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2
*
Division of Human Nutrition and Epidemiology, Wageningen University, Wageningen, The Netherlands and
Department of Gastroenterology, University Medical Centre Nijmegen, Nijmegen, The Netherlands
2To whom correspondence should be addressed. E-mail: clive.west{at}staff.nutepi.wau.nl.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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KEY WORDS: • vitamin A • vitamin A deficiency • carotenoids • bioavailability • bioefficacy
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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Background |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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), wrote in 1978, with respect to vitamin A capsules, that "the whole procedure of vitamin distribution would be wholly superfluous if adequate carotene were present in the children’s diet" (2
). He assumed that 30 g of dark-green leafy vegetables was sufficient to meet the vitamin A requirements of a child. This assumption was based on the 1967 Food and Agriculture Organization (FAO)3
/World Health Organization (WHO) recommendation (3
) that 6 µg of ß-carotene has the same vitamin A activity as 1 µg of retinol. This recommendation remained unchanged in the 1988 revision (4
). The amount of vitamin A or provitamin A having the same vitamin A activity as 1 µg of retinol is referred to in the FAO/WHO recommendations as 1 retinol equivalent (RE). This is equivalent to 1 µg of retinol, 6 µg of ß-carotene or 12 µg of other provitamin A carotenoids such as 
-carotene and ß-cryptoxanthin.
We became suspicious of this hard-held belief. We saw that pregnant Indonesian women had intakes of provitamin A that would have been expected to supply about three times the recommended daily allowance of vitamin A. Nevertheless, a high proportion of them had marginal vitamin A deficiency (5
). One possible explanation was that early methods of measuring the provitamin A content of plant foods, based on measuring the optical extinction of an extract at 450 nm, overestimated vitamin A content (6
). Even so, the vitamin A intake of the women still should have been sufficient to maintain adequate vitamin A status (serum retinol concentrations >1.05 µmol/L) (5
). To clarify the situation, we compared the effect of feeding a daily supplement of stir-fried vegetables containing 3.7 mg of ß-carotene with a chocolate wafer containing a similar amount of ß-carotene in an oil matrix (7
). A third group of women received a wafer that contained no additional ß-carotene (Table 1
). The additional daily portion of dark-green leafy vegetables did not improve vitamin A status, as measured by retinol concentrations in serum and in breast milk, whereas the identical amount of ß-carotene in the oil matrix of the chocolate-coated wafer dramatically improved vitamin A status. A review of the literature reveals that many studies purporting to show that dark-green leafy vegetables improve vitamin A status were based on faulty designs (17
). Others have demonstrated that ß-carotene from vegetables has low bioavailability. Micozzi et al. (8
), for example, reported in 1992 that the bioavailability of ß-carotene from broccoli and carrots, as measured by ß-carotene response, was 12 and 18%, respectively, which at a 1:2 bioconversion means it yields only 6–9% RE on an equimolar basis.
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Definitions |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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). Bioavailability is the fraction of an ingested nutrient available for use in normal physiologic functions and storage (16
), and bioconversion is the fraction of a bioavailable nutrient (absorbed provitamin A carotenoid) converted to the active form of the nutrient (retinol). Bioefficacy is the efficiency with which ingested nutrients (dietary provitamin A carotenoids) are absorbed and converted to the active form of the nutrient (retinol). Most of this conversion takes place in the intestinal mucosa but occurs in other tissues such as the liver. Thus, bioefficacy is a product of bioavailability and bioconversion: often it is referred to as bioconversion. To address the biological activity of dietary components, the term functional bioefficacy has been introduced (19
). Functional bioefficacy is the proportion of an ingested nutrient that carries out a given metabolic function, such as the ability of ingested ß-carotene to reverse or prevent abnormal dark adaptation. |
Bioefficacy of ß-carotene in oil |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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). The most quoted early study is the Sheffield experiment, carried out during World War II, in which the amount of ß-carotene in oil required to reverse and prevent abnormal dark adaptation was compared with the amount of retinol to carry out the same functions. For the reversal of abnormal dark adaptation the functional bioefficacy was 1:3.8, whereas for preventing abnormal dark adaptation the value was 1:4 (22
). Based on prevention and reversal of dark adaptation, a value of 1:3.5 had been reported earlier by Booher et al. (20
) in the United States and a value of 1:4 was reported by Wagner (21
) in Germany (Table 2)
. In 1974 a value of 1:2 was reported by Sauberlich et al. (23
) in a study on reversing abnormal dark adaptation (Table 2)
. Based on studies in 112 children in Indonesia using retinol and ß-carotene labeled with 13C, van Lieshout et al. (15
,18
) reported a value of 1:2.6 (Table 2)
.
