Salt Used for the National School Nutrition Program (NSNP) in Rural Schools of Limpopo Province, South Africa, has Adequate Levels of Iodine

Background Salt iodisation is considered the most effective long-term public health intervention for achieving optimal iodine nutrition. Effective salt iodisation is a prerequisite for the sustainable elimination of iodine deficiency disorders. The aim of this study was to determine iodine concentration of salt used for the National School Nutrition Program (NSNP). Methods A cross-sectional study was conducted in 359 food handlers from Vhembe and Mopani districts of Limpopo Province, South Africa. The questionnaire was administered to solicit data on demographic information, general questions on salt fortification, and iodine nutrition knowledge. After the interviews, two tablespoons of salt used for the NSNP food preparation was collected from 318 schools in small zip-lock plastic bags. The salt samples were coded and stored at room temperature and protected from light and moisture until the time of analysis. Salt iodine concentrations were determined at the North-West University (NWU) in Potchefstroom by means of the iCheck test method. Results The median iodine concentration of both Mopani (31.65 ppm) and Vhembe (32.56 ppm) districts signified adequate iodine levels. Of 318 salt samples, 113 (71%) samples in Mopani and 104 (65%) in Vhembe had an iodine concentration of 15–64 ppm. A few (6%) food handlers in Mopani and almost half (45.9%) in Vhembe could correctly identify iodated salt as the main source of iodine. Almost half of the food handlers (%) in Mopani and 36.5% in Vhembe did not know which part of body needs iodine for functioning. Conclusion More than 20 years after the implementation of the USI program, the result of the study shows that the international goal of 90% coverage is still far from being realised.


Introduction
Malnutrition is a risk factor for early mortality and morbidity in children and adolescents [1]. Malnutrition and hunger accounts for nearly half of the death rate of children worldwide, with approximately 26% of undernourished children residing in Africa [2]. An estimated one-fifth (20%) of the total population comprises those of school age. It is said that approximately 25% of all children in developing countries are vitamin A deficient, whilst other nutrients most likely to be deficient in school aged children are reportedly iron and iodine, with the prevalence rates of the latter being between 35% and 70% [3][4][5][6][7]. Iversen et al. [5] report that undernutrition particularly affects young children residing in rural areas of the country.
Nutrients are not only important for growth and development but also offer children with energy to perform physical and metabolic functions [8]. Nutrition influences the efficiency of educational programmes [9]. us, adequate nutrition is vital during the school-age years because nutrition and health influences a child's cognitive development [3,10]. Children lacking certain nutrients in their diet and who suffer from persistent hunger, parasitic infections, or other nutrition-related diseases are likely to have reduced potential for learning compared to healthy, well-nourished children [11]. Nutrient deficiencies account for the inability of children to achieve their full mental and physical potential because of stunted growth, low physical work capacity, reduced IQ, and a lower resistance to infection [4].
In response to malnutrition, shortly after independence in 1994, the South African government initiated the Primary School Nutrition Programme (PSNP) under the purview of the Department of Health to promote and advocate for malnutrition control, nutritional education, and dietary guidelines in children from low socioeconomic status [5]. e programme was renamed the National School Nutrition Program (NSNP), and implementation was transferred to the Department of Education in 2004 to strengthen action and buy in. e NSNP was introduced as a vehicle for transporting micronutrients such as iron, iodine, and vitamin A to school-aged children [12]. e deficiencies of the three micronutrients of public health significance are iron deficiency anaemia (IDA), iodine deficiency disorders (IDD), and vitamin A deficiency (VAD). Iodine deficiency holds a notorious place among the micronutrient deficiencies which now poses a major worldwide health problem as it is the leading cause of both thyroid and brain abnormalities in children [13].
Salt iodisation is considered the most effective long-term public health intervention for achieving optimal iodine nutrition [14]. Effective salt iodisation is a prerequisite for the sustainable elimination of iodine deficiency disorders. In South Africa, direct and indirect evidence of continued endemic goitre and iodine deficiency led, in 1995, to the introduction of mandatory iodisation of table salt at an iodine concentration of 40-60 ppm. In 2007, the revision of the regulation led to a bigger acceptable range of 35-65 mg iodine/kg salt. Most studies have determined the iodine concentration of household salt but neglected the salt used in the NSNP. is observation underlines the need to determine the iodine concentration of salt used in the NSNP. e main aim of the present study was to determine the iodine concentration of salt used in the NSNP. is may assist in explaining the excessive urinary iodine concentration (UIC) that has been reported recently in South African school children. e secondary aim was to determine the knowledge of food handlers about iodine nutrition and salt iodisation.

