Iodine deficiency is the largest preventable cause of brain damage and mental impairment worldwide. Iodine is required for thyroid hormone production, which is central to metabolism and growth through the lifecycle. As well as irreversible mental retardation in its most severe form, iodine deficiency can also result in miscarriages, stillbirths, and impaired psychomotor development and behavioural problems in children born to iodine deficient mothers [1
] Australia was identified as a country with mild iodine deficiency, based on urinary iodine concentrations identified in school children aged 8–10 years across five mainland states in the Australian National Iodine Nutrition Study, 2003–2004 [2
] as well as smaller, non-representative studies of pregnant and lactating women [3
]. To address the re-emergence of iodine deficiency in Australia [7
], the government introduced mandatory iodine fortification of salt used in bread in 2009 [8
]. The level of iodine required by mandatory fortification to be added to salt used in the bread-making process was modelled using bread consumption patterns of 100 g/day, equating to approximately three slices [8
]. However, dietary and food composition data at that time was outdated [9
] and current patterns of bread intake were unknown. In a small convenience sample in Victoria, median bread intake in pregnant women was reported to be only two slices per day, while less than half (43%) of participants ate three or more slices per day [10
]. Despite the mandatory iodine fortification policy, high-risk groups with increased requirements, including pregnant and lactating women, may still not be adequately protected [11
]. Dietary studies report an increased iodine intake in pregnant women since the implementation of fortification [12
]. But these studies were not conducted in nationally representative samples of the population. Young children are also vulnerable to inadequate iodine intakes because of their less varied dietary exposure and importance of the nutrient for growth and development. The International Council for the Control of Iodine Deficiency Disorders (ICCIDD) recommends that primary school children aged 6–12 years are the universal reference group to be used as an indicator of population-level iodine status. Children of this age are targeted for collection of spot urine samples for determination of median urinary iodine concentrations (UIC) which are compared against reference values of 100–199 µg/L that suggest adequacy of intake.
Studies have shown a socioeconomic gradient for micronutrient intakes, with low socioeconomic status (SES) groups more likely to have poor micronutrient intakes compared with their higher SES counterparts [15
]. In Australia, low SES groups are less likely to comply with dietary guidelines compared with higher SES groups. Despite sparse information about dietary iodine intake in Australian pregnant women [18
], low SES groups have been documented to be less likely to consume recommended iodine supplements during pregnancy as compared with higher SES groups [19
], as reported in other countries [15
]. Low SES groups are also less likely to comply with dietary guidelines when compared with higher SES groups [20
] and have various barriers to healthy eating which affects nutrient intakes, including high costs [20
], lack of priority for health [17
], difficulties accessing healthy foods [21
], and a lack of social support [22
]. Previous investigations into iodine deficiency have speculated that the high cost of iodine-rich food sources such as fish and seafood, as well as a lack of knowledge, low uptake of iodine supplements, and taste preferences might be major barriers to achieving adequate iodine intake in pregnant women [3
Ensuring adequate iodine intake amongst women of childbearing-age is important, in order to ensure optimal iodine intake during early pregnancy and to avoid disruption to foetal brain growth and body development [11
]. The most recent national dietary survey in Australia, the National Nutrition and Physical Activity Survey (NNPAS), conducted in 2011–2012 did not sample pregnant or breastfeeding women, therefore this study will instead draw primarily on data for women of childbearing age (14–50 years).
Currently, in Australia no studies have determined contributions of food sources, including fortified bread, to iodine intake across life stages and by sociodemographic factors in a nationally representative sample. Further to this, assessing at risk groups such as women of childbearing age and children who have been previously been found to have inadequate iodine status is necessary to evaluate the effectiveness of the fortification program in eradicating iodine deficiency. This information is required to inform the development of dietary guidance related to achieving and optimal iodine intake. The aims of the present study were: (1) to determine sociodemographic factors associated with achieving an adequate dietary iodine intake post-fortification in the Australian population as a whole, and to identify food group contributions to total dietary iodine intake; (2) to assess whether bread consumption patterns (≥100 g bread/day) affect iodine status in high risk groups (women of childbearing age, 14–50 years; and children, 2–18 years), after adjusting for high iodine food sources, SES, geographical location and age; and (3) to determine the effect of age, and SES on bread consumption patterns and iodine intake in primary school children aged 5–9 years.
