The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage

Abstract

Carotenoids are important dietary nutrients with health-promoting effects. The biofortification of staple foods with carotenoids provides an efficient delivery strategy but little is known about the fate and distribution of carotenoids supplied in this manner. The chicken provides a good model of human carotenoid metabolism so we supplemented the diets of laying hens using two biofortified maize varieties with distinct carotenoid profiles and compared the fate of the different carotenoids in terms of distribution in the feed, the hen's livers and the eggs. We found that after a period of depletion, pro-vitamin A (PVA) carotenoids were preferentially diverted to the liver and relatively depleted in the eggs, whereas other carotenoids were transported to the eggs even when the liver remained depleted. When retinol was included in the diet, it accumulated more in the eggs than the livers, whereas PVA carotenoids showed the opposite profile. Our data suggest that a transport nexus from the intestinal lumen to the eggs introduces bottlenecks that cause chemically-distinct classes of carotenoids to be partitioned in different ways. This nexus model will allow us to optimize animal feed and human diets to ensure that the health benefits of carotenoids are delivered in the most effective manner.

Figure 1. Carotenoid levels in the four diets used in the feeding trial presented as mean values in μg/g freeze dried (fd) ± SE from five samples (biological replicates).

WT = wild-type M37W maize, HC = high-carotenoid maize, BKT = ketocarotenoid maize, COM = commercial yellow maize plus retinol. Individual carotenoids are shown (neox = neoxanthin, viol = violoxanthin, lut = lutein, zeax = zeaxanthin, α-cry = α-cryptoxanthin, β-cry =β-cryptoxanthin, β-car = β-carotene, astax = astaxanthin, keto-Z = other ketocarotenoids) as well as the total levels of pro-vitamin A (PVA) and non-PVA carotenoids.

Figure 2. Carotenoid levels in the yolk of eggs laid by hens after 31 days on four different diets (WT = wild-type M37W maize, HC = high-carotenoid maize, BKT = ketocarotenoid maize, COM = commercial yellow maize plus retinol).

Values are means in μg/g freeze dried (fd) ± SE from 3–5 independent samples (biological replicates). Individual carotenoids are shown (neox = neoxanthin, viol = violoxanthin, lut = lutein, zeax = zeaxanthin, α-cry = α-cryptoxanthin, β-cry = β-cryptoxanthin, β-car = β-carotene, C427 = most likely β-cryptoxanthin-5,8-epoxide, astax = astaxanthin) as well as the total levels of pro-vitamin A (PVA) and non-PVA carotenoids.

Figure 3. Carotenoid and retinoid levels in the livers of hens after 31 days on four different diets (WT = wild-type M37W maize, HC = high-carotenoid maize, BKT = ketocarotenoid maize, COM = commercial yellow maize plus retinol).

Values are means μg/g freeze dried (fd) ± SE from five independent samples (biological replicates). Individual carotenoids are shown using the scale on the left axis (viol = violoxanthin, lut = lutein, zeax = zeaxanthin, α-cry = α-cryptoxanthin, β-cry = β-cryptoxanthin, β-car = β-carotene, C450 = most likely β-carotene-5,6-epoxide or β-carotene-5,6,5′,6′-diepoxide, astax = astaxanthin, keto-Z = other ketocarotenoids) as well as the total levels of pro-vitamin A (PVA) and non-PVA carotenoids. Retinoids are shown using the scale on the right axis and are isolated in a box for clarity. R350 is a non-polar retinoid product with an absorbance spectrum showing three distinct peaks at 328, 348, 370 nm.

Figure 4

Appearance of egg yolks (a) raw and (b) cooked by boiling for 10 min produced from hens fed (left to right) on the COM, BKT, HC and WT diets. The color scale in panel (a) is provided by the YolkFan^TM (DSM N.V., Heerlen, Netherlands).

Figure 5. The nexus model, showing the fate of carotenoids provided to poultry as biofortified diets.

(a) General assumptions of the model based on observations of carotenoid distribution in feed and different tissues. (b) The routes through the nexus (black) and mechanisms that may be involved (red) based on this study and previous reports.