Sample Design.
e study was conducted in selected schools of Mopani and Vhembe districts receiving the NSNP. e Mopani District is situated in the north-eastern part of Limpopo Province. It is the second biggest of the five districts in Limpopo Province. According to the 2016 community survey, it has an estimated population of 1159185 of whom the majority speak Xitsonga and Northern Sotho. ere are 16 urban areas (towns and townships), 354 villages (rural settlements), and a total of 125 wards. ere are 562 schools on the NSNP in the Mopani District. On the other hand, the Vhembe District is a category C municipality located in the northern part of Limpopo Province. e district has an estimated population of 1294722 of whom the majority speak Tshivenda and Xitsonga, and the settlement pattern is largely rural with approximately 774 dispersed villages [15].
ere are 968 schools on the NSP in the Vhembe District.
Simple random sampling was used to select schools that were included in the sample. A list of schools (both secondary and primary) was obtained from the Departments of Education in Vhembe and Mopani districts. e target population was food handlers employed in schools receiving the NSNP from the two districts. Food handlers are persons responsible for preparing meals for school children and preventing outbreaks of food-borne diseases in schools by adhering to food safety guidelines. A total of 359 food handlers (Mopani � 200 vs. Vhembe � 159) were conveniently selected from 318 schools of the two districts. In Mopani, the principals insisted that all food handlers participate in the study, hence an extra 41 food handlers. e two districts were selected based on their history of reported cases iodine deficiency. e study's population was from both rural and urban areas. Food handlers in schools receiving the NSNP in the Mopani and Vhembe districts, 18 years and above, were appointed formally by the school governing body and trained before presuming duties as food handlers and were included in the study. Voluteers and relatives who were standing in for food handlers on the day of data collection were excluded from the study. e reason for the exclusion was the fact that they did not receive training.

Data Collection.
Data were collected at the school sites from May 2017 to March 2018. An existing validated researcher-administered questionnaire on knowledge of iodine in the South African adult population [15][16][17] was used to gather information on iodine nutrition knowledge of food handlers. e questionnaire was administered to solicit data on demographic information, general questions on salt fortification, and iodine nutrition knowledge. e questionnaire was translated into the local languages (Tshivenda, Northern Sotho, and Xitsonga) by the researchers. An expert from the Department of Languages was consulted to translate the questionnaire back to English, and the two were compared. After completing the questionnaire, two tablespoons of salt used for the NSNP food preparation was collected from 318 schools in small plastic zip-lock bags. e salt samples were coded and stored at room temperature and protected from light and moisture until the time of analysis. e level of knowledge was asssessed using the iodine nutrition knowledge test. e following scores from Umalusi were used to classify the level of knowledge of food handlers: 0-29.9% � poor; 30-49.9% � fair; 50-69.9% � good; 70-89.9% � very good; and 90-100% � excellent (https:// www.umalusi.org.za/docs/research/2013/nsc_pass.pdf ).

Measurement of Iodine Concentration in Salt by iCheck.
Salt iodine concentrations were determined in the iodine laboratory at the North-West University (NWU) in Potchefstroom by means of the iCheck test method [18]. A total of 318 salt samples were analysed representing 100% successfully analysed samples. e analysis was performed in duplicates. e procedure is outlined as follows: 2 Biochemistry Research International First step: the salt was diluted with distilled water. e sample per analysis was 1.0 mL, the concentration range was >3 ppm (mg/kg), and the minimum dilution factor was 1 : 3. Second step: the sample was injected in the ready-touse reagent vial, and if the solution changed colour to purple, it indicated that iodine was present.

Statistical Analysis.
e data were entered into Microsoft excel spread sheet and exported to the Statistical Package of Social Science (SPSS). e data were analysed using SPSS version 25, and they were expressed as means, standard deviation, median, and interquartile ranges. For categorical data, the percentages and number of samples are presented. To compare differences between Mopani and Vhembe districts, the Mann-Whitney U test and independent t-tests were used. p < 0.05 was considered statistically significant.

Results
A total of 359 food handlers were recruited and completed the study. Table 1 shows the age, level of education, marital status, household income, and number of children. e age of the participants ranged from 18 years to 46 years and above. With regard to the level of education, a majority (Mopani � 64% vs. Vhembe � 82.4%) of food handlers had grades 8-12 in both districts. e marital statuses, single and married, had almost equal percentages in both districts. A majority of food handlers from both districts (Mopani � 82.5% vs. Vhembe � 66%) had an income ranging from R1001 to R2000. Almost all food handlers from both districts had children in the school they are working in (Table 1).
Of 359 food handlers, 147 (73.5%) in Mopani and 93 (58.2%) in Vhembe were trained before they were appointed as food handlers. e training period ranged from one day to a week (  (Table 3). Few samples in Mopani (9%) and Vhembe (11%) were noniodised. Further fewer samples in Mopani (8%) and Vhembe (4%) were excessively iodised (Table 3).     Biochemistry Research International e iodine nutrition knowledge of food handlers was poor with majority scores ranging from 0 to 29.9%. e distribution of scores by food handlers is summarised in Table 6.

Discussion
An iodine concentration of 15-64.9 ppm denotes that the salt is adequately iodised [18].
e results suggest that a majority of the salt samples in Mopani and Vhembe districts were adequately iodised.
A portion of samples was inadequately or noniodised or excessively iodised in the current study. One would expect all salt samples used for the NSNP to be adequately iodised; however, this was not the case in the current study. Inadequate iodine intake may result in a variety of disorders, termed iodine deficiency disorders (IDD), such as goitre, cretinism, spontaneous abortion, perinatal mortality, and heart failure [18,[20][21][22]. On the other hand, excess iodine may impair thyroid function [23]. Recently, a study [24] conducted in Limpopo Province has reported excess UIC in SAC which is a problem. A possible explanation for the variation in iodine concentration levels could be that, in South Africa, there is no proper monitoring of salt fortifications at production sites [25]. is may result in some salt producers underiodising and some overiodising as observed in the current study. e use of adequately iodised salt for the NSNP in Mopani (71%) and Vhembe (65%) was below the international coverage of 90%. It is noteworthy to assume that salt producers iodising salt at a concentration of more than 20 ppm contributes to the elimination of iodine deficiency [22].
e results of the current study indicated that food handlers in Mopani and Vhembe stored salt either in the plastic bag in which the salt was bought in or in containers with/without a lid. When iodised salt is not stored in closed plastic bags, sealed waterproof materials, or closed containers, iodine losses occur leading to reduction in the iodine content of salt before it is consumed [26].
Again, when improperly packed iodated salt is transported over long distances under humid conditions, it will attract moisture and become wet, dissolving and carrying the iodate to the bottom of the bag, and finally, it can be lost if the bag is porous to water [27,28]. Salt packed in such materials may lose as much as 75% of its iodine content over nine months. High-density polyethylene bags and polyethylene laminated bags are recommended for bulk packaging purposes [29]. Contrary to the results of the current study are the findings of a study conducted in Ethiopia where it was reported that most of the salt containers had covers at the household and the majority of caterers stored salt in a cool, dry area [30]. e iodine content of the salt remained constant, and its distribution remained uniform for many months when the salt is packed and kept dry, preferably in a cool place and away from sunlight [31]. Gebremariam et al. [32] also found that using packed salt at the household level was significantly associated with the availability of adequately iodised salt.
e results of the study suggest that there is limited iodine nutrition knowledge among the food handlers working for the NSNP, despite international efforts to eradicate IDD worldwide and the notable progress South Africa and other countries have made towards this goal. It can be concluded that these efforts have not yielded the expected growth regarding the iodine nutrition knowledge.
e results of the current study have yielded similar results to studies conducted among the South African adult population [33], where it was found that the knowledge level of iodine nutrition is low, particularly among the low socioeconomic groups. e current study and studies conducted in the Bargarh District [34], Kashmir Valley [35] of India, and the Andaman and Nicobar Islands have demonstrated low levels of iodine nutrition knowledge among the general public. Low levels of iodine nutrition knowledge is evident in the current study since more than a third of participants in Mopani and almost half of those in Vhembe did not know what iodine is, a few knew that salt was the main source of iodine, and half did not know which part of the body required iodine for functioning. Although international efforts have been put in place to emphasise the consequences of iodine deficiency on brain damage, it is surprising to note that the food handlers were not aware that mental retardation may result from iodine deficiency. To close this IDD communication gap, which appears to inhibit the transfer of this message to the consumer level, Jooste Joubert [33] maintains that both educational and public health communication strategies are required. In Turkey, the percentage of women using iodised salt increased significantly during a 3-month regional educational mass media campaign [36], indicating that improved IDD knowledge may lead to a more widespread consumption of iodised salt [33].
Nutrition knowledge is the knowledge of nutrients and foods [37]. Good nutrition knowledge is a rudiment for healthy living. erefore, adequate nutrition knowledge is needed when purchasing and preparing balanced meals [38]. Apart from purchasing and preparing meals, nutrition knowledge is extremely useful in an intervention  [39]. However, poor nutrition knowledge affects food choices and dietary interventions and can possibly compromise [40] the purpose of the NSNP. A food handler or cook working for the NSNP needs to know the various nutrient contents of each food type, proper application derived from great ideas, and benefit maximisation [38]. Failure to acquire potential and competent nutrition knowledge by food handlers of the NSNP may jeopardise addressing the micronutrient deficiencies, which is one of the crucial aims of the NSNP that has been widely neglected [41].

Conclusions
Since the introduction of mandatory salt iodisation by 40-60 ppm in South Africa in 1995, substantial progress has been made to eliminate IDD. More than 20 years after the implementation of the USI program, the results of the study show that the international goal of 90% coverage is still far from being realised. In the IDD Newsletter [42] of November 2013, Jooste indicated that household coverage of adequately iodised salt in South Africa was greater than 77%. Proper measures must be put in place to monitor fortification of salt at production sites. e results also show that food handlers have limited information about the iodine nutrition. Effective iodine nutrition education should be included in the training of food handlers.

Data Availability
Data will be available on request.
Ethical Approval e University of Venda (UNIVEN) Ethics Committee approved the study and an ethics certificate (SHS/16/NUT/ 01/1011) was issued. e Limpopo Provincial Department of Education granted permission for the study to be conducted. Furthermore, cooperation was sought from the Department of Education of Mopani and Vhembe districts, which gave clearance for the researcher to access the schools. e study was conducted in accordance with the principles of the Declaration of Helsinki [43] and the laws and regulations of South Africa. Consent e participating food handlers gave written informed consent.

Conflicts of Interest
e authors declare that they have no conflicts of interest.