et al. Substrate specificity of purified recombinant human β-carotene 15, 15'-oxygenase (BCO1). J. Biol. Chem. 2013, 288, 37094-37103.
38. Wang, T. T. Edwards, A. J. Clevidence, B. A. Strong and weak plasma response to dietary carotenoids identified by cluster analysis and linked to beta-carotene 15, 15'-monooxygenase 1 single nucleotide polymorphisms. J. Nutr. Biochem. 2013, 24, 1538-1546.
39. Borel, P. Desmarchelier, C. Nowicki, M. Bott, R. et al. Interindividual variability of lutein bioavailability in healthy men: characterization, genetic variants involved, and relation with fasting. Am. J. Clin. Nutr. 2014, 100, 168-175.
40. Nierenberg, D. W. Stukel, T. A. Baron, J. A. Dain, B. J. et al. Determinants of increase in plasma concentration of beta-carotene after chronic oral supplementation. Am. J. Clin. Nutr. 1991, 53, 1443-1449.
41. Lietz, G. Oxley, A. Berry, P. Mesketh, J. et al. Gender differences in retinol metabolism are independent of beta-carotene conversion. Carotenoid Sci. 2014, 18, 121.
42. Gartner, C. Stahl, W. Sies, H. Lycopene is more bioavailable from tomato paste than from fresh tomatoes. Am. J. Clin. Nutr. 1997, 66, 116-122.
43. Diwadkar-Navsariwala, V. Novotny, J. A. Gustin, D. M. Sosman, J. A. et al. A physiological pharmacokinetic model describing the disposition of lycopene in healthy men. J. Lipid Res. 2003, 44, 1927-1939.
44. Gustin, D. M. Rodvold, K. A. Sosman, J. A. Diwadkar-Navsariwala, V. et al. Single-dose pharmacokinetic study of lycopene delivered in a well-defined food-based lycopene delivery system (tomato paste-oil mixture) in healthy adult male subjects. Cancer Epidemiol. Biomarkers Prev. 2004, 13, 850-860.
45. Boileau, T. W. M. Liao, Z. Kim, S. Lemeshow, S. et al. Prostate carcinogenesis in N-methyl-N-nitrosourea (NMU)-testosterone-treated rats fed tomato powder, lycopene, or energy-restricted diets. J. Natl. Cancer Inst. 2003, 95, 1578-1586.
46. Campbell, J. K. Engelmann, N. J. Lila, M. A. Erdman, J. W. Phytoene, phytofluene, and lycopene from tomato powder differentially accumulate in tissues of male fisher 344 rats. Nutr. Res. 2007, 27, 794-801.
47. Moran, N. E. Clinton, S. K. Erdman Jr, J. W. Differential bioavailability, clearance, and tissue distribution of the acyclic tomato carotenoids lycopene and phytoene in Mongolian gerbils. J. Nutr. 2013, 143, 1920-1926.
48. Khachik, F. Beecher, G. R. Goli, M. B. Lusby, W. R. Separation, identification, and quantification of carotenoids in fruits, vegetables and human plasma by high performance liquid chromatography. Pure Appl. Chem. 1991, 63, 71-80.
49. Khachik, F. Carvalho, L. Bernstein, P. S. Muir, G. J. et al. Chemistry, distribution, and metabolism of tomato carotenoids and their impact on human health. Exp. Biol. Med. 2002, 227, 845-851.