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Bioefficacy and bioavailability of ß-carotene in fruits and vegetables |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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) and breast-feeding women in Vietnam (11
) (Table 1)
. In each study there were four dietary groups: low-retinol, low-carotenoid diet (negative control); dark-green leafy vegetables (as well as carrots in the Indonesian study); yellow and orange fruits; and a retinol-containing diet (positive control). For dark-green leafy vegetables, the bioefficacy was 1:26 and 1:28; while for fruit, the bioefficacy was 1:12. This suggests that, with a mixture of vegetables and fruits in a ratio of 4:1, which is typical for both developing and developed countries, the bioefficacy of ß-carotene from a mixed diet is 1:21. Chinese children aged 5–6.5 y yielded similar results for green and yellow vegetables (1:27) (14
). Van Lieshout et al. (15
), using the plateau isotopic enrichment method, also found relatively poor bioefficacy of ß-carotene in dark-green leafy vegetables. ß-Carotene in pumpkin was 1.7 times as potent as that in spinach (Table 1)
.
A number of studies in developed countries have examined the bioavailability of ß-carotene from individual vegetables (Table 1)
. The bioavailability of ß-carotene in raw carrots was 26% of that of ß-carotene in oil (9
). However, in carrot juice, in which the structure of the carrot is destroyed, the bioavailability was nearly twice as high, 45%. Castenmiller et al. (12
) reported that the bioavailability of ß-carotene in whole spinach was 5% that of ß-carotene in oil and that breaking down the structure of the spinach by treating it with a mixture of cellulases and pectinases could increase the bioavailability to 9%. These studies (9
,12
) demonstrate that the matrix plays an important role in determining carotene bioavailability and hence bioefficacy.
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IOM recommendations on bioefficacy |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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). In fact, for the bioefficacy of ß-carotene from oil (Table 2)
, they drew only on the functional bioefficacy study of Sauberlich et al. (23
), which is at variance with the other functional bioefficacy studies (Table 2)
. They did not quote the papers by Booher et al. (20
) and Wagner (21
). In addition, when IOM recommendations were first released, they assumed Hume and Krebs (22
) had reported that 2 µg of ß-carotene had the same activity as 1 µg of retinol based on 1 international unit (IU) of retinol and of ß-carotene both being 0.3 µg. This resulted in values similar to those reported by Sauberlich et al. (23
) instead of values similar to those of Booher et al. (20
) and Wagner (21
) (Table 2)
. It would be interesting to know whether IOM (25
) would have proposed a bioefficacy of ß-carotene in oil of 1:2 if they were aware of this information. For the bioavailability of ß-carotene from mixed fruit and vegetables, IOM used the value of Van het Hof et al. (13
) of 14% (i.e., 1:7) and adjusted it to 1:6 because of the low content of fruit in the mixed diet used in that study. Thus, the bioefficacy of ß-carotene in a mixed fruit and vegetable diet was calculated from the product of 1:2 (bioefficacy in oil) and 1:6 (relative bioavailability of ß-carotene in plant sources related to that in oil)—that is, 1:12 (Fig. 1
). For other provitamin A carotenoids, the bioefficacy has been set at half that value. As indicated in Figure 1
, IOM has introduced a new term, retinol activity equivalent (RAE), to express the activity of carotenoids in terms of vitamin A (25
). For a given amount of provitamin A in a mixed diet, IOM estimates that the number of RAE is half the number of RE suggested by FAO/WHO (4
). Until now, there have been no published studies in developed countries estimating the bioefficacy of ß-carotene from a vegetable diet by comparing the serum retinol response to that obtained when a retinol-rich diet is fed or by using stable isotope techniques. Thus, it may well be that the bioefficacy of ß-carotene from a vegetable diet in developed countries approximates the value of 1:21 reported from developing countries (10
,11
). In contrast, it has been speculated that the low bioefficacy of ß-carotene from a vegetable diet in individuals in developing countries may be attributable to them being generally less healthy and more malnourished than people in developed countries.
