Applicability of in Vitro Models in Predicting the in Vivo Bioavailability of Lycopene and β-Carotene from Differently Processed Soups

Marie Alminger, Cecilia Svelander, Anna Wellner, Rebeca Martinez-Tomas, Lucy Bialek, Elvira Larque, Francisca Perez-Llamas

Department of Chemical and Biological Engineering, Food Science, Chalmers University of Technology, G?teborg, Sweden.
Physiology Department, Faculty of Biology, University of Murcia, Murcia, Spain.
Unilever Discover R&D, Unilever Food and Health Research Institute, Vlaardingen, The Netherlands..

DOI: 10.4236/fns.2012.34068                

Abstract

Presently, there is no clear consensus on the best approach to estimate carotenoid bioavailability. The best alternative would be to use human studies, but they are labour-intensive and expensive and can only be used to investigate a limited number of samples. Hence, a number of in vitro: models have been developed to study pre-absorptive processes and factors affecting bioavailability. The question is, however, how well the results obtained by the various methods correlate to each other and to the in vivo situation. In the present paper, we have compared in vivo data from two human studies on differently processed soups containing carrots, tomato and broccoli, with results obtained by in vitro characterisation of the same soups. In vitro bioaccessibility was estimated by a static in vitro digestion investigating matrix release and micellarization of carotenoids and by uptake studies in a human intestinal cell line (Caco-2). In vivo data was obtained from clinical studies measuring total plasma carotenoid concentrations in human subjects after 4 weeks daily consumption of the soups. Comparison of the in vitro and in vivo results indicate that the combination of a two-step in vitro digestion and Caco-2 cells seems to be a useful tool for estimation of β-carotene bioaccessibility and screening of factors governing the release of β-carotene from this type of food. For lycopene the in vitro and in vivo results were less consistent, suggesting that reliable prediction of lycopene bioavailability might be more problematic.

Keywords

In Vitro Digestion; Human; Uptake; Caco-2 Cells; β-Carotene; Lycopene; Carotene Bioavailability

