Provitamin a carotenoid bioavailability: What really matters?

International Journal for Vitamin and Nutrition Research

Volumn 80, Issue 4-5, 2010, Pages 336-350

  Tanumihardjo, Sherry A ^a   Palacios, Natalia ^b   Pixley, Kevin V ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

Author keywords

Bioavailability; Biofortification; Cassava; Maize; Provitamin A carotenoids; Rice

Indexed keywords

ALPHA CAROTENE; BETA CAROTENE; CARBOHYDRATE; CAROTENOID; RETINOL;

AGRICULTURE; ARTICLE; BANANA; BIOAVAILABILITY; BIOTRANSFORMATION; CASSAVA; DIETARY FIBER; HEALTH PROMOTION; HUMAN; HUNGER; MAIZE; MATERNAL WELFARE; MORTALITY; NUTRITION EDUCATION; RICE; SCALE UP; SWEET POTATO; VEGETABLE;

BIOLOGICAL AVAILABILITY; CAROTENOIDS; FOOD, FORTIFIED; HUMANS; INTESTINAL ABSORPTION; MANIHOT; ORYZA SATIVA; VITAMIN A; ZEA MAYS;

IPOMOEA BATATAS; MANIHOT ESCULENTA; ZEA MAYS;

EID: 79953785371     PISSN: 03009831     EISSN: None     Source Type: Journal    
DOI: 10.1024/0300-9831/a000042     Document Type: Article

References (87)