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Factors that affect bioavailability and bioefficacy |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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,26
): Species of carotenoid, molecular Linkage; Amount of carotene consumed in a meal; Matrix in which the carotenoid is incorporated; Effectors of absorption and bioconversion; Nutrient status of the host; genetic factors; Host-related factors; and Interactions between the other factors. As mentioned above, the most important of these influencing bioavailability is the food matrix (factor M). Because disrupting the food matrix has been shown to increase bioavailability (9
,12
,26
,27
), such disruption is expected to increase bioefficacy. However, reported increases in the bioavailability of ß-carotene generally have been on the order of 50%, which may mean the bioefficacy of ß-carotene in dark-green leafy vegetables cannot be increased sufficiently to meet dietary requirements. The amount of dietary fat required to ensure maximum carotenoid absorption (included under factor E) appears to be quite low, 3–5 g per meal (26
). Most populations, except perhaps some in South Asia, generally have fat intakes during meals that are above this value. |
Implications of the new bioefficacy factors for estimating vitamin A supply to populations in developing and developed countries |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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). With the RE proposed by FAO/WHO used as a measure of bioefficacy, populations in all regions of the world should be able to meet their required level of intake of 600 RE (4
). However, if RAE, as suggested by the recent IOM report for healthy populations (Fig. 1)
(25
), are used to calculate effective vitamin A supply, populations in Asia, South America and Africa will not be able to meet their vitamin A requirements. Even these estimates may be overly optimistic. As mentioned above, the bioefficacy of ß-carotene in a mixed vegetable diet measured in Indonesia and Vietnam was 1:21. This produces even lower estimates of the effective vitamin A supply (28
). In Asia, for example, the effective vitamin A supply would be only 40% of the FAO/WHO estimates for a safe level of intake.
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). Data on vitamin A intake calculated from estimates of food intake over a longer period of time are available from Indonesia and Great Britain for women of reproductive age and for children under 5 y of age (Tables 4
and 5
, respectively). Regardless of which bioefficacy factor is used, the median vitamin A intake of both women and children in South Kalimantan is lower than the dietary reference intake. The situation is somewhat better in South Sulawesi but, when the bioefficacy of ß-carotene is lowered from 1:6 to 1:12 (IOM estimate for well nourished, healthy children), the dietary reference intake for vitamin A is not met. The situation is even worse when a less favorable, but more realistic with respect to developing countries, bioefficacy factor is used. Even in the United Kingdom, the vitamin A intake of women falls short of the dietary reference intake when the bioefficacy of ß-carotene is set at 1:12. This may explain the low concentrations of serum retinol in the United Kingdom as presented by de Pee and Dary (33
). Median vitamin A intake of women in The Netherlands, based on 2-d food records and a bioefficacy of ß-carotene of 1:12, is about one-third higher (920 RAE) than the values presented for women in the United Kingdom. In this regard, it may be important that the vitamin A intake of Dutch women (Table 6
) comes predominantly from milk (including dairy products), meat and the synthetic vitamin A added to spreadable fats such as margarine. Consumption of milk and spreadable fats is higher in The Netherlands than in the United Kingdom. The situation for 4-y-old children in the United Kingdom is somewhat better than for Indonesian children <5 y old (Table 5)
. The median intake almost meets the dietary reference intake regardless of which bioefficacy factor is used. The intake of preformed vitamin A from food in 4-y-old children has fallen by more than half since 1950, mainly because of the lower consumption of milk (including milk products) and meat (32
). Thus, the increasing trend to use vitamin supplements and fortified foods in developed countries may be important for retaining vitamin A adequacy. Currently, reliable data on the contribution of synthetic vitamin A, especially in supplements, to vitamin A intake in developed countries are difficult to find.
