Provitamin A-biofortified maize consumption increases serum xanthophylls and ¹³C-natural abundance of retinol in Zambian children

Abstract

Plants that undergo C photosynthesis, such as maize, are enriched in the stable isotope of carbon (C) compared with other dietary plants and foods. Consumption of maize that has been biofortified to contain elevated levels of provitamin A carotenoids (orange maize) increased the abundance of C in serum retinol of Mongolian gerbils. We evaluated this method in humans to determine if it has potential for further use in intervention effectiveness studies. A random subset of samples from a two-month randomized controlled feeding trial of rural three- to five-year old Zambian children were used to determine the impact of orange maize intake on serum carotenoid concentrations ( n = 88) andC-natural abundance in serum retinol ( n = 77). Concentrations of β-cryptoxanthin (a xanthophyll provitamin A carotenoid) and the dihydroxy xanthophylls lutein and zeaxanthin, which do not have vitamin A activity, were elevated in children consuming orange maize compared with those consuming a white maize control ( P < 0.001), while β-carotene was not different ( P > 0.3). Furthermore, C natural abundance was higher after two months' intervention in the orange maize group compared with the white maize group ( P = 0.049). Predictions made from equations developed in the aforementioned gerbil study estimated that maize provided 11% (2-21%, 95% confidence interval) of the recent dietary vitamin A to these children. These results demonstrate that orange maize is efficacious at providing retinol to the vitamin A pool in children through provitamin A carotenoids, as monitored by the change inC enrichment, which was not reflected in serum β-carotene concentrations. Further effectiveness studies in countries who have adopted orange maize should consider determining differences in retinol C-enrichment among target groups in addition to profiling serum xanthophyll carotenoids with specific emphasis on zeaxanthin. Impact statement Maize biofortified with provitamin A carotenoids (orange) has been released in some African markets. Responsive and sensitive methods to evaluate dissemination effectiveness are needed. This study investigated methods to evaluate effectiveness of orange maize consumption using serum from Zambian children fed orange maize for two months. Many varieties of orange maize contain higher amounts of the xanthophyll carotenoids in addition to β-carotene compared with typical varieties. This study uniquely showed higher concentrations of the maize xanthophylls lutein, zeaxanthin, and β-cryptoxanthin in children who consumed orange maize compared with white. Furthermore, maize is a C plant and is therefore naturally enriched with C. HigherC was detected in the serum retinol of the orange maize consumers with no change in serum β-carotene concentration suggesting preferential bioconversion to retinol. The combined analyses of serum zeaxanthin specifically and C-natural abundance of retinol could prove useful in effectiveness studies between orange maize adopters and non-adopters.

Use of Stable Isotopes to Evaluate Bioefficacy of Provitamin A Carotenoids, Vitamin A Status, and Bioavailability of Iron and Zinc

“…This phenomenon was studied in overweight individuals when a negative shift was measured in the ratio of 13 C to 12 C in serum retinol after a 3-mo vegetable intervention ( 79 ). In the first Zambian study mentioned above, the change in natural abundance of 13 C in serum retinol was positively shifted in the 3- to 5-y-old children eating orange maize for 46 d ( 45 ), showing that the β-carotene from this maize is efficacious and contributed to the vitamin A requirements of these children, even though liver stores did not increase. Similarly, gerbils fed an orange maize feed showed an increase in 13 C enrichment in serum retinol compared with controls ( 80 ).…”

“…When the paired RID test is used, it is necessary to determine a baseline serum retinol isotopic natural abundance postintervention because some of the baseline isotopic tracer may still be measurable and the intervention itself could change isotope enrichment depending on foods consumed. Specifically, provitamin A–biofortified C4 plants, such as maize, sorghum, and millet, are enriched in 13 C, and therefore vitamin A produced from these provitamin A sources could change the serum 13 C-enrichment of retinol in the subjects when consumed ( 45 ). This effect has been proposed as a biomarker for biofortified C4 crop intervention effectiveness ( 45 ), discussed later in this review.…”

“…Specifically, provitamin A–biofortified C4 plants, such as maize, sorghum, and millet, are enriched in 13 C, and therefore vitamin A produced from these provitamin A sources could change the serum 13 C-enrichment of retinol in the subjects when consumed ( 45 ). This effect has been proposed as a biomarker for biofortified C4 crop intervention effectiveness ( 45 ), discussed later in this review.…”

“…The bioefficacy factors for β-carotene in these studies were 2.80 ± 1.77 and 4.5 ± 3.1 μg β-carotene to 1 μg retinol, indicating readily bioaccessible β-carotene. Larger human studies should consider stable isotope methods, especially during effectiveness evaluations ( 45 , 56 ).…”

Nutritional security through crop biofortification in India: Status & future prospects

“…A study conducted on 246 children of 12-16 yr of age in Maharashtra, by feeding them with ‘ bhakri ’ (round flat unleavened bread) made from iron-rich and conventional pearl millet grains, demonstrated that feeding iron-rich pearl millet was an efficient approach to improve iron status in school-age children28. In another, serum xanthophylls and retinol were significantly improved in Zambia children fed with provitamin-A rich maize grains29. In a study on 679 Zambian children, it was found that consumption of β-carotene-rich maize significantly improved their serum β-carotene concentrations compared with traditional maize30.…”