1. Introduction
Iodine is an essential micronutrient for the human body. It is an indispensable component for the synthesis of thyroid hormones and plays important roles in promoting body growth and brain development, regulating metabolism, and maintaining normal function of the cardiovascular and digestive systems. Either excessive or insufficient iodine intake will induce abnormal functioning of the thyroid gland, thereby causing adverse effects on the body. The Wolff–Chaikoff effect, an acute and temporary inhibition of the synthesis and secretion of thyroid hormones, occurs in cases of excessive iodine intake. Normally, the body will adapt to and escape from this effect after a few weeks due to the auto-regulatory mechanism of the thyroid gland. However, the long-term intake of excessive iodine will lead to the imbalance and dysfunction of this self-regulation, resulting in hyperthyroidism or hypothyroidism, as well as autoimmune thyroiditis. Iodine deficiency can cause varying degrees of damage to the body depending on various factors, including the severity of deficiency, time of occurrence in the life cycle and differences in individual responses to iodine deficiency. A compensatory goiter will be induced even when one is mildly deficient in iodine. Other health consequences of iodine deficiency include stillbirth and congenital anomalies in the fetus, cretinism and increased infant mortality among neonates, impaired mental function and delayed physical development in children and adolescents, iodine-induced hyperthyroidism in adults and spontaneous abortion in pregnant women. These symptoms are collectively known as iodine deficiency disorders (IDD) [
1,
2].
Approximately 80% of the iodine required for the human body can be obtained through dietary intake, while drinking water accounts for 10–20% and atmospheric sources provide less than 5% [
2]. Marine products from the ocean are the main sources of iodine in nature, such as seaweed, kelp, shellfish and seawater fish [
3]. Even if the intake of iodine in the diet is insufficient, the iodine metabolism cycle will accelerate and maintain the normal function of the body in a compensatory form. When iodine intake is completely absent, the iodine store in the body still can meet its needs for the next 2–3 months. However, IDD will be triggered when compensatory mechanisms are insufficient to cope with the body’s needs [
2].
IDD can significantly restrain intellectual development and therefore represents a leading global nutritional challenge that poses a threat of brain damage. Studies have shown that children residing in regions with inadequate iodine intake exhibited an ap-proximate 13.5-point reduction in intelligence quotient (IQ) scores. This reflects that iodine deficiency affects the learning ability of school-age children and even their quality of life and long-term productivity in those regions [
1]. A longitudinal study of parents and children from the United Kingdom assessed the association between maternal iodine status and children’s IQ at the age of 8 years and reading ability at the age of 9 years. The data supported the hypothesis that low maternal iodine status was associated with an increased risk of sub-optimal scores for IQ at age 8 and reading accuracy, in addition to comprehension and reading scores, at age 9 [
4]. Shenzhen of Guangdong Province, China, was originally a mildly iodine-deficient area. Since the implementation of salt iodization measures in 1996, the average IQ score of 8–10-year-old school-age children has shown an upward trend, increasing from 100.88 in 2002 to 108.45 in 2014 [
5].
In accordance with statistical data provided by the World Health Organization (WHO), one can extrapolate whether a country’s population is afflicted by iodine deficiency from the prevalence of iodine insufficiency among pupils aged 6–12 years. The current estimates suggest that the proportion of individuals affected by inadequate iodine intake globally is as high as 31%, with particularly concentrated rates observed within regions of Southeast Asia and Europe [
1]. Although the condition of IDD may vary in severity across different countries, it can be prevented conveniently and economically. Compared with other micronutrient deficiencies, it is less affected by low income or poor-quality in diets of the population [
6]. The WHO pointed out that the serious health effects caused by a lack of iodine could be eliminated by adding just a small amount of iodine to table salt in daily life; thus, governments around the world should actively face and address this public health problem [
1].
Considering that adolescents are in a stage of growth and development and have an increased demand for iodine and are also more autonomous in their dietary choices and begin to establish dietary patterns in adulthood, this study aimed to evaluate iodine intake, the main food sources of iodine and the intake frequency of iodine-rich foods among secondary school students in Macao, build a foundation for iodine-related nutrition research and draw public attention to adequate iodine intake in Macao.
4. Discussion
Currently, mandatory salt iodization is legislatively mandated in over 120 countries, whereas voluntary salt iodization is practiced in more than 20 countries [
12]. Overall, the percentage of the world’s population who consume iodized salt is 89% [
13]. The 2021 annual report of the Iodine Global Network (IGN) evaluated the general populations of 111 countries, which adequate iodine intake exhibited in a total of 141 nations with available data. This represents a two-fold increase from the levels observed over the past two decades, which highlights the efficacy of salt-iodization-based interventions in combating IDD. However, despite this positive trend, there remain 19 countries in which inadequate iodine intake persists owing to factors such as the low coverage and suboptimal utilization of iodized salt [
14].
The major methods of iodine supplementation in the diet are using iodized salt and eating iodine-rich foods. In addition, nutritional supplements can also be used as a source of iodine. Based on the WHO recommendation, the daily iodine intake for adolescents is 150 µg. However, from the results of the I-FFQ in this study, it was found that the median daily iodine intake of secondary school students in Macao was only 74.4 µg, which is an inadequate level, and this also tended to decrease with age or grade. Although the daily iodine intake was significantly higher among iodized salt users, overall, nearly 90% of the subjects did not use iodized salt and were not aware of the type of salt they used at home. Apart from the use of iodized salt, the subjects did not consume seaweed, mushrooms and seafood as the main sources of iodine in their diets and did not use these types of foods with higher iodine to compensate for their insufficient iodine intake due to a lack of use of iodized salt. Thus, without the habits of using iodized salt or obtaining enough iodine from the diet and increasing the frequency of iodine intake, the risk of iodine deficiency will be greatly increased.
