Maize grain and soil surveys reveal suboptimal dietary selenium intake is widespread in Malawi

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Selenium is an essential element in human diets but the risk of suboptimal intake increases where food choices are narrow. Here we show that suboptimal dietary intake (i.e. 20–30 µg Se person−1 d−1) is widespread in Malawi, based on a spatial integration of Se concentrations of maize (Zea mays L.) grain and soil surveys for 88 field sites, representing 10 primary soil types and >75% of the national land area. The median maize grain Se concentration was 0.019 mg kg−1 (range 0.005–0.533), a mean intake of 6.7 µg Se person−1 d−1 from maize flour based on national consumption patterns. Maize grain Se concentration was up to 10-fold higher in crops grown on soils with naturally high pH (>6.5) (Eutric Vertisols). Under these less acidic conditions, Se becomes considerably more available to plants due to the greater solubility of Se(IV) species and oxidation to Se(VI).

Selenium (Se) is an essential element for humans and livestock. A total of 25 genes encoding selenoproteins have been identified in humans, including iodothyronine deiodinases, thioredoxin reductases, glutathione peroxidases, and a range of other selenoproteins (e.g. SelP, SelM, SelT)1. These proteins have critical roles in thyroid functioning, cell proliferation and survival through redox homeostasis, antioxidant defence and the immune response. When Se intake is suboptimal, the selenoprotein status of people decreases and there are increased risks of adverse health effects. At extremely low Se intake levels (where habitual intakes for adults are <20 µg Se d−1), clinical deficiency disorders have been reported including Keshan disease (a cardiomyopathy) and Kashin-Beck disease (an osteoarthropathy). Where habitual intakes for adults are less than those needed for maximal expression of glutathione peroxidase, typically at least 40 µg Se d−1, there is an increased risk of health disorders, including cardiovascular disorders, impaired immune functions, and some cancers1. The relationships between Se intake, Se status in terms of selenoprotein expression and health outcomes have still to be fully resolved2,3. These uncertainties are reflected in the wide range of Dietary Reference Intake (DRI) levels in different countries1. Some DRIs are set to reduce risks of overt deficiency (i.e. recommending intakes of ∼40 µg Se d−1), although most countries have recommended intake levels of 50–70 µg Se d−1. As high habitual levels of Se intake are potentially toxic (>400–900 µg Se d−1), care must be taken in setting DRIs and recommending dietary supplementation.

Selenium intake in human populations is derived primarily from dietary sources and can be determined from direct dietary analyses or surveys and food composition tables. Reported Se intakes range from 3 to 7000 µg Se d−1 globally4 due to differing dietary preferences and the levels of plant available Se in the soil on which crops are grown for consumption1,4,5,6,7. Populations in many European countries and elsewhere have intakes <50 µg Se d−1, which are likely to be suboptimal in terms of selenoprotein expression2. Higher dietary Se intake levels (>150 µg Se d−1) occur in Se-rich (seleniferous) environments (e.g. parts of China, India, North America, and Venezuela) and where seafood-based diets containing high concentrations of Se are prevalent (e.g. notably in parts of Greenland and Japan). Selenium intake from water and air is usually insignificant, except where environmental Se concentrations are high due to natural or anthropogenic factors4.

The extent of Se deficiency in human populations is unclear, although it is likely to be widespread in global terms and especially where food choices are narrow. For example, surveys of Se concentrations in rice grain show that Se intake is likely to be suboptimal in many populations reliant on a staple diet of rice8. In Sub-Saharan Africa (SSA), Se intake levels are often very low in rural populations where fish consumption is limited. Thus, in rural Burundi, intakes of 17 µg Se d−1 have been reported in adults9. In southern Malawi, intakes of 15–21 µg Se d−1 have been reported among children living in rural areas of Zomba District10, consistent with low blood plasma Se concentrations (<55 µg L−1) among adults in the same area11,12. A substantial proportion of dietary Se intake in SSA has been attributed to fish consumption10,13. Indeed, higher Se intakes (44–46 µg Se d−1) have been reported in Mangochi District, adjacent to the southern end of Lake Malawi, where fish consumption is likely to be high14. In Burundi, higher Se intakes have also been reported in middle-class men (82 µg Se d−1) and mothers (38 µg Se d−1), which have been linked to variation in fish consumption between groups9.