1. WHO (World Health Organization). (1995) Vitamin A deficiency and its consequences: a fi eld guide to detection and control (third edition). Available: http://www.who.int/nutrition/publications/micronutrients/vitamin_a_deficieny/9241544783/en/index.html. Accessed November 2010.
2. Sun, T., Surles, R.L. and Tanumihardjo, S.A. (2008) Vitamin A concentrations in piglet extrahepatic tissues respond differently 10 d after vitamin A treatment. J. Nutr. 138, 1101 - 1106.
3. Penniston, K.L. and Tanumihardjo, S.A. (2001) Subtoxic hepatic vitamin A concentrations in captive rhesus monkeys ( Macaca mulatta ). J. Nutr. 131, 2904 - 2909.
4. Tanumihardjo, S.A., Anderson, C., Kaufer-Horwitz, M., Bode, L., Emenaker, N.J., Haqq, A.M., Satia, J.A., Silver, H.J. and Stadler, D.D. (2007) Poverty, obesity and malnutrition: an international perspective recognizing the paradox. J. Am. Diet. Assn. 107, 1966 - 1972.
5. Tanumihardjo, S.A. (2008) Food-based approaches for ensuring adequate vitamin A nutrition. Comp. Rev. Food Sci. Food Safety 7, 373 - 381.
6. Tanumihardjo, S.A., Bouis, H., Hotz, C., Meenakshi, J.V. and McClafferty, B. (2008) Biofortification of staple crops: An emerging strategy to combat hidden hunger. Comp. Rev. Food Sci. Food Safety 7, 329 - 334.
7. De Pee, S. and West, C.E. (1996) Dietary carotenoids and their role in combating vitamin A deficency: a review of the literature. Eur. J. Clin. Nutr. 50 (Suppl.3), S38 - 53.
8. Castenmiller, J.J.M. and West, C.E. (1998) Bioavailability and bioconversion of carotenoids. Annu. Rev. Nutr. 18, 19 - 38.
9. Furr, H.C., Green, M., Haskell, M., Mokhtar, N., Nestel, P., Newton, S., Ribaya-Mercado, J., Tang, G., Tanumihardjo, S.A. and Wasantwisut E. (2005) Stable isotope dilution techniques for assessing vitamin A status and bioefficacy of provitamin A carotenoids in humans. Public Health Nutr. 8, 596 - 607.
10. de Pee, S., West, C.E., Muhilal, Karyadi, D. and Hautvast, J.G. (1995) Lack of improvement in vitamin A status with increased consumption of dark-green leafy vegetables. Lancet 346, 75 - 81.
11. Parker, R.S. (1996) Absorption, metabolism, and transport of carotenoids. FASEB J. 10, 542 - 551.
12. Canfield, L.M., Fritz, T.A. and Tarara, T.E. (1990) Incorporation of β-carotene into mixed micelles. Methods Enzymol. 189, 418 - 422.
13. Tanumihardjo, S.A. (2002) Factors influencing the conversion of carotenoids to retinol: Bioavailability to bioconversion to bioefficacy. Int. J. Vitam. Nutr. Res. 72, 40 - 45.
14. Van Lieshout, M., West, C.E., Muhilal, Permaesih, D., Wang T., Xu, X. van Breemen, R.B., Creemers, A.F.L., Verhoeven, M.A. and Lugtenburg, J. (2001) Bioefficacy of β-carotene dissolved in oil studied in children in Indonesia. Am. J. Clin. Nutr. 73, 949 - 958.
15. De Pee, S., West, C.E., Permaesih, D., Martuti, S., Muhilal and Hautvast, J.G.A.J. (1998) Orange fruit is more effective than are dark-green leafy vegetables in increasing serum concentrations of retinol and β-carotene in schoolchildren in Indonesia. Am. J. Clin. Nutr. 68: 1058 - 1067.
16. th edition. National Academy Press, Washington, D.C.
17. Institute of Medicine. (2001) Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. pp. 65 - 126, National Academy Press, Washington, D.C.
18. FAO (Food and Agricultural Organization of the United Nations). (2001) Chapter 7: Vitamin A. In: Human vitamin and mineral requirements. Available: ftp://ftp.fao.org/docrep/fao/004/y2809e/y2809e07.pdf. Accessed November 9, 2010.
19. Li, S., Nugroho, A., Rocheford, T. and White, W.S. (2010) Vitamin A equivalence of the β-carotene in β-carotene biofortified maize porridge consumed by women. Am. J. Clin. Nutr. 92, 1105 - 1112.
20. Bouis, H.E. (2002) Plant breeding: a new tool for fighting micronutrient malnutrition. J. Nutr. 132, 491S-494S.
21. Hirschi, K.D. (2009) Nutrient biofortification of food crops. Annu. Rev. Nutr. 29, 401 - 421.
22. Meenakshi, J.V. (2009) Best practice paper: Cost-effectiveness of biofortification. Copenhagen Consensus Center, Frederiksberg, Denmark. www.copenhagenconsensus.com.
23. Pfeiffer, W.H. and McClafferty, B. (2007) HarvestPlus: Breeding crops for better nutrition. Crop Sci. 47, S88-S105.
24. Tanumihardjo, S.A. and Howe, J.A. (2005) Twice the amount of α-carotene isolated from carrots is as effective as β-carotene in maintaining the vitamin A status of Mongolian gerbils. J. Nutr. 135, 2622 - 2626.
