Abstract
Introduction:
National programs of salt iodization were implemented in Brazil to combat iodine deficiency (ID) in children of school age. Currently, there are limited data in Brazil on those still vulnerable to this deficiency and the state of nutritional iodine status in the northeast region of Brazil, where children are vulnerable to malnutrition.
Objective:
The aim of this study was to analyze the iodine nutritional status, household food insecurity, socioeconomic and demographic characteristics among schoolchildren from the public school system living in state the state of Bahia, Brazil.
Methods:
A cross-sectional study was conducted on 1419 schoolchildren in Bahia between the ages of 6 and 14 years old. Anthropometric parameters, urinary iodine concentrations (UIC), and thyrotropin (TSH) measurements were evaluated from blood spots on filter paper.
Results:
The mean UIC was 206.4 ± 80.5 μg/L, with a median of 221.6 μg/L, indicating sufficient iodine intake in the region. Low urinary iodide concentration (<100 μg/L) was detected in 12.3% of the schoolchildren (n = 174), with 6.2% with mild (<100 μg/L), 3.0% with moderate (20–49 μg/L), and 3.1% with severe ID (<20 μg/L). Moreover, 9.4% (n = 134) had a urinary iodide concentration of >300 μg/L, indicating the coexistence of excessive iodine intake (EII). The mean TSH was 1.0 ± 0.6 mIU/L. The body mass index category “overweight/obesity” was a protective factor against EII (odds ratio [OR] = 0.64 [confidence interval (CI) 0.4–1.0]; p = 0.07). Urban areas (73%) had a mean UIC of 213.1 ± 80 μg/L compared with 176.8 ± 76.1 μg/L in rural areas. The risk for EII increased in children living in a house with more than six people (OR = 1.62 [CI 0.9–2.6]; p < 0.05) and water consumption from shallow wells (OR = 1.70 [CI 0.9–3.1]; p = 0.09). The risk of ID was increased by 70% in schoolchildren who had moderate or severe food insecurity (OR = 1.70 [CI 0.9–3.0]; p > 0.05).
Conclusion:
A significant proportion of schoolchildren still have ID or EII in the northeast region of Brazil, emphasizing the importance of committed public policies to address this problem. Socioeconomic factors and the lack of education about nutritional importance of iodine were important influencing factors in the presence of ID in schoolchildren.
Introduction
I
Research has shown that ID has a well-established socioeconomic component (7,8). It has been demonstrated that severe ID is particularly prevalent in poor and less-educated people living in less-developed countries. Education has been shown to be a strong predictor of iodine intake levels (9) at both the population and individual level. For example, in 2000, the Belgium population began to consume more foods with iodine, resulting in a silent prophylaxis process, even before the salt iodization program was implemented (10), or as documented at the individual level in Indonesian (11), African (8), and Asian populations (12) where the mother's education is the strongest predictor of inadequately low iodine intake in children from urban slums and rural areas. In Africa, where 40% of the population (321.1 million) has insufficient iodine intake, those of lower socioeconomic status were less informed about ID-related disorders (7), thus clearly linking, as one might expect, level of education and poverty.
In Latin America, iodine nutrition has improved considerably over the last decade (13,14). Currently, with the exception of Guatemala, ID is no longer present in Latin America, with the levels of iodine nutrition having been directly impacted by the salt iodization programs. However, three countries— Chile, Ecuador, and Brazil—are now considered at risk for iodine excess, along with its adverse health consequences (1). Recently, a Mexican study evaluating ID and excessive iodine intake (EII) in children from state elementary schools found both a positive correlation between urinary iodine concentration (UIC) values and the prevalence of overweight/obesity, and a significant negative correlation between UIC and index of social development (15). However, this study was not able to clarify the association between poverty and ID completely, since only 4% of schools had insufficient iodine intake, and half of them were living in municipalities with a higher social development index (15).
In Brazil, a national survey conducted in 1994 detected a relatively low iodine intake (median UIC <100 μg/L) in >50% of the 20,000 schoolchildren evaluated (16). As a consequence, the Brazilian health authorities increased the iodization of table salt from 40–60 mg/kg to 40–100 mg/kg in 1998 (16). Later, results of the Thyromobil Project, conducted after the iodine fortification, documented that the examined subjects had an elevated median UIC (300 μg/L), indicating that the Brazilian population had ingested excessive levels of iodine from 1998 to 2003, after which iodization of table salt was lowered to 20–60 mg/kg (17). Ten years after, in 2013, the levels of salt iodization were further reduced to 15–45 mg/kg (18), although the Brazilian Endocrine Society has expressed concerns about this reduction (19).
A recent meta-analysis has shown that the actual ID prevalence in Brazil is very complex due to the high heterogeneity and bias of available studies (20). Several factors and regional variations may influence iodine intake that must be considered in Brazil, such as changes in diet, differences in goitrogen consumption (including cassava), geographical and social demographic characteristics, and the availability of processed foods—all factors that may lead to a coexistence of ID and EII, depending on the regional characteristics (20). Without doubt, the scarcity of new representative national data is worrisome, mainly because most of the previous estimates were based on subnational data that may under- or overestimate the extent of ID (20). Moreover, the majority of studies (94.1%) were performed in the southern and southeastern regions of Brazil, known to be more developed and easily accessible areas where the population potentially has greater access to iodized salt, and may not be representative for Brazil as a whole (20). Moreover, it is important to note that all surveys were conducted when the level of salt iodination was at 20–40 ppm (20), and the iodine intake has yet to be evaluated since the further reduction in 2013.
The objectives of the present study are twofold: (i) to assess the current nutritional iodine status of schoolchildren from the public school system, a population considered vulnerable to ID, and (ii) to evaluate possible associations with socioeconomic, demographic, and household food insecurity (HFI) indicators.
Methods
This study was approved by the Federal University of Bahia—Ethical Committee for Research Projects and carried out in accordance with the Declaration of Helsinki (21) of the World Medical Association. Participation was voluntary with written consent obtained from at least one parent or guardian. The data are reported in accordance with the STROBE reporting guidelines for observational research (22).
Study design
A cross-sectional study was performed using a multistage cluster sampling technique evaluating schoolchildren's height, weight, UIC values, socio-demographic variables, and iodine consumption and storage. Recruitment was performed in elementary public schools at the middle to lower socioeconomic level between October of 2013 and September of 2014 in four micro-regions in Bahia: Alagoinhas, Salvador, Santo Antonio de Jesus, and Santa Maria da Vitoria. In each city, two to six schools were randomly selected to represent a specific geographic area of the state (coast, northeast, and west region) and to include both urban and rural areas. In all municipalities, the sources of dietary iodine were the local foods and variable amounts of iodized salt.
Setting
The study was performed in the northeastern state of Bahia (20°30′–20°30′ N, 20°30′–20°30′ W), approximately 1500 km to the northeast of Brasilia in Brazil. The Brazilian northeast is the poorest region in Brazil, with a median annual income of U.S.$1800 (23) and a human development index of 0.660, which is considered very low and at position 22/27 states in Brazil (24). According to the 2014 national census, the state of Bahia has 15,126,371 inhabitants with 2,343,159 between 6 and 14 years old. The total population of the four micro-regions evaluated in this study represents 0.06% of the total population of the state (25) (Table 1).
As detailed in IBGE 2013 Estados@—Bahia (25).
Subjects
It was calculated that the study needed 1314 children or more based upon a single population proportion formula, utilizing a recent meta-analysis, which estimated a 15% prevalence (p = 0.15) of ID (26), a Z-value of 1.96 for a 95% confidence level, DEFF of 1.5 (expected sampling error for small populations), and a degree of precision of 0.2 for the study.
The inclusion criteria were (i) attending one of the public schools in the study, and (ii) between 6 and 14 years of age. Children were excluded from participating in this study if they were outside the age range specified for inclusion, reported a chronic disease or the use of chronic medications or iodine supplements, or were pregnant at the time the study was conducted.
Growth
Both height and weight were measured using standard anthropometric techniques (27). The anthropometric assessment is described in Table 2. The software ANTRHO PLUS (World Health Organization [WHO], Geneva, Switzerland;
UIC analysis
Spot urine samples were collected in universal containers and transferred to monovette tubes for transport and storage at –20°C until analysis. The adapted Sandell–Kolthoff reaction was used to determine urinary iodine levels (26,28). The UIC was determined from a catalytic reduction of ceric ammonium sulfate in the presence of arsenious acid utilizing a spectrophotometer (Uv-Vis; wavelength 405 nm) to verify the ceric ammonium sulfate reduction. For each child's sample, the analysis was performed in duplicate. To establish a standard curve, a standard iodine solution was used with potassium iodate. UIC values from populations are usually not normally distributed. Therefore, the median rather than the mean was used as a measure of trend. The iodine nutrition status classification was based on the criteria established by the WHO (29).
Thyrotropin dosage procedures
Thyrotropin (TSH) measurements were performed according to Ward et al. (30). In summary, whole blood was collected with a lancet from the children's finger and dropped on SS 903 filter paper. TSH was measured by an immunofluorimetric method—Luminex—using a monoclonal capture antibody bound to a solid phase and a monoclonal detection antibody. This method has a sensitivity of 0.1 mIU/L and intra- and inter-assay coefficients of variation of 5% and 10%, respectively. The measurements were performed by the Association of Parents and Friends of Exceptional Children/Salvador-BA (APAE), a laboratory accredited by the Ministry of Health that is used for screening for congenital hypothyroidism. The samples were stored under refrigeration and transported to the APAE laboratory at room temperature. The reference value used was 0.72–6.0 mIU/L.
Socio-demographic and health questionnaire
Socioeconomic, demographic, and health information was collected by applying a semi-structured questionnaire addressing: (i) socioeconomic conditions—home location (rural or urban), household income, income spent on food, number of people in the household, and food and nutritional security situation; and (ii) biological/health data—age, sex, water source (urban treatment or surface water), patient and/or family history of thyroid disease, as well as consumption and storage of iodized salt. Food insecurity status was evaluated using responses to the core set of 15 questions taken from the Brazilian scale of food insecurity (31) and was scored in accordance with established procedures.
Data processing and statistical analysis
All data are expressed as mean ± standard deviation, median, range or frequency distribution, as appropriate. Data were stratified by level of UIC, age, sex, and different groups of socio-demographic and geographic characteristics to explore influencing factors. To determine statistical difference between groups, a p-value of <0.05 was considered significant in t-test, Pearson's chi-square test, Fisher's exact test, and Mann–Whitney U-test calculations. All statistical analyses were made using IBM SPSS Statistics for Windows v22.0 (IBM Corp., Armonk, NY).
Results
Subjects
A total of 1419 schoolchildren from 17 schools were included (70.6% rural and 29.4% urban). The children were regionally distributed among the four micro-regions as follows: Alagoinhas (n = 218), Salvador (n = 197), Santo Antonio de Jesus (n = 376), and Santa Maria da Vitoria (n = 628). The male/female ratio was 1.05, and the mean age of the children was 11 ± 2.83 years. Table 1 shows the most relevant socio-demographic information, including total population, school population (32), and Human Development Index (Programa das Nações Unidas para o Desenvolvimento [PNUD]: Human Development Report 2014) of each municipality studied (33). A summary of the main findings can be found in Table 3.
UIC
The total average UIC was 206.40 ± 80 μg/L, with a median of 221.60 μg/L (25th–75th percentile 159.32–271.20), indicating sufficient iodine intake. The majority of schoolchildren (80.9%) fell within the normal range for UIC (100–299 μg/L). A low UIC (<100 μg/L) was detected in 12.3% (n = 174) of the schoolchildren. Of these, 6.2% (n = 88) had UIC values <100 μg/L (mild ID), 3.0% (n = 42) between 20 and 49 μg/L (moderate ID), and 3.1% (n = 44) <20 μg/L, indicating severe ID. EII was found in 9.4% (n = 134) of the samples, with a UIC >300 μg/L. The average UIC was 213.1 ± 80 μg/L in urban areas and 176.8 ± 76.1 μg/L in rural areas (p < 0.001). Supplementary Table S1 (Supplementary Data are available online at
TSH level concentration
The TSH levels (determined from 880 blood samples) ranged from 0.24 mIU/L to 7.71 mIU/L, with a mean of 1.01 ± 0.55 mIU/L and a median of 0.89 mIU/L. Only one schoolchild had a TSH >6.0 mIU/L (7.71 mIU/L). However, for this patient, the UIC pointed to a more than adequate iodine nutrition status (243.70 μg/L).
Anthropometric, socio-demographic, and food insecurity status
An anthropometric evaluation found 72% of the schoolchildren were within the normal weight for age and sex. There were 0.7% having markedly low weight and 4.0% with low weight, and 15% were classified as overweight, 6.2% obese, and 2.1% severely obese (Table 2). It was noted that 48.4% of the families interviewed had a monthly income lower than a single minimum wage, and of these, 32.6% had less than half the minimum wage for provision of their basic needs (data not shown). Concerning the knowledge about the consumption of iodized salt, the risk for ID increased by 16% for children whose parents or guardians reported lack of knowledge about the use of iodized salt, but the association was not significant (p > 0.05). On the other hand, the risk of EII reduced by 64% for those whose caregivers reported not consuming iodized salt (p < 0.05; data not shown). Further, dietary factors that could change the iodine nutritional status were investigated, such as goitrogenic foods, particularly cassava flour, and the use of supplements. It was found that there was a large consumption of cassava flour (90.8%), with 52.9% of respondents reporting daily intake (data not shown).
Multiple linear regression analysis
Table 2 shows the analysis including UIC stratified by age, sex, body mass index/age (BMI/A), home location, income (in minimum wages), number of people in the household, origin of water consumption, type of water treatment, access to electricity, consumption and storage of table salt, salt storage area, use of industrial seasoning, use of nutritional supplements, cassava intake, and the frequency of cassava intake.
Overweight/obesity (odds ratio [OR] = 0.64 [confidence interval (CI) 0.4–1.0]; p = 0.07) and the use of industrial seasoning (OR = 0.65 [CI 0.4–0.9]; p < 0.05) protected against EII. Risk for EII increased for children living in a house with more than six people (OR = 1.62 [CI 0.9–2.6]; p < 0.05) and consuming water from shallow wells (OR = 1.70 [CI 0.9–3.1]; p = 0.09; Supplementary Table S1). There was a 70% greater risk for IDD in those with moderate and severe food insecurity by HFIAS (OR = 1.70 [CI 0.9–2.9], p = 0.06; and OR = 1.69 [CI 0.9–3.0], p = 0.07, respectively; Supplementary Table S1).
Discussion
This study is the largest of its type to be performed in this region, and brings new information about the current nutritional iodine status in schoolchildren from public schools in Bahia, Brazil. In this public schoolchildren population, an overall mean UIC of 206.30 ± 80.6 μg/L was found, indicating an iodine intake mildly above requirements (200–299 μg/L) established by WHO criteria. However, 12.3% of schoolchildren had UIC levels suggestive for ID (3.1%, 3.0%, and 6.2% of mild, moderate, and severe ID, respectively), and 9.4% had a level suggestive of EII.
Despite important differences in geography, altitude, and human development index, significant differences in UIC levels were not observed between the four analyzed micro-regions. However, a significant difference was found between UIC values from children living in urban compared with those living in rural areas (213.1 ± 80 μg/L vs. 176.8 ± 76.1 μg/L, p < 0.05). Similar to another study (17), it was found that individuals living in coastal regions had higher UIC levels compared with individuals living in more remote areas (17). The coastal region of Salvador that was evaluated had higher UIC levels (253.54 ± 75.84 μg/L, but this region was also found to have higher social development and greater access to other dietary sources of iodine compared with the other micro-regions. Furthermore, in Salvador, there was a clear preponderance of UIC in the range of 200–299 μg/L, indicating a high risk of EII in this area.
The present study found that currently, in the historically ID endemic micro-region of Santa Maria da Vitoria, there were improvements of the iodine nutritional status, though the region still maintains the lowest mean UIC (127.60 ± 34.19 μg/L) and highest prevalence of ID (15.8%) when compared with the other areas in Bahia. It was found that in this micro-region, there is a coexistence of both ID (defined as <100 μg/L) and iodine excess (>300 μg/L). The coexistence of vastly different iodine nutrition within the same region has been found in several Latin America studies, such as the Thyromobile Project conducted in Latin America from 2000 to 2004 (11.3% ID in an iodine sufficient region) (17), the study by Camargo et al. conducted in 2008 in the city of Sao Paulo including 1085 adults (7.8% ID and 45.1% EII) (34), and in the study by Rates et al. performed in 2010 in 486 adolescents in the state of Minas Gerais (5.6% and 2.5% ID and 16% and 28.3% in 10–14 and 14–19 year olds, respectively) (35).
A positive correlation was not found between TSH levels and UIC (parametric Pearson correlation r = 0.115; p = 0.002), indicating that in this study, iodine nutrition status did not play an important role for defining the TSH level. This finding is supported by Ristic-Medic et al. (36), who suggested that in general, TSH levels have limited utility in evaluating children and adolescents, but are better indicators of iodine nutritional status in pregnant and lactating women. However, it should be noted that the low and high UIC levels may simply reflect daily variation, and the median is expected to be a more effective indicator of nutritional iodine status.
Aside from daily variations, the National Health and Nutrition Examination Survey 2003–2006 reported that socioeconomic factors and variables such as age, sex, ethnicity, education, and BMI may impact UIC differences in the nutritional iodine status of children (37). The identification of factors associated with a low (UIC <100 μg/L) or a high UIC (>300 μg/L) in the same population is of importance. However, little is known about the correlation of socio-demographic factors with the iodine nutritional status in developing countries such as Brazil.
In the investigation of dietary influences, it was found that the daily cassava flour intake was associated with a 43% greater risk for ID and a reduction of 29% in EII. However, these associations were not significant (p > 0.05). The high intake of cassava flour found in this study was similar to that found by a previous study in the northeast of Brazil (38). It is well known that thiocyanate and perchlorate are elements found in some plants and can inhibit thyroidal iodide uptake because they are competitive substrates of iodide for the sodium–iodide symporter (39). It has also been suggested that changes in eating behavior could impact both global nutritional indicators and UIC levels, with the increase of consumption of processed foods such as canned goods, snack foods, and processed meats (40,41).
No significant correlation was found in this study between UIC and BMI/A (r = 0.079; p = 0.037), and the risk of EII was found to be 36% lower in overweight/obese children (p = 0.07; Supplementary Table S1). This is contrary to the hypothesis of García-Solis et al. (15), who suggested that a high consumption of snack foods rich in energy and iodized salt could be the etiology of the positive correlation found between UIC and BMI (r = 0.47; p < 0.005), and overweight/obesity (r = 0.41; p < 0.05) in their 2013 Mexican study.
Globally, the iodine concentration in drinking water has been shown to vary greatly, both between and within countries. In the present investigation of this factor, it was found that the use of water of shallow wells or cisterns for drinking increased the risk of EII by 69%, but this association did not reach significance (p > 0.05). While a survey in Somalia revealed that the excessive consumption of iodine was associated with the household drinking water source (42), this may be a more regionally specific characteristic, which needs further investigation in order to delineate the levels of iodine concentration from household drinking water sources.
There was a significant association between several socioeconomic factors and iodine nutritional status. It was found that the presence of food insecurity increased the risk for ID by 70% (p = 0.06; Supplementary Table S1). This is expected, as ID has historically been considered an issue for developing countries, especially those living in extreme poverty and deprivation, who are among the most vulnerable. It is well established that poverty and malnutrition disrupt the normal course of childhood development, and if it is associated with mild ID, damage in full intellectual potential might occur (43,44). Moreover, 24.6% of parents or guardians were unaware of the concept of iodized salt and the importance of the micronutrient for child health, despite a national salt iodization having been implemented since 1977 (17). Even more telling is the fact that 7.7% denied the use of iodized salt, suggesting a lack of knowledge about it. These findings on the impact of education on nutritional iodide status are in line with those of Macedo et al. (45), who investigated factors that could be related to the iodine deterioration in salt, such as storage form and expiration date. This study suggested that there is a higher ID risk among students who lived in homes where caregivers did not have knowledge about the concept of iodized salt (45).
One of the limitations of this study concerns the selected study sites. Efforts were made to obtain information about different environmental and social strata to investigate their influence on iodine nutritional status, but the sites should not be considered representative for the whole of Brazil. Therefore, the data presented here should not be used to develop nationwide programs, and further evaluations need to be performed at other sites. However, the current study does provide a more current understanding of iodine levels in children in the northeast of Brazil.
It is clear that much has changed in the Bahia region since the early 1990s, where a survey detected that despite the salt iodization program, there was a high prevalence of ID in the municipalities of Cocos, Canapolis, and Correntina in the State of Bahia, with median UICs of 44 μg/L, 55 μg/L, and 68 μg/L, respectively (28). More than 20 years later, and after several changes in nutrition and national salt iodization programs (including the last salt iodization reduction in 2013 to 15–45 ppm) (18), clear improvements in nutritional iodine status were found among children in the four regions that were assessed. On the one hand, these findings are encouraging for the health of the overall population. However, unfortunately and all too frequently, those who remain most vulnerable to iodide deficiency stem from poor and uneducated families. It would be unwarranted to claim that a uniform salt iodization is ineffective in Brazil, as it is likely a problem that requires multiple dimensions of intervention that must include education of iodide nutrition. Understanding the complexities of the individual iodide nutritional status in Brazil is difficult, not only due to the vast territory and different natural environmental, but also due to the dramatically disparate socioeconomic dimensions in the country.
In conclusion, it was found that the overall UIC levels in the Bahia region have improved. Nutritional habits and TSH levels were not associated with UIC levels in this population. National programs to reduce iodide deficiency should target educating individuals in Brazil from the lowest socioeconomic strata, independently of the nutritional iodine status of the overall region in which they reside.
Footnotes
Acknowledgments
This study was supported by State of Bahia Research Foundation (FAPESB Edital 029/2012) grant (TOU PET0002/2013). A grant by CAPES, supported R.O.C. We are grateful to the authorities in each city studied (Alagoinhas, Cruz das Almas, Salvador, and Santana e Santa Maria da Vitoria), parents, and schoolchildren participants. We gratefully acknowledge the contribution and support of Regina Catarino, Caio Castro, Helvio Ramos, and Walnice Ramos. We would also like to thank the congressman Paulo Azi.
Author Disclosure Statement
There are no conflicts of interest.