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	A. V. Rao and L. G. Rao, “Carotenoids and Human Health,” Pharmacological Research, Vol. 55, No. 3, 2007, pp. 207-216. doi:10.1016/j.phrs.2007.01.012
[2]	K. J. Yeum and R. M. Russell, “Carotenoid Bioavailability and Bioconversion,” Annual Review of Nutrition, Vol. 22, 2002, pp. 483-504. doi:10.1146/annurev.nutr.22.010402.102834
[3]	L. Yonekura and A. Nagao, “Intestinal Absorption of Dietary Carotenoids,” Molecular Nutrition & Food Research, Vol. 51, No. 1, 2007, pp. 107-115. doi:10.1002/mnfr.200600145
[4]	R. S. Parker, “Absorption, Metabolism, and Transport of Carotenoids,” FASEB Journal, Vol. 10, No. 5, 1996, pp. 542-551.
[5]	J. Shi and J. Le Maguer, “Lycopene in Tomatoes: Chemical and Physical Properties Affected by Food Processing,” Critical Reviews in Biotechnology, Vol. 20, 2000, pp. 293-334. doi:10.1080/07388550091144212
[6]	M. L. Nguen and S. J. Schwarz, “Lycopene Stability during Food Processing,” Proceedings of the Society for Experimental Biology and Medicine, Vol. 218, 1998, pp. 101-105.
[7]	S. K. Clinton, C. Emenhiser, S. J. Schwarz, D. G. Bostwick, A. W. Williams, B. J. Moore and J.-W. Erdman, “Cis-Trans Lycopene Isomers, Carotenoids, and Retinol in the Human Prostate,” Cancer Epidemiology, Biomarkers & Prevention, Vol. 5, 1996, pp. 823-833.
[8]	J. Schierle, W. Bretzel, I. Buhler, N. Faccin, D. Hess, K. Steiner and W. Schuep, “Content and Isomeric Ratios of Lycopene in Food and Human Blood Plasma,” Food Chemistry, Vol. 59, No. 3, 1997, pp. 459-465. doi:10.1016/S0308-8146(96)00177-X
[9]	C. G?rtner, W. Stahl and H. Sies, “Lycopene Is More Bioavailabile from Tomato Paste than from Fresh Tomatoes,” American Journal of Clinical Nutrition, Vol. 66, No. 1, 1997, pp. 116-122
[10]	A. C. Boileau, N. R. Merchen, K. Wasson, C. A. Atkinson and J. W. Erdman, “Cis-lycopene Is More Bioavailable than Trans-Lycopene in Vitro and in Vivo in Lymph-Cannulated Ferrets,” Journal of Nutrition, Vol. 129, No. 6, 1999, pp. 1176-1181.
[11]	N. Z. Unlu, T. Bohn, D. Francis, H. N. Nagaraja, S. K. Clinton, S. J. Schwartz, “Lycopene from Heat-Induced Cis-Isomer-Rich Tomato Sauce Is More Bioavailable than from All-Trans-Rich Tomato Sauce in Human Subjects,” British Journal of Nutrition, Vol. 98, No. 1, 2007, pp. 140-146. doi:10.1017/S0007114507685201
[12]	M. Richelle, B. Sanchez, I. Tavazzi, P. Lambelet, K. Bortlik and G. Williamsson, “Lycopene Isomerization Takes Place within Enterocytes during Absorption in Human Subjects,” British Journal of Nutrition, Vol. 103, No. 12, 2010, pp. 1800-1807. doi:10.1017/S0007114510000103
[13]	E. Hedrén, V. Diaz and U. Svanber, “Estimation of Carotenoid Accessibility from Carrots Determined by an in Vitro Digestion Method,” European Journal of Clinical Nutrition, Vol. 56, No. 5, 2002, pp. 425-430. doi:10.1038/sj.ejcn.1601329
[14]	F. Granado-Lorencio, B. Olmedilla-Alonso, C. HerreroBarbudo, B. Perez-Sacristan, I. Blanco-Navarro and S. Blazquez-Garcia, “Comparative in Vitro Bioaccessibility of Carotenoids from Relevant Contributors to Carotenoid Intake,” Journal of Agricultural and Food Chemistry, Vol. 55, No. 15, 2007, pp. 6387-6394. doi:10.1021/jf070301t
[15]	F. Granado-Lorencio, B. Olmedilla-Alonso, C. HerreroBarbudo, I. Blanco-Navarro, B. Perez-Sacristan and S. Blazquez-Garcia, “In Vitro Bioaccessibility of Carotenpids and Tocopherols from Furits and Vegetables,” Food Chemistry, Vol. 102, No. 3, 2007, pp. 641-648. doi:10.1016/j.foodchem.2006.05.043
[16]	D. A. Garrett, M. L. Failla and R. J. Sarama, “Development of an in Vitro Digestion Method to Assess Carotenoid Bioavalability from Meals,” Journal of Agricultural and Food Chemistry, Vol. 47, No. 10, 1999, pp. 4301-4309. doi:10.1021/jf9903298
[17]	S. K. Thakkar, B. Maziya-Dixon, A. G. O. Dixon and M. L. Failla, “β-Carotene Micellarization during in Vitro Digestion and Uptake by Caco-2 Cells Is Directly Proportional to β-Carotene Content in Different Genotypes of Cassava,” Journal of Nutrition, Vol. 137, No. 10, 2007, pp. 2229-2233.
