Research ArticleAGRICULTURE

Micronutrient-fortified rice can be a significant source of dietary bioavailable iron in schoolchildren from rural Ghana

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Science Advances  27 Mar 2019:
Vol. 5, no. 3, eaau0790
DOI: 10.1126/sciadv.aau0790
  • Fig. 1 Study flowchart for human absorption study.

    At inclusion, subjects who had anemia [defined as hemoglobin (Hb) <11.5 g/dl] and/or IDE [defined as zinc protoporphyrin/heme (ZnPP/H) >43 μmol/mol] were selected (4244).

  • Fig. 2 Boxplots for the absolute iron absorption (mg/day) assessed measuring absorption from six different rice meals in iron-deficient and/or anemic Ghanaian children.

    Horizontal bars show the median iron absorption for each day (100 g of rice); each box represents the first to third quartile, and whiskers represent the lowest and highest data points regardless of outliers. Gray dots indicate outliers 1.5 interquartile ranges above the third quartile. Different letters indicate significant differences. P < 0.05, Bonferroni-corrected linear mixed model; n = 26. 54FeZnO, rice extruded with 54FePP, ZnO, and a vitamin premix; 57FeZnSO4, rice extruded with 57FePP, ZnSO4, and a vitamin premix; 54FeZnOCT, rice extruded with 54FePP, ZnO, a vitamin premix, CA, and TSC; 57FeZnSO4CT, rice extruded with 54FePP, ZnO, a vitamin premix, CA, and TSC; 58FeZnOCE, rice extruded with 54FePP, ZnO, a vitamin premix, CA, TSC, and EDTA; Reference, rice extruded with a vitamin premix, 58FeSO4 added before consumption.

  • Table 1 Composition of extruded rice formulations fortified with iron and zinc including relative iron solubility and visual scores.

    Solubility values without a common script differ significantly (P < 0.05) using univariate general linear model with multiple comparisons Bonferroni correction. All rices were fortified with Fe (4 mg/g) except otherwise stated.

    Fe compoundZn compoundSolubilizing agentMolar ratios
    (Fe/Zn/solubilizing
    agent)
    Relative solubility*ΔE to basmati rice
    FeSO481.6a ± 3.2214.6
    FePP7.68b,c ± 0.905.09
    ZnO1:0.713.6b,c ± 0.356.46
    ZnSO41:0.74.35c ± 0.436.83
    NaPP1:0.7:115.1b,d ± 0.845.59
    NaPP1:0.7:1.537.0e ± 0.676.61
    NaPP1:0.7:3.063.9f ± 6.156.74
    NaPP and EDTA1:0.7:1:1112g,h ± 6.174.60
    NaPP, EDTA, CA + TSC1:0.7:1:1:0.1:1.7102.7g ± 1.236.27
    EDTA, CA1:0.7:1:0.199.2g ± 3.285.36
    EDTA1:0.7:1108g ± 0.57.37
    EDTA1:0.7:0.337.3d ± 0.355.94
    EDTA, CA + TSC1:0.7:1:0.1:1.7118.9h ± 3.646.24
    CA + TSC1:0.1:1.750.9i ± 3.97.55
    CA + TSC + 20%1:0.12:2.059.9i ± 6.97.39
    CA + TSC + 40%1:0.15:2.560.3i ± 5.067.91
    FePPZnSO4NaFeEDTA1:0.7:0.0524.0d,l ± 2.488.34
    ZnSO4NaFeEDTA1:0.7:0.1743.9e,i ± 1.668.55
    FeOP17.3b,l ± 0.937.31
    ZnSO41:0.710.4b,c ± 0.528.19
    CA + TSC1:0.7:0.1:1.739.4e ± 1.038.74

    *Solubility relative to unfortified basmati rice fortified with FeSO4 after cooking.

    †Color differences relative to unfortified basmati rice. Rices with discoloration above ΔE values of ≥13 were distinguishable from unfortified basmati rice. In previous studies, rices with ΔE in the range of 5.1 to 6.7 compared to basmati rice were undistinguishable from unfortified basmati rice in triangle tests (20).

    ‡Fe (5 mg/g).

    • Table 2 Novel iron compounds screened for suitability for rice fortification using a premix approach.

      Rice was fortified with Fe (5 mg/g).

      Iron compounds used for fortificationΔE to basmati rice*
      Fe glycinate taste free38.8
      Fe (III) tartrate 1 hydrate36.1
      Fe (II) bisglycinate27.1
      Fe (II) succinate11.4
      Fe (II) ammonium phosphate6.73
      Soluble FePP17.4
      Soluble FePP (III) + citrate10.8
      FeSO414.6
      FeSO4 + CA + TSC20.1

      *Color differences relative to unfortified basmati rice. ΔE values of ≥13 were distinguishable from unfortified basmati rice. In previous studies, rices with ΔE in the range of 5.1 to 6.7 compared to basmati rice were undistinguishable from unfortified basmati rice in triangle tests (20).

      • Table 3 Composition of extruded rice, administered study meals, human iron absorption, and in vitro iron solubility.