3.1. Iodine Intake by Age, SES and Geographical Remoteness in the Australian Population (n = 7735)
Median iodine intake differed between age groups (p
< 0.001, η2
= 0.001) (Figure 1
), SES quintiles (p
< 0.001, η2
= 0.002) (Figure 2
), and geographical remoteness area (p
< 0.001, η2
= 0.000). Adolescents 14–18 years had the highest median iodine intake (177 µg/day), while children 4–8 years had the lowest median iodine intake (152 µg/day) (Figure 1
). However, age-related differences were small, with <0.98% difference between groups (η2
No trend was evident for iodine intake between SES quintiles. Inner regional areas of Australia had slightly higher dietary iodine intakes (mean= 170 µg/day), followed by major cities (mean = 168 µg/day) and then other regions of Australia (mean = 166 µg/day) (p < 0.001; η2 < 0.002), with less than 0.1% variance in iodine intake explained by age group, SES and location.
3.2. Food Group Contributions to Total Iodine Intake in the Australian Population (n = 7735)
The four main sources of iodine for the total Australian population at the time of the survey were: cereals and cereal products (mean 48.1; SD ± 34.5 µg/day, 29%); milk products and dishes (46.7 ± 45.5 µg/day, 26%); non-alcoholic beverages (23.6 ± 21.1 µg/day, 15%) and cereal based products and dishes (19.6 ± 24.4 µg/day, 12%). Smaller contributions were provided by fish and seafood products and dishes (7.1 ± 21.1 µg/day, 4%), egg products and dishes (7.2 ± 15.3 µg/day, 4%), meat, poultry and game products and dishes (4.9 ± 7.2 µg/day, 3%), and vegetable products and dishes (3.7 ± 8.1 µg/day, 2%). In the non-alcoholic beverages group, water provided the greatest contribution (6.6 ± 5.5 µg/day, 38% of food group), followed by coffee and coffee substitutes (8.2 ± 18.4 µg/day, 21%). Within the cereals and cereal products major food group, regular breads/bread rolls contributed the largest amount of iodine (38.1 ± 31.8 µg/day, 72%), followed by English-style muffins, flat breads and savoury and sweet breads (5.1 ± 12.2 µg/day, 10%). The greatest contribution of cereal based products and dishes were from mixed dishes where cereal is the major ingredient (14.1 ± 22.7 µg/day, 49%). Within the fish and seafood products and dishes food group, finfish (2.1 ± 11.6 µg/day, 31%) made the greatest contribution, followed by similar amounts from packed fish/seafood (0.8 ± 5.6 µg/day, 26%) and fish and seafood products (homemade/takeaway) (2.3 ± 12 µg/day, 25%). The greatest contribution of iodine from milk products and dishes was provided by milk (32.2 ± 38.3 µg/day, 62%).
The only difference in food group contribution to iodine according to age was observed for non-alcoholic beverages (p
< 0.001), in the direction of increased contribution with decreasing age of the women (Table A1
). Regarding SES, contribution of iodine from cereals/cereal products (p
< 0.001) increased with increasing SES, while milk products/dishes showed an increasing contribution in the opposite direction (p
< 0.001) (Table A2
). Those living in areas of higher geographical remoteness had a lower contribution of iodine from fish and seafood products and dishes (p
< 0.001) and vegetable products and dishes (p
< 0.001). The most remote areas obtained significantly more iodine from cereals and cereal products (p
< 0.001), and meat, poultry and game products and dishes (p
< 0.001) when compared with all inner regional and major cities.
3.3. Association between Bread Intake and Adequacy of Iodine Intake in Women of Child-Bearing Age and Children Aged 2–18 Years
At the time of the survey only 8.0% of Australian children aged 2–18 years (n
= 142/1772) and 8.6% of women of child-bearing age (n
= 301/3496) reported consuming ≥100 g bread per day. Median bread consumption was 156.5 g/day (IQR 41–71; mean = 57 ± 33 g/day) for children. Women aged 14–50 years had a median intake of 60 g/day (IQR 41–71; mean = 58 ± 35 g/day). A number of logistic regression models were conducted to assess the effect of bread intake on adequacy of iodine intake. The proportion of children who had inadequate iodine intakes below the age-specific EAR was 8.1% (n
= 144/1772) and was highest in the oldest age groups (5.5%, 8.4%, 7.3% and 14.8%, according to age groups 2–3 years, 4–8 years, 9–13 years, and 14–18 years, respectively; I2
= 43.52, p
< 0.001). After adjusting for fish intake (Table 1
; Model 2), women of childbearing age consuming ≥100 g bread per day were six times more likely to have an adequate iodine intake than women consuming <100 g bread per day. Inclusion of dairy intake (Table 1
; Model 3) reduced the OR slightly but significance of bread intake remained. Adjustment for SES, geographical remoteness area and age (Models 4, 5 and 6) did not further influence the odds of women achieving an adequate iodine intake (i.e., had little predictive value in the model). Similar findings were found for children (Table 2
), but a higher OR was found for all the models.