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Options for controlling vitamin A deficiency |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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). The effective supply of vitamin A depends on the amount of food consumed, the amount of vitamin A and provitamin A in the food, the bioavailability of retinol and the bioefficacy of provitamin A.
Thus, what are the possibilities and limitations of food-based approaches in developing countries for controlling vitamin A deficiency? The amount of food consumed depends not only on its being accessible but also on appetite, which can be increased by controlling infection (36
) and improving zinc status (37
). Increasing the consumption of foods rich in vitamin A or provitamin A can be based on choosing foods that are naturally rich in those nutrients, including breast milk, fortified foods and genetically modified foods. The problem with many naturally rich foods, such as dark-green leafy vegetables, is the low bioavailability of provitamin A. It seems to be difficult to increase the bioavailability of ß-carotene in such foods. Animal products, including milk and dairy products, are rich in vitamin A of high bioavailability but often are too expensive for poor people in developing countries. This is why there is increased emphasis on foods fortified with vitamin A as discussed by Dary and Mora (38
). In the future, genetically modified foods such as golden rice (39
) may play a useful role. However, more developmental work and testing is required before they provide significant relief, especially among those who consume such foods.
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Conclusions and recommendations |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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FOOTNOTES |
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3 Abbreviations used: FAO, Food and Agriculture Organization; IOM, U.S. Institute of Medicine; IU, international unit; RAE, retinol activity equivalent; RE, retinol equivalent; WHO, World Health Organization.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONBackgroundDefinitionsBioefficacy of ß...Bioefficacy and bioavailability...IOM recommendations on...Factors that affect...Implications of the new...Options for controlling vitamin...Conclusions and recommendationsLITERATURE CITED |
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1. Oomen, H. P., McLaren, D. S. & Escapini, H. (1964) Epidemiology and public health aspects of hypovitaminosis A: a global survey on xerophthalmia. Trop. Geogr. Med. 4:271-315.
2. Oomen, H. A. & Grubben, G. J. (1978) Tropical Leaf Vegetables in Human Nutrition 2nd ed. 1978 Koninklijk Instituut voor de Tropen Amsterdam. .
3. FAO/WHO (1967) Requirements of vitamin A, thiamin, riboflavin and niacin. FAO Food and Nutrition Series No. 8: FAO, Rome. WHO Technical Report Series No. 362 1967 WHO Geneva, Switzerland. .
4. FAO/WHO Joint Expert Consultation (1988) Requirements of vitamin A, iron, folate and vitamin B12. FAO Food and Nutrition Series No. 23 1988 FAO Rome, Italy. .
5. Suharno, D., West, C. E., Muhilal, , Karyadi, D. & Hautvast, J. G. A. J. (1994) Vitamin A and iron intake and status of anaemic pregnant women in West Java, Indonesia. Suharno, D. eds. The Role of Vitamin A in Nutritional Anaemia: A Study in Pregnant Women in West Java, Indonesia 1994:57-85 Wageningen Agricultural University Wageningen, The Netherlands. Thesis.
6. West, C. E. & Poortvliet, E. J. (1993) The Carotenoid Content of Foods with Special Reference to Developing Countries 1993 U.S. Agency for International Development-VITAL Washington, DC. .
7. De Pee, S., West, C. E., Muhilal, , Karyadi, D. & Hautvast, J. G. A. J. (1995) Lack of improvement in vitamin A status with increased consumption of dark-green leafy vegetables. Lancet 346:75-81.[Medline]
8. Micozzi, M. S., Brown, E. D., Edwards, B. K., Bieri, J. G., Taylor, P. R., Khachik, F., Beecher, G. R. & Smith, J. C., Jr. (1992) Plasma carotenoid response to chronic intake of selected foods and ß-carotene supplements in men. Am. J. Clin. Nutr. 55:1120-1125.