[18]	S. Veda, A. Kamath, K. Platel, K. Begum and K. Srinivasan, “Determination of Bioaccessibility of Beta-Carotene in Vegetables by in Vitro Methods,” Molecular Nutrition & Food Research, Vol. 50, No. 11, 2006, pp. 1047-1052. doi:10.1002/mnfr.200600076
[19]	E. Reboul, M. Richelle, E. Perrot, C. DesmoulinsMalezet, V. Pirisi and P. Borel, “Bioaccessibility of Carotenoids and Vitamin E from Their Main Dietary Sources,” Journal of Agricultural and Food Chemistry, Vol. 54, No. 23, 2006, pp. 7849-8755. doi:10.1021/jf061818s
[20]	F. Granado, B. Olmedilla, C. Herrero and B. Perez-Sacristan, “Bioavailability of Carotenoids and Tocopherols from Broccoli: In Vivo and in Vitro Assessment,” Experimental Biology and Medicine, Vol. 231, 2006, pp. 1733-1738.
[21]	A. Bengtsson, M. Larsson Alminger and U. Svanberg, “In Vitro Bioaccessibility of β Carotene from Heat-Processed Orange-Fleshed Sweet Potato,” Journal of Agricultural and Food Chemistry, Vol. 57, No. 20, 2009, pp. 96939698. doi:10.1021/jf901692r
[22]	A. Bengtsson, C. Brackmann, A. Enejder, M. Larsson Alminger and U. Svanberg,” Effects of Thermal Processing on the in Vitro Bioaccessibility and Microstructure of β-Carotene in Orange-Fleshed Sweet Potato,” Journal of Agricultural and Food Chemistry, Vol. 58, No. 20, 2010, pp. 11090-11096. doi:10.1021/jf1024104
[23]	D. A. Garrett, M. L. Failla, R. J. Sarama and N. Craft, “Accumulation and Retention of Micellar β-Carotene and Lutein by Caco-2 Human Intestinal Cells,” Journal of Nutritional Biochemistry, Vol. 10, No. 10, 1999, pp. 573581. doi:10.1016/S0955-2863(99)00044-3
[24]	A. During, M. Mahmood Hussain, D. W. Morel and E. H. Harrisson, “Carotenoid Uptake and Secretion by Caco-2 Cells: β-Carotene Isomer Selectivity and Carotenoid Interactions,” Journal of Lipid Research, Vol. 43, No. 7, 2002, pp. 1086-1095. doi:10.1194/jlr.M200068-JLR200
[25]	R. Martínez-Tomás, E. Larqué, D. González-Silvera, M. Sánchez-Campillo, M. I. Burgos, A. Wellner, S. Parra, L. Bialek, M. Alminger and F. Pérez-Llamas, “Effect of the Consumption of a Fruit and Vegetable Soup with High in Vitro Carotenoid Accessibility on Serum Carotenoid Concentrations and Markers of Oxidative Stress in Young Men,” European Journal of Nutrition, 2011, pp. 1-9.
[26]	R. Martínez-Tomás, F. Pérez-Llamas, M. SánchezCampillo, D. González-Silvera, A. I. Cascales, M. García-Fernández, J. ángel López-Jiménez, S. Zamora, M. I. Burgos, F. López-Azorín A. Wellner, S. Parra, L. Bialek, M. Alminger and E. Larqué, “Daily Intakes of Fruit and Vegetable Soups Processed in Different Ways Increase Human Serum Carotenoid Responses and Reduced Levels of Several Oxidative Stress Markers,” Food Chemistry, 2012, D-11-02661R.
[27]	G. Sadler and J. Davies, “Rapid Extraction of Lycopene and β-Carotene from Reconstituted Tomato Paste and Pink Grapefruit,” Journal of Food Science, Vol. 55, No. 5, 1990, pp. 1460-1461. doi:10.1111/j.1365-2621.1990.tb03958.x
[28]	C. Svelander, E. Tib?ck, L. Ahrné M. Langton U. Svanberg and M. Alminger, “Processing of Tomato: Impact on in Vitro Bioaccessibility of Lycopene and Textural Properties,” Journal of the Science of Food and Agriculture, Vol. 90, No. 10, 2010, pp. 1665-1672. doi:10.1002/jsfa.4000
[29]	V. Tyssandier, B. Lyan and P. Borel, “Main factors Governing the Transfer of Carotenoids from Emulsion Lipid Droplest to Micells,” Biochimica et Biophysica Acta, Vol. 1533, 2001, pp. 285-292.
[30]	D. A. Garrett, M. L. Failla and R. J. Sarama, “Estimation of Carotenoid Bioavailability from Fresh Stir-Fried Vegetables Using an in Vitro Digestion/Caco-2 Cell Culture Model,” Journal of Nutritional Biochemistry, Vol. 11, No. 11, 2000, pp. 574-580. doi:10.1016/S0955-2863(00)00122-4
[31]	W. Stahl, H. van den Berg, J. Arthur, A. Bast, J. Dainty, R. M. Faulks, C. G?rtner, G. Haenen, P. Hollman, B. Holst, F. J. Kelly, M. C. Polidori, C. Rice-Evans, S. Southon, T. van Vliet, J. Vina-Ribes, G. Williamsson and S. B. Astely, “Bioavailability and Metabolism,” Molecular Aspects of Medicine, Vol. 23, No. 1-3, 2002, pp. 39-100. doi:10.1016/S0098-2997(02)00016-X