In order to assess whether young children were being exposed to excessive iodine in the food supply, the proportion of children with reported iodine intakes that exceeded the age-specific Upper Level was calculated. Thirty percent of children aged 2–3 years had intakes above the UL of 200 µg/day, while 5.9% of 4–8 years old had intakes above 300 µg/day, while none of the children aged 9–14 years and 15–18 years had intakes above 600 and 900 µg/day, respectively (I2 = 333.94, p < 0.001).
3.4. Effect of SES on Bread Consumption Patterns and Association with Iodine Intake in a Subgroup of Children Aged 5–9 Years
Ten percent of Australian children aged 5–9 years (n
= 50/488) reported consuming ≥100 g bread per day. Children consuming ≥100 g bread per day had a higher median dietary iodine intake of 198 µg/day (IQR 161–238 µg/day) than those consuming <100 g of bread per day (149 µg/day (113–201 µg/day); p
< 0.001, η2
= 0.01). All children consuming ≥100 g exceeded the Estimated Average Requirement [31
], with 14% also exceeding the upper limit for their age. The proportion of children consuming ≥100 g bread per day was significantly different between all levels of SES (p
< 0.01) (Table 3
). Children from the middle socio-economic group (quintile 3) were least likely to consume ≥100 g bread per day (7%), as compared with the lowest (15%–16%) and highest (10%–13%) SES groups (p
< 0.01). The interpretation of Cramer’s V measure of effect size using Cohen’s criteria indicated a relatively weak association between SES and the level of bread consumption (V
Analysis of dietary intake data obtained from Australia’s most recent national nutrition survey indicates that iodine fortification of salt used for bread-making has the potential to improve iodine intake. We report that women consuming 100 g or more of bread per day (equivalent to approximately 3 slices) were five times more likely to achieve an adequate iodine intake (EAR = 100 µg/day) compared to those consuming less than this amount, after adjusting for age, dairy intake, fish intake, SES, and geographical location. We also investigated the impact of achieving this bread intake in children aged 2–18 years and identified a much larger magnitude of effect in this age group. Children consuming 100 g or more of bread per day were twelve times more likely to have a dietary iodine intake considered to be adequate. Given these findings, it is noteworthy that our data identified that only 8%–9% of Australian women and children are currently consuming bread at the level that was modelled by Food Standards Australia New Zealand to arrive at the fortificant level of 45 µg iodine per 100 g bread [8
]. Given this, the amount of iodine added to bread may need to be adjusted to continue to meet the needs of women, or alternatively additional vehicles for the fortificant may need to be explored. The challenge is to meet the needs of women without exceeding upper levels of iodine intake in very young children, as bread consumption in women and children differed across socio-economic groups and geographical locations within Australia. It is concerning that 30% of the youngest age group of children included in the national dietary survey (2–3 years), had reported iodine intakes that exceeded the age-specific Upper Level of 200 µg/day [31
]. Investigation of the contribution of foods to total iodine intake in younger children is warranted in future studies.