25. Davis, C.R., Jing, H., Howe, J.A., Rocheford, T.R. and Tanumihardjo, S.A. (2008) β-Cryptoxanthin from supplements or carotenoid enhanced maize maintains liver vitamin A in Mongolian gerbils ( Meriones unguiculatus ) better than or equal to β-carotene supplements. Br. J. Nutr. 100, 786 - 793.
26. Davis, C.R., Howe, J.A., Rocheford, T.R. and Tanumihardjo, S.A. (2008) The xanthophyll composition of biofortified maize ( Zea mays sp.) does not influence the bioefficacy of provitamin A carotenoids in Mongolian gerbils ( Meriones unguiculatus ). J. Agric. Food Chem. 56, 6745 - 6750.
27. Howe, J.A. and Tanumihardjo, S.A. (2006) Carotenoid-biofortifi ed maize maintains adequate vitamin A status in Mongolian gerbils. J. Nutr. 136, 2562 - 2567.
28. Muzhingi, T., Tang, G., Siwela, A., Gadaga, H.T. and Grusak, M. (2010) Vitamin A value of high beta-carotene yellow maize in humans. FASEB J. 24, 103.1.
29. Thakkar, S.K. and Failla, M.L. (2008) Bioaccessibility of pro-vitamin A carotenoids is minimally affected by non pro-vitamin A xanthophylls in maize (Zea mays sp.). J. Agric. Food Chem. 56, 11441 - 11446.
30. Howe, J.A., Maziya-Dixon, B. and Tanumihardjo, S.A. (2009) Cassava with enhanced β-carotene maintains adequate vitamin A status in Mongolian gerbils (Meriones unguiculatus) despite substantial cis-isomer content. Br. J. Nutr. 102, 342 - 349.
31. Deming, D.M., Teixeira, S.R. and Erdman, J.W. Jr. (2002) All-trans β-carotene appears to be more bioavailable than 9-cis or 13-cis β -carotene in gerbils given single oral doses of each isomer. J. Nutr. 132, 2700 - 2708.
32. Deming, D.M., Baker, D.H. and Erdman, J.W. Jr. (2002) The relative vitamin A value of 9-cis β-carotene is less and that of 13-cis β-carotene may be greater than the accepted 50 % that of all-trans β-carotene in gerbils. J. Nutr. 132, 2709 - 2712.
33. Bresnahan, K., Davis, C.R. and Tanumihardjo, S.A. (2011) The relative vitamin A value of 9-cis-and 13-cis-β-carotene did not differ in vitamin A-depleted Mongolian gerbils ( Meriones unguicalatus). FASEB J. (In press).
34. Leitz, G., Lange, J. and Rimbach, G. (2010) Molecular and dietary regulation for β, β-carotene 15, 15'-monooxygenase 1 (BCMO1). Arch. Biochem. Biophys. 502, 8 - 16.
35. Ribaya-Mercado, J.D., Solon, F.S., Solon, M.A., Cabal-Barza, M.A., Perfecto, C.S., Tang, G., Solon, J.A.A., Fjeld, C.R. and Russell, R.M. (2000) Bioconversion of plant carotenoids to vitamin A in Filipino school-aged children varies inversely with vitamin A status. Am. J. Clin. Nutr. 72, 455 - 465.
36. Ribaya-Mercado, J.D., Solomons, N.W., Medrano, Y., Bulux, J., Dolnikowski, G.G., Russell, R.M. and Wallace, C.B. (2004) Use of the deuterated-retinol-dilution technique to monitor the vitamin A status of Nicaraguan schoolchildren 1 y after initiation of the Nicaraguan national program of sugar fortification with vitamin A. Am. J. Clin. Nutr. 80, 1291 - 1298.
37. Suharno, D., West, C.E., Muhilal, Karyadi, D. and Hautvast, J.G. (1993) Supplementation with vitamin A and iron for nutritional anaemia in pregnant women in West Java, Indonesia. Lancet 342, 1325 - 1328.
38. Ahmed, F., Khan, M.R. and Jackson, A.A. (2001) Concomitant supplemental vitamin A enhances the response to weekly supplemental iron and folic acid in anemic teenagers in urban Bangladesh. Am. J. Clin. Nutr. 74, 108 - 115.
39. Muslimatun, S., Schmidt, M.K., Schultink, W., West, C.E., Hautvast, J.A., Gross, R. and Muhilal (2001) Weekly supplementation with iron and vitamin A during pregnancy increases hemoglobin concentration but decreases serum ferritin concentration in Indonesian pregnant women. J. Nutr. 131, 85 - 90.
40. Tanumihardjo, S.A. (2002) Vitamin A and iron status are improved with vitamin A and iron supplementation in pregnant Indonesian women. J. Nutr. 132, 1909 - 1912.
41. Semba, R.D. and Bloem, M.W. (2002) The anemia of vitamin A deficiency: epidemiology and pathogenesis. Eur. J. Clin. Nutr. 56, 271 - 281.
42. Dijkhuizen, M.A., Wieringa, F.T., West, C.E. and Muhilal (2004) Zinc plus β-carotene supplementation of pregnant women is superior to β-carotene supplementation alone in improving vitamin A status in both mothers and infants. Am. J. Clin. Nutr. 80, 1299 - 1307.
43. Christian, P. and West, K.P., Jr. (1998) Interactions between zinc and vitamin A: an update. Am. J. Clin. Nutr. 68, 435S-441S.