[32]	E. A. Tib?ck, C. A. Svelander, I. J. P. Colle, A. I. Altsk?r, M. A. G. Alminger, M. E. G. Hendrickx, L. M. Ahrné and M. I. B. C. Langton, “Mechanical and Thermal Pretreatments of Crushed Tomatoes: Effects on Consistency and in Vitro Accessibility of Lycopene,” Journal of Food Science, Vol. 74, No. 7, 2009, pp. 386-395. doi:10.1111/j.1750-3841.2009.01255.x
[33]	I. Colle, S. van Buggenhout, A. van Loey and M. Hendrickx, “High Pressure Homogenization Followed by Thermal Processing of Tomatopulp: Influence on Microstructure and Lycopene in Vitro Bioaccessibility,” Food Research International, Vol. 43, No. 8, 2010, pp. 21932200. doi:10.1016/j.foodres.2010.07.029
[34]	A. Bengtsson, N. Scheers, T. Andlid, M. Alminger, A. S. Sandberg and U. Svanberg, “Impaired Uptake of BetaCarotene by Caco-2 Human Intestinal Cells in the Presence of Iron,” International Journal of Food Sciences and Nutrition, Vol. 60, No.S5, 2009, pp. 125-135. doi:10.1080/09637480802641270
[35]	T. Huo, M. G. Ferruzzi, S. J. Schwartz and M. L. Failla, “Impact of Fatty Acyl Composition and Quantity of Triglycerides on Bioaccessibility of Dietary Carotenoids,” Journal of Agricultural and Food Chemistry, Vol. 55, No. 22, 2007, pp. 8950-8957. doi:10.1021/jf071687a
[36]	J. D. Bryant, J. D. McCord, L. K. Unlu and J. W. Erdman, “Isolation and Partial Characterization of αand βCarotene-Containing Carotenoprotein from Carrot (Daucus carota L.) Root Chromoplast,” Journal of Agricultural and Food Chemistry, Vol. 40, No. 4, 1992, pp. 545-549. doi:10.1021/jf00016a003
[37]	W. P. Mohr, “Pigment Bodies Found in Fruits of Crimson and High Pigment Lines of Tomatoes,” Annals of Botany, Vol. 44, 1979, pp. 427-434.
[38]	L. Ryan, O. O’Connell, L. O’Sullivan, S. A. Aherne and N. M. O’Brien, “Micellarisation of Carotenoids from Raw and Cooked Vegetables,” Plant Foods for Human Nutrition, Vol. 63, No. 3, 2008, pp. 127-133. doi:10.1007/s11130-008-0081-0
[39]	M. L. Failla, C. Chitchumroonchokchai and B. Ishida, “In Vitro Micellarization and Intestinal Uptake of Cis-Isomers of Lycopene Exceed Those of All-Trans Lycopene,” Journal of Nutrition, Vol. 138, No. 3, 2008, pp. 482-486.
[40]	J. Serrano, I. Goni and F. Saura-Calixto, “Determination of β Carotene and Lutein Available from Green Leafy Vegetables by an in Vitro Digestion and Colonic Fermentation Method,” Journal of Agricultural and Food Chemistry, Vol. 53, No. 8, 2005, pp. 2936-2940. doi:10.1021/jf0480142
[41]	P. Borel, “Factors Affecting Intestinal Absorption of Highly Lipohilic Food Microconstituents (Fat-Soluble Vitamins, Carotenoids and Phytosterols,” Clinical Chemistry and Laboratory Medicine, Vol. 41, No. 8, 2003, pp. 979-994.
[42]	V. Tyssandier, E. Reboul, J. F. Dumas, C. BouteloupDemange, M. Armand, J. Marcand, M. Sallas and P. Borel, “Processing of Vegetable-Born Carotenoids in the Human Stomach and Duodenum,” American Journal of Physiology—Gastrointestinal and Liver Physiology, Vol. 284, 2003, pp. 913-923.
[43]	H. Van den Berg, “Carotenoid Interactions,” Nutrition Reviews, Vol. 57, No. 1, 1999, pp. 1-10. doi:10.1111/j.1753-4887.1999.tb01769.x
[44]	V. Tyssandier, N. Cardinault, C. Caris-Veyrat, M.J. Amiot, P. Grolier, C. Bouteloup, V. Azai-Braesco and P. Borel, “Vegetable-Borne Lutein, Lycopene, and β-Carotene Compete for Incorporation into Chylomicrons with No Adverse Effect on the Medium-Term (3-wk) Plasma Status of Carotenoids in Humans,” American Journal of Clinical Nutrition, Vol. 75, 2002, pp. 526-534.
[45]	K. J. Yeum and R. M. Russell, “Carotenoid Bioavailability and Bioconversion,” Annual Review of Nutrition, Vol. 22, 2002, pp. 483-504. doi:10.1146/annurev.nutr.22.010402.102834
[46]	P. Borel, P. Grolier, N. Mekki, Y. Boirie, Y. Rochette, B. Le Roy, M. C. Alexandre-Gouabou, D. Lairon and V. Azais-Braesco, “Low and High Responders to Pharmacological Doses of Beta-Carotene: Proportion in the Population, Mechanisms Involved and Consequences on Beta-Carotene Metabolism,” Journal of Lipid Research, Vol. 39, No. 11, 1998, pp. 2250-2260.
[47]	M. E. O’Neill and D. I. Thurnham, “Intestinal Absorption of β-Carotene, Lycopene and Lutein in Men and Women Following a Standard Meal: Response Curves in Triacylglycerol-Rich Lipoprotein Fraction,” British Journal of Nutrition, Vol. 79, No. 2, 1998, pp. 149-159. doi:10.1079/BJN19980026