9. Törrönen, R., Lehmusaho, M., Häkkinen, S., Hänninen, O. & Mykkänen, H. (1996) Serum ß-carotene response to supplementation with raw carrots, carrot juice or purified ß-carotene in healthy non-smoking women. Nutr. Res. 16:565-575.
10. De Pee, S., West, C. E., Permaesih, D., Martuti, S. & Muhilal & Hautvast, J. G. A. J. (1998) Orange fruits are more effective in increasing serum concentrations of retinol and ß-carotene than dark-green leafy vegetables in school children in Indonesia. Am. J. Clin. Nutr. 68:1058-1067.[Abstract]
11. Khan, N. C., West, C. E., de Pee, S. & Khôi, H. H. (1998) Comparison of the effectiveness of carotenoids from dark-green leafy vegetables and yellow and orange fruits in improving vitamin A status of breastfeeding women in Vietnam. Report of the XVIII International Vitamin A Consultative Group meeting [abstract] 1998 International Life Sciences Institute Washington, DC. .
12. Castenmiller, J. J., West, C. E., Linssen, J. P., van het Hof, K. H. & Voragen, A. G. (1999) The food matrix of spinach is a limiting factor in determining the bioavailability of ß-carotene and to a lesser extent of lutein in humans. J. Nutr. 129:349-355.
13. Van het Hof, K. H., Brouwer, I. A., West, C. E., Haddeman, E., Steegers-Theunissen, R. P., van Dusseldorp, M., Weststrate, J. A., Ekes, T. K. & Hautvast, J. G. A. J. (1999) Bioavailability of lutein from vegetables is five times higher than that of ß-carotene. Am. J. Clin. Nutr. 70:261-268.
14. Tang, G., Gu, X.-F., Hu, S.-M., Xu, Q.-M., Qin, J., Dolnikowski, G. G., Fjeld, C. R., Gao, X., Russell, R. M. & 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.
15. Van Lieshout, M., West, C. E., Wang, Y., van Breemen, R. B., Permaesih, D., Muhilal, , Verhoeven, M. A., Creemers, A. F. L. & Lugtenburg, J. (2001) Bioavailability and bioefficacy of ß-carotene measured using ß-carotene and retinol, labeled with 13C, in Indonesian children. Van Lieshout, M. eds. Bioavailability and Bioefficacy of ß-Carotene Measured Using 13C-Labeled ß-Carotene and Retinol: Studies in Indonesian Children 2001:49-72 Wageningen University Wageningen, the Netherlands. Thesis.
16. Jackson, M. J. (1997) The assessment of bioavailability of micronutrients: introduction. Eur. J. Clin. Nutr. 51:S1-S2.
17. De Pee, S. & West, C. E. (1996) Dietary carotenoids and their role in combating vitamin A deficiency: a review of the literature. Eur. J. Clin. Nutr. 50:S38-S53.
18. Van Lieshout, M., West, C. E., Muhilal, , Permaesih, D., Wang, Y., Xu, X., van Breemen, R. B., Creemers, A. F. L., Verhoeven, M. A. & Lugtenburg, J. (2001) Bioefficacy of ß-carotene dissolved in oil studied in children in Indonesia. Am. J. Clin. Nutr. 73:949-958.
19. Brouwer, I. A., van Dusseldorp, M., West, C. E. & Steegers-Theunissen, R. P. M. (2001) Bioavailability and bioefficacy of folate and folic acid in humans. Nutr. Res. Rev. 14:267-293.
20. Booher, L. E., Calliston, E. C. & Hewston, E. M. (1939) An experimental determination of the minimum vitamin A requirements of normal adults. J. Nutr. 17:317-331.
21. Wagner, K. H. (1940) Die experimentelle Avitaminose A beim Menschen. [Erratum appears in 1940 Ztschrf. Physiol. Chem. 264: 59.]. Ztschrf. Physiol. Chem. 264:153-188.