44. Sundaresan, P.R., Cope, F.O. and Smith, J.C., Jr. (1977) Influence of zinc deficiency on retinal reductase and oxidase activities in rat liver and testes. J. Nutr. 107, 2189 - 2197.
45. Ribaya-Mercado, J.D., Maramag, C.C., Tengco, L.W., Dolnikowski, G.G., Blumberg, J.B. and Solon, F.S. (2007) Carotene-rich plant foods ingested with minimal dietary fat enhance the total-body vitamin A pool size in Filipino schoolchildren as assessed by stable-isotope-dilution methodology. Am. J. Clin. Nutr. 85, 1041 - 1049.
46. Mills, J.P., Tumuhimbise, G., Jamil, K.M., Thakkar, S., Failla, M.L. and Tanumihardjo, S.A. (2009) Sweet potato β-carotene bioefficacy is enhanced by dietary fat and not reduced by soluble fi ber intake in Mongolian gerbils. J. Nutr. 139, 44 - 50.
47. Chitchumroonchokchai, C., Failla, M.L., Ferruzzi, M.G. and Campbell, W.W. (2010) Dietary fats with increased ratio of unsaturated to saturated fatty acids enhance absorption of carotenoid and vitamin E by increasing both efficiency of micellarization and lipoprotein secretion. FASEB J. 24, 539.3.
48. Porter Dosti, M., Mills, J.P., Simon, P.W. and Tanumihardjo, S.A. (2006) Bioavailability of β-carotene (βC) from purple carrots is the same as typical orange carrots while high-βC carrots increase βC stores in Mongolian gerbils ( Meriones unguiculatus ). Br. J. Nutr. 96, 258 - 267.
49. USDA National Nutrient Database for standard reference. Available: http://www.nal.usda.gov/fnic/foodcomp/search/. Accessed November 19, 2010.
50. Liu, W., Zhou, Y., Sanchez, T., Ceballos, H., and White, W.S. (2010) The vitamin A equivalence of β-carotene in β-carotene-biofortifi ed cassava ingested by women. FASEB J. 24, 92.7.
51. Tang, G., Qin, J., Dolnikowski, G.G., Russell, R.M. and Grusak, M.A. (2009) Golden Rice is an effective source of vitamin A. Am. J. Clin. Nutr. 89, 1776 - 1783.
52. Tang, G., Yin, S.-A., Wang, Y., Grusak, M. and Russell, R. (2010) Provitamin A from Golden Rice is as effective as provitamin A in oil to children. FASEB J. 24, 537.24.
53. Haskell, M.J., Jamil, K.M., Hassan, F., Peerson, J.M., Hossain, M.I., Fuchs, G.J. and Brown, K.H. (2004) Daily consumption of Indian spinach ( Basella alba) or sweet potatoes has a positive effect on total-body vitamin A stores in Bangladeshi men. Am. J. Clin. Nutr. 80, 705 - 714.
54. van Jaarsveld, P.J., Faber, M., Tanumihardjo, S.A., Nestel, P., Lombard, C.J. and Benade, A.J. (2005) β-Carotene-rich orange-fleshed sweet potato improves the vitamin A status of primary school children assessed with the modified-relative-dose-response test. Am. J. Clin. Nutr. 81, 1080 - 1087.
55. Low, J.W., Arimond, M., Osman, N., Cunguara, B., Zano, F. and Tschirley, D. (2007) A food-based approach introducing orange-fleshed sweet potatoes increased vitamin A intake and serum retinol concentrations in young children in rural Mozambique. J. Nutr. 137,1320 - 1327.
56. Low, J.W. and van Jaarsveld, P.J. (2008) The potential contribution of bread buns fortified with beta-carotene-rich sweet potato in Central Mozambique. Food Nutr. Bull. 29, 98 - 107.
57. Paine, J.A., Shipton, C.A., Chaggar, S., Howells, R.M., Kennedy, M.J., Vernon, G., Wright, S.Y., Hinchliffe, E., Adams, J.L., Silverstone, A.L. and Drake, R. (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat. Biotechnol. 23, 482 - 487.
58. Arscott, S.A., Howe, J.A., Davis, C.R. and Tanumihardjo, S.A. (2010) Carotenoid profiles in provitamin A-containing fruits and vegetables affect the bioefficacy in Mongolian gerbils. Exp. Biol. Med. (Maywood). 235, 839 - 848.
59. Davey, M.W., Garming, H., Ekesa, B., Roux, N. and Van den Bergh, I. (2007) Exploiting banana biodiversity to reduce vitamin A deficiency related illness: a fast and cost-effective strategy. J. Agric. Food Chem. 55, 2633 - 2644.
60. Bresnahan, K., Arscott, S.A. and Tanumihardjo, S.A. (2011) Vitamin A bioefficacy of traditional and provitamin A-biofortified banana. FASEB J. (In press).
61. Ejoh, R.A., Dever, J.T., Mills, J.P. and Tanumihardjo, S.A. (2010) Small quantities of carotenoid-rich tropical green leafy-vegetables indigenous to Africa maintain vitamin A status in Mongolian gerbils ( Meriones unguiculatus ). Br. J. Nutr. 103, 1594 - 1601.
62. Tanumihardjo, S.A. (2001) Can lack of improvement in vitamin A status indicators be explained by little or no overall change in vitamin A status of humans? J. Nutr. 131, 3316 - 3318.
63. Tang, G., Gu, X., Hu, S., Xu, Q.-M., Qin, J., Dolnikowski, G.G., Fjeld, C.R., Gao, X., Russell, R.M. and Yin, S.-A. (1999) Green and yellow vegetables can maintain body stores of vitamin A in Chinese children. Am. J. Clin. Nutr. 70, 1069 - 1076.
64. Kang, W. and Kudsk, K.A. (2007) Is there evidence that the gut contributes to mucosal immunity in humans? J. Parenter. Enteral. Nutr. 31, 246 - 258.
65. Latham, M. (2010) The great vitamin A fi asco. World Nutr. 1, 12 - 45.
66. Beaton, G.H., Martorell, R. and L'Abbé, K.A. (1993) Effectiveness of vitamin A supplementation in the control of young child morbidity and mortality in developing countries: Summary report. University of Toronto, Toronto, Canada.
67. Neidecker-Gonzales, O., Nestel, P. and Bouis, H. (2007) Estimating the global costs of vitamin A capsule supplementation: A review of the literature. Food Nutr. Bull. 28, 307 - 316.
68. Mills, J.P., Simon, P.W. and Tanumihardjo, S.A. (2008) Biofortified carrot intake enhances liver antioxidant capacity and vitamin A status in Mongolian gerbils. J. Nutr. 138, 1692 - 1698.
69. MyPyramid.gov [homepage on the Internet]. Washington, D.C.: United States Department of Agriculture Center for Nutrition Policy and Promotion [released 2005 Apr]. Available from: http://www.mypyramid.gov/.
70. Tanumihardjo, S.A., Valentine, A.R., Zhang, Z., Whigham, L.D., Lai, H.J. and Atkinson, R.L. (2009) Strategies to increase vegetable or reduce energy and fat intake induce weight loss in adults. Exp. Biol. Med. 234, 542 - 552.
71. Welch, R. M. (2002) Breeding strategies for biofortified staple plant foods to reduce micronutrient malnutrition globally. J. Nutr. 132, 495S-499S.
72. United Nations Department of Economic and Social Affairs. The Millennium Development Goals Report. New York, 2006.
73. United Nations Department of Economic and Social Affairs. The Millennium Development Goals Report. New York, 2010.
74. World Bank. The World Development Report 2008: Agriculture for Development. World Bank, Washington, D.C., 2008.
75. Spielman, D.J. and Pandya-Lorch, R. (2009) Millions fed: Proven successes in agricultural development. International Food Policy Research Institute, Washington, D.C.
76. Welch, R.M. and Graham, R.D. (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 55, 353 - 364.
77. Nuss, E.T. and Tanumihardjo, S.A. (2010) Maize: A paramount staple crop in the context of global nutrition. Comp. Rev. Food Sci. Food Saf. 9, 417 - 436.
78. Harvest Plus. (2007) Biofortified maize crops for better nutrition. Retrieved July, 2010 from http://crop.scijournals.org/cgi/reprint/47/Supplement_3/S-88.
79. Thakkar, S.K. and Failla, M.L. (2008) Bioaccessibility of pro-vitamin A carotenoids is minimally affected by non pro-vitamin A xanthophylls in maize (Zea mays sp.). J. Agric. Food Chem. 56, 11441 - 11446.
80. Kean, E.G., Hamaker, B.R. and Ferruzzi, M.G. (2008) Carotenoid bioaccessibility from whole grain and degermed maize meal products. J. Agric. Food Chem. 56, 9918 - 9926.
81. Li, S., Tayie, F.A.K., Young, M.F., Rocheford, T. and White, W.S. (2007) Retention of provitamin A carotenoids in high-β-carotene maize (Zea mays) during traditional African household processing. J. Agric. Food Chem. 55, 10744 - 10750.
82. Nuss, E.T., Arscott, S.A., Bresnahan, K., Pixley, K.V., Rocheford, T., Hotz, C., Siamusantu, W., Chileshe, J. and Tanumihardjo, S.A. (2011) Adaptation to and intake patterns of traditional foods made from biofortified orange maize (Zea mays) in rural Zambian children. FASEB J. (In press).
83. Horton, S., Shekar, M., McDonald, C., Mahal, A. and Brooks, J.K. (2010) Scaling up nutrition: What will it cost? The World Bank: Washington, D.C.
84. Hawkes, C. and Ruel, M. (2006) Understanding the links between agriculture and health. IFPRI 2020 vision focus briefs.
85. Mills, J.P., Terasawa, E. and Tanumihardjo, S.A. (2007) Excessive preformed vitamin A intake by mothers amplifies early fetal liver retinylester storage in captive Old World monkeys. Comp. Med. 57, 505 - 511.
86. Allen, L.H. and Haskell, M. (2002) Estimating the potential for vitamin A toxicity in women and young children. J. Nutr. 132, 2907S-2919S.
87. Myhre, A.M., Carlsen, M.H., Bohn, S.K., Wold, H.L., Laake, P. and Blomhoff, R. (2003) Water-miscible, emulsified, and solid forms of retinol supplements are more toxic than oil-based preparations. Am. J. Clin. Nutr. 78, 1152 - 1159.