        Each rice meal serving contained 49.5 g of unfortified rice and 0.5 g of fortified rice with 50 g of either bean or tomato sauce. Values are means ± SDs or geometric means (95% CI). Labeled means in a column without a common letter differ. P < 0.05, Bonferroni-corrected linear mixed model. Designated micronutrient composition of fortified kernels can be found in the Supplementary Materials. 54FeZnO, extruded rice containing 54FePP, ZnO, and a micronutrient mix (MN); 57FeZnSO4, extruded rice containing 57FePP, ZnSO4, and MN; 54FeZnOCT, extruded rice containing 54FePP, ZnO, MN, CA, and TSC; 57FeZnSO4CT, extruded rice containing 57FePP, ZnSO4, MN, CA, and TSC; 58FeZnOCE, extruded rice containing 58FePP, ZnO, MN, CA, and EDTA; Reference, extruded rice containing MN and 58FeSO4 solution added before consumption. N/A, not applicable.

        Iron (mg/g)*Zinc (mg/g)*Fe/Zn/CA/TSC/
        EDTA
        (mol/mol)
        Fe/Zn/PA/AA
        (mol/mol)
        Fractional iron
        absorption (%)§
        RBV (%)§,||Relative iron
        solubility (%)
        54FeZnO3.5 ± 0. 504.2 ± 0.081:1.0:0:0:01:1.0:0.8:0.02.3 (1.9–2.8)a36a3.6 ± 0.5a
        57FeZnSO43.2 ± 0.504.1 ± 0.191:1.1:0:0:01:1.1:1.0:0.03.5 (2.7–4.5)b54b4.7 ± 0.5a
        54FeZnOCT3.2 ± 0. 504.2 ± 0.11:1.1:0.3:6.0:01:1.1:0.9:0.04.5 (3.6–5.5)b70.4b19.8 ± 2.7b
        57FeZnSO4CT3.4 ± 0. 504.1 ± 0.191:1.1:0.3:5.5:01:1.1:0.9:0.06.3 (5.3–7.4)c98.3c27.1 ± 4.0b
        58FeZnOCE3.3 ± 0. 504.1 ± 0. 191:1.1:0.3:0:0.61:1.1:0.9:0.06.4 (5.1–8.1)c101c24.1 ± 3.1b
        Reference3.6 ± 0. 101.3 ± 0.01N/A1:0.3:0.8:0.06.4 (5.2–7.8)cN/AN/A

        *Calculated iron and zinc contents in composite meals were based on the means from the analysis of single components [49.5 g of regular basmati rice, 0.5 g of extruded rice, and average mineral contents from the two different sauces (50 g of sauce); n = 3], and SDs for iron and zinc contents of composite meals were adapted by calculating the square root of the squared and summed SDs from each single component.

        †Molar ratio in fortified rice.

        ‡Molar ratio per serving of rice—average mineral, PA, and AA contents from the two different sauces were calculated.

        §n = 26.

        ||RBV calculation based on geometric mean fractional iron absorption (%) relative to fractional iron absorption from the reference meal for each subject.

        ¶Iron solubility was assessed in fortified rice kernels. For details on the calculation, please refer to the text, n = 3.

        • Table 4 Anthropometric, iron, and inflammatory variables of the Ghanaian children (n = 26), assessed before first meal administration.

          Values are means ± SD if not otherwise stated. Vitamin A deficiency defined as RBP < 0.7 μM.

          Sex (female), %42
          Age, years7.6 ± 1.3
          Weight, kg22 ± 3.6
          Height, cm115 ± 9.3
          Weight for age, Z score−1.3 ± 0.81
          Height for age, Z score−1.2 ± 0.96
          Body mass index for age, Z score−0.7 ± 0.65
          Zinc protoporphyrin/heme ratio*,
          μmol/mol
          52.0 (44.6–59.5)
          Hemoglobin, g/liter112 ± 9
          Plasma ferritin*, μg/liter43.6 (32.5–58.4)
          Body iron stores, mg/kg body
          weight
          4.2 ± 0.70
          Soluble transferrin receptor*,
          mg/liter
          8.8 (7.75–10.05)
          Hepcidin*, nM12.0 (7.4–19.1)
          Iron-deficient, non-anemic,
          prevalence, n (%)
          4 (15)
          Anemia‡,§ prevalence, n (%)15 (58)
            Non-IDA5 (19)
            IDA10 (39)
          Retinol binding protein, μM0.79 ± 0.19
          Vitamin A deficiency prevalence,
          n (%)
          8 (24)
          C-reactive protein >5 mg/liter,
          prevalence, n (%)
          3 (12)
          α1-Acid glycoprotein >1 g/liter,
          prevalence, n (%)
          6 (23)
          Positive malaria by microscopy,
          prevalence, n (%)
          11 (42)

          *Values are geometric means (95% CI).

          †ID defined as sTfR >8.3 mg/liter and/or plasma ferritin <30 μg/liter.

          ‡Anemia was defined as Hb <115 g/liter.

          §IDA defined as sTfR >8.3 mg/liter and/or plasma ferritin <30 μg/liter in combination with Hb <115 g/liter.

          Supplementary Materials

          • Supplementary Materials

            This PDF file includes:

            • Table S1A. Components (mg/g rice flour) used for extrusion.
            • Table S1B. Vitamin premix composition in % per gram premix.
            • Table S2. Target nutrient concentration in the fortified rice per gram of extruded rice kernels, corresponding to 100 g of finished product.
            • Table S3. Ingredients for two different sauces provided with cooked rice.

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