22. Hume, E. M. Krebs, H. A. eds. Vitamin A requirements of human adults: an experimental study of vitamin A deprivation in man. Medical Research Council Special Report No. 264 1949 HMSO London, UK. .
23. Sauberlich, H. E., Hodges, R. E., Wallace, D. L., Kolder, H., Canham, J. E., Hood, J., Raica, W., Jr. & Lowry, L. K. (1974) Vitamin A metabolism and requirements in the human studied with the use of labeled retinol. Vitam. Horm. 32:251-275.[Medline]
24. Tang, G., Qin, J., Dolnikowski, G. G. & Russell, R. M. (2000) Vitamin A equivalence of ß-carotene in a woman as determined by a stable isotope reference method. Eur. J. Nutr. 39:7-11.[Medline]
25. U.S. Institute of Medicine, Food and Nutrition Board, Standing Committee on the Scientific Evaluation of Dietary Reference Intakes (2000) Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc 2000 National Academy Press Washington, DC. .
26. Castenmiller, J. J. M. & West, C. E. (1998) Bioavailability and bioconversion of carotenoids. Annu. Rev. Nutr. 18:19-38.[Medline]
27. Van het Hof, K. H., West, C. E., Weststrate, J. A. & Hautvast, J. G. A. J. (2000) Dietary factors that affect the bioavailability of carotenoids. J. Nutr. 130:503-506.
28. West, C. E. (2000) Meeting requirements for vitamin A. Nutr. Rev. 58:341-345.[Medline]
29. Bingham, S. A., Nelson, M., Paul, A. A., Haraldsdottir, J., Loken, E. B. & Van Staveren, W. A. (1988) Method for data collection at an individual level. Cameron, M. E. Van Staveren, W. eds. Manual on Methodology for Food Consumption Studies 1988:83-88 Oxford University Press New York, NY. .
30. Melse-Boonstra, A., de Pee, S., Martini, E., Halati, S., Sari, M., Kosen, S. & Muhilal & Bloem, M. W. (2000) The potential of various foods to serve as a carrier for micronutrient fortification: data from remote areas in Indonesia. Eur. J. Clin. Nutr. 54:822-827.[Medline]
31. Gregory, J., Foster, K., Tyler, H. & Wiseman, M. (1990) The dietary and nutritional survey of British adults 1990 Office Population Census and Survey, Social Survey Division. HMSO London, UK. .
32. Prynne, C. J., Paul, A. A., Price, G. M., Day, K. C., Hilder, W. S. & Wadsworth, M. E. (1999) Food and nutrient intake of a national sample of 4-year old children in 1950: comparison with the 1990s. Public Health Nutr. 2:537-547.[Medline]
33. de Pee, S. & Dary, O. (2001) Biochemical indicators of vitamin A deficiency: serum retinol and serum retinol binding protein. J. Nutr. :2895S-2901S.
34. Hulshof, K. F. A. M., Kruizinga, A. G. & Kistemaker, C. (1998) De bijdrage van enkele subgroepen voedingsmiddelen (differentiatie naar vetgehalte en type dranken) aan de inname van energie en voedingsstoffen. Report V98.808, Vols. 1 and 2 1998 TNO Nutrition and Food Research Zeist. .
35. West, C. E. (2000) Vitamin A and measles. Nutr. Rev. 58:S46-S54.[Medline]
36. Van Crevel, R., Karyadi, E., Netea, M. G., Verhoef, H., Nelwan, R. H., West, C. E. & van der Meer, J. W. (2002) Plasma leptin, nutritional status and the acute phase response in patients with tuberculosis. J. Clin. Endocrin. Metab. 87:758-763.
37. Umeta, M., West, C. E., Haidar, J., Deurenberg, P. & Hautvast, J. G. A. J. (2000) Zinc supplementation and stunted infants in Ethiopia: a randomised controlled trial. Lancet 355:2021-2026.[Medline]
38. Dary, O. & Mora, J. O. (2001) Food fortification to reduce vitamin A deficiency: IVACG recommendations. J. Nutr. :2927S-2933S.