In rural SSA, maize grain is the dominant staple food. In Malawi (mean energy intake 2172 kcal person−1 d−1) and neighbouring Zambia (1873 kcal person−1 d−1), ∼52% of total dietary calorie intake is derived from maize (2007 data; ref. 15). This equates to 0.354 and 0.315 kg person d−1 in Malawi and Zambia, respectively. Consumption of animal products from all sources (meat, offal, fats, milk and eggs) is typically low, accounting for 64 and 97 kcal person−1 d−1 in Malawi and Zambia, respectively, of which fish accounts for 9 and 11 kcal person−1 d−1. Maize grain is therefore likely to be critical in determining Se intakes to the average SSA diet despite being low in terms of Se concentration according to local food composition tables. For example, in Malawi, whole-grain maize flour contained 25 µg Se kg−1 in Zomba District13 and 49 µg Se kg−1 in Mangochi District16.

This study aimed to determine the contribution of maize grain to dietary Se intake in rural Malawi and establish whether maize grain Se concentration is dependent on soil Se concentration and/or other soil factors (e.g. pH, organic matter content). Malawi was chosen because: (1) a large proportion of the population engages in subsistence farming and their diets are dominated by maize; (2) dietary Se intakes and Se status are likely to be low among rural populations10,11,12,13; (3) there is a high national prevalence of immunological disorders (e.g. HIV/AIDS) and other morbidity symptoms which are associated with low micronutrient status1,17,18; (4) the national government operates a national Farm Input Subsidy Programme19 which provides the opportunity to consider agronomic biofortification via incorporation of trace quantities of Se in compound fertilisers. Such a strategy to alleviate suboptimal dietary Se intakes was adopted at a national scale in Finland in 1984 and is feasible in other contexts20,21,22.

National food consumption patterns and published Se concentration data for food were used to estimate baseline Se intakes for two Districts in rural Malawi. Mean dietary Se intakes of 39.8 and 24.4 µg Se person−1 d−1 were estimated for Mangochi and Zomba Districts, respectively, with Se intake from all non-maize sources being 22.4 and 15.5 µg Se person−1 d−1, respectively (Table 1). Thus, maize was the single major foodstuff contributing to dietary Se intake. As food consumption data are based on national per capita supplies which will overestimate food intake due to food wastage during storage, preparation and cooking15, Se intakes are likely to be lower than these estimated values.

The use of a single national food consumption metric masks substantial within-country variation in Se intake due to differing food consumption patterns. For example, fish consumption is likely to be higher in Mangochi, near Lake Malawi, than in Zomba District. A median Se intake of 45 µg person−1 d−1 (interquartile range = 30) for Mangochi District was reported by Eick et al.14, based largely on the same food composition data, using dietary recall surveys and questionnaires. Adult Se intake was not reported for Zomba District10, but Se intake by children aged 4–6 ranged from 15–20 µg person d−1. The link between fish consumption and dietary Se intake has previously been associated with income levels in Burundi9. The higher dietary Se intake estimate at Mangochi compared to Zomba in the present analysis reflects differences in the Se concentration of edible crop portions reported by Donovan et al.13 and Eick16. For example, the Se concentration of whole-grain maize flour was 49 µg Se kg−1 in Mangochi compared to 25 µg Se kg−1 in Zomba. If food consumption patterns were identical in both Districts, maize would account for 46% and 36% of dietary Se intake in Mangochi and Zomba, respectively. In addition, the Se concentration of mango, banana, pigeon pea, and kidney bean was ∼2–6-fold higher in Mangochi than in Zomba. Assuming there were no systematic differences in sample collection, preparation or analysis between Donovan et al.13 and Eick16, these consistent differences in crop Se concentration between Districts probably result from soil factors rather than cultivar differences20,21,22,23. However, the combined Se intake from fruit, vegetables, other cereals and starchy staples was still less than that from maize in both Mangochi and Zomba. Selenium intake from animal sources other than fish is likely to be low, based on the limited contribution of these food sources to the typical Malawian diet. However, as there are gaps in Se concentration data for these categories in local food composition tables, this conclusion requires further validation.

To determine the wider contribution of maize grain to dietary Se intakes in Malawi, samples of soil and grain were collected nationwide (Fig. 1). In 2009, Se concentration in maize grain from 73 sites ranged from 0.0045 to 0.533 mg Se kg−1 with a median value of 0.016 mg Se kg−1; over 70% of the samples had a lower Se concentrations than reported by Donovan et al.13. However, there was a disjunct distribution of grain Se concentrations as 69 samples contained <0.08 mg Se kg−1 whereas one sample from Lisungwi EPA contained 0.146 mg Se kg−1 and another from Mikalango EPA contained 0.533 mg Se kg−1. The sample from Mikalango was from a crop growing on a Eutric Vertisol24 with a pH of 7.9. Therefore, in 2010, a further 15 samples were collected from other Shire Valley Eutric Vertisol sites in the Mangoti, Dolo and Mikalango EPAs with soil pH values ranging from 6.97–8.02. In 2010, grain Se ranged from 0.173–0.413 mg Se kg−1 for 13 of the sites, although two sites in Mangoti had lower concentrations of 0.0054 mg Se kg−1. Mean grain Se concentrations expressed on an EPA basis are presented, in ascending order, in Figure 2a. Based on a mean per capita consumption of 0.354 kg d−1 and an overall median grain Se concentration of 0.019 mg Se kg−1 from all 88 sites, the estimated median Se intake from maize is 6.7 µg Se person−1 d−1 (range 1.6 to 189).

Figure 1: Location of farmers’ fields sampling sites in Malawi produced using ArcGIS (v. 9.3).

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Figure 2: Concentrations of Se in maize grain (a) and soil (b,c) from farmers’ fields surveys in Malawi.

Figure 2

Soil Se is expressed as total (b) and KH2PO4-extractable (c) Se forms. Data are presented on an Extension Planning Area (EPA) basis (mean ±s.e.m.). Note, total and KH2PO4-extractable soil Se data are missing for Chinguluwe EPA due to the loss of the soil sample. For Chitsime, Mbawa, and Ntonda EPAs there was insufficient soil sample remaining for KH2PO4-extractable Se to be analysed following other soil analyses.

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Soil factors affect maize grain Se concentration

Mean and median total soil Se concentrations were 0.1941 and 0.1623 mg Se kg−1, respectively and there was ∼12-fold variation in values between 0.0521 and 0.6195 mg Se kg−1. Mean and median KH2PO4-extractable soil Se concentrations were 0.0056 and 0.0046 mg Se kg−1, respectively and there was again a ∼12-fold variation in values between 0.0013 and 0.0158 mg Se kg−1. There was no obvious link between grain and soil Se concentrations when data were expressed on a mean EPA basis (Fig. 2). Across all sites, there was evidence of a correlation between grain Se concentration and soil pH, especially at pH >6.5 (Fig. 3). There were weaker positive correlations between total soil Se, KH2PO4-extractable Se and soil organic matter. There was also a weak positive correlation between grain Se concentration and KH2PO4-extractable, but not total, soil Se concentration.

Figure 3: Relationships between soil Se (total and KH2PO4-extractable forms) and soil pH, soil organic matter and maize grain Se concentration from a survey of farmers’ fields in Malawi.

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Districts are numbered #1 (Balaka District) to #28 (Zomba District) as stated in Table 2 (NSO, 2008; ref. 37; N.B. Neno District (#18) maps within Mwanza District (#16) and is not shown), (b) soil series maps based on ref. 24.Figure produced using ArcGIS (v. 9.3).
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Figure produced using ArcGIS (v. 9.3).