Dietary diversification is another potential way to improve dietary iodine intake. As well as fortified bread, we identified that other major sources of iodine for the total Australian population in 2011–2013 included milk products and dishes (26%), non-alcoholic beverages (15%) and cereal based products and dishes (12%). Despite being rich in iodine, fish and seafood contributed only minimally to total iodine intake due to low reported consumption, as has been reported by other studies [23
]. Previous studies in pregnant Australian women identified that dairy foods were a major contributor to total iodine intake (57%–62%), followed by bread and cereals (19%–21%) with minor contributions from fish and seafood (3%–8%) [14
Pregnant women are most at risk for iodine deficiency because of the increased iodine requirements of both the mother and unborn foetus. However, pregnant women were not adequately sampled in the AHS which is why we have focused the current analyses on women of child-bearing age. Women aged 14–50 years had a mean dietary iodine intake of 155 µg/day, which is only a 9 µg/day increase in mean iodine intake from the 146 µg/day iodine intake estimated from the last national nutrition survey conducted in 1995 [9
], despite improvements in food composition data during this time. The fortification program was estimated to increase iodine intake in women of childbearing age by 46 µg/day [8
]. Compared to the EAR for pregnancy (160 µg/day), we found that only women consuming ≥100 g of bread per day would be able to meet this, and thereby be adequately protected if they were to become pregnant (and not alter their intakes). It is important to note that the mandatory fortification program was not designed to meet increased requirements during pregnancy and lactation, and instead iodine supplementation has been recommended by the NHMRC [35
For children, we investigated the impact of bread consumption on iodine intake across the age range of 2–18 years. We also investigated the impact of socioeconomic status on bread and iodine intake in a sub group of children aged 5–9 years. This subgroup was chosen because primary schoolchildren are recommended by the ICCIDD as being the universal reference group for assessing iodine status in populations. Spot urinary iodine concentrations (UIC), expressed as median values, are compared against reference values of 100–199 µg/L as being adequate [36
]. Another reason to choose this age group rather than pre-school aged children was guided by the observational data from Tasmania that has demonstrated an association between mild maternal iodine deficiency during pregnancy and reduced educational attainment in children that this is evident at the age of 9 years [37
]. Similarly, in the United Kingdom, mild maternal iodine deficiency has been shown to result in decreased IQ in the offspring at the age of 8 years and decreased reading comprehension by age 9 years [38
]. It is unknown whether such deficits can be reversed through later iodine supplementation or increased intake. However, three randomised controlled studies support the benefit of an improved iodine status on cognitive functioning in children aged between 6 and 13 years. It is therefore important to identify dietary sources of iodine intake in this age group in order to recommend dietary modifications to address inadequate intakes, for improved health outcomes, if necessary.
The Australian Health Survey collected UIC in a biomedical subsample of the survey, in participants aged 5 years and older. An adequate median UIC was found across all age and sex groups, post fortification [39
], with children aged 5–11 years having the highest median UIC (177 µg/L), and only 5.9% of this group having iodine levels under 50 μg/L. This is a major improvement compared to the mild iodine deficiency identified in schoolchildren aged 8–10 years across five mainland states in the Australian National Iodine Nutrition Study, 2003–2004 [2
]. The current analysis of dietary iodine intake data allows identification of food sources, including the contribution of fortified bread, to total iodine intake. Additionally, identification of socioeconomic and geographical determinants of iodine intake are useful for dietary guidance purposes and monitoring of the iodine fortification programme.
We found associations with age, SES and geographic remoteness area. However, the small effect sizes of these differences suggest that these factors are of minor consequence. Both women and children in the lowest SES group and those in regional, rather than major cities, had higher bread intakes. This is consistent with findings from New Zealand, which found that low SES pregnant women had a higher iodine intake from bread compared to women in higher SES groups post fortification [18
]. Other foods that were found to be more important sources of iodine for high SES groups compared to those in lower quintiles, included fish and seafood, eggs, and vegetables. We hypothesize that this may be due to the high cost of seafood, often making it unaffordable for lower SES groups [16
These analyses have several limitations. Dietary data collected for the NNPAS consisted of two 24-h recalls, and was adjusted for within person variation by using an average of the two day dietary data. It is well known that repeated 24 h recalls may not be a suitable method for estimating “usual intake” as the method does not account for all sources of error [27
]. Under-reporting is a major limitation associated with nutrition surveys using self-reported intake due to a widely observed tendency for people to underestimate their food intakes [40
]. In this regard, the contribution of iodised table salt was not assessed in the survey. Australia does not implement universal salt iodisation, but manufacturers are permitted to add iodine to table salt voluntarily [8
]. In non-quantitative questions, 29% of NNPAS participants reported using iodised salt during food preparation and 21% reported using iodised salt at the table, thus the current analysis probably underestimates total dietary iodine intake [25
]. However, we have previously found that self-reported use of iodised table salt is unreliable, and did not differ between pregnant women who were iodine deficient or iodine replete [3
There is a possibility that the 24-h recall method may have missed foods that are high in iodine but not regularly consumed, such as fish and seafood. A further limitation is that SEIFA, which was used in the survey to report SES, represents an average of all people living in an area; it does not represent the individual situation of each person. Larger areas are more likely to have greater diversity of people and households. However this measure of socioeconomic disadvantage is considered the most appropriate for use in a national survey of this scale [29
Despite these limitations, the NNPAS data are the most current and comprehensive nationally representative data available on food and nutrient intakes of Australians. This data contributes to evidence regarding the impact of the iodine fortification program and has identified factors associated with group level reported adequate iodine intake on a national level.