39. Ye, X., Al-Babili, S., Klöti, A., Zhang, J., Lucca, P., Beyer, P. & Potrykus, L. (2000) Engineering the provitamin A (ß-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303-305.
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B. B. Maziya-Dixon, I. O. Akinyele, R. A. Sanusi, T. E. Oguntona, S. K. Nokoe, and E. W. Harris Vitamin A Deficiency Is Prevalent in Children Less Than 5 y of Age in Nigeria J. Nutr., August 1, 2006; 136(8): 2255 - 2261. [Abstract] [Full Text] [PDF]
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R. Wegmuller, F. Camara, M. B. Zimmermann, P. Adou, and R. F. Hurrell Salt Dual-Fortified with Iodine and Micronized Ground Ferric Pyrophosphate Affects Iron Status but Not Hemoglobin in Children in Cote d'Ivoire J. Nutr., July 1, 2006; 136(7): 1814 - 1820. [Abstract] [Full Text] [PDF]
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G. Tang, J. Qin, G. G Dolnikowski, R. M Russell, and M. A Grusak Spinach or carrots can supply significant amounts of vitamin A as assessed by feeding with intrinsically deuterated vegetables Am. J. Clinical Nutrition, October 1, 2005; 82(4): 821 - 828. [Abstract] [Full Text] [PDF]
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S. Gueguen, P. Leroy, R. Gueguen, G. Siest, S. Visvikis, and B. Herbeth Genetic and environmental contributions to serum retinol and {alpha}-tocopherol concentrations: the Stanislas Family Study Am. J. Clinical Nutrition, May 1, 2005; 81(5): 1034 - 1044. [Abstract] [Full Text] [PDF]
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P. J van Jaarsveld, M. Faber, S. A Tanumihardjo, P. Nestel, C. J Lombard, and A. J S. Benade {beta}-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. Clinical Nutrition, May 1, 2005; 81(5): 1080 - 1087. [Abstract] [Full Text] [PDF]
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M. van Lieshout and S. de Pee Vitamin A equivalency estimates: understanding apparent differences Am. J. Clinical Nutrition, April 1, 2005; 81(4): 943 - 945. [Full Text] [PDF]
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M. B Zimmermann, N. Chaouki, and R. F Hurrell Iron deficiency due to consumption of a habitual diet low in bioavailable iron: a longitudinal cohort study in Moroccan children Am. J. Clinical Nutrition, January 1, 2005; 81(1): 115 - 121. [Abstract] [Full Text] [PDF]
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M. B Zimmermann, R. Wegmueller, C. Zeder, N. Chaouki, R. Biebinger, R. F Hurrell, and E. Windhab Triple fortification of salt with microcapsules of iodine, iron, and vitamin A Am. J. Clinical Nutrition, November 1, 2004; 80(5): 1283 - 1290. [Abstract] [Full Text] [PDF]
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M. A Dijkhuizen, F. T Wieringa, C. E West, and Muhilal Zinc plus {beta}-carotene supplementation of pregnant women is superior to {beta}-carotene supplementation alone in improving vitamin A status in both mothers and infants Am. J. Clinical Nutrition, November 1, 2004; 80(5): 1299 - 1307. [Abstract] [Full Text] [PDF]
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 R. D. Semba, S. de Pee, D. Panagides, O. Poly, and M. W. Bloem Risk Factors for Xerophthalmia Among Mothers and Their Children and for Mother-Child Pairs With Xerophthalmia in Cambodia Arch Ophthalmol, April 1, 2004; 122(4): 517 - 523. [Abstract] [Full Text] [PDF]
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C. E. West, A. Eilander, and M. van Lieshout Reply to Russell et al. J. Nutr., September 1, 2003; 133(9): 2917 - 2917. [Full Text] [PDF]
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M. Umeta, C. E. West, H. Verhoef, J. Haidar, and J. G.A.J. |