As early as 1994, the WHO and United Nations International Children’s Education Fund (UNICEF) recommended Universal Salt Iodization (USI) as a safe, economic and sustainable strategy to ensure adequate iodine intake for populations at a health policy joint meeting. Nearly all countries with iodine deficiency agree that USI is the most cost- effective countermeasure for eliminating IDD. The USI covers the addition of iodine to salt used for humans and livestock, including salt used in the food industry. The sufficient iodine supplementation of table salt provides adequate iodine availability to the population, and this needs to be implemented on a continuous and self-sustaining basis. The WHO recommendation for iodine added to table salt is 20–40 mg/kg. Countries have also formulated different recommendations according to the needs of their residents [
1], such as Australia, with 25–65 mg/kg, New Zealand, with 25–65 mg/kg [
15], France, with 18 mg/kg, Germany, with 15–25 mg/kg, Denmark, with 20 mg/kg [
16], and Switzerland, with 20–25 mg/kg [
17]. The “Iodine of edible salt” (GB 26878-2011) standard issued by China in 2012 stipulates that the average amount of iodine added to edible salt should be 20–30 mg/kg, and the allowable fluctuation range is ±30% [
18].
The prevention and treatment of iodine deficiency disorders is a public health issue of global concern. Many countries have actively performed the evaluation and monitoring of people’s iodine intake and formulated strategies and regulations according to local conditions to improve the iodine intake of their residents. On the contrary, there are currently no iodine-related supplementation measures, iodine intake assessments or research data in Macao, and the use of iodized salt in Macao is not widespread. Therefore, continuous assessment and the regular adjustment of measures are required to ensure that each population maintains an appropriate level of iodine intake in different life stages.
The median urinary iodine is conventionally used as an objective biological indicator to evaluate the iodine nutritional status of the population. However, due to various considerations such as human resources, time limitations and respondents’ acceptance, the median urinary iodine indicator is more likely to be affected by recent iodine intake. Thus, a food frequency questionnaire was used to evaluate the long-term dietary iodine intake of the subjects in this study.
The advantage of using the FFQ as a dietary survey tool is that it can be used to quickly obtain the types and amounts of foods that are often consumed, which can reflect the long-term nutrient intake pattern and serve as a basis for studying the relationship between dietary patterns and chronic diseases. The results can also be used as a reference for dietary guidance and the health education of the population. Countries currently using the FFQ to assess iodine nutritional status include the United States, Finland, Colombia [
19], Australia [
8], New Zealand [
20], the UK [
21], Poland [
22], Denmark [
23], Norway [
24], China [
25] and Malaysia [
26]. With the popularization of the internet, many countries have carried out online dietary evaluations through the internet and mobile phone applications [
27,
28]. Compared with paper questionnaires, the FFQ is not only more accurate, efficient and cost-effective but also reduces errors caused by human operations and increases acceptance among participants [
29]. For example, food frequency questionnaire survey methods include “Food4Me” in Europe [
30], the “SFFFQ” in the UK [
31] and the “QFFQ” in South Africa [
32]. The 24 h diet review methods include the “ASA24” in the United States [
33], “Oxford WebQ” in the United Kingdom [
34], “myfood24” [
35] and “ INTAKE24” [
36].
Although the reliability of the iodine food frequency questionnaire has been confirmed by many studies, the questionnaire has been widely used [
8,
21,
25], and many countries have carried out online dietary evaluations on the internet and mobile applications [
27], the food frequency questionnaire method used here can only analyze the iodine intake of the research subjects from a dietary perspective. There are still shortcomings that may lead to errors, including the facts that the survey method is qualitative rather than quantitative, cooking oils and seasonings can easily be overlooked, and food portion estimation can be inaccurate. Hence, it is necessary to perform median urinary iodine measurements for Macao residents, as this is the most accurate and objective indicator for evaluating the iodine intake status of the population. From the results of the median urinary iodine measurements, we can formulate comprehensive regulations and action plans for achieving the goal of IDD prevention.
Moreover, individuals should proactively seek to gain more iodine-related knowledge and understand the recommended intake of iodine for their age. They should also use iodized salt in their daily diets according to their dietary habits and moderately consume iodine-rich foods such as seaweed, kelp, shellfish and seawater fish to ensure that their iodine intake is within the appropriate range. Irrespective of whether iodine is sourced through iodized salt or natural food, it is essential to account for the potential loss of iodine or other essential nutrients due to various environmental conditions, including cooking and storage. A judicious approach to cooking techniques can minimize nutrient loss by reducing the duration of exposure to high temperatures. Cooking methods such as steaming and stir-frying are preferable over high-temperature techniques such as deep-frying, which may lead to a diminished iodine content when preparing dishes. Moreover, iodized salt should be added to meals after culinary preparation but prior to serving in order to maximize the preservation of the iodine content. Finally, the storage of iodized salt in an opaque, tightly sealed container has been found to be effective in maintaining its iodine content while protecting